Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.

The limited ability of common variants to account for the genetic contribution to complex disease has prompted searches for rare variants of large effect, to partly explain the 'missing heritability'. Analyses of genome-wide genotyping data have identified genomic structural variants (GSVs...

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Main Authors: Robin G Walters, Lachlan J M Coin, Aimo Ruokonen, Adam J de Smith, Julia S El-Sayed Moustafa, Sebastien Jacquemont, Paul Elliott, Tõnu Esko, Anna-Liisa Hartikainen, Jaana Laitinen, Katrin Männik, Danielle Martinet, David Meyre, Matthias Nauck, Claudia Schurmann, Rob Sladek, Gudmar Thorleifsson, Unnur Thorsteinsdóttir, Armand Valsesia, Gerard Waeber, Flore Zufferey, Beverley Balkau, François Pattou, Andres Metspalu, Henry Völzke, Peter Vollenweider, Kári Stefansson, Marjo-Riitta Järvelin, Jacques S Beckmann, Philippe Froguel, Alexandra I F Blakemore
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0058048&type=printable
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author Robin G Walters
Lachlan J M Coin
Aimo Ruokonen
Adam J de Smith
Julia S El-Sayed Moustafa
Sebastien Jacquemont
Paul Elliott
Tõnu Esko
Anna-Liisa Hartikainen
Jaana Laitinen
Katrin Männik
Danielle Martinet
David Meyre
Matthias Nauck
Claudia Schurmann
Rob Sladek
Gudmar Thorleifsson
Unnur Thorsteinsdóttir
Armand Valsesia
Gerard Waeber
Flore Zufferey
Beverley Balkau
François Pattou
Andres Metspalu
Henry Völzke
Peter Vollenweider
Kári Stefansson
Marjo-Riitta Järvelin
Jacques S Beckmann
Philippe Froguel
Alexandra I F Blakemore
author_facet Robin G Walters
Lachlan J M Coin
Aimo Ruokonen
Adam J de Smith
Julia S El-Sayed Moustafa
Sebastien Jacquemont
Paul Elliott
Tõnu Esko
Anna-Liisa Hartikainen
Jaana Laitinen
Katrin Männik
Danielle Martinet
David Meyre
Matthias Nauck
Claudia Schurmann
Rob Sladek
Gudmar Thorleifsson
Unnur Thorsteinsdóttir
Armand Valsesia
Gerard Waeber
Flore Zufferey
Beverley Balkau
François Pattou
Andres Metspalu
Henry Völzke
Peter Vollenweider
Kári Stefansson
Marjo-Riitta Järvelin
Jacques S Beckmann
Philippe Froguel
Alexandra I F Blakemore
author_sort Robin G Walters
collection DOAJ
description The limited ability of common variants to account for the genetic contribution to complex disease has prompted searches for rare variants of large effect, to partly explain the 'missing heritability'. Analyses of genome-wide genotyping data have identified genomic structural variants (GSVs) as a source of such rare causal variants. Recent studies have reported multiple GSV loci associated with risk of obesity. We attempted to replicate these associations by similar analysis of two familial-obesity case-control cohorts and a population cohort, and detected GSVs at 11 out of 18 loci, at frequencies similar to those previously reported. Based on their reported frequencies and effect sizes (OR≥25), we had sufficient statistical power to detect the large majority (80%) of genuine associations at these loci. However, only one obesity association was replicated. Deletion of a 220 kb region on chromosome 16p11.2 has a carrier population frequency of 2×10(-4) (95% confidence interval [9.6×10(-5)-3.1×10(-4)]); accounts overall for 0.5% [0.19%-0.82%] of severe childhood obesity cases (P = 3.8×10(-10); odds ratio = 25.0 [9.9-60.6]); and results in a mean body mass index (BMI) increase of 5.8 kg.m(-2) [1.8-10.3] in adults from the general population. We also attempted replication using BMI as a quantitative trait in our population cohort; associations with BMI at or near nominal significance were detected at two further loci near KIF2B and within FOXP2, but these did not survive correction for multiple testing. These findings emphasise several issues of importance when conducting rare GSV association, including the need for careful cohort selection and replication strategy, accurate GSV identification, and appropriate correction for multiple testing and/or control of false discovery rate. Moreover, they highlight the potential difficulty in replicating rare CNV associations across different populations. Nevertheless, we show that such studies are potentially valuable for the identification of variants making an appreciable contribution to complex disease.
