Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region

Christine F. Skibola; Sonja I. Berndt; Joseph Vijai; Lucia Conde; Zhaoming Wang; Meredith Yeager; Paul I.W. De Bakker; Brenda M. Birmann; Claire M. Vajdic; Jia Nee Foo; Paige M. Bracci; Roel C.H. Vermeulen; Susan L. Slager; Silvia De Sanjose; Sophia S. Wang; Martha S. Linet; Gilles Salles; Qing Lan; Gianluca Severi; Henrik Hjalgrim; Tracy Lightfoot; Mads Melbye; Jian Gu; Hervé Ghesquières; Brian K. Link; Lindsay M. Morton; Elizabeth A. Holly; Alex Smith; Lesley F. Tinker; Lauren R. Teras; Anne Kricker; Nikolaus Becker; Mark P. Purdue; John J. Spinelli; Yawei Zhang; Graham G. Giles; Paolo Vineis; Alain Monnereau; Kimberly A. Bertrand; Demetrius Albanes; Anne Zeleniuch-Jacquotte; Attilio Gabbas; Charles C. Chung; Laurie Burdett; Amy Hutchinson; Charles Lawrence; Rebecca Montalvan; Liming Liang; Jinyan Huang; Baoshan Ma; Jianjun Liu; Hans Olov Adami; Bengt Glimelius; Yuanqing Ye; Grzegorz S. Nowakowski; Ahmet Dogan; Carrie A. Thompson; Thomas M. Habermann; Anne J. Novak; Mark Liebow; Thomas E. Witzig; George J. Weiner; Maryjean Schenk; Patricia Hartge; Anneclaire J. De Roos; Wendy Cozen; Degui Zhi; Nicholas K. Akers; Jacques Riby; Martyn T. Smith; Mortimer Lacher; Danylo J. Villano; Ann Maria; Eve Roman; Eleanor Kane; Rebecca D. Jackson; Kari E. North; W. Ryan Diver; Jenny Turner; Bruce K. Armstrong; Yolanda Benavente; Paolo Boffetta; Paul Brennan; Lenka Foretova; Marc Maynadie; Anthony Staines; James McKay; Angela R. Brooks-Wilson; Tongzhang Zheng; Theodore R. Holford; Saioa Chamosa; Rudolph Kaaks; Rachel S. Kelly; Bodil Ohlsson; Ruth C. Travis; Elisabete Weiderpass; Jacqueline Clavel; Edward Giovannucci; Peter Kraft; Jarmo Virtamo; Patrizio Mazza; Pierluigi Cocco; Maria Grazia Ennas; Brian C.H. Chiu; Joseph F. Fraumeni; Alexandra Nieters; Kenneth Offit; Xifeng Wu; James R. Cerhan; Karin E. Smedby; Stephen J. Chanock; Nathaniel Rothman

doi:10.1016/j.ajhg.2014.09.004

Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region

Christine F. Skibola
, Sonja I. Berndt
, Joseph Vijai
, Lucia Conde
, Zhaoming Wang
, Meredith Yeager
, Paul I.W. De Bakker
, Brenda M. Birmann
, Claire M. Vajdic
, Jia Nee Foo
, Paige M. Bracci
, Roel C.H. Vermeulen
, Susan L. Slager
, Silvia De Sanjose
, Sophia S. Wang
, Martha S. Linet
, Gilles Salles
, Qing Lan
, Gianluca Severi
, Henrik Hjalgrim

