Mechanism by which HLA-DR4 regulates sex-bias of arthritis in humanized mice

Journal of Autoimmunity

Volumn 35, Issue 1, 2010, Pages 1-9

  Behrens, Marshall ^a   Trejo, Theodore ^a   Luthra, Harvinder ^b   Griffiths, Marie ^c   David, Chella S ^a   Taneja, Veena ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen presentation; HLA DR4; Rheumatoid arthritis; Sex bias; Transgenic mice

Indexed keywords

AUTOANTIBODY; ESTRADIOL; GAMMA INTERFERON; HLA DR4 ANTIGEN; INTERLEUKIN 13; INTERLEUKIN 23; TRANSFORMING GROWTH FACTOR BETA; AUTOANTIGEN; HLA DR ANTIGEN; HLA DRB1 ANTIGEN; HLA-DRB1*04:01 ANTIGEN; PEPTIDE FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CASTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; FEMALE; GENDER BIAS; HAPLOTYPE; HORMONAL REGULATION; IMMUNOREGULATION; LYMPHOCYTE COUNT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SEX DIFFERENCE; TRANSGENIC MOUSE; ANIMAL; ARTHRITIS, RHEUMATOID; CELL CULTURE; COMPARATIVE STUDY; DRUG EFFECTS; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INCIDENCE; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; SCID MOUSE; SECRETION (PROCESS); T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; ARTHRITIS, RHEUMATOID; AUTOANTIGENS; B-LYMPHOCYTES; CASTRATION; CELLS, CULTURED; ESTRADIOL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HLA-DR ANTIGENS; HUMANS; IMMUNE TOLERANCE; INCIDENCE; INTERFERON-GAMMA; INTERLEUKIN-13; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, SCID; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; SEX FACTORS; T-LYMPHOCYTES; HLA-DRB1 CHAINS;

EID: 77953287830     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2009.12.007     Document Type: Article

References (39)

