Risk for ACPA-positive rheumatoid arthritis is driven by shared HLA amino acid polymorphisms in Asian and European populations

Human Molecular Genetics

Volumn 23, Issue 25, 2014, Pages 6916-6926

  Okada, Yukinori ^a,b,c,d   Kim, Kwangwoo ^c,d,e   Han, Buhm ^c,d   Pillai, Nisha E ^f   Ong, Rick T H ^f   Saw, Woei Yuh ^f   Luo, Ma ^g,h   Jiang, Lei ⁱ   Yin, Jian ⁱ   Bang, So Young ^e   Lee, Hye Soon ^e   Brown, Matthew A ^j   Bae, Sang Cheol ^e   Xu, Huji ⁱ   Teo, Yik Ying ^f,k   De Bakker, Paul I W ^l   Raychaudhuri, Soumya ^c,d,m  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b Institute of Physical and Chemical Research   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e Hanyang University Hospital for Rheumatic Diseases   (South Korea)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^g UNIVERSITY OF MANITOBA   (Canada)

^h PUBLIC HEALTH AGENCY OF CANADA   (Canada)

ⁱ SECOND MILITARY MEDICAL UNIVERSITY   (China)

^j UNIVERSITY OF QUEENSLAND   (Australia)

^k GENOME INSTITUTE OF SINGAPORE   (Singapore)

^l UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^m UNIVERSITY OF MANCHESTER   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AUTOANTIBODY; CITRULLINE; EPITOPE; HLA B ANTIGEN; HLA DP ANTIGEN; HLA DRB1 ANTIGEN; HLA-DPB1 ANTIGEN;

ALLELE; ASIAN CONTINENTAL ANCESTRY GROUP; BIOSYNTHESIS; CAUCASIAN; CHEMISTRY; CHROMOSOMAL MAPPING; ETHNOLOGY; GENE EXPRESSION; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETICS; HUMAN; IMMUNOLOGY; PATHOLOGY; RHEUMATOID ARTHRITIS; RISK;

ALLELES; AMINO ACIDS; ARTHRITIS, RHEUMATOID; ASIAN CONTINENTAL ANCESTRY GROUP; AUTOANTIBODIES; CHROMOSOME MAPPING; CITRULLINE; EPITOPES; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENE EXPRESSION; GENE FREQUENCY; HLA-B ANTIGENS; HLA-DP BETA-CHAINS; HLA-DRB1 CHAINS; HUMANS; POLYMORPHISM, GENETIC; RISK;

EID: 84911495256     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu387     Document Type: Article

References (36)

