Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.

The phenotypic effect of some single nucleotide polymorphisms (SNPs) depends on their parental origin. We present a novel approach to detect parent-of-origin effects (POEs) in genome-wide genotype data of unrelated individuals. The method exploits increased phenotypic variance in the heterozygous ge...

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Main Authors: Clive J Hoggart, Giulia Venturini, Massimo Mangino, Felicia Gomez, Giulia Ascari, Jing Hua Zhao, Alexander Teumer, Thomas W Winkler, Natalia Tšernikova, Jian'an Luan, Evelin Mihailov, Georg B Ehret, Weihua Zhang, David Lamparter, Tõnu Esko, Aurelien Macé, Sina Rüeger, Pierre-Yves Bochud, Matteo Barcella, Yves Dauvilliers, Beben Benyamin, David M Evans, Caroline Hayward, Mary F Lopez, Lude Franke, Alessia Russo, Iris M Heid, Erika Salvi, Sailaja Vendantam, Dan E Arking, Eric Boerwinkle, John C Chambers, Giovanni Fiorito, Harald Grallert, Simonetta Guarrera, Georg Homuth, Jennifer E Huffman, David Porteous, Generation Scotland Consortium, LifeLines Cohort study, GIANT Consortium, Darius Moradpour, Alex Iranzo, Johannes Hebebrand, John P Kemp, Gert J Lammers, Vincent Aubert, Markus H Heim, Nicholas G Martin, Grant W Montgomery, Rosa Peraita-Adrados, Joan Santamaria, Francesco Negro, Carsten O Schmidt, Robert A Scott, Tim D Spector, Konstantin Strauch, Henry Völzke, Nicholas J Wareham, Wei Yuan, Jordana T Bell, Aravinda Chakravarti, Jaspal S Kooner, Annette Peters, Giuseppe Matullo, Henri Wallaschofski, John B Whitfield, Fred Paccaud, Peter Vollenweider, Sven Bergmann, Jacques S Beckmann, Mehdi Tafti, Nicholas D Hastie, Daniele Cusi, Murielle Bochud, Timothy M Frayling, Andres Metspalu, Marjo-Riitta Jarvelin, André Scherag, George Davey Smith, Ingrid B Borecki, Valentin Rousson, Joel N Hirschhorn, Carlo Rivolta, Ruth J F Loos, Zoltán Kutalik
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-07-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1004508
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author Clive J Hoggart
Giulia Venturini
Massimo Mangino
Felicia Gomez
Giulia Ascari
Jing Hua Zhao
Alexander Teumer
Thomas W Winkler
Natalia Tšernikova
Jian'an Luan
Evelin Mihailov
Georg B Ehret
Weihua Zhang
David Lamparter
Tõnu Esko
Aurelien Macé
Sina Rüeger
Pierre-Yves Bochud
Matteo Barcella
Yves Dauvilliers
Beben Benyamin
David M Evans
Caroline Hayward
Mary F Lopez
Lude Franke
Alessia Russo
Iris M Heid
Erika Salvi
Sailaja Vendantam
Dan E Arking
Eric Boerwinkle
John C Chambers
Giovanni Fiorito
Harald Grallert
Simonetta Guarrera
Georg Homuth
Jennifer E Huffman
David Porteous
Generation Scotland Consortium
LifeLines Cohort study
GIANT Consortium
Darius Moradpour
Alex Iranzo
Johannes Hebebrand
John P Kemp
Gert J Lammers
Vincent Aubert
Markus H Heim
Nicholas G Martin
Grant W Montgomery
Rosa Peraita-Adrados
Joan Santamaria
Francesco Negro
Carsten O Schmidt
Robert A Scott
Tim D Spector
Konstantin Strauch
Henry Völzke
Nicholas J Wareham
Wei Yuan
Jordana T Bell
