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array:23 [ "pii" => "S1807593221000028" "issn" => "18075932" "doi" => "10.1016/j.clinsp.2021.100002" "estado" => "S300" "fechaPublicacion" => "2022-01-01" "aid" => "100002" "copyright" => "HCFMUSP" "copyrightAnyo" => "2022" "documento" => "article" "crossmark" => 1 "subdocumento" => "fla" "cita" => "Clinics. 2022;77C:" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "itemSiguiente" => array:17 [ "pii" => "S180759322100003X" "issn" => "18075932" "doi" => "10.1016/j.clinsp.2021.100003" "estado" => "S300" "fechaPublicacion" => "2022-01-01" "aid" => "100003" "documento" => "article" "crossmark" => 1 "subdocumento" => "fla" "cita" => "Clinics. 2022;77C:" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "en" => array:12 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Original articles</span>" "titulo" => "Cardiopulmonary exercise test in patients with refractory angina: functional and ischemic evaluation" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => array:2 [ 0 => "en" 1 => "en" ] "contieneResumen" => array:1 [ "en" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:8 [ "identificador" => "fig0003" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2051 "Ancho" => 1500 "Tamanyo" => 91326 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0006" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spara003" class="elsevierStyleSimplePara elsevierViewall">Relationship between HR at onset of flattening oxygen pulse response detected by CPET and ischemic changes with contractile modifications in the ESE (panel A); and HR at onset of angina detected by CPET and ESE. CPET, cardiopulmonary exercise test; ESE, exercise stress echocardiography.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Camila R.A. de Assumpção, Danilo M.L. do Prado, Camila P. Jordão, Luciana O.C. Dourado, Marcelo L.C. Vieira, Carla G. de S.P. Montenegro, Carlos E. Negrão, Luís H.W. Gowdak, Luciana D.N.J. De Matos" "autores" => array:9 [ 0 => array:2 [ "nombre" => "Camila R.A." "apellidos" => "de Assumpção" ] 1 => array:2 [ "nombre" => "Danilo M.L." "apellidos" => "do Prado" ] 2 => array:2 [ "nombre" => "Camila P." "apellidos" => "Jordão" ] 3 => array:2 [ "nombre" => "Luciana O.C." "apellidos" => "Dourado" ] 4 => array:2 [ "nombre" => "Marcelo L.C." "apellidos" => "Vieira" ] 5 => array:2 [ "nombre" => "Carla G. de S.P." "apellidos" => "Montenegro" ] 6 => array:2 [ "nombre" => "Carlos E." "apellidos" => "Negrão" ] 7 => array:2 [ "nombre" => "Luís H.W." "apellidos" => "Gowdak" ] 8 => array:2 [ "nombre" => "Luciana D.N.J." "apellidos" => "De Matos" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<span id="abss0001" class="elsevierStyleSection elsevierViewall"><p id="spara010" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="celist0001"><li class="elsevierStyleListItem" id="celistitem0001"><span class="elsevierStyleLabel">•</span><p id="para0002" class="elsevierStylePara elsevierViewall">OUES analysis is useful for assessing functional capacity in refractory angina.</p></li><li class="elsevierStyleListItem" id="celistitem0002"><span class="elsevierStyleLabel">•</span><p id="para0003" class="elsevierStylePara elsevierViewall">O<span class="elsevierStyleInf">2</span> pulse curve is correlated with contractile alterations in exercise echocardiogram.</p></li><li class="elsevierStyleListItem" id="celistitem0003"><span class="elsevierStyleLabel">•</span><p id="para0004" class="elsevierStylePara elsevierViewall">Cardiopulmonary exercise test is useful toll in patients with refractory angina.</p></li></ul></p></span>" ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S180759322100003X?idApp=UINPBA00004N" "url" => "/18075932/000000770000000C/v3_202308251443/S180759322100003X/v3_202308251443/en/main.assets" ] "itemAnterior" => array:18 [ "pii" => "S1807593222033221" "issn" => "18075932" "doi" => "10.1016/j.clinsp.2022.100121" "estado" => "S300" "fechaPublicacion" => "2022-01-01" "aid" => "100121" "copyright" => "HCFMUSP" "documento" => "simple-article" "crossmark" => 1 "subdocumento" => "edi" "cita" => "Clinics. 2022;77C:" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "en" => array:8 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Editorials</span>" "titulo" => "Sex differences in Parkinson's Disease: An emerging health question" "tienePdf" => "en" "tieneTextoCompleto" => "en" "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Luiz Philipe de Souza Ferreira, Rafael André da Silva, Matheus Marques Mesquita da Costa, Vinicius Moraes de Paiva Roda, Santiago Vizcaino, Nilma R.L.L. Janisset, Renata Ramos Vieira, José Marcos Sanches, José Maria Soares Junior, Manuel de Jesus Simões" "autores" => array:10 [ 0 => array:2 [ "nombre" => "Luiz" "apellidos" => "Philipe de Souza Ferreira" ] 1 => array:2 [ "nombre" => "Rafael" "apellidos" => "André da Silva" ] 2 => array:2 [ "nombre" => "Matheus" "apellidos" => "Marques Mesquita da Costa" ] 3 => array:2 [ "nombre" => "Vinicius" "apellidos" => "Moraes de Paiva Roda" ] 4 => array:2 [ "nombre" => "Santiago" "apellidos" => "Vizcaino" ] 5 => array:2 [ "nombre" => "Nilma R.L.L." "apellidos" => "Janisset" ] 6 => array:2 [ "nombre" => "Renata" "apellidos" => "Ramos Vieira" ] 7 => array:2 [ "nombre" => "José" "apellidos" => "Marcos Sanches" ] 8 => array:2 [ "nombre" => "José" "apellidos" => "Maria Soares Junior" ] 9 => array:2 [ "nombre" => "Manuel" "apellidos" => "de Jesus Simões" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1807593222033221?idApp=UINPBA00004N" "url" => "/18075932/000000770000000C/v3_202308251443/S1807593222033221/v3_202308251443/en/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Original articles</span>" "titulo" => "Long non-coding RNA DLGAP1 antisense RNA 1 accelerates glioma progression via the microRNA-628-5p/DEAD-box helicase 59 pathway" "tieneTextoCompleto" => true "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Ke-qi Hu, Xiang-sheng Ao" "autores" => array:2 [ 0 => array:2 [ "nombre" => "Ke-qi" "apellidos" => "Hu" ] 1 => array:4 [ "nombre" => "Xiang-sheng" "apellidos" => "Ao" "email" => array:1 [ 0 => "wo05818@163.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0001" ] ] ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Department of Neurosurgery, Xiangyang Central Hospital, Affiliated Hospital of Hubei University of Arts and Science, China" "identificador" => "aff0001" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0001" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:8 [ "identificador" => "fig0005" "etiqueta" => "Figure 5." "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 1095 "Ancho" => 1500 "Tamanyo" => 135670 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0005" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spara005" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">DLGAP1-AS1</span> regulates glioma cell proliferation, migration, invasion, and EMT via the miR-628-5p/DDX59 axis. A, The <span class="elsevierStyleItalic">DLGAP1-AS1</span> overexpression vector and <span class="elsevierStyleItalic">DLGAP1-AS1</span> overexpression vector+miR-628-5p mimic were transfected into LN299 cells, and the expression of <span class="elsevierStyleItalic">DLGAP1-AS1</span> was detected using qRT-PCR. B, qRT-PCR was used to detect the expression of <span class="elsevierStyleItalic">miR-628-5p</span> in LN299 cells. C, Western blotting was used to detect the expression of <span class="elsevierStyleItalic">DDX59</span> and EMT-related proteins E-cadherin and vimentin in LN299 cells. (D–E) The proliferation of LN229 cells was detected using CCK-8 (D) and EdU assays (E). F, Transwell assay was used to detect the migration and invasion of LN229 cells. The experiments were repeated three times, and the average was recorded. *p < 0.05, **p < 0.01, and ***p < 0.001, ns was not statistically significant.