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spelling doaj-art-b391834b6bdd459fa5a7a4d8da996c622025-08-20T03:25:08ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0183e5804810.1371/journal.pone.0058048Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.Robin G WaltersLachlan J M CoinAimo RuokonenAdam J de SmithJulia S El-Sayed MoustafaSebastien JacquemontPaul ElliottTõnu EskoAnna-Liisa HartikainenJaana LaitinenKatrin MännikDanielle MartinetDavid MeyreMatthias NauckClaudia SchurmannRob SladekGudmar ThorleifssonUnnur ThorsteinsdóttirArmand ValsesiaGerard WaeberFlore ZuffereyBeverley BalkauFrançois PattouAndres MetspaluHenry VölzkePeter VollenweiderKári StefanssonMarjo-Riitta JärvelinJacques S BeckmannPhilippe FroguelAlexandra I F BlakemoreThe limited ability of common variants to account for the genetic contribution to complex disease has prompted searches for rare variants of large effect, to partly explain the 'missing heritability'. Analyses of genome-wide genotyping data have identified genomic structural variants (GSVs) as a source of such rare causal variants. Recent studies have reported multiple GSV loci associated with risk of obesity. We attempted to replicate these associations by similar analysis of two familial-obesity case-control cohorts and a population cohort, and detected GSVs at 11 out of 18 loci, at frequencies similar to those previously reported. Based on their reported frequencies and effect sizes (OR≥25), we had sufficient statistical power to detect the large majority (80%) of genuine associations at these loci. However, only one obesity association was replicated. Deletion of a 220 kb region on chromosome 16p11.2 has a carrier population frequency of 2×10(-4) (95% confidence interval [9.6×10(-5)-3.1×10(-4)]); accounts overall for 0.5% [0.19%-0.82%] of severe childhood obesity cases (P = 3.8×10(-10); odds ratio = 25.0 [9.9-60.6]); and results in a mean body mass index (BMI) increase of 5.8 kg.m(-2) [1.8-10.3] in adults from the general population. We also attempted replication using BMI as a quantitative trait in our population cohort; associations with BMI at or near nominal significance were detected at two further loci near KIF2B and within FOXP2, but these did not survive correction for multiple testing. These findings emphasise several issues of importance when conducting rare GSV association, including the need for careful cohort selection and replication strategy, accurate GSV identification, and appropriate correction for multiple testing and/or control of false discovery rate. Moreover, they highlight the potential difficulty in replicating rare CNV associations across different populations. Nevertheless, we show that such studies are potentially valuable for the identification of variants making an appreciable contribution to complex disease.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0058048&type=printable
spellingShingle Robin G Walters
Lachlan J M Coin
Aimo Ruokonen
Adam J de Smith
Julia S El-Sayed Moustafa
Sebastien Jacquemont
Paul Elliott
Tõnu Esko
Anna-Liisa Hartikainen
Jaana Laitinen
Katrin Männik
Danielle Martinet
David Meyre
Matthias Nauck
Claudia Schurmann
Rob Sladek
Gudmar Thorleifsson
Unnur Thorsteinsdóttir
Armand Valsesia
Gerard Waeber
Flore Zufferey
Beverley Balkau
François Pattou
Andres Metspalu
Henry Völzke
Peter Vollenweider
Kári Stefansson
Marjo-Riitta Järvelin
Jacques S Beckmann
Philippe Froguel
Alexandra I F Blakemore
Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.
PLoS ONE
title Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.
title_full Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.
title_fullStr Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.
title_full_unstemmed Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.
title_short Rare genomic structural variants in complex disease: lessons from the replication of associations with obesity.
title_sort rare genomic structural variants in complex disease lessons from the replication of associations with obesity
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0058048&type=printable
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