Transancestral mapping and genetic load in systemic lupus erythematosus

Nature Communications

Volumn 8, Issue , 2017, Pages

  Langefeld, Carl D ^a   Ainsworth, Hannah C ^a   Graham, Deborah S Cunninghame ^b   Kelly, Jennifer A ^c   Comeau, Mary E ^a   Marion, Miranda C ^a   Howard, Timothy D ^a   Ramos, Paula S ^d   Croker, Jennifer A ^e   Morris, David L ^b   Sandling, Johanna K ^f   Almlöf, Jonas Carlsson ^f   Acevedo Vásquez, Eduardo M ^g   Alarcón, Graciela S ^e   Babini, Alejandra M ^h   Baca, Vicente ⁱ   Bengtsson, Anders A ^j   Berbotto, Guillermo A ^k   Bijl, Marc ^l   Brown, Elizabeth E ^e   Brunner, Hermine I ^m   Cardiel, Mario H ⁿ   Catoggio, Luis ^h   Cervera, Ricard ^o   Cucho Venegas, Jorge M ^g   Dahlqvist, Solbritt Rantapää ^p   D'Alfonso, Sandra ^q   Da Silva, Berta Martins ^r   De La RúaFigueroa, Inígo ^s   Doria, Andrea ^t   Edberg, Jeffrey C ^e   Endreffy, Emoke ^u   Esquivel Valerio, Jorge A ^v   Fortin, Paul R ^w   Freedman, Barry I ^a   Frostegård, Johan ^x   Garcýá, Mercedes A ^y   De La Torre, Ignacio Garcýá ^z   Gilkeson, Gary S ^d   Gladman, Dafna D ^aa   Gunnarsson, Iva ^ab   Guthridge, Joel M ^c   Huggins, Jennifer L ^m   James, Judith A ^c,ac   Kallenberg, Cees G M ^ad   Kamen, Diane L ^d   Karp, David R ^ae   Kaufman, Kenneth M ^af   Kottyan, Leah C ^af   Kovács, László ^u   Laustrup, Helle ^ag   Lauwerys, Bernard R ^ah   Li, Quan Zhen ^ae   Maradiaga Ceceną, Marco A ^ai   Martín, Javier ^aj   McCune, Joseph M ^ak   McWilliams, David R ^a   Merrill, Joan T ^c   Miranda, Pedro ^al   Moctezuma, José F ^am   Nath, Swapan K ^c   Niewold, Timothy B ^an   Orozco, Lorena ^ao   Ortego Centeno, Norberto ^ap   Petri, Michelle ^aq   Pineau, Christian A ^ar   Pons Estel, Bernardo A ^as   Pope, Janet ^at   Raj, Prithvi ^ae   Ramsey Goldman, Rosalind ^au   Reveille, John D ^av   Russell, Laurie P ^a   Sabio, José M ^aw   Aguilar Salinas, Carlos A ^ax   Scherbarth, Hugo R ^ay   Scorza, Raffaella ^az   Seldin, Michael F ^ba   Sjöwall, Christopher ^bb   Svenungsson, Elisabet ^ab   Thompson, Susan D ^af   Toloza, Sergio M A ^bc   Truedsson, Lennart ^j   Tusié Luna, Teresa ^bd   Vasconcelos, Carlos ^r   Vilá, Luis M ^be   Wallace, Daniel J ^bf   Weisman, Michael H ^bf   Wither, Joan E ^aa   Bhangale, Tushar ^bg   Oksenberg, Jorge R ^bh   Rioux, John D ^bi   Gregersen, Peter K ^bj   Syvänen, Ann Christine ^f   Rönnblom, Lars ^f   Criswell, Lindsey A ^bk   Jacob, Chaim O ^bl   Sivils, Kathy L ^c   Tsao, Betty P ^d   Schanberg, Laura E ^bm   Behrens, Timothy W ^bg   Silverman, Earl D ^bn   Alarcón Riquelme, Marta E ^c,x,bo   Kimberly, Robert P ^e   Harley, John B ^af   Wakeland, Edward K ^ae   Graham, Robert R ^bg   Gaffney, Patrick M ^c   Vyse, Timothy J ^b   more..

