Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin

Journal of Clinical Investigation

Volumn 122, Issue 5, 2012, Pages 1791-1802

  Harre, Ulrike ^a   Georgess, Dan ^b   Bang, Holger ^c   Bozec, Aline ^a   Axmann, Roland ^a   Ossipova, Elena ^d   Jakobsson, Per Johan ^d   Baum, Wolfgang ^a   Nimmerjahn, Falk ^a   Szarka, Eszter ^e   Sarmay, Gabriella ^e   Krumbholz, Grit ^f   Neumann, Elena ^f   Toes, Rene ^g   Scherer, Hans Ulrich ^g   Catrina, Anca Irinel ^c   Klareskog, Lars ^c   Jurdic, Pierre ^b   Schett, Georg ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITÉ DE LYON   (France)

^c Orgentec Diagnostika   (Germany)

^d KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^e EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^f JUSTUS LIEBIG UNIVERSITY   (Germany)

^g LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME 5B; AUTOANTIBODY; CATHEPSIN K; CITRULLINATED VIMENTIN ANTIBODY; COLLAGEN TYPE 1; PROTEIN ARGININE DEIMINASE; PROTEIN ARGININE DEIMINASE 2; PROTEIN ARGININE DEIMINASE 4; RHEUMATOID FACTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIMENTIN;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BONE METABOLISM; CASE REPORT; CELL COUNT; CELL DIFFERENTIATION; CELL SURFACE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; HUMAN; HUMAN CELL; LASER MICROSCOPY; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPENIA; PRIORITY JOURNAL; PROTEIN CITRULLINATION; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; STEM CELL; WESTERN BLOTTING;

ANIMALS; ANTIBODY SPECIFICITY; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; BIOLOGICAL MARKERS; BONE AND BONES; BONE RESORPTION; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CELLS, CULTURED; CITRULLINE; COLLAGEN TYPE I; HUMANS; HYDROLASES; MICE; MICE, TRANSGENIC; OSTEOCLASTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TUMOR NECROSIS FACTOR-ALPHA; VIMENTIN;

EID: 84860561645     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI60975     Document Type: Article

References (42)

1. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature. 2003;423(6937):356-361. (Pubitemid 40852711)
2. McInnes IB, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol. 2007;7(6):429-442. (Pubitemid 46834849)
3. Klareskog L, et al. A new model for an etiology of rheumatoid arthritis: smoking may trigger HLADR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum. 2006;54(1):38-46.
4. Mahdi H, et al. Specific interaction between genotype, smoking and autoimmunity to citrullinated alpha-enolase in the etiology of rheumatoid arthritis. Nat Genet. 2009;41(12):1319-1324.
5. Vossenaar ER, Zendman AJ, van Venrooij WJ, Pruijn GJ. PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays. 2003;25(11):1106-1118. (Pubitemid 37411770)
6. Wegner N, et al. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum. 2010;62(9):2662-2672.
7. Vincent C, de Keyser F, Masson-Bessiere C, Sebbag M, Veys E, Serre G. Anti-perinuclear factor compared with the so called "antikeratin" antibodies and antibodies to human epidermis filaggrin, in the diagnosis of arthritides. Ann Rheum Dis. 1999;58(1):42-48. (Pubitemid 29112949)
8. De Rycke L, et al. Rheumatoid factor and anticitrullinated protein antibodies in rheumatoid arthritis: diagnostic value, associations with radiological progression rate, and extra-articular manifestations. Ann Rheum Dis. 2004;63(12):1587-1593. (Pubitemid 39573686)
9. van der Woude D, et al. Epitope spreading of the anti-citrullinated protein antibody response occurs before disease onset and is associated with the disease course of early arthritis. Ann Rheum Dis. 2010;69(8):1554-1561.
10. Schett G, Teitelbaum SL. Osteoclasts and arthritis. J Bone Miner Res. 2009;24(7):1142-1146.
11. Schett G, et al. High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch Intern Med. 2006;166(22):2495-2501. (Pubitemid 44913235)
12. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol. 2007;7(4):292-304. (Pubitemid 46480961)
13. van Gaalen FA, et al. Autoantibodies to cyclic citrullinated peptides predict progression to rheumatoid arthritis in patients with undifferentiated arthritis: a prospective cohort study. Arthritis Rheum. 2004;50(3):709-715.
14. Syversen SW, et al. Prediction of radiographic progression in rheumatoid arthritis and the role of antibodies against mutated citrullinated vimentin: results from a 10-year prospective study. Ann Rheum Dis. 2010;69(2):345-351.
15. van der Linden MP, et al. Value of anti-modified citrullinated vimentin and third-generation anticyclic citrullinated peptide compared with secondgeneration anti-cyclic citrullinated peptide and rheumatoid factor in predicting disease outcome in undifferentiated arthritis and rheumatoid arthritis. Arthritis Rheum. 2009;60(8):2232-2241.
16. Raza K, Mathsson L, Buckley CD, Filer A, Rönnelid J. Anti-modified citrullinated vimentin (MCV) antibodies in patients with very early synovitis. Ann Rheum Dis. 2010;69(3):627-628.
17. Bang H, et al. Mutation and citrullination modifies vimentin to a novel autoantigen for rheumatoid arthritis. Arthritis Rheum. 2007;56(8):2503-2511. (Pubitemid 47237269)
18. Mathsson L, et al. Antibodies against citrullinated vimentin in rheumatoid arthritis: higher sensitivity and extended prognostic value concerning future radiographic progression as compared with antibodies against cyclic citrullinated peptides. Arthritis Rheum. 2008;58(1):36-45.
19. Dellagi K, Vainchenker W, Vinci G, Paulin D, Brouet JC. Alteration of vimentin intermediate filament expression during differentiation of human hemopoietic cells. EMBO J. 1983;2(9):1509-1514.
20. Kuhn KA, et al. Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J Clin Invest. 2006;116(4):961-973.
21. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest. 2000;106(12):1481- 1488. (Pubitemid 32038586)
22. Li P, et al. RANK signaling is not required for TNF-mediated increase in CD11(hi) osteoclast precursors but is essential for mature osteoclast formation in TNFalpha-mediated inflammatory arthritis. J Bone Miner Res. 2004;19(2):207-213. (Pubitemid 38116734)
23. Sato K, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006; 203(12):2673-2682. (Pubitemid 44833343)
24. Riches PL, McRorie E, Fraser WD, Determann C, van't Hof R, Ralston SH. Osteoporosis associated with neutralizing autoantibodies against osteoprotegerin. N Engl J Med. 2009;361(15):1459-1465.
25. Clavel C, 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(3):678-688. (Pubitemid 351364865)
26. Laurent L, et al. Fc{gamma} receptor profile of monocytes and macrophages from rheumatoid arthritis patients and their response to immune complexes formed with autoantibodies to citrullinated proteins. Ann Rheum Dis. 2011;70(6):1052-1059.
27. Lu MC, Lai NS, Yu HC, Huang HB, Hsieh SC, Yu CL. Anti-citrullinated protein antibodies bind surfaceexpressed citrullinated Grp78 on monocyte/macrophages and stimulate tumor necrosis factor alpha production. Arthritis Rheum. 2010;62(5):1213-1223.
28. Sokolove J, Zhao X, Chandra PE, Robinson WH. Immune complexes containing citrullinated fibrinogen costimulate macrophages via Toll-like receptor 4 and Fcγ receptor. Arthritis Rheum. 2011;63(1):53-62.
29. Lian N, Wang W, Li L, Elefteriou F, Yang X. Vimentin inhibits ATF4-mediated osteocalcin transcription and osteoblast differentiation. J Biol Chem. 2009;284(44):30518-30525.
30. Guler-Yuksel M, et al. Changes in hand and generalised bone mineral density in patients with recent-onset rheumatoid arthritis. Ann Rheum Dis. 2009;68(3):330-336.
31. Rantapää-Dahlqvist S, et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum. 2003;48(10):2741-2749. (Pubitemid 37280601)
32. Vossenaar ER, et al. Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macrophages. Ann Rheum Dis. 2004;63(4):373-381. (Pubitemid 38453302)
33. Foulquier C, et al. 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(11):3541-3553. (Pubitemid 350100687)
34. Chang X, et al. Localization of peptidylarginine deiminase 4 (PADI4) and citrullinated protein in synovial tissue of rheumatoid arthritis. Rheumatology (Oxford). 2005;44(1):40-50. (Pubitemid 40124330)
35. Hojo-Nakashima I, Sato R, Nakashima K, Hagiwara T, Yamada M. Dynamic expression of peptidylarginine deiminase 2 in human monocytic leukaemia THP-1 cells during macrophage differentiation. J Biochem. 2009;146(4):471-479.
36. Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med. 2010;207(9):1853-1862.
37. Arita K, Hashimoto H, Shimizu T, Nakashima K, Yamada M, Sato M. Structural basis for Ca(2+)- induced activation of human PAD4. Nat Struct Mol Biol. 2004;11(8):777-783 (Pubitemid 39014504)
38. Marchisio PC, Cirillo D, Naldini L, Primavera MV, Teti A, Zambonin-Zallone A. Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures. J Cell Biol. 1984;99(5):1696-1705. (Pubitemid 15223606)
39. Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM. Vimentin is secreted by activated macrophages. Nat Cell Biol. 2003;5(1):59-63. (Pubitemid 36054330)
40. Auger I, Balandraud N, Rak J, Lambert N, Martin M, Roudier J. New autoantigens in rheumatoid arthritis (RA): screening 8268 protein arrays with sera from patients with RA. Ann Rheum Dis. 2009;68(4):591-594.
41. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010;25(7):1468-1486.
42. Hildebrand T, Laib A, Muller R, Dequeker J, Ruegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. 1999;14(7):1167-1174. (Pubitemid 29314060)