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0001" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0008">Introduction</span><p id="para0007" class="elsevierStylePara elsevierViewall">Glioma – a cancer of the brain and spinal cord – has a high recurrence rate, morbidity and mortality, and poor prognosis.<a class="elsevierStyleCrossRefs" href="#bib0001"><span class="elsevierStyleSup">1-3</span></a> Elucidating the mechanism of glioma progression has great significance with respect to improving the prognosis of patients with this deadly disease.</p><p id="para0008" class="elsevierStylePara elsevierViewall">Long non-coding RNAs (lncRNAs) are ≥ 200 nt in length, lack protein-coding capabilities but are involved in regulating biological processes, such as gene imprinting, RNA splicing, and chromatin modification.<a class="elsevierStyleCrossRefs" href="#bib0004"><span class="elsevierStyleSup">4-6</span></a> LncRNAs can control gene expression at the transcriptional and post-transcriptional levels and thus play key roles in cancer biology.<a class="elsevierStyleCrossRef" href="#bib0007"><span class="elsevierStyleSup">7</span></a> In addition, as lncRNA expression exhibits tissue specificity,<a class="elsevierStyleCrossRef" href="#bib0008"><span class="elsevierStyleSup">8</span></a> they may serve as biomarkers and potential therapeutic targets. For example, lncRNA <span class="elsevierStyleItalic">ATB</span> promotes the growth of gastric cancer by regulating the <span class="elsevierStyleItalic">miR-141-3p</span>/TGF-β2 axis.<a class="elsevierStyleCrossRef" href="#bib0009"><span class="elsevierStyleSup">9</span></a> LncRNA <span class="elsevierStyleItalic">SIK1-LNC</span> inhibits the proliferation and metastasis of lung cancer cells, and its expression is downregulated in lung cancer.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">10</span></a> Recently, lncRNA DLGAP1 antisense RNA 1 <span class="elsevierStyleItalic">(DLGAP1-AS1)</span> has been found to act as an oncogenic lncRNA with its expression upregulated in hepatocellular carcinoma.<a class="elsevierStyleCrossRef" href="#bib0011"><span class="elsevierStyleSup">11</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0012"><span class="elsevierStyleSup">12</span></a> However, little is known about the role of <span class="elsevierStyleItalic">DLGAP1-AS1</span> in gliomas.</p><p id="para0009" class="elsevierStylePara elsevierViewall">MicroRNAs (miRNAs) – small non-coding RNAs approximately 21–25 nt in length – are crucial players in cancer biology.<a class="elsevierStyleCrossRefs" href="#bib0013"><span class="elsevierStyleSup">13-16</span></a> They can repress gene expression by binding to the 3ʹ-untranslated region (3’-UTR) of an mRNA, regulating various physiological and pathological processes.<a class="elsevierStyleCrossRef" href="#bib0017"><span class="elsevierStyleSup">17</span></a> Reportedly, <span class="elsevierStyleItalic">miR-628-5p</span> represses the malignant phenotypes of glioma cells by targeting high mobility group protein B3 (<span class="elsevierStyleItalic">HMGB3</span>) and DEAD-box helicase 59 (<span class="elsevierStyleItalic">DDX59).</span> It is downregulated in glioma tissues and cells, indicating that <span class="elsevierStyleItalic">miR-628-5p</span> is a tumor suppressor in the brain.<a class="elsevierStyleCrossRef" href="#bib0018"><span class="elsevierStyleSup">18</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0019"><span class="elsevierStyleSup">19</span></a></p><p id="para0010" class="elsevierStylePara elsevierViewall">In the present study, the authors investigated the expression patterns, biological functions, and mechanisms of action of <span class="elsevierStyleItalic">DLGAP1-AS1</span> in gliomas. The authors found that <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression was significantly upregulated in glioma tissues and cell lines, and it promoted the proliferation, migration, invasion, and Epithelial-Mesenchymal Transition (EMT) of glioma cells. Mechanistically, <span class="elsevierStyleItalic">DLGAP1-AS1</span> functions as a competitive endogenous RNA (ceRNA) to sponge <span class="elsevierStyleItalic">miR-628-5p</span> and upregulate DDX59 expression. The present study proposes a novel ceRNA network for glioma progression.</p></span><span id="sec0002" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0009">Material and methods</span><span id="sec0003" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0010">Tissues collection</span><p id="para0011" class="elsevierStylePara elsevierViewall">Tissue samples were obtained from patients who underwent surgery in the Department of Neurosurgery, Xiangyang Central Hospital, from May 2014 to July 2018, including 59 glioma tissue samples and 59 corresponding adjacent non-tumor tissue samples. After removal, the samples were stored in liquid nitrogen at -196°C. This study followed the 2007 World Health Organization (WHO) classification of tumors of the central nervous system (WHO grade I, n = 12: pilocytic astrocytomas (n = 8) and myxopapillary ependymomas (n = 4); grade II, n = 23: diffuse astrocytomas (n = 17), oligoastrocytomas (n = 3), and oligodendrogliomas (n = 3); grade III, n=14, anaplastic astrocytomas (n=6), anaplastic oligodendrogliomas (n = 5), and anaplastic oligoastrocytomas (n = 3); grade IV, n = 10: glioblastomas). The tumor samples were divided into low-grade tumors (grade I and II, n = 35) and high-grade tumors (grade III and IV, n = 24).<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">20</span></a> This study was approved by the Research Ethics Committee of the Xiangyang Central Hospital. Written informed consent was obtained from each patient.</p></span><span id="sec0004" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0011">Cell lines and cell culture</span><p id="para0012" class="elsevierStylePara elsevierViewall">The Cell Bank of Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences (Shanghai, China) provided the glioma cell lines (U-118MG, U251, U87MG, and LN229 cells), astroglia cell line (HA cells), and human embryonic kidney cell line (HEK-293 cells). The cells were maintained in Dulbecco's modified Eagle's medium (DMEM, Thermo Fisher Scientific, Waltham, MA, USA) supplemented with 10% fetal bovine serum (FBS, Gibco, Carlsbad, CA, USA), 100 U/mL penicillin, and 100 μg/mL streptomycin (Gibco, Carlsbad, CA, USA) in 5% CO<span class="elsevierStyleInf">2</span> at 37°C.