Tracy Lightfoot, Mads Melbye, Jian Gu, Hervé Ghesquières, Brian K. Link, Lindsay M. Morton, Elizabeth A. Holly, Alex Smith, Lesley F. Tinker, Lauren R. Teras, Anne Kricker, Nikolaus Becker, Mark P. Purdue, John J. Spinelli, Yawei Zhang, Graham G. Giles, Paolo Vineis, Alain Monnereau, Kimberly A. Bertrand, Demetrius Albanes, Anne Zeleniuch-Jacquotte, Attilio Gabbas, Charles C. Chung, Laurie Burdett, Amy Hutchinson, Charles Lawrence, Rebecca Montalvan, Liming Liang, Jinyan Huang, Baoshan Ma, Jianjun Liu, Hans Olov Adami, Bengt Glimelius, Yuanqing Ye, Grzegorz S. Nowakowski, Ahmet Dogan, Carrie A. Thompson, Thomas M. Habermann, Anne J. Novak, Mark Liebow, Thomas E. Witzig, George J. Weiner, Maryjean Schenk, Patricia Hartge, Anneclaire J. De Roos, Wendy Cozen, Degui Zhi, Nicholas K. Akers, Jacques Riby, Martyn T. Smith, Mortimer Lacher, Danylo J. Villano, Ann Maria, Eve Roman, Eleanor Kane, Rebecca D. Jackson, Kari E. North, W. Ryan Diver, Jenny Turner, Bruce K. Armstrong, Yolanda Benavente, Paolo Boffetta, Paul Brennan, Lenka Foretova, Marc Maynadie, Anthony Staines, James McKay, Angela R. Brooks-Wilson, Tongzhang Zheng, Theodore R. Holford, Saioa Chamosa, Rudolph Kaaks, Rachel S. Kelly, Bodil Ohlsson, Ruth C. Travis, Elisabete Weiderpass, Jacqueline Clavel, Edward Giovannucci, Peter Kraft, Jarmo Virtamo, Patrizio Mazza, Pierluigi Cocco, Maria Grazia Ennas, Brian C.H. Chiu, Joseph F. Fraumeni, Alexandra Nieters, Kenneth Offit, Xifeng Wu, James R. Cerhan, Karin E. Smedby, Stephen J. Chanock, Nathaniel Rothman

University of Alabama at Birmingham
University of California at Berkeley
National Institutes of Health
Memorial Sloan-Kettering Cancer Center
Utrecht University
Brigham and Women’s Hospital
University of New South Wales
Agency for Science, Technology and Research, Singapore
University of California at San Francisco
Mayo Clinic Rochester, MN
Bellvitge Biomedical Research Institute
CIBER Epidemiología y Salud Pública (CIBERESP)
City of Hope National Med Center
Hospices civils de Lyon
Universite Claude Bernard Lyon 1
CNRS
Human Genetics Foundation
Cancer Council Victoria
University of Melbourne
Statens Serum Institut
University of York
Stanford University
University of Texas MD Anderson Cancer Center
Centre Léon Bérard
University of Iowa
Fred Hutchinson Cancer Research Center
American Cancer Society
The University of Sydney
German Cancer Research Center
Provincial Health Services Authority
University of British Columbia
Yale University
Imperial College London
Université Paris-Saclay
Centre Georges-François Leclerc
Harvard University
New York University
University of Cagliari
Westat
Dalian Maritime University
Karolinska Institutet
Uppsala University
Wayne State University
Drexel University
University of Southern California
Ohio State University
University of North Carolina at Chapel Hill
Macquarie University
Sonic Healthcare
International Agency for Research on Cancer
Masaryk Memorial Cancer Institute
Université de Bourgogne
Dublin City University
Simon Fraser University
Instituto de Investigación Sanitaria Biodonostia
Lund University
University of Oxford
University of Tromsø – The Arctic University of Norway
Cancer Registry of Norway Institute of Population-Based Cancer Research
Folkhalsan
National Institute for Health and Welfare
Ospedale Nord
The University of Chicago
University of Freiburg

