C57BL/6 mice need MHC class II Aq to develop collagen-induced arthritis dependent on autoreactive T cells

Annals of the Rheumatic Diseases

Volumn 72, Issue 7, 2013, Pages 1225-1232

  Bäcklund, Johan ^a   Li, Cuiqin ^a,b   Jansson, Erik ^a   Carlsen, Stefan ^a   Merky, Patrick ^a   Nandakumar, Kutty Selva ^a   Haag, Sabrina ^a   Ytterberg, Jimmy ^c   Zubarev, Roman A ^a   Holmdahl, Rikard ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SHAANXI NORMAL UNIVERSITY   (China)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPSIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTHRITIS; ARTICLE; CHRONIC DISEASE; CONTROLLED STUDY; CROSS REACTION; DISEASE PREDISPOSITION; DISEASE SEVERITY; FEMALE; IMMUNE RESPONSE; IMMUNOGENICITY; MALE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE;

AUTOIMMUNE DISEASES; INFLAMMATION; T CELLS;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CHICKENS; COLLAGEN TYPE II; DISEASE MODELS, ANIMAL; EPITOPES, T-LYMPHOCYTE; GENES, MHC CLASS II; HAPLOTYPES; IMMUNIZATION; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, INBRED STRAINS; MYCOBACTERIUM; RATS; T-LYMPHOCYTES;

EID: 84878397333     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2012-202055     Document Type: Article

References (56)

