Interactions of the complement system with molecules of extracellular matrix: Relevance for joint diseases

Immunobiology

Volumn 217, Issue 11, 2012, Pages 1088-1096

  Happonen, Kaisa E ^a   Heinegård, Dick ^b   Saxne, Tore ^b   Blom, Anna M ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Complement; Extracellular matrix; Osteoarthritis; Rheumatoid arthritis

Indexed keywords

C REACTIVE PROTEIN; CARTILAGE OLIGOMERIC MATRIX PROTEIN; CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT MEMBRANE ATTACK COMPLEX; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; GLYCOSAMINOGLYCAN; HYALURONIC ACID; INTER ALPHA TRYPSIN INHIBITOR; MANNOSE BINDING LECTIN; METHOTREXATE; SMALL LEUCINE RICH REPEAT PROTEIN; STRUCTURAL PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR INHIBITOR; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTHROPATHY; ARTICULAR CARTILAGE; COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT DEPOSITION; COMPLEMENT INHIBITION; COMPLEMENT SYSTEM; CYTOKINE PRODUCTION; DISEASE ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; JOINT DESTRUCTION; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; REMISSION; REVIEW; RHEUMATOID ARTHRITIS; SYNOVITIS;

EID: 84866033089     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.07.013     Document Type: Review

References (105)

1. Banda N.K., Thurman J.M., Kraus D., Wood A., Carroll M.C., Arend W.P., Holers V.M. Alternative complement pathway activation is essential for inflammation and joint destruction in the passive transfer model of collagen-induced arthritis. J. Immunol. 2006, 177:1904-1912.
2. Banda N.K., Takahashi K., Wood A.K., Holers V.M., Arend W.P. Pathogenic complement activation in collagen antibody-induced arthritis in mice requires amplification by the alternative pathway. J. Immunol. 2007, 179:4101-4109.
3. Banda N.K., Levitt B., Glogowska M.J., Thurman J.M., Takahashi K., Stahl G.L., Tomlinson S., Arend W.P., Holers V.M. Targeted inhibition of the complement alternative pathway with complement receptor 2 and factor H attenuates collagen antibody-induced arthritis in mice. J. Immunol. 2009, 183:5928-5937.
4. Banda N.K., Takahashi M., Levitt B., Glogowska M., Nicholas J., Takahashi K., Stahl G.L., Fujita T., Arend W.P., Holers V.M. Essential role of complement mannose-binding lectin-associated serine proteases-1/3 in the murine collagen antibody-induced model of inflammatory arthritis. J. Immunol. 2010, 185:5598-5606.
5. Banda N.K., Hyatt S., Glogowska M., Takahashi K., Merkel T.J., Stahl G.L., Lu B., Gerard C., Wetsel R.A., Arend W.P., Holers V.M. Independent roles for complement C3a and C5a receptors and the membrane attack complex in the pathogenesis of collagen antibody-induced arthritis in mice: potential therapeutic implications. Mol. Immunol. 2011, 48:1670.
6. Bianco P., Fisher L.W., Young M.F., Termine J.D., Robey P.G. Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. J. Histochem. Cytochem. 1990, 38:1549-1563.
7. Bing D.H., Almeda S., Isliker H., Lahav J., Hynes R.O. Fibronectin binds to the C1q component of complement. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:4198-4201.
8. Blom A.M., Mörgelin M., Oyen M., Jarvet J., Fries E. Structural characterization of inter-alpha-inhibitor. Evidence for an extended shape. J. Biol. Chem. 1999, 274:298-304.
9. Blom A.M., Nandakumar K.S., Holmdahl R. C4b-binding protein (C4BP) inhibits development of experimental arthritis in mice. Ann. Rheum. Dis. 2009, 68:136-142.
10. Bohnsack J.F., Tenner A.J., Laurie G.W., Kleinman H.K., Martin G.R., Brown E.J. The C1q subunit of the first component of complement binds to laminin: a mechanism for the deposition and retention of immune complexes in basement membrane. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:3824-3828.
11. Brodeur J.P., Ruddy S., Schwartz L.B., Moxley G. Synovial fluid levels of complement SC5b-9 and fragment Bb are elevated in patients with rheumatoid arthritis. Arthritis Rheum. 1991, 34:1531-1537.