Research output: Contribution to journal › Article › peer-review

99 Scopus citations

Abstract

Genome-wide association studies (GWASs) of follicular lymphoma (FL) have previously identified human leukocyte antigen (HLA) gene variants. To identify additional FL susceptibility loci, we conducted a large-scale two-stage GWAS in 4,523 case subjects and 13,344 control subjects of European ancestry. Five non-HLA loci were associated with FL risk: 11q23.3 (rs4938573, p = 5.79 × 10 ^-20) near CXCR5; 11q24.3 (rs4937362, p = 6.76 × 10 ^-11) near ETS1; 3q28 (rs6444305, p = 1.10 × 10 ^-10) in LPP; 18q21.33 (rs17749561, p = 8.28 × 10 ^-10) near BCL2; and 8q24.21 (rs13254990, p = 1.06 × 10 ^-8) near PVT1. In an analysis of the HLA region, we identified four linked HLA-DRβ1 multiallelic amino acids at positions 11, 13, 28, and 30 that were associated with FL risk (p_omnibus = 4.20 × 10 ^-67 to 2.67 × 10 ^-70). Additional independent signals included rs17203612 in HLA class II (odds ratio [OR_per-allele] = 1.44; p = 4.59 × 10 ^-16) and rs3130437 in HLA class I (OR_per-allele = 1.23; p = 8.23 × 10 ^-9). Our findings further expand the number of loci associated with FL and provide evidence that multiple common variants outside the HLA region make a significant contribution to FL risk.

Original language	English
Pages (from-to)	462-471
Number of pages	10
Journal	American Journal of Human Genetics
Volume	95
Issue number	4
DOIs	https://doi.org/10.1016/j.ajhg.2014.09.004
State	Published - 2014

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10.1016/j.ajhg.2014.09.004

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Skibola, C. F., Berndt, S. I., Vijai, J., Conde, L., Wang, Z., Yeager, M., De Bakker, P. I. W., Birmann, B. M., Vajdic, C. M., Foo, J. N., Bracci, P. M., Vermeulen, R. C. H., Slager, S. L., De Sanjose, S., Wang, S. S., Linet, M. S., Salles, G., Lan, Q., Severi, G., ... Rothman, N. (2014). Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region. American Journal of Human Genetics, 95(4), 462-471. https://doi.org/10.1016/j.ajhg.2014.09.004

@article{f1b92241066340ebbc463640547793bd,

title = "Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region",

abstract = "Genome-wide association studies (GWASs) of follicular lymphoma (FL) have previously identified human leukocyte antigen (HLA) gene variants. To identify additional FL susceptibility loci, we conducted a large-scale two-stage GWAS in 4,523 case subjects and 13,344 control subjects of European ancestry. Five non-HLA loci were associated with FL risk: 11q23.3 (rs4938573, p = 5.79 × 10 -20) near CXCR5; 11q24.3 (rs4937362, p = 6.76 × 10 -11) near ETS1; 3q28 (rs6444305, p = 1.10 × 10 -10) in LPP; 18q21.33 (rs17749561, p = 8.28 × 10 -10) near BCL2; and 8q24.21 (rs13254990, p = 1.06 × 10 -8) near PVT1. In an analysis of the HLA region, we identified four linked HLA-DRβ1 multiallelic amino acids at positions 11, 13, 28, and 30 that were associated with FL risk (pomnibus = 4.20 × 10 -67 to 2.67 × 10 -70). Additional independent signals included rs17203612 in HLA class II (odds ratio [ORper-allele] = 1.44; p = 4.59 × 10 -16) and rs3130437 in HLA class I (ORper-allele = 1.23; p = 8.23 × 10 -9). Our findings further expand the number of loci associated with FL and provide evidence that multiple common variants outside the HLA region make a significant contribution to FL risk.",

