Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32

Lucia Conde; Eran Halperin; Nicholas K. Akers; Kevin M. Brown; Karin E. Smedby; Nathaniel Rothman; Alexandra Nieters; Susan L. Slager; Angela Brooks-Wilson; Luz Agana; Jacques Riby; Jianjun Liu; Hans Olov Adami; Hatef Darabi; Henrik Hjalgrim; Hui Qi Low; Keith Humphreys; Mads Melbye; Ellen T. Chang; Bengt Glimelius; Wendy Cozen; Scott Davis; Patricia Hartge; Lindsay M. Morton; Maryjean Schenk; Sophia S. Wang; Bruce Armstrong; Anne Kricker; Sam Milliken; Mark P. Purdue; Claire M. Vajdic; Peter Boyle; Qing Lan; Shelia H. Zahm; Yawei Zhang; Tongzhang Zheng; Nikolaus Becker; Yolanda Benavente; Paolo Boffetta; Paul Brennan; Katja Butterbach; Pierluigi Cocco; Lenka Foretova; Marc Maynadié; Silvia De Sanjosé; Anthony Staines; John J. Spinelli; Sara J. Achenbach; Timothy G. Call; Nicola J. Camp; Martha Glenn; Neil E. Caporaso; James R. Cerhan; Julie M. Cunningham; Lynn R. Goldin; Curtis A. Hanson; Neil E. Kay; Mark C. Lanasa; Jose F. Leis; Gerald E. Marti; Kari G. Rabe; Laura Z. Rassenti; Logan G. Spector; Sara S. Strom; Celine M. Vachon; J. Brice Weinberg; Elizabeth A. Holly; Stephen Chanock; Martyn T. Smith; Paige M. Bracci; Christine F. Skibola

doi:10.1038/ng.626

Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32

Lucia Conde, Eran Halperin, Nicholas K. Akers, Kevin M. Brown, Karin E. Smedby, Nathaniel Rothman, Alexandra Nieters, Susan L. Slager, Angela Brooks-Wilson, Luz Agana, Jacques Riby, Jianjun Liu, Hans Olov Adami, Hatef Darabi, Henrik Hjalgrim, Hui Qi Low, Keith Humphreys, Mads Melbye, Ellen T. Chang, Bengt GlimeliusWendy Cozen, Scott Davis, Patricia Hartge, Lindsay M. Morton, Maryjean Schenk, Sophia S. Wang, Bruce Armstrong, Anne Kricker, Sam Milliken, Mark P. Purdue, Claire M. Vajdic, Peter Boyle, Qing Lan, Shelia H. Zahm, Yawei Zhang, Tongzhang Zheng, Nikolaus Becker, Yolanda Benavente, Paolo Boffetta, Paul Brennan, Katja Butterbach, Pierluigi Cocco, Lenka Foretova, Marc Maynadié, Silvia De Sanjosé, Anthony Staines, John J. Spinelli, Sara J. Achenbach, Timothy G. Call, Nicola J. Camp, Martha Glenn, Neil E. Caporaso, James R. Cerhan, Julie M. Cunningham, Lynn R. Goldin, Curtis A. Hanson, Neil E. Kay, Mark C. Lanasa, Jose F. Leis, Gerald E. Marti, Kari G. Rabe, Laura Z. Rassenti, Logan G. Spector, Sara S. Strom, Celine M. Vachon, J. Brice Weinberg, Elizabeth A. Holly, Stephen Chanock, Martyn T. Smith, Paige M. Bracci, Christine F. Skibola

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Abstract

To identify susceptibility loci for non-Hodgkin lymphoma subtypes, we conducted a three-stage genome-wide association study. We identified two variants associated with follicular lymphoma at 6p21.32 (rs10484561, combined P = 1.12 × 10^-29 and rs7755224, combined P = 2.00 × 10-19; r² = 1.0), supporting the idea that major histocompatibility complex genetic variation influences follicular lymphoma susceptibility. We also found confirmatory evidence of a previously reported association between chronic lymphocytic leukemia/small lymphocytic lymphoma and rs735665 (combined P = 4.24 × 10^-9).