</p></span><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0012">Quantitative real-time polymerase chain reaction (qRT-PCR)</span><p id="para0013" class="elsevierStylePara elsevierViewall">To determine <span class="elsevierStyleItalic">DLGAP1-AS1</span> and <span class="elsevierStyleItalic">DDX59</span> expression, the authors extracted the total RNA from tissues or cells using TRIzol reagent (Invitrogen, Carlsbad, CA, USA), reverse transcribed cDNA using a reverse transcriptase kit (Takara, Dalian, China), and performed qRT-PCR with SYBR Green Master Mix (Takara, Dalian, China). The NormFinder program was used to determine the appropriate housekeeping genes for the normalization of qRT-PCR data. After evaluating <span class="elsevierStyleItalic">GAPDH</span> (M-value = 0.518) and <span class="elsevierStyleItalic">ACTB</span> (M-value=0.646), the authors used them as the endogenous controls.<a class="elsevierStyleCrossRef" href="#bib0021"><span class="elsevierStyleSup">21</span></a> To determine <span class="elsevierStyleItalic">miR-628-5p</span> expression, qRT-PCR was performed using a TaqMan miRNA reverse transcription kit (Applied Biosystems, Grand Island, NY) with U6 and U48 as endogenous controls. Relative expression levels of <span class="elsevierStyleItalic">DLGAP1-AS1, DDX59,</span> and <span class="elsevierStyleItalic">miR-628-5p</span> were estimated using the 2<span class="elsevierStyleSup">−△△CT</span> method, △Ct=Ct (target gene)−Ct (endogenous control), △△Ct=△Ct (test group)−△Ct(normal group).<a class="elsevierStyleCrossRef" href="#bib0022"><span class="elsevierStyleSup">22</span></a> The primer sequences were as follows: <span class="elsevierStyleItalic">DLGAP1-AS1</span> forward, 5′-TATGATGATATCAAGAGGGTAGT-3′ and reverse, 5′-TGTATCCAAACTCATTGTCATAC-3′. <span class="elsevierStyleItalic">DDX59</span> forward, 5′-GATGTTCCCGTTGATGCTGT-3′ and reverse, 5′-GAGCTTTATTCGAGAGCAAAACT-3′. <span class="elsevierStyleItalic">GAPDH</span> forward, 5′-TGGGTGTGAACCATGAGAAG-3′ and reverse, 5′-GTGTCGCTGTTGAAGTCAGA-3′. <span class="elsevierStyleItalic">ACTB</span> forward, 5′-GTCAGGTCATCACTATCGGCAAT-3′ and reverse, 5′-AGAGGTCTTTACGGATGTCAACGT-3′. <span class="elsevierStyleItalic">miR-628-5p</span> primers, <span class="elsevierStyleItalic">U6</span> and <span class="elsevierStyleItalic">U48</span> were provided in the TaqMan miRNA reverse transcription kit.</p></span><span id="sec0006" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0013">Cell transfection</span><p id="para0014" class="elsevierStylePara elsevierViewall">Specific short hairpin RNAs (shRNAs) against <span class="elsevierStyleItalic">DLGAP1-AS1</span> (sh-<span class="elsevierStyleItalic">DLGAP1-AS1</span>#1, sh-<span class="elsevierStyleItalic">DLGAP1-AS1</span>#2, and sh-<span class="elsevierStyleItalic">DLGAP1-AS1</span>#3), negative control shRNA (sh-NC), pcDNA3.1 vector overexpressing DLGAP1-AS1, and the empty vector were all purchased from GeneChem (Shanghai, China). miR-628-5p mimics, miR-628-5p inhibitor, negative control mimic (NC mimic), and negative control inhibitor (NC inhibitor) were obtained from GenePharma (Shanghai, China). U251, U87MG, or LN229 cells were transfected with Lipofectamine 3000 (Invitrogen, Carlsbad, CA, USA) according to the manufacturer's instructions.</p></span><span id="sec0007" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0014">Cell counting kit-8 (CCK-8) assay</span><p id="para0015" class="elsevierStylePara elsevierViewall">The transfected glioma cells were transferred into a 96-well plate (1 × 10<span class="elsevierStyleSup">3</span> cells/well), and CCK-8 solution (Dojindo Laboratories, Kumamoto, Japan) was loaded into each well at 0, 24, 48, 72, and 96h, respectively, followed by incubation for 3h. The absorbance of each well was recorded at 450 nm using a microplate reader (BioTek, Winooski, VT, USA).</p></span><span id="sec0008" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0015">5-Ethynyl-2′-deoxyuridine (EdU) assay</span><p id="para0016" class="elsevierStylePara elsevierViewall">The EdU kit was obtained from RiboBio (Guangzhou, China). The transfected cells were cultured in a 96-well plate (5 × 10<span class="elsevierStyleSup">3</span> cells/well) for 24h and then incubated with 50 mM EdU reagent for 4h. After discarding the medium, the cells were fixed with 4% paraformaldehyde and incubated for 30 min in the dark with the Apollo fluorescent staining solution. The authors then washed them twice with PBS and incubated with Hoechst staining solution for 20 min. Finally, the authors rinsed the cells three times with PBS and observed and counted them under a fluorescence microscope.</p></span><span id="sec0009" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0016">Transwell assay</span><p id="para0017" class="elsevierStylePara elsevierViewall">Transwell assays were performed using a Transwell system with 8 μm pore size (Corning Incorporated, Corning, NY, USA). In the migration assay, 100 μL of cell suspension (approximately 1 × 10<span class="elsevierStyleSup">4</span> cells) prepared in serum-free medium was added to the upper chamber, and 500 μL of medium containing 10% FBS was added to the lower chamber. After the cells were cultured for 12h, the cells on the upper side of the membrane were scraped off, and the remaining cells were fixed with 4% paraformaldehyde and then stained with 0.1% crystal violet for 30 min. Subsequently, the number of stained cells was counted under a microscope. For the cell invasion assay, 50 μL of diluted Matrigel (1:8, Sigma-Aldrich, St Louis, MO, USA) was dripped into the upper chamber of the Transwell system to cover the membrane before the inoculation of the cells, and the remaining steps were the same as in the migration assay.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0017">Dual-luciferase reporter assay</span><p id="para0018" class="elsevierStylePara elsevierViewall">Wild-type and mutant type <span class="elsevierStyleItalic">DLGAP1-AS1</span> sequences containing <span class="elsevierStyleItalic">miR-628-5p</span> binding sites were synthesized and inserted into the pGL3 vector (Promega, Madison, WI, USA) to construct a wide-type reporter plasmid (DLGAP1-AS1-WT) and mutant reporter plasmid (DLGAP1-AS1-MUT). HEK-293 cells were then co-transfected with the reporter plasmids, miR-628-5p mimic, or control miRNA using Lipofectamine 3000 (Invitrogen, Carlsbad, CA, USA). After 48h, the cells were harvested, and the luciferase activity of each group was measured using a Dual-Luciferase Reporter Assay kit (Promega, Madison, WI, USA).</p></span><span id="sec0011" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0018">Western blot</span><p id="para0019" class="elsevierStylePara elsevierViewall">Total protein was extracted using RIPA buffer (Beyotime, Shanghai, China). Protein samples were quantified using a BCA Protein Assay Kit (Pierce, Rockford, IL, USA), suspended in loading buffer, and denatured. Subsequently, the protein samples were separated via SDS-PAGE and transferred to polyvinylidene fluoride membranes (Life Technologies, Gaithersburg, MD, USA). After blocking with 5% skimmed milk for 1h at room temperature, the PVDF membranes were incubated with primary antibody [Anti-DDX59 (Abcam, ab109592, 1:200) or anti-GAPDH (Abcam, ab8245, 1:2000)] at 4°C overnight and then with secondary antibody (HRP-labeled, Beyotime, 1:2000) for 1.5h at room temperature. Finally, the protein bands were visualized using an ECL Plus kit (Life Technologies, Gaithersburg, MD, USA). GAPDH was used as an endogenous control.