HLA-DRB111 and variants of the MHC class II locus are strong risk factors for systemic juvenile idiopathic arthritis
To determine whether genetic variation within the MHC locus influences the risk of developing systemic juvenile idiopathic arthritis (sJIA), we examined a dense set of MHC region single nucleotide polymorphisms, classic HLA alleles, and the individual amino acids of HLA molecules in nine independent...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 52; pp. 15970 - 15975 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article Web Resource |
| Language | English |
| Published |
United States
National Acad Sciences
29.12.2015
National Academy of Sciences |
| Series | From the Cover |
| Subjects | |
| Online Access | Get full text |
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| Abstract | To determine whether genetic variation within the MHC locus influences the risk of developing systemic juvenile idiopathic arthritis (sJIA), we examined a dense set of MHC region single nucleotide polymorphisms, classic HLA alleles, and the individual amino acids of HLA molecules in nine independent sJIA case-control populations. Association testing revealed that genetic variants within the MHC class II gene cluster significantly influenced sJIA risk in every study population. The strongest risk factor for sJIA was
HLA-DRB1*11
, which conferred at least a two-fold increase in disease risk in each population studied. These data implicate the interaction of antigen presenting cells with T cells in the pathogenesis of sJIA.
Systemic juvenile idiopathic arthritis (sJIA) is an often severe, potentially life-threatening childhood inflammatory disease, the pathophysiology of which is poorly understood. To determine whether genetic variation within the MHC locus on chromosome 6 influences sJIA susceptibility, we performed an association study of 982 children with sJIA and 8,010 healthy control subjects from nine countries. Using meta-analysis of directly observed and imputed SNP genotypes and imputed classic HLA types, we identified the MHC locus as a bona fide susceptibility locus with effects on sJIA risk that transcended geographically defined strata. The strongest sJIA-associated SNP, rs151043342 [
P
= 2.8 × 10
−17
, odds ratio (OR) 2.6 (2.1, 3.3)], was part of a cluster of 482 sJIA-associated SNPs that spanned a 400-kb region and included the class II HLA region. Conditional analysis controlling for the effect of rs151043342 found that rs12722051 independently influenced sJIA risk [
P
= 1.0 × 10
−5
, OR 0.7 (0.6, 0.8)]. Meta-analysis of imputed classic HLA-type associations in six study populations of Western European ancestry revealed that
HLA-DRB1*11
and its defining amino acid residue, glutamate 58, were strongly associated with sJIA [
P
= 2.7 × 10
−16
, OR 2.3 (1.9, 2.8)], as was the
HLA-DRB1*11—HLA-DQA1*05—HLA-DQB1*03
haplotype [6.4 × 10
−17
, OR 2.3 (1.9, 2.9)]. By examining the MHC locus in the largest collection of sJIA patients assembled to date, this study solidifies the relationship between the class II HLA region and sJIA, implicating adaptive immune molecules in the pathogenesis of sJIA. |
|---|---|
| AbstractList | Systemic juvenile idiopathic arthritis (sJIA) is an often severe, potentially life-threatening childhood inflammatory disease, the pathophysiology of which is poorly understood. To determine whether genetic variation within the MHC locus on chromosome 6 influences sJIA susceptibility, we performed an association study of 982 children with sJIA and 8,010 healthy control subjects from nine countries. Using meta-analysis of directly observed and imputed SNP genotypes and imputed classic HLA types, we identified the MHC locus as a bona fide susceptibility locus with effects on sJIA risk that transcended geographically defined strata. The strongest sJIA-associated SNP, rs151043342 [P = 2.8 × 10(-17), odds ratio (OR) 2.6 (2.1, 3.3)], was part of a cluster of 482 sJIA-associated SNPs that spanned a 400-kb region and included the class II HLA region. Conditional analysis controlling for the effect of rs151043342 found that rs12722051 independently influenced sJIA