Citrullination of fibronectin modulates synovial fibroblast behavior

Arthritis Research and Therapy

Volumn 14, Issue 6, 2012, Pages

  Shelef, Miriam A ^a   Bennin, David A ^a,b   Mosher, Deane F ^a   Huttenlocher, Anna ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITRULLINATED FIBRONECTIN; FIBRONECTIN; FOCAL ADHESION KINASE; PAXILLIN; UNCLASSIFIED DRUG; CITRULLINE; GELATIN; INTEGRIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL SPREADING; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYNOVIOCYTE; TIME LAPSE IMAGING; WESTERN BLOTTING; ANIMAL; ANKLE; ARTHRITIS; C57BL MOUSE; CELL CULTURE; CELL MOTION; CYTOLOGY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SYNOVIAL FLUID; TRANSGENIC MOUSE;

ANIMALS; ANKLE JOINT; ARTHRITIS; ARTHRITIS, RHEUMATOID; BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CITRULLINE; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GELATIN; HUMANS; INTEGRINS; MICE, INBRED C57BL; MICE, TRANSGENIC; PAXILLIN; PHOSPHORYLATION; SYNOVIAL FLUID;

EID: 84868236825     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4083     Document Type: Article

References (40)

1. Wegner N, Lundberg K, Kinloch A, Fisher B, Malmstrom V, Feldmann M, Venables PJ. Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol Rev 2010, 233:34-54. 10.1111/j.0105-2896.2009.00850.x, 20192991.
2. Trouw LA, Haisma EM, Levarht EW, van der Woude D, Ioan-Facsinay A, Daha MR, Huizinga TW, Toes RE. Anti-cyclic citrullinated peptide antibodies from rheumatoid arthritis patients activate complement via both the classical and alternative pathways. Arthritis Rheum 2009, 60:1923-1931. 10.1002/art.24622, 19565507.
3. Courvoisier N, Dougados M, Cantagrel A, Goupille P, Meyer O, Sibilia J, Daures JP, Combe B. Prognostic factors of 10-year radiographic outcome in early rheumatoid arthritis: a prospective study. Arthritis Res Ther 2008, 10:R106. 10.1186/ar2498, 2592783, 18771585.
4. Kinloch A, Lundberg K, Wait R, Wegner N, Lim NH, Zendman AJ, Saxne T, Malmstrom V, Venables PJ. Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis. Arthritis Rheum 2008, 58:2287-2295. 10.1002/art.23618, 18668562.
5. Foulquier C, Sebbag M, Clavel C, Chapuy-Regaud S, Al Badine R, Mechin MC, Vincent C, Nachat R, Yamada M, Takahara H, Simon M, Guerrin M, Serre G. Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation. Arthritis Rheum 2007, 56:3541-3553. 10.1002/art.22983, 17968929.
6. Chang X, Yamada R, Suzuki A, Sawada T, Yoshino S, Tokuhiro S, Yamamoto K. Localization of peptidylarginine deiminase 4 (PADI4) and citrullinated protein in synovial tissue of rheumatoid arthritis. Rheumatology (Oxford) 2005, 44:40-50.
7. Makrygiannakis D, Revu S, Engstrom M, Af Klint E, Nicholas AP, Pruijn GJ, Catrina AI. Local administration of glucocorticoids decrease synovial citrullination in rheumatoid arthritis. Arthritis Res Ther 2012, 14:R20. 10.1186/ar3702, 3392813, 22284820.
8. Makrygiannakis D, Af Klint E, Lundberg IE, Lofberg R, Ulfgren AK, Klareskog L, Catrina AI. Citrullination is an inflammation-dependent process. Ann Rheum Dis 2006, 65:1219-1222. 10.1136/ard.2005.049403, 1798285, 16540548.
9. Moscarello MA, Wood DD, Ackerley C, Boulias C. Myelin in multiple sclerosis is developmentally immature. J Clin Invest 1994, 94:146-154. 10.1172/JCI117300, 296292, 7518827.
10. Hill JA, Bell DA, Brintnell W, Yue D, Wehrli B, Jevnikar AM, Lee DM, Hueber W, Robinson WH, Cairns E. Arthritis induced by posttranslationally modified (citrullinated) fibrinogen in DR4-IE transgenic mice. J Exp Med 2008, 205:967-979. 10.1084/jem.20072051, 2292232, 18391064.
