Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.

Genome-wide association studies (GWAS) have identified 14 tagging single nucleotide polymorphisms (tagSNPs) that are associated with the risk of colorectal cancer (CRC), and several of these tagSNPs are near bone morphogenetic protein (BMP) pathway loci. The penalty of multiple testing implicit in G...

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Main Authors: Ian P M Tomlinson, Luis G Carvajal-Carmona, Sara E Dobbins, Albert Tenesa, Angela M Jones, Kimberley Howarth, Claire Palles, Peter Broderick, Emma E M Jaeger, Susan Farrington, Annabelle Lewis, James G D Prendergast, Alan M Pittman, Evropi Theodoratou, Bianca Olver, Marion Walker, Steven Penegar, Ella Barclay, Nicola Whiffin, Lynn Martin, Stephane Ballereau, Amy Lloyd, Maggie Gorman, Steven Lubbe, COGENT Consortium, CORGI Collaborators, EPICOLON Consortium, Bryan Howie, Jonathan Marchini, Clara Ruiz-Ponte, Ceres Fernandez-Rozadilla, Antoni Castells, Angel Carracedo, Sergi Castellvi-Bel, David Duggan, David Conti, Jean-Baptiste Cazier, Harry Campbell, Oliver Sieber, Lara Lipton, Peter Gibbs, Nicholas G Martin, Grant W Montgomery, Joanne Young, Paul N Baird, Steven Gallinger, Polly Newcomb, John Hopper, Mark A Jenkins, Lauri A Aaltonen, David J Kerr, Jeremy Cheadle, Paul Pharoah, Graham Casey, Richard S Houlston, Malcolm G Dunlop
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-06-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1002105
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author Ian P M Tomlinson
Luis G Carvajal-Carmona
Sara E Dobbins
Albert Tenesa
Angela M Jones
Kimberley Howarth
Claire Palles
Peter Broderick
Emma E M Jaeger
Susan Farrington
Annabelle Lewis
James G D Prendergast
Alan M Pittman
Evropi Theodoratou
Bianca Olver
Marion Walker
Steven Penegar
Ella Barclay
Nicola Whiffin
Lynn Martin
Stephane Ballereau
Amy Lloyd
Maggie Gorman
Steven Lubbe
COGENT Consortium
CORGI Collaborators
EPICOLON Consortium
Bryan Howie
Jonathan Marchini
Clara Ruiz-Ponte
Ceres Fernandez-Rozadilla
Antoni Castells
Angel Carracedo
Sergi Castellvi-Bel
David Duggan
David Conti
Jean-Baptiste Cazier
Harry Campbell
Oliver Sieber
Lara Lipton
Peter Gibbs
Nicholas G Martin
Grant W Montgomery
Joanne Young
Paul N Baird
Steven Gallinger
Polly Newcomb
John Hopper
Mark A Jenkins
Lauri A Aaltonen
David J Kerr
Jeremy Cheadle
Paul Pharoah
Graham Casey
Richard S Houlston
Malcolm G Dunlop
author_facet Ian P M Tomlinson
Luis G Carvajal-Carmona
Sara E Dobbins
Albert Tenesa
Angela M Jones
Kimberley Howarth
Claire Palles
Peter Broderick
Emma E M Jaeger
Susan Farrington
Annabelle Lewis
James G D Prendergast
Alan M Pittman
Evropi Theodoratou
Bianca Olver
Marion Walker
Steven Penegar
Ella Barclay
Nicola Whiffin
Lynn Martin
Stephane Ballereau
Amy Lloyd
Maggie Gorman
Steven Lubbe
COGENT Consortium
CORGI Collaborators
EPICOLON Consortium
Bryan Howie
Jonathan Marchini
Clara Ruiz-Ponte
Ceres Fernandez-Rozadilla
Antoni Castells
Angel Carracedo
Sergi Castellvi-Bel
David Duggan
David Conti
Jean-Baptiste Cazier
Harry Campbell
Oliver Sieber
Lara Lipton
Peter Gibbs
Nicholas G Martin
Grant W Montgomery
Joanne Young
Paul N Baird
Steven Gallinger
Polly Newcomb
John Hopper
Mark A Jenkins
Lauri A Aaltonen
David J Kerr
Jeremy Cheadle
Paul Pharoah
Graham Casey
Richard S Houlston
Malcolm G Dunlop
author_sort Ian P M Tomlinson
collection DOAJ
description Genome-wide association studies (GWAS) have identified 14 tagging single nucleotide polymorphisms (tagSNPs) that are associated with the risk of colorectal cancer (CRC), and several of these tagSNPs are near bone morphogenetic protein (BMP) pathway loci. The penalty of multiple testing implicit in GWAS increases the attraction of complementary approaches for disease gene discovery, including candidate gene- or pathway-based analyses. The strongest candidate loci for additional predisposition SNPs are arguably those already known both to have functional relevance and to be involved in disease risk. To investigate this proposition, we searched for novel CRC susceptibility variants close to the BMP pathway genes GREM1 (15q13.3), BMP4 (14q22.2), and BMP2 (20p12.3) using sample sets totalling 24,910 CRC cases and 26,275 controls. We identified new, independent CRC predisposition SNPs close to BMP4 (rs1957636, P = 3.93×10(-10)) and BMP2 (rs4813802, P = 4.65×10(-11)). Near GREM1, we found using fine-mapping that the previously-identified association between tagSNP rs4779584 and CRC actually resulted from two independent signals represented by rs16969681 (P = 5.33×10(-8)) and rs11632715 (P = 2.30×10(-10)). As low-penetrance predisposition variants become harder to identify-owing to small effect sizes and/or low risk allele frequencies-approaches based on informed candidate gene selection may become increasingly attractive. Our data emphasise that genetic fine-mapping studies can deconvolute associations that have arisen owing to independent correlation of a tagSNP with more than one functional SNP, thus explaining some of the apparently missing heritability of common diseases.
