Información del artículo
Resumen
Las ficolinas son proteínas de defensa que forman oligómeros a partir de tallos homólogos al colágeno y dominios semejantes a fibrinógeno. Son capaces de sentir señales de peligro tales como patrones moleculares asociados patógenos o a células apoptóticas. En el hombre, las ficolinas L y H se han caracterizado en el suero, mientras que la ficolina M es secretada por células monocíticas. Al igual que la lectina de unión a manano (“mannan-binding lectin”, MBL), pueden asociarse a las serina-proteasas asociadas a MBL e iniciar la vía de activación de complemento de las lectinas, un importante sistema efector de la inmunidad innata humoral. También pueden actuar como opsoninas, incrementando la eliminación de sus dianas por fagocitosis. Estudios estructurales recientes muestran que la ficolina L es una proteína de reconocimiento versátil, capaz de unir moléculas acetiladas y carbohidratos neutros por medio de sitios de unión diferentes, mientras que la ficolina H posee un único sitio de unión con una especificidad más restringida hacia los carbohidratos neutros. Los estudios filogenéticos revelan que las ficolinas han sido conservadas en el proceso evolutivo, apoyando la hipótesis de que el sistema de complemento primitivo era un sistema de opsonización basado en lectinas, y ponen de relieve la importancia de las proteínas de reconocimiento de carbohidratos en la inmunidad innata.
Palabras clave:
Ficolina
Inmunidad Innata
Receptores de reconocimiento de modelos
Activación del Complemento
MASP
Abstract
Ficolins are oligomeric defence proteins assembled from collagen-like stalks and fibrinogen-like domains that are able to sense danger signals such as pathogen- or apoptotic cell-associated molecular patterns. In humans, L- and H-ficolins have been characterized in serum whereas M-ficolin is secreted by monocytic cells. Like mannan-binding lectin (MBL), they are able to associate with MBL-associated serine proteases and to trigger activation of the lectin pathway of complement, a major effector system of humoral innate immunity. They can also act as opsonins to enhance clearance of their targets by phagocytosis. Recent structural studies have shown that L-ficolin is a versatile recognition protein able to bind acetylated molecules and neutral carbohydrates through different binding sites, whereas H-ficolin has a single binding site with a more restricted specificity for neutral carbohydrates. Phylogenetic studies reveal that ficolins have been conserved through evolution, supporting the hypothesis that the primitive complement system was a lectin-based opsonic system, and emphasizing the essential role of carbohydrate recognition proteins in innate immunity.
Key words:
Ficolin
Innate immunity
Pattern recognition receptor
Complement activation
MASP
El Texto completo está disponible en PDF
References
[1.]
D.T. Fearon, R.M. Locksley.
The instructive role of innate immunity in the acquired immune response.
Science, 272 (1996), pp. 50-53
[2.]
P. Matzinger.
The danger model: a renewed sense of self.
Science, 296 (2002), pp. 301-305
[3.]
C.A. Janeway.
Approaching the asymptote? Evolution and revolution in immunology.
Cold Spring Harbor Symp Quant Biol, 54 (1989), pp. 1-13
[4.]
N.C. Franc, K. White, R.A. Ezekowitz.
Phagocytosis and development: back to the future.
Curr Opin Immunol, 11 (1999), pp. 47-52
[5.]
G.J. Arlaud, M.G. Colomb, J. Gagnon.
A functional model of the human C1 complex.
Immunol Today, 8 (1987), pp. 106-111
[6.]
M. Gadjeva, S. Thiel, J.C. Jensenius.
The mannan-binding-lectin pathway of the innate immune response.
Curr Opin Immunol, 13 (2001), pp. 74-78
[7.]
M. Matsushita, T. Fujita.
Ficolins and the lectin complement pathway.
Immunol Rev, 180 (2001), pp. 78-85
[8.]
M.C. Caroll.
The complement system in regulation of adaptive immunity.
Nat Immunol, 5 (2004), pp. 981-986
[9.]
H. Ichijo, L. Rönnstrand, K. Miyagawa, H. Ohashi, C.H. Heldin, K. Miyazono.
Purification of transforming growth factor-beta 1 binding proteins from porcine uterus membranes.
J Biol Chem, 266 (1991), pp. 22459-22464
[10.]
