Post-GWAS gene-environment interplay in breast cancer: Results from the Breast and Prostate Cancer Cohort Consortium and a meta-analysis on 79 000 women

Human Molecular Genetics

Volumn 23, Issue 19, 2014, Pages 5260-5270

  Barrdahl, Myrto ^a   Canzian, Federico ^b   Joshi, Amit D ^c   Travis, Ruth C ^d   Chang Claude, Jenny ^a   Auer, Paul L ^e,f   Gapstur, Susan M ^g   Gaudet, Mia ^g   Diver, W Ryan ^g   Henderson, Brian E ^h   Haiman, Christopher A ^h   Schumacher, Fredrick R ^h   Le Marchand, Loïc ⁱ   Berg, Christine D ^j   Chanock, Stephen J ^j   Hoover, Robert N ^j   Rudolph, Anja ^a   Ziegler, Regina G ^j   Giles, Graham G ^k,l,m   Baglietto, Laura ^k,l   Severi, Gianluca ^k,l   Hankinson, Susan E ^c,n,o   Lindström, Sara ^c   Willet, Walter ^c   Hunter, David J ^c   Buring, Julie E ^c   Lee, I Min ^c   Zhang, Shumin ^c   Dossus, Laure ^p,q   Cox, David G ^r,s,t,u,v   Khaw, Kay Tee ^w   Lund, Eiliv ^x   Naccarati, Alessio ^y   Peeters, Petra H ^r,z   Quirós, J Ramón ^aa   Riboli, Elio ^r   Sund, Malin ^ab   Trichopoulos, Dimitrios ^c,ac,ad   Prentice, Ross L ^e   Kraft, Peter ^c   Kaaks, Rudolf ^a   Campa, Daniele ^a   more..

^a Division of Cancer Epidemiology   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Fred Hutchinson Cancer Research Center   (United States)

^f UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^g AMERICAN CANCER SOCIETY   (United States)

^h UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

ⁱ UNIVERSITY OF HAWAII   (United States)

^j NATIONAL CANCER INSTITUTE   (United States)

^k CANCER EPIDEMIOLOGY CENTRE   (Australia)

^l UNIVERSITY OF MELBOURNE   (Australia)

^m MONASH UNIVERSITY   (Australia)

ⁿ BRIGHAM AND WOMEN S HOSPITAL   (United States)

^o UNIVERSITY OF MASSACHUSETTS   (United States)

^p INSTITUT GUSTAVE ROUSSY   (France)

^q UNIVERSITÉ PARIS SACLAY   (France)

^r IMPERIAL COLLEGE LONDON   (United Kingdom)

^s UNIVERSITÉ LYON 1   (France)

^t INSERM   (France)

^u CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^v CENTRE LÉON BÉRARD   (France)

^w UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^x UNIVERSITY OF TROMSØ   (Norway)

^y Human Genetics Foundation   (Italy)

^z UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^aa PUBLIC HEALTH DIRECTORATE   (Spain)

^ab UMEÅ UNIVERSITY   (Sweden)

^ac BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^ad HELLENIC HEALTH FOUNDATION   (Greece)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 2; PROGESTERONE RECEPTOR; TUMOR MARKER;

ALCOHOL CONSUMPTION; ALLELE; ARTICLE; BODY HEIGHT; BODY MASS; BREAST CANCER; CANCER PROGNOSIS; CANCER RISK; CANCER SIZE; CANCER STAGING; CASE CONTROL STUDY; FAMILY HISTORY; FEMALE; GENETIC ASSOCIATION; GENETIC RISK; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; MENARCHE; MENOPAUSE; META ANALYSIS; PARITY; PREGNANCY; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SMOKING; BREAST NEOPLASMS; CHROMOSOME MAP; GENETIC PREDISPOSITION; GENOTYPE; RISK;

ALLELES; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CASE-CONTROL STUDIES; CHROMOSOME MAPPING; FEMALE; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK;

EID: 84929481929     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu223     Document Type: Article

References (60)