author = "Skibola, \{Christine F.\} and Berndt, \{Sonja I.\} and Joseph Vijai and Lucia Conde and Zhaoming Wang and Meredith Yeager and \{De Bakker\}, \{Paul I.W.\} and Birmann, \{Brenda M.\} and Vajdic, \{Claire M.\} and Foo, \{Jia Nee\} and Bracci, \{Paige M.\} and Vermeulen, \{Roel C.H.\} and Slager, \{Susan L.\} and \{De Sanjose\}, Silvia and Wang, \{Sophia S.\} and Linet, \{Martha S.\} and Gilles Salles and Qing Lan and Gianluca Severi and Henrik Hjalgrim and Tracy Lightfoot and Mads Melbye and Jian Gu and Herv{\'e} Ghesqui{\`e}res and Link, \{Brian K.\} and Morton, \{Lindsay M.\} and Holly, \{Elizabeth A.\} and Alex Smith and Tinker, \{Lesley F.\} and Teras, \{Lauren R.\} and Anne Kricker and Nikolaus Becker and Purdue, \{Mark P.\} and Spinelli, \{John J.\} and Yawei Zhang and Giles, \{Graham G.\} and Paolo Vineis and Alain Monnereau and Bertrand, \{Kimberly A.\} and Demetrius Albanes and Anne Zeleniuch-Jacquotte and Attilio Gabbas and Chung, \{Charles C.\} and Laurie Burdett and Amy Hutchinson and Charles Lawrence and Rebecca Montalvan and Liming Liang and Jinyan Huang and Baoshan Ma and Jianjun Liu and Adami, \{Hans Olov\} and Bengt Glimelius and Yuanqing Ye and Nowakowski, \{Grzegorz S.\} and Ahmet Dogan and Thompson, \{Carrie A.\} and Habermann, \{Thomas M.\} and Novak, \{Anne J.\} and Mark Liebow and Witzig, \{Thomas E.\} and Weiner, \{George J.\} and Maryjean Schenk and Patricia Hartge and \{De Roos\}, \{Anneclaire J.\} and Wendy Cozen and Degui Zhi and Akers, \{Nicholas K.\} and Jacques Riby and Smith, \{Martyn T.\} and Mortimer Lacher and Villano, \{Danylo J.\} and Ann Maria and Eve Roman and Eleanor Kane and Jackson, \{Rebecca D.\} and North, \{Kari E.\} and Diver, \{W. Ryan\} and Jenny Turner and Armstrong, \{Bruce K.\} and Yolanda Benavente and Paolo Boffetta and Paul Brennan and Lenka Foretova and Marc Maynadie and Anthony Staines and James McKay and Brooks-Wilson, \{Angela R.\} and Tongzhang Zheng and Holford, \{Theodore R.\} and Saioa Chamosa and Rudolph Kaaks and Kelly, \{Rachel S.\} and Bodil Ohlsson and Travis, \{Ruth C.\} and Elisabete Weiderpass and Jacqueline Clavel and Edward Giovannucci and Peter Kraft and Jarmo Virtamo and Patrizio Mazza and Pierluigi Cocco and Ennas, \{Maria Grazia\} and Chiu, \{Brian C.H.\} and Fraumeni, \{Joseph F.\} and Alexandra Nieters and Kenneth Offit and Xifeng Wu and Cerhan, \{James R.\} and Smedby, \{Karin E.\} and Chanock, \{Stephen J.\} and Nathaniel Rothman",

year = "2014",

doi = "10.1016/j.ajhg.2014.09.004",

language = "English",

volume = "95",

pages = "462--471",

journal = "American Journal of Human Genetics",

issn = "0002-9297",

number = "4",

}

Skibola, CF, Berndt, SI, Vijai, J, Conde, L, Wang, Z, Yeager, M, De Bakker, PIW, Birmann, BM, Vajdic, CM, Foo, JN, Bracci, PM, Vermeulen, RCH, Slager, SL, De Sanjose, S, Wang, SS, Linet, MS, Salles, G, Lan, Q, Severi, G, Hjalgrim, H, Lightfoot, T, Melbye, M, Gu, J, Ghesquières, H, Link, BK, Morton, LM, Holly, EA, Smith, A, Tinker, LF, Teras, LR, Kricker, A, Becker, N, Purdue, MP, Spinelli, JJ, Zhang, Y, Giles, GG, Vineis, P, Monnereau, A, Bertrand, KA, Albanes, D, Zeleniuch-Jacquotte, A, Gabbas, A, Chung, CC, Burdett, L, Hutchinson, A, Lawrence, C, Montalvan, R, Liang, L, Huang, J, Ma, B, Liu, J, Adami, HO, Glimelius, B, Ye, Y, Nowakowski, GS, Dogan, A, Thompson, CA, Habermann, TM, Novak, AJ, Liebow, M, Witzig, TE, Weiner, GJ, Schenk, M, Hartge, P, De Roos, AJ, Cozen, W, Zhi, D, Akers, NK, Riby, J, Smith, MT, Lacher, M, Villano, DJ, Maria, A, Roman, E, Kane, E, Jackson, RD, North, KE, Diver, WR, Turner, J, Armstrong, BK, Benavente, Y, Boffetta, P, Brennan, P, Foretova, L, Maynadie, M, Staines, A, McKay, J, Brooks-Wilson, AR, Zheng, T, Holford, TR, Chamosa, S, Kaaks, R, Kelly, RS, Ohlsson, B, Travis, RC, Weiderpass, E, Clavel, J, Giovannucci, E, Kraft, P, Virtamo, J, Mazza, P, Cocco, P, Ennas, MG, Chiu, BCH, Fraumeni, JF, Nieters, A, Offit, K, Wu, X, Cerhan, JR, Smedby, KE, Chanock, SJ & Rothman, N 2014, 'Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region', American Journal of Human Genetics, vol. 95, no. 4, pp. 462-471. https://doi.org/10.1016/j.ajhg.2014.09.004