12. Carlsen S., Hansson A.S., Olsson H., Heinegård D., Holmdahl R. Cartilage oligomeric matrix protein (COMP)-induced arthritis in rats. Clin. Exp. Immunol. 1998, 114:477-484.
13. Carlsen S., Nandakumar K.S., Bäcklund J., Holmberg J., Hultqvist M., Vestberg M., Holmdahl R. Cartilage oligomeric matrix protein induction of chronic arthritis in mice. Arthritis Rheum. 2008, 58:2000-2011.
14. Chang N.S., Boackle R.J., Armand G. Hyaluronic acid-complement interactions. I. Reversible heat-induced anticomplementary activity. Mol. Immunol. 1985, 22:391-397.
15. Colmegna I., Ohata B.R., Menard H.A. Current understanding of rheumatoid arthritis therapy. Clin. Pharmacol. Ther. 2012, 91:607-620. 10.1038/clpt.2011.325.
16. Danfelter M., önnerfjord P., Heinegård D. Fragmentation of proteins in cartilage treated with interleukin-1: specific cleavage of type IX collagen by matrix metalloproteinase 13 releases the NC4 domain. J. Biol. Chem. 2007, 282:36933-36941.
17. Day A.A., Ramis C.I., Fisher L.W., Gehron-Robey P., Termine J.D., Young M.F. Characterization of bone PG II cDNA and its relationship to PG II mRNA from other connective tissues. Nucleic Acids Res. 1986, 14:9861-9876.
18. Dempsey P.W., Allison M.E., Akkaraju S., Goodnow C.C., Fearon D.T. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996, 271:348-350.
19. Dickinson S.C., Vankemmelbeke M.N., Buttle D.J., Rosenberg K., Heinegård D., Hollander A.P. Cleavage of cartilage oligomeric matrix protein (thrombospondin-5) by matrix metalloproteinases and a disintegrin and metalloproteinase with thrombospondin motifs. Matrix Biol. 2003, 22:267-278.
20. Douglas T., Heinemann S., Bierbaum S., Scharnweber D., Worch H. Fibrillogenesis of collagen types I, II, and III with small leucine-rich proteoglycans decorin and biglycan. Biomacromolecules 2006, 7:2388-2393.
21. Firestein G.S., Yeo M., Zvaifler N.J. Apoptosis in rheumatoid arthritis synovium. J. Clin. Invest. 1995, 96:1631-1638.
22. Fischetti F., Durigutto P., Macor P., Marzari R., Carretta R., Tedesco F. Selective therapeutic control of C5a and the terminal complement complex by anti-C5 single-chain Fv in an experimental model of antigen-induced arthritis in rats. Arthritis Rheum. 2007, 56:1187-1197.
23. Flannery C.R. Usurped SLRPs: novel arthritis biomarkers exposed by catabolism of small leucine-rich proteoglycans?. Arthritis Res. Ther. 2006, 8:106-107.
24. Fosang A.J., Stanton H., Little C.B., Atley L.M. Neoepitopes as biomarkers of cartilage catabolism. Inflamm. Res. 2003, 52:277-282.
25. Fraser D.A., Harris C.L., Williams A.S., Mizuno M., Gallagher S., Smith R.A., Morgan B.P. Generation of a recombinant, membrane-targeted form of the complement regulator CD59: activity in vitro and in vivo. J. Biol. Chem. 2003, 278:48921-48927.
26. Fries E., Blom A.M. Bikunin-not just a plasma proteinase inhibitor. Int. J. Biochem. Cell Biol. 2000, 32:125-137.
27. Ganu V., Goldberg R., Peppard J., Rediske J., Melton R., Hu S.I., Wang W., Duvander C., Heinegård D. Inhibition of interleukin-1alpha-induced cartilage oligomeric matrix protein degradation in bovine articular cartilage by matrix metalloproteinase inhibitors: potential role for matrix metalloproteinases in the generation of cartilage oligomeric matrix protein fragments in arthritic synovial fluid. Arthritis Rheum. 1998, 41:2143-2151.