1. Easton, D.F., Pooley, K.A., Dunning, A.M., Pharoah, P.D., Thompson, D., Ballinger, D.G., Struewing, J.P., Morrison, J., Field, H., Luben, R. et al. (2007) Genome-wide association study identifies novel breast cancer susceptibility loci. Nature, 447, 1087-1093.
2. Stacey, S.N., Manolescu, A., Sulem, P., Rafnar, T., Gudmundsson, J., Gudjonsson, S.A., Masson, G., Jakobsdottir, M., Thorlacius, S., Helgason, A. et al. (2007) Common variants on chromosomes 2q35 and 16q12 confer susceptibility to estrogen receptor-positive breast cancer. Nat. Genet., 39, 865-869.
3. Murabito, J.M., Rosenberg, C.L., Finger, D., Kreger, B.E., Levy, D., Splansky, G.L., Antman, K. and Hwang, S.J. (2007) A genome-wide association study of breast and prostate cancer in the NHLBI's Framingham Heart Study. BMC Med. Genet., 8 (Suppl. 1), S6.
4. Cox, A., Dunning, A.M., Garcia-Closas, M., Balasubramanian, S., Reed, M.W., Pooley, K.A., Scollen, S., Baynes, C., Ponder, B.A., Chanock, S. et al. (2007)A common coding variant in CASP8 is associated with breast cancer risk. Nat. Genet., 39, 352-358.
5. Stacey, S.N., Manolescu, A., Sulem, P., Thorlacius, S., Gudjonsson, S.A., Jonsson, G.F., Jakobsdottir, M., Bergthorsson, J.T., Gudmundsson, J., Aben, K.K. et al. (2008) Common variants on chromosome 5p12 confer susceptibility to estrogen receptor-positive breast cancer. Nat. Genet., 40, 703-706.
6. Gold, B., Kirchhoff, T., Stefanov, S., Lautenberger, J., Viale, A., Garber, J., Friedman, E., Narod, S., Olshen, A.B., Gregersen, P. et al. (2008) Genome-wide association study provides evidence for a breast cancer risk locus at 6q22.33. Proc. Natl Acad. Sci. USA, 105, 4340-4345.
7. Zheng, W., Long, J., Gao, Y.T., Li, C., Zheng, Y., Xiang, Y.B., Wen, W., Levy, S., Deming, S.L., Haines, J.L. et al. (2009) Genome-wide association study identifies a new breast cancer susceptibility locus at 6q25.1. Nat. Genet., 41, 324-328.
8. Ahmed, S., Thomas, G., Ghoussaini, M., Healey, C.S., Humphreys, M.K., Platte, R., Morrison, J., Maranian, M., Pooley, K.A., Luben, R. et al. (2009) Newlydiscovered breast cancer susceptibility loci on 3p24 and 17q23.2. Nat. Genet., 41, 585-590.
9. Thomas, G., Jacobs, K.B., Kraft, P., Yeager, M., Wacholder, S., Cox, D.G., Hankinson, S.E., Hutchinson, A., Wang, Z., Yu, K. et al. (2009)Amultistage genome-wide association study in breast cancer identifies two new risk alleles at 1p11.2 and 14q24.1 (RAD51L1). Nat. Genet., 41, 579-584.
10. Turnbull, C., Ahmed, S., Morrison, J., Pernet, D., Renwick, A., Maranian, M., Seal, S., Ghoussaini, M., Hines, S., Healey, C.S. et al. (2010) Genomewide association study identifies five new breast cancer susceptibility loci. Nat. Genet., 42, 504-507.
11. Gaudet, M.M., Kirchhoff, T., Green, T., Vijai, J., Korn, J.M., Guiducci, C., Segre, A.V., McGee, K., McGuffog, L., Kartsonaki, C. et al. (2010) Common genetic variants and modification of penetrance of BRCA2-associated breast cancer. PLoS Genet., 6, e1001183.
12. Haiman, C.A., Chen, G.K., Vachon, C.M., Canzian, F., Dunning, A., Millikan, R.C., Wang, X., Ademuyiwa, F., Ahmed, S., Ambrosone, C.B. et al. (2011) A common variant at the TERT-CLPTM1L locus is associated with estrogen receptor-negative breast cancer. Nat. Genet., 43, 1210-1214.
