Identification of a Systemic Lupus Erythematosus Risk Locus Spanning ATG16L2, FCHSD2, and P2RY2 in Koreans

Arthritis and Rheumatology

Volumn 68, Issue 5, 2016, Pages 1197-1209

  Lessard, Christopher J ^a   Sajuthi, Satria ^b   Zhao, Jian ^c   Kim, Kwangwoo ^d   Ice, John A ^a   Li, He ^e   Ainsworth, Hannah ^b   Rasmussen, Astrid ^a   Kelly, Jennifer A ^a   Marion, Miranda ^b   Bang, So Young ^d   Bin Joo, Young ^d   Choi, Jeongim ^d   Lee, Hye Soon ^d   Mo Kang, Young ^f   Suh, Chang Hee ^g   Tae Chung, Won ^h   Lee, Soo Kon ⁱ   Choe, Jung Yoon ^j   Cheol Shim, Seung ^k   Hee Oh, Ji ^l   Jin Kim, Young ^l   Han, Bok Ghee ^l   Shen, Nan ^m   Siew Howe, Hwee ⁿ   Wakeland, Edward K ^o   Li, Quan Zhen ^o   Wook Song, Yeong ^p   Gaffney, Patrick M ^a   Alarcón Riquelme, Marta E ^q   Criswell, Lindsey A ^r   Jacob, Chaim O ^s   Kimberly, Robert P ^t   Vyse, Timothy J ^u   Harley, John B ^v   Sivils, Kathy L ^e   Bae, Sang Cheol ^d   Langefeld, Carl D ^b   Tsao, Betty P ^c   more..

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

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

^e UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^f Kyungpook National University Hospital   (South Korea)

^g Ajou University Medical Center   (South Korea)

^h Dong A University College of Medicine   (South Korea)

ⁱ Yonsei University College of Medicine   (South Korea)

^j Catholic University of Daegu   (South Korea)

^k Chungnam National University College of Medicine   (South Korea)

^l Korea National Institute of Health   (South Korea)

^m SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

ⁿ TAN TOCK SENG HOSPITAL   (Singapore)

^o UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^p Seoul National University Hospital   (South Korea)

^q JUNTA DE ANDALUCÍA   (Spain)

^r UNIVERSITY OF CALIFORNIA   (United States)

^s UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^t UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^u KING'S COLLEGE LONDON   (United Kingdom)

^v CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ATG16L2 PROTEIN; BLK PROTEIN; ETSI PROTEIN; FCHSD2 PROTEIN; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; HLA DPB1 ANTIGEN; HLA DQA1 ANTIGEN; HLA DQB1 ANTIGEN; HLA DRB1 ANTIGEN; IKZF1 PROTEIN; INTERFERON REGULATORY FACTOR 5; IRAKI PROTEIN; METHYL CPG BINDING PROTEIN 2; OX40 LIGAND; PROTEIN; PURINERGIC P2 RECEPTOR; STAT1 PROTEIN; STAT4 PROTEIN; TNFAIP3 PROTEIN; UNCLASSIFIED DRUG; WDFY4 PROTEIN; ATG16L1 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN; CARRIER PROTEIN; FCHSD2 PROTEIN, HUMAN; HLA DQ ANTIGEN; HLA-DQB1 ANTIGEN; HLA-DRB1*15:01 ANTIGEN; MEMBRANE PROTEIN; P2RY2 PROTEIN, HUMAN; PURINERGIC P2Y2 RECEPTOR; TNFAIP3 PROTEIN, HUMAN; TNFSF4 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR ALPHA INDUCED PROTEIN 3;

ADULT; ALLELE; ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC ASSOCIATION; HUMAN; KOREAN (PEOPLE); MAJOR CLINICAL STUDY; MALE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUALITY CONTROL; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS; ASIAN CONTINENTAL ANCESTRY GROUP; CASE CONTROL STUDY; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; SOUTH KOREA;

ASIAN CONTINENTAL ANCESTRY GROUP; AUTOPHAGY-RELATED PROTEINS; CARRIER PROTEINS; CASE-CONTROL STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HLA-DQ BETA-CHAINS; HLA-DRB1 CHAINS; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MEMBRANE PROTEINS; OX40 LIGAND; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, PURINERGIC P2Y2; REPUBLIC OF KOREA; TUMOR NECROSIS FACTOR ALPHA-INDUCED PROTEIN 3;

EID: 84964600746     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39548     Document Type: Article

References (50)