28. Garantziotis S., Hollingsworth J.W., Ghanayem R.B., Timberlake S., Zhuo L., Kimata K., Schwartz D.A. Inter-alpha-trypsin inhibitor attenuates complement activation and complement-induced lung injury. J. Immunol. 2007, 179:4187-4192.
29. Groeneveld T.W., Oroszlan M., Owens R.T., Faber-Krol M.C., Bakker A.C., Arlaud G.J., McQuillan D.J., Kishore U., Daha M.R., Roos A. Interactions of the extracellular matrix proteoglycans decorin and biglycan with C1q and collectins. J. Immunol. 2005, 175:4715-4723.
30. Halasz K., Kassner A., Mörgelin M., Heinegård D. COMP acts as a catalyst in collagen fibrillogenesis. J. Biol. Chem. 2007, 282:31166-31173.
31. Hanauske-Abel H.M., Pontz B.F., Schorlemmer H.U. Cartilage specific collagen activates macrophages and the alternative pathway of complement: evidence for an immunopathogenic concept of rheumatoid arthritis. Ann. Rheum. Dis. 1982, 41:168-176.
32. Happonen K.E., Sjöberg A.P., Mörgelin M., Heinegård D., Blom A.M. Complement inhibitor C4b-binding protein interacts directly with small glycoproteins of the extracellular matrix. J. Immunol. 2009, 182:1518-1525.
33. Happonen K.E., Saxne T., Aspberg A., Mörgelin M., Heinegård D., Blom A.M. Regulation of complement by cartilage oligomeric matrix protein allows for a novel molecular diagnostic principle in rheumatoid arthritis. Arthritis Rheum. 2010, 62:3574-3583.
34. Happonen K.E., Fürst C.M., Saxne T., Heinegård D., Blom A.M. PRELP protein inhibits the formation of the complement membrane attack complex. J. Biol. Chem. 2012, 287:8092-8100. 10.1074/jbc.M111.291476.
35. Happonen K.E., Saxne T., Geborek P., Andersson M., Bengtsson A.A., Hesselstrand R., Heinegård D., Blom A.M. Serum COMP-C3b complexes in rheumatic diseases and relation to anti-TNF-alpha treatment. Arthritis Res. Ther. 2012, 14:R15.
36. Heathfield T.F., Onnerfjord P., Dahlberg L., Heinegard D. Cleavage of fibromodulin in cartilage explants involves removal of the N-terminal tyrosine sulfate-rich region by proteolysis at a site that is sensitive to matrix metalloproteinase-13. J. Biol. Chem. 2004, 279:6286-6295.
37. Hedbom E., Heinegård D. Binding of fibromodulin and decorin to separate sites on fibrillar collagens. J. Biol. Chem. 1993, 268:27307-27312.
38. Heinegård D., Larsson T., Sommarin Y., Franzen A., Paulsson M., Hedbom E. Two novel matrix proteins isolated from articular cartilage show wide distributions among connective tissues. J. Biol. Chem. 1986, 261:13866-13872.
39. Heinegård D. Proteoglycans and more-from molecules to biology. Int. J. Exp. Pathol. 2009, 90:575-586.
40. Holmqvist M.E., Wedren S., Jacobsson L.T., Klareskog L., Nyberg F., Rantapaa-Dahlqvist S., Alfredsson L., Askling J. Rapid increase in myocardial infarction risk following diagnosis of rheumatoid arthritis amongst patients diagnosed between 1995 and 2006. J. Intern. Med. 2010, 268:578-585.
41. Islander U., Jochems C., Lagerquist M.K., Forsblad-d'Elia H., Carlsten H. Estrogens in rheumatoid arthritis; the immune system and bone. Mol. Cell. Endocrinol. 2010, 335:14-29.
42. Jiang D., Liang J., Fan J., Yu S., Chen S., Luo Y., Prestwich G.D., Mascarenhas M.M., Garg H.G., Quinn D.A., Homer R.J., Goldstein D.R., Bucala R., Lee P.J., Medzhitov R., Noble P.W. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 2005, 11:1173-1179.