TY - JOUR

T1 - Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region

AU - Skibola, Christine F.

AU - Berndt, Sonja I.

AU - Vijai, Joseph

AU - Conde, Lucia

AU - Wang, Zhaoming

AU - Yeager, Meredith

AU - De Bakker, Paul I.W.

AU - Birmann, Brenda M.

AU - Vajdic, Claire M.

AU - Foo, Jia Nee

AU - Bracci, Paige M.

AU - Vermeulen, Roel C.H.

AU - Slager, Susan L.

AU - De Sanjose, Silvia

AU - Wang, Sophia S.

AU - Linet, Martha S.

AU - Salles, Gilles

AU - Lan, Qing

AU - Severi, Gianluca

AU - Hjalgrim, Henrik

AU - Lightfoot, Tracy

AU - Melbye, Mads

AU - Gu, Jian

AU - Ghesquières, Hervé

AU - Link, Brian K.

AU - Morton, Lindsay M.

AU - Holly, Elizabeth A.

AU - Smith, Alex

AU - Tinker, Lesley F.

AU - Teras, Lauren R.

AU - Kricker, Anne

AU - Becker, Nikolaus

AU - Purdue, Mark P.

AU - Spinelli, John J.

AU - Zhang, Yawei

AU - Giles, Graham G.

AU - Vineis, Paolo

AU - Monnereau, Alain

AU - Bertrand, Kimberly A.

AU - Albanes, Demetrius

AU - Zeleniuch-Jacquotte, Anne

AU - Gabbas, Attilio

AU - Chung, Charles C.

AU - Burdett, Laurie

AU - Hutchinson, Amy

AU - Lawrence, Charles

AU - Montalvan, Rebecca

AU - Liang, Liming

AU - Huang, Jinyan

AU - Ma, Baoshan

AU - Liu, Jianjun

AU - Adami, Hans Olov

AU - Glimelius, Bengt

AU - Ye, Yuanqing

AU - Nowakowski, Grzegorz S.

AU - Dogan, Ahmet

AU - Thompson, Carrie A.

AU - Habermann, Thomas M.

AU - Novak, Anne J.

AU - Liebow, Mark

AU - Witzig, Thomas E.

AU - Weiner, George J.

AU - Schenk, Maryjean

AU - Hartge, Patricia

AU - De Roos, Anneclaire J.

AU - Cozen, Wendy

AU - Zhi, Degui

AU - Akers, Nicholas K.

AU - Riby, Jacques

AU - Smith, Martyn T.

AU - Lacher, Mortimer

AU - Villano, Danylo J.

AU - Maria, Ann

AU - Roman, Eve

AU - Kane, Eleanor

AU - Jackson, Rebecca D.

AU - North, Kari E.

AU - Diver, W. Ryan

AU - Turner, Jenny

AU - Armstrong, Bruce K.

AU - Benavente, Yolanda

AU - Boffetta, Paolo

AU - Brennan, Paul

AU - Foretova, Lenka

AU - Maynadie, Marc

AU - Staines, Anthony

AU - McKay, James

AU - Brooks-Wilson, Angela R.

