Immune recognition of citrullinated proteoglycan aggrecan epitopes in mice with proteoglycan-induced arthritis and in patients with rheumatoid arthritis

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Markovics, Adrienn ^a   Ocskó, Tímea ^a   Katz, Robert S ^a   Buzás, Edit I ^b   Glant, Tibor T ^a   Mikecz, Katalin ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; ARGININE; CITRULLINATED PROTEIN ANTIBODY; CITRULLINATED PROTEOGLYCAN PEPTIDE 49; EPITOPE; PROTEIN ANTIBODY; PROTEOGLYCAN; UNCLASSIFIED DRUG; CITRULLINE; CYTOKINE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN RECOGNITION; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EXPERIMENTAL ARTHRITIS; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEOGLYCAN INDUCED ARTHRITIS; RHEUMATOID ARTHRITIS; SPLEEN CELL; T LYMPHOCYTE; AMINO ACID SEQUENCE; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; CASE CONTROL STUDY; CELL CULTURE; CELL PROLIFERATION; CHEMICALLY INDUCED; CHEMISTRY; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; SPLEEN; VALIDATION STUDY;

AGGRECANS; AMINO ACID SEQUENCE; ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; B-LYMPHOCYTES; CASE-CONTROL STUDIES; CELL PROLIFERATION; CELLS, CULTURED; CITRULLINE; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; FLOW CYTOMETRY; HUMANS; MICE; PROTEOGLYCANS; SPLEEN; T-LYMPHOCYTES;

EID: 84979964965     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0160284     Document Type: Article

References (49)

1. Firestein GS. Rheumatoid arthritis: Etiology and pathogeneis of rheumatoid arthritis. In: Ruddy S, Harris ED, Sledge CB, Kelley WN, editors. Kelley's Textbook of Rheumatology. Philadelphia, PA: W.B. Saunders Co. 2005; pp. 996-1045
2. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003; 423: 356-361. PMID: 12748655
3. Demoruelle MK, Deane K. Antibodies to citrullinated protein antigens (ACPAs): clinical and pathophysiologic significance. Curr Rheumatol Rep 2011; 13: 421-430 doi: 10.1007/s11926-011-0193-7 PMID: 21713412
4. Anzilotti C, Pratesi F, Tommasi C, Migliorini P. Peptidylarginine deiminase 4 and citrullination in health and disease. Autoimmun Rev 2010; 9: 158-160 doi: 10.1016/j.autrev.2009.06.002 PMID: 19540364
5. Wegner N, Lundberg K, Kinloch A, Fisher B, Malmstrom V, Feldmann M, et al. Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol Rev 2010; 233: 34-54 doi: 10.1111/j.0105-2896.2009.00850.x PMID: 20192991
6. Arend WP, Firestein GS. Pre-rheumatoid arthritis: predisposition and transition to clinical synovitis. Nat Rev Rheumatol 2012; 8: 573-586 doi: 10.1038/nrrheum.2012.134 PMID: 22907289
7. Rantapaa-Dahlqvist S, de Jong BA, Berglin E, Hallmans G, Wadell G, Stenlund H, et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum 2003; 48: 2741-2749 PMID: 14558078
8. van de Stadt LA, de Koning MH, van de Stadt RJ, Wolbink G, Dijkmans BA, Hamann D, et al. Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis. Arthritis Rheum 2011; 63: 3226-3233 doi: 10.1002/art.30537 PMID: 21792832
9. Szodoray P, Szabo Z, Kapitany A, Gyetvai A, Lakos G, Szanto S, et al. Anti-citrullinated protein/peptide autoantibodies in association with genetic and environmental factors as indicators of disease outcome in rheumatoid arthritis. Autoimmun Rev 2010; 9: 140-143 doi: 10.1016/j.autrev.2009.04.006 PMID: 19427413
