Citrullinated calreticulin potentiates rheumatoid arthritis shared epitope signaling

Arthritis and Rheumatism

Volumn 65, Issue 3, 2013, Pages 618-626

  Ling, Song ^a   Cline, Erika N ^a   Haug, Timothy S ^a   Fox, David A ^a   Holoshitz, Joseph ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CALRETICULIN; CELL SURFACE CALRETICULIN; HLA DRB1 ANTIGEN; NITRIC OXIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; BINDING SITE; CELL CULTURE; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MASS SPECTROMETRY; MOUSE; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; SITE DIRECTED MUTAGENESIS; SURFACE PLASMON RESONANCE; SYNOVIOCYTE; SYNOVIUM; TWO DIMENSIONAL ELECTROPHORESIS;

ANIMALS; ANTIGENS, SURFACE; ARGININE; ARTHRITIS, RHEUMATOID; BINDING SITES; CALRETICULIN; CELL LINE; CITRULLINE; EPITOPES; FIBROBLASTS; GENE-ENVIRONMENT INTERACTION; HLA-DRB1 CHAINS; HUMANS; MICE; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; SYNOVIAL MEMBRANE;

EID: 84874405711     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37814     Document Type: Article

References (48)

1. Gregersen PK, Silver J, Winchester RJ,. The shared epitope hypothesis: an approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum 1987; 30: 1205-13.
2. Turesson C, Schaid DJ, Weyand CM, Jacobsson LT, Goronzy JJ, Petersson, IF, et al. The impact of HLA-DRB1 genes on extra-articular disease manifestations in rheumatoid arthritis. Arthritis Res Ther 2005; 7: R1386-93.
3. Moreno I, Valenzuela A, Garcia A, Yelamos J, Sanchez, B, Hernanz W,. Association of the shared epitope with radiological severity of rheumatoid arthritis. J Rheumatol 1996; 23: 6-9.
4. Ling S, Lai A, Borschukova O, Pumpens P, Holoshitz J,. Activation of nitric oxide signaling by the rheumatoid arthritis shared epitope. Arthritis Rheum 2006; 54: 3423-32.
5. Ling S, Li Z, Borschukova O, Xiao L, Pumpens P, Holoshitz J,. The rheumatoid arthritis shared epitope increases cellular susceptibility to oxidative stress by antagonizing an adenosine-mediated anti-oxidative pathway. Arthritis Res Ther 2007; 9: R5.
6. Ling S, Pi X, Holoshitz J,. The rheumatoid arthritis shared epitope triggers innate immune signaling via cell surface calreticulin. J Immunol 2007; 179: 6359-67.
7. De Almeida DE, Ling S, Pi X, Hartmann-Scruggs AM, Pumpens P, Holoshitz J,. Immune dysregulation by the rheumatoid arthritis shared epitope. J Immunol 2010; 185: 1927-34.
8. Ling S, Cheng A, Pumpens P, Michalak M, Holoshitz J,. Identification of the rheumatoid arthritis shared epitope binding site on calreticulin. PLoS One 2010; 5: e11703.
9. Silman AJ, MacGregor A, Thomson W, Holligan S, Carthy D, Ollier WE,. Twin concordance rates for rheumatoid arthritis: results of a nationwide study. Br J Rheumatol 1993; 32: 903-7.
10. Jungel A, Ospelt C, Gay S,. What can we learn from epigenetics in the year 2009? Curr Opin Rheumatol 2010; 22: 284-92.
11. Makrygiannakis D, af Klint E, Lundberg IE, Lofberg R, Ulfgren AK, Klareskog L, et al. Citrullination is an inflammation-dependent process. Ann Rheum Dis 2006; 65: 1219-22.
12. Vossenaar ER, Smeets TJ, Kraan MC, Raats JM, van Venrooij WJ, Tak PP,. The presence of citrullinated proteins is not specific for rheumatoid synovial tissue. Arthritis Rheum 2004; 50: 3485-94.