H. Ichijo, U. Hellman, C. Wernstedt, L.J. Gonez, L. Claesson-Welsh, C.H. Heldin, et al.
Molecular cloning and characterization of ficolin, a multimeric protein with fibrinogen- and collagen-like domains.
J Biol Chem, 268 (1993), pp. 14505-14513
[11.]
Y. Le, S.M. Tan, S.H. Lee, O.L. Kon, J. Lu.
Purification and binding properties of a human ficolin-like protein.
J Immunol Methods, 204 (1997), pp. 43-49
[12.]
P.F. Edgar.
Hucolin, a new corticosteroid-binding protein from human plasma with structural similarities to ficolins, transforming growth factor-beta 1-binding proteins.
FEBS Lett, 375 (1995), pp. 159-161
[13.]
S. Harumiya, A. Omori, T. Sugiura, Y. Fukumoto, H. Tachikawa, D. Fujimoto.
EBP-37, a new elastin-binding protein in human plasma: structural similarity to ficolins, transforming growth factor-beta 1- binding proteins.
J Biochem (Tokyo), 117 (1995), pp. 1029-1035
[14.]
M. Matsushita, Y. Endo, S. Taira, Y. Sato, T. Fujita, N. Ichikawa, et al.
A novel human serum lectin with collagen- and fibrinogen-like domains that functions as an opsonin.
J Biol Chem, 271 (1996), pp. 2448-2454
[15.]
Y. Le, S.H. Lee, O.L. Kon, J. Lu.
Human L-ficolin: plasma levels, sugar specificity, and assignment of its lectin activity to the fibrinogen-like (FBG) domain.
FEBS Lett, 425 (1998), pp. 367-370
[16.]
D.C. Kilpatrick, T. Fujita, M. Matsushita.
P35, an opsonic lectin of the ficolin family, in human blood from neonates, normal adults, and recurrent miscarriage patients.
Immunol Lett, 67 (1999), pp. 109-112
[17.]
A. Krarup, U.B. Sørensen, M. Matsushita, J.C. Jensenius, S. Thiel.
Effect of capsulation of opportunistic pathogenic bacteria on binding of the pattern recognition molecules mannan-binding lectin L-ficolin, and H-ficolin.
Infect Immun, 73 (2005), pp. 1052-1060
[18.]
T. Hummelshoj, L. Munthe-Fog, H.O. Madsen, T. Fujita, M. Matsushita, P. Garred.
Polymorphisms in the FCN2 gene determine serum variation and function of Ficolin-2.
Hum Mol Genet, 14 (2005), pp. 1651-1658
[19.]
K.C. Gulla, K. Gupta, R.K. Gupta, V. Vyas, K. Hajela.
Development of a fluorescence assay for the detection of L-ficolin-MASP in serum or purified samples.
J Biochem Biophys Methods, 66 (2006), pp. 59-71
[20.]
L. Munthe-Fog, T. Hummelshøj, B.E. Hansen, C. Koch, H.O. Madsen, K. Skjødt, et al.
The impact of FCN2 polymorphisms and haplotypes on the Ficolin-2 serum levels.
Scand J Immunol, 65 (2007), pp. 383-392
[21.]
S. Taira, N. Kodama, M. Matsushita, T. Fujita.
Opsonic function and concentration of human serum ficolin/P35.
Fukushima J Med Sci, 46 (2000), pp. 13-23
[22.]
Y. Endo, Y. Sato, M. Matsushita, T. Fujita.
Cloning and characterization of the human lectin P35 gene and its related gene.
Genomics, 36 (1996), pp. 515-521
[23.]
S. Inaba, K. Okochi.
On a new precipitating antibody against normal human serum found in two patients with SLE.
Igaku No Ayumi, 107 (1978), pp. 690-691
[24.]
Y. Yae, S. Inaba, H. Sato, K. Okochi, F. Tokunaga, S. Iwanaga.
Isolation and characterization of a thermolabile beta-2 macroglycoprotein (’thermolabile substance’ or ‘Hakata antigen’) detected by precipitating (auto) antibody in sera of patients with systemic lupus erythematosus.
Biochim Biophys Act, 1078 (1991), pp. 369-376
[25.]