10. van Venrooij WJ, van Beers JJ, Pruijn GJ. Anti-CCP antibodies: the past, the present and the future. Nat Rev Rheumatol 2011; 7: 391-398 doi: 10.1038/nrrheum.2011.76 PMID: 21647203
11. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO, et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis 2010; 69: 1580-1588 doi: 10.1136/ard.2010.138461 PMID: 20699241
12. Van Steendam K, Tilleman K, De Ceuleneer M, de Keyser F, Elewaut D, Deforce D. Citrullinated vimentin as an important antigen in immune complexes from synovial fluid of rheumatoid arthritis patients with antibodies against citrullinated proteins. Arthritis Res Ther 2010; 12: R132 doi: 10.1186/ar3070 PMID: 20609218
13. Van Steendam K, Tilleman K, Deforce D. The relevance of citrullinated vimentin in the production of antibodies against citrullinated proteins and the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 2011; 50: 830-837
14. Clavel C, Nogueira L, Laurent L, Iobagiu C, Vincent C, Sebbag M, et al. Induction of macrophage secretion of tumor necrosis factor alpha through Fcgamma receptor IIa engagement by rheumatoid arthritis-specific autoantibodies to citrullinated proteins complexed with fibrinogen. Arthritis Rheum 2008; 58: 678-688 doi: 10.1002/art.23284 PMID: 18311806
15. Trouw LA, Haisma EM, Levarht EW, van der Woude D, Ioan-Facsinay A, Daha MR, et al. Anti-cyclic citrullinated peptide antibodies from rheumatoid arthritis patients activate complement via both the classical and alternative pathways. Arthritis Rheum 2009; 60: 1923-1931 doi: 10.1002/art.24622 PMID: 19565507
16. Courtenay JS, Dallman MJ, Dayan AD, Martin A, Mosedale B. Immunization against heterologous type II collagen induces arthritis in mice. Nature 1980; 282: 666-668
17. Glant TT, Mikecz K, Arzoumanian A, Poole AR. Proteoglycan-induced arthritis in BALB/c mice. Clinical features and histopathology. Arthritis Rheum 1987; 30: 201-212 PMID: 3827960
18. Glant TT, Mikecz K. Proteoglycan aggrecan-induced arthritis. A murine autoimmune model of rheumatoid arthritis. Methods Mol Med 2004; 102: 313-338 PMID: 15286393
19. Buzas E, Vegvari A, Murad YM, Finnegan A, Mikecz K, Glant TT. T-cell recognition of differentially tolerated epitopes of cartilage proteoglycan aggrecan in arthritis. Cell Immunol 2005; 235: 98-108 PMID: 16185673
20. Szanto S, Bárdos T, Szabo Z, David CS, Buzás E, Mikecz K, et al. Induction of arthritis in HLA-DR4-humanized and HLA-DQ8-humanized mice by human cartilage proteoglycan aggrecan but only in the presence of an appropriate (non-MHC) genetic background. Arthritis Rheum 2004; 50: 1984-1995 PMID: 15188376
21. Berlo SE, Guichelaar T, Ten Brink CB, Van Kooten PJ, Hauet-Broere F, Ludanyi K, et al. Increased arthritis susceptibility in cartilage proteoglycan-specific T cell receptor-transgenic mice. Arthritis Rheum 2006; 54: 2423-2433 PMID: 16869010
22. Glant TT, Radacs M, Nagyeri G, Olasz K, Laszlo A, Boldizsar F, et al. Proteoglycan-induced arthritis and recombinant human proteoglycan aggrecan G1 domain-induced arthritis in BALB/c mice resembling two subtypes of rheumatoid arthritis. Arthritis Rheum 2011; 63: 1312-1321 doi: 10.1002/art.30261 PMID: 21305522