Original language	English (US)
Pages (from-to)	661-664
Number of pages	4
Journal	Nature Genetics
Volume	42
Issue number	8
DOIs	https://doi.org/10.1038/ng.626
State	Published - Aug 2010

ASJC Scopus subject areas

Genetics

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Conde, L., Halperin, E., Akers, N. K., Brown, K. M., Smedby, K. E., Rothman, N., Nieters, A., Slager, S. L., Brooks-Wilson, A., Agana, L., Riby, J., Liu, J., Adami, H. O., Darabi, H., Hjalgrim, H., Low, H. Q., Humphreys, K., Melbye, M., Chang, E. T., ... Skibola, C. F. (2010). Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32. Nature Genetics, 42(8), 661-664. https://doi.org/10.1038/ng.626

Conde, L, Halperin, E, Akers, NK, Brown, KM, Smedby, KE, Rothman, N, Nieters, A, Slager, SL, Brooks-Wilson, A, Agana, L, Riby, J, Liu, J, Adami, HO, Darabi, H, Hjalgrim, H, Low, HQ, Humphreys, K, Melbye, M, Chang, ET, Glimelius, B, Cozen, W, Davis, S, Hartge, P, Morton, LM, Schenk, M, Wang, SS, Armstrong, B, Kricker, A, Milliken, S, Purdue, MP, Vajdic, CM, Boyle, P, Lan, Q, Zahm, SH, Zhang, Y, Zheng, T, Becker, N, Benavente, Y, Boffetta, P, Brennan, P, Butterbach, K, Cocco, P, Foretova, L, Maynadié, M, De Sanjosé, S, Staines, A, Spinelli, JJ, Achenbach, SJ, Call, TG, Camp, NJ, Glenn, M, Caporaso, NE, Cerhan, JR , Cunningham, JM, Goldin, LR, Hanson, CA, Kay, NE, Lanasa, MC, Leis, JF, Marti, GE, Rabe, KG, Rassenti, LZ, Spector, LG, Strom, SS, Vachon, CM, Weinberg, JB, Holly, EA, Chanock, S, Smith, MT, Bracci, PM & Skibola, CF 2010, 'Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32', Nature Genetics, vol. 42, no. 8, pp. 661-664. https://doi.org/10.1038/ng.626

@article{93a98bcf8844433cab8adde262f2c5e7,

title = "Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32",

abstract = "To identify susceptibility loci for non-Hodgkin lymphoma subtypes, we conducted a three-stage genome-wide association study. We identified two variants associated with follicular lymphoma at 6p21.32 (rs10484561, combined P = 1.12 × 10-29 and rs7755224, combined P = 2.00 × 10-19; r2 = 1.0), supporting the idea that major histocompatibility complex genetic variation influences follicular lymphoma susceptibility. We also found confirmatory evidence of a previously reported association between chronic lymphocytic leukemia/small lymphocytic lymphoma and rs735665 (combined P = 4.24 × 10-9).",