R. Sugimoto, Y. Yae, M. Akaiwa, S. Kitajima, Y. Shibata, H. Sato, et al.
Cloning and characterization of the Hakata antigen, a member of the ficolin/opsonin p35 lectin family.
J Biol Chem, 273 (1998), pp. 20721-20727
[26.]
D.C. Kilpatrick, L.A. McLintock, E.K. Allan, M. Copland, T. Fujita, N.E. Jordanides, et al.
No strong relationship between mannan binding lectin or plasma ficolins and chemotherapy-related infections.
Clin Exp Immunol, 134 (2003), pp. 279-284
[27.]
M. Akaiwa, Y. Yae, R. Sugimoto, S.O. Suzuki, T. Iwaki, K. Izuhara, et al.
Hakata antigen, a new member of the ficolin/opsonin p35 family, is a novel human lectin secreted into bronchus/alveolus and bile.
Histochem Cytochem, 47 (1999), pp. 777-786
[28.]
M. Kuraya, M. Matsushita, Y. Endo, S. Thiel, T. Fujita.
Expression of H-ficolin/Hakata antigen, mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 by human glioma cell line T98G.
Int Immunol, 15 (2003), pp. 109-117
[29.]
Y. Endo, Y. Liu, K. Kanno, M. Takahashi, M. Matsushita, T. Fujita.
Identification of the mouse H-ficolin gene as a pseudogene and orthology between mouse ficolins A/B and human L-/M-ficolins.
Genomics, 84 (2004), pp. 737-744
[30.]
S. Harumiya, K. Takeda, T. Sugiura, Y. Fukumoto, H. Tachikawa, K. Miyazono, et al.
Characterization of ficolins as novel elastin-binding proteins and molecular cloning of human ficolin-1.
J Biochem (Tokyo), 120 (1996),
[31.]
J. Lu, P.N. Tay, O.L. Kon, K.B. Reid.
Human ficolin: cDNA cloning, demonstration of peripheral blood leucocytes as the major site of synthesis and assignment of the gene to chromosome 9.
Biochem J, 313 (1996), pp. 473-478
[32.]
C. Teh, Y. Le, S.H. Lee, J. Lu.
M-ficolin is expressed on monocytes and is a lectin binding to N-acetyl-D-glucosamine and mediates monocyte adhesion and phagocytosis of Escherichia coli.
Immunology, 101 (2000), pp. 225-232
[33.]
P.D. Frederiksen, S. Thiel, C.B. Larsen, J.C. Jensenius.
M-ficolin, an innate immune defence molecule, binds patterns of acetyl groups and activates complement.
Scand J Immunol, 62 (2005), pp. 462-473
[34.]
Y. Liu, Y. Endo, D. Iwaki, M. Nakata, M. Matsushita, I. Wada, et al.
Human M-ficolin is a secretory protein that activates the lectin complement pathway.
J Immunol, 175 (2005), pp. 3150-3156
[35.]
T. Ohashi, H.P. Erickson.
The disulfide bonding pattern in ficolin multimers.
J Biol Chem, 279 (2004), pp. 6534-6539
[36.]
T. Hummelshoj, N.M. Thielens, H.O. Madsen, G.J. Arlaud, R.B. Sim, P. Garred.
Molecular organization of human Ficolin-2.
Mol Immunol, 44 (2007), pp. 401-411
[37.]
T. Ohashi, H.P. Erickson.
Oligomeric structure and tissue distribution of ficolins from mouse, pig and human.
Arch Biochem Biophys, 360 (1998), pp. 223-232
[38.]
N.J. Lynch, S. Roscher, T. Hartung, S. Morath, M. Matsushita, D.N. Maennel, et al.
L-ficolin specifically binds to lipoteichoic acid, a cell wall constituent of Gram-positive bacteria, and activates the lectin pathway of complement.
J Immunol, 172 (2004), pp. 1198-1202
[39.]
Y.G. Ma, M.Y. Cho, M. Zhao, J.W. Park, M. Matsushita, T. Fujita, et al.
Human mannose-binding lectin and L-ficolin function as specific pattern recognition proteins in the lectin activation pathway of complement.
J Biol Chem, 279 (2004), pp. 25307-25312
[40.]