23. Glant TT, Ocsko T, Markovics A, Szekanecz Z, Katz RS, Rauch TA, et al. Characterization and Localization of Citrullinated Proteoglycan Aggrecan in Human Articular Cartilage. PLoS ONE 2016; 11: e0150784 doi: 10.1371/journal.pone.0150784 PMID: 26943656
24. von Delwig A, Locke J, Robinson JH, Ng WF. Response of Th17 cells to a citrullinated arthritogenic aggrecan peptide in patients with rheumatoid arthritis. Arthritis Rheum 2010; 62: 143-149 doi: 10.1002/art.25064 PMID: 20039419
25. Law SC, Street S, Yu CH, Capini C, Ramnoruth S, Nel HJ, et al. T cell autoreactivity to citrullinated autoantigenic peptides in rheumatoid arthritis patients carrying HLA-DRB1 shared epitope alleles. Arthritis Res Ther 2012; 14: R118 doi: 10.1186/ar3848 PMID: 22594821
26. Misjak P, Bosze S, Horvati K, Pasztoi M, Paloczi K, Holub MC, et al. The role of citrullination of an immunodominant proteoglycan (PG) aggrecan T cell epitope in BALB/c mice with PG-induced arthritis. Immunol Lett 2013; 152: 25-31 PMID: 23578666
27. Aggarwal A, Srivastava R, Agrawal S. T cell responses to citrullinated self-peptides in patients with rheumatoid arthritis. Rheumatol Int 2013; 33: 2359-2363 doi: 10.1007/s00296-013-2731-2 PMID: 23543349
28. Mikecz K, Glant TT, Poole AR. Immunity to cartilage proteoglycans in BALB/c mice with progressive polyarthritis and ankylosing spondylitis induced by injection of human cartilage proteoglycan. Arthritis Rheum 1987; 30: 306-318 PMID: 3566822
29. Glant TT, Cs-Szabo G, Nagase H, Jacobs JJ, Mikecz K. Progressive polyarthritis induced in BALB/c mice by aggrecan from human osteoarthritic cartilage. Arthritis Rheum 1998; 41: 1007-1018 PMID: 9627010
30. Hanyecz A, Berlo SE, Szanto S, Broeren CPM, Mikecz K, Glant TT. Achievement of a synergistic adjuvant effect on arthritis induction by activation of innate immunity and forcing the immune response toward the Th1 phenotype. Arthritis Rheum 2004; 50: 1665-1676 PMID: 15146438
31. Glant TT, Finnegan A, Mikecz K. Proteoglycan-induced arthritis: immune regulation, cellular mechanisms and genetics. Crit Rev Immunol 2003; 23: 199-250 PMID: 14584879
32. Kurko J, Vida A, Ocsko T, Tryniszewska B, Rauch TA, Glant TT, et al. Suppression of proteoglycan-induced autoimmune arthritis by myeloid-derived suppressor cells generated in vitro from murine bone marrow. PLoS ONE 2014; 9: e111815 doi: 10.1371/journal.pone.0111815 PMID: 25369029
33. Boldizsar F, Tarjanyi O, Nemeth P, Mikecz K, Glant TT. Th1/Th17 polarization and acquisition of an arthritogenic phenotype in arthritis-susceptible BALB/c, but not in MHC-matched, arthritis-resistant DBA/2 mice. Int Immunol 2009; 21: 511-522 doi: 10.1093/intimm/dxp018 PMID: 19254958
34. Kugyelka R, Kohl Z, Olasz K, Mikecz K, Rauch TA, Glant TT, et al. Enigma of IL-17 and Th17 Cells in Rheumatoid Arthritis and in Autoimmune Animal Models of Arthritis. Mediators Inflamm 2016; 2016: 6145810 doi: 10.1155/2016/6145810 PMID: 26903711
