DRB1*0402 may influence arthritis by promoting naive CD4+ T-cell differentiation in to regulatory T cells

European Journal of Immunology

Volumn 44, Issue 11, 2014, Pages 3429-3438

  Luckey, David ^a   Behrens, Marshall ^a   Smart, Michele ^a   Luthra, Harvinder ^b   David, Chella S ^a   Taneja, Veena ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Humanized mice; Immune dysregulation; Regulatory T cells; Rheumatoid arthritis; T cell polarization

Indexed keywords

HLA DRB1 ANTIGEN; HLA-DRB1*04:01 ANTIGEN; HLA-DRB1*04:02 ANTIGEN; INTERLEUKIN 17; LIPOPOLYSACCHARIDE;

ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; EXPERIMENTAL ARTHRITIS; FEMALE; GENETICS; IMMUNOLOGY; INFLAMMATION; MALE; MOUSE; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; TH1 CELL; TH17 CELL; TH2 CELL; TRANSGENIC MOUSE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; HLA-DRB1 CHAINS; INFLAMMATION; INTERLEUKIN-17; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, TRANSGENIC; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH17 CELLS; TH2 CELLS;

EID: 84916889594     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344424     Document Type: Article

References (36)

1. Wordsworth, B. P., Lanchbury, J. S., Sakkas, L. I., Welsh, K. I., Panayi, G. S. and Bell, J. I., HLA-DR4 subtype frequencies in rheumatoid arthritis indicate that DRB1 is the major susceptibility locus within the HLA class II region. Proc. Natl. Acad. Sci. USA 1989. 86: 10049-10053.
2. Stastny, P., Association of the B-cell alloantigen DRw4 with rheumatoid arthritis. N. Engl. J. Med. 1978. 298: 869-871.
3. Gregersen, P. K., Shen, M., Song, Q. L., Merryman, P., Degar, S., Seki, T., Maccari, J. et al., Molecular diversity of HLA-DR4 haplotypes. Proc. Natl. Acad. Sci. USA 1986. 83: 2642-2646.
4. Gregersen, P. K., Silver, J. and Winchester, R. J., The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987. 30: 1205-1213.
5. Moller, E., Bohme, J., Valugerdi, M. A., Ridderstad, A. and Olerup, O., Speculations on mechanisms of HLA associations with autoimmune diseases and the specificity of "autoreactive" T lymphocytes. Immunol. Rev. 1990. 118: 5-19.
6. Taneja, V., Taneja, N., Behrens, M., Pan, S., Trejo, T., Griffiths, M., Luthra, H. et al., HLA-DRB1*0402 (DW10) transgene protects collagen-induced arthritis-susceptible H2Aq and DRB1*0401 (DW4) transgenic mice from arthritis. J. Immunol. 2003. 171: 4431-4438.
7. Snijders, A., Elferink, D. G., Geluk, A., van Der Zanden, A. L., Vos, K., Schreuder, G. M., Breedveld, F. C. et al., An HLA-DRB1-derived peptide associated with protection against rheumatoid arthritis is naturally processed by human APCs. J. Immunol. 2001. 166: 4987-4993.
8. Kirschmann, D. A., Duffin, K. L., Smith, C. E., Welply, J. K., Howard, S. C., Schwartz, B. D. and Woulfe, S. L., Naturally processed peptides from rheumatoid arthritis associated and non-associated HLA-DR alleles. J. Immunol. 1995. 155: 5655-5662.
9. Taneja, V., Behrens, M., Mangalam, A., Griffiths, M. M., Luthra, H. S. and David, C. S., New humanized HLA-DR4-transgenic mice that mimic the sex bias of rheumatoid arthritis. Arthritis Rheum. 2007. 56: 69-78.
10. Taneja, V., Behrens, M., Basal, E., Sparks, J., Griffiths, M. M., Luthra, H. and David, C. S., Delineating the role of the HLA-DR4 "shared epitope" in susceptibility versus resistance to develop arthritis. J. Immunol. 2008. 181: 2863-2877.
11. Nurieva, R., Yang, X. O., Chung, Y. and Dong, C., Cutting edge: in vitro generated Th17 cells maintain their cytokine expression program in normal but not lymphopenic hosts. J. Immunol. 2009. 182: 2565-2568.
12. Diab, B. Y., Lambert, N. C., L'Faqihi, F. E., Loubet-Lescoulie, P., de Preval, C. and Coppin, H., Human collagen II peptide 256-271 preferentially binds to HLA-DR molecules associated with susceptibility to rheumatoid arthritis. Immunogenetics 1999. 49: 36-44.
13. Behrens, M., Trejo, T., Luthra, H., Griffiths, M., David, C. S. and Taneja, V., Mechanism by which HLA-DR4 regulates sex-bias of arthritis in humanized mice. J. Autoimmun. 2010. 35: 1-9.
14. Taneja, V., Griffiths, M. M., Luthra, H. and David, C. S., Modulation of HLA-DQ-restricted collagen-induced arthritis by HLA-DRB1 polymorphism. Int. Immunol. 1998. 10: 1449-1457.
15. Chen, J., Li, J., Gao, H., Wang, C., Luo, J., Lv, Z. and Li, X., Comprehensive evaluation of different T-helper cell subsets differentiation and function in rheumatoid arthritis. J. Biomed. Biotechnol. 2012. 2012: 535361.
