Positional identification of RT1-B (HLA-DQ) as susceptibility locus for autoimmune arthritis

Journal of Immunology

Volumn 194, Issue 6, 2015, Pages 2539-2550

  Haag, Sabrina ^a   Tuncel, Jonatan ^a   Thordardottir, Soley ^a   Mason, Daniel E ^b   Yau, Anthony C Y ^a   Dobritzsch, Doreen ^a,c   Bäcklund, Johan ^a   Peters, Eric C ^b   Holmdahl, Rikard ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Genomics Institute   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HLA DQ ANTIGEN; HLA DQA1 ANTIGEN; HLA DQB1 ANTIGEN; HLA DR ANTIGEN; INTERLEUKIN 6; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 14 4 4S; MONOCLONAL ANTIBODY OX17; MONOCLONAL ANTIBODY OX6; PRISTANE; TUBERIN; UNCLASSIFIED DRUG; AMINO ACID; BLOCKING ANTIBODY; HISTOCOMPATIBILITY ANTIGEN; HISTOCOMPATIBILITY ANTIGENS RT, RAT; TERPENE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; CONGENIC STRAIN; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE EXACERBATION; DISEASE SEVERITY; DRUG BINDING SITE; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG RESPONSE; DRUG TARGETING; GENE; GENE LOCUS; GENETIC CORRELATION; GENETIC POLYMORPHISM; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; ORTHOLOGY; PEPTIDE ANALYSIS; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; QUANTITATIVE TRAIT LOCUS; RAT; RHEUMATOID ARTHRITIS; RT1 B GENE; RT1 BA GENE; RT1 BB GENE; RT1 D GENE; STRUCTURAL HOMOLOGY; T LYMPHOCYTE ACTIVATION; TCS2 GENE; ANIMAL; BINDING SITE; BODY WEIGHT; CHEMICAL STRUCTURE; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL ARTHRITIS; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; HAPLOTYPE; HUMAN; IMMUNOLOGY; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEVERITY OF ILLNESS INDEX;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; ANTIBODIES, BLOCKING; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; BINDING SITES; BODY WEIGHT; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HAPLOTYPES; HISTOCOMPATIBILITY ANTIGENS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; PROTEIN STRUCTURE, TERTIARY; RATS; SEVERITY OF ILLNESS INDEX; TERPENES;

EID: 84924561306     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402238     Document Type: Article

References (53)

1. Gregersen, P. K., J. Silver, and R. J. Winchester. 1987. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 30: 1205-1213.
2. Raychaudhuri, S., C. Sandor, E. A. Stahl, J. Freudenberg, H.-S. Lee, X. Jia, L. Alfredsson, L. Padyukov, L. Klareskog, J. Worthington, et al. 2012. Five amino acids in three HLA proteins explain most of the association between MHC and seropositive rheumatoid arthritis. Nat. Genet. 44: 291-296.
3. Bossini-Castillo, L., C. de Kovel, H. Kallberg, R. van 't Slot, A. Italiaander, M. Coenen, P. P. Tak, M. D. Posthumus, C. Wijmenga, T. Huizinga, et al. 2014. A genome-wide association study of rheumatoid arthritis without antibodies against citrullinated peptides. Ann. Rheum. Dis. DOI: 10.1136/annrheumdis-2013-204591.
4. Han, B., D. Diogo, S. Eyre, H. Källberg, A. Zhernakova, J. Bowes, L. Padyukov, Y. Okada, M. A. González-Gay, S. Rantapää-Dahlqvist, et al. 2014. Fine mapping seronegative and seropositive rheumatoid arthritis to shared and distinct HLA alleles by adjusting for the effects of heterogeneity. Am. J. Hum. Genet. 94: 522-532.
5. Firestein, G. S. 2003. Evolving concepts of rheumatoid arthritis. Nature 423: 356-361.
6. Kobezda, T., S. Ghassemi-Nejad, K. Mikecz, T. T. Glant, and Z. Szekanecz. 2014. Of mice and men: how animal models advance our understanding of T-cell function in RA. Nat Rev Rheumatol 10: 160-170.
7. Jenkins, R. N., A. Nikaein, A. Zimmermann, K. Meek, and P. E. Lipsky. 1993. T cell receptor V beta gene bias in rheumatoid arthritis. J. Clin. Invest. 92: 2688-2701.