35. Burmester GR, Feist E, Dorner T. Emerging cell and cytokine targets in rheumatoid arthritis. Nat Rev Rheumatol 2014; 10: 77-88 doi: 10.1038/nrrheum.2013.168 PMID: 24217582
36. Kobezda T, Ghassemi-Nejad S, Mikecz K, Glant TT, Szekanecz Z. Of mice and men: how animal models advance our understanding of T-cell function in RA. Nat Rev Rheumatol 2014; 10: 160-170 doi: 10.1038/nrrheum.2013.205 PMID: 24394350
37. Adarichev VA, Valdez JC, Bardos T, Finnegan A, Mikecz K, Glant TT. Combined autoimmune models of arthritis reveal shared and independent qualitative (binary) and quantitative trait loci. J Immunol 2003; 170: 2283-2292 PMID: 12594249
38. Wieten L, Berlo SE, ten Brink CB, Van Kooten PJ, Singh M, Van der ZR, et al. IL-10 is critically involved in mycobacterial HSP70 induced suppression of proteoglycan-induced arthritis. PLoS ONE 2009; 4: e4186 doi: 10.1371/journal.pone.0004186 PMID: 19142233
39. Kurko J, Vida A, Glant TT, Scanzello CR, Katz RS, Nair A, et al. Identification of myeloid-derived suppressor cells in the synovial fluid of patients with rheumatoid arthritis: a pilot study. BMC Musculoskelet Disord 2014; 15: 281 doi: 10.1186/1471-2474-15-281 PMID: 25138129
40. Hickman-Brecks CL, Racz JL, Meyer DM, LaBranche TP, Allen PM. Th17 cells can provide B cell help in autoantibody induced arthritis. J Autoimmun 2011; 36: 65-75 doi: 10.1016/j.jaut.2010.10.007 PMID: 21075597
41. Conti P, Kempuraj D, Kandere K, Di GM, Barbacane RC, Castellani ML, et al. IL-10, an inflammatory/inhibitory cytokine, but not always. Immunol Lett 2003; 86: 123-129 PMID: 12644313
42. Benedetti G, Miossec P. Interleukin 17 contributes to the chronicity of inflammatory diseases such as rheumatoid arthritis. Eur J Immunol 2014; 44: 339-347 doi: 10.1002/eji.201344184 PMID: 24310226
43. Fonseca JE, Santos MJ, Canhao H, Choy E. Interleukin-6 as a key player in systemic inflammation and joint destruction. Autoimmun Rev 2009; 8: 538-542 doi: 10.1016/j.autrev.2009.01.012 PMID: 19189867
44. Hilbert DM, Cancro MP, Scherle PA, Nordan RP, Van SJ, Gerhard W, et al. T cell derived IL-6 is differentially required for antigen-specific antibody secretion by primary and secondary B cells. J Immunol 1989; 143: 4019-4024 PMID: 2480384
45. Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F, Mazzinghi B, et al. Phenotypic and functional features of human Th17 cells. J Exp Med 2007; 204: 1849-1861 PMID: 17635957
46. Nistala K, Adams S, Cambrook H, Ursu S, Olivito B, de JW, et al. Th17 plasticity in human autoimmune arthritis is driven by the inflammatory environment. Proc Natl Acad Sci U S A 2010; 107: 14751-14756 doi: 10.1073/pnas.1003852107 PMID: 20679229
47. Geginat J, Paroni M, Maglie S, Alfen JS, Kastirr I, Gruarin P, et al. Plasticity of human CD4 T cell subsets. Front Immunol 2014; 5: 630 doi: 10.3389/fimmu.2014.00630 PMID: 25566245
48. Livingstone AM, Fathman CG. The structure of T-cell epitopes. Annu Rev Immunol 1987; 5: 477-501 PMID: 2439104
49. Hill JA, Southwood S, Sette A, Jevnikar AM, Bell DA, Cairns E. Cutting edge: the conversion of arginine to citrulline allows for a high-affinity peptide interaction with the rheumatoid arthritis-associated HLA-DRB1∗0401 MHC class II molecule. J Immunol 2003; 171: 538-541 PMID: 12847215