16. Maini, R., St Clair, E. W., Breedveld, F., Furst, D., Kalden, J., Weisman, M., Smolen, J. et al., Infliximab (chimeric anti-tumour necrosis factor alpha monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: a randomised phase III trial. ATTRACT Study Group. Lancet 1999. 354: 1932-1939.
17. Hummelshoj, L., Ryder, L. P. and Poulsen, L. K., The role of the interleukin-10 subfamily members in immunoglobulin production by human B cells. Scand. J. Immunol. 2006. 64: 40-47.
18. Rosloniec, E. F., Brand, D. D., Myers, L. K., Esaki, Y., Whittington, K. B., Zaller, D. M., Woods, A. 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: 2573-2578.
19. Mangalam, A. K., Taneja, V. and David, C. S., HLA class II molecules influence susceptibility versus protection in inflammatory diseases by determining the cytokine profile. J. Immunol. 2013. 190: 513-518.
20. Liu, X., Zhan, Z., Li, D., Xu, L., Ma, F., Zhang, P., Yao, H. et al., Intracellular MHC class II molecules promote TLR-triggered innate immune responses by maintaining activation of the kinase Btk. Nat. Immunol. 2011. 12: 416-424.
21. Gomez, A., Luckey, D., Yeoman, C. J., Marietta, E. V., Berg Miller, M. E., Murray, J. A., White, B. A. et al., Loss of sex and age driven differences in the gut microbiome characterize arthritis-susceptible 0401 mice but not arthritis-resistant 0402 mice. PloS One 2012. 7: e36095.
22. Cua, D. J. and Tato, C. M., Innate IL-17-producing cells: the sentinels of the immune system Nat. Rev. Immunol. 2010. 10: 479-489.
23. van den Berg, W. B. and Miossec, P., IL-17 as a future therapeutic target for rheumatoid arthritis Nat. Rev. Rheumatol. 2009. 5: 549-553.
24. Patel, D. D., Lee, D. M., Kolbinger, F. and Antoni, C., Effect of IL-17A blockade with secukinumab in autoimmune diseases. Annal. Rheumatic Dis. 2013. 72 (Suppl 2): iii116-iii123.
25. Minty, A., Chalon, P., Derocq, J. M., Dumont, X., Guillemot, J. C., Kaghad, M., Labit, C. et al., Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature 1993. 362: 248-250.
26. Defrance, T., Carayon, P., Billian, G., Guillemot, J. C., Minty, A., Caput, D. and Ferrara, P., Interleukin 13 is a B cell stimulating factor. J. Exp. Med. 1994. 179: 135-143.
27. Behrens, M., Smart, M., Luckey, D., Luthra, H. and Taneja, V., To B or not to B: role of B cells in pathogenesis of arthritis in HLA transgenic mice. J. Autoimmun. 2011. 37: 95-103.
28. Taneja, V., Krco, C. J., Behrens, M. D., Luthra, H. S., Griffiths, M. M. and 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.
29. Luckey, D., Medina, K. and Taneja, V., B cells as effectors and regulators of sex-biased arthritis. Autoimmunity 2012. 45: 364-376.
30. Tokayer, A., Carsons, S. E., Chokshi, B. and Santiago-Schwarz, F., High levels of interleukin 13 in rheumatoid arthritis sera are modulated by tumor necrosis factor antagonist therapy: association with dendritic cell growth activity. J. Rheumatol. 2002. 29: 454-461.
31. Elyaman, W., Bradshaw, E. M., Uyttenhove, C., Dardalhon, V., Awasthi, A., Imitola, J., Bettelli, E. et al., IL-9 induces differentiation of TH17 cells and enhances function of FoxP3+ natural regulatory T-cells. Proc. Natl. Acad. Sci. USA 2009. 106: 12885-12890.
32. Cornish, A. L., Campbell, I. K., McKenzie, B. S., Chatfield, S. and Wicks, I. P., G-CSF and GM-CSF as therapeutic targets in rheumatoid arthritis. Nat. Rev. Rheumatol. 2009. 5: 554-559.
33. Hsu, Y. H., Hsieh, M. S., Liang, Y. C., Li, C. Y., Sheu, M. T., Chou, D. T., Chen, T. F. et al., Production of the chemokine eotaxin-1 in osteoarthritis and its role in cartilage degradation. J. Cell. Biochem. 2004. 93: 929-939.
34. Page, C. E., Smale, S., Carty, S. M., Amos, N., Lauder, S. N., Goodfellow, R. M., Richards, P. J. et al., Interferon-gamma inhibits interleukin-1beta-induced matrix metalloproteinase production by synovial fibroblasts and protects articular cartilage in early arthritis. Arthritis Res. Ther. 2010. 12: R49.
35. Pan, S., Trejo, T., Hansen, J., Smart, M. and David, C. S., HLA-DR4 (DRB1*0401) transgenic mice expressing an altered CD4-binding site: specificity and magnitude of DR4-restricted T-cell response. J. Immunol. 1998. 161: 2925-2929.
36. Kouskoff, V., Fehling, H. J., Lemeur, M., Benoist, C. and Mathis, D., A vector driving the expression of foreign cDNAs in the MHC class II-positive cells of transgenic mice. J. Immunol. Methods 1993. 166: 287-291.