1. Gabriel, S.E. (2001) The epidemiology of rheumatoid arthritis. Rheum. Dis. Clin. North. Am., 27, 269 – 281.
2. Neogi, T., Aletaha, D., Silman, A.J., Naden, R.L., Felson, D.T., Aggarwal, R., Bingham, C.O. III, Birnbaum, N.S., Burmester, G.R., Bykerk, V.P. et al. (2010) The 2010 American College of Rheumatology/European League Against Rheumatism classification criteria for rheumatoid arthritis: Phase 2 methodological report. Arthritis Rheum., 62, 2582 – 2591.
3. Stahl, E.A., Wegmann, D., Trynka, G., Gutierrez-Achury, J., Do, R., Voight, B.F., Kraft, P., Chen, R., Kallberg, H.J., Kurreeman, F.A. et al. (2012) Bayesian inference analyses of the polygenic architecture of rheumatoid arthritis. Nat. Genet., 44, 483 – 489.
4. van der Woude, D., Houwing-Duistermaat, J.J., Toes, R.E., Huizinga, T.W., Thomson, W., Worthington, J., van der Helm-van Mil, A.H. and de Vries, R.R. (2009) Quantitative heritability of anti-citrullinated protein antibody-positive and anti-citrullinated protein antibody-negative rheumatoid arthritis. Arthritis Rheum., 60, 916 – 923.
5. Ding, B., Padyukov, L., Lundstrom, E., Seielstad, M., Plenge, R.M., Oksenberg, J.R., Gregersen, P.K., Alfredsson, L. and Klareskog, L. (2009) Different patterns of associations with anti-citrullinated protein antibody-positive and anti-citrullinated protein antibody-negative rheumatoid arthritis in the extended major histocompatibility complex region. Arthritis Rheum., 60, 30–38.
6. Gregersen, P.K., Silver, J. and Winchester, R.J. (1987) The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum., 30, 1205–1213.
7. Okada, Y., Yamada, R., Suzuki, A., Kochi, Y., Shimane, K., Myouzen, K., Kubo, M., Nakamura, Y. and Yamamoto, K. (2009) Contribution of a haplotype in the HLA region to anti-cyclic citrullinated peptide antibody positivity in rheumatoid arthritis, independently of HLA-DRB1. Arthritis Rheum., 60, 3582–3590.
8. Kazkaz, L., Marotte, H., Hamwi, M., Angelique Cazalis, M., Roy, P., Mougin, B. and Miossec, P. (2007) Rheumatoid arthritis and genetic markers in Syrian and French populations: different effect of the shared epitope. Ann. Rheum. Dis., 66, 195 – 201.
9. Hughes, L.B., Morrison, D., Kelley, J.M., Padilla, M.A., Vaughan, L.K., Westfall, A.O., Dwivedi, H., Mikuls, T.R., Holers, V.M., Parrish, L.A. et al. (2008) The HLA-DRB1 shared epitope is associated with susceptibility to rheumatoid arthritis in African Americans through European genetic admixture. Arthritis Rheum., 58, 349 – 358.
10. Kochi, Y., Yamada, R., Kobayashi, K., Takahashi, A., Suzuki, A., Sekine, A., Mabuchi, A., Akiyama, F., Tsunoda, T., Nakamura, Y. et al. (2004) Analysis of single-nucleotide polymorphisms in Japanese rheumatoid arthritis patients shows additional susceptibility markers besides the classic shared epitope susceptibility sequences. Arthritis Rheum., 50, 63–71.
11. ∗0901. Arthritis Rheum., 50, 3468 – 3475.
12. Raychaudhuri, S., Sandor, C., Stahl, E.A., Freudenberg, J., Lee, H.S., Jia, X., Alfredsson, L., Padyukov, L., Klareskog, L., Worthington, J. 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.
13. Pillai, N.E., Okada, Y., Ong, R.T., Wang, X., Tantoso, E., Xu, W., Peterson, T.A., Belawney, T., Ali, M., Poh, W. et al. (2014) Predicting HLA alleles from high-resolution SNP data in three Southeast Asian populations. Hum. Mol. Genet. doi: 10.1093/hmg/ddu149.
14. de Bakker, P.I.W., McVean, G., Sabeti, P.C., Miretti, M.M., Green, T., Marchini, J., Ke, X., Monsuur, A.J., Whittaker, P., Delgado, M. et al. (2006) A high-resolution HLA and SNP haplotype map for disease association studies in the extended human MHC. Nat. Genet., 38, 1166 – 1172.
15. The International HIV Controllers Study. (2010) The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science, 330, 1551–1557.
16. Jia, X., Han, B., Onengut-Gumuscu, S., Chen, W.M., Concannon, P.J., Rich, S.S., Raychaudhuri, S. and de Bakker, P.I.W. (2013) Imputing amino acid polymorphisms in human leukocyte antigens. PLoS ONE, 8, e64683.
17. Rich, S.S., Concannon, P., Erlich, H., Julier, C., Morahan, G., Nerup, J., Pociot, F. and Todd, J.A. (2006) The Type 1 Diabetes Genetics Consortium. Ann. N. Y. Acad. Sci., 1079, 1 – 8.