43. Jiang D., Liang J., Noble P.W. Hyaluronan as an immune regulator in human diseases. Physiol. Rev. 2011, 91:221-264.
44. Jose P.J., Moss I.K., Maini R.N., Williams T.J. Measurement of the chemotactic complement fragment C5a in rheumatoid synovial fluids by radioimmunoassay: role of C5a in the acute inflammatory phase. Ann. Rheum. Dis. 1990, 49:747-752.
45. Kalchishkova N., Melin Fürst C., Heinegård D., Blom A.M. The NC4 domain of the cartilage-specific collagen IX inhibits complement directly due to attenuation of membrane attack formation and indirectly through binding and enhancing activity of complement inhibitors C4B-binding protein and factor H. J. Biol. Chem. 2011, 286:27915-27926.
46. Kazatchkine M.D., Fearon D.T., Metcalfe D.D., Rosenberg R.D., Austen K.F. Structural determinants of the capacity of heparin to inhibit the formation of the human amplification C3 convertase. J. Clin. Invest. 1981, 67:223-228.
47. Kemper C., Mitchell L.M., Zhang L., Hourcade D.E. The complement protein properdin binds apoptotic T cells and promotes complement activation and phagocytosis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9023-9028.
48. Kida D., Yoneda M., Miyaura S., Ishimaru T., Yoshida Y., Ito T., Ishiguro N., Iwata H., Kimata K. The SHAP-HA complex in sera from patients with rheumatoid arthritis and osteoarthritis. J. Rheumatol. 1999, 26:1230-1238.
49. Kimura Y., Zhou L., Miwa T., Song W.C. Genetic and therapeutic targeting of properdin in mice prevents complement-mediated tissue injury. J. Clin. Invest. 2010, 120:3545-3554.
50. Konttinen Y.T., Ceponis A., Meri S., Vuorikoski A., Kortekangas P., Sorsa T., Sukura A., Santavirta S. Complement in acute and chronic arthritides: assessment of C3c C9, and protectin (CD59) in synovial membrane. Ann. Rheum. Dis. 1996, 55:888-894.
51. Korb L.C., Ahearn J.M. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 1997, 158:4525-4528.
52. Krumdieck R., Hook M., Rosenberg L.C., Volanakis J.E. The proteoglycan decorin binds C1q and inhibits the activity of the C1 complex. J. Immunol. 1992, 149:3695-3701.
53. Kuhn K.A., Cozine C.L., Tomooka B., Robinson W.H., Holers V.M. Complement receptor CR2/CR1 deficiency protects mice from collagen-induced arthritis and associates with reduced autoantibodies to type II collagen and citrullinated antigens. Mol. Immunol. 2008, 45:2808-2819.
54. Larsson T., Sommarin Y., Paulsson M., Antonsson P., Hedbom E., Wendel M., Heinegård D. Cartilage matrix proteins. A basic 36-kDa protein with a restricted distribution to cartilage and bone. J. Biol. Chem. 1991, 266:20428-20433.
55. Leffler J., Herbert A.P., Norstrom E., Schmidt C.Q., Barlow P.N., Blom A.M., Martin M. Annexin-II DNA, and histones serve as factor H ligands on the surface of apoptotic cells. J. Biol. Chem. 2010, 285:3766-3776. 10.1074/jbc.M109.045427.
56. Liu C.J., Kong W., Ilalov K., Yu S., Xu K., Prazak L., Fajardo M., Sehgal B., Di Cesare P.E. ADAMTS-7: a metalloproteinase that directly binds to and degrades cartilage oligomeric matrix protein. FASEB J. 2006, 20:988-990.
57. Liu C.J., Kong W., Xu K., Luan Y., Ilalov K., Sehgal B., Yu S., Howell R.D., Di Cesare P.E. ADAMTS-12 associates with and degrades cartilage oligomeric matrix protein. J. Biol. Chem. 2006, 281:15800-15808.
58. Macor P., Durigutto P., De Maso L., Garrovo C., Biffi S., Cortini A., Fischetti F., Sblattero D., Pitzalis C., Marzari R., Tedesco F. Treatment of arthritis models by targeting synovial endothelium with a neutralizing recombinant antibody to C5. Arthritis Rheum. 2012, 10.1002/art.34430.