11. Lundberg K, Nijenhuis S, Vossenaar ER, Palmblad K, van Venrooij WJ, Klareskog L, Zendman AJ, Harris HE. Citrullinated proteins have increased immunogenicity and arthritogenicity and their presence in arthritic joints correlates with disease severity. Arthritis Res Ther 2005, 7:R458-R467. 10.1186/ar1697, 1174941, 15899032.
12. Sokolove J, Zhao X, Chandra PE, Robinson WH. Immune complexes containing citrullinated fibrinogen costimulate macrophages via Toll-like receptor 4 and Fcgamma receptor. Arthritis Rheum 2011, 63:53-62. 3015008, 20954191.
13. Willis VC, Gizinski AM, Banda NK, Causey CP, Knuckley B, Cordova KN, Luo Y, Levitt B, Glogowska M, Chandra P, Kulik L, Robinson WH, Arend WP, Thompson PR, Holers VM. N-alpha-benzoyl-N5-(2-chloro-1-iminoethyl)-l-ornithine amide, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis. J Immunol 2011, 186:4396-4404. 10.4049/jimmunol.1001620, 3085980, 21346230.
14. Loos T, Mortier A, Gouwy M, Ronsse I, Put W, Lenaerts JP, Van Damme J, Proost P. Citrullination of CXCL10 and CXCL11 by peptidylarginine deiminase: a naturally occurring posttranslational modification of chemokines and new dimension of immunoregulation. Blood 2008, 112:2648-2656. 10.1182/blood-2008-04-149039, 18645041.
15. Proost P, Loos T, Mortier A, Schutyser E, Gouwy M, Noppen S, Dillen C, Ronsse I, Conings R, Struyf S, Opdenakker G, Maudgal PC, Van Damme J. Citrullination of CXCL8 by peptidylarginine deiminase alters receptor usage, prevents proteolysis, and dampens tissue inflammation. J Exp Med 2008, 205:2085-2097. 10.1084/jem.20080305, 2526203, 18710930.
16. Struyf S, Noppen S, Loos T, Mortier A, Gouwy M, Verbeke H, Huskens D, Luangsay S, Parmentier M, Geboes K, Schols D, Van Damme J, Proost P. Citrullination of CXCL12 differentially reduces CXCR4 and CXCR7 binding with loss of inflammatory and anti-HIV-1 activity via CXCR4. J Immunol 2009, 182:666-674.
17. Tabushi Y, Nakanishi T, Takeuchi T, Nakajima M, Ueda K, Kotani T, Makino S, Shimizu A, Hanafusa T, Takubo T. Detection of citrullinated proteins in synovial fluids derived from patients with rheumatoid arthritis by proteomics-based analysis. Ann Clin Biochem 2008, 45:413-417. 10.1258/acb.2007.007205, 18583628.
18. Yoshida M, Tsuji M, Kurosaka D, Yasuda J, Ito Y, Nishizawa T, Yamada A. Autoimmunity to citrullinated type II collagen in rheumatoid arthritis. Mod Rheumatol 2006, 16:276-281. 10.1007/s10165-006-0498-y, 2780673, 17039307.
19. Shiozawa K, Shiozawa S, Shimizu S, Fujita T. Fibronectin on the surface of articular cartilage in rheumatoid arthritis. Arthritis Rheum 1984, 27:615-622. 10.1002/art.1780270603, 6203543.
20. Shiozawa S, Yoshihara R, Kuroki Y, Fujita T, Shiozawa K, Imura S. Pathogenic importance of fibronectin in the superficial region of articular cartilage as a local factor for the induction of pannus extension on rheumatoid articular cartilage. Annals Rheum Dis 1992, 51:869-873.
21. Lauzier A, Charbonneau M, Harper K, Jilaveanu-Pelmus M, Dubois CM. Formation of invadopodia-like structures by synovial cells promotes cartilage breakdown in collagen-induced arthritis: involvement of the protein tyrosine kinase Src. Arthritis Rheum 2011, 63:1591-1602. 10.1002/art.30305, 21337539.
22. Lefevre S, Knedla A, Tennie C, Kampmann A, Wunrau C, Dinser R, Korb A, Schnaker EM, Tarner IH, Robbins PD, Evans CH, Sturz H, Steinmeyer J, Gay S, Scholmerich J, Pap T, Muller-Ladner U, Neumann E. Synovial fibroblasts spread rheumatoid arthritis to unaffected joints. Nat Med 2009, 15:1414-1420. 10.1038/nm.2050, 19898488.
23. Lowin T, Straub RH. Integrins and their ligands in rheumatoid arthritis. Arthritis Res Ther 2011, 13:244. 10.1186/ar3464, 3308078, 22077951.
24. Scott DL, Delamere JP, Walton KW. The distribution of fibronectin in the pannus in rheumatoid arthritis. Br J Exp Pathol 1981, 62:362-368. 2041679, 7028072.