risk [P = 1.0 × 10(-5), OR 0.7 (0.6, 0.8)]. Meta-analysis of imputed classic HLA-type associations in six study populations of Western European ancestry revealed that HLA-DRB1*11 and its defining amino acid residue, glutamate 58, were strongly associated with sJIA [P = 2.7 × 10(-16), OR 2.3 (1.9, 2.8)], as was the HLA-DRB1*11-HLA-DQA1*05-HLA-DQB1*03 haplotype [6.4 × 10(-17), OR 2.3 (1.9, 2.9)]. By examining the MHC locus in the largest collection of sJIA patients assembled to date, this study solidifies the relationship between the class II HLA region and sJIA, implicating adaptive immune molecules in the pathogenesis of sJIA. Systemic juvenile idiopathic arthritis (sJIA) is an often severe, potentially life-threatening childhood inflammatory disease, the pathophysiology of which is poorly understood. To determine whether genetic variation within the MHC locus on chromosome 6 influences sJIA susceptibility, we performed an association study of 982 children with sJIA and 8,010 healthy control subjects from nine countries. Using meta-analysis of directly observed and imputed SNP genotypes and imputed classic HLA types, we identified the MHC locus as a bona fide susceptibility locus with effects on sJIA risk that transcended geographically defined strata. The strongest sJIA-associated SNP, rs151043342 [P = 2.8 x 10..., odds ratio (OR) 2.6 (2.1, 3.3)], was part of a cluster of 482 sJIA-associated SNPs that spanned a 400-kb region and included the class II HLA region. Conditional analysis controlling for the effect of rs151043342 found that rs12722051 independently influenced sJIA risk [P = 1.0 x 10..., OR 0.7 (0.6, 0.8)]. Meta-analysis of imputed classic HLA-type associations in six study populations of Western European ancestry revealed that HLA-DRB1*11 and its defining amino acid residue, glutamate 58, were strongly associated with sJIA [P = 2.7 x 10..., OR 2.3 (1.9, 2.8)], as was the HLA-DRB1*11-HLA-DQA1*05-HLA-DQB1*03 haplotype [6.4 x 10..., OR 2.3 (1.9, 2.9)]. By examining the MHC locus in the largest collection of sJIA patients assembled to date, this study solidifies the relationship between the class II HLA region and sJIA, implicating adaptive immune molecules in the pathogenesis of sJIA. (ProQuest: ... denotes formulae/symbols omitted.) Systemic juvenile idiopathic arthritis (sJIA) is an often severe, potentially life-threatening childhood inflammatory disease, the pathophysiology of which is poorly understood. To determine whether genetic variation within the MHC locus on chromosome 6 influences sJIA susceptibility, we performed an association study of 982 children with sJIA and 8,010 healthy control subjects from nine countries. Using meta-analysis of directly observed and imputed SNP genotypes and imputed classic HLA types, we identified the MHC locus as a bona fide susceptibility locus with effects on sJIA risk that transcended geographically defined strata. The strongest sJIA-associated SNP, rs151043342 [P = 2.8 x 10(-17), odds ratio (OR) 2.6 (2.1, 3.3)], was part of a cluster of 482 sJIA-associated SNPs that spanned a 400-kb region and included the class II HLA region. Conditional analysis controlling for the effect of rs151043342 found that rs12722051 independently influenced sJIA risk [P = 1.0 x 10(-5), OR 0.7 (0.6, 0.8)]. Meta-analysis of imputed classic HLA-type associations in six study populations of Western European ancestry revealed that HLA-DRB1*11 and its defining amino acid residue, glutamate 58, were strongly associated with sJIA [P = 2.7 x 10(=16), OR 2.3 (1.9, 2.8)], as was the HLA-DRB1*11-HLA-DQA1*05-HLA-DQB1*03 haplotype [6.4 x 10(-17), OR 2.3 (1.9, 2.9)]. By examining the MHC locus in the largest collection of sJIA patients assembled to date, this study solidifies the relationship between the class II HLA region and sJIA, implicating adaptive immune molecules in the pathogenesis of sJIA. To determine whether genetic variation within the MHC locus influences the risk of developing systemic juvenile idiopathic arthritis (sJIA), we examined a dense set of MHC region single nucleotide polymorphisms, classic HLA alleles, and the individual amino acids of HLA molecules in