59. Malhotra R., Wormald M.R., Rudd P.M., Fischer P.B., Dwek R.A., Sim R.B. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat. Med. 1995, 1:237-243.
60. Mann H.H., Ozbek S., Engel J., Paulsson M., Wagener R. Interactions between the cartilage oligomeric matrix protein and matrilins. Implications for matrix assembly and the pathogenesis of chondrodysplasias. J. Biol. Chem. 2004, 279:25294-25298.
61. Månsson B., Carey D., Alini M., Ionescu M., Rosenberg L.C., Poole A.R., Heinegård D., Saxne T. Cartilage and bone metabolism in rheumatoid arthritis. Differences between rapid and slow progression of disease identified by serum markers of cartilage metabolism. J. Clin. Invest. 1995, 95:1071-1077.
62. Matsui H., Tsuji S., Nishimura H., Nagasawa S. Activation of the alternative pathway of complement by apoptotic Jurkat cells. FEBS Lett. 1994, 351:419-422.
63. McEwan P.A., Scott P.G., Bishop P.N., Bella J. Structural correlations in the family of small leucine-rich repeat proteins and proteoglycans. J. Struct. Biol. 2006, 155:294-305.
64. Merline R., Moreth K., Beckmann J., Nastase M.V., Zeng-Brouwers J., Tralhao J.G., Lemarchand P., Pfeilschifter J., Schaefer R.M., Iozzo R.V., Schaefer L. Signaling by the matrix proteoglycan decorin controls inflammation and cancer through PDCD4 and MicroRNA-21. Sci. Signal. 2011, 4:ra75.
65. Morgan B.P., Daniels R.H., Williams B.D. Measurement of terminal complement complexes in rheumatoid arthritis. Clin. Exp. Immunol. 1988, 73:473-478.
66. Moxley G., Ruddy S. Elevated C3 anaphylatoxin levels in synovial fluids from patients with rheumatoid arthritis. Arthritis Rheum. 1985, 28:1089-1095.
67. Nandakumar K.S., Jansson A., Xu B., Rydell N., Ahooghalandari P., Hellman L., Blom A.M., Holmdahl R. A recombinant vaccine effectively induces c5a-specific neutralizing antibodies and prevents arthritis. PLoS One 2010, 5:e13511.
68. Neidhart M., Hauser N., Paulsson M., DiCesare P.E., Michel B.A., Hauselmann H.J. Small fragments of cartilage oligomeric matrix protein in synovial fluid and serum as markers for cartilage degradation. Br. J. Rheumatol. 1997, 36:1151-1160.
69. Nishioka K., Hasunuma T., Kato T., Sumida T., Kobata T. Apoptosis in rheumatoid arthritis: a novel pathway in the regulation of synovial tissue. Arthritis Rheum. 1998, 41:1-9.
70. Ogden C.A., deCathelineau A., Hoffmann P.R., Bratton D., Ghebrehiwet B., Fadok V.A., Henson P.M. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 2001, 194:781-795.
71. Okroj M., Heinegård D., Holmdahl R., Blom A.M. Rheumatoid arthritis and the complement system. Ann. Med. 2007, 39:517-530.
72. Okroj M., Holmquist E., Sjölander J., Corrales L., Saxne T., Wisniewski H.G., Blom A.M. Heavy chains of inter alpha inhibitor (IalphaI) inhibit the human complement system at early stages of the cascade. J. Biol. Chem. 2012, 10.1074/jbc.M111.324913.
73. Oldberg A., Antonsson P., Lindblom K., Heinegård D. COMP (cartilage oligomeric matrix protein) is structurally related to the thrombospondins. J. Biol. Chem. 1992, 267:22346-22350.
74. Revell P.A., Mayston V., Lalor P., Mapp P. The synovial membrane in osteoarthritis: a histological study including the characterisation of the cellular infiltrate present in inflammatory osteoarthritis using monoclonal antibodies. Ann. Rheum. Dis. 1988, 47:300-307.
75. Rosenberg K., Olsson H., Mörgelin M., Heinegård D. Cartilage oligomeric matrix protein shows high affinity zinc-dependent interaction with triple helical collagen. J. Biol. Chem. 1998, 273:20397-20403.
