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Breast Cancer Research
Published in: Breast Cancer Research 1/2016

Open Access 01-12-2016 | Research article

Identification of independent association signals and putative functional variants for breast cancer risk through fine-scale mapping of the 12p11 locus

Authors: Chenjie Zeng, Xingyi Guo, Jirong Long, Karoline B. Kuchenbaecker, Arnaud Droit, Kyriaki Michailidou, Maya Ghoussaini, Siddhartha Kar, Adam Freeman, John L. Hopper, Roger L. Milne, Manjeet K. Bolla, Qin Wang, Joe Dennis, Simona Agata, Shahana Ahmed, Kristiina Aittomäki, Irene L. Andrulis, Hoda Anton-Culver, Natalia N. Antonenkova, Adalgeir Arason, Volker Arndt, Banu K. Arun, Brita Arver, Francois Bacot, Daniel Barrowdale, Caroline Baynes, Alicia Beeghly-Fadiel, Javier Benitez, Marina Bermisheva, Carl Blomqvist, William J. Blot, Natalia V. Bogdanova, Stig E. Bojesen, Bernardo Bonanni, Anne-Lise Borresen-Dale, Judith S. Brand, Hiltrud Brauch, Paul Brennan, Hermann Brenner, Annegien Broeks, Thomas Brüning, Barbara Burwinkel, Saundra S. Buys, Qiuyin Cai, Trinidad Caldes, Ian Campbell, Jane Carpenter, Jenny Chang-Claude, Ji-Yeob Choi, Kathleen B. M. Claes, Christine Clarke, Angela Cox, Simon S. Cross, Kamila Czene, Mary B. Daly, Miguel de la Hoya, Kim De Leeneer, Peter Devilee, Orland Diez, Susan M. Domchek, Michele Doody, Cecilia M. Dorfling, Thilo Dörk, Isabel dos-Santos-Silva, Martine Dumont, Miriam Dwek, Bernd Dworniczak, Kathleen Egan, Ursula Eilber, Zakaria Einbeigi, Bent Ejlertsen, Steve Ellis, Debra Frost, Fiona Lalloo, Peter A. Fasching, Jonine Figueroa, Henrik Flyger, Michael Friedlander, Eitan Friedman, Gaetana Gambino, Yu-Tang Gao, Judy Garber, Montserrat García-Closas, Andrea Gehrig, Francesca Damiola, Fabienne Lesueur, Sylvie Mazoyer, Dominique Stoppa-Lyonnet, Graham G. Giles, Andrew K. Godwin, David E. Goldgar, Anna González-Neira, Mark H. Greene, Pascal Guénel, Lothar Haeberle, Christopher A. Haiman, Emily Hallberg, Ute Hamann, Thomas V. O. Hansen, Steven Hart, Jaana M. Hartikainen, Mikael Hartman, Norhashimah Hassan, Sue Healey, Frans B. L. Hogervorst, Senno Verhoef, Carolyn B. Hendricks, Peter Hillemanns, Antoinette Hollestelle, Peter J. Hulick, David J. Hunter, Evgeny N. Imyanitov, Claudine Isaacs, Hidemi Ito, Anna Jakubowska, Ramunas Janavicius, Katarzyna Jaworska-Bieniek, Uffe Birk Jensen, Esther M. John, Charles Joly Beauparlant, Michael Jones, Maria Kabisch, Daehee Kang, Beth Y. Karlan, Saila Kauppila, Michael J. Kerin, Sofia Khan, Elza Khusnutdinova, Julia A. Knight, Irene Konstantopoulou, Peter Kraft, Ava Kwong, Yael Laitman, Diether Lambrechts, Conxi Lazaro, Loic Le Marchand, Chuen Neng Lee, Min Hyuk Lee, Jenny Lester, Jingmei Li, Annelie Liljegren, Annika Lindblom, Artitaya Lophatananon, Jan Lubinski, Phuong L. Mai, Arto Mannermaa, Siranoush Manoukian, Sara Margolin, Frederik Marme, Keitaro Matsuo, Lesley McGuffog, Alfons Meindl, Florence Menegaux, Marco Montagna, Kenneth Muir, Anna Marie Mulligan, Katherine L. Nathanson, Susan L. Neuhausen, Heli Nevanlinna, Polly A. Newcomb, Silje Nord, Robert L. Nussbaum, Kenneth Offit, Edith Olah, Olufunmilayo I. Olopade, Curtis Olswold, Ana Osorio, Laura Papi, Tjoung-Won Park-Simon, Ylva Paulsson-Karlsson, Stephanie Peeters, Bernard Peissel, Paolo Peterlongo, Julian Peto, Georg Pfeiler, Catherine M. Phelan, Nadege Presneau, Paolo Radice, Nazneen Rahman, Susan J. Ramus, Muhammad Usman Rashid, Gad Rennert, Kerstin Rhiem, Anja Rudolph, Ritu Salani, Suleeporn Sangrajrang, Elinor J. Sawyer, Marjanka K Schmidt, Rita K. Schmutzler, Minouk J. Schoemaker, Peter Schürmann, Caroline Seynaeve, Chen-Yang Shen, Martha J. Shrubsole, Xiao-Ou Shu, Alice Sigurdson, Christian F. Singer, Susan Slager, Penny Soucy, Melissa Southey, Doris Steinemann, Anthony Swerdlow, Csilla I. Szabo, Sandrine Tchatchou, Manuel R. Teixeira, Soo H. Teo, Mary Beth Terry, Daniel C. Tessier, Alex Teulé, Mads Thomassen, Laima Tihomirova, Marc Tischkowitz, Amanda E. Toland, Nadine Tung, Clare Turnbull, Ans M. W. van den Ouweland, Elizabeth J. van Rensburg, David ven den Berg, Joseph Vijai, Shan Wang-Gohrke, Jeffrey N. Weitzel, Alice S. Whittemore, Robert Winqvist, Tien Y. Wong, Anna H. Wu, Drakoulis Yannoukakos, Jyh-Cherng Yu, Paul D. P. Pharoah, Per Hall, Georgia Chenevix-Trench, Alison M. Dunning, Jacques Simard, Fergus J. Couch, Antonis C. Antoniou, Douglas F. Easton, Wei Zheng, on behalf of EMBRACE, behalf of GEMO Study Collaborators, on behalf of HEBON, on behalf of KConFab, AOCS Investigators