13. Masson-Bessiere C, Sebbag M, Girbal-Neuhauser E, Nogueira L, Vincent C, Senshu T, et al. The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the α- and β-chains of fibrin. J Immunol 2001; 166: 4177-84.
14. Matsuo K, Xiang Y, Nakamura H, Masuko K, Yudoh K, Noyori K, et al. Identification of novel citrullinated autoantigens of synovium in rheumatoid arthritis using a proteomic approach. Arthritis Res Ther 2006; 8: R175.
15. Chang X, Yamada R, Suzuki A, Kochi Y, Sawada T, Yamamoto K,. Citrullination of fibronectin in rheumatoid arthritis synovial tissue. Rheumatology (Oxford) 2005; 44: 1374-82.
16. Klareskog L, Ronnelid J, Lundberg K, Padyukov L, Alfredsson L,. Immunity to citrullinated proteins in rheumatoid arthritis. Annu Rev Immunol 2008; 26: 651-75.
17. Huizinga TW, Amos CI, van der Helm-van Mil AH, Chen W, van Gaalen FA, Jawaheer D, et al. Refining the complex rheumatoid arthritis phenotype based on specificity of the HLA-DRB1 shared epitope for antibodies to citrullinated proteins. Arthritis Rheum 2005; 52: 3433-8.
18. Padyukov L, Silva C, Stolt P, Alfredsson L, Klareskog L, for the Epidemiological Investigation of Rheumatoid Arthritis Study Group. A gene-environment interaction between smoking and shared epitope genes in HLA-DR provides a high risk of seropositive rheumatoid arthritis. Arthritis Rheum 2004; 50: 3085-92.
19. Pedersen M, Jacobsen S, Garred P, Madsen HO, Klarlund M, Svejgaard A, et al. Strong combined gene-environment effects in anti-cyclic citrullinated peptide-positive rheumatoid arthritis: a nationwide case-control study in Denmark. Arthritis Rheum 2007; 56: 1446-53.
20. Karlson EW, Chang SC, Cui J, Chibnik LB, Fraser PA, Devivo I, et al. Gene-environment interaction between HLA-DRB1 shared epitope and heavy cigarette smoking in predicting incident RA. Ann Rheum Dis 2010; 69: 54-60.
21. Makrygiannakis D, Hermansson M, Ulfgren AK, Nicholas AP, Zendman AJ, Eklund A, et al. Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis 2008; 67: 1488-92.
22. Tran CN, Davis MJ, Tesmer LA, Endres JL, Motyl CD, Smuda C, et al. Presentation of arthritogenic peptide to antigen-specific T cells by fibroblast-like synoviocytes. Arthritis Rheum 2007; 56: 1497-506.
23. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988; 31: 315-24.
24. Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause KH, et al. Calreticulin is essential for cardiac development. J Cell Biol 1999; 144: 857-68.
25. Vossenaar ER, Nijenhuis S, Helsen MM, van der Heijden A, Senshu T, van den Berg WB, et al. Citrullination of synovial proteins in murine models of rheumatoid arthritis. Arthritis Rheum 2003; 48: 2489-500.
26. Holm A, Rise F, Sessler N, Sollid LM, Undheim K, Fleckenstein B,. Specific modification of peptide-bound citrulline residues. Anal Biochem 2006; 352: 68-76.
27. Vivekanandan-Giri A, Slocum JL, Buller CL, Basrur V, Ju W, Pop-Busui R, et al. Urine glycoprotein profile reveals novel markers for chronic kidney disease. Int J Proteomics 2011; 214715.
28. Goicoechea S, Pallero MA, Eggleton P, Michalak M, Murphy-Ullrich JE,. The anti-adhesive activity of thrombospondin is mediated by the N-terminal domain of cell surface calreticulin. J Biol Chem 2002; 277: 37219-28.
29. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13: 54-61.
30. Gyorgy B, Toth E, Tarcsa E, Falus A, Buzas EI,. Citrullination: a posttranslational modification in health and disease. Int J Biochem Cell Biol 2006; 38: 1662-77.
