Meta-analysis of genome-wide association studies discovers multiple loci for chronic lymphocytic leukemia

Sonja I. Berndt, Nicola J. Camp, Christine F. Skibola, Joseph Vijai, Zhaoming Wang, Jian Gu, Alexandra Nieters, Rachel S. Kelly, Karin E. Smedby, Alain Monnereau, Wendy Cozen, Angela Cox, Sophia S. Wang, Qing Lan, Lauren R. Teras, Moara Machado, Meredith Yeager, Angela R. Brooks-Wilson, Patricia Hartge, Mark P. PurdueBrenda M. Birmann, Claire M. Vajdic, Pierluigi Cocco, Yawei Zhang, Graham G. Giles, Anne Zeleniuch-Jacquotte, Charles Lawrence, Rebecca Montalvan, Laurie Burdett, Amy Hutchinson, Yuanqing Ye, Timothy G. Call, Tait D. Shanafelt, Anne J Novak, Neil Elliot Kay, Mark Liebow, Julie M Cunningham, Cristine Allmer, Henrik Hjalgrim, Hans Olov Adami, Mads Melbye, Bengt Glimelius, Ellen T. Chang, Martha Glenn, Karen Curtin, Lisa A. Cannon-Albright, W. Ryan Diver, Brian K. Link, George J. Weiner, Lucia Conde, Paige M. Bracci, Jacques Riby, Donna K. Arnett, Degui Zhi, Justin M. Leach, Elizabeth A. Holly, Rebecca D. Jackson, Lesley F. Tinker, Yolanda Benavente, Nuria Sala, Delphine Casabonne, Nikolaus Becker, Paolo Boffetta, Paul Brennan, Lenka Foretova, Marc Maynadie, James McKay, Anthony Staines, Kari G. Chaffee, Sara J. Achenbach, Celine M Vachon, Lynn R. Goldin, Sara S. Strom, Jose F. Leis, J. Brice Weinberg, Neil E. Caporaso, Aaron D. Norman, Anneclaire J. De Roos, Lindsay M. Morton, Richard K. Severson, Elio Riboli, Paolo Vineis, Rudolph Kaaks, Giovanna Masala, Elisabete Weiderpass, Maria Dolores Chirlaque, Roel C H Vermeulen, Ruth C. Travis, Melissa C. Southey, Roger L. Milne, Demetrius Albanes, Jarmo Virtamo, Stephanie Weinstein, Jacqueline Clavel, Tongzhang Zheng, Theodore R. Holford, Danylo J. Villano, Ann Maria, John J. Spinelli, Randy D. Gascoyne, Joseph M. Connors, Kimberly A. Bertrand, Edward Giovannucci, Peter Kraft, Anne Kricker, Jenny Turner, Maria Grazia Ennas, Giovanni M. Ferri, Lucia Miligi, Liming Liang, Baoshan Ma, Jinyan Huang, Simon Crouch, Ju Hyun Park, Nilanjan Chatterjee, Kari E. North, John A. Snowden, Josh Wright, Joseph F. Fraumeni, Kenneth Offit, Xifeng Wu, Silvia De Sanjose, James R Cerhan, Stephen J. Chanock, Nathaniel Rothman, Susan L Slager

Research output: Contribution to journalArticle

41 Citations (Scopus)

Abstract

Chronic lymphocytic leukemia (CLL) is a common lymphoid malignancy with strong heritability. To further understand the genetic susceptibility for CLL and identify common loci associated with risk, we conducted a meta-analysis of four genome-wide association studies (GWAS) composed of 3,100 cases and 7,667 controls with follow-up replication in 1,958 cases and 5,530 controls. Here we report three new loci at 3p24.1 (rs9880772, EOMES, P=2.55 × 10-11), 6p25.2 (rs73718779, SERPINB6, P=1.97 × 10-8) and 3q28 (rs9815073, LPP, P=3.62 × 10-8), as well as a new independent SNP at the known 2q13 locus (rs9308731, BCL2L11, P=1.00 × 10-11) in the combined analysis. We find suggestive evidence (P