Published in: Breast Cancer Research | Issue 1/2016

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Abstract

Background

Multiple recent genome-wide association studies (GWAS) have identified a single nucleotide polymorphism (SNP), rs10771399, at 12p11 that is associated with breast cancer risk.

Method

We performed a fine-scale mapping study of a 700 kb region including 441 genotyped and more than 1300 imputed genetic variants in 48,155 cases and 43,612 controls of European descent, 6269 cases and 6624 controls of East Asian descent and 1116 cases and 932 controls of African descent in the Breast Cancer Association Consortium (BCAC; http://​bcac.​ccge.​medschl.​cam.​ac.​uk/​), and in 15,252 BRCA1 mutation carriers in the Consortium of Investigators of Modifiers of BRCA1/2 (CIMBA). Stepwise regression analyses were performed to identify independent association signals. Data from the Encyclopedia of DNA Elements project (ENCODE) and the Cancer Genome Atlas (TCGA) were used for functional annotation.

Results

Analysis of data from European descendants found evidence for four independent association signals at 12p11, represented by rs7297051 (odds ratio (OR) = 1.09, 95 % confidence interval (CI) = 1.06–1.12; P = 3 × 10-9), rs805510 (OR = 1.08, 95 % CI = 1.04–1.12, P = 2 × 10-5), and rs1871152 (OR = 1.04, 95 % CI = 1.02–1.06; P = 2 × 10-4) identified in the general populations, and rs113824616 (P = 7 × 10-5) identified in the meta-analysis of BCAC ER-negative cases and BRCA1 mutation carriers. SNPs rs7297051, rs805510 and rs113824616 were also associated with breast cancer risk at P < 0.05 in East Asians, but none of the associations were statistically significant in African descendants. Multiple candidate functional variants are located in putative enhancer sequences. Chromatin interaction data suggested that PTHLH was the likely target gene of these enhancers. Of the six variants with the strongest evidence of potential functionality, rs11049453 was statistically significantly associated with the expression of PTHLH and its nearby gene CCDC91 at P < 0.05.