13. Long, J., Cai, Q., Sung, H., Shi, J., Zhang, B., Choi, J.Y., Wen, W., Delahanty, R.J., Lu, W., Gao, Y.T. et al. (2012) Genome-wide association study in east Asians identifies novel susceptibility loci for breast cancer. PLoS Genet., 8, e1002532.
14. Kim, H.C., Lee, J.Y., Sung, H., Choi, J.Y., Park, S.K., Lee, K.M., Kim, Y.J., Go, M.J., Li, L., Cho, Y.S. et al. (2012) A genome-wide association study identifies a breast cancer risk variant in ERBB4 at 2q34: results from the Seoul Breast Cancer Study. Breast Cancer Res., 14, R56.
15. Siddiq, A., Couch, F., Chen, G., Lindström, S., Eccles, D., Millikan, R., Michailidou, K., Stram, D., Beckmann, L., Rhie, S. et al. (2012) A meta-analysis of genome-wide association studies of breast cancer identifies two novel susceptibility loci at 6q14 and 20q11. Hum. Mol. Genet., 21, 5373-5384.
16. Antoniou, A.C., Kuchenbaecker, K.B., Soucy, P., Beesley, J., Chen, X., McGuffog, L., Lee, A., Barrowdale, D., Healey, S., Sinilnikova, O.M. et al. (2012) Common variants at 12p11, 12q24, 9p21, 9q31.2 and in ZNF365 are associated with breast cancer risk for BRCA1 and/or BRCA2 mutation carriers. Breast Cancer Res., 14, R33.
17. Lambrechts, D., Truong, T., Justenhoven, C., Humphreys, M.K., Wang, J., Hopper, J.L., Dite, G.S., Apicella, C., Southey, M.C., Schmidt, M.K. et al. (2012) 11q13 is a susceptibility locus for hormone receptor positive breast cancer. Hum. Mutat., 33, 1123-1132.
18. Travis, R.C., Reeves, G.K., Green, J., Bull, D., Tipper, S.J., Baker, K., Beral, V., Peto, R., Bell, J., Zelenika, D. et al. (2010) Gene-environment interactions in 7610 women with breast cancer: prospective evidence from the Million Women Study. Lancet, 375, 2143-2151.
19. Milne, R.L., Gaudet, M.M., Spurdle, A.B., Fasching, P.A., Couch, F.J., Benitez, J., Arias Perez, J.I., Zamora, M.P., Malats, N., Dos Santos Silva, I. et al. (2010) Assessing interactions between the associations of common genetic susceptibility variants, reproductive history and body mass index with breast cancer risk in the breast cancer association consortium: a combined case-control study. Breast Cancer Res., 12, R110.
20. Prentice, R.L., Huang, Y., Hinds, D.A., Peters, U., Pettinger, M., Cox, D.R., Beilharz, E., Chlebowski, R.T., Rossouw, J.E., Caan, B. et al. (2009) Variation in the FGFR2 gene and the effects of postmenopausal hormone therapy on invasive breast cancer. Cancer Epidemiol. Biomarkers Prev., 18, 3079-3085.
21. Campa, D., Kaaks, R., Le Marchand, L., Haiman, C.A., Travis, R.C., Berg, C.D., Buring, J.E., Chanock, S.J., Diver, W.R., Dostal, L. et al. (2011) Interactions between genetic variants and breast cancer risk factors in the breast and prostate cancer cohort consortium. J. Natl. Cancer Inst., 103, 1252-1263.
22. Nickels, S., Truong, T., Hein, R., Stevens, K., Buck, K., Behrens, S., Eilber, U., Schmidt, M., Haberle, L., Vrieling, A. et al. (2013) Evidence of geneenvironment interactions between common breast cancer susceptibility loci and established environmental risk factors. PLoS Genet., 9, e1003284.
23. Sueta, A., Ito, H., Kawase, T., Hirose, K., Hosono, S., Yatabe, Y., Tajima, K., Tanaka, H., Iwata, H., Iwase, H. et al. (2012) A genetic risk predictor for breast cancer using a combination of low-penetrance polymorphisms in a Japanese population. Breast Cancer Res. Treat., 132, 711-721.