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spelling doaj-art-c10c8a90b2ce4383b4aa02c682b347282025-08-20T03:10:22ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042011-06-0176e100210510.1371/journal.pgen.1002105Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.Ian P M TomlinsonLuis G Carvajal-CarmonaSara E DobbinsAlbert TenesaAngela M JonesKimberley HowarthClaire PallesPeter BroderickEmma E M JaegerSusan FarringtonAnnabelle LewisJames G D PrendergastAlan M PittmanEvropi TheodoratouBianca OlverMarion WalkerSteven PenegarElla BarclayNicola WhiffinLynn MartinStephane BallereauAmy LloydMaggie GormanSteven LubbeCOGENT ConsortiumCORGI CollaboratorsEPICOLON ConsortiumBryan HowieJonathan MarchiniClara Ruiz-PonteCeres Fernandez-RozadillaAntoni CastellsAngel CarracedoSergi Castellvi-BelDavid DugganDavid ContiJean-Baptiste CazierHarry CampbellOliver SieberLara LiptonPeter GibbsNicholas G MartinGrant W MontgomeryJoanne YoungPaul N BairdSteven GallingerPolly NewcombJohn HopperMark A JenkinsLauri A AaltonenDavid J KerrJeremy CheadlePaul PharoahGraham CaseyRichard S HoulstonMalcolm G DunlopGenome-wide association studies (GWAS) have identified 14 tagging single nucleotide polymorphisms (tagSNPs) that are associated with the risk of colorectal cancer (CRC), and several of these tagSNPs are near bone morphogenetic protein (BMP) pathway loci. The penalty of multiple testing implicit in GWAS increases the attraction of complementary approaches for disease gene discovery, including candidate gene- or pathway-based analyses. The strongest candidate loci for additional predisposition SNPs are arguably those already known both to have functional relevance and to be involved in disease risk. To investigate this proposition, we searched for novel CRC susceptibility variants close to the BMP pathway genes GREM1 (15q13.3), BMP4 (14q22.2), and BMP2 (20p12.3) using sample sets totalling 24,910 CRC cases and 26,275 controls. We identified new, independent CRC predisposition SNPs close to BMP4 (rs1957636, P = 3.93×10(-10)) and BMP2 (rs4813802, P = 4.65×10(-11)). Near GREM1, we found using fine-mapping that the previously-identified association between tagSNP rs4779584 and CRC actually resulted from two independent signals represented by rs16969681 (P = 5.33×10(-8)) and rs11632715 (P = 2.30×10(-10)). As low-penetrance predisposition variants become harder to identify-owing to small effect sizes and/or low risk allele frequencies-approaches based on informed candidate gene selection may become increasingly attractive. Our data emphasise that genetic fine-mapping studies can deconvolute associations that have arisen owing to independent correlation of a tagSNP with more than one functional SNP, thus explaining some of the apparently missing heritability of common diseases.https://doi.org/10.1371/journal.pgen.1002105
spellingShingle Ian P M Tomlinson
Luis G Carvajal-Carmona
Sara E Dobbins
Albert Tenesa
Angela M Jones
Kimberley Howarth
Claire Palles
Peter Broderick
Emma E M Jaeger
Susan Farrington
Annabelle Lewis
James G D Prendergast
Alan M Pittman
Evropi Theodoratou
Bianca Olver
Marion Walker
Steven Penegar
Ella Barclay
Nicola Whiffin
Lynn Martin
Stephane Ballereau
Amy Lloyd
Maggie Gorman
Steven Lubbe
COGENT Consortium
CORGI Collaborators
EPICOLON Consortium
Bryan Howie
Jonathan Marchini
Clara Ruiz-Ponte
Ceres Fernandez-Rozadilla
Antoni Castells
Angel Carracedo
Sergi Castellvi-Bel
David Duggan
David Conti
Jean-Baptiste Cazier
Harry Campbell
Oliver Sieber
Lara Lipton
Peter Gibbs
Nicholas G Martin
Grant W Montgomery
Joanne Young
Paul N Baird
Steven Gallinger
Polly Newcomb
John Hopper
Mark A Jenkins
Lauri A Aaltonen
David J Kerr
Jeremy Cheadle
Paul Pharoah
Graham Casey
Richard S Houlston
Malcolm G Dunlop
Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.
PLoS Genetics
title Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.
title_full Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.
title_fullStr Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.
title_full_unstemmed Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.
title_short Multiple common susceptibility variants near BMP pathway loci GREM1, BMP4, and BMP2 explain part of the missing heritability of colorectal cancer.
title_sort multiple common susceptibility variants near bmp pathway loci grem1 bmp4 and bmp2 explain part of the missing heritability of colorectal cancer
url https://doi.org/10.1371/journal.pgen.1002105
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