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PMID: 23698362 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Negligible impact of rare autoimmune-locus coding-region variants on missing heritability.

Nature ·Vol. 498 ·No. 7453 ·2013-06-13 ·Pages 232-5

Hunt KA, Mistry V, Bockett NA, Ahmad T, Ban M, Barker JN, Barrett JC, Blackburn H, Brand O, Burren O, Capon F, Compston A, Gough SC, Jostins L, Kong Y, Lee JC, Lek M, MacArthur DG, Mansfield JC, Mathew CG, Mein CA, Mirza M, Nutland S, Onengut-Gumuscu S, Papouli E, Parkes M, Rich SS, Sawcer S, Satsangi J, Simmonds MJ, Trembath RC, Walker NM, Wozniak E, Todd JA, Simpson MA, Plagnol V, van Heel DA

Abstract

Genome-wide association studies (GWAS) have identified common variants of modest-effect size at hundreds of loci for common autoimmune diseases; however, a substantial fraction of heritability remains unexplained, to which rare variants may contribute. To discover rare variants and test them for association with a phenotype, most studies re-sequence a small initial sample size and then genotype the discovered variants in a larger sample set. This approach fails to analyse a large fraction of the rare variants present in the entire sample set. Here we perform simultaneous amplicon-sequencing-based variant discovery and genotyping for coding exons of 25 GWAS risk genes in 41,911 UK residents of white European origin, comprising 24,892 subjects with six autoimmune disease phenotypes and 17,019 controls, and show that rare coding-region variants at known loci have a negligible role in common autoimmune disease susceptibility. These results do not support the rare-variant synthetic genome-wide-association hypothesis (in which unobserved rare causal variants lead to association detected at common tag variants). Many known autoimmune disease risk loci contain multiple, independently associated, common and low-frequency variants, and so genes at these loci are a priori stronger candidates for harbouring rare coding-region variants than other genes. Our data indicate that the missing heritability for common autoimmune diseases may not be attributable to the rare coding-region variant portion of the allelic spectrum, but perhaps, as others have proposed, may be a result of many common-variant loci of weak effect.