8. Struyk, L., J. T. Kurnick, G. E. Hawes, J. M. van Laar, R. Schipper, J. R. Oksenberg, L. Steinman, R. R. de Vries, F. C. Breedveld, and P. van den Elsen. 1993. T-cell receptor V-gene usage in synovial fluid lymphocytes of patients with chronic arthritis. Hum. Immunol. 37: 237-251.
9. Bäcklund, J., A. Treschow, R. Bockermann, B. Holm, L. Holm, S. Issazadeh-Navikas, J. Kihlberg, and R. Holmdahl. 2002. Glycosylation of type II collagen is of major importance for T cell tolerance and pathology in collagen-induced arthritis. Eur. J. Immunol. 32: 3776-3784.
10. Matsumoto, I., A. Staub, C. Benoist, and D. Mathis. 1999. Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme. Science 286: 1732-1735.
11. Holmberg, J., J. Tuncel, H. Yamada, S. Lu, P. Olofsson, and R. Holmdahl. 2006. Pristane, a non-antigenic adjuvant, induces MHC class II-restricted, arthritogenic T cells in the rat. J. Immunol. 176: 1172-1179.
12. Tuncel, J., S. Haag, S. Carlsén, A. C. Y. Yau, S. Lu, H. Burkhardt, and R. Holmdahl. 2012. Class II major histocompatibility complex-associated response to type XI collagen regulates the development of chronic arthritis in rats. Arthritis Rheum. 64: 2537-2547.
13. Vingsbo, C., P. Sahlstrand, J. G. Brun, R. Jonsson, T. Saxne, and R. Holmdahl. 1996. Pristane-induced arthritis in rats: a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. Am. J. Pathol. 149: 1675-1683.
14. Rintisch, C., M. Förster, and R. Holmdahl. 2009. Detection of arthritissusceptibility loci, including Ncf1, and variable effects of the major histocompatibility complex region depending on genetic background in rats. Arthritis Rheum. 60: 419-427.
15. Olofsson, P., N. Nordquist, C. Vingsbo-Lundberg, A. Larsson, C. Falkenberg, U. Pettersson, B. Akerström, and R. Holmdahl. 2002. Genetic links between the acute-phase response and arthritis development in rats. Arthritis Rheum. 46: 259-268.
16. Hoffmann, M. H., K. Skriner, S. Herman, C. Baumann, C.-W. Steiner, C. Ospelt, B. Meyer, A. Gleiss, J. Pfatschbacher, B. Niederreiter, et al. 2011. Nucleic acidstimulated antigen-presenting cells trigger T cells to induce disease in a rat transfer model of inflammatory arthritis. J. Autoimmun. 36: 288-300.
17. Olofsson, P., J. Holmberg, U. Pettersson, and R. Holmdahl. 2003. Identification and isolation of dominant susceptibility loci for pristane-induced arthritis. J. Immunol. 171: 407-416.
18. Björk, J., S. Kleinau, T. Midtvedt, L. Klareskog, and G. Smedegard. 1994. Role of the bowel flora for development of immunity to hsp 65 and arthritis in three experimental models. Scand. J. Immunol. 40: 648-652.
19. Tuncel, J., S. Haag, A. C. Y. Yau, U. Norin, A. Baud, E. Lönnblom, K. Maratou, A. J. Ytterberg, D. Ekman, S. Thordardottir, et al. 2014. Natural polymorphisms in Tap2 influence negative selection and CD4:CD8 lineage commitment in the rat. PLoS Genet. 10: e1004151.
20. Nicklas, W. 2010. FELASA guidelines for the accreditation of health monitoring programmes and for testing laboratories involved in health monitoring. Lab. Anim. 44: 69.
21. Mikulowska, A., M. Vestberg, U. Brunsberg, A. S. Hansson, M. Sunduall, L. Jansson, and U. Pettersson. 1997. Genetic analysis of mouse models for rheumatoid arthritis. In Human Genome Methods 215. K. W. Adolph, ed. CRC Press, New York, p. 215-238.
22. Batsalova, T., B. Dzhambazov, P. Merky, A. Bäcklund, and J. Bäcklund. 2010. Breaking T cell tolerance against self type II collagen in HLA-DR4-transgenic mice and development of autoimmune arthritis. Arthritis Rheum. 62: 1911-1920.