</p></span><span id="sec0012" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0019">Statistical analysis</span><p id="para0020" class="elsevierStylePara elsevierViewall">The data are shown as the mean ± standard deviation. The normality of the data was evaluated using the Kolmogorov-Smirnov test. For normally distributed data, the Student's <span class="elsevierStyleItalic">t</span>-test or one-way analysis of variance (ANOVA) was employed to analyze the differences between two or multiple groups. For skewed data, comparisons between two groups were performed using the Wilcoxon signed-rank test. In survival analysis, glioblastoma (GBM) patients were divided into two groups: <span class="elsevierStyleItalic">DLGAP1-AS1</span> high expression (group cutoff: 50%) and <span class="elsevierStyleItalic">DLGAP1-AS1</span> low expression (group cutoff: 50%) (n=81 in each group), and the overall survival rate of GBM patients was analyzed using the Kaplan-Meier method and log-rank test. GraphPad Prism 6.0 was used for drafting, and SPSS software (version 18.0; SPSS, Inc., Chicago, IL, USA) was used for statistical analysis. Statistical significance was set at p < 0.05.</p></span></span><span id="sec0013" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0020">Results</span><span id="sec0014" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0021">DLGAP1-AS1 expression is elevated in glioma tissues and cell lines</span><p id="para0021" class="elsevierStylePara elsevierViewall">The GEPIA database showed that <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in GBM tissues was higher than that in normal tissues (<a class="elsevierStyleCrossRef" href="#fig0001">Fig. 1</a>A). Additionally, Kaplan-Meier survival analysis revealed that high <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression was associated with poor survival in GBM patients (<a class="elsevierStyleCrossRef" href="#fig0001">Fig. 1</a>B). Next, the authors performed qRT-PCR to determine <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in gliomas and adjacent non-tumor tissues of 59 glioma patients. The results indicated that <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in glioma tissues was remarkably higher than that in adjacent non-tumor tissues, and <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression was higher in high-grade tumor samples than in low-grade tumor samples (<a class="elsevierStyleCrossRef" href="#fig0001">Fig. 1</a>C and Supplementary Fig. 1A). Consistently, <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression was significantly elevated in glioma cell lines (compared to that in HA cells) (<a class="elsevierStyleCrossRef" href="#fig0001">Fig. 1</a>D and Supplementary Fig. 1B). In U251 and U87MG cells, <span class="elsevierStyleItalic">DLGAP1-AS1</span> was highly expressed, and therefore, U251 and U87MG cells were chosen for the follow-up experiments.</p><elsevierMultimedia ident="fig0001"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0022">DLGAP1-AS1 knockdown represses the proliferation, migration, invasion, and EMT of glioma cells</span><p id="para0022" class="elsevierStylePara elsevierViewall">To determine the biological function of <span class="elsevierStyleItalic">DLGAP1-AS1</span> in glioma cells, the authors used shRNAs to knockdown <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in U251 and U87MG cells and determined the transfection efficiency using qRT-PCR. It was found that sh-DLGAP1-AS1#1 had the highest efficiency and used it for subsequent experiments (<a class="elsevierStyleCrossRef" href="#fig0002">Fig. 2</a>A and Supplementary Fig. 1C). CCK-8 and EdU assays suggested that <span class="elsevierStyleItalic">DLGAP1-AS1</span> knockdown significantly reduced the proliferation of U251 and U87MG cells compared to the control group (<a class="elsevierStyleCrossRef" href="#fig0002">Fig. 2</a>B-D). The authors performed Transwell assays to evaluate the migration and invasion of glioma cells and found that <span class="elsevierStyleItalic">DLGAP1-AS1</span> knockdown markedly reduced the migration and invasion of U251 and U87MG cells (compared with the control group) (<a class="elsevierStyleCrossRef" href="#fig0002">Fig. 2</a>E-F). Additionally, western blotting suggested that <span class="elsevierStyleItalic">DLGAP1-AS1</span> knockdown increased E-cadherin expression and decreased vimentin expression in glioma cells (<a class="elsevierStyleCrossRef" href="#fig0002">Fig. 2</a>G). These findings highlight that <span class="elsevierStyleItalic">DLGAP1-AS1</span> knockdown could repress the malignancy of glioma cells.</p><elsevierMultimedia ident="fig0002"></elsevierMultimedia></span><span id="sec0016" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0023">DLGAP1-AS1 targets miR-628-5p in glioma</span><p id="para0023" class="elsevierStylePara elsevierViewall">To identify the candidate miRNAs that could interact with <span class="elsevierStyleItalic">DLGAP1-AS1</span>, the authors searched the StarBase database (version 2.0) and found that the <span class="elsevierStyleItalic">DLGAP1-AS1</span> sequence had a binding site for <span class="elsevierStyleItalic">miR-628-5p</span> (<a class="elsevierStyleCrossRef" href="#fig0003">Fig. 3</a>A). The results of the dual-luciferase reporter assay revealed that <span class="elsevierStyleItalic">miR-628-5p</span> restrains the luciferase activity of the DLGAP1-AS1-WT reporter but had no significant effect on the luciferase activity of the DLGAP1-AS1-MUT reporter (<a class="elsevierStyleCrossRef" href="#fig0003">Fig. 3</a>B). qRT-PCR showed elevated expression of <span class="elsevierStyleItalic">miR-628-5p</span> in U251 and U87MG cells transfected with sh-DLGAP1-AS1, indicating that <span class="elsevierStyleItalic">DLGAP1-AS1</span> negatively regulates <span class="elsevierStyleItalic">miR-628-5p</span> expression (<a class="elsevierStyleCrossRef" href="#fig0003">Fig. 3</a>C and Supplementary Fig. 1D). Additionally, consistent with a previous report,<a class="elsevierStyleCrossRef" href="#bib0018"><span class="elsevierStyleSup">18</span></a><span class="elsevierStyleItalic">miR-628-5p</span> expression was significantly decreased in glioma tissues (compared to that in adjacent non-tumor tissues) (<a class="elsevierStyleCrossRef" href="#fig0003">Fig. 3</a>D and Supplementary Fig. 1E). Next, the authors analyzed the correlation between <span class="elsevierStyleItalic">DLGAP1-AS1</span> and <span class="elsevierStyleItalic">miR-628-5p</span> expression in glioma tissues using Pearson's correlation analysis, and the authors demonstrated that <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression was negatively correlated with <span class="elsevierStyleItalic">miR-628-5p</span> expression in glioma tissues (<a class="elsevierStyleCrossRef" href="#fig0003">Fig. 3</a>E, R<span class="elsevierStyleSup">2</span>=0.3425), further implying that <span class="elsevierStyleItalic">DLGAP1-AS1</span> targets <span class="elsevierStyleItalic">miR-628-5p</span> and represses its expression in gliomas.