MeSH Terms
Autoimmune Diseases/genetics Exons/genetics Gene Frequency Genetic Predisposition to Disease/genetics Genetic Variation/genetics Genome-Wide Association Study Humans Models, Genetic Mutation/genetics Open Reading Frames/genetics Phenotype Sample Size United Kingdom Whites/genetics
Authors & Affiliations
37 authors, click to expand affiliations / ORCID
Hunt Karen A
Blizard Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London E1 2AT, UK.
Mistry Vanisha
Bockett Nicholas A
Ahmad Tariq
Ban Maria
Barker Jonathan N
Barrett Jeffrey C
Blackburn Hannah
Brand Oliver
Burren Oliver
Capon Francesca
Compston Alastair
Gough Stephen C L
Jostins Luke
Kong Yong
Lee James C
Lek Monkol
MacArthur Daniel G
Mansfield John C
Mathew Christopher G
Mein Charles A
Mirza Muddassar
Nutland Sarah
Onengut-Gumuscu Suna
Papouli Efterpi
Parkes Miles
Rich Stephen S
Sawcer Steven
Satsangi Jack
Simmonds Matthew J
Trembath Richard C
Walker Neil M
Wozniak Eva
Todd John A
Simpson Michael A
Plagnol Vincent
van Heel David A
References (30)
30 references, click to expand
  1. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease.
    Nature. 2012 Nov 1;491(7422):119-24 PMID: 23128233
  2. An abundance of rare functional variants in 202 drug target genes sequenced in 14,002 people.
    Science. 2012 Jul 6;337(6090):100-4 PMID: 22604722
  3. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes.
    Nat Genet. 2009 Jun;41(6):703-7 PMID: 19430480
  4. Bayesian inference analyses of the polygenic architecture of rheumatoid arthritis.
    Nat Genet. 2012 Mar 25;44(5):483-9 PMID: 22446960
  5. Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity.
    Nat Genet. 2012 Dec;44(12):1341-8 PMID: 23143594
  6. Finding the sources of missing heritability in a yeast cross.
    Nature. 2013 Feb 14;494(7436):234-7 PMID: 23376951
  7. Lupus-associated causal mutation in neutrophil cytosolic factor 2 (NCF2) brings unique insights to the structure and function of NADPH oxidase.
    Proc Natl Acad Sci U S A. 2012 Jan 10;109(2):E59-67 PMID: 22203994
  8. Rare and common variants in CARD14, encoding an epidermal regulator of NF-kappaB, in psoriasis.
    Am J Hum Genet. 2012 May 4;90(5):796-808 PMID: 22521419
  9. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis.
    Nature. 2011 Aug 10;476(7359):214-9 PMID: 21833088
  10. Dense genotyping identifies and localizes multiple common and rare variant association signals in celiac disease.
    Nat Genet. 2011 Nov 06;43(12):1193-201 PMID: 22057235
  11. Resequencing of positional candidates identifies low frequency IL23R coding variants protecting against inflammatory bowel disease.
    Nat Genet. 2011 Jan;43(1):43-7 PMID: 21151126
  12. Rare and common variants: twenty arguments.
    Nat Rev Genet. 2012 Jan 18;13(2):135-45 PMID: 22251874
  13. Common SNPs explain a large proportion of the heritability for human height.
    Nat Genet. 2010 Jul;42(7):565-9 PMID: 20562875
  14. Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes.
    Science. 2009 Apr 17;324(5925):387-9 PMID: 19264985
  15. Cell-specific protein phenotypes for the autoimmune locus IL2RA using a genotype-selectable human bioresource.
    Nat Genet. 2009 Sep;41(9):1011-5 PMID: 19701192
  16. Estimation of effect size distribution from genome-wide association studies and implications for future discoveries.
    Nat Genet. 2010 Jul;42(7):570-5 PMID: 20562874
  17. Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease.
    Nat Genet. 2011 Oct 09;43(11):1066-73 PMID: 21983784
  18. Estimating genetic effects and quantifying missing heritability explained by identified rare-variant associations.
    Am J Hum Genet. 2012 Oct 5;91(4):585-96 PMID: 23022102
  19. Neutrophil recruitment and function in health and inflammation.
    Nat Rev Immunol. 2013 Mar;13(3):159-75 PMID: 23435331
  20. Rare, low-frequency, and common variants in the protein-coding sequence of biological candidate genes from GWASs contribute to risk of rheumatoid arthritis.
    Am J Hum Genet. 2013 Jan 10;92(1):15-27 PMID: 23261300
  21. Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies.
    Genomics. 2011 Aug;98(2):152-3 PMID: 21651976
  22. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1.
    Nat Genet. 2010 Nov;42(11):985-90 PMID: 20953190
  23. Seven newly identified loci for autoimmune thyroid disease.
    Hum Mol Genet. 2012 Dec 1;21(23):5202-8 PMID: 22922229
  24. Deep resequencing reveals excess rare recent variants consistent with explosive population growth.
    Nat Commun. 2010 Nov 30;1:131 PMID: 21119644
  25. CARD15/NOD2 mutational analysis and genotype-phenotype correlation in 612 patients with inflammatory bowel disease.
    Am J Hum Genet. 2002 Apr;70(4):845-57 PMID: 11875755
  26. A systematic survey of loss-of-function variants in human protein-coding genes.
    Science. 2012 Feb 17;335(6070):823-8 PMID: 22344438
  27. Evolution and functional impact of rare coding variation from deep sequencing of human exomes.
    Science. 2012 Jul 6;337(6090):64-9 PMID: 22604720
  28. Finding the missing heritability of complex diseases.
    Nature. 2009 Oct 8;461(7265):747-53 PMID: 19812666
  29. Analysis of 6,515 exomes reveals the recent origin of most human protein-coding variants.
    Nature. 2013 Jan 10;493(7431):216-20 PMID: 23201682
  30. Rare variants create synthetic genome-wide associations.
    PLoS Biol. 2010 Jan 26;8(1):e1000294 PMID: 20126254
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2013-06-13
Epub
2013-00-22
Pages
232-5
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3736321
Subset
IM
Grants
Wellcome Trust · 068181 · United Kingdom
Wellcome Trust · 068545/Z/02 · United Kingdom
Wellcome Trust · WT061858 · United Kingdom
Medical Research Council · G1001158 · United Kingdom
Chief Scientist Office · ETM/137 · United Kingdom
Medical Research Council · G0000934 · United Kingdom
Wellcome Trust · 076113/C/04/Z · United Kingdom
Wellcome Trust · 091157 · United Kingdom
Wellcome Trust · 100140 · United Kingdom
Medical Research Council · G0800759 · United Kingdom
Chief Scientist Office · ETM/75 · United Kingdom
Chief Scientist Office · CZB/4/540 · United Kingdom
Medical Research Council · G0601387 · United Kingdom
Medical Research Council · G1001158(95979) · United Kingdom
Medical Research Council · G0800675 · United Kingdom
Medical Research Council · G0600329 · United Kingdom
Wellcome Trust · JDRF 4-2001-1008 · United Kingdom
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