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b GUY S HOSPITAL   (United Kingdom)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e The University of Alabama at Birmingham   (United States)

^f UPPSALA UNIVERSITY   (Sweden)

^g UNIVERSIDAD NACIONAL MAYOR DE SAN MARCOS   (Peru)

^h HOSPITAL ITALIANO DE BUENOS AIRES   (Argentina)

ⁱ INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^j LUND UNIVERSITY   (Sweden)

^k Hospital Eva Peron   (Argentina)

^l MARTINI HOSPITAL   (Netherlands)

^m UNIVERSITY OF CINCINNATI   (United States)

ⁿ Centro de Investigacion Clinica de Morelia   (Mexico)

^o UNIVERSITY OF BARCELONA   (Spain)

^p UMEÅ UNIVERSITY   (Sweden)

^q UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^r UNIVERSITY OF PORTO   (Portugal)

^s HOSPITAL UNIVERSITARIO DE GRAN CANARIA DR NEGRÍN   (Spain)

^t UNIVERSITY OF PADOVA   (Italy)

^u UNIVERSITY OF SZEGED   (Hungary)

^v HOSPITAL UNIVERSITARIO DR JOSÉ ELEUTERIO GONZÁLEZ   (Mexico)

^w LAVAL UNIVERSITY   (Canada)

^x KAROLINSKA INSTITUTE   (Sweden)

^y Hospital Interzonal General de Agudos de La Plata   (Argentina)

^z UNIVERSITY OF GUADALAJARA   (Mexico)

^aa UNIVERSITY HEALTH NETWORK   (Canada)

^ab KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^ac UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^ad UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

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

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

^ag ODENSE UNIVERSITY HOSPITAL   (Denmark)

^ah CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^ai Hospital General de Culiacán   (Mexico)

^aj INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^ak UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^al Centro de Estudios Reumatologicos   (Chile)

^am SECRETARÍA DE SALUD   (Mexico)

^an MAYO CLINIC   (United States)

^ao INSTITUTO NACIONAL DE MEDICINA GENÓMICA   (Mexico)

^ap HOSPITAL UNIVERSITARIO SAN CECILIO   (Spain)

^aq JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^ar MCGILL UNIVERSITY   (Canada)

^as Sanatorio Parque   (Argentina)

^at UNIVERSITY OF WESTERN ONTARIO   (Canada)

^au NORTHWESTERN UNIVERSITY   (United States)

^av UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^aw HOSPITAL UNIVERSITARIO VIRGEN DE LAS NIEVES   (Spain)

^ax INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^ay Unidad Reumatologí y Enfermedades   (Argentina)

^az UNIVERSITY OF MILAN   (Italy)

^ba UNIVERSITY OF CALIFORNIA   (United States)

^bb LINKÖPING UNIVERSITY   (Sweden)

^bc Linköping University ^*  (Argentina)

^bd UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^be UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^bf CEDARS SINAI MEDICAL CENTER   (United States)

^bg GENENTECH INC   (United States)

^bh UNIVERSITY OF CALIFORNIA   (United States)

^bi MONTREAL HEART INSTITUTE   (Canada)

^bj FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^bk UNIVERSITY OF CALIFORNIA   (United States)

^bl UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^bm DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^bn HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^bo UNIVERSITY OF GRANADA   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; GAMMA INTERFERON; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HERMES ANTIGEN; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; HLA DPB1 ANTIGEN; HLA DQA1 ANTIGEN; HLA DQB1 ANTIGEN; HLA DRB1 ANTIGEN; INTERFERON REGULATORY FACTOR 5; INTERLEUKIN 12 RECEPTOR BETA2; INTERLEUKIN 2; INTERLEUKIN 21; PROTEIN KINASE LYN; HLA ANTIGEN;

ALLELE; ANCESTRY; DISEASE; GENETIC ANALYSIS; GENOTYPE; IMMUNE SYSTEM; MAPPING;

AFRICAN; AFRICAN AMERICAN; ALLELE; AMERICAN INDIAN; ANCESTRY GROUP; ARTICLE; CONTROLLED STUDY; EUROPEAN; GENE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC LOAD; GENOTYPE; HETEROZYGOSITY; HISPANIC; HUMAN; LRRC16A GENE; MAJOR CLINICAL STUDY; PKIA GENE; SLC17A4 GENE; SYSTEMIC LUPUS ERYTHEMATOSUS; X CHROMOSOME; ZC2HC1A GENE; BLACK PERSON; CASE CONTROL STUDY; CAUCASIAN; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; MULTIFACTORIAL INHERITANCE; ONSET AGE; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL MODEL;

AFRICAN CONTINENTAL ANCESTRY GROUP; AGE OF ONSET; AMERICAN NATIVE CONTINENTAL ANCESTRY GROUP; CASE-CONTROL STUDIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENETIC LOAD; HISPANIC AMERICANS; HLA ANTIGENS; HUMANS; LOGISTIC MODELS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MULTIFACTORIAL INHERITANCE; MUTAGENESIS, INSERTIONAL; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE DELETION;