Aravinda Chakravarti
Jaspal S Kooner
Annette Peters
Giuseppe Matullo
Henri Wallaschofski
John B Whitfield
Fred Paccaud
Peter Vollenweider
Sven Bergmann
Jacques S Beckmann
Mehdi Tafti
Nicholas D Hastie
Daniele Cusi
Murielle Bochud
Timothy M Frayling
Andres Metspalu
Marjo-Riitta Jarvelin
André Scherag
George Davey Smith
Ingrid B Borecki
Valentin Rousson
Joel N Hirschhorn
Carlo Rivolta
Ruth J F Loos
Zoltán Kutalik
author_facet Clive J Hoggart
Giulia Venturini
Massimo Mangino
Felicia Gomez
Giulia Ascari
Jing Hua Zhao
Alexander Teumer
Thomas W Winkler
Natalia Tšernikova
Jian'an Luan
Evelin Mihailov
Georg B Ehret
Weihua Zhang
David Lamparter
Tõnu Esko
Aurelien Macé
Sina Rüeger
Pierre-Yves Bochud
Matteo Barcella
Yves Dauvilliers
Beben Benyamin
David M Evans
Caroline Hayward
Mary F Lopez
Lude Franke
Alessia Russo
Iris M Heid
Erika Salvi
Sailaja Vendantam
Dan E Arking
Eric Boerwinkle
John C Chambers
Giovanni Fiorito
Harald Grallert
Simonetta Guarrera
Georg Homuth
Jennifer E Huffman
David Porteous
Generation Scotland Consortium
LifeLines Cohort study
GIANT Consortium
Darius Moradpour
Alex Iranzo
Johannes Hebebrand
John P Kemp
Gert J Lammers
Vincent Aubert
Markus H Heim
Nicholas G Martin
Grant W Montgomery
Rosa Peraita-Adrados
Joan Santamaria
Francesco Negro
Carsten O Schmidt
Robert A Scott
Tim D Spector
Konstantin Strauch
Henry Völzke
Nicholas J Wareham
Wei Yuan
Jordana T Bell
Aravinda Chakravarti
Jaspal S Kooner
Annette Peters
Giuseppe Matullo
Henri Wallaschofski
John B Whitfield
Fred Paccaud
Peter Vollenweider
Sven Bergmann
Jacques S Beckmann
Mehdi Tafti
Nicholas D Hastie
Daniele Cusi
Murielle Bochud
Timothy M Frayling
Andres Metspalu
Marjo-Riitta Jarvelin
André Scherag
George Davey Smith
Ingrid B Borecki
Valentin Rousson
Joel N Hirschhorn
Carlo Rivolta
Ruth J F Loos
Zoltán Kutalik
author_sort Clive J Hoggart
collection DOAJ
description The phenotypic effect of some single nucleotide polymorphisms (SNPs) depends on their parental origin. We present a novel approach to detect parent-of-origin effects (POEs) in genome-wide genotype data of unrelated individuals. The method exploits increased phenotypic variance in the heterozygous genotype group relative to the homozygous groups. We applied the method to >56,000 unrelated individuals to search for POEs influencing body mass index (BMI). Six lead SNPs were carried forward for replication in five family-based studies (of ∼4,000 trios). Two SNPs replicated: the paternal rs2471083-C allele (located near the imprinted KCNK9 gene) and the paternal rs3091869-T allele (located near the SLC2A10 gene) increased BMI equally (beta = 0.11 (SD), P<0.0027) compared to the respective maternal alleles. Real-time PCR experiments of lymphoblastoid cell lines from the CEPH families showed that expression of both genes was dependent on parental origin of the SNPs alleles (P<0.01). Our scheme opens new opportunities to exploit GWAS data of unrelated individuals to identify POEs and demonstrates that they play an important role in adult obesity.