A. Krarup, S. Thiel, A. Hansen, T. Fujita, J.C. Jensenius.
L-ficolin is a pattern recognition molecule specific for acetyl groups.
J Biol Chem, 279 (2004), pp. 47513-47519
[41.]
Y. Aoyagi, E.E. Adderson, J.G. Min, M. Matsushita, T. Fujita, S. Takahashi, et al.
Role of L-ficolin/mannose-binding lectin-associated serine protease complexes in the opsonophagocytosis of type III group B streptococci.
J Immunol, 174 (2005), pp. 418-425
[42.]
M. Matsushita, M. Kuraya, N. Hamasaki, M. Tsujimura, H. Shiraki, T. Fujita.
Activation of the lectin complement pathway by H-ficolin (Hakata antigen).
J Immunol, 168 (2002), pp. 3502-3506
[43.]
M. Tsujimura, C. Ishida, Y. Sagara, T. Miyazaki, K. Murakami, H. Shiraki, et al.
Detection of serum thermolabile beta-2 macroglycoprotein (Hakata antigen) by enzyme-linked immunosorbent assay using polysaccharide produced by Aerococcus viridans.
Clin Diagn Lab Immunol, 8 (2001), pp. 454-459
[44.]
M. Kuraya, Z. Ming, X. Liu, M. Matsushita, T. Fujita.
Specific binding of L-ficolin and H-ficolin to apoptotic cells leads to complement activation.
Immunobiology, 209 (2005), pp. 689-697
[45.]
C. Honoré, T. Hummelshoj, B.E. Hansen, H.O. Madsen, P. Eggleton, P. Garred.
The innate immune component ficolin 3 (Hakata antigen) mediates the clearance of late apoptotic cells.
Arthritis Rheum, 56 (2007), pp. 1598-1607
[46.]
M.L. Jensen, C. Honoré, T. Hummelshøj, B.E. Hansen, H.O. Madsen, P. Garred.
Ficolin-2 recognizes DNA and participates in the clearance of dying host cells.
Mol Immunol, 44 (2007), pp. 856-865
[47.]
V. Garlatti, N. Belloy, L. Martin, M. Lacroix, M. Matsushita, Y. Endo, et al.
Structural insights into the innate immune recognition specificities of L- and H-ficolins.
EMBO J, 26 (2007), pp. 623-633
[48.]
N. Kairies, H.G. Beisel, P. Fuentes-Prior, R. Tsuda, T. Muta, S. Iwanaga, et al.
The 2.0-A crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems.
Proc Natl Acad Sci U S A, 98 (2001), pp. 13519-13524
[49.]
W.I. Weis, K. Drickamer, W.A. Hendrickson.
Structure of a C-type mannose-binding protein complexed with an oligosaccharide.
Nature, 360 (1992), pp. 127-134
[50.]
M. Tanio, S. Kondo, S. Sugio, T. Kohno.
Trivalent recognition unit of innate immunity system: crystal structure of trimeric human Mficolin fibrinogen-like domain.
J Biol Chem, 282 (2007), pp. 3889-3895
[51.]
C. Gaboriaud, J. Juanhuix, A. Gruez, M. Lacroix, C. Darnault, D. Pignol, et al.
The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties.
J Biol Chem, 278 (2003), pp. 46974-46982
[52.]
W.I. Weis, K. Drickamer.
Trimeric structure of a C-type mannose-binding protein.
Structure, 2 (1994), pp. 1227-1240
[53.]
S. Sheriff, C.Y. Chang, R.A. Ezekowitz.
Human mannose-binding protein carbohydrate recognition domain trimerizes through a triple alpha-helical coiled-coil.
Nat Struct Biol, 1 (1994), pp. 789-974
[54.]
K. Ikeda, T. Sannoh, N. Kawasaki, T. Kawasaki, I. Yamashina.
Serum lectin with known structure activates complement through the classical pathway.
J Biol Chem, 262 (1987), pp. 7451-7454
[55.]
Y.H. Ji, T. Fujita, H. Hatsuse, A. Takahashi, M. Matsushita, M. Kawakami.
Activation of the C4 and C2 components of complement by a proteinase in serum bactericidal factor, Ra reactive factor.
J Immunol, 150 (1993), pp. 571-578
[56.]