1. Michaelsson E, Andersson M, Engstrom A, et al. Identification of an immunodominant type-II collagen peptide recognized by T cells in H-2q mice: self tolerance at the level of determinant selection. Eur J Immunol 1992;22:1819-25.
2. Brunsberg U, Gustafsson K, Jansson L, et al. Expression of a transgenic class II Ab gene confers susceptibility to collagen-induced arthritis. Eur J Immunol 1994;24:1698-702. (Pubitemid 24203781)
3. Andersson EC, Hansen BE, Jacobsen H, et al. Definition of MHC and T cell receptor contacts in the HLA-DR4restricted immunodominant epitope in type II collagen and characterization of collagen-induced arthritis in HLA-DR4 and human CD4 transgenic mice. Proc Natl Acad Sci USA 1998;95:7574-9.
4. Fugger L, Rothbard JB, Sonderstrup-McDevitt G. Specificity of an HLA-DRB1*0401-restricted T cell response to type II collagen. Eur J Immunol 1996;26:928-33.
5. Rosloniec EF, Brand DD, Myers LK, et al. Induction of autoimmune arthritis in HLA-DR4 (DRB1*0401) transgenic mice by immunization with human and bovine type II collagen. J Immunol 1998;160:2573-8. (Pubitemid 28136706)
6. Rosloniec EF, Brand DD, Myers LK, et al. An HLA-DR1 transgene confers susceptibility to collagen-induced arthritis elicited with human type II collagen. J Exp Med 1997;185:1113-22. (Pubitemid 27136803)
7. Rosloniec EF, Whittington KB, Zaller DM, et al. HLA-DR1 (DRB1*0101) and DR4 (DRB1*0401) use the same anchor residues for binding an immunodominant peptide derived from human type II collagen. J Immunol 2002;168:253-9. (Pubitemid 34014125)
8. Holmdahl R, Jansson L, Andersson M, et al. Immunogenetics of type II collagen autoimmunity and susceptibility to collagen arthritis. Immunology 1988;65:305-10.
9. Wooley PH, Luthra HS, Stuart JM, et al. Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates. J Exp Med 1981;154:688-700. (Pubitemid 11060781)
10. Inglis JJ, Criado G, Medghalchi M, et al. Collagen-induced arthritis in C57BL/6 mice is associated with a robust and sustained T-cell response to type II collagen. Arthritis Res Ther 2007;9:R113.
11. Inglis JJ, Simelyte E, McCann FE, et al. Protocol for the induction of arthritis in C57BL/6 mice. Nat Protoc 2008;3:612-8. (Pubitemid 351516757)
12. Campbell IK, Hamilton JA, Wicks IP. Collagen-induced arthritis in C57BL/6 (H-2b) mice: new insights into an important disease model of rheumatoid arthritis. Eur J Immunol 2000;30:1568-75. (Pubitemid 30342798)
13. Holmdahl R, Jansson L, Andersson M. Female sex hormones suppress development of collagen-induced arthritis in mice. Arthritis Rheum 1986;29:1501-9. (Pubitemid 17003889)
14. Andersson M, Holmdahl R. Analysis of type II collagen-reactive T cells in the mouse. I. Different regulation of autoreactive vs. non-autoreactive anti-type II collagen T cells in the DBA/1 mouse. Eur J Immunol 1990;20:1061-6. (Pubitemid 20206058)
15. Strawich E, Nimni ME. Properties of a collagen molecule containing three identical components extracted from bovine articular cartilage. Biochemistry 1971;10:3905-11.
16. Lee-Own V, Anderson JC. Interaction between proteoglycan subunit and type II collagen from bovine nasal cartilage, and the preferential binding of proteoglycan subunit to type I collagen. Biochem J 1976;153:259-64.
17. Michaelsson E, Malmstrom V, Reis S, et al. T cell recognition of carbohydrates on type II collagen. J Exp Med 1994;180:745-9. (Pubitemid 24224156)
18. Spiro RG. Studies on the renal glomerular basement membrane. Nature of the carbohydrate units and their attachment to the peptide portion. J Biol Chem 1967;242:1923-32.
19. Batsalova T, Dzhambazov B, Merky P, et al. Breaking T cell tolerance against self type II collagen in HLA-DR4-transgenic mice and development of autoimmune arthritis. Arthritis Rheum 2010;62:1911-20.
20. Holmdahl R, Carlsen S, Mikulowska A, et al. Genetic analysis of mouse models for rheumatoid arthritis. Boca Raton: CRC Press, 1998.
21. Holmdahl R, Klareskog L, Andersson M, et al. High antibody response to autologous type II collagen is restricted to H-2q. Immunogenetics 1986;24:84-9. (Pubitemid 16040983)
22. Corthay A, Backlund J, Broddefalk J, et al. Epitope glycosylation plays a critical role for T cell recognition of type II collagen in collagen-induced arthritis. Eur J Immunol 1998;28:2580-90. (Pubitemid 28362732)
23. Michaelsson E, Holmdahl M, Engstrom A, et al. Macrophages, but not dendritic cells, present collagen to T cells. Eur J Immunol 1995;25:2234-41.
24. Zlabinger GJ, Menzel EJ, Steffen C. Induction of anti-pepsin antibodies after immunization with pepsin-extracted collagen. Matrix 1989;9:135-9.
25. Vingsbo C, Larsson P, Andersson M, et al. Association of pepsin with type II collagen (CII) breaks control of CII autoimmunity and triggers development of arthritis in rats. Scand J Immunol 1993;37:337-42. (Pubitemid 23070509)
26. Pettitt SJ, Liang Q, Rairdan XY, et al. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat Methods 2009;6:493-5.
27. Mekada K, Abe K, Murakami A, et al. Genetic differences among C57BL/6 substrains. Exp Anim 2009;58:141-9.
28. Zurita E, Chagoyen M, Cantero M, et al. Genetic polymorphisms among C57BL/6 mouse inbred strains. Transgenic Res 2011;20:481-9.
29. Kiselycznyk C, Holmes A. All (C57BL/6) mice are not created equal. Front Neurosci 2011;5:10.