</p><elsevierMultimedia ident="fig0003"></elsevierMultimedia></span><span id="sec0017" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0024">Inhibiting miR-628-5p promotes the proliferation, migration, invasion, and EMT of glioma cells</span><p id="para0024" class="elsevierStylePara elsevierViewall">Previous studies have shown that <span class="elsevierStyleItalic">miR-628-5p</span> overexpression inhibits the proliferation of glioma cells.<a class="elsevierStyleCrossRef" href="#bib0018"><span class="elsevierStyleSup">18</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0019"><span class="elsevierStyleSup">19</span></a> In the present study, the authors transfected <span class="elsevierStyleItalic">miR-628-5p</span> inhibitor into U251 and U87MG cells and verified the transfection efficiency using qRT-PCR (<a class="elsevierStyleCrossRef" href="#fig0004">Fig. 4</a>A and Supplementary Fig. 1F). Subsequently, CCK-8, EdU, and Transwell assays and western blotting revealed that the inhibiting <span class="elsevierStyleItalic">miR-628-5p</span> promoted the proliferation, migration, invasion, and EMT of U251 and U87MG cells, indicating that <span class="elsevierStyleItalic">miR-628-5p</span> exerted tumor-suppressive functions in gliomas (<a class="elsevierStyleCrossRef" href="#fig0004">Fig. 4</a>B-G).</p><elsevierMultimedia ident="fig0004"></elsevierMultimedia></span><span id="sec0018" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0025">DLGAP1-AS1 regulates glioma cell proliferation, migration, invasion, and EMT via the miR-628-5p/DDX59 axis</span><p id="para0025" class="elsevierStylePara elsevierViewall">Reportedly, <span class="elsevierStyleItalic">miR-628-5p</span> impedes the proliferation of glioma cells by negatively regulating DDX59 expression.<a class="elsevierStyleCrossRef" href="#bib0019"><span class="elsevierStyleSup">19</span></a> To elaborate on the mechanism of <span class="elsevierStyleItalic">DLGAP1-AS1</span> in the biology glioma cells, the authors performed compensation experiments. The authors divided LN229 cells into three groups and transfected them with either the empty vector+NC mimics, pcDNA3.1 overexpressing DLGAP1-AS1+NC mimics, or pcDNA3.1 overexpressing DLGAP1-AS1+miR-628-5p mimics (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 5</a>A-B and Supplementary Fig. 1G). Western blotting was performed to detect DDX59, E-cadherin, and vimentin expression after transfection. The authors found that <span class="elsevierStyleItalic">DLGAP1-AS1</span> overexpression promoted the expression of DDX59 and vimentin and repressed the expression of E-cadherin, while miR-628-5p overexpression partially reversed these effects (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 5</a>C). Furthermore, <span class="elsevierStyleItalic">DLGAP1-AS1</span> overexpression promoted the proliferation, migration, invasion, and EMT of LN229 cells, and co-transfection with miR-628-5p mimics partially counteracted the functions of <span class="elsevierStyleItalic">DLGAP1-AS1</span> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 5</a>D-F). These experiments indicated that <span class="elsevierStyleItalic">DLGAP1-AS1</span> could promote the proliferation, migration, invasion, and EMT of glioma cells by sponging <span class="elsevierStyleItalic">miR-628-5p</span> and upregulating DDX59 expression.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span></span><span id="sec0019" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0026">Discussion</span><p id="para0026" class="elsevierStylePara elsevierViewall">LncRNAs play vital roles in human diseases, including tumors.<a class="elsevierStyleCrossRef" href="#bib0023"><span class="elsevierStyleSup">23</span></a> They are abnormally expressed in diverse tumors, including glioma, and help regulate the malignant biological behaviors of tumor cells, such as proliferation, migration, invasion, apoptosis, and drug resistance.<a class="elsevierStyleCrossRef" href="#bib0024"><span class="elsevierStyleSup">24</span></a> Many lncRNAs are associated with the pathogenesis and progression of gliomas. For example, increased <span class="elsevierStyleItalic">LINC00689</span> expression in glioma tissues and cell lines is associated with rapid deterioration and poor prognosis of patients.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">25</span></a> LncRNA <span class="elsevierStyleItalic">PLAC2</span> inhibits the nuclear translocation of STAT1, thus reducing <span class="elsevierStyleItalic">RPL36</span> expression, inhibiting glioma cell proliferation, and inducing cell cycle arrest.<a class="elsevierStyleCrossRef" href="#bib0026"><span class="elsevierStyleSup">26</span></a> LncRNA <span class="elsevierStyleItalic">PVT1</span> promotes the expression of <span class="elsevierStyleItalic">BMP2</span> and <span class="elsevierStyleItalic">BMP4</span> by regulating <span class="elsevierStyleItalic">GREM1</span> expression and promoting glioma progression.<a class="elsevierStyleCrossRef" href="#bib0027"><span class="elsevierStyleSup">27</span></a> Herein, the authors confirmed the elevated <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in glioma, which was linked to unfavorable pathological characteristics and poor prognosis of the patients. Functionally, <span class="elsevierStyleItalic">DLGAP1-AS1</span> overexpression promoted the proliferation, migration, invasion, and EMT of glioma cells, while its knockdown exerted opposite effects, indicating that <span class="elsevierStyleItalic">DLGAP1-AS1</span> is a novel oncogenic lncRNA in glioma and might be a promising therapeutic target.</p><p id="para0027" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">miR-628-5p</span> is a well-known regulator in cancer biology. In most cancers, <span class="elsevierStyleItalic">miR-628-5p</span> functions as a tumor suppressor. However, the elevated levels of <span class="elsevierStyleItalic">miR-628-5p</span> in osteosarcoma are related to the adverse prognosis of the patients.<a class="elsevierStyleCrossRef" href="#bib0028"><span class="elsevierStyleSup">28</span></a> The serum of patients with prostate cancer has low levels of circulating <span class="elsevierStyleItalic">miR-628-5p</span>, suggesting that <span class="elsevierStyleItalic">miR-628-5p</span> is a promising non-invasive biomarker for the diagnosis and prognostic evaluation of prostate cancer. Functionally, <span class="elsevierStyleItalic">miR-628</span> reduces the proliferation and invasion of prostate cancer cells by repressing <span class="elsevierStyleItalic">FGFR2</span> expression.<a class="elsevierStyleCrossRef" href="#bib0029"><span class="elsevierStyleSup">29</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">30</span></a> In pancreatic ductal adenocarcinoma, <span class="elsevierStyleItalic">miR-628-5p</span> suppresses the migration and invasion of cancer cells by repressing Akt/NF-κB signaling.<a class="elsevierStyleCrossRef" href="#bib0031"><span class="elsevierStyleSup">31</span></a> In gastric cancer, <span class="elsevierStyleItalic">miR-628-5p</span> targets <span class="elsevierStyleItalic">PIN1</span> to inhibit cancer progression.