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publisher Public Library of Science (PLoS)
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series PLoS Genetics
spelling doaj-art-6b5ebe329cc640c482a2dc731b70d7f42025-08-20T03:46:43ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042014-07-01107e100450810.1371/journal.pgen.1004508Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.Clive J HoggartGiulia VenturiniMassimo ManginoFelicia GomezGiulia AscariJing Hua ZhaoAlexander TeumerThomas W WinklerNatalia TšernikovaJian'an LuanEvelin MihailovGeorg B EhretWeihua ZhangDavid LamparterTõnu EskoAurelien MacéSina RüegerPierre-Yves BochudMatteo BarcellaYves DauvilliersBeben BenyaminDavid M EvansCaroline HaywardMary F LopezLude FrankeAlessia RussoIris M HeidErika SalviSailaja VendantamDan E ArkingEric BoerwinkleJohn C ChambersGiovanni FioritoHarald GrallertSimonetta GuarreraGeorg HomuthJennifer E HuffmanDavid PorteousGeneration Scotland ConsortiumLifeLines Cohort studyGIANT ConsortiumDarius MoradpourAlex IranzoJohannes HebebrandJohn P KempGert J LammersVincent AubertMarkus H HeimNicholas G MartinGrant W MontgomeryRosa Peraita-AdradosJoan SantamariaFrancesco NegroCarsten O SchmidtRobert A ScottTim D SpectorKonstantin StrauchHenry VölzkeNicholas J WarehamWei YuanJordana T BellAravinda ChakravartiJaspal S KoonerAnnette PetersGiuseppe MatulloHenri WallaschofskiJohn B WhitfieldFred PaccaudPeter VollenweiderSven BergmannJacques S BeckmannMehdi TaftiNicholas D HastieDaniele CusiMurielle BochudTimothy M FraylingAndres MetspaluMarjo-Riitta JarvelinAndré ScheragGeorge Davey SmithIngrid B BoreckiValentin RoussonJoel N HirschhornCarlo RivoltaRuth J F LoosZoltán KutalikThe phenotypic effect of some single nucleotide polymorphisms (SNPs) depends on their parental origin. We present a novel approach to detect parent-of-origin effects (POEs) in genome-wide genotype data of unrelated individuals. The method exploits increased phenotypic variance in the heterozygous genotype group relative to the homozygous groups. We applied the method to >56,000 unrelated individuals to search for POEs influencing body mass index (BMI). Six lead SNPs were carried forward for replication in five family-based studies (of ∼4,000 trios). Two SNPs replicated: the paternal rs2471083-C allele (located near the imprinted KCNK9 gene) and the paternal rs3091869-T allele (located near the SLC2A10 gene) increased BMI equally (beta = 0.11 (SD), P<0.0027) compared to the respective maternal alleles. Real-time PCR experiments of lymphoblastoid cell lines from the CEPH families showed that expression of both genes was dependent on parental origin of the SNPs alleles (P<0.01). Our scheme opens new opportunities to exploit GWAS data of unrelated individuals to identify POEs and demonstrates that they play an important role in adult obesity.https://doi.org/10.1371/journal.pgen.1004508
spellingShingle Clive J Hoggart
Giulia Venturini
Massimo Mangino
Felicia Gomez
Giulia Ascari
Jing Hua Zhao
Alexander Teumer
Thomas W Winkler
Natalia Tšernikova
Jian'an Luan
Evelin Mihailov
Georg B Ehret
Weihua Zhang
David Lamparter
Tõnu Esko
Aurelien Macé
Sina Rüeger
Pierre-Yves Bochud
Matteo Barcella
Yves Dauvilliers
Beben Benyamin
David M Evans
Caroline Hayward
Mary F Lopez
Lude Franke
Alessia Russo
Iris M Heid
Erika Salvi
Sailaja Vendantam
Dan E Arking
Eric Boerwinkle
John C Chambers
Giovanni Fiorito
Harald Grallert
Simonetta Guarrera
Georg Homuth
Jennifer E Huffman
David Porteous
Generation Scotland Consortium
LifeLines Cohort study
GIANT Consortium
Darius Moradpour
Alex Iranzo
Johannes Hebebrand
John P Kemp
Gert J Lammers
Vincent Aubert
Markus H Heim
Nicholas G Martin
Grant W Montgomery
Rosa Peraita-Adrados
Joan Santamaria
Francesco Negro
Carsten O Schmidt
Robert A Scott
Tim D Spector
Konstantin Strauch
Henry Völzke
Nicholas J Wareham
Wei Yuan
Jordana T Bell
Aravinda Chakravarti
Jaspal S Kooner
Annette Peters
Giuseppe Matullo
Henri Wallaschofski
John B Whitfield
Fred Paccaud
Peter Vollenweider
Sven Bergmann
Jacques S Beckmann
Mehdi Tafti
Nicholas D Hastie
Daniele Cusi
Murielle Bochud
Timothy M Frayling
Andres Metspalu
Marjo-Riitta Jarvelin
André Scherag
George Davey Smith
Ingrid B Borecki
Valentin Rousson
Joel N Hirschhorn
Carlo Rivolta
Ruth J F Loos
Zoltán Kutalik
Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.
PLoS Genetics
title Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.
title_full Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.
title_fullStr Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.
title_full_unstemmed Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.
title_short Novel approach identifies SNPs in SLC2A10 and KCNK9 with evidence for parent-of-origin effect on body mass index.
title_sort novel approach identifies snps in slc2a10 and kcnk9 with evidence for parent of origin effect on body mass index
url https://doi.org/10.1371/journal.pgen.1004508
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