24. Fletcher, O., Johnson, N., Orr, N., Hosking, F.J., Gibson, L.J., Walker, K., Zelenika, D., Gut, I., Heath, S., Palles, C. et al. (2011) Novel breast cancer susceptibility locus at 9q31.2: results of a genome-wide association study. J. Natl. Cancer Inst., 103, 425-435.
25. Cai, Q., Long, J., Lu, W., Qu, S., Wen, W., Kang, D., Lee, J.Y., Chen, K., Shen, H., Shen, C.Y. et al. (2011) Genome-wide association study identifies breast cancer risk variant at 10q21.2: results from the Asia Breast Cancer Consortium. Hum. Mol. Genet., 20, 4991-4999.
26. Palmer, J.R., Ruiz-Narvaez, E.A., Rotimi, C.N., Cupples, L.A., Cozier, Y.C., Adams-Campbell, L.L. and Rosenberg, L. (2013) Genetic susceptibility Loci for subtypes of breast cancer in an African American population. Cancer Epidemiol. Biomarkers Prev., 22, 127-134.
27. Milne, R.L., Benitez, J., Nevanlinna, H., Heikkinen, T., Aittomaki, K., Blomqvist, C., Arias, J.I., Zamora, M.P., Burwinkel, B., Bartram, C.R. et al. (2009) Risk of estrogen receptor-positive and -negative breast cancer and single-nucleotide polymorphism 2q35-rs13387042. J. Natl. Cancer Inst., 101, 1012-1018.
28. Broeks, A., Schmidt, M.K., Sherman, M.E., Couch, F.J., Hopper, J.L., Dite, G.S., Apicella, C., Smith, L.D., Hammet, F., Southey, M.C. et al. (2011)Low penetrance breast cancer susceptibility loci are associated with specific breast tumor subtypes: findings from the Breast Cancer Association Consortium. Hum. Mol. Genet., 20, 3289-3303.
29. Thomas, D. (2010) Gene-environment-wide association studies: emerging approaches. Nat. Rev. Genet., 11, 259-272.
30. García-Closas, M.N., Malats, N., Silverman, D., Dosemeci, M., Kogevinas, M., Hein, D.W., Tardón, A., Serra, C., Carrato, A., García-Closas, R. et al. (2005) NAT2 slow acetylation and GSTM1 null genotypes increase bladder cancer risk: results fromtheSpanishBladderCancerStudyandmeta-analyses. Lancet, 20, 649-659.
31. Brooks, P.J., Goldman, D. and Li, T.K. (2009) Alleles of alcohol and acetaldehyde metabolism genes modulate susceptibility to oesophageal cancer from alcohol consumption. Hum. Genomics, 3, 103-105.
32. Wu, C., Kraft, P., Zhai, K., Chang, J., Wang, Z., Li, Y., Hu, Z., He, Z., Jia, W., Abnet, C.C. et al. (2012) Genome-wide association analyses of esophageal squamous cell carcinoma in Chinese identify multiple susceptibility loci and gene-environment interactions. Nat. Genet., 44, 1090-1097.
33. Whitfield, J.B., Dy, V., McQuilty, R., Zhu, G., Montgomery, G.W., Ferreira, M.A., Duffy, D.L., Neale, M.C., Heijmans, B.T., Heath, A.C. et al. (2007) Evidence of genetic effects on blood lead concentration. Environ. Health Perspect., 115, 1224-1230.
34. Chiba, M. and Masironi, R. (1992) Toxic and trace elements in tobacco and tobacco smoke. Bull. World Health Organ., 70, 269-275.
35. Chelchowska, M., Ambroszkiewicz, J., Jablonka-Salach, K., Gajewska, J., Maciejewski, T.M., Bulska, E., Laskowska-Klita, T. and Leibschang, J. (2013) Tobacco smoke exposure during pregnancy increases maternal blood lead levels affecting neonate birth weight. Biol. Trace Elem. Res., 155, 169-175.
36. Alatise, O.I. and Schrauzer, G.N. (2010) Lead exposure: a contributing cause of the current breast cancer epidemic in Nigerian women. Biol. Trace Elem. Res., 136, 127-139.