<a class="elsevierStyleCrossRef" href="#bib0032"><span class="elsevierStyleSup">32</span></a> In glioma, <span class="elsevierStyleItalic">miR-628-5p</span> represses the malignant behavior of glioma cells.<a class="elsevierStyleCrossRef" href="#bib0018"><span class="elsevierStyleSup">18</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0019"><span class="elsevierStyleSup">19</span></a> In the present study, the authors found that reduced <span class="elsevierStyleItalic">miR-628-5p</span> expression in glioma tissues promoted the proliferation, migration, invasion, and EMT of glioma cells, further confirming the anti-tumor effects of <span class="elsevierStyleItalic">miR-628-5p</span> on glioma cells.</p><p id="para0028" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">DDX59</span> is a member of the DEAD/Deah box RNA helicase family.<a class="elsevierStyleCrossRef" href="#bib0033"><span class="elsevierStyleSup">33</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0034"><span class="elsevierStyleSup">34</span></a> Reportedly, <span class="elsevierStyleItalic">DDX59</span> is highly expressed in lung adenocarcinoma tissues and contributes to the growth of EGFR⁻ lung cancer cells.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">35</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0036"><span class="elsevierStyleSup">36</span></a><span class="elsevierStyleItalic">DDX59</span> knockdown restrained the proliferation of glioma cells, and DDX59 overexpression partially weakened the inhibitory effects of <span class="elsevierStyleItalic">miR-628-5p</span>, suggesting that it is also an oncogene in gliomas.<a class="elsevierStyleCrossRef" href="#bib0019"><span class="elsevierStyleSup">19</span></a> In the present study, the authors proposed a ceRNA network of <span class="elsevierStyleItalic">DLGAP1-AS1, miR-628-5p,</span> and <span class="elsevierStyleItalic">DDX59</span>. LncRNAs, like ceRNAs, can modulate gene expression by competitively binding to miRNAs, and an imbalance in the ceRNA network can cause diseases.<a class="elsevierStyleCrossRef" href="#bib0037"><span class="elsevierStyleSup">37</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#bib0038"><span class="elsevierStyleSup">38</span></a> For example, in gastric cancer, <span class="elsevierStyleItalic">LINC01133</span> sponges <span class="elsevierStyleItalic">miR-106-3p</span> to upregulate <span class="elsevierStyleItalic">APC</span> expression and inhibit cancer progression.<a class="elsevierStyleCrossRef" href="#bib0037"><span class="elsevierStyleSup">37</span></a> In hepatocellular carcinoma, as a ceRNA, <span class="elsevierStyleItalic">DLGAP1-AS1</span> elevates the level of the carcinogenic cytokine IL-6 by sponging <span class="elsevierStyleItalic">miR-26a/b-5p</span> and activating the Wnt/β-catenin pathway.<a class="elsevierStyleCrossRef" href="#bib0012"><span class="elsevierStyleSup">12</span></a> In the present study, through bioinformatics analysis, a dual-luciferase reporter assay, and qRT-PCR, the interaction between <span class="elsevierStyleItalic">DLGAP1-AS1</span> and <span class="elsevierStyleItalic">miR-628-5p</span> was predicted and validated in glioma cells. The authors also demonstrated that <span class="elsevierStyleItalic">DLGAP1-AS1</span> promotes the malignant phenotypes of glioma cells by sponging <span class="elsevierStyleItalic">miR-628-5p</span> and elevating <span class="elsevierStyleItalic">DDX59</span> expression. These results not only partly explain the mechanism underlying the dysregulation of <span class="elsevierStyleItalic">miR-628-5p</span> and <span class="elsevierStyleItalic">DDX59</span> in gliomas but also elucidate the mechanism by which <span class="elsevierStyleItalic">DLGAP1-AS1</span> participates in glioma progression.</p><p id="para0029" class="elsevierStylePara elsevierViewall">To briefly recapitulate, the present study confirms that <span class="elsevierStyleItalic">DLGAP1-AS1</span> is overexpressed in glioma and promotes aggressive cancer progression by regulating the <span class="elsevierStyleItalic">miR-628-5p</span>/<span class="elsevierStyleItalic">DDX59</span> axis. These findings help clarify the mechanism of glioma progression and provide potential targets for molecular therapy of gliomas. In future studies, animal experiments are needed to verify these results, and it is necessary to enroll more patients from different medical centers to evaluate the potential value of <span class="elsevierStyleItalic">DLGAP1-AS1</span> as a biomarker to predict the prognosis of the patients.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0027">Author contributions</span><p id="para0030" class="elsevierStylePara elsevierViewall">Ke-qi Hu and Xiang-sheng Ao contributed equally to the experimental design and execution, statistical analysis, and manuscript writing.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:3 [ "identificador" => "xres1954011" "titulo" => "Highlights" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abss0001" ] ] ] 1 => array:3 [ "identificador" => "xres1954012" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abss0003" "titulo" => "Objectives" ] 1 => array:2 [ "identificador" => "abss0004" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abss0005" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abss0006" "titulo" => "Conclusion" ] ] ] 2 => array:2 [ "identificador" => "xpalclavsec1682100" "titulo" => "Keywords" ] 3 => array:2 [ "identificador" => "sec0001" "titulo" => "Introduction" ] 4 => array:3 [ "identificador" => "sec0002" "titulo" => "Material and methods" "secciones" => array:10 [ 0 => array:2 [ "identificador" => "sec0003" "titulo" => "Tissues collection" ] 1 => array:2 [ "identificador" => "sec0004" "titulo" => "Cell lines and cell culture" ] 2 => array:2 [ "identificador" => "sec0005" "titulo" => "Quantitative real-time polymerase chain reaction (qRT-PCR)" ] 3 => array:2 [ "identificador" => "sec0006" "titulo" => "Cell transfection" ] 4 => array:2 [ "identificador" => "sec0007" "titulo" => "Cell counting kit-8 (CCK-8) assay" ] 5 => array:2 [ "identificador" => "sec0008" "titulo" => "5-Ethynyl-2′-deoxyuridine (EdU) assay" ] 6 => array:2 [ "identificador" => "sec0009" "titulo" => "Transwell assay" ] 7 => array:2 [ "identificador" => "sec0010" "titulo" => "Dual-luciferase reporter assay" ] 8 => array:2 [ "identificador" => "sec0011" "titulo" => "Western blot" ] 9 => array:2 [ "identificador" => "sec0012" "titulo" => "Statistical analysis" ] ] ] 5 => array:3 [ "identificador" => "sec0013" "titulo" => "Results" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0014" "titulo" => "DLGAP1-AS1 expression is elevated in glioma tissues and cell lines" ] 1 => array:2 [ "identificador" => "sec0015" "titulo" => "DLGAP1-AS1 knockdown represses the proliferation, migration, invasion, and EMT of glioma cells" ] 2 => array:2 [ "identificador" => "sec0016" "titulo" => "DLGAP1-AS1 targets miR-628-5p in glioma" ] 3 => array:2 [ "identificador" => "sec0017" "titulo" => "Inhibiting miR-628-5p promotes the proliferation, migration, invasion, and