Original languageEnglish (US)
Article number10933
JournalNature Communications
Volume7
DOIs
StatePublished - Mar 9 2016

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leukemias
genome
Genome-Wide Association Study
B-Cell Chronic Lymphocytic Leukemia
loci
Meta-Analysis
Genes
Genetic Predisposition to Disease
Single Nucleotide Polymorphism
magnetic permeability
Neoplasms

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Chemistry(all)
  • Physics and Astronomy(all)

Cite this

Meta-analysis of genome-wide association studies discovers multiple loci for chronic lymphocytic leukemia. / Berndt, Sonja I.; Camp, Nicola J.; Skibola, Christine F.; Vijai, Joseph; Wang, Zhaoming; Gu, Jian; Nieters, Alexandra; Kelly, Rachel S.; Smedby, Karin E.; Monnereau, Alain; Cozen, Wendy; Cox, Angela; Wang, Sophia S.; Lan, Qing; Teras, Lauren R.; Machado, Moara; Yeager, Meredith; Brooks-Wilson, Angela R.; Hartge, Patricia; Purdue, Mark P.; Birmann, Brenda M.; Vajdic, Claire M.; Cocco, Pierluigi; Zhang, Yawei; Giles, Graham G.; Zeleniuch-Jacquotte, Anne; Lawrence, Charles; Montalvan, Rebecca; Burdett, Laurie; Hutchinson, Amy; Ye, Yuanqing; Call, Timothy G.; Shanafelt, Tait D.; Novak, Anne J; Kay, Neil Elliot; Liebow, Mark; Cunningham, Julie M; Allmer, Cristine; Hjalgrim, Henrik; Adami, Hans Olov; Melbye, Mads; Glimelius, Bengt; Chang, Ellen T.; Glenn, Martha; Curtin, Karen; Cannon-Albright, Lisa A.; Diver, W. Ryan; Link, Brian K.; Weiner, George J.; Conde, Lucia; Bracci, Paige M.; Riby, Jacques; Arnett, Donna K.; Zhi, Degui; Leach, Justin M.; Holly, Elizabeth A.; Jackson, Rebecca D.; Tinker, Lesley F.; Benavente, Yolanda; Sala, Nuria; Casabonne, Delphine; Becker, Nikolaus; Boffetta, Paolo; Brennan, Paul; Foretova, Lenka; Maynadie, Marc; McKay, James; Staines, Anthony; Chaffee, Kari G.; Achenbach, Sara J.; Vachon, Celine M; Goldin, Lynn R.; Strom, Sara S.; Leis, Jose F.; Weinberg, J. Brice; Caporaso, Neil E.; Norman, Aaron D.; De Roos, Anneclaire J.; Morton, Lindsay M.; Severson, Richard K.; Riboli, Elio; Vineis, Paolo; Kaaks, Rudolph; Masala, Giovanna; Weiderpass, Elisabete; Chirlaque, Maria Dolores; Vermeulen, Roel C H; Travis, Ruth C.; Southey, Melissa C.; Milne, Roger L.; Albanes, Demetrius; Virtamo, Jarmo; Weinstein, Stephanie; Clavel, Jacqueline; Zheng, Tongzhang; Holford, Theodore R.; Villano, Danylo J.; Maria, Ann; Spinelli, John J.; Gascoyne, Randy D.; Connors, Joseph M.; Bertrand, Kimberly A.; Giovannucci, Edward; Kraft, Peter; Kricker, Anne; Turner, Jenny; Ennas, Maria Grazia; Ferri, Giovanni M.; Miligi, Lucia; Liang, Liming; Ma, Baoshan; Huang, Jinyan; Crouch, Simon; Park, Ju Hyun; Chatterjee, Nilanjan; North, Kari E.; Snowden, John A.; Wright, Josh; Fraumeni, Joseph F.; Offit, Kenneth; Wu, Xifeng; De Sanjose, Silvia; Cerhan, James R; Chanock, Stephen J.; Rothman, Nathaniel; Slager, Susan L.

