The 3-hydroxy-3-methylglutaryl coenzyme-A reductases from fungi: A proposal as a therapeutic target and as a study model

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Upper panel, α-1,4-glycosidic bond; lower panel, β-1,3-glycosidic bond, and branching point showing a β-1,6-glycosidic bond. β-Glucan has repetitive units of this structure." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Roberto Lara-Lemus, Noé Alvarado-Vásquez, Edgar Zenteno, Patricia Gorocica" "autores" => array:4 [ 0 => array:2 [ "nombre" => "Roberto" "apellidos" => "Lara-Lemus" ] 1 => array:2 [ "nombre" => "Noé" "apellidos" => "Alvarado-Vásquez" ] 2 => array:2 [ "nombre" => "Edgar" "apellidos" => "Zenteno" ] 3 => array:2 [ "nombre" => "Patricia" "apellidos" => "Gorocica" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1130140613001095?idApp=UINPBA00004N" "url" => "/11301406/0000003100000001/v1_201402070026/S1130140613001095/v1_201402070026/en/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "Mycologic Forum" "titulo" => "The 3-hydroxy-3-methylglutaryl coenzyme-A reductases from fungi: A proposal as a therapeutic target and as a study model" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "81" "paginaFinal" => "85" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Dulce Andrade-Pavón, Eugenia Sánchez-Sandoval, Blanca Rosales-Acosta, José Antonio Ibarra, Joaquín Tamariz, César Hernández-Rodríguez, Lourdes Villa-Tanaca" "autores" => array:7 [ 0 => array:2 [ "nombre" => "Dulce" "apellidos" => "Andrade-Pavón" ] 1 => array:2 [ "nombre" => "Eugenia" "apellidos" => "Sánchez-Sandoval" ] 2 => array:2 [ "nombre" => "Blanca" "apellidos" => "Rosales-Acosta" ] 3 => array:2 [ "nombre" => "José Antonio" "apellidos" => "Ibarra" ] 4 => array:2 [ "nombre" => "Joaquín" "apellidos" => "Tamariz" ] 5 => array:2 [ "nombre" => "César" "apellidos" => "Hernández-Rodríguez" ] 6 => array:4 [ "nombre" => "Lourdes" "apellidos" => "Villa-Tanaca" "email" => array:2 [ 0 => "lourdesvilla@hotmail.com" 1 => "mvillat@ipn.mx" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "¿" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, México, D.F., México" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "La enzima 3-hidroxi-3-metilglutaril coenzima A reductasa de hongos: propuesta como diana terapéutica y como modelo de estudio" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1764 "Ancho" => 2066 "Tamanyo" => 222268 ] ] "descripcion" => array:1 [ "en" => "Model for the secondary structure of Candida glabrata HMGR (HMGRCg) and Ustilago maydis HMGR (HMGRUm). Secondary structure was determined from HMGRCg (A) and HMGRUm (B). Both enzymes show some characteristics of other eukaryotic HMGRs, this is: an amino terminus facing the lumen of the endoplasmic reticulum and the carboxyl terminus facing the cytoplasm, eighth or four transmembrane segments (C. glabrata and U. maydis, respectively), and a multimerization domain which forms the binding domain for the substrate and the cofactor NADPH." ] ] ] "textoCompleto" => "The enzyme 3-hydroxy-3-methylglutaryl coenzyme-A reductase (HMGR) catalyzes the conversion of 3-hydroxy-3-methylglutaryl coenzyme-A (HMG-CoA) to mevalonate, an oxido-reduction reaction that is a rate-limiting step in cholesterol synthesis in mammals, including humans, ergosterol in fungi, and other isoprenoids. The reaction catalyzed by HMGR is:<elsevierMultimedia ident="eq0005"></elsevierMultimedia>This enzyme is found in both eukaryotes (localized to the endoplasmic reticulum) and prokaryotes (soluble and cytoplasmic).<a class="elsevierStyleCrossRef" href="#bib0055">11</a> Phylogenetic analysis has revealed two classes of HMGRs, class I enzymes grouping those from eukaryotes and some Archaea and class II enzymes grouping bacteria and certain other Archaea HMGRs.<a class="elsevierStyleCrossRef" href="#bib0045">9</a> The reaction catalyzed by human HMGR is a target for hypocholesterolemic drugs such as statins, which are intended to lower cholesterol levels in serum.<a class="elsevierStyleCrossRef" href="#bib0115">23</a> Furthermore, the HMGR enzyme of some opportunistic pathogenic fungi has been proposed as a target for inhibiting ergosterol synthesis as an alternative for solving the problem of the antifungal resistance.<a class="elsevierStyleCrossRefs" href="#bib0020">4,25</a> To this end, the effect of statins on HMGR inhibition in some fungi has been studied resulting in production of sterols, dolichol and coenzyme Q10 being affected.<a class="elsevierStyleCrossRefs" href="#bib0020">4,15,20,25</a>Despite the fact that HMGR activity in some yeasts such as Saccharomyces cerevisiae, Candida glabrata, Schizosaccharomyces pombe and others, has been described, there are no studies dealing with the genes encoding for this enzyme. Comparative analyses of putative proteins deduced from the nucleotide sequences encoding HMGRs have not been performed. Such analyses would provide relevant information to endorse the proposal of considering the HMGR enzyme as a therapeutic target. This review evaluates the conservation of the catalytic site HMGR from various fungi, its topology, activity inhibition and its possible use from to study HMGR inhibitors for human therapeutic use.Fungal HMGR gene organizationAnalysis of genome sequences identified hmgr genes in organisms from all three domains of life. More than 150 HMGR sequences are recorded in public databases.<a class="elsevierStyleCrossRef" href="#bib0045">9</a> The number of genes encoding the HMGR enzyme may depend on the organism or species. Animals, Archaea, and bacteria have only one hmgr gene, while plants exhibit multiple HMGR isoenzymes. S. cerevisiae has two HMGR isoenzymes (hmgr-1 and hmgr-2)<a class="elsevierStyleCrossRef" href="#bib0010">2</a> while C. glabrata has a single gene (hmgr-1-Cg). In this review, we have identified HMGR sequences from S. cerevisiae (HMGRSC1 and HMGRSC2), S. pombe (HMGRSp), Candida albicans (HMGRCa), C. glabrata (HMGRCg), Ustilago maydis (HMGRUm), Cryptococcus neoformans (HMGRCn), and Aspegillus niger (HMGRAn), which were compared to human HMGR (HMGRH) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Comparison of deduced aminoacid sequences confirms that analyzed fungal HMGRs belong to class I group. This latter means that all these enzymes are comprised of three characteristic domains: the membrane anchor domain, a linker and the catalytic domain. Some subdomains have been defined within the catalytic domain. The N domain connects the L domain to the linker domain; L domain contains an HMG-CoA binding region; and the S binds NADP(H)<a class="elsevierStyleCrossRef" href="#bib0045">9</a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). The HMGR enzymes from ascomycetes (Sc, Cg, An) and basidiomycetes (Um, Cn) show the three characteristic domains (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Analyzed proteins also have the amino acid sequence that binds the cofactor NADPH (indicated by a black box in <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>, see residues 839–851aa from S. cerevisiae).<a class="elsevierStyleCrossRef" href="#bib0045">9</a> Identity and similarity analyses of HMGR soluble fraction (i.e. the catalytic fraction) from multiple organisms, including different mammals and fungi, showed that all these catalytic domains are highly conserved (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). When a comparison was carried out between HMGRs from different fungi and the human counterpart we observed that S. pombe, Candida parapsilosis and U. maydis presented the highest similarity with human HMGR (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia>The analysis of the open reading frame (ORF) of different HMGRs showed that these can vary in size but sequences of all deduced proteins have the three characteristic HMGR domains from eukaryotic class I proteins: membrane anchor, linker and catalytic domains (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). The analyses of the genes encoding different HMGRs, also demonstrated that have no introns (data not shown), unlike the genes encoding mammals HMGRs, which may contain up to 20 introns.<a class="elsevierStyleCrossRef" href="#bib0045">9</a><elsevierMultimedia ident="tbl0010"></elsevierMultimedia>Characteristic structural featuresHigh-resolution crystal structures have been solved for class I human HMGR (HMGRH).<a class="elsevierStyleCrossRef" href="#bib0060">12</a> The crystal structure shows the oligomeric state of this enzyme and suggests relevance for activity and a mechanism for cholesterol sensing. The active site architecture of human HMGR is different from that of bacterial HMGR and this may explain why HMGR inhibitors in bacteria have not been reported. Owing to the fact that the active site domain of S. pombe HMGR is quite similar to that of humans, a new approach has been developed by using the fungal HMGR (HMGRf) as a straight forward in vitro assay for measuring inhibitory activity of the test compounds designed as hypocholesterolemic in vivo in a murine model.