EMT of glioma cells" ] 4 => array:2 [ "identificador" => "sec0018" "titulo" => "DLGAP1-AS1 regulates glioma cell proliferation, migration, invasion, and EMT via the miR-628-5p/DDX59 axis" ] ] ] 6 => array:2 [ "identificador" => "sec0019" "titulo" => "Discussion" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Author contributions" ] 8 => array:2 [ "identificador" => "xack684943" "titulo" => "Acknowledgments" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2021-05-17" "fechaAceptado" => "2021-10-15" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1682100" "palabras" => array:4 [ 0 => "Glioma" 1 => "<span class="elsevierStyleItalic">DLGAP1-AS1</span>" 2 => "<span class="elsevierStyleItalic">miR-628-5p</span>" 3 => "<span class="elsevierStyleItalic">DDX59</span>" ] ] ] ] "tieneResumen" => true "highlights" => array:2 [ "titulo" => "Highlights" "resumen" => "<span id="abss0001" class="elsevierStyleSection elsevierViewall"><p id="spara006" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="celist0001"><li class="elsevierStyleListItem" id="celistitem0001"><span class="elsevierStyleLabel">•</span><p id="para0001" class="elsevierStylePara elsevierViewall">The expression of DLGAP1-AS1 expression is increased in glioma.</p></li><li class="elsevierStyleListItem" id="celistitem0002"><span class="elsevierStyleLabel">•</span><p id="para0002" class="elsevierStylePara elsevierViewall">DLGAP1-AS1 promotes the malignancy of glioma via modulating miR-628-5p/DDX59 axis.</p></li></ul></p></span>" ] "resumen" => array:1 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "<span id="abss0003" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0003">Objectives</span><p id="spara007" class="elsevierStyleSimplePara elsevierViewall">Abnormal expression of long non-coding RNAs (lncRNAs) plays a prominent role in glioma progression. However, the biological function and mechanism of lncRNA DLGAP1 antisense RNA 1 (<span class="elsevierStyleItalic">DLGAP1-AS1</span>) in gliomas are still unknown.</p></span> <span id="abss0004" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0004">Methods</span><p id="spara008" class="elsevierStyleSimplePara elsevierViewall">The authors assessed <span class="elsevierStyleItalic">DLGAP1-AS1</span> and <span class="elsevierStyleItalic">miR-628-5p</span> expression in glioma tissues and cell lines using quantitative real-time polymerase chain reaction (qRT-PCR) and evaluated their effects on glioma cell proliferation, migration, invasion, and epithelial-mesenchymal transition (EMT) using the cell counting kit-8 (CCK-8) assay, 5-Ethynyl-2′-deoxyuridine (EdU) assay, Transwell assay, and western blot, respectively. The expression of DEAD-box helicase 59 (<span class="elsevierStyleItalic">DDX59</span>) was quantified using western blotting, and a dual-luciferase reporter gene assay was performed to detect the interaction between <span class="elsevierStyleItalic">DLGAP1-AS1</span> and <span class="elsevierStyleItalic">miR-628-5p</span>.</p></span> <span id="abss0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0005">Results</span><p id="spara009" class="elsevierStyleSimplePara elsevierViewall">The authors observed increased <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in glioma tissues and cell lines with higher WHO grades and shorter survival time. <span class="elsevierStyleItalic">DLGAP1-AS1</span> promoted the proliferation, migration, invasion, and EMT of glioma cells, while <span class="elsevierStyleItalic">miR-628-5p</span> counteracted these effects. The authors identified <span class="elsevierStyleItalic">DLGAP1-AS1</span> as a molecular sponge of <span class="elsevierStyleItalic">miR-628-5p</span> in glioma cells as the biological functions of <span class="elsevierStyleItalic">DLGAP1-AS1</span> are partially mediated via <span class="elsevierStyleItalic">miR-628-5p</span>. In addition, <span class="elsevierStyleItalic">DLGAP1-AS1</span> upregulated <span class="elsevierStyleItalic">DDX59</span> expression by inhibiting <span class="elsevierStyleItalic">miR-628-5p</span> expression.</p></span> <span id="abss0006" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cesectitle0006">Conclusion</span><p id="spara010" class="elsevierStyleSimplePara elsevierViewall">The <span class="elsevierStyleItalic">DLGAP1-AS1</span>/<span class="elsevierStyleItalic">miR-628-5p</span>/<span class="elsevierStyleItalic">DDX59</span> axis regulates glioma progression.</p></span>" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abss0003" "titulo" => "Objectives" ] 1 => array:2 [ "identificador" => "abss0004" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abss0005" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abss0006" "titulo" => "Conclusion" ] ] ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "<p id="para0031a" class="elsevierStylePara elsevierViewall"><elsevierMultimedia ident="ecom0001"></elsevierMultimedia></p>" "etiqueta" => "Appendix" "titulo" => "Supplementary materials" "identificador" => "sec0022" ] ] ] ] "multimedia" => array:6 [ 0 => array:8 [ "identificador" => "fig0001" "etiqueta" => "Figure 1." "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1372 "Ancho" => 1166 "Tamanyo" => 123487 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0001" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spara001" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">DLGAP1-AS1</span> expression is upregulated in glioma tissues and cell lines. A, Bioinformatic analysis was used to analyze <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in GBM and normal brain tissues. B, The GEPIA database was used to perform survival analysis of GBM patients with high and low <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression. C, The expression of <span class="elsevierStyleItalic">DLGAP1-AS1</span> in glioma tissues and adjacent non-tumor tissues was detected using qRT-PCR (n = 59). D, <span class="elsevierStyleItalic">DLGAP1-AS1</span> expression in glioma cell lines (U-118MG, U251, U87MG, and LN229 cells) and normal cell lines (HA cells) was detected using qRT-PCR. The experiments were repeated three times, and the average was recorded. *p < 0.05, **p < 0.01, and ***p < 0.001.</p>" ] ] 1 => array:8 [ "identificador" => "fig0002" "etiqueta" => "Figure 2." "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2123 "Ancho" => 2334 "Tamanyo" => 341482 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0002" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spara002" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">DLGAP1-AS1</span> knockdown suppresses the proliferation, migration, invasion, and EMT of glioma cells. A, sh-NC, sh-DLGAP1-AS1#1, sh-DLGAP1-AS1#2, and sh-DLGAP1-AS1#3 were transfected into U251 and U87MG cells to construct low expression models of <span class="elsevierStyleItalic">DLGAP1-AS1</span>, and the transfection efficiency was determined using qRT-PCR. (B–D) The proliferation of U251 and U87MG cells transfected with sh-NC or sh-DLGAP1-AS1#1 was detected using CCK-8 (B) and EdU assays (C–D). (E–F) Transwell assay was used to detect the migration and invasion of U251 cells (E) and U87MG cells (F) transfected with sh-NC or sh-DLGAP1-AS1#1. G, The expression levels of EMT-related proteins E-cadherin and vimentin in U251 and U87MG cells transfected with sh-NC or sh-DLGAP1-AS1#1 were detected using western blotting. The experiments were repeated three times, and the average was recorded. *p < 0.05, **p < 0.01, and ***p < 0.001, ns was not statistically significant.