M. Matsushita, T. Fujita.
Activation of the classical complement pathway by mannose-binding protein in association with a novel C1s-like serine protease.
J Exp Med, 176 (1992), pp. 1497-1502
[57.]
F. Takada, Y. Takayama, H. Hatsuse, M. Kawakami.
A new member of the C1s family of complement proteins found in a bactericidal factor, Ra-reactive factor, in human serum.
Biochem Biophys Res Commun, 196 (1993), pp. 1003-1009
[58.]
S. Thiel, T. Vorup-Jensen, C.M. Stover, W. Schwaeble, S.B. Laursen, K. Poulsen, et al.
A second serine protease associated with mannan-binding lectin that activates complement.
Nature, 386 (1997), pp. 506-510
[59.]
M.R. Dahl, S. Thiel, M. Matsushita, T. Fujita, A.C. Willis, T. Christensen, et al.
MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway.
Immunity, 15 (2001), pp. 127-135
[60.]
C.M. Stover, S. Thiel, M. Thelen, N.J. Lynch, T. Vorup-Jensen, J.C. Jensenius, et al.
Two constituents of the initiation complex of the mannanbinding lectin activation pathway of complement are encoded by a single structural gene.
J Immunol, 162 (1999),
[61.]
M. Takahashi, Y. Endo, T. Fujita, M. Matsushita.
A truncated form of mannose-binding lectin-associated serine protease (MASP)-2 expressed by alternative polyadenylation is a component of the lectin complement pathway.
Int Immunol, 11 (1999), pp. 859-863
[62.]
T. Vorup-Jensen, S.V. Petersen, A. Hansen, K. Poulsen, W. Schwaeble, R.B. Sim, et al.
Distinct pathways of mannan-binding lectin (MBL)-and C1-complex autoactivation revealed by reconstitution of MBL with recombinant MBL-associated serine protease-2.
J Immunol, 165 (2000), pp. 2093-2100
[63.]
M. Matsushita, Y. Endo, T. Fujita.
Complement-activating complex of ficolin and mannose-binding lectin-associated serine protease.
J Immunol, 164 (2000), pp. 2281-2284
[64.]
R. Wallis, R.B. Dodd.
Interaction of mannose-binding protein with associated serine proteases: effects of naturally occurring mutations.
J Biol Chem, 275 (2000), pp. 30962-30969
[65.]
N.M. Thielens, S. Cseh, S. Thiel, T. Vorup-Jensen, V. Rossi, J.C. Jensenius, et al.
Interaction properties of human mannan-binding lectin (MBL)-associated serine proteases-1 and -2, MBL-associated protein 19, and MBL.
J Immunol, 166 (2001), pp. 5068-5077
[66.]
S. Cseh, L. Vera, M. Matsushita, T. Fujita, G.J. Arlaud, N.M. Thielens.
Characterization of the interaction between L-ficolin/p35 and mannan-binding lectin-associated serine proteases-1 and -2.
J Immunol, 169 (2002), pp. 5735-5743
[67.]
S. Zundel, S. Cseh, M. Lacroix, M.R. Dahl, M. Matsushita, J-.P. Andrieu, et al.
Characterization of recombinant mannan-binding lectin-associated serine protease (MASP)-3 suggests an activation mechanism different from that of MASP-1 and MASP-2.
J Immunol, 172 (2004), pp. 4342-4350
[68.]
L.A. Gregory, N.M. Thielens, M. Matsushita, R. Sorensen, G.J. Arlaud, J.C. Fontecilla-Camps, et al.
The X-ray structure of human mannan-binding lectin-associated protein 19 (MAp19) and its interaction site with mannan-binding lectin and L-ficolin.
J Biol Chem, 279 (2004), pp. 29391-29397
[69.]
F. Teillet, C. Gaboriaud, L. Martin, M. Lacroix, S. Ogbi, J.C. Fontecilla-Camps, et al.
The CUB1-EGF-CUB2 interaction domain of human MBL-associated serine protease-3: X-ray structure and binding sites for MBL and ficolins.
Mol Immunol, 44 (2007), pp. 249
[70.]
F. Teillet, M. Lacroix, S. Thiel, D. Weilguny, T. Agger, G.J. Arlaud, et al.
Identification of the site of human mannan-binding lectin involved in the interaction with its partner serine proteases: the essential role of Lys55.