In: Nature Communications, Vol. 7, 10933, 09.03.2016.

Research output: Contribution to journalArticle

Berndt, SI, Camp, NJ, Skibola, CF, Vijai, J, Wang, Z, Gu, J, Nieters, A, Kelly, RS, Smedby, KE, Monnereau, A, Cozen, W, Cox, A, Wang, SS, Lan, Q, Teras, LR, Machado, M, Yeager, M, Brooks-Wilson, AR, Hartge, P, Purdue, MP, Birmann, BM, Vajdic, CM, Cocco, P, Zhang, Y, Giles, GG, Zeleniuch-Jacquotte, A, Lawrence, C, Montalvan, R, Burdett, L, Hutchinson, A, Ye, Y, Call, TG, Shanafelt, TD, Novak, AJ, Kay, NE, Liebow, M, Cunningham, JM, Allmer, C, Hjalgrim, H, Adami, HO, Melbye, M, Glimelius, B, Chang, ET, Glenn, M, Curtin, K, Cannon-Albright, LA, Diver, WR, Link, BK, Weiner, GJ, Conde, L, Bracci, PM, Riby, J, Arnett, DK, Zhi, D, Leach, JM, Holly, EA, Jackson, RD, Tinker, LF, Benavente, Y, Sala, N, Casabonne, D, Becker, N, Boffetta, P, Brennan, P, Foretova, L, Maynadie, M, McKay, J, Staines, A, Chaffee, KG, Achenbach, SJ, Vachon, CM, Goldin, LR, Strom, SS, Leis, JF, Weinberg, JB, Caporaso, NE, Norman, AD, De Roos, AJ, Morton, LM, Severson, RK, Riboli, E, Vineis, P, Kaaks, R, Masala, G, Weiderpass, E, Chirlaque, MD, Vermeulen, RCH, Travis, RC, Southey, MC, Milne, RL, Albanes, D, Virtamo, J, Weinstein, S, Clavel, J, Zheng, T, Holford, TR, Villano, DJ, Maria, A, Spinelli, JJ, Gascoyne, RD, Connors, JM, Bertrand, KA, Giovannucci, E, Kraft, P, Kricker, A, Turner, J, Ennas, MG, Ferri, GM, Miligi, L, Liang, L, Ma, B, Huang, J, Crouch, S, Park, JH, Chatterjee, N, North, KE, Snowden, JA, Wright, J, Fraumeni, JF, Offit, K, Wu, X, De Sanjose, S, Cerhan, JR, Chanock, SJ, Rothman, N & Slager, SL 2016, 'Meta-analysis of genome-wide association studies discovers multiple loci for chronic lymphocytic leukemia', Nature Communications, vol. 7, 10933. https://doi.org/10.1038/ncomms10933
Berndt, Sonja I. ; Camp, Nicola J. ; Skibola, Christine F. ; Vijai, Joseph ; Wang, Zhaoming ; Gu, Jian ; Nieters, Alexandra ; Kelly, Rachel S. ; Smedby, Karin E. ; Monnereau, Alain ; Cozen, Wendy ; Cox, Angela ; Wang, Sophia S. ; Lan, Qing ; Teras, Lauren R. ; Machado, Moara ; Yeager, Meredith ; Brooks-Wilson, Angela R. ; Hartge, Patricia ; Purdue, Mark P. ; Birmann, Brenda M. ; Vajdic, Claire M. ; Cocco, Pierluigi ; Zhang, Yawei ; Giles, Graham G. ; Zeleniuch-Jacquotte, Anne ; Lawrence, Charles ; Montalvan, Rebecca ; Burdett, Laurie ; Hutchinson, Amy ; Ye, Yuanqing ; Call, Timothy G. ; Shanafelt, Tait D. ; Novak, Anne J ; Kay, Neil Elliot ; Liebow, Mark ; Cunningham, Julie M ; Allmer, Cristine ; Hjalgrim, Henrik ; Adami, Hans Olov ; Melbye, Mads ; Glimelius, Bengt ; Chang, Ellen T. ; Glenn, Martha ; Curtin, Karen ; Cannon-Albright, Lisa A. ; Diver, W. Ryan ; Link, Brian K. ; Weiner, George J. ; Conde, Lucia ; Bracci, Paige M. ; Riby, Jacques ; Arnett, Donna K. ; Zhi, Degui ; Leach, Justin M. ; Holly, Elizabeth A. ; Jackson, Rebecca D. ; Tinker, Lesley F. ; Benavente, Yolanda ; Sala, Nuria ; Casabonne, Delphine ; Becker, Nikolaus ; Boffetta, Paolo ; Brennan, Paul ; Foretova, Lenka ; Maynadie, Marc ; McKay, James ; Staines, Anthony ; Chaffee, Kari G. ; Achenbach, Sara J. ; Vachon, Celine M ; Goldin, Lynn R. ; Strom, Sara S. ; Leis, Jose F. ; Weinberg, J. Brice ; Caporaso, Neil E. ; Norman, Aaron D. ; De Roos, Anneclaire J. ; Morton, Lindsay M. ; Severson, Richard K. ; Riboli, Elio ; Vineis, Paolo ; Kaaks, Rudolph ; Masala, Giovanna ; Weiderpass, Elisabete ; Chirlaque, Maria Dolores ; Vermeulen, Roel C H ; Travis, Ruth C. ; Southey, Melissa C. ; Milne, Roger L. ; Albanes, Demetrius ; Virtamo, Jarmo ; Weinstein, Stephanie ; Clavel, Jacqueline ; Zheng, Tongzhang ; Holford, Theodore R. ; Villano, Danylo J. ; Maria, Ann ; Spinelli, John J. ; Gascoyne, Randy D. ; Connors, Joseph M. ; Bertrand, Kimberly A. ; Giovannucci, Edward ; Kraft, Peter ; Kricker, Anne ; Turner, Jenny ; Ennas, Maria Grazia ; Ferri, Giovanni M. ; Miligi, Lucia ; Liang, Liming ; Ma, Baoshan ; Huang, Jinyan ; Crouch, Simon ; Park, Ju Hyun ; Chatterjee, Nilanjan ; North, Kari E. ; Snowden, John A. ; Wright, Josh ; Fraumeni, Joseph F. ; Offit, Kenneth ; Wu, Xifeng ; De Sanjose, Silvia ; Cerhan, James R ; Chanock, Stephen J. ; Rothman, Nathaniel ; Slager, Susan L. / Meta-analysis of genome-wide association studies discovers multiple loci for chronic lymphocytic leukemia. In: Nature Communications. 2016 ; Vol. 7.
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abstract = "Chronic lymphocytic leukemia (CLL) is a common lymphoid malignancy with strong heritability. To further understand the genetic susceptibility for CLL and identify common loci associated with risk, we conducted a meta-analysis of four genome-wide association studies (GWAS) composed of 3,100 cases and 7,667 controls with follow-up replication in 1,958 cases and 5,530 controls. Here we report three new loci at 3p24.1 (rs9880772, EOMES, P=2.55 × 10-11), 6p25.2 (rs73718779, SERPINB6, P=1.97 × 10-8) and 3q28 (rs9815073, LPP, P=3.62 × 10-8), as well as a new independent SNP at the known 2q13 locus (rs9308731, BCL2L11, P=1.00 × 10-11) in the combined analysis. We find suggestive evidence (P",
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AU - Zeleniuch-Jacquotte, Anne

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AU - Montalvan, Rebecca

AU - Burdett, Laurie

AU - Hutchinson, Amy

AU - Ye, Yuanqing

AU - Call, Timothy G.