<a class="elsevierStyleCrossRef" href="#bib0005">1</a> Although the fungal enzymes examined in this review showed the characteristic domains of the class I enzymes (transmembranal, linker and catalytic), certain differences can be observed in the protein topology. For instance, C. glabrata HMGR (HMGRCg) has eigth possible transmembrane sequences while U. maydis HMGRUm has only four (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). This suggests a different regulation between both enzymes. As a matter of fact, it has been suggested that the transmembrane region participates in HMGR degradation (post-translational regulation).<a class="elsevierStyleCrossRef" href="#bib0045">9</a> HMGRH was purified as a homotetramer and the predicted topology of HMGRCg and HMGRUm shows multimerization domains too, suggesting that these may also form multimers (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Regulation by HMGR and sterol biosynthetic pathway in yeastAs we mentioned before, yeasts produce ergosterol using a metabolic pathway that in many enzymatic steps is similar to that found in mammals, with HMGR being the limiting step. With such a relevant role in cell physiology, this enzyme is tightly regulated at different levels including transcriptional, post-transcriptional, traductional and post-traductional regulation.<a class="elsevierStyleCrossRef" href="#bib0070">14</a> Interestingly, the enzymatic activity of HMGR does not produce toxic precursors and therefore it is an attractive target for controlling cholesterol levels in humans.<a class="elsevierStyleCrossRef" href="#bib0115">23</a> After the discovery of compactin in 1970, a specific HMGR inhibitor, in growing cultures of Penicillium citrinum,<a class="elsevierStyleCrossRef" href="#bib0040">8</a> many other models have been studied, including rabbits, non-human primates, rats and dogs, to detect changes in cholesterol levels. In 1978 the Aspergillus terreus HMGR was used as a model to study the inhibitory effect of mevinolin, later called lovastatin.<a class="elsevierStyleCrossRef" href="#bib0115">23</a> These and other studies served for the classification of inhibitors in two groups: analogs of the 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA) and those that are not, such as alpha-asarone-based analogs.<a class="elsevierStyleCrossRef" href="#bib0110">22</a> Despite the fact that multicellular organisms models are attractive because of their similarity with humans they have proven to be difficult to work with. Therefore, the development of new unicellular models has become an attractive option. For instance, the yeast S. pombe has been used to study the regulatory aspects of sterol biosynthesis.<a class="elsevierStyleCrossRef" href="#bib0005">1</a>The ergosterol biosynthetic pathway is fully known in the yeast S. cerevisiae.<a class="elsevierStyleCrossRef" href="#bib0080">16</a> It is composed of 20 enzymatic reactions and it is divided into the mevalonate pathway, which includes 9 reactions and ends with the synthesis of farnesyl pyrophosphate, and the pathway that converts this intermediate into ergosterol with the involvement of 11 enzymatic reactions.<a class="elsevierStyleCrossRef" href="#bib0035">7</a> This pathway is responsible for the biosynthesis of important intermediate products such as the geranylgeraniol group, which is involved in protein post-traductional modifications (i.e. Ras, Rac), dolichol, heme group and quinolone synthesis.<a class="elsevierStyleCrossRefs" href="#bib0035">7,10</a> Experimental evidence has shown that synthesis of ergosterol in S. pombe follows a similar pathway to that of S. cerevisiae.<a class="elsevierStyleCrossRefs" href="#bib0015">3,13</a>Inhibition of viability and ergosterol synthesis in yeasts as a consequence of the inhibition of the HMGRUp to date there have been published some studies about the effect of statins, azoles or their combination against fungi in liquid or solid medium to determine antifungal activity. Accordingly, it has been observed that lovastatin is capable of affecting sterol levels in S. cerevisiae.<a class="elsevierStyleCrossRef" href="#bib0090">18</a> Statins may also inhibit the growth of Candida species and Aspergillus fumigatus.<a class="elsevierStyleCrossRef" href="#bib0105">21</a> Other studies demonstrated synergism of azoles with statins, such as fluvastatin with fluconazole or itraconazole which together, can reduce ergosterol levels and viability in Candida spp. and C. neoformans.<a class="elsevierStyleCrossRef" href="#bib0025">5</a> Similarly it has been demonstrated that the synergism of statin and azoles inhibit ergosterol synthesis in S. cerevisiae and Candida utilis in a bioassay on solid medium.<a class="elsevierStyleCrossRef" href="#bib0020">4</a> On the other hand, a series of alpha-asarone and fibrate-based analogs were designed by docking approaches with published crystal structures of human HMGR and the partial purification of the enzyme from S. pombe allowed the test of analog compounds, resulting in positive and significant inhibitory activity.<a class="elsevierStyleCrossRefs" href="#bib0005">1,24</a> The use of simvastatin in C. glabrata has shown that in addition of reducing the levels of ergosterol and inhibiting growth, this statin can lead to the loss of mitochondrial DNA (mtDNA).<a class="elsevierStyleCrossRef" href="#bib0125">25</a> This may restrict the use of statins as antifungal agents, because, the loss of mtDNA and the generation of “petite” mutants are related to azole resistance in C. glabrata. Therefore, new synthetic compounds are being designed, analogs of statins, capable of inhibiting the synthesis of ergosterol but with no loss of mtDNA (data not shown).HMGR enzyme as model to identify novel therapies to modulate cholesterol synthesis and to study sterol biosynthesisAlthough yeasts synthesize ergosterol instead of cholesterol, fungi share many of the enzymes involved in the sterol synthesis pathway in mammals, including HMGR. Therefore, the fungal HMGR have proven to be suitable models for studying the inhibition by compounds structurally related to statins or fibrates. In this sense, the enzyme from S. pombe has been proposed as a model to study some aspects of regulation of sterol biosynthesis that have been difficult to address in other organisms.<a class="elsevierStyleCrossRefs" href="#bib0005">1,17,20</a> Heterologous expression of genes encoding the HMGR from different fungi also has been successful to study pharmaceutical compounds inhibiting cholesterol synthesis. Accordingly, the Rhizomucor miehei HMGR gene, has been expressed in Mucor circinelloides.<a class="elsevierStyleCrossRef" href="#bib0095">19</a> HMGR C-terminal from U. maydis was expressed in Escherichia coli and shown to be blocked by a potent inhibitor of mammalian and fungal HMG-CoA reductases.<a class="elsevierStyleCrossRef" href="#bib0030">6</a>ConclusionsGiven the similarities in the initial steps of cholesterol and ergosterol synthesis pathways, the fact that HMGR is a critical control point in both of them and that the enzyme from S. pombe and U. maydis are very similar to the human counterpart in the catalytic regions, we propose that fungal enzymes can be used to test inhibitors with a potential use in humans.Conflict of interestThe authors declare that they have no conflict of interests." "textoCompletoSecciones" => array:1 [ "secciones" => array:13 [ 0 => array:2 [ "identificador" => "xres311239" "titulo" => "Abstract" ] 1 => array:2 [ "identificador" => "xpalclavsec294391" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "xres311238" "titulo" => "Resumen" ] 3 => array:2 [ "identificador" => "xpalclavsec294392" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Fungal HMGR gene organization" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Characteristic structural features" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Regulation by HMGR and sterol biosynthetic pathway in yeast" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Inhibition of viability and ergosterol synthesis in yeasts as a consequence of the inhibition of the HMGR" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "HMGR enzyme as model to identify novel therapies to modulate cholesterol synthesis and to study sterol biosynthesis" ] 9 => array:2 [ "identificador" => "sec0030" "titulo" => "Conclusions" ] 10 => array:2 [ "identificador" => "sec0035" "titulo" => "Conflict of interest" ] 11 => array:2 [ "identificador" => "xack73827" "titulo" => "Acknowledgments" ] 12 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2013-09-06" "fechaAceptado" => "2013-10-09" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec294391" "palabras" => array:3 [ 0 => "3-Hydroxy-3-methylglutaryl coenzyme A reductase" 1 => "(EC 1.1.1.34)" 2 => "Ergosterol synthesis" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec294392" "palabras" => array:3 [ 0 => "3-Hidroxi-3-metilglutaril coenzima A reductasa" 1 => "(EC 1.1.1.34)" 2 => "Síntesis de colesterol" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "The enzyme 3-hydroxy-3-methylglutaryl coenzyme-A reductase (HMGR) catalyzes the conversion of HMG-Co-A into mevalonate. This step is the limiting point for the synthesis of cholesterol in mammals and ergosterol in fungi. We describe in this article the genome organization of HMGR coding genes and those deduced from different fungi, recount the evidence showing statins as HMGR inhibitors for ergosterol synthesis and its effect in yeast viability, and propose fungal HMGR (HMGRf) as a model to study the use of pharmaceutical compounds to inhibit cholesterol and ergosterol synthesis. Bibliographical search and bioinformatic analyses were performed and discussed. HMGRfs belong to the class I with a high homology in the catalytic region. The sterol biosynthetic pathway in humans and fungi share many enzymes in the initial steps (such as the HMGR enzyme), but in the last steps enzymes are different rendering the two final products: cholesterol in mammals and ergosterol in fungi. With regards to inhibitors such as statins and other compounds, these affect also fungal viability. Since HMGR from Schizosaccharomyces pombe and Ustilago maydis are very similar to the human HMGR in the catalytic regions, we propose that fungal enzymes can be used to test inhibitors for a potential use in humans. We consider that HMGRf is a good therapeutic target to design and test new antifungal compounds.This manuscript is part of the series of works presented at the “V International Workshop: Molecular genetic approaches to the study of human pathogenic fungi” (Oaxaca, Mexico, 2012)." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "La enzima 3-hidroxi-3-metilglutaril coenzima A reductasa (HMGR) cataliza la conversión de HMG-Co-A a mevalonato, paso limitante en la síntesis de colesterol en mamíferos y de ergosterol en hongos. El presente artículo describe la organización de genes codificantes y proteínas de las diferentes HMGR de hongos (HMGRf), expone las evidencias disponibles en la inhibición de HMGR en la síntesis de ergosterol y su efecto en la viabilidad de los hongos, y propone las HMGRf como modelo de estudio para la aplicación de fármacos inhibidores de las síntesis de colesterol y ergosterol. Para ello se realizó una búsqueda bibliográfica y análisis bioinformáticos, con descripción de los datos. Las HMGRf son de clase i y presentan una alta homología en la región catalítica. La vía biosintética de esteroles en el ser humano y en los hongos comparte algunas enzimas iniciales (como la HMGR) pero, en los últimos pasos, las enzimas son diferentes, lo que genera productos finales distintos: colesterol y ergosterol, respectivamente. La inhibición de HMGRf por estatinas afecta a la síntesis de ergosterol y la viabilidad. Dado que el sitio catalítico de las HMGR de Schizosaccharomyces pombe y Ustilago maydis es muy similar al de la enzima humana, podrían servir como modelos para el estudio de fármacos inhibidores de la síntesis de colesterol. La HMGRf es una diana terapéutica adecuada para el diseño de nuevos antimicóticos.Este artículo forma parte de una serie de estudios presentados en el «V International Workshop: Molecular genetic approaches to the study of human pathogenic fungi» (Oaxaca, México, 2012)." ] ] "multimedia" => array:5 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2642 "Ancho" => 2176 "Tamanyo" => 293312 ] ] "descripcion" => array:1 [ "en" => "Schematic representation of HMGR proteins. Diagram shows features of HMGR proteins from: Human (HMGRH), S. cerevisiae (HMGRSC1 and HMGRSC2), S. pombe (HMGRSp), C. albicans (HMGRCa), C. glabrata (HMGRCg), U. maydis (HMGRUm), C. neoformans (HMGRCn), and A. niger (HMGRAn). Indicated domains are as follows: Nter, N-terminal domain containing a membrane anchor domain; Linker (connects membrane anchor domain to catalytic domain); the catalytic domain which has subdomains N, L, S, and L. N domain: connects L domain to linker; L domain: contains an HMG-CoA binding site; S domain: binds NADPH. Black box shows the cis-loop connects the HMG-CoA-binding region with the NADP-H-binding region." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1764 "Ancho" => 2066 "Tamanyo" => 222268 ] ] "descripcion" => array:1 [ "en" => "Model for the secondary structure of Candida glabrata HMGR (HMGRCg) and Ustilago maydis HMGR (HMGRUm). Secondary structure was determined from HMGRCg (A) and HMGRUm (B). Both enzymes show some characteristics of other eukaryotic HMGRs, this is: an amino terminus facing the lumen of the endoplasmic reticulum and the carboxyl terminus facing the cytoplasm, eighth or four transmembrane segments (C. glabrata and U. maydis, respectively), and a multimerization domain which forms the binding domain for the substrate and the cofactor NADPH." ] ] 2 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">H. sapiens \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">S. pombe \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. albicans \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. glabrata \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Similarity/identity % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Similarity/identity % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Similarity/identity % \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Similarity/identity % \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Mus musculus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">52.64/48.08 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16.91/5.31 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14.76/4.38 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">13.86/4.16 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Rattus norvegicus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">52.87/48.19 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">17.24/5.41 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14.76/4.28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14.20/4.45 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Homo sapiens \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.60/6.07 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">17.02/5.31 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">13.86/5.01 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">S. cerevisiae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16.68/5.69 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.27/6.55 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">49.49/31.96 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">32.13/16.19 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">(HMG1/HMG2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16.34/6.12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.27/7.21 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">23.33/8.10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">22.20/9.18 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">S. pombe \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.60/6.07 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.60/7.17 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">20.51/6.62 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. albicans \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">17.02/5.31 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.60/7.17 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.72/7. 76 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. glabrata \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">13.86/5.01 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">20.51/6.62 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.72/7.76 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Candida dubliniensis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16.34/5.35 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.82/6.28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">70.23/52.01 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.71/7.32 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. parapsilosis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">17.47/6.67 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.82/6.28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">24.80/10.54 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.15/5.99 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. neoformans \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14.43/4.28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">20.29/6.15 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">21.87/6.31 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">20.63/5.37 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Yarrowia lipolytica \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16.23/5.50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.50/7.20 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.72/7.20 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.05/7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">U. maydis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">17. 