1. Tsokos GC., Systemic lupus erythematosus. N Engl J Med 2011; 365: 2110-21.
2. Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, et al., Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 2003; 349: 1526-33.
3. Moser KL, Kelly JA, Lessard CJ, Harley JB., Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun 2009; 10: 373-9.
4. Deng Y, Tsao BP., Advances in lupus genetics and epigenetics. Curr Opin Rheumatol 2014; 26: 482-92.
5. Dai C, Deng Y, Quinlan A, Gaskin F, Tsao BP, Fu SM., Genetics of systemic lupus erythematosus: immune responses and end organ resistance to damage. Curr Opin Immunol 2014; 31: 87-96.
6. Han JW, Zheng HF, Cui Y, Sun LD, Ye DQ, Hu Z, et al., Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat Genet 2009; 41: 1234-7.
7. Yang W, Tang H, Zhang Y, Tang X, Zhang J, Sun L, et al., Meta-analysis followed by replication identifies loci in or near CDKN1B, TET3, CD80, DRAM1, and ARID5B as associated with systemic lupus erythematosus in Asians. Am J Hum Genet 2013; 92: 41-51.
8. Yang W, Shen N, Ye DQ, Liu Q, Zhang Y, Qian XX, et al, Asian Lupus Genetics Consortium (ALGC). Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet 2010; 6: e1000841.
9. Okada Y, Shimane K, Kochi Y, Tahira T, Suzuki A, Higasa K, et al., A genome-wide association study identified AFF1 as a susceptibility locus for systemic lupus eyrthematosus in Japanese. PLoS Genet 2012; 8: e1002455.
10. Kim K, Bang SY, Lee HS, Cho SK, Choi CB, Sung YK, et al., High-density genotyping of immune loci in Koreans and Europeans identifies eight new rheumatoid arthritis risk loci. Ann Rheum Dis 2015; 74: e13.
11. Lessard CJ, Adrianto I, Ice JA, Wiley GB, Kelly JA, Glenn SB, et al., Identification of IRF8, TMEM39A, and IKZF3-ZPBP2 as susceptibility loci for systemic lupus erythematosus in a large-scale multiracial replication study. Am J Hum Genet 2012; 90: 648-60.
12. Kaiser R, Taylor KE, Deng Y, Zhao J, Li Y, Nititham J, et al., Single-nucleotide polymorphisms in VKORC1 are risk factors for systemic lupus erythematosus in Asians. Arthritis Rheum 2013; 65: 211-5.
13. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al., The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982; 25: 1271-7.
14. Hochberg MC, for the Diagnostic and Therapeutic Criteria Committee of the American College of Rheumatology. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus [letter]. Arthritis Rheum 1997; 40: 1725.
15. Manichaikul A, Mychaleckyj JC, Rich SS, Daly K, Sale M, Chen WM., Robust relationship inference in genome-wide association studies. Bioinformatics 2010; 26: 2867-73.
16. Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, Gibbs RA, et al., A second generation human haplotype map of over 3.1 million SNPs. Nature 2007; 449: 851-61.
17. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D., Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 2006; 38: 904-9.
18. Willer CJ, Li Y, Abecasis GR., METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 2010; 26: 2190-1.
19. Cochran WG., The combination of estimates from different experiments. Biometrics 1954; 10: 101-29.
20. Higgins JP, Thompson SG, Deeks JJ, Altman DG., Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-60.
21. Durbin RM, Abecasis GR, Altshuler DL, Auton A, Brooks LD, Gibbs RA, et al., A map of human genome variation from population-scale sequencing. Nature 2010; 467: 1061-73.
22. Delaneau O, Marchini J, Zagury JF., A linear complexity phasing method for thousands of genomes. Nat Methods 2012; 9: 179-81.
23. Howie BN, Donnelly P, Marchini J., A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet 2009; 5: e1000529.
24. Marchini J, Howie B., Genotype imputation for genome-wide association studies. Nat Rev Genet 2010; 11: 499-511.
25. Zheng X, Shen J, Cox C, Wakefield JC, Ehm MG, Nelson MR, et al., HIBAG-HLA genotype imputation with attribute bagging. Pharmacogenomics J 2014; 14: 192-200.
26. Ward LD, Kellis M., HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res 2012; 40: D930-4.
27. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, et al., An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489: 57-74.
28. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al., Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462: 315-22.