nine independent sJIA case-control populations. Association testing revealed that genetic variants within the MHC class II gene cluster significantly influenced sJIA risk in every study population. The strongest risk factor for sJIA was HLA-DRB1*11 , which conferred at least a two-fold increase in disease risk in each population studied. These data implicate the interaction of antigen presenting cells with T cells in the pathogenesis of sJIA. Systemic juvenile idiopathic arthritis (sJIA) is an often severe, potentially life-threatening childhood inflammatory disease, the pathophysiology of which is poorly understood. To determine whether genetic variation within the MHC locus on chromosome 6 influences sJIA susceptibility, we performed an association study of 982 children with sJIA and 8,010 healthy control subjects from nine countries. Using meta-analysis of directly observed and imputed SNP genotypes and imputed classic HLA types, we identified the MHC locus as a bona fide susceptibility locus with effects on sJIA risk that transcended geographically defined strata. The strongest sJIA-associated SNP, rs151043342 [ P = 2.8 × 10 −17 , odds ratio (OR) 2.6 (2.1, 3.3)], was part of a cluster of 482 sJIA-associated SNPs that spanned a 400-kb region and included the class II HLA region. Conditional analysis controlling for the effect of rs151043342 found that rs12722051 independently influenced sJIA risk [ P = 1.0 × 10 −5 , OR 0.7 (0.6, 0.8)]. Meta-analysis of imputed classic HLA-type associations in six study populations of Western European ancestry revealed that HLA-DRB1*11 and its defining amino acid residue, glutamate 58, were strongly associated with sJIA [ P = 2.7 × 10 −16 , OR 2.3 (1.9, 2.8)], as was the HLA-DRB1*11—HLA-DQA1*05—HLA-DQB1*03 haplotype [6.4 × 10 −17 , OR 2.3 (1.9, 2.9)]. By examining the MHC locus in the largest collection of sJIA patients assembled to date, this study solidifies the relationship between the class II HLA region and sJIA, implicating adaptive immune molecules in the pathogenesis of sJIA. |
| Author | Terri H. Finkel Bianca Bica Eileen Baildam Colleen Satorius Jordi Anton Lennox Holt Stanton Newman Paul Dancey Adam Huber Mark Friswell Randomized Placebo Phase Study of Rilonacept in sJIA (RAPPORT) Investigators Kevin Murray John F. Bohnsack Michael J. Ombrello Annette Duggan Katrin Burkle Carl D. Langefeld Yelda Bilginer David A. Cabral Janet Gardener-Medwin Stefan Berg Susan Thompson M. Hall Janet Ellsworth Soumya Raychaudhuri Ioanna Tachmazidou Alan Rosenberg Clive Ryder Suzanne Ramsey Elizabeth Baskin Pamela Whitworth Kirstin Minden Kelly Hadfield Andrew S. Zeft Joanne Buckley Alberto Martini Kristi Prather Halima Moncrieffe Shashi Hirani Gaëlle Chedeville David D. Sherry Elizabeth D. Mellins Jeffrey Chaitow Normal T. Ilowite Joel David Michele Gibbon Stephen W. Scherer Sharon Watson Laura E. Schanberg Rayfel Schneider Karen Watanabe Duffy Rosie Scuccimarri Ciaran Duffy Norman T. Ilowite Lucy R. Wedderburn Daniel L. Kastner Vikki Gould Helen Venning Kenneth M. Kaufman Marco Gattorno Ross Petty Lawrence S. Zemel Christy I. Sandborg Marta E. Al |
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Gaslini Institute, 16147 Genoa, Italy – sequence: 8 givenname: Marco surname: Gattorno fullname: Gattorno, Marco organization: Pediatrics II Unit, G. 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Universitat de Barcelona, Barcelona, Spain – sequence: 55 givenname: Elizabeth surname: Baskin fullname: Baskin, Elizabeth organization: Translational Genetics and Genomics Unit, National Institute of Arthritis Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892 – sequence: 56 givenname: Stefan surname: Berg fullname: Berg, Stefan organization: Queen Silvia Children’s Hospital, Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 57 givenname: Bianca surname: Bica fullname: Bica, Bianca organization: Hospital Universitário Clementino Fraga Filho, Rio de Janeiro, Brazil – sequence: 58 givenname: Yelda surname: Bilginer fullname: Bilginer, Yelda organization: Hacettepe University, Ankara, Turkey – sequence: 59 givenname: John F. surname: Bohnsack fullname: Bohnsack, John