1. Cuotolo M. Sex and rheumatoid arthritis: mouse model versus human disease. Arthritis Rheum 2007, 56:1-3.
2. Bouman A., Schipper M., Heineman M.J., Faas M.M. Gender difference in the non-specific and specific immune response in humans. Am J Reprod Immunol 2004, 52:19-26.
3. Giron-Gonzalez J.A., Moral F.J., Elvira J., García-Gil D., Guerrero F., Gavilán I., et al. Consistent production of a higher TH1:TH2 cytokine ratio by stimulated T cells in men compared with women. Eur J Endocrinol 2000, 143:31-36.
4. Winchester R., Dawyer E., Rose S. The genetic basis of rheumatoid arthritis. The shared epitope hypothesis. Rheum Dis Clin North Am 1992, 18:761-783.
5. Taneja V., Mehra N.K., Chandershekaran A.N., Ahuja R.K., Singh Y.N., Malaviya A.N. HLA-DR4-DQw8 but not DR4-DQw7 haplotypes occur in Indian patients with rheumatoid arthritis. Rheumatol Int 1992, 11:251-255.
6. Stephens H.A., Sakkas L.I., Vaughan R.W., Teitsson I., Welsh K.I., Panayi G.S. HLA-DQw7 is a disease severity marker in patients with rheumatoid arthritis. Immunogenetics 1989, 30:119-122.
7. Moller E., Bohme J., Valugerdi M.A., Ridderstad A., Olerup O. Speculations on the mechanism of HLA association with autoimmune diseases and the specificity of autoreactive T lymphocytes. Immunol Rev 1990, 118:5-19.
8. Meyer J.M., Han J., Singh R., Moxley G. Sex influences on the penetrance of HLA shared-epitope genotypes for rheumatoid arthritis. Am J Hum Genet 1996, 58:371-383.
9. Jawaheer D., Lum R.F., Gregersen P.K., Criswell L.A. Influence of male sex on disease phenotype in familial rheumatoid arthritis. Arthritis Rheum 2006, 54:3087-3094.
10. He X., Kang A.H., Stuart J.M. Accumulation of T cells reactive to type II collagen in synovial fluid of patients with rheumatoid arthritis. J Rheumatol 2000, 27:589-593.
11. Nishimura K., Sugiyama D., Kogata Y., Tsuji G., Nakazawa T., Kawano S., et al. Meta-analysis: diagnostic accuracy of anti-cyclic citrullinated peptide antibody and rheumatoid factor for rheumatoid arthritis. Ann Intern Med 2007, 146:797-808.
12. Huseyin U., Bockermann R., Nandakumar K.S., Sehnert B., Bajtner E., Engström A., et al. Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. J Exp Med 2009, 206:449-462.
13. Taneja V., Taneja N., Paisansinsup T., Behrens M., Griffiths M., Luthra H.S., et al. CD4 and CD8 T cells in susceptibility/protection to collagen-induced arthritis in HLA-DQ8 transgenic mice: implications for rheumatoid arthritis. J Immunol 2002, 168:5867-5875.
14. Taneja V., Griffiths M.M., Luthra H.S., David C.S. Modulation of HLA-DQ-restricted collagen-induced arthritis by HLA-DRB1 polymorphism. Int Immunol 1998, 10:1449-1457.
15. Taneja V., Behrens M., Mangalam A., Griffiths M.M., Luthra H.S., David C.S. New humanized HLA-DR4-transgenic mice that mimic the sex bias of rheumatoid arthritis. Arthritis Rheum 2007, 56:69-78.
16. Taneja V., Behrens M., Basal E., Sparks J., Griffiths M.M., Luthra H.S., et al. Delineating the role of HLA-DR4 shared epitope in susceptibility versus resistance to develop arthritis. J Immunol 2008, 181:2869-2877.
17. Reddy J., Waldner H., Zhang X., Illes Z., Wucherpfennig K.W., Sobel R.A., et al. CD4+CD25+ regulatory T cells contribute to gender differences in susceptibility to experimental autoimmune encephalomyelitis. J Immunol 2005, 175:5591-5595.
18. Brennan F.M., McInnes I.B. Evidence that cytokines play a role in rheumatoid arthritis. J Clin Invest 2008, 118:3537-3545.
19. Bettelli E., Oukka M., Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007, 8:345-350.
20. Irmler I.M., Gajda M., Bräuer R. Exacerbation of antigen-induced arthritis in IFN-gamma-deficient mice as a result of unrestricted IL-17 response. J Immunol 2007, 179:6228-6236.
21. Shen H., Goodall J.C., Hill Gaston J.S. Frequency and phenotype of the peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid factor. Arthritis Rheum 2009, 60:1647-1656.
22. Suryani S., Sutton I. An interferon-gamma-producing Th1 subset is the major source of IL-17 in experimental autoimmune encephalitis. J Neuroimmunol 2007, 183:96-110.
23. de Waal Malefyt R., Figdor C.G., Huijbens R., Mohan-Peterson S., Bennett B., Culpepper J., et al. Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J Immunol 1993, 151:6370-6381.
24. Minty A., Chalon P., Derocq J.M., Dumont X., Guillemot J.C., Kaghad M., et al. Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature 1993, 362:248-250.
25. Defrance T., Carayon P., Billian G., Guillemot J.C., Minty A., Caput D., et al. Interleukin 13 is a B cell stimulating factor. J Exp Med 1994, 179:135-143.
26. Sinha S., Kaler L.J., Proctor T.M., Teuscher C., Vandenbark A.A., Offner H. IL-13-mediated gender difference in susceptibility to autoimmune encephalomyelitis. J Immunol 2008, 180:2679-2685.
27. Hitchon C.A., Alex P., Erdile L.B., Frank M.B., Dozmorov I., Tang Y., et al. A distinct multicytokine profile is associated with anti-cyclical citrullinated peptide antibodies in patients with early untreated inflammatory arthritis. J Rheumatol 2004, 31:2336-2346.
28. Yanaba K., Bouaziz J.D., Haas K.M., Poe J.C., Fujimoto M., Tedder T.F. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008, 28:639-650.
29. Taneja V., Krco C.J., Behrens M., Luthra H.S., Griffiths M.M., David C.S. B cells are important as antigen presenting cells for induction of MHC-restricted arthritis in transgenic mice. Mol Immunol 2007, 44:2988-2996.
30. Edwards J.C., Szczepanski L., Szechinski J., Filipowicz-Sosnowska A., Emery P., Close D.R., et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004, 350:2572-2581.
31. Roll P., Dorner T., Tony H.P. Anti-CD20 therapy in patients with rheumatoid arthritis. Arthritis Rheum 2008, 58:1566-1575.
32. Grimaldi C.M., Cleary J., Dagtas A.S., Moussai D., Diamond B. Estrogen alters thresholds for B cell. J Clin Invest 2002, 109:1625-1633.
33. Tengstrand B., Carlström K., Felländer-Tsai L., Hafström I. Abnormal levels of serum dehydroepiandrosterone, estrone, and estradiol in men with rheumatoid arthritis: high correlation between serum estradiol and current degree of inflammation. J Rheumatol 2003, 30:2338-2343.
34. Cutolo M., Capellino S., Sulli A., Serioli B., Secchi M.E., Villaggio B., et al. Estrogens and autoimmune diseases. Ann N Y Acad Sci 2006, 1089:538-547.
35. Whitacre C.C. Sex differences in autoimmune disease. Nat Immunol 2001, 2:777-780.
36. Kinloch A., Lundberg K., Venables P. The pathogenic role of antibodies to citrullinated proteins in rheumatoid arthritis. Exp Rev Clin Immunol 2006, 2:365-375.
37. Van der Helm-van Mil A.H., Verpoort K.N., Breedveld F.C., Huizinga T.W., Toes R.E., de Vries R.R. The HLA-DRB1 shared epitope alleles are primarily a risk factor for anti-cyclic citrullinated peptide antibodies and are not an independent risk factor for development of rheumatoid arthritis. Arthritis Rheum 2006, 54:1117-1121.
38. Senshu T., Akiyama K., Nagata S., Watanabe K., Hikichi K. Peptidylarginine deiminase in rat pituitary: sex difference, estrous cycle-related changes, and estrogen dependence. Endocrinology 1989, 124:2666-2670.
39. Mowen M.A., Schurter B.T., Fathman J.W., David M., Glincher L.H. Arginine methylation of NIP45 modulates cytokine gene expression in effector T lymphocytes. Mol Cell 2004, 15:559-571.