EID: 85024906085     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms16021     Document Type: Article

References (61)

1. Danchenko, N., Satia, J. A. & Anthony, M. S. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus 15, 308-318 (2006).
2. International Consortium for Systemic Lupus Erythematosus Genetics (SLEGEN) et al. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat. Genet. 40, 204-210 (2008).
3. Chung, S. A. et al. Lupus nephritis susceptibility loci in women with systemic lupus erythematosus. J. Am. Soc. Nephrol. 25, 2859-2870 (2014).
4. Hom, G. et al. Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX. N. Engl. J. Med. 358, 900-909 (2008).
5. Rullo, O. J. & Tsao, B. P. Recent insights into the genetic basis of systemic lupus erythematosus. Ann. Rheum. Dis. 72, ii56-ii61 (2013).
6. Bentham, J. et al. Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat. Genet. 47, 1457-1464 (2015).
7. Sun, C. et al. High-density genotyping of immune-related loci identifies new SLE risk variants in individuals with Asian ancestry. Nat. Genet. 48, 323-330 (2016).
8. Morris, D. L. et al. Genome-wide association meta-analysis in Chinese and European individuals identifies ten new loci associated with systemic lupus erythematosus. Nat. Genet. 48, 940-946 (2016).
9. Cortes, A. & Brown, M. A. Promise and pitfalls of the Immunochip. Arthritis Res. Ther. 13, 101 (2010).
10. Chung, S. A. et al. Differential genetic associations for systemic lupus erythematosus based on anti-dsDNA autoantibody production. PLoS Genet. 7, e1001323 (2011).
11. Graham, R. R. 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. 15, 823-830 (2007).
12. Lenz, T. L. et al. Widespread non-additive and interaction effects within HLA loci modulate the risk of autoimmune diseases. Nat. Genet. 47, 1085-1090 (2015).
13. Erlich, H. et al. HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk analysis of the type 1 diabetes genetics consortium families. Diabetes 57, 1084-1092 (2008).
14. Reche, P. A. & Reinherz, E. L. Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J. Mol. Biol. 331, 623-641 (2003).
15. Raychaudhuri, S. et al. Five amino acids in three HLA proteins explain most of the association between MHC and seropositive rheumatoid arthritis. Nat. Genet. 44, 291-296 (2012).
16. Gregersen, P. K., Silver, J. & Winchester, R. J. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 30, 1205-1213 (1987).
17. du Montcel, S. T. et al. New classification of HLA-DRB1 alleles supports the shared epitope hypothesis of rheumatoid arthritis susceptibility. Arthritis Rheum. 52, 1063-1068 (2005).
18. Raymond, C. K. et al. Ancient haplotypes of the HLA Class II region. Genome Res. 15, 1250-1257 (2005).
19. Bossini-Castillo, L. et al. A GWAS follow-up study reveals the association of the IL12RB2 gene with systemic sclerosis in Caucasian populations. Hum. Mol. Genet. 21, 926-933 (2012).
20. Hirschfield, G. M. et al. Primary biliary cirrhosis associated with HLA, IL12A, and IL12RB2 variants. N. Engl. J. Med. 360, 2544-2555 (2009).
21. Gray-McGuire, C. et al. Genome scan of human systemic lupus erythematosus by regression modeling: evidence of linkage and epistasis at 4p16-15.2. Am. J. Hum. Genet. 67, 1460-1469 (2000).
22. Boyle, A. P. et al. Annotation of functional variation in personal genomes using RegulomeDB. Genome Res. 22, 1790-1797 (2012).
23. Ward, L. D. & Kellis, M. HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res. 40, D930-D934 (2012).
24. Huang, C. et al. Cutting edge: a novel, human-specific interacting protein couples FOXP3 to a chromatin-remodeling complex that contains KAP1/TRIM28. J. Immunol. 190, 4470-4473 (2013).
25. Han, J.-W. et al. Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat. Genet. 41, 1234-1237 (2009).
26. Wang, C. et al. Genes identified in Asian SLE GWASs are also associated with SLE in Caucasian populations. Eur. J. Hum. Genet. 21, 994-999 (2013).
27. Ahmed, Z. et al. Direct binding of Grb2 SH3 domain to FGFR2 regulates SHP2 function. Cell. Signal. 22, 23-33 (2010).
28. Sun, J. et al. Antagonism between binding site affinity and conformational dynamics tunes alternative cis-interactions within Shp2. Nat. Commun. 4, 2037 (2013).