AU - Shanafelt, Tait D.

AU - Novak, Anne J

AU - Kay, Neil Elliot

AU - Liebow, Mark

AU - Cunningham, Julie M

AU - Allmer, Cristine

AU - Hjalgrim, Henrik

AU - Adami, Hans Olov

AU - Melbye, Mads

AU - Glimelius, Bengt

AU - Chang, Ellen T.

AU - Glenn, Martha

AU - Curtin, Karen

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AU - Diver, W. Ryan

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AU - Weiner, George J.

AU - Conde, Lucia

AU - Bracci, Paige M.

AU - Riby, Jacques

AU - Arnett, Donna K.

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AU - Leach, Justin M.

AU - Holly, Elizabeth A.

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AU - Tinker, Lesley F.

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AU - Achenbach, Sara J.

AU - Vachon, Celine M

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AU - Strom, Sara S.

AU - Leis, Jose F.

AU - Weinberg, J. Brice

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AU - Norman, Aaron D.

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AU - Chirlaque, Maria Dolores

AU - Vermeulen, Roel C H

AU - Travis, Ruth C.

AU - Southey, Melissa C.

AU - Milne, Roger L.

AU - Albanes, Demetrius

AU - Virtamo, Jarmo

AU - Weinstein, Stephanie

AU - Clavel, Jacqueline

AU - Zheng, Tongzhang

AU - Holford, Theodore R.

AU - Villano, Danylo J.

AU - Maria, Ann

AU - Spinelli, John J.

AU - Gascoyne, Randy D.

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AU - Giovannucci, Edward

AU - Kraft, Peter

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AU - Turner, Jenny

AU - Ennas, Maria Grazia

AU - Ferri, Giovanni M.

AU - Miligi, Lucia

AU - Liang, Liming

AU - Ma, Baoshan

AU - Huang, Jinyan

AU - Crouch, Simon

AU - Park, Ju Hyun

AU - Chatterjee, Nilanjan

AU - North, Kari E.

AU - Snowden, John A.

AU - Wright, Josh

AU - Fraumeni, Joseph F.

AU - Offit, Kenneth

AU - Wu, Xifeng

AU - De Sanjose, Silvia

AU - Cerhan, James R

AU - Chanock, Stephen J.

AU - Rothman, Nathaniel

AU - Slager, Susan L

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N2 - Chronic lymphocytic leukemia (CLL) is a common lymphoid malignancy with strong heritability. To further understand the genetic susceptibility for CLL and identify common loci associated with risk, we conducted a meta-analysis of four genome-wide association studies (GWAS) composed of 3,100 cases and 7,667 controls with follow-up replication in 1,958 cases and 5,530 controls. Here we report three new loci at 3p24.1 (rs9880772, EOMES, P=2.55 × 10-11), 6p25.2 (rs73718779, SERPINB6, P=1.97 × 10-8) and 3q28 (rs9815073, LPP, P=3.62 × 10-8), as well as a new independent SNP at the known 2q13 locus (rs9308731, BCL2L11, P=1.00 × 10-11) in the combined analysis. We find suggestive evidence (P

AB - Chronic lymphocytic leukemia (CLL) is a common lymphoid malignancy with strong heritability. To further understand the genetic susceptibility for CLL and identify common loci associated with risk, we conducted a meta-analysis of four genome-wide association studies (GWAS) composed of 3,100 cases and 7,667 controls with follow-up replication in 1,958 cases and 5,530 controls. Here we report three new loci at 3p24.1 (rs9880772, EOMES, P=2.55 × 10-11), 6p25.2 (rs73718779, SERPINB6, P=1.97 × 10-8) and 3q28 (rs9815073, LPP, P=3.62 × 10-8), as well as a new independent SNP at the known 2q13 locus (rs9308731, BCL2L11, P=1.00 × 10-11) in the combined analysis. We find suggestive evidence (P

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