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 HjalgrimTracy 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 Matthew Habermann, Anne J Novak, Mark Liebow, Thomas Elmer 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

Research output: Contribution to journalArticle

55 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)462-471
Number of pages10
JournalAmerican Journal of Human Genetics
Volume95
Issue number4
DOIs
StatePublished - 2014

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Follicular Lymphoma
Genome-Wide Association Study
HLA Antigens
Alleles
Odds Ratio
Amino Acids
Genes

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)
  • Medicine(all)

Cite this

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

In: American Journal of Human Genetics, Vol. 95, No. 4, 2014, p. 462-471.

Research output: Contribution to journalArticle

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
Skibola, Christine F. ; Berndt, Sonja I. ; Vijai, Joseph ; Conde, Lucia ; Wang, Zhaoming ; Yeager, Meredith ; De Bakker, Paul I W ; Birmann, Brenda M. ; Vajdic, Claire M. ; Foo, Jia Nee ; Bracci, Paige M. ; Vermeulen, Roel C H ; Slager, Susan L ; De Sanjose, Silvia ; Wang, Sophia S. ; Linet, Martha S. ; Salles, Gilles ; Lan, Qing ; Severi, Gianluca ; Hjalgrim, Henrik ; Lightfoot, Tracy ; Melbye, Mads ; Gu, Jian ; Ghesquières, Hervé ; Link, Brian K. ; Morton, Lindsay M. ; Holly, Elizabeth A. ; Smith, Alex ; Tinker, Lesley F. ; Teras, Lauren R. ; Kricker, Anne ; Becker, Nikolaus ; Purdue, Mark P. ; Spinelli, John J. ; Zhang, Yawei ; Giles, Graham G. ; Vineis, Paolo ; Monnereau, Alain ; Bertrand, Kimberly A. ; Albanes, Demetrius ; Zeleniuch-Jacquotte, Anne ; Gabbas, Attilio ; Chung, Charles C. ; Burdett, Laurie ; Hutchinson, Amy ; Lawrence, Charles ; Montalvan, Rebecca ; Liang, Liming ; Huang, Jinyan ; Ma, Baoshan ; Liu, Jianjun ; Adami, Hans Olov ; Glimelius, Bengt ; Ye, Yuanqing ; Nowakowski, Grzegorz S ; Dogan, Ahmet ; Thompson, Carrie A ; Habermann, Thomas Matthew ; Novak, Anne J ; Liebow, Mark ; Witzig, Thomas Elmer ; Weiner, George J. ; Schenk, Maryjean ; Hartge, Patricia ; De Roos, Anneclaire J. ; Cozen, Wendy ; Zhi, Degui ; Akers, Nicholas K. ; Riby, Jacques ; Smith, Martyn T. ; Lacher, Mortimer ; Villano, Danylo J. ; Maria, Ann ; Roman, Eve ; Kane, Eleanor ; Jackson, Rebecca D. ; North, Kari E. ; Diver, W. Ryan ; Turner, Jenny ; Armstrong, Bruce K. ; Benavente, Yolanda ; Boffetta, Paolo ; Brennan, Paul ; Foretova, Lenka ; Maynadie, Marc ; Staines, Anthony ; McKay, James ; Brooks-Wilson, Angela R. ; Zheng, Tongzhang ; Holford, Theodore R. ; Chamosa, Saioa ; Kaaks, Rudolph ; Kelly, Rachel S. ; Ohlsson, Bodil ; Travis, Ruth C. ; Weiderpass, Elisabete ; Clavel, Jacqueline ; Giovannucci, Edward ; Kraft, Peter ; Virtamo, Jarmo ; Mazza, Patrizio ; Cocco, Pierluigi ; Ennas, Maria Grazia ; Chiu, Brian C H ; Fraumeni, Joseph F. ; Nieters, Alexandra ; Offit, Kenneth ; Wu, Xifeng ; Cerhan, James R ; Smedby, Karin E. ; Chanock, Stephen J. ; Rothman, Nathaniel. / Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region. In: American Journal of Human Genetics. 2014 ; Vol. 95, No. 4. pp. 462-471.
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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.",
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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 Matthew

AU - Novak, Anne J

AU - Liebow, Mark

AU - Witzig, Thomas Elmer

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.

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UR - http://www.scopus.com/inward/citedby.url?scp=84921517901&partnerID=8YFLogxK

U2 - 10.1016/j.ajhg.2014.09.004

DO - 10.1016/j.ajhg.2014.09.004

M3 - Article

C2 - 25279986

AN - SCOPUS:84921517901

VL - 95

SP - 462

EP - 471

JO - American Journal of Human Genetics

JF - American Journal of Human Genetics

SN - 0002-9297

IS - 4

ER -