29. Wang, J. et al. Inhibition of SHP2 ameliorates the pathogenesis of systemic lupus erythematosus. J. Clin. Invest. 126, 2077-2092 (2016).
30. Sawalha, A. H. et al. Genetic association of interleukin-21 polymorphisms with systemic lupus erythematosus. Ann. Rheum. Dis. 67, 458-461 (2008).
31. Choi, J.-Y. et al. Circulating follicular helper-like T cells in systemic lupus erythematosus: association with disease activity: circulating Tfh-like cells in SLE. Arthritis Rheumatol. 67, 988-999 (2015).
32. Löfgren, S. E. et al. Genetic association of miRNA-146a with systemic lupus erythematosus in Europeans through decreased expression of the gene. Genes Immun. 13, 268-274 (2012).
33. Liu, J. Z. et al. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat. Genet. 47, 979-986 (2015).
34. Kwok, W. W., Kovats, S., Thurtle, P. & Nepom, G. T. HLA-DQ allelic polymorphisms constrain patterns of class II heterodimer formation. J. Immunol. 150, 2263-2272 (1993).
35. Miyadera, H., Ohashi, J., Lernmark, Å., Kitamura, T. & Tokunaga, K. Cell-surface MHC density profiling reveals instability of autoimmunity-associated HLA. J. Clin. Invest. 125, 275-291 (2015).
36. van Heemst, J., Huizinga, T. J., van der Woude, D. & Toes, R. E. Fine-mapping the human leukocyte antigen locus in rheumatoid arthritis and other rheumatic diseases: identifying causal amino acid variants? Curr. Opin. Rheumatol. 27, 256-261 (2015).
37. Segal, M. R., Cummings, M. P. & Hubbard, A. E. Relating amino acid sequence to phenotype: analysis of peptide-binding data. Biometrics 57, 632-643 (2001).
38. Majumder, P. & Boss, J. M. DNA methylation dysregulates and silences the HLA-DQ locus by altering chromatin architecture. Genes Immun. 12, 291-299 (2011).
39. Kaushansky, N. et al. Role of a novel HLA-DQA1∗ 01: 02; DRB1∗ 15: 01 mixed-isotype heterodimer in the pathogenesis of 'humanized' multiple sclerosis-like disease. J. Biol. Chem. 290, 15260-15278 (2015).
40. Tan, E. M. et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25, 1271-1277 (1982).
41. Hochberg, M. C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40, 1725 (1997).
42. Shah, T. S. et al. optiCall: a robust genotype-calling algorithm for rare, low-frequency and common variants. Bioinformatics 28, 1598-1603 (2012).
43. Morris, J. A., Randall, J. C., Maller, J. B. & Barrett, J. C. Evoker: a visualization tool for genotype intensity data. Bioinformatics 26, 1786-1787 (2010).
44. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009).
45. Johnson, R. A. & Wichern, D. W. Applied Multivariate Statistical Analysis (Pearson Prentice Hall, 2007).
46. Price, A. L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904-909 (2006).
47. Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).
48. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289-300 (1995).
49. Willer, C. J., Li, Y. & Abecasis, G. R. METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 26, 2190-2191 (2010).
50. Pruim, R. J. et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26, 2336-2337 (2010).
51. Zheng, X. et al. HIBAG-HLA genotype imputation with attribute bagging. Pharmacogenomics J. 14, 192-200 (2014).
52. Browning, S. R. & Browning, B. L. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084-1097 (2007).
53. Dilthey, A. et al. Multi-population classical HLA type imputation. PLoS Comput. Biol. 9, e1002877 (2013).
54. Jia, X. et al. Imputing amino acid polymorphisms in human leukocyte antigens. PLoS ONE 8, e64683 (2013).
55. Robinson, J. et al. The IMGT/HLA database. Nucleic Acids Res. 41, D1222-D1227 (2013).
56. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539-539 (2014).
57. Yang, Z. & Rannala, B. Molecular phylogenetics: principles and practice. Nat. Rev. Genet. 13, 303-314 (2012).
58. Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).
59. Huson, D. H. & Scornavacca, C. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst. Biol. 61, 1061-1067 (2012).
60. Johnson, A. D. et al. SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24, 2938-2939 (2008).
61. Westra, H.-J. et al. Systematic identification of trans eQTLs as putative drivers of known disease associations. Nat. Genet. 45, 1238-1243 (2013).