29. Raj T, Rothamel K, Mostafavi S, Ye C, Lee MN, Replogle JM, et al., Polarization of the effects of autoimmune and neurodegenerative risk alleles in leukocytes. Science 2014; 344: 519-23.
30. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al., A method and server for predicting damaging missense mutations. Nat Methods 2010; 7: 248-9.
31. Lee HS, Kim T, Bang SY, Na YJ, Kim I, Kim K, et al., Ethnic specificity of lupus-associated loci identified in a genome-wide association study in Korean women. Ann Rheum Dis 2014; 73: 1240-5.
32. Adrianto I, Wen F, Templeton A, Wiley G, King JB, Lessard CJ, et al., Association of a functional variant downstream of TNFAIP3 with systemic lupus erythematosus. Nat Genet 2011; 43: 253-8.
33. Musone SL, Taylor KE, Lu TT, Nititham J, Ferreira RC, Ortmann W, et al., Multiple polymorphisms in the TNFAIP3 region are independently associated with systemic lupus erythematosus. Nat Genet 2008; 40: 1062-4.
34. Cunninghame Graham DS, Graham RR, Manku H, Wong AK, Whittaker JC, Gaffney PM, et al., Polymorphism at the TNF superfamily gene TNFSF4 confers susceptibility to systemic lupus erythematosus. Nat Genet 2008; 40: 83-9.
35. Manku H, Langefeld CD, Guerra SG, Malik TH, Alarcon-Riquelme M, Anaya JM, et al., Trans-ancestral studies fine map the SLE-susceptibility locus TNFSF4. PLoS Genet 2013; 9: e1003554.
36. Zhao H, Yang W, Qiu R, Li J, Xin Q, Wang X, et al., An intronic variant associated with systemic lupus erythematosus changes the binding affinity of Yinyang1 to downregulate WDFY4. Genes Immun 2012; 13: 536-42.
37. Yang SK, Hong M, Zhao W, Jung Y, Baek J, Tayebi N, et al., Genome-wide association study of Crohn's disease in Koreans revealed three new susceptibility loci and common attributes of genetic susceptibility across ethnic populations. Gut 2014; 63: 80-7.
38. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, Huse K, et al., A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 2007; 39: 207-11.
39. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, et al., BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 2009; 10: R130.
40. Harley JB, Alarcon-Riquelme ME, Criswell LA, Jacob CO, Kimberly RP, Moser KL, et al., Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 2008; 40: 204-10.
41. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, et al., Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 2003; 116: 1679-88.
42. Cao H, Yin X, Cao Y, Jin Y, Wang S, Kong Y, et al., FCHSD1 and FCHSD2 are expressed in hair cell stereocilia and cuticular plate and regulate actin polymerization in vitro. PLoS One 2013; 8: e56516.
43. Lafouresse F, Cotta-de-Almeida V, Malet-Engra G, Galy A, Valitutti S, Dupre L., Wiskott-Aldrich syndrome protein controls antigen-presenting cell-driven CD4+ T-cell motility by regulating adhesion to intercellular adhesion molecule-1. Immunology 2012; 137: 183-96.
44. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, et al., Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009; 461: 282-6.
45. Higgins KR, Kovacevic W, Stokes L., Nucleotides regulate secretion of the inflammatory chemokine CCL2 from human macrophages and monocytes. Mediators Inflamm 2014; 2014: 293925.
46. Lee HS, Chung YH, Kim TG, Kim TH, Jun JB, Jung S, et al., Independent association of HLA-DR and FCγ receptor polymorphisms in Korean patients with systemic lupus erythematosus. Rheumatology (Oxford) 2003; 42: 1501-7.
47. Graham RR, Ortmann W, Rodine P, Espe K, Langefeld C, Lange E, et al., Specific combinations of HLA-DR2 and DR3 class II haplotypes contribute graded risk for disease susceptibility and autoantibodies in human SLE. Eur J Hum Genet 2007; 15: 823-30.
48. Furukawa H, Oka S, Shimada K, Sugii S, Hashimoto A, Komiya A, et al., Association of increased frequencies of HLA-DPB1∗ 05:01 with the presence of anti-Ro/SS-A and anti-La/SS-B antibodies in Japanese rheumatoid arthritis and systemic lupus erythematosus patients. PLoS One 2013; 8: e53910.
49. Furukawa H, Kawasaki A, Oka S, Ito I, Shimada K, Sugii S, et al., Human leukocyte antigens and systemic lupus erythematosus: a protective role for the HLA-DR6 alleles DRB1∗13:02 and∗14:03. PLoS One 2014; 9: e87792.
50. Kim K, Bang SY, Lee HS, Okada Y, Han B, Saw WY, et al., The HLA-DRβ1 amino acid positions 11-13-26 explain the majority of SLE-MHC associations. Nat Commun 2014; 5: 5902.