J Immunol, 178 (2007), pp. 5710-5716
[71.]
R. Wallis, J.M. Shaw, J. Uitdehaag, C.-B. Chen, D. Torgersen, K. Drickamer.
Localization of the serine protease-binding sites in the collagen-like domain of mannose-binding protein.
J Biol Chem, 279 (2004), pp. 14065-14073
[72.]
F. Teillet, B. Dublet, J.-P. Andrieu, C. Gaboriaud, G.J. Arlaud, N.M. Thielens.
The two major oligomeric forms of human mannan-binding lectin: chemical characterization, carbohydrate-binding properties, and interaction with MBL-associated serine proteases.
J Immunol, 174 (2005), pp. 2870-2877
[73.]
C.B. Chen, R. Wallis.
Two mechanisms for mannose-binding protein modulation of the activity of its associated serine proteases.
J Biol Chem, 279 (2004), pp. 26058-26065
[74.]
G.R. Stuart, N.J. Lynch, A.J. Day, W.J. Schwaeble, R.B. Sim.
The C1q and collectin binding site within C1q receptor (cell surface calreticulin).
Immunopharmacology, 38 (1997), pp. 73-80
[75.]
C.A. Ogden, A. deCathelineau, P.R. Hoffmann, D. Bratton, B. Ghebrehiwet, V.A. Fadok, et al.
C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells.
J Exp Med, 194 (2001), pp. 781-795
[76.]
R.W. Vandivier, C.A. Ogden, V.A. Fadok, P.R. Hoffmann, K.K. Brown, M. Botto, et al.
Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex.
J Immunol, 169 (2002), pp. 3978-3986
[77.]
M. Arora, E. Munoz, A.J. Tenner.
Identification of a site on mannan-binding lectin critical for enhancement of phagocytosis.
J Biol Chem, 276 (2001), pp. 43087-43094
[78.]
P. Steinberger, A. Szekeres, S. Wille, J. Stöckl, N. Selenko, E. Prager, et al.
Identification of human CD93 as the phagocytic C1q receptor (C1qRp) by expression cloning.
J Leukoc Biol, 71 (2002), pp. 133-140
[79.]
P.J. Norsworthy, L. Fossati-Jimack, J. Cortes-Hernandez, P.R. Taylor, A.E. Bygrave, R.D. Thompson, et al.
Murine CD93 (C1qRp) contributes to the removal of apoptotic cells in vivo but is not required for C1q-mediated enhancement of phagocytosis.
J Immunol, 172 (2004), pp. 3406-3414
[80.]
L.B. Klickstein, S.F. Barbashov, T. Liu, R.M. Jack, A. Nicholson-Weller.
Complement receptor type 1 (CR1, CD35) is a receptor for C1q.
Immunity, 7 (1997), pp. 345-355
[81.]
I. Ghiran, S.F. Barbashov, L.B. Klickstein, S.W. Tas, J.C. Jensenius, A. Nicholson-Weller.
Complement receptor 1/CD35 is a receptor for mannan-binding lectin.
J Exp Med, 192 (2000), pp. 1797-1808
[82.]
B.T. Edelson, T.P. Stricker, Z. Li, S.K. Dickeson, V.L. Shepherd, S.A. Santoro, et al.
Novel collectin/C1q receptor mediates mast cell activation and innate immunity.
Blood, 107 (2006), pp. 143-150
[83.]
B.L. Herpers, M.M. Immink, B.A. de Jong, H. van Velzen-Blad, B.M. de Jongh, E.J. van Hannen.
Coding and non-coding polymorphisms in the lectin pathway activator L-ficolin gene in 188 Dutch blood bank donors.
Mol Immunol, 43 (2006), pp. 851-855
[84.]
A.P. Atkinson, M. Cedzynski, J. Szemraj, A. St Swierzko, L. Bak-Romaniszyn, M. Banasik, et al.
L-ficolin in children with recurrent respiratory infections.
Clin Exp Immunol, 138 (2004), pp. 517-520
[85.]
A. Roos, M.P. Rastaldi, N. Calvaresi, B.D. Oortwijn, N. Schlagwein, D.J. van Gijlswijk-Janssen, et al.
Glomerular activation of the lectin pathway of complement in IgA nephropathy is associated with more severe renal disease.