31. Senshu T, Akiyama K, Nomura K,. Identification of citrulline residues in the V subdomains of keratin K1 derived from the cornified layer of newborn mouse epidermis. Exp Dermatol 1999; 8: 392-401.
32. Guo Q, Fast W,. Citrullination of inhibitor of growth 4 (ING4) by peptidylarginine deminase 4 (PAD4) disrupts the interaction between ING4 and p53. J Biol Chem 2011; 286: 17069-78.
33. 2+-dependent deimination-induced disassembly of intermediate filaments involves specific modification of the amino-terminal head domain. J Biol Chem 1989; 264: 18119-27.
34. Pritzker LB, Joshi S, Gowan JJ, Harauz G, Moscarello MA,. Deimination of myelin basic protein. 1. Effect of deimination of arginyl residues of myelin basic protein on its structure and susceptibility to digestion by cathepsin D. Biochemistry 2000; 39: 5374-81.
35. Holoshitz J, De Almeida DE, Ling S,. A role for calreticulin in the pathogenesis of rheumatoid arthritis. Ann N Y Acad Sci 2010; 1209: 91-8.
36. De Almeida DE, Ling S, Holoshitz J,. New insights into the functional role of the rheumatoid arthritis shared epitope. FEBS Lett 2011; 585: 3619-2.
37. De Almeida DE, Holoshitz J,. MHC molecules in health and disease: at the cusp of a paradigm shift. Self Nonself 2011; 2: 43-8.
38. Goeb V, Thomas-L'Otellier M, Daveau R, Charlionet R, Fardellone P, Le Loet X, et al. Candidate autoantigens identified by mass spectrometry in early rheumatoid arthritis are chaperones and citrullinated glycolytic enzymes. Arthritis Res Ther 2009; 11: R38.
39. Ishigami A, Ohsawa T, Hiratsuka M, Taguchi H, Kobayashi S, Saito Y, et al. Abnormal accumulation of citrullinated proteins catalyzed by peptidylarginine deiminase in hippocampal extracts from patients with Alzheimer's disease. J Neurosci Res 2005; 80: 120-8.
40. De Ceuleneer M, Van Steendam K, Dhaenens M, Deforce D,. In vivo relevance of citrullinated proteins and the challenges in their detection. Proteomics 2012; 12: 752-60.
41. Neeli I, Kahn SN, Radic M,. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008; 180: 1895-902.
42. Musse AA, Harauz G,. Molecular "negativity" may underlie multiple sclerosis: role of the myelin basic protein family in the pathogenesis of MS. Int Rev Neurobiol 2007; 79: 149-72.
43. Uysal H, Nandakumar KS, Kessel C, Haag S, Carlsen S, Burkhardt H, et al. Antibodies to citrullinated proteins: molecular interactions and arthritogenicity. Immunol Rev 2010; 233: 9-33.
44. Hill JA, Bell DA, Brintnell W, Yue D, Wehrli B, Jevnikar AM, et al. Arthritis induced by posttranslationally modified (citrullinated) fibrinogen in DR4-IE transgenic mice. J Exp Med 2008; 205: 967-79.
45. Harre U, Georgess D, Bang H, Bozec A, Axmann R, Ossipova E, et al. Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 2012; 122: 1791-802.
46. James EA, Moustakas AK, Bui J, Papadopoulos GK, Bondinas G, Buckner JH, et al. HLA-DR1001 presents "altered-self" peptides derived from joint-associated proteins by accepting citrulline in three of its binding pockets. Arthritis Rheum 2010; 62: 2909-18.
47. Hill JA, Bell DA, Brintnell W, Yue D, Wehrli B, Jevnikar AM, et al. Arthritis induced by posttranslationally modified (citrullinated) fibrinogen in DR4-IE transgenic mice. J Exp Med 2008; 205: 967-79.
48. Curtis MM, Way SS,. Interleukin-17 in host defense against bacterial, mycobacterial and fungal pathogens. Immunology 2009; 126: 177-85.