author = "Lucia Conde and Eran Halperin and Akers, {Nicholas K.} and Brown, {Kevin M.} and Smedby, {Karin E.} and Nathaniel Rothman and Alexandra Nieters and Slager, {Susan L.} and Angela Brooks-Wilson and Luz Agana and Jacques Riby and Jianjun Liu and Adami, {Hans Olov} and Hatef Darabi and Henrik Hjalgrim and Low, {Hui Qi} and Keith Humphreys and Mads Melbye and Chang, {Ellen T.} and Bengt Glimelius and Wendy Cozen and Scott Davis and Patricia Hartge and Morton, {Lindsay M.} and Maryjean Schenk and Wang, {Sophia S.} and Bruce Armstrong and Anne Kricker and Sam Milliken and Purdue, {Mark P.} and Vajdic, {Claire M.} and Peter Boyle and Qing Lan and Zahm, {Shelia H.} and Yawei Zhang and Tongzhang Zheng and Nikolaus Becker and Yolanda Benavente and Paolo Boffetta and Paul Brennan and Katja Butterbach and Pierluigi Cocco and Lenka Foretova and Marc Maynadi{\'e} and {De Sanjos{\'e}}, Silvia and Anthony Staines and Spinelli, {John J.} and Achenbach, {Sara J.} and Call, {Timothy G.} and Camp, {Nicola J.} and Martha Glenn and Caporaso, {Neil E.} and Cerhan, {James R.} and Cunningham, {Julie M.} and Goldin, {Lynn R.} and Hanson, {Curtis A.} and Kay, {Neil E.} and Lanasa, {Mark C.} and Leis, {Jose F.} and Marti, {Gerald E.} and Rabe, {Kari G.} and Rassenti, {Laura Z.} and Spector, {Logan G.} and Strom, {Sara S.} and Vachon, {Celine M.} and Weinberg, {J. Brice} and Holly, {Elizabeth A.} and Stephen Chanock and Smith, {Martyn T.} and Bracci, {Paige M.} and Skibola, {Christine F.}",

note = "Funding Information: This work was supported by grants CA122663 and CA104682 from the National Cancer Institute (NCI), US National Institutes of Health (NIH) (C.F.S.); grants Funding Information: CA45614 and CA89745 from the NCI, NIH (E.A.H.); the American Cancer Society (IRG-07-06401) and a charitable donation by S. Chase (K.B.). E.H. is a faculty fellow of the Edmond J. Safra Bioinformatics program at Tel-Aviv University. SCALE study: We thank X.Y. Chen, H.B. Toh, K.K. Heng and W.Y. Meah from Genome Institute of Singapore for their support in genotyping analyses. We are also grateful to L. Klareskog, Center for Molecular Medicine, and L. Alfredsson, Institute of Environmental Medicine at the Karolinska Institute, Stockholm, Sweden, for sharing DNA from their EIRA study control population and to E. Rehnberg for help with imputing genotypes in the SCALE study. The following agencies contributed funding to SCALE that facilitated the present project: Agency for Science and Technology and Research of Singapore (A*STAR), NCI, the Swedish Cancer Society, the Swedish Research Council and the Danish Medical Research Council. GEC-Mayo Study: This study is supported by grants R01 CA91253 and R01 CA118444 from the NCI. NCI-SEER study: We thank P. Hui of the Information Management Services, Inc. for programming support, and we acknowledge the contributions of the staff and scientists at the SEER centers of Iowa, Los Angeles, Detroit and Seattle for conducting the study{\textquoteright}s field effort. We especially acknowledge the contributions of study site principal investigator L. Bernstein (Los Angeles). The NCI-SEER study was supported by the Intramural Research Program of the NIH (NCI) and by US Public Health Service (PHS) contracts N01-PC-65064, N01-PC-67008, N01-PC-67009, N01-PC-67010 and N02-PC-71105. Yale study: This study is supported by grant CA62006 from the NCI and the Intramural Research Program of the NIH (NCI). NSW study: The NSW study was supported by a National Health and Medical Research Council of Australia project grant, Cancer Council NSW, a University of Sydney Medical Foundation Program Grant and the Intramural Research Program of the NIH (NCI). BC study: Funding for the British Columbia study was from the Canadian Cancer Society and the Canadian Institutes of Health Research. A.B.-W. is a Senior Scholar of the Michael Smith Foundation for Health Research. EpiLymph study: Funding was available from the German Jos{\'e} Carreras Leukemia Foundation (DJCLS_R04/08 and R07/26f) (A.N.), the EC 5th Framework Program Quality of Life grant No. QLK4-CT-2000-00422 (P. Boffetta, P. Brennan), the Federal Office for Radiation Protection grants No. StSch4261 and StSch4420 (Germany), the Spanish Ministry of Health grants Centro de Investigaci{\'o}n Biom{\'e}dica en Red de Epidemiolog{\'i}a y Salud P{\'u}blica (CIBERESP) (06/02/0073), FIS 08-1555 and Marato TV3 (051210) (Spain), La Fondation de France, no. 1999 0084 71 (M. Maynadi{\'e}), Compagnia di San Paolo di Torino, Programma Oncologia 2001 (P.C.), the Health Research Board, Ireland, and the Ministry of Health of the Czech Republic, MZ0 MOU 2005 (L.F.).",