70/5.36 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.48/6.05 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.26/5.26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">21.98/7.24 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Coccidioides immitis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15.67/5.02 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.94/6.34 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">20.63/5.73 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.16/5.29 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Kluyveromyces lactis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14.88/5.59 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">23.78/8.20 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">23.67/8.58 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">25.25/10.82 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Aspergillus clavatus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16/5.65 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.72/6.44 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">22.77/5.74 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">17.58/4.94 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">A. niger \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15.67/4.95 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.82/5.92 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">20.74/5.48 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18.48/4.95 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Candida tropicalis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">13.86/4.02 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.27/6. 13 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">23.22/10.06 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19.84/7.76 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab457248.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Similarity and identity of multiple HMGRs class 1 from mammals and fungi." ] ] 3 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Organism \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Accession number \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Family \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Gene length (bp) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black">Protein size (aa) \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Mus musculus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0005" href="ncbi-p:NP_032281">NP_032281</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3996 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">887 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Rattus norvegicus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0010" href="ncbi-p:AAH64654">AAH64654</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4319 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">887 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Homo sapiens \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0015" href="ncbi-p:NP_000850">NP_000850</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2904 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">888 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">S. cerevisiae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0020" href="ncbi-p:AAA34676">AAA34676</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3165 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1054 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0025" href="ncbi-p:AAA34677">AAA34677</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3338 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1045 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">S. pombe \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0030" href="ncbi-p:NP_588235">NP_588235</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3162 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1053 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. albicans \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0035" href="ncbi-p:XP_713681">XP_713681</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3222 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1073 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. glabrata \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0040" href="ncbi-p:XP_449268">XP_449268</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3171 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1056 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Candida lusitaniae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">CLUG_04490 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3027 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1098 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Candida tropicalis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0045" href="ncbi-p:EER31565">EER31565</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3132 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1043 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Candida dubliniensis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0050" href="ncbi-p:CAX44612">CAX44612</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3195 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1065 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. parapsilosis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0055" href="ncbi-p:CCE40995">CCE40995</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3102 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1033 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">C. neoformans var. neoformans \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0060" href="ncbi-p:XP_571450">XP_571450</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3849 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1282 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Yarrowia lipolytica \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0065" href="ncbi-p:XP_503558">XP_503558</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2997 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">998 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">U. maydis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0070" href="ncbi-p:XP_759161">XP_759161</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3021 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1006 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Coccidioides immitis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0075" href="ncbi-p:XP_001245047">XP_001245047</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3405 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1134 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Kluyveromyces lactis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0080" href="ncbi-p:XP_451740">XP_451740</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3219 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1072 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Aspergillus clavatus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0085" href="ncbi-p:XP_001272815">XP_001272815</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3399 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1132 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">A. niger \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0090" href="ncbi-p:XP_001391903">XP_001391903</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3345 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1114 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drosophila melanogaster \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><a class="elsevierStyleInterRef" id="intr0095" href="ncbi-p:NP_732900">NP_732900</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">HMG1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3818 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1272 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab457249.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Details of the sequences used for the structural protein analysis in <a 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Mycologic Forum

The 3-hydroxy-3-methylglutaryl coenzyme-A reductases from fungi: A proposal as a therapeutic target and as a study model

La enzima 3-hidroxi-3-metilglutaril coenzima A reductasa de hongos: propuesta como diana terapéutica y como modelo de estudio

Dulce Andrade-Pavón, Eugenia Sánchez-Sandoval, Blanca Rosales-Acosta, José Antonio Ibarra, Joaquín Tamariz, César Hernández-Rodríguez, Lourdes Villa-Tanaca

Corresponding author

lourdesvilla@hotmail.com
mvillat@ipn.mx

Corresponding author.

Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, México, D.F., México

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which are intended to lower cholesterol levels in serum&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> Furthermore&#44; the HMGR enzyme of some opportunistic pathogenic fungi has been proposed as a target for inhibiting ergosterol synthesis as an alternative for solving the problem of the antifungal resistance&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#44;25</span></a> To this end&#44; the effect of statins on HMGR inhibition in some fungi has been studied resulting in production of sterols&#44; dolichol and coenzyme Q10 being affected&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#44;15&#44;20&#44;25</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Despite the fact that HMGR activity in some yeasts such as <span class="elsevierStyleItalic">Saccharomyces cerevisiae</span>&#44; <span class="elsevierStyleItalic">Candida glabrata</span>&#44; <span class="elsevierStyleItalic">Schizosaccharomyces pombe</span> and others&#44; has been described&#44; there are no studies dealing with the genes encoding for this enzyme&#46; Comparative analyses of putative proteins deduced from the nucleotide sequences encoding HMGRs have not been performed&#46; Such analyses would provide relevant information to endorse the proposal of considering the HMGR enzyme as a therapeutic target&#46; This review evaluates the conservation of the catalytic site HMGR from various fungi&#44; its topology&#44; activity inhibition and its possible use from to study HMGR inhibitors for human therapeutic use&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Fungal HMGR gene organization</span><p id="par0020" class="elsevierStylePara elsevierViewall">Analysis of genome sequences identified <span class="elsevierStyleItalic">hmgr</span> genes in organisms from all three domains of life&#46; More than 150 HMGR sequences are recorded in public databases&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> The number of genes encoding the HMGR enzyme may depend on the organism or species&#46; Animals&#44; Archaea&#44; and bacteria have only one <span class="elsevierStyleItalic">hmgr</span> gene&#44; while plants exhibit multiple HMGR isoenzymes&#46; <span class="elsevierStyleItalic">S&#46; cerevisiae</span> has two HMGR isoenzymes &#40;<span class="elsevierStyleItalic">hmgr</span>-1 and <span class="elsevierStyleItalic">hmgr</span>-2&#41;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> while <span class="elsevierStyleItalic">C&#46; glabrata</span> has a single gene &#40;<span class="elsevierStyleItalic">hmgr</span>-1-Cg&#41;&#46; In this review&#44; we have identified HMGR sequences from <span class="elsevierStyleItalic">S&#46; cerevisiae</span> &#40;HMGR<span class="elsevierStyleInf">SC1</span> and HMGR<span class="elsevierStyleInf">SC2</span>&#41;&#44; <span class="elsevierStyleItalic">S&#46; pombe</span> &#40;HMGR<span class="elsevierStyleInf">Sp</span>&#41;&#44; <span class="elsevierStyleItalic">Candida albicans</span> &#40;HMGR<span class="elsevierStyleInf">Ca</span>&#41;&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span> &#40;HMGR<span class="elsevierStyleInf">Cg</span>&#41;&#44; <span class="elsevierStyleItalic">Ustilago maydis</span> &#40;HMGR<span class="elsevierStyleInf">Um</span>&#41;&#44; <span class="elsevierStyleItalic">Cryptococcus neoformans</span> &#40;HMGR<span class="elsevierStyleInf">Cn</span>&#41;&#44; and <span class="elsevierStyleItalic">Aspegillus niger</span> &#40;HMGR<span class="elsevierStyleInf">An</span>&#41;&#44; which were compared to human HMGR &#40;HMGR<span class="elsevierStyleInf">H</span>&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Comparison of deduced aminoacid sequences confirms that analyzed fungal HMGRs belong to class I group&#46; This latter means that all these enzymes are comprised of three characteristic domains&#58; the membrane anchor domain&#44; a linker and the catalytic domain&#46; Some subdomains have been defined within the catalytic domain&#46; The N domain connects the L domain to the linker domain&#59; L domain contains an HMG-CoA binding region&#59; and the S binds NADP&#40;H&#41;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; The HMGR enzymes from ascomycetes &#40;Sc&#44; Cg&#44; An&#41; and basidiomycetes &#40;Um&#44; Cn&#41; show the three characteristic domains &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Analyzed proteins also have the amino acid sequence that binds the cofactor NADPH &#40;indicated by a black box in <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#44; see residues 839&#8211;851<span class="elsevierStyleHsp" style=""></span>aa from <span class="elsevierStyleItalic">S&#46; cerevisiae</span>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> Identity and similarity analyses of HMGR soluble fraction &#40;i&#46;e&#46; the catalytic fraction&#41; from multiple organisms&#44; including different mammals and fungi&#44; showed that all these catalytic domains are highly conserved &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; When a comparison was carried out between HMGRs from different fungi and the human counterpart we observed that <span class="elsevierStyleItalic">S&#46; pombe</span>&#44; <span class="elsevierStyleItalic">Candida parapsilosis</span> and <span class="elsevierStyleItalic">U&#46; maydis</span> presented the highest similarity with human HMGR &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">The analysis of the open reading frame &#40;ORF&#41; of different HMGRs showed that these can vary in size but sequences of all deduced proteins have the three characteristic HMGR domains from eukaryotic class I proteins&#58; membrane anchor&#44; linker and catalytic domains &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; The analyses of the genes encoding different HMGRs&#44; also demonstrated that have no introns &#40;data not shown&#41;&#44; unlike the genes encoding mammals HMGRs&#44; which may contain up to 20 introns&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a></p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Characteristic structural features</span><p id="par0030" class="elsevierStylePara elsevierViewall">High-resolution crystal structures have been solved for class I human HMGR &#40;HMGR<span class="elsevierStyleInf">H</span>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> The crystal structure shows the oligomeric state of this enzyme and suggests relevance for activity and a mechanism for cholesterol sensing&#46; The active site architecture of human HMGR is different from that of bacterial HMGR and this may explain why HMGR inhibitors in bacteria have not been reported&#46; Owing to the fact that the active site domain of <span class="elsevierStyleItalic">S&#46; pombe</span> HMGR is quite similar to that of humans&#44; a new approach has been developed by using the fungal HMGR &#40;HMGRf&#41; as a straight forward in vitro assay for measuring inhibitory activity of the test compounds designed as hypocholesterolemic in vivo in a murine model&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Although the fungal enzymes examined in this review showed the characteristic domains of the class I enzymes &#40;transmembranal&#44; linker and catalytic&#41;&#44; certain differences can be observed in the protein topology&#46; For instance&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span> HMGR &#40;HMGR<span class="elsevierStyleInf">Cg</span>&#41; has