76. Rugg M.S., Willis A.C., Mukhopadhyay D., Hascall V.C., Fries E., Fulop C., Milner C.M., Day A.J. Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J. Biol. Chem. 2005, 280:25674-25686.
77. Saxne T., Heinegård D. Cartilage oligomeric matrix protein: a novel marker of cartilage turnover detectable in synovial fluid and blood. Br. J. Rheumatol. 1992, 31:583-591.
78. Saxne T., Lindell M., Månsson B., Petersson I.F., Heinegård D. Inflammation is a feature of the disease process in early knee joint osteoarthritis. Rheumatology (Oxford) 2003, 42:903-904.
79. Schaefer L., Babelova A., Kiss E., Hausser H.J., Baliova M., Krzyzankova M., Marsche G., Young M.F., Mihalik D., Gotte M., Malle E., Schaefer R.M., Grone H.J. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J. Clin. Invest. 2005, 115:2223-2233.
80. Scott D.L., Wolfe F., Huizinga T.W. Rheumatoid arthritis. Lancet 2010, 376:1094-1108.
81. Sjöberg A., önnerfjord P., Mörgelin M., Heinegård D., Blom A.M. The extracellular matrix and inflammation: fibromodulin activates the classical pathway of complement by directly binding C1q. J. Biol. Chem. 2005, 280:32301-32308.
82. Sjöberg A.P., Manderson G.A., Mörgelin M., Day A.J., Heinegård D., Blom A.M. Short leucine-rich glycoproteins of the extracellular matrix display diverse patterns of complement interaction and activation. Mol. Immunol. 2009, 46:830-839.
83. Sjöberg A.P., Trouw L.A., Blom A.M. Complement activation and inhibition: a delicate balance. Trends Immunol. 2009, 30:83-90.
84. Skliris A., Happonen K.E., Terpos E., Labropoulou V., Borset M., Heinegård D., Blom A.M., Theocharis A.D. Serglycin inhibits the classical and lectin pathways of complement via its glycosaminoglycan chains: implications for multiple myeloma. Eur. J. Immunol. 2011, 41:437-449.
85. Smith M.D., Triantafillou S., Parker A., Youssef P.P., Coleman M. Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J. Rheumatol. 1997, 24:365-371.
86. Sofat N., Robertson S.D., Wait R. Fibronectin III 13-14 domains induce joint damage via Toll-like receptor 4 activation and synergize with interleukin-1 and tumour necrosis factor. J. Innate. Immun. 2012, 4:69-79. 10.1159/000329632.
87. Sommarin Y., Wendel M., Shen Z., Hellman U., Heinegård D. Osteoadherin, a cell-binding keratan sulfate proteoglycan in bone, belongs to the family of leucine-rich repeat proteins of the extracellular matrix. J. Biol. Chem. 1998, 273:16723-16729.
88. Souto-Carneiro M.M., Burkhardt H., Muller E.C., Hermann R., Otto A., Kraetsch H.G., Sack U., Konig A., Heinegard D., Muller-Hermelink H.K., Krenn V. Human monoclonal rheumatoid synovial B lymphocyte hybridoma with a new disease-related specificity for cartilage oligomeric matrix protein. J. Immunol. 2001, 166:4202-4208.
89. Spector T.D., Hart D.J., Nandra D., Doyle D.V., Mackillop N., Gallimore J.R., Pepys M.B. Low-level increases in serum C-reactive protein are present in early osteoarthritis of the knee and predict progressive disease. Arthritis Rheum. 1997, 40:723-727.
90. Swaak A.J., Van Rooyen A., Planten O., Han H., Hattink O., Hack E. An analysis of the levels of complement components in the synovial fluid in rheumatic diseases. Clin. Rheumatol. 1987, 6:350-357.
91. Trouw L.A., Nilsson S.C., Goncalves I., Landberg G., Blom A.M. C4b-binding protein binds to necrotic cells and DNA, limiting DNA release and inhibiting complement activation. J. Exp. Med. 2005, 201:1937-1948.