year = "2010",

month = aug,

doi = "10.1038/ng.626",

language = "English (US)",

volume = "42",

pages = "661--664",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Publishing Group",

number = "8",

}

TY - JOUR

T1 - Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32

AU - Conde, Lucia

AU - Halperin, Eran

AU - Akers, Nicholas K.

AU - Brown, Kevin M.

AU - Smedby, Karin E.

AU - Rothman, Nathaniel

AU - Nieters, Alexandra

AU - Slager, Susan L.

AU - Brooks-Wilson, Angela

AU - Agana, Luz

AU - Riby, Jacques

AU - Liu, Jianjun

AU - Adami, Hans Olov

AU - Darabi, Hatef

AU - Hjalgrim, Henrik

AU - Low, Hui Qi

AU - Humphreys, Keith

AU - Melbye, Mads

AU - Chang, Ellen T.

AU - Glimelius, Bengt

AU - Cozen, Wendy

AU - Davis, Scott

AU - Hartge, Patricia

AU - Morton, Lindsay M.

AU - Schenk, Maryjean

AU - Wang, Sophia S.

AU - Armstrong, Bruce

AU - Kricker, Anne

AU - Milliken, Sam

AU - Purdue, Mark P.

AU - Vajdic, Claire M.

AU - Boyle, Peter

AU - Lan, Qing

AU - Zahm, Shelia H.

AU - Zhang, Yawei

AU - Zheng, Tongzhang

AU - Becker, Nikolaus

AU - Benavente, Yolanda

AU - Boffetta, Paolo

AU - Brennan, Paul

AU - Butterbach, Katja

AU - Cocco, Pierluigi

AU - Foretova, Lenka

AU - Maynadié, Marc

AU - De Sanjosé, Silvia

AU - Staines, Anthony

AU - Spinelli, John J.

AU - Achenbach, Sara J.

AU - Call, Timothy G.

AU - Camp, Nicola J.

AU - Glenn, Martha

AU - Caporaso, Neil E.

AU - Cerhan, James R.

AU - Cunningham, Julie M.

AU - Goldin, Lynn R.

AU - Hanson, Curtis A.

AU - Kay, Neil E.

AU - Lanasa, Mark C.

AU - Leis, Jose F.

AU - Marti, Gerald E.

AU - Rabe, Kari G.

AU - Rassenti, Laura Z.

AU - Spector, Logan G.

AU - Strom, Sara S.

AU - Vachon, Celine M.

AU - Weinberg, J. Brice

AU - Holly, Elizabeth A.

AU - Chanock, Stephen

AU - Smith, Martyn T.

AU - Bracci, Paige M.

AU - Skibola, Christine F.