eigth possible transmembrane sequences while <span class="elsevierStyleItalic">U&#46; maydis</span> HMGR<span class="elsevierStyleItalic">Um</span> has only four &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; This suggests a different regulation between both enzymes&#46; As a matter of fact&#44; it has been suggested that the transmembrane region participates in HMGR degradation &#40;post-translational regulation&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> HMGR<span class="elsevierStyleInf">H</span> was purified as a homotetramer and the predicted topology of HMGR<span class="elsevierStyleInf">Cg</span> and HMGR<span class="elsevierStyleInf">Um</span> shows multimerization domains too&#44; suggesting that these may also form multimers &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Regulation by HMGR and sterol biosynthetic pathway in yeast</span><p id="par0035" class="elsevierStylePara elsevierViewall">As we mentioned before&#44; yeasts produce ergosterol using a metabolic pathway that in many enzymatic steps is similar to that found in mammals&#44; with HMGR being the limiting step&#46; With such a relevant role in cell physiology&#44; this enzyme is tightly regulated at different levels including transcriptional&#44; post-transcriptional&#44; traductional and post-traductional regulation&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> Interestingly&#44; the enzymatic activity of HMGR does not produce toxic precursors and therefore it is an attractive target for controlling cholesterol levels in humans&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> After the discovery of compactin in 1970&#44; a specific HMGR inhibitor&#44; in growing cultures of <span class="elsevierStyleItalic">Penicillium citrinum</span>&#44;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> many other models have been studied&#44; including rabbits&#44; non-human primates&#44; rats and dogs&#44; to detect changes in cholesterol levels&#46; In 1978 the <span class="elsevierStyleItalic">Aspergillus terreus</span> HMGR was used as a model to study the inhibitory effect of mevinolin&#44; later called lovastatin&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> These and other studies served for the classification of inhibitors in two groups&#58; analogs of the 3-hydroxy-3-methylglutaryl-CoA &#40;HMG-CoA&#41; and those that are not&#44; such as alpha-asarone-based analogs&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> Despite the fact that multicellular organisms models are attractive because of their similarity with humans they have proven to be difficult to work with&#46; Therefore&#44; the development of new unicellular models has become an attractive option&#46; For instance&#44; the yeast <span class="elsevierStyleItalic">S&#46; pombe</span> has been used to study the regulatory aspects of sterol biosynthesis&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">The ergosterol biosynthetic pathway is fully known in the yeast <span class="elsevierStyleItalic">S&#46; cerevisiae</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> It is composed of 20 enzymatic reactions and it is divided into the mevalonate pathway&#44; which includes 9 reactions and ends with the synthesis of farnesyl pyrophosphate&#44; and the pathway that converts this intermediate into ergosterol with the involvement of 11 enzymatic reactions&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> This pathway is responsible for the biosynthesis of important intermediate products such as the geranylgeraniol group&#44; which is involved in protein post-traductional modifications &#40;i&#46;e&#46; Ras&#44; Rac&#41;&#44; dolichol&#44; heme group and quinolone synthesis&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;10</span></a> Experimental evidence has shown that synthesis of ergosterol in <span class="elsevierStyleItalic">S&#46; pombe</span> follows a similar pathway to that of <span class="elsevierStyleItalic">S&#46; cerevisiae</span>&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;13</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Inhibition of viability and ergosterol synthesis in yeasts as a consequence of the inhibition of the HMGR</span><p id="par0045" class="elsevierStylePara elsevierViewall">Up to date there have been published some studies about the effect of statins&#44; azoles or their combination against fungi in liquid or solid medium to determine antifungal activity&#46; Accordingly&#44; it has been observed that lovastatin is capable of affecting sterol levels in <span class="elsevierStyleItalic">S&#46; cerevisiae</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> Statins may also inhibit the growth of <span class="elsevierStyleItalic">Candida</span> species and <span class="elsevierStyleItalic">Aspergillus fumigatus</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> Other studies demonstrated synergism of azoles with statins&#44; such as fluvastatin with fluconazole or itraconazole which together&#44; can reduce ergosterol levels and viability in <span class="elsevierStyleItalic">Candida</span> spp&#46; and <span class="elsevierStyleItalic">C&#46; neoformans</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> Similarly it has been demonstrated that the synergism of statin and azoles inhibit ergosterol synthesis in <span class="elsevierStyleItalic">S&#46; cerevisiae</span> and <span class="elsevierStyleItalic">Candida utilis</span> in a bioassay on solid medium&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> On the other hand&#44; a series of alpha-asarone and fibrate-based analogs were designed by docking approaches with published crystal structures of human HMGR and the partial purification of the enzyme from <span class="elsevierStyleItalic">S&#46; pombe</span> allowed the test of analog compounds&#44; resulting in positive and significant inhibitory activity&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;24</span></a> The use of simvastatin in <span class="elsevierStyleItalic">C&#46; glabrata</span> has shown that in addition of reducing the levels of ergosterol and inhibiting growth&#44; this statin can lead to the loss of mitochondrial DNA &#40;mtDNA&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> This may restrict the use of statins as antifungal agents&#44; because&#44; the loss of mtDNA and the generation of &#8220;petite&#8221; mutants are related to azole resistance in <span class="elsevierStyleItalic">C&#46; glabrata</span>&#46; Therefore&#44; new synthetic compounds are being designed&#44; analogs of statins&#44; capable of inhibiting the synthesis of ergosterol but with no loss of mtDNA &#40;data not shown&#41;&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">HMGR enzyme as model to identify novel therapies to modulate cholesterol synthesis and to study sterol biosynthesis</span><p id="par0050" class="elsevierStylePara elsevierViewall">Although yeasts synthesize ergosterol instead of cholesterol&#44; fungi share many of the enzymes involved in the sterol synthesis pathway in mammals&#44; including HMGR&#46; Therefore&#44; the fungal HMGR have proven to be suitable models for studying the inhibition by compounds structurally related to statins or fibrates&#46; In this sense&#44; the enzyme from <span class="elsevierStyleItalic">S&#46; pombe</span> has been proposed as a model to study some aspects of regulation of sterol biosynthesis that have been difficult to address in other organisms&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;17&#44;20</span></a> Heterologous