AU - Zheng, Tongzhang

AU - Holford, Theodore R.

AU - Chamosa, Saioa

AU - Kaaks, Rudolph

AU - Kelly, Rachel S.

AU - Ohlsson, Bodil

AU - Travis, Ruth C.

AU - Weiderpass, Elisabete

AU - Clavel, Jacqueline

AU - Giovannucci, Edward

AU - Kraft, Peter

AU - Virtamo, Jarmo

AU - Mazza, Patrizio

AU - Cocco, Pierluigi

AU - Ennas, Maria Grazia

AU - Chiu, Brian C.H.

AU - Fraumeni, Joseph F.

AU - Nieters, Alexandra

AU - Offit, Kenneth

AU - Wu, Xifeng

AU - Cerhan, James R.

AU - Smedby, Karin E.

AU - Chanock, Stephen J.

AU - Rothman, Nathaniel

PY - 2014

Y1 - 2014

N2 - Genome-wide association studies (GWASs) of follicular lymphoma (FL) have previously identified human leukocyte antigen (HLA) gene variants. To identify additional FL susceptibility loci, we conducted a large-scale two-stage GWAS in 4,523 case subjects and 13,344 control subjects of European ancestry. Five non-HLA loci were associated with FL risk: 11q23.3 (rs4938573, p = 5.79 × 10 -20) near CXCR5; 11q24.3 (rs4937362, p = 6.76 × 10 -11) near ETS1; 3q28 (rs6444305, p = 1.10 × 10 -10) in LPP; 18q21.33 (rs17749561, p = 8.28 × 10 -10) near BCL2; and 8q24.21 (rs13254990, p = 1.06 × 10 -8) near PVT1. In an analysis of the HLA region, we identified four linked HLA-DRβ1 multiallelic amino acids at positions 11, 13, 28, and 30 that were associated with FL risk (pomnibus = 4.20 × 10 -67 to 2.67 × 10 -70). Additional independent signals included rs17203612 in HLA class II (odds ratio [ORper-allele] = 1.44; p = 4.59 × 10 -16) and rs3130437 in HLA class I (ORper-allele = 1.23; p = 8.23 × 10 -9). Our findings further expand the number of loci associated with FL and provide evidence that multiple common variants outside the HLA region make a significant contribution to FL risk.

AB - Genome-wide association studies (GWASs) of follicular lymphoma (FL) have previously identified human leukocyte antigen (HLA) gene variants. To identify additional FL susceptibility loci, we conducted a large-scale two-stage GWAS in 4,523 case subjects and 13,344 control subjects of European ancestry. Five non-HLA loci were associated with FL risk: 11q23.3 (rs4938573, p = 5.79 × 10 -20) near CXCR5; 11q24.3 (rs4937362, p = 6.76 × 10 -11) near ETS1; 3q28 (rs6444305, p = 1.10 × 10 -10) in LPP; 18q21.33 (rs17749561, p = 8.28 × 10 -10) near BCL2; and 8q24.21 (rs13254990, p = 1.06 × 10 -8) near PVT1. In an analysis of the HLA region, we identified four linked HLA-DRβ1 multiallelic amino acids at positions 11, 13, 28, and 30 that were associated with FL risk (pomnibus = 4.20 × 10 -67 to 2.67 × 10 -70). Additional independent signals included rs17203612 in HLA class II (odds ratio [ORper-allele] = 1.44; p = 4.59 × 10 -16) and rs3130437 in HLA class I (ORper-allele = 1.23; p = 8.23 × 10 -9). Our findings further expand the number of loci associated with FL and provide evidence that multiple common variants outside the HLA region make a significant contribution to FL risk.

UR - https://www.scopus.com/pages/publications/84921517901

U2 - 10.1016/j.ajhg.2014.09.004

DO - 10.1016/j.ajhg.2014.09.004

M3 - Article

C2 - 25279986

AN - SCOPUS:84921517901

SN - 0002-9297

VL - 95

SP - 462

EP - 471

JO - American Journal of Human Genetics

JF - American Journal of Human Genetics

IS - 4

ER -

Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region

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