23. Bäcklund, J., C. Li, E. Jansson, S. Carlsen, P. Merky, K. S. Nandakumar, S. Haag, J. Ytterberg, R. A. Zubarev, and R. Holmdahl. 2013. C57BL/6 mice need MHC class II Aq to develop collagen-induced arthritis dependent on autoreactive T cells. Ann. Rheum. Dis. 72: 1225-1232.
24. Fissolo, N., S. Haag, K. L. de Graaf, O. Drews, S. Stevanovic, H. G. Rammensee, and R. Weissert. 2009. Naturally presented peptides on major histocompatibility complex I and II molecules eluted from central nervous system of multiple sclerosis patients. Mol. Cell. Proteomics 8: 2090-2101.
25. Emsley, P., B. Lohkamp, W. G. Scott, and K. Cowtan. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66: 486-501.
26. Powis, S. J., J. C. Howard, and G. W. Butcher. 1991. The major histocompatibility complex class II-linked cim locus controls the kinetics of intracellular transport of a classical class I molecule. J. Exp. Med. 173: 913-921.
27. Powis, S. J., E. V. Deverson, W. J. Coadwell, A. Ciruela, N. S. Huskisson, H. Smith, G. W. Butcher, and J. C. Howard. 1992. Effect of polymorphism of an MHC-linked transporter on the peptides assembled in a class I molecule. Nature 357: 211-215.
28. Nielsen, M., C. Lundegaard, P. Worning, C. S. Hvid, K. Lamberth, S. Buus, S. Brunak, and O. Lund. 2004. Improved prediction of MHC class I and class II epitopes using a novel Gibbs sampling approach. Bioinformatics 20: 1388-1397.
29. Chaves, F. A., K. A. Richards, A. Torelli, J. Wedekind, and A. J. Sant. 2006. Peptide-binding motifs for the I-Ad MHC class II molecule: alternate pHdependent binding behavior. Biochemistry 45: 6426-6433.
30. Traherne, J. A., R. Horton, A. N. Roberts, M. M. Miretti, M. E. Hurles, C. A. Stewart, J. L. Ashurst, A. M. Atrazhev, P. Coggill, S. Palmer, et al. 2006. Genetic analysis of completely sequenced disease-associated MHC haplotypes identifies shuffling of segments in recent human history. PLoS Genet. 2: e9.
31. Livingstone, A. M., S. J. Powis, E. Günther, D. V. Cramer, J. C. Howard, and G. W. Butcher. 1991. Cim: an MHC class II-linked allelism affecting the antigenicity of a classical class I molecule for T lymphocytes. Immunogenetics 34: 157-163.
32. Joly, E., E. V. Deverson, J. W. Coadwell, E. Günther, J. C. Howard, and G. W. Butcher. 1994. The distribution of Tap2 alleles among laboratory rat RT1 haplotypes. Immunogenetics 40: 45-53.
33. Xystrakis, E., A. S. Dejean, I. Bernard, P. Druet, R. Liblau, D. Gonzalez-Dunia, and A. Saoudi. 2004. Identification of a novel natural regulatory CD8 T-cell subset and analysis of its mechanism of regulation. Blood 104: 3294-3301.
34. Guillonneau, C., M. Hill, F.-X. Hubert, E. Chiffoleau, C. Hervé, X.-L. Li, M. Heslan, C. Usal, L. Tesson, S. Ménoret, et al. 2007. CD40Ig treatment results in allograft acceptance mediated by CD8CD45RC T cells, IFN-g, and indoleamine 2,3-dioxygenase. J. Clin. Invest. 117: 1096-1106.
35. Leavenworth, J. W., X. Tang, H.-J. Kim, X. Wang, and H. Cantor. 2013. Amelioration of arthritis through mobilization of peptide-specific CD8+ regulatory T cells. J. Clin. Invest. 123: 1382-1389.
36. Baumgart, M., V. Moos, D. Schuhbauer, and B. Müller. 1998. Differential expression of major histocompatibility complex class II genes on murine macrophages associated with T cell cytokine profile and protective/suppressive effects. Proc. Natl. Acad. Sci. USA 95: 6936-6940.
37. Swanberg, M., O. Lidman, L. Padyukov, P. Eriksson, E. Akesson, M. Jagodic, A. Lobell, M. Khademi, O. Börjesson, C. M. Lindgren, et al. 2005. MHC2TA is associated with differential MHC molecule expression and susceptibility to rheumatoid arthritis, multiple sclerosis and myocardial infarction. Nat. Genet. 37: 486-494.