expression of genes encoding the HMGR from different fungi also has been successful to study pharmaceutical compounds inhibiting cholesterol synthesis&#46; Accordingly&#44; the <span class="elsevierStyleItalic">Rhizomucor miehei</span> HMGR gene&#44; has been expressed in <span class="elsevierStyleItalic">Mucor circinelloides</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> HMGR C-terminal from <span class="elsevierStyleItalic">U&#46; maydis</span> was expressed in <span class="elsevierStyleItalic">Escherichia coli</span> and shown to be blocked by a potent inhibitor of mammalian and fungal HMG-CoA reductases&#46;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusions</span><p id="par0055" class="elsevierStylePara elsevierViewall">Given the similarities in the initial steps of cholesterol and ergosterol synthesis pathways&#44; the fact that HMGR is a critical control point in both of them and that the enzyme from <span class="elsevierStyleItalic">S&#46; pombe</span> and <span class="elsevierStyleItalic">U&#46; maydis</span> are very similar to the human counterpart in the catalytic regions&#44; we propose that fungal enzymes can be used to test inhibitors with a potential use in humans&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Conflict of interest</span><p id="par0060" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interests&#46;</p></span></span>"
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          "titulo" => "Fungal HMGR gene organization"
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          "titulo" => "Characteristic structural features"
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          "titulo" => "Regulation by HMGR and sterol biosynthetic pathway in yeast"
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          "titulo" => "Inhibition of viability and ergosterol synthesis in yeasts as a consequence of the inhibition of the HMGR"
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          "titulo" => "HMGR enzyme as model to identify novel therapies to modulate cholesterol synthesis and to study sterol biosynthesis"
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          "titulo" => "Conclusions"
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            0 => "3-Hydroxy-3-methylglutaryl coenzyme A reductase"
            1 => "&#40;EC 1&#46;1&#46;1&#46;34&#41;"
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            0 => "3-Hidroxi-3-metilglutaril coenzima A reductasa"
            1 => "&#40;EC 1&#46;1&#46;1&#46;34&#41;"
            2 => "S&#237;ntesis de colesterol"
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        "resumen" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The enzyme 3-hydroxy-3-methylglutaryl coenzyme-A reductase &#40;HMGR&#41; catalyzes the conversion of HMG-Co-A into mevalonate&#46; This step is the limiting point for the synthesis of cholesterol in mammals and ergosterol in fungi&#46; We describe in this article the genome organization of HMGR coding genes and those deduced from different fungi&#44; recount the evidence showing statins as HMGR inhibitors for ergosterol synthesis and its effect in yeast viability&#44; and propose fungal HMGR &#40;HMGRf&#41; as a model to study the use of pharmaceutical compounds to inhibit cholesterol and ergosterol synthesis&#46; Bibliographical search and bioinformatic analyses were performed and discussed&#46; HMGRfs belong to the class I with a high homology in the catalytic region&#46; The sterol biosynthetic pathway in humans and fungi share many enzymes in the initial steps &#40;such as the HMGR enzyme&#41;&#44; but in the last steps enzymes are different rendering the two final products&#58; cholesterol in mammals and ergosterol in fungi&#46; With regards to inhibitors such as statins and other compounds&#44; these affect also fungal viability&#46; Since HMGR from <span class="elsevierStyleItalic">Schizosaccharomyces pombe</span> and <span class="elsevierStyleItalic">Ustilago maydis</span> are very similar to the human HMGR in the catalytic regions&#44; we propose that fungal enzymes can be used to test inhibitors for a potential use in humans&#46; We consider that HMGRf is a good therapeutic target to design and test new antifungal compounds&#46;</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">This manuscript is part of the series of works presented at the &#8220;V International Workshop&#58; Molecular genetic approaches to the study of human pathogenic fungi&#8221; &#40;Oaxaca&#44; Mexico&#44; 2012&#41;&#46;</p>"
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        "resumen" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">La enzima 3-hidroxi-3-metilglutaril coenzima A reductasa &#40;HMGR&#41; cataliza la conversi&#243;n de HMG-Co-A a mevalonato&#44; paso limitante en la s&#237;ntesis de colesterol en mam&#237;feros y de ergosterol en hongos&#46; El presente art&#237;culo describe la organizaci&#243;n de genes codificantes y prote&#237;nas de las diferentes HMGR de hongos &#40;HMGRf&#41;&#44; expone las evidencias disponibles en la inhibici&#243;n de HMGR en la s&#237;ntesis de ergosterol y su efecto en la viabilidad de los hongos&#44; y propone las HMGRf como modelo de estudio para la aplicaci&#243;n de f&#225;rmacos inhibidores de las s&#237;ntesis de colesterol y ergosterol&#46; Para ello se realiz&#243; una b&#250;squeda bibliogr&#225;fica y an&#225;lisis bioinform&#225;ticos&#44; con descripci&#243;n de los datos&#46; Las HMGRf son de clase <span class="elsevierStyleSmallCaps">i</span> y presentan una alta homolog&#237;a en la regi&#243;n catal&#237;tica&#46; La v&#237;a biosint&#233;tica de esteroles en el ser humano y en los hongos comparte algunas enzimas iniciales &#40;como la HMGR&#41; pero&#44; en los &#250;ltimos pasos&#44; las enzimas son diferentes&#44; lo que genera productos finales distintos&#58; colesterol y ergosterol&#44; respectivamente&#46; La inhibici&#243;n de HMGRf por estatinas afecta a la s&#237;ntesis de ergosterol y la viabilidad&#46; Dado que el sitio catal&#237;tico de las HMGR de <span class="elsevierStyleItalic">Schizosaccharomyces pombe</span> y <span class="elsevierStyleItalic">Ustilago maydis</span> es muy similar al de la enzima humana&#44; podr&#237;an servir como modelos para el estudio de f&#225;rmacos inhibidores de la s&#237;ntesis de colesterol&#46; La HMGRf es una diana terap&#233;utica adecuada para el dise&#241;o de nuevos antimic&#243;ticos&#46;</p><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Este art&#237;culo forma parte de una serie de estudios presentados en el &#171;V International Workshop&#58; Molecular genetic approaches to the study of human pathogenic fungi&#187; &#40;Oaxaca&#44; M&#233;xico&#44; 2012&#41;&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Schematic representation of HMGR proteins&#46; Diagram shows features of HMGR proteins from&#58; Human &#40;HMGR<span class="elsevierStyleInf">H</span>&#41;&#44; <span class="elsevierStyleItalic">S&#46; cerevisiae</span> &#40;HMGR<span class="elsevierStyleInf">SC1</span> and HMGR<span class="elsevierStyleInf">SC2</span>&#41;&#44; <span class="elsevierStyleItalic">S&#46; pombe</span> &#40;HMGR<span class="elsevierStyleInf">Sp</span>&#41;&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> &#40;HMGR<span class="elsevierStyleInf">Ca</span>&#41;&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span> &#40;HMGR<span class="elsevierStyleInf">Cg</span>&#41;&#44; <span class="elsevierStyleItalic">U&#46; maydis</span> &#40;HMGR<span class="elsevierStyleInf">Um</span>&#41;&#44; <span class="elsevierStyleItalic">C&#46; neoformans</span> &#40;HMGR<span class="elsevierStyleInf">Cn</span>&#41;&#44; and <span class="elsevierStyleItalic">A&#46; niger</span> &#40;HMGR<span class="elsevierStyleInf">An</span>&#41;&#46; Indicated domains are as follows&#58; Nter&#44; N-terminal domain containing a membrane anchor domain&#59; Linker &#40;connects membrane anchor domain to catalytic domain&#41;&#59; the catalytic domain which has subdomains N&#44; L&#44; S&#44; and L&#46; N domain&#58; connects L domain to linker&#59; L domain&#58; contains an HMG-CoA binding site&#59; S domain&#58; binds NADPH&#46; Black box shows the cis-loop connects the HMG-CoA-binding region with the NADP-H-binding region&#46;</p>"