</p>" ] ] 2 => array:8 [ "identificador" => "fig0003" "etiqueta" => "Figure 3." "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2411 "Ancho" => 2917 "Tamanyo" => 395783 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0003" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spara003" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">DLGAP1-AS1</span> targets <span class="elsevierStyleItalic">miR-628-5p</span> in glioma. A, <span class="elsevierStyleItalic">DLGAP1-AS1</span>-WT luciferase reporter vector and <span class="elsevierStyleItalic">DLGAP1-AS1</span>-MUT luciferase reporter vector were constructed. B, <span class="elsevierStyleItalic">DLGAP1-AS1</span>-WT or <span class="elsevierStyleItalic">DLGAP1-AS1</span>-MUT luciferase reporter vector and miR-628-5p mimics or control miRNA were co-transfected into HEK-293T cells, and the luciferase activity of the cells in each group was determined. C, qRT-PCR was used to detect the expression of <span class="elsevierStyleItalic">miR-628-5p</span> in U251 and U87MG cells transfected with sh-NC or sh-DLGAP1-AS1#1. D, The expression of <span class="elsevierStyleItalic">miR-628-5p</span> in glioma cell lines (U-118MG, U251, U87MG, and LN229 cells) and normal cell lines (HA cells) was detected using qRT-PCR. E, Pearson's correlation analysis showed that the expression of <span class="elsevierStyleItalic">DLGAP1-AS1</span> and <span class="elsevierStyleItalic">miR-628-5p</span> was negatively correlated in glioma tissues. The experiments were repeated three times, and the average was recorded. **p < 0.01 and ***p < 0.001.</p>" ] ] 3 => array:8 [ "identificador" => "fig0004" "etiqueta" => "Figure 4." "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 1365 "Ancho" => 1500 "Tamanyo" => 187789 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0004" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spara004" class="elsevierStyleSimplePara elsevierViewall">The inhibition of <span class="elsevierStyleItalic">miR-628-5p</span> expression promotes the proliferation, migration, invasion, and EMT of glioma cells. A, miRNA inhibitor control (miR-con in) and miR-628-5p inhibitor (miR-628-5p in) were transfected into U251 and U87MG cells to construct models of the inhibition of miR-628-5p expression, and the transfection efficiency was detected using qRT-PCR. (B–D) The proliferation of U251 and U87MG cells was detected using CCK-8 (B) and EdU assays (C-D). (E-F) Transwell assay was used to detect the migration and invasion of U251 (E) and U87MG cells (F). G, Western blot assay was used to detect the expression of EMT-related proteins E-cadherin and vimentin in U251 and U87MG cells. The experiments were repeated three times, and the average was recorded. *p < 0.05, **p < 0.01, and ***p < 0.001.</p>" ] ] 4 => array:8 [ "identificador" => "fig0005" "etiqueta" => "Figure 5." "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 1095 "Ancho" => 1500 "Tamanyo" => 135670 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0005" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "<p id="spara005" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">DLGAP1-AS1</span> regulates glioma cell proliferation, migration, invasion, and EMT via the miR-628-5p/DDX59 axis. A, The <span class="elsevierStyleItalic">DLGAP1-AS1</span> overexpression vector and <span class="elsevierStyleItalic">DLGAP1-AS1</span> overexpression vector+miR-628-5p mimic were transfected into LN299 cells, and the expression of <span class="elsevierStyleItalic">DLGAP1-AS1</span> was detected using qRT-PCR. B, qRT-PCR was used to detect the expression of <span class="elsevierStyleItalic">miR-628-5p</span> in LN299 cells. C, Western blotting was used to detect the expression of <span class="elsevierStyleItalic">DDX59</span> and EMT-related proteins E-cadherin and vimentin in LN299 cells. (D–E) The proliferation of LN229 cells was detected using CCK-8 (D) and EdU assays (E). F, Transwell assay was used to detect the migration and invasion of LN229 cells. The experiments were repeated three times, and the average was recorded. *p < 0.05, **p < 0.01, and ***p < 0.001, ns was not statistically significant.</p>" ] ] 5 => array:6 [ "identificador" => "ecom0001" "tipo" => "MULTIMEDIAECOMPONENTE" "mostrarFloat" => false "mostrarDisplay" => true "detalles" => array:1 [ 0 => array:3 [ "identificador" => "alt0006" "detalle" => "Image, application " "rol" => "short" ] ] "Ecomponente" => array:2 [ "fichero" => "mmc1.docx" "ficheroTamanyo" => 136713 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "cebibsec1" "bibliografiaReferencia" => array:38 [ 0 => array:3 [ "identificador" => "bib0001" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Two novel genetic variants in the STK38L and RAB27A genes are associated with glioma susceptibility" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "H Chen" 1 => "G Chen" 2 => "G Li" 3 => "S Zhang" 4 => "H Chen" 5 => "Y Chen" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1002/ijc.32179" "Revista" => array:7 [ "tituloSerie" => "Int J Cancer" "fecha" => "2019" "volumen" => "145" "numero" => "9" "paginaInicial" => "2372" "paginaFinal" => "2382" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/30714141" "web" => "Medline" ] ] ] ] ] ] ] ] 1 => array:3 [ "identificador" => "bib0002" "etiqueta" => "2" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Tumor infiltrating immune cells in gliomas and meningiomas" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "P Domingues" 1 => "M González-Tablas" 2 => "Á Otero" 3 => "D Pascual" 4 => "D Miranda" 5 => "L Ruiz" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.bbi.2015.07.019" "Revista" => array:6 [ "tituloSerie" => "Brain Behav Immun" "fecha" => "2016" "volumen" => "53" "paginaInicial" => "1" "paginaFinal" => "15" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/26216710" "web" => "Medline" ] ] ] ] ] ] ] ] 2 => array:3 [ "identificador" => "bib0003" "etiqueta" => "3" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "B7-H3 as a novel CAR-T therapeutic target for glioblastoma" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "X Tang" 1 => "S Zhao" 2 => "Y Zhang" 3 => "Y Wang" 4 => "Z Zhang" 5 => "M Yang" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.omto.2019.07.002" "Revista" => array:6 [ "tituloSerie" => "Mol Ther Oncolytics" "fecha" => "2019" "volumen" => "14" "paginaInicial" => "279" "paginaFinal" => "287" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/31485480" "web" => "Medline" ] ] ] ] ] ] ] ] 3 => array:3 [ "identificador" => "bib0004" "etiqueta" => "4" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Risk assessment model constructed by differentially expressed lncRNAs for the prognosis of glioma" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "C Hu" 1 => "Y Zhou" 2 => "C Liu" 3 => "Y. 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