18. Jiang, L., Yin, J., Ye, L., Yang, J., Hemani, G., Liu, A.J., Zou, H., He, D., Sun, L., Zeng, X. et al. (2014) Novel risk loci for rheumatoid arthritis in han chinese and congruence with risk variants in europeans. Arthritis Rheum. doi: 10.1002/art.38353.
19. Freudenberg, J., Lee, H.S., Han, B.G., Shin, H.D., Kang, Y.M., Sung, Y.K., Shim, S.C., Choi, C.B., Lee, A.T., Gregersen, P.K. et al. (2011) Genome-wide association study of rheumatoid arthritis in Koreans: population-specific loci as well as overlap with European susceptibility loci. Arthritis Rheum., 63, 884 – 893.
20. Kim, K., Bang, S., Lee, H., Cho, S., Choi, C., Sung, Y., Kim, T., Jun, J., Yoo, D., Kang, Y. et al. (2014) High-density genotyping of immune loci in Koreans and Europeans identifies 8 new rheumatoid arthritis risk loci. Ann. Rheum. Dis. doi: 10.1136/annrheumdis.
21. Gunther, S., Schlundt, A., Sticht, J., Roske, Y., Heinemann, U., Wiesmuller, K.H., Jung, G., Falk, K., Rotzschke, O. and Freund, C. (2010) Bidirectional binding of invariant chain peptides to an MHC class II molecule. Proc. Natl. Acad. Sci. USA, 107, 22219 – 22224.
22. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera – a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605 – 1612.
23. Nepom, B.S., Nepom, G.T., Coleman, M. and Kwok, W.W. (1996) Critical contribution of beta chain residue 57 in peptide binding ability of both HLA-DR and -DQ molecules. Proc. Natl. Acad. Sci. USA, 93, 7202–7206.
24. ∗0901 lowers anti-cyclic citrullinated peptide antibody levels in Japanese patients with rheumatoid arthritis. Ann. Rheum. Dis., 69, 1569–1570.
25. Kallberg, H., Padyukov, L., Plenge, R.M., Ronnelid, J., Gregersen, P.K., van der Helm-van Mil, A.H., Toes, R.E., Huizinga, T.W., Klareskog, L. and Alfredsson, L. (2007) Gene-gene and gene-environment interactions involving HLA-DRB1, PTPN22, and smoking in two subsets of rheumatoid arthritis. Am. J. Hum. Genet., 80, 867 – 875.
26. Aguillon, J.C., Cruzat, A., Aravena, O., Salazar, L., Llanos, C. and Cuchacovich, M. (2006) Could single-nucleotide polymorphisms (SNPs) affecting the tumour necrosis factor promoter be considered as part of rheumatoid arthritis evolution? Immunobiology, 211, 75–84.
27. Kirsten, H., Petit-Teixeira, E., Scholz, M., Hasenclever, D., Hantmann, H., Heider, D., Wagner, U., Sack, U., Hugo Teixeira, V., Prum, B. et al. (2009) Association of MICA with rheumatoid arthritis independent of known HLA-DRB1 risk alleles in a family-based and a case control study. Arthritis. Res. Ther., 11, R60.
28. Lopez-Arbesu, R., Ballina-Garcia, F.J., Alperi-Lopez, M., Lopez-Soto, A., Rodriguez-Rodero, S., Martinez-Borra, J., Lopez-Vazquez, A., Fernandez-Morera, J.L., Riestra-Noriega, J.L., Queiro-Silva, R. et al. (2007) MHC class I chain-related gene B (MICB) is associated with rheumatoid arthritis susceptibility. Rheumatology (Oxford), 46, 426 – 430.
29. Vignal, C., Bansal, A.T., Balding, D.J., Binks, M.H., Dickson, M.C., Montgomery, D.S. and Wilson, A.G. (2008) Genetic association of the major histocompatibility complex with rheumatoid arthritis implicates two non-DRB1 loci. Arthritis Rheum., 60, 53 – 62.
30. Arnett, F.C., Edworthy, S.M., Bloch, D.A., McShane, D.J., Fries, J.F., Cooper, N.S., Healey, L.A., Kaplan, S.R., Liang, M.H., Luthra, H.S. et al. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum., 31, 315 – 324.
31. Okada, Y., Wu, D., Trynka, G., Raj, T., Terao, C., Ikari, K., Kochi, Y., Ohmura, K., Suzuki, A., Yoshida, S. et al. (2014) Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature, 506, 376–381.
32. The International HapMap, Consortium. (2003) The international HapMap project. Nature, 426, 789–796.
33. ∗1502 haplotype increases risk for ulcerative colitis but reduces risk for Crohn’s disease. Gastroenterology, 141, 864 – 871.
34. Kurreeman, F.A., Liao, K., Chibnik, L., Hickey, B., Stahl, E.A., Gainer, V., Li, G., Bry, L., Mahan, S., Ardlie, K. et al. (2011) Genetic basis of autoantibody positive and negative rheumatoid arthritis risk in a multi-ethnic cohort derived from electronic health records. Am. J. Hum. Genet., 88, 57–69.
35. Lewontin, R.C. and Krakauer, J. (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics, 74, 175 – 195.
36. Viatte, S., Plant, D. and Raychaudhuri, S. (2013) Genetics and epigenetics of rheumatoid arthritis. Nat. Rev. Rheumatol., 9, 141 – 153.