N1 - Funding Information: This work was supported by grants CA122663 and CA104682 from the National Cancer Institute (NCI), US National Institutes of Health (NIH) (C.F.S.); grants Funding Information: CA45614 and CA89745 from the NCI, NIH (E.A.H.); the American Cancer Society (IRG-07-06401) and a charitable donation by S. Chase (K.B.). E.H. is a faculty fellow of the Edmond J. Safra Bioinformatics program at Tel-Aviv University. SCALE study: We thank X.Y. Chen, H.B. Toh, K.K. Heng and W.Y. Meah from Genome Institute of Singapore for their support in genotyping analyses. We are also grateful to L. Klareskog, Center for Molecular Medicine, and L. Alfredsson, Institute of Environmental Medicine at the Karolinska Institute, Stockholm, Sweden, for sharing DNA from their EIRA study control population and to E. Rehnberg for help with imputing genotypes in the SCALE study. The following agencies contributed funding to SCALE that facilitated the present project: Agency for Science and Technology and Research of Singapore (A*STAR), NCI, the Swedish Cancer Society, the Swedish Research Council and the Danish Medical Research Council. GEC-Mayo Study: This study is supported by grants R01 CA91253 and R01 CA118444 from the NCI. NCI-SEER study: We thank P. Hui of the Information Management Services, Inc. for programming support, and we acknowledge the contributions of the staff and scientists at the SEER centers of Iowa, Los Angeles, Detroit and Seattle for conducting the study’s field effort. We especially acknowledge the contributions of study site principal investigator L. Bernstein (Los Angeles). The NCI-SEER study was supported by the Intramural Research Program of the NIH (NCI) and by US Public Health Service (PHS) contracts N01-PC-65064, N01-PC-67008, N01-PC-67009, N01-PC-67010 and N02-PC-71105. Yale study: This study is supported by grant CA62006 from the NCI and the Intramural Research Program of the NIH (NCI). NSW study: The NSW study was supported by a National Health and Medical Research Council of Australia project grant, Cancer Council NSW, a University of Sydney Medical Foundation Program Grant and the Intramural Research Program of the NIH (NCI). BC study: Funding for the British Columbia study was from the Canadian Cancer Society and the Canadian Institutes of Health Research. A.B.-W. is a Senior Scholar of the Michael Smith Foundation for Health Research. EpiLymph study: Funding was available from the German José Carreras Leukemia Foundation (DJCLS_R04/08 and R07/26f) (A.N.), the EC 5th Framework Program Quality of Life grant No. QLK4-CT-2000-00422 (P. Boffetta, P. Brennan), the Federal Office for Radiation Protection grants No. StSch4261 and StSch4420 (Germany), the Spanish Ministry of Health grants Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP) (06/02/0073), FIS 08-1555 and Marato TV3 (051210) (Spain), La Fondation de France, no. 1999 0084 71 (M. Maynadié), Compagnia di San Paolo di Torino, Programma Oncologia 2001 (P.C.), the Health Research Board, Ireland, and the Ministry of Health of the Czech Republic, MZ0 MOU 2005 (L.F.).

PY - 2010/8

Y1 - 2010/8

N2 - To identify susceptibility loci for non-Hodgkin lymphoma subtypes, we conducted a three-stage genome-wide association study. We identified two variants associated with follicular lymphoma at 6p21.32 (rs10484561, combined P = 1.12 × 10-29 and rs7755224, combined P = 2.00 × 10-19; r2 = 1.0), supporting the idea that major histocompatibility complex genetic variation influences follicular lymphoma susceptibility. We also found confirmatory evidence of a previously reported association between chronic lymphocytic leukemia/small lymphocytic lymphoma and rs735665 (combined P = 4.24 × 10-9).

AB - To identify susceptibility loci for non-Hodgkin lymphoma subtypes, we conducted a three-stage genome-wide association study. We identified two variants associated with follicular lymphoma at 6p21.32 (rs10484561, combined P = 1.12 × 10-29 and rs7755224, combined P = 2.00 × 10-19; r2 = 1.0), supporting the idea that major histocompatibility complex genetic variation influences follicular lymphoma susceptibility. We also found confirmatory evidence of a previously reported association between chronic lymphocytic leukemia/small lymphocytic lymphoma and rs735665 (combined P = 4.24 × 10-9).

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U2 - 10.1038/ng.626

DO - 10.1038/ng.626

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AN - SCOPUS:77955091394

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VL - 42

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EP - 664

JO - Nature Genetics

JF - Nature Genetics

IS - 8

ER -

Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32

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