38. Lee, H.-S., B. D. Korman, J.M. Le, D. L. Kastner, E. F. Remmers, P. K. Gregersen, and S.-C. Bae. 2009. Genetic risk factors for rheumatoid arthritis differ in Caucasian and Korean populations. Arthritis Rheum. 60: 364-371.
39. Kelley, J. M., L. B. Hughes, A. Malik, M. I. Danila, Y. Edberg, G. S. Alarcón, D. L. Conn, B. L. Jonas, L. F. Callahan, E. A. Smith, et al. 2010. Genetic variants of STAT4 associated with rheumatoid arthritis in persons of Asian and European ancestry do not replicate in African Americans. Ann. Rheum. Dis. 69: 625-626.
40. Reske, K., U. Möhle, D. Sun, and H. Wekerle. 1987. Synthesis and cell surface display of class II determinants by long-term propagated rat T line cells. Eur. J. Immunol. 17: 909-914.
41. Kamradt, T., and O. Frey. 2010. Arthritis: where are the T cells? Arthritis Res. Ther. 12: 122.
42. Hoffmann, M. H., J. Tuncel, K. Skriner, M. Tohidast-Akrad, B. Türk, S. Pinol-Roma, G. Serre, G. Schett, J. S. Smolen, R. Holmdahl, and G. Steiner. 2007. The rheumatoid arthritis-associated autoantigen hnRNP-A2 (RA33) is a major stimulator of autoimmunity in rats with pristane-induced arthritis. J. Immunol. 179: 7568-7576.
43. Denzin, L. K., and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II ab dimers and facilitates peptide loading. Cell 82: 155-165.
44. Martin, W. D., G. G. Hicks, S. K. Mendiratta, H. I. Leva, H. E. Ruley, and L. Van Kaer. 1996. H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation, and T cell repertoire selection. Cell 84: 543-550.
45. Riberdy, J. M., J. R. Newcomb, M. J. Surman, J. A. Barbosa, and P. Cresswell. 1992. HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 360: 474-477.
46. Fallang, L.-E., S. Roh, A. Holm, E. Bergseng, T. Yoon, B. Fleckenstein, A. Bandyopadhyay, E. D. Mellins, and L. M. Sollid. 2008. Complexes of two cohorts of CLIP peptides and HLA-DQ2 of the autoimmune DR3-DQ2 haplotype are poor substrates for HLA-DM. J. Immunol. 181: 5451-5461.
47. Pos, W., D. K. Sethi, M. J. Call, M.-S. E. D. Schulze, A.-K. Anders, J. Pyrdol, and K. W. Wucherpfennig. 2012. Crystal structure of the HLA-DM-HLA-DR1 complex defines mechanisms for rapid peptide selection. Cell 151: 1557-1568.
48. van Lith, M., R. M. McEwen-Smith, and A. M. Benham. 2010. HLA-DP, HLADQ, and HLA-DR have different requirements for invariant chain and HLA-DM. J. Biol. Chem. 285: 40800-40808.
49. Cucca, F., R. Lampis, M. Congia, E. Angius, S. Nutland, S. C. Bain, A. H. Barnett, and J. A. Todd. 2001. A correlation between the relative predisposition of MHC class II alleles to type 1 diabetes and the structure of their proteins. Hum. Mol. Genet. 10: 2025-2037.
50. Busch, R., A. De Riva, A. V. Hadjinicolaou, W. Jiang, T. Hou, and E. D. Mellins. 2012. On the perils of poor editing: regulation of peptide loading by HLA-DQ and H2-A molecules associated with celiac disease and type 1 diabetes. Expert Rev. Mol. Med. 14: e15.
51. Suri, A., J. J. Walters, O. Kanagawa, M. L. Gross, and E. R. Unanue. 2003. Specificity of peptide selection by antigen-presenting cells homozygous or heterozygous for expression of class II MHC molecules: The lack of competition. Proc. Natl. Acad. Sci. USA 100: 5330-5335.
52. Pos, W., D. K. Sethi, and K. W. Wucherpfennig. 2013. Mechanisms of peptide repertoire selection by HLA-DM. Trends Immunol. 34: 495-501.
53. Mellins, E. D., and L. J. Stern. 2014. HLA-DM and HLA-DO, key regulators of MHC-II processing and presentation. Curr. Opin. Immunol. 26: 115-122.