F. organization: University of Utah, Salt Lake City, UT 84112 – sequence: 60 givenname: Andre surname: Cavalcanti fullname: Cavalcanti, Andre organization: Universidade Federal de Pernambuco, Recife, PE, Brazil – sequence: 61 givenname: Jeffrey surname: Chaitow fullname: Chaitow, Jeffrey organization: Children’s Hospital Westmead, Westmead, New South Wales, Australia – sequence: 62 givenname: Joanna surname: Cobb fullname: Cobb, Joanna organization: Arthritis Research UK Centre for Genetics and Genomics, Centre for Musculoskeletal Research, Institute for Inflammation and Repair, Manchester Academic Health Science Centre, The University of Manchester, Manchester, U.K.;, NIHR Manchester Musculoskeletal Biomedical Research Unit, Central Manchester NHF Foundation Trust, Manchester Academic Health Centre, The University of Manchester, Manchester, U.K – sequence: 63 givenname: Rubin surname: Cuttica fullname: Cuttica, Rubin organization: Hospital General de Niños Pedro de Elizalde, Buenos Aires, Argentina – sequence: 64 givenname: Paul I. 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Ilyas surname: Kamboh fullname: Kamboh, M. 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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26598658$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article Web Resource |
| Contributor | Allen, Roger Quartier, Pierre Cook, Lucy Finkel, Terri H Prahalad, Sampath Chaitow, Jeffrey Remmers, Elaine F Kamboh, M Ilyas Hall, M Ozen, Seza Friel, Elizabeth Estivill, Xavier Park, Jane Pountain, Gillian Venning, Helen Buckley, Joanne Zeggini, Eleftheria Abinum, Mario Bell, A Friswell, Mark Mellins, Elizabeth D Singh-Gerwal, Davinder Han, Buhm Raychaudhuri, Soumya Schwarz, Tobias Docampo, Elisa Ellis, Justine Scherer, Stephen W Crawley, Esther Cuttica, Rubin Rosenberg, Alan Baskin, Elizabeth Jones, Stan Berg, Stefan Carrasco, Roberto Duerr, Richard Holt, Lennox Bishop, Nick Len, Claudio Griffin, Jane Achkar, J P Ryder, Clive Kastner, Daniel L Craft, Alan W Foster, Helen Bilginer, Yelda Yeung, Rae S M Minden, Kirstin Tachmazidou, Ioanna Wedderburn, Lucy R Oliveira, Sheila Woo, Patricia Eltringham, Michael Cobb, Joanna Gül, Ahmet Bohnsack, John F de Bakker, Paul I W Anton, Jordi Hollingworth, Peter Wyatt, Sue Brown, Lynsey Hakonarson, Hakon Murray, Kevin Bica, Bianca Ombrello, Michael J Schneider, Rayfel Hinks, Anne Alarcón-Riquelme, Marta E Foell, D |
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| Copyright | Copyright National Academy of Sciences Dec 29, 2015 |
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| Issue | 52 |
| Keywords | systemic juvenile idiopathic arthritis autoinflammation human leukocyte antigen Still’s disease |
| Language | English |
| License | Freely available online through the PNAS open access option. |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 scopus-id:2-s2.0-84952685055 Reviewers: J.v.d.M., Radboud University Nijmegen Medical Centre; and S.Y., Yokohama City University. Contributed by Daniel L. Kastner, October 21, 2015 (sent for review June 8, 2015; reviewed by Jos van der Meer and Shumpei Yokota) Author contributions: M.J.O., E.F.R., I.T., A. Grom, D.F., J.-P.H., A.M., M.G., S.Ö., S.P., A.S.Z., J.F.B., E.D.M., N.T.I., R.R., C.L., M.O.E.H., S.O., R.S.M.Y., A.R., L.R.W., J.A., T.S., A.H., Y.B., J.P., J.C., C.L.S., E.B., R.H.D., J.P.A., M.I.K., K.M.K., L.C.K., D.P., S.W.S., M.E.A.-R., E.D., X.E., A. Gül, BSPAR, CAPS, RAPPORT, CHARMS, BBOP, C.D.L., E.Z., W.T., D.L.K., P.W., and INCHARGE designed research; M.J.O., E.F.R., I.T., A. Grom, D.F., J.-P.H., A.M., M.G., S.Ö, S.P., A.S.Z., J.F.B., E.D.M., N.T.I., R.R., C.L., M.O.E.H., S.O., R.S.M.Y., A.R., L.R.W., J.A., T.S., Y.B., C.L.S., E.B., S.S., E.Z., W.T., D.L.K., and P.W. performed research; B.H., P.I.W.d.B., and S.R. contributed new reagents/analytic tools; M.J.O., E.F.R., I.T., A. Grom, A.M., M.G., S.Ö., E.D.M., R.S.M.Y., C.D.L., S.T., E.Z., W.T., D.L.K., and P.W. analyzed data; and M.J.O., E.F.R., A. Grom, M.G., S.Ö., J.F.B., E.D.M., R.R., R.S.M.Y., L.R.W., S.T., E.Z., W.T., D.L.K., and P.W. wrote the paper. |