25. Mueller SC, Chen WT. Cellular invasion into matrix beads: localization of beta 1 integrins and fibronectin to the invadopodia. J Cell Sci 1991, 99:213-225.
26. Guo D, Ding L, Homandberg GA. Telopeptides of type II collagen upregulate proteinases and damage cartilage but are less effective than highly active fibronectin fragments. Inflamm Res 2009, 58:161-169. 10.1007/s00011-009-8090-5, 19190855.
27. Chang X, Yamada R, Suzuki A, Kochi Y, Sawada T, Yamamoto K. Citrullination of fibronectin in rheumatoid arthritis synovial tissue. Rheumatology (Oxford) 2005, 44:1374-1382.
28. Douni E, Akassoglou K, Alexopoulou L, Georgopoulos S, Haralambous S, Hill S, Kassiotis G, Kontoyiannis D, Pasparakis M, Plows D, Probert L, Kollias G. Transgenic and knockout analyses of the role of TNF in immune regulation and disease pathogenesis. J Inflamm 1995, 47:27-38.
29. Neidhart M, Seemayer CA, Hummel KM, Michel BA, Gay RE, Gay S. Functional characterization of adherent synovial fluid cells in rheumatoid arthritis: destructive potential in vitro and in vivo. Arthritis Rheum 2003, 48:1873-1880. 10.1002/art.11166, 12847681.
30. Ruoslahti E, Hayman EG, Pierschbacher M, Engvall E. Fibronectin: purification, immunochemical properties, and biological activities. Methods Enzymol 1982, 82:803-831.
31. Knipp M, Vasak M. A colorimetric 96-well microtiter plate assay for the determination of enzymatically formed citrulline. Anal Biochem 2000, 286:257-264. 10.1006/abio.2000.4805, 11067748.
32. Maurer LM, Tomasini-Johansson BR, Ma W, Annis DS, Eickstaedt NL, Ensenberger MG, Satyshur KA, Mosher DF. Extended binding site on fibronectin for the functional upstream domain of protein F1 of Streptococcus pyogenes. J Biol Chem 2010, 285:41087-41099. 10.1074/jbc.M110.153692, 3003407, 20947497.
33. Cortesio CL, Chan KT, Perrin BJ, Burton NO, Zhang S, Zhang ZY, Huttenlocher A. Calpain 2 and PTP1B function in a novel pathway with Src to regulate invadopodia dynamics and breast cancer cell invasion. J Cell Biol 2008, 180:957-971. 10.1083/jcb.200708048, 2265405, 18332219.
34. Hynes RO, Yamada KM. Fibronectins: multifunctional modular glycoproteins. J Cell Biol 1982, 95:369-377. 10.1083/jcb.95.2.369, 2112946, 6128348.
35. Homandberg GA, Erickson JW. Model of fibronectin tertiary structure based on studies of interactions between fragments. Biochemistry 1986, 25:6917-6925. 10.1021/bi00370a027, 3801402.
36. Makrygiannakis D, Hermansson M, Ulfgren AK, Nicholas AP, Zendman AJ, Eklund A, Grunewald J, Skold CM, Klareskog L, Catrina AI. Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis 2008, 67:1488-1492. 10.1136/ard.2007.075192, 18413445.
37. Chang X, Han J, Pang L, Zhao Y, Yang Y, Shen Z. Increased PADI4 expression in blood and tissues of patients with malignant tumors. BMC Cancer 2009, 9:40. 10.1186/1471-2407-9-40, 2637889, 19183436.
38. Sachchidanand, Lequin O, Staunton D, Mulloy B, Forster MJ, Yoshida K, Campbell ID. Mapping the heparin-binding site on the 13-14F3 fragment of fibronectin. J Biol Chem 2002, 277:50629-50635. 10.1074/jbc.M208956200, 12377765.
39. Tarcsa E, Marekov LN, Mei G, Melino G, Lee SC, Steinert PM. Protein unfolding by peptidylarginine deiminase. Substrate specificity and structural relationships of the natural substrates trichohyalin and filaggrin. J Biol Chem 1996, 271:30709-30716. 10.1074/jbc.271.48.30709, 8940048.
40. van Beers JJ, Willemze A, Stammen-Vogelzangs J, Drijfhout JW, Toes RE, GJMP. Anti-citrullinated fibronectin antibodies in rheumatoid arthritis are associated with human leukocyte antigen-DRB1 shared epitope alleles. Arthritis Res Ther 2012, 14:R35. 10.1186/ar3744, 3392834, 22339947.