J Am Soc Nephrol, 17 (2006), pp. 1724-1734
[86.]
X. Chen, Y. Katoh, K. Nakamura, N. Oyama, F. Kaneko, Y. Endo, et al.
Single nucleotide polymorphisms of Ficolin 2 gene in Behçet's disease.
J Dermatol Sci, 43 (2006), pp. 201-205
[87.]
S.J. Chapman, F.O. Vannberg, C.C. Khor, S. Segal, C.E. Moore, K. Knox, et al.
Functional polymorphisms in the FCN2 gene are not associated with invasive pneumococcal disease.
Mol Immunol, 44 (2007), pp. 3267-3270
[88.]
S. Yoshizawa, K. Nagasawa, Y. Yae, Y. Niho, K. Okochi.
A thermolabile beta 2-macroglycoprotein (TMG) and the antibody against TMG in patients with systemic lupus erythematosus.
Clin Chim Acta, 264 (1997), pp. 219-225
[89.]
T. Fukutomi, B. Ando, S. Sakamoto, H. Sakai, H. Nawata.
Thermolabile beta-2 macroglycoprotein (Hakata antigen) in liver disease: biochemical and immunohistochemical study.
Clin Chim Acta, 255 (1996), pp. 93-106
[90.]
R.G. Nielsen, I. Vind, P. Munkholm, J.C. Jensenius, S. Thiel, S. Husby.
Genetic polymorphisms of mannan binding lectin (MBL), serum levels of MBL, the MBL associated serine protease and H-ficolin in patients with Crohn's disease.
Gut, 56 (2007), pp. 311-312
[91.]
B.N. Lillie, A.S. Brooks, N.D. Keirstead, M.A. Hayes.
Comparative genetics and innate immune functions of collagenous lectins in animals.
Vet Immunol Immunopathol, 108 (2005), pp. 97-110
[92.]
Y. Fujimori, S. Harumiya, Y. Fukumoto, Y. Miura, K. Yagasaki, H. Tachikawa, et al.
Molecular cloning and characterization of mouse ficolin-A.
Biochem Biophys Res Commun, 244 (1998), pp. 796-800
[93.]
T. Omori-Satoh, Y. Yamakawa, D. Mebs.
The antihemorrhagic factor, erinacin, from the European hedgehog (Erinaceus europaeus), a metalloprotease inhibitor of large molecular size possessing ficolin/opsonin P35 lectin domains.
Toxicon, 38 (2000), pp. 1561-1580
[94.]
N.J. Lynch, S.U. Khan, C.M. Stover, S.M. Sandrini, D. Marston, J.S. Presanis, et al.
Composition of the lectin pathway of complement in Gallus gallus: absence of mannan-binding lectin-associated serine protease-1 in birds.
J Immunol, 174 (2005), pp. 4998-5006
[95.]
Y. Kakinuma, Y. Endo, M. Takahashi, M. Nakata, M. Matsushita, S. Takenoshita, et al.
Molecular cloning and characterization of novel ficolins from Xenopus laevis.
Immunogenetics, 55 (2003), pp. 29-37
[96.]
A. Kenjo, M. Takahashi, M. Matsushita, Y. Endo, M. Nakata, T. Mizuochi, et al.
Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi.
J Biol Chem, 276 (2001), pp. 19959-19965
[97.]
S. Gokudan, T. Muta, R. Tsuda, K. Koori, T. Kawahara, N. Seki, et al.
Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen.
Proc Natl Acad Sci U S A, 96 (1999), pp. 10086-10091
[98.]
H. Sekine, A. Kenjo, K. Azumi, G. Ohi, M. Takahashi, R. Kasukawa, et al.
An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi.
J Immunol, 167 (2001), pp. 4504-4510
[99.]
M. Nonaka, F. Yoshizaki.
Primitive complement system of invertebrates.
Immunol Rev, 198 (2004), pp. 203-215
[100.]
Y. Zhu, S. Thangamani, B. Ho, J.L. Ding.
The ancient origin of the complement system.
EMBO J, 24 (2005), pp. 382-394
Copyright © 2007. Sociedad Española de Inmunología