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| References | Behrens EM (e_1_3_3_5_2) 2007; 34 Petty RE (e_1_3_3_1_2) 2004; 31 Trede NS (e_1_3_3_27_2) 1991; 146 e_1_3_3_17_2 e_1_3_3_16_2 Desaymard C (e_1_3_3_13_2) 1996; 63 e_1_3_3_19_2 e_1_3_3_18_2 e_1_3_3_12_2 e_1_3_3_15_2 e_1_3_3_14_2 e_1_3_3_10_2 e_1_3_3_6_2 Bedford PA (e_1_3_3_11_2) 1992; 10 e_1_3_3_8_2 e_1_3_3_7_2 e_1_3_3_9_2 e_1_3_3_24_2 e_1_3_3_23_2 e_1_3_3_26_2 e_1_3_3_25_2 e_1_3_3_2_2 e_1_3_3_20_2 e_1_3_3_4_2 e_1_3_3_22_2 e_1_3_3_3_2 e_1_3_3_21_2 26677874 - Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):15785-6. doi: 10.1073/pnas.1521837113. |
| References_xml | – volume: 34 start-page: 1133 year: 2007 ident: e_1_3_3_5_2 article-title: Occult macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis publication-title: J Rheumatol – ident: e_1_3_3_7_2 doi: 10.1016/S0140-6736(08)60998-8 – ident: e_1_3_3_14_2 doi: 10.1002/art.27424 – ident: e_1_3_3_16_2 doi: 10.1093/rheumatology/41.10.1183 – ident: e_1_3_3_21_2 doi: 10.1006/clin.1997.4457 – ident: e_1_3_3_12_2 doi: 10.1002/1529-0131(199912)42:12<2577::AID-ANR10>3.0.CO;2-O – ident: e_1_3_3_15_2 doi: 10.1002/art.1780280207 – ident: e_1_3_3_18_2 doi: 10.1002/art.38698 – volume: 10 start-page: 189 year: 1992 ident: e_1_3_3_11_2 article-title: Increased frequency of DR4 in systemic onset juvenile chronic arthritis publication-title: Clin Exp Rheumatol – ident: e_1_3_3_20_2 doi: 10.1038/nri1805 – ident: e_1_3_3_8_2 doi: 10.3899/jrheum.100726 – ident: e_1_3_3_9_2 doi: 10.1016/B978-1-4160-6581-4.10014-7 – ident: e_1_3_3_3_2 doi: 10.1016/j.autrev.2012.07.022 – ident: e_1_3_3_25_2 doi: 10.1182/blood-2003-01-0273 – ident: e_1_3_3_10_2 doi: 10.1016/j.jbspin.2013.09.003 – volume: 146 start-page: 2310 year: 1991 ident: e_1_3_3_27_2 article-title: Transcriptional activation of IL-1 beta and tumor necrosis factor-alpha genes by MHC class II ligands publication-title: J Immunol doi: 10.4049/jimmunol.146.7.2310 – ident: e_1_3_3_17_2 doi: 10.1038/nrrheum.2011.68 – ident: e_1_3_3_2_2 doi: 10.1038/ncprheum0084 – ident: e_1_3_3_26_2 doi: 10.1371/journal.pone.0015985 – ident: e_1_3_3_22_2 doi: 10.1093/rheumatology/kes162 – volume: 63 start-page: 9 year: 1996 ident: e_1_3_3_13_2 article-title: Major histocompatibility complex markers and disease heterogeneity in one hundred eight patients with systemic onset juvenile chronic arthritis publication-title: Rev Rhum Engl Ed – ident: e_1_3_3_23_2 doi: 10.1002/eji.200838992 – volume: 31 start-page: 390 year: 2004 ident: e_1_3_3_1_2 article-title: International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: Second revision, Edmonton, 2001 publication-title: J Rheumatol – ident: e_1_3_3_6_2 doi: 10.1002/art.23437 – ident: e_1_3_3_19_2 doi: 10.1002/art.33376 – ident: e_1_3_3_24_2 doi: 10.1038/ni.2015 – ident: e_1_3_3_4_2 doi: 10.1146/annurev-med-061813-012806 – reference: 26677874 - Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):15785-6. doi: 10.1073/pnas.1521837113. |
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| Snippet | To determine whether genetic variation within the MHC locus influences the risk of developing systemic juvenile idiopathic arthritis (sJIA), we examined a... Systemic juvenile idiopathic arthritis (sJIA) is an often severe, potentially life-threatening childhood inflammatory disease, the pathophysiology of which is... |
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| SubjectTerms | Amino acids Arthritis Arthritis, Juvenile - genetics autoinflammation Biological Sciences Child Gene Frequency Genes Genetic diversity Genetic Predisposition to Disease - genetics Genetics & genetic processes Genotype Genotypes Génétique & processus génétiques Haplotypes Histocompatibility Antigens Class II - genetics HLA-DRB1 Chains - genetics human leukocyte antigen Humans Life sciences Linkage Disequilibrium Meta-analysis Meta-Analysis as Topic Molecules Odds Ratio Pathogenesis Polymorphism, Single Nucleotide Risk Factors Sciences du vivant Still's disease systemic juvenile idiopathic arthritis |
| Title | HLA-DRB111 and variants of the MHC class II locus are strong risk factors for systemic juvenile idiopathic arthritis |
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