30. Holm B, Backlund J, Recio MA, et al. Glycopeptide specificity of helper T cells obtained in mouse models for rheumatoid arthritis. Chembiochem 2002;3:1209-22. (Pubitemid 36005313)
31. Brand DD, Myers LK, Terato K, et al. Characterization of the T cell determinants in the induction of autoimmune arthritis by bovine alpha 1(II)-CB11 in H-2q mice. J Immunol 1994;152:3088-97.
32. Kim HY, Kim WU, Cho ML, et al. Enhanced T cell proliferative response to type II collagen and synthetic peptide CII (255-274) in patients with rheumatoid arthritis. Arthritis Rheum 1999;42:2085-93.
33. Backlund J, Carlsen S, Hoger T, et al. Predominant selection of T cells specific for the glycosylated collagen type II epitope (263-270) in humanized transgenic mice and in rheumatoid arthritis. Proc Natl Acad Sci U S A 2002;99:9960-5. (Pubitemid 34831155)
34. Burkhardt H, Koller T, Engstrom A, et al. Epitope-specific recognition of type II collagen by rheumatoid arthritis antibodies is shared with recognition by antibodies that are arthritogenic in collagen-induced arthritis in the mouse. Arthritis Rheum 2002;46:2339-48.
35. Ohnishi Y, Tsutsumi A, Sakamaki T, et al. T cell epitopes of type II collagen in HLA-DRB1*0101 or DRB1*0405-positive Japanese patients with rheumatoid arthritis. Int J Mol Med 2003;11:331-5.
36. Uysal H, Nandakumar KS, Kessel C, et al. Antibodies to citrullinated proteins: molecular interactions and arthritogenicity. Immunol Rev 2010;233:9-33.
37. Snir O, Backlund J, Bostrom J, et al. Multifunctional T cell reactivity to native and glycosylated type-II collagen in rheumatoid arthritis. Arthritis Rheum 2012;64:2482-8.
38. Malmstrom V, Michaelsson E, Burkhardt H, et al. Systemic versus cartilage-specific expression of a type II collagen-specific T-cell epitope determines the level of tolerance and susceptibility to arthritis. Proc Natl Acad Sci U S A 1996;93:4480-5.
39. Malmstrom V, Backlund J, Jansson L, et al. T cells that are naturally tolerant to cartilage-derived type II collagen are involved in the development of collagen-induced arthritis. Arthritis Res 2000;2:315-26. (Pubitemid 32223758)
40. Nandakumar KS, Lindqvist AK, Holmdahl R. A dominant suppressive MHC class II haplotype interacting with autosomal genes controls autoantibody production and chronicity of arthritis. Ann Rheum Dis 2011;70:1664-70.
41. Bockermann R, Holmdahl R. Type II collagen without adjuvant induces eosinophilic arthritis. Eur J Immunol 2007;37:540-8. (Pubitemid 46915592)
42. Kollias G, Papadaki P, Apparailly F, et al. Animal models for arthritis: innovative tools for prevention and treatment. Ann Rheum Dis 2011;70:1357-62.
43. Yuasa T, Kubo S, Yoshino T, et al. Deletion of fcgamma receptor IIB renders H-2(b) mice susceptible to collagen-induced arthritis. J Exp Med 1999;189:187-94. (Pubitemid 29047038)
44. Guedez YB, Whittington KB, Clayton JL, et al. Genetic ablation of interferon-gamma up-regulates interleukin-1beta expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum 2001;44:2413-24. (Pubitemid 32977511)
45. Chu CQ, Song Z, Mayton L, et al. IFNgamma deficient C57BL/6 (H-2b) mice develop collagen induced arthritis with predominant usage of T cell receptor Vbeta6 and Vbeta8 in arthritic joints. Ann Rheum Dis 2003;62:983-90. (Pubitemid 37159498)
46. Kai H, Shibuya K, Wang Y, et al. Critical role of M. tuberculosis for dendritic cell maturation to induce collagen-induced arthritis in H-2b background of C57BL/6 mice. Immunology 2006;118:233-9. (Pubitemid 43727428)
47. Carlsen S, Nandakumar KS, Backlund J, et al. Cartilage oligomeric matrix protein induction of chronic arthritis in mice. Arthritis Rheum 2008;58:2000-11. (Pubitemid 351988092)
48. Cremer MA, Ye XJ, Terato K, et al. Type XI collagen-induced arthritis in the Lewis rat. Characterization of cellular and humoral immune responses to native types XI, V, and II collagen and constituent alpha-chains. J Immunol 1994;153:824-32. (Pubitemid 24206313)
49. Lu S, Carlsen S, Hansson AS, et al. Immunization of rats with homologous type XI collagen leads to chronic and relapsing arthritis with different genetics and joint pathology than arthritis induced with homologous type II collagen. J Autoimmun 2002;18:199-211. (Pubitemid 36269069)
50. Glant TT, Mikecz K, Arzoumanian A, et al. Proteoglycan-induced arthritis in BALB/c mice. Clinical features and histopathology. Arthritis Rheum 1987;30:201-12. (Pubitemid 17060776)
51. Zhang Y, Guerassimov A, Leroux JY, et al. Induction of arthritis in BALB/c mice by cartilage link protein: involvement of distinct regions recognized by T and B lymphocytes. Am J Pathol 1998;153:1283-91. (Pubitemid 28465852)
52. Brand DD, Kang AH, Rosloniec EF. Immunopathogenesis of collagen arthritis. Springer Semin Immunopathol 2003;25:3-18. (Pubitemid 37000035)
53. Malmstrom V, Kjellen P, Holmdahl R. Type II collagen in cartilage evokes peptide-specific tolerance and skews the immune response. J Autoimmun 1998;11:213-21. (Pubitemid 28319786)
54. Rowley MJ, Nandakumar KS, Holmdahl R. The role of collagen antibodies in mediating arthritis. Mod Rheumatol 2008;18:429-41.
55. Eyre DR, Pietka T, Weis MA, et al. Covalent cross-linking of the NC1 domain of collagen type IX to collagen type II in cartilage. J Biol Chem 2004;279:2568-74. (Pubitemid 38114242)
56. Holmdahl R, Malissen B. The need for littermate controls. Eur J Immunol 2012;42:45-7.