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Model for the secondary structure of <span class="elsevierStyleItalic">Candida glabrata</span> HMGR &#40;HMGR<span class="elsevierStyleInf">Cg</span>&#41; and <span class="elsevierStyleItalic">Ustilago maydis</span> HMGR &#40;HMGR<span class="elsevierStyleInf">Um</span>&#41;&#46; Secondary structure was determined from HMGR<span class="elsevierStyleInf">Cg</span> &#40;A&#41; and HMGR<span class="elsevierStyleInf">Um</span> &#40;B&#41;&#46; Both enzymes show some characteristics of other eukaryotic HMGRs&#44; this is&#58; an amino terminus facing the lumen of the endoplasmic reticulum and the carboxyl terminus facing the cytoplasm&#44; eighth or four transmembrane segments &#40;<span class="elsevierStyleItalic">C&#46; glabrata</span> and <span class="elsevierStyleItalic">U&#46; maydis</span>&#44; respectively&#41;&#44; and a multimerization domain which forms the binding domain for the substrate and the cofactor NADPH&#46;</p>"
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                  \t\t\t\t"><span class="elsevierStyleItalic">H&#46; sapiens</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">S&#46; pombe</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">C&#46; glabrata</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">Similarity&#47;identity &#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">Similarity&#47;identity &#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">Similarity&#47;identity &#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">Similarity&#47;identity &#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Mus musculus</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">52&#46;64&#47;48&#46;08&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Rattus norvegicus</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Homo sapiens</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">18&#46;60&#47;6&#46;07&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">13&#46;86&#47;5&#46;01&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">S&#46; cerevisiae</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">&#40;<span class="elsevierStyleItalic">HMG1&#47;HMG2</span>&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">S&#46; pombe</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">C&#46; albicans</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">19&#46;72&#47;7&#46; 76&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">C&#46; glabrata</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Candida dubliniensis</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">C&#46; parapsilosis</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">C&#46; neoformans</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Yarrowia lipolytica</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">U&#46; maydis</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
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                  """
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                  \t\t\t\t\ttop\n
                  \t\t\t\t">HMG2&nbsp;\t\t\t\t\t\t\n
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        "texto" => "<p id="par0065" class="elsevierStylePara elsevierViewall">We would like to thank Cesar I&#46; Ort&#237;z-Garc&#237;a for assisting us preparing material for this review&#46; DAP&#44; ESS&#44; and BRA&#44; are CONACyT fellowships&#44; DAP is PIFI fellowship&#44; and grants from <span class="elsevierStyleGrantSponsor" id="gs0005">CONACyT</span> 133695 and <span class="elsevierStyleGrantSponsor" id="gs0010">SIP-IPN-20131171</span> were received&#46; JT&#44; CHR and LVT are EDI and COFAA fellowships&#46; JAI was hired by program &#8220;Contrataci&#243;n de investigadores para el apoyo a la investigaci&#243;n y posgrado-IPN&#8221;&#46;</p>"
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Article information

ISSN: 11301406
Original language: English

DOI:10.1016/j.riam.2013.10.004

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Year/Month	Html	Pdf	Total

2024 October	42	3	45
2024 September	92	9	101
2024 August	70	8	78
2024 July	58	4	62
2024 June	63	1	64
2024 May	45	2	47
2024 April	62	7	69
2024 March	73	6	79
2024 February	68	4	72
2024 January	107	6	113
2023 December	68	4	72
2023 November	72	5	77
2023 October	104	15	119
2023 September	77	3	80
2023 August	65	7	72
2023 July	69	8	77
2023 June	86	2	88
2023 May	98	3	101
2023 April	75	0	75
2023 March	103	2	105
2023 February	76	13	89
2023 January	72	19	91
2022 December	47	7	54
2022 November	35	12	47
2022 October	61	13	74
2022 September	69	21	90
2022 August	70	10	80
2022 July	45	8	53
2022 June	26	5	31
2022 May	38	16	54
2022 April	42	19	61
2022 March	59	7	66
2022 February	80	5	85
2022 January	71	9	80
2021 December	42	8	50
2021 November	38	12	50
2021 October	53	19	72
2021 September	43	12	55
2021 August	40	4	44
2021 July	38	11	49
2021 June	42	12	54
2021 May	64	16	80
2021 April	139	22	161
2021 March	73	13	86
2021 February	60	15	75
2021 January	65	21	86
2020 December	52	16	68
2020 November	94	16	110
2020 October	42	36	78
2020 September	24	15	39
2020 August	40	15	55
2020 July	26	15	41
2020 June	39	13	52
2020 May	42	17	59
2020 April	41	7	48
2020 March	40	9	49
2020 February	34	12	46
2020 January	32	9	41
2019 December	30	20	50
2019 November	39	13	52
2019 October	56	6	62
2019 September	58	5	63
2019 August	46	16	62
2019 July	40	13	53
2019 June	89	14	103
2019 May	161	18	179
2019 April	57	37	94
2019 March	21	3	24
2019 February	18	7	25
2019 January	19	5	24
2018 December	27	9	36
2018 November	41	6	47
2018 October	38	26	64
2018 September	16	5	21
2018 August	22	6	28
2018 July	14	3	17
2018 June	16	2	18
2018 May	16	12	28
2018 April	24	4	28
2018 March	15	0	15
2018 February	20	3	23
2018 January	9	4	13
2017 December	16	1	17
2017 November	26	3	29
2017 October	23	4	27
2017 September	5	5	10
2017 August	7	10	17
2017 July	15	4	19
2017 June	28	15	43
2017 May	21	17	38
2017 April	12	3	15
2017 March	18	26	44
2017 February	18	4	22
2017 January	13	3	16
2016 December	26	7	33
2016 November	33	8	41
2016 October	39	3	42
2016 September	37	7	44
2016 August	27	8	35
2016 July	43	3	46
2016 June	36	11	47
2016 May	31	16	47
2016 April	23	16	39
2016 March	19	21	40
2016 February	17	19	36
2016 January	18	20	38
2015 December	19	15	34
2015 November	16	10	26
2015 October	19	16	35
2015 September	26	9	35
2015 August	46	10	56
2015 July	33	9	42
2015 June	19	7	26
2015 May	28	6	34
2015 April	20	16	36
2015 March	8	12	20
2015 February	14	2	16
2015 January	12	3	15
2014 December	8	3	11
2014 November	8	2	10
2014 October	10	3	13
2014 September	20	6	26
2014 August	27	11	38
2014 July	19	12	31
2014 June	18	6	24
2014 May	22	9	31
2014 April	17	11	28
2014 March	14	6	20
2014 February	13	7	20

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