Conclusion

This study identified four independent association signals at 12p11 and revealed potentially functional variants, providing additional insights into the underlying biological mechanism(s) for the association observed between variants at 12p11 and breast cancer risk.
Appendix
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Metadata
Title
Identification of independent association signals and putative functional variants for breast cancer risk through fine-scale mapping of the 12p11 locus
Authors
Chenjie Zeng
Xingyi Guo
Jirong Long
Karoline B. Kuchenbaecker
Arnaud Droit
Kyriaki Michailidou
Maya Ghoussaini
Siddhartha Kar
Adam Freeman
John L. Hopper
Roger L. Milne
Manjeet K. Bolla
Qin Wang
Joe Dennis
Simona Agata
Shahana Ahmed
Kristiina Aittomäki
Irene L. Andrulis
Hoda Anton-Culver
Natalia N. Antonenkova
Adalgeir Arason
Volker Arndt
Banu K. Arun
Brita Arver
Francois Bacot
Daniel Barrowdale
Caroline Baynes
Alicia Beeghly-Fadiel
Javier Benitez
Marina Bermisheva
Carl Blomqvist
William J. Blot
Natalia V. Bogdanova
Stig E. Bojesen
Bernardo Bonanni
Anne-Lise Borresen-Dale
Judith S. Brand
Hiltrud Brauch
Paul Brennan
Hermann Brenner
Annegien Broeks
Thomas Brüning
Barbara Burwinkel
Saundra S. Buys
Qiuyin Cai
Trinidad Caldes
Ian Campbell
Jane Carpenter
Jenny Chang-Claude
Ji-Yeob Choi
Kathleen B. M. Claes
Christine Clarke
Angela Cox
Simon S. Cross
Kamila Czene
Mary B. Daly
Miguel de la Hoya
Kim De Leeneer
Peter Devilee
Orland Diez
Susan M. Domchek
Michele Doody
Cecilia M. Dorfling
Thilo Dörk
Isabel dos-Santos-Silva
Martine Dumont
Miriam Dwek
Bernd Dworniczak
Kathleen Egan
Ursula Eilber
Zakaria Einbeigi
Bent Ejlertsen
Steve Ellis
Debra Frost
Fiona Lalloo
Peter A. Fasching
Jonine Figueroa
Henrik Flyger
Michael Friedlander
Eitan Friedman
Gaetana Gambino
Yu-Tang Gao
Judy Garber
Montserrat García-Closas
Andrea Gehrig
Francesca Damiola
Fabienne Lesueur
Sylvie Mazoyer
Dominique Stoppa-Lyonnet
Graham G. Giles
Andrew K. Godwin
David E. Goldgar
Anna González-Neira
Mark H. Greene
Pascal Guénel
Lothar Haeberle
Christopher A. Haiman
Emily Hallberg
Ute Hamann
Thomas V. O. Hansen
Steven Hart
Jaana M. Hartikainen
Mikael Hartman
Norhashimah Hassan
Sue Healey
Frans B. L. Hogervorst
Senno Verhoef
Carolyn B. Hendricks
Peter Hillemanns
Antoinette Hollestelle
Peter J. Hulick
David J. Hunter
Evgeny N. Imyanitov
Claudine Isaacs
Hidemi Ito
Anna Jakubowska
Ramunas Janavicius
Katarzyna Jaworska-Bieniek
Uffe Birk Jensen
Esther M. John
Charles Joly Beauparlant
Michael Jones
Maria Kabisch
Daehee Kang
Beth Y. Karlan
Saila Kauppila
Michael J. Kerin
Sofia Khan
Elza Khusnutdinova
Julia A. Knight
Irene Konstantopoulou
Peter Kraft
Ava Kwong
Yael Laitman
Diether Lambrechts
Conxi Lazaro
Loic Le Marchand
Chuen Neng Lee
Min Hyuk Lee
Jenny Lester
Jingmei Li
Annelie Liljegren
Annika Lindblom
Artitaya Lophatananon
Jan Lubinski
Phuong L. Mai
Arto Mannermaa
Siranoush Manoukian
Sara Margolin
Frederik Marme
Keitaro Matsuo
Lesley McGuffog
Alfons Meindl
Florence Menegaux
Marco Montagna
Kenneth Muir
Anna Marie Mulligan
Katherine L. Nathanson
Susan L. Neuhausen
Heli Nevanlinna
Polly A. Newcomb
Silje Nord
Robert L. Nussbaum
Kenneth Offit
Edith Olah
Olufunmilayo I. Olopade
Curtis Olswold
Ana Osorio
Laura Papi
Tjoung-Won Park-Simon
Ylva Paulsson-Karlsson
Stephanie Peeters
Bernard Peissel
Paolo Peterlongo
Julian Peto
Georg Pfeiler
Catherine M. Phelan
Nadege Presneau
Paolo Radice
Nazneen Rahman
Susan J. Ramus
Muhammad Usman Rashid
Gad Rennert
Kerstin Rhiem
Anja Rudolph
Ritu Salani
Suleeporn Sangrajrang
Elinor J. Sawyer
Marjanka K Schmidt
Rita K. Schmutzler
Minouk J. Schoemaker
Peter Schürmann
Caroline Seynaeve
Chen-Yang Shen
Martha J. Shrubsole
Xiao-Ou Shu
Alice Sigurdson
Christian F. Singer
Susan Slager
Penny Soucy
Melissa Southey
Doris Steinemann
Anthony Swerdlow
Csilla I. Szabo
Sandrine Tchatchou
Manuel R. Teixeira
Soo H. Teo
Mary Beth Terry
Daniel C. Tessier
Alex Teulé
Mads Thomassen
Laima Tihomirova
Marc Tischkowitz
Amanda E. Toland
Nadine Tung
Clare Turnbull
Ans M. W. van den Ouweland
Elizabeth J. van Rensburg
David ven den Berg
Joseph Vijai
Shan Wang-Gohrke
Jeffrey N. Weitzel
Alice S. Whittemore
Robert Winqvist
Tien Y. Wong
Anna H. Wu
Drakoulis Yannoukakos
Jyh-Cherng Yu
Paul D. P. Pharoah
Per Hall
Georgia Chenevix-Trench
Alison M. Dunning
Jacques Simard
Fergus J. Couch
Antonis C. Antoniou
Douglas F. Easton
Wei Zheng
on behalf of EMBRACE
behalf of GEMO Study Collaborators
on behalf of HEBON
on behalf of KConFab
AOCS Investigators
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 1/2016
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/s13058-016-0718-0

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