92. Trouw L.A., Bengtsson A.A., Gelderman K.A., Dahlbäck B., Sturfelt G., Blom A.M. C4b-binding protein and factor H compensate for the loss of membrane-bound complement inhibitors to protect apoptotic cells against excessive complement attack. J. Biol. Chem. 2007, 282:28540-28548.
93. Trouw L.A., Haisma E.M., Levarht E.W., van der Woude D., Ioan-Facsinay A., Daha M.R., Huizinga T.W., Toes R.E. Anti-cyclic citrullinated peptide antibodies from rheumatoid arthritis patients activate complement via both the classical and alternative pathways. Arthritis Rheum. 2009, 60:1923-1931.
94. Vergunst C.E., Gerlag D.M., Dinant H., Schulz L., Vinkenoog M., Smeets T.J., Sanders M.E., Reedquist K.A., Tak P.P. Blocking the receptor for C5a in patients with rheumatoid arthritis does not reduce synovial inflammation. Rheumatology (Oxford) 2007, 46:1773-1778.
95. Wagner S., Fritz P., Einsele H., Sell S., Saal J.G. Evaluation of synovial cytokine patterns in rheumatoid arthritis and osteoarthritis by quantitative reverse transcription polymerase chain reaction. Rheumatol. Int. 1997, 16:191-196.
96. Wang Q., Rozelle A.L., Lepus C.M., Scanzello C.R., Song J.J., Larsen D.M., Crish J.F., Bebek G., Ritter S.Y., Lindstrom T.M., Hwang I., Wong H.H., Punzi L., Encarnacion A., Shamloo M., Goodman S.B., Wyss-Coray T., Goldring S.R., Banda N.K., Thurman J.M., Gobezie R., Crow M.K., Holers V.M., Lee D.M., Robinson W.H. Identification of a central role for complement in osteoarthritis. Nat. Med. 2011, 17:1674-1679.
97. Wang Y., Rollins S.A., Madri J.A., Matis L.A. Anti-C5 monoclonal antibody therapy prevents collagen-induced arthritis and ameliorates established disease. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:8955-8959.
98. Wang Y., Kristan J., Hao L., Lenkoski C.S., Shen Y., Matis L.A. A role for complement in antibody-mediated inflammation: C5-deficient DBA/1 mice are resistant to collagen-induced arthritis. J. Immunol. 2000, 164:4340-4347.
99. Webb J.H., Blom A.M., Dahlback B. Vitamin K-dependent protein S localizing complement regulator C4b-binding protein to the surface of apoptotic cells. J. Immunol. 2002, 169:2580-2586.
100. Williams A.S., Mizuno M., Richards P.J., Holt D.S., Morgan B.P. Deletion of the gene encoding CD59a in mice increases disease severity in a murine model of rheumatoid arthritis. Arthritis Rheum. 2004, 50:3035-3044.
101. Woodruff T.M., Nandakumar K.S., Tedesco F. Inhibiting the C5-C5a receptor axis. Mol. Immunol. 2011, 48:1631-1642.
102. Wouters D., Voskuyl A.E., Molenaar E.T., Dijkmans B.A., Hack C.E. Evaluation of classical complement pathway activation in rheumatoid arthritis: measurement of C1q-C4 complexes as novel activation products. Arthritis Rheum. 2006, 54:1143-1150.
103. Xu W., Berger S.P., Trouw L.A., de Boer H.C., Schlagwein N., Mutsaers C., Daha M.R., van Kooten C. Properdin binds to late apoptotic and necrotic cells independently of C3b and regulates alternative pathway complement activation. J. Immunol. 2008, 180:7613-7621.
104. Yingsung W., Zhuo L., Morgelin M., Yoneda M., Kida D., Watanabe H., Ishiguro N., Iwata H., Kimata K. Molecular heterogeneity of the SHAP-hyaluronan complex. Isolation and characterization of the complex in synovial fluid from patients with rheumatoid arthritis. J. Biol. Chem. 2003, 278:32710-32718.
105. Zhuo L., Hascall V.C., Kimata K. Inter-alpha-trypsin inhibitor, a covalent protein-glycosaminoglycan-protein complex. J. Biol. Chem. 2004, 279:38079-38082.