37. McElroy, J.A., Shafer, M.M., Gangnon, R.E., Crouch, L.A. and Newcomb, P.A. (2008) Urinary lead exposure and breast cancer risk in a population-based case-control study. Cancer Epidemiol. Biomarkers Prev., 17, 2311-2317.
38. Florea, A.M. and Busselberg, D. (2011) Metals and breast cancer: risk factors or healing agents? J. Toxicol., 2011, 159619.
39. Rashidi, M., Rameshat, M.H., Gharib, H., Rouzbahani, R., Ghias, M. and Poursafa, P. (2012) The association between spatial distribution of common malignancies and soil lead concentration in Isfahan, Iran. J. Res. Med. Sci., 17, 348-354.
40. Boyle, A.P., Hong, E.L., Hariharan, M., Cheng, Y., Schaub, M.A., Kasowski, M., Karczewski, K.J., Park, J., Hitz, B.C., Weng, S. et al. (2012) Annotation of functional variation in personal genomes using RegulomeDB. Genome Res., 22, 1790-1797.
41. Cornelis, M.C., Tchetgen, E.J., Liang, L., Qi, L., Chatterjee, N., Hu, F.B. and Kraft, P. (2012) Gene-environment interactions in genome-wide association studies: a comparative study of tests applied to empirical studies of type 2 diabetes. Am. J. Epidemiol., 175, 191-202.
42. Hamza, T.H., Chen, H., Hill-Burns, E.M., Rhodes, S.L., Montimurro, J., Kay, D.M., Tenesa, A., Kusel, V.I., Sheehan, P., Eaaswarkhanth, M. et al. (2011) Genome-wide gene-environment study identifies glutamate receptor gene GRIN2A as a Parkinson's disease modifier gene via interaction with coffee. PLoS Genet., 7, e1002237.
43. Hancock, D.B., Artigas, M.S., Gharib, S.A., Henry, A., Manichaikul, A., Ramasamy, A., Loth, D.W., Imboden, M., Koch, B., McArdle, W.L. et al. (2012) Genome-wide joint meta-analysis of SNP and SNP-by-smoking interaction identifies novel loci for pulmonary function. PLoS Genet., 8, e1003098.
44. Rudolph, A., Hein, R., Lindström, S., Beckmann, L., Behrens, S., Liu, J., Aschard, H., Bolla, M.K., Wang, J., Truong, T. et al. (2013) Genetic modifiers of menopausal hormone replacement therapy and breast 1 cancer risk: a genome-wide interaction study. Endocr. Relat. Cancer, 20, 875-887.
45. Tang, H., Wei, P., Duell, E.J., Risch, H.A., Olson, S.H., Bueno-de-Mesquita, H.B., Gallinger, S., Holly, E.A., Petersen, G.M., Bracci, P.M. et al. (2014) Genes-environment interactions in obesity- and diabetes-associated pancreatic cancer: a GWAS data analysis. Cancer Epidemiol. Biomarkers Prev., 23, 98-106.
46. Manning, A.K., LaValley, M., Liu, C.T., Rice, K., An, P., Liu, Y., Miljkovic, I., Rasmussen-Torvik, L., Harris, T.B., Province, M.A. et al. (2011) Meta-analysis of gene-environment interaction: joint estimation of SNP and SNP × environment regression coefficients. Genet. Epidemiol., 35, 11-18.
47. Hutter, C.M., Mechanic, L.E., Chatterjee, N., Kraft, P. and Gillanders, E.M. (2013) Gene-environment interactions in cancer epidemiology: a national cancer institute think tank report. Genet. Epidemiol., 37, 643-657.
48. Antoniou, A.C., Kartsonaki, C., Sinilnikova, O.M., Soucy, P., McGuffog, L., Healey, S., Lee, A., Peterlongo, P., Manoukian, S., Peissel, B. et al. (2011) Common alleles at 6q25.1 and 1p11.2 are associated with breast cancer risk for BRCA1 and BRCA2 mutation carriers. Hum. Mol. Genet., 20, 3304-3321.
49. Kraft, P. and Haiman, C.A. (2010)GWASidentifies a commonbreast cancer risk allele among BRCA1 carriers. Nat. Genet., 42, 819-820.
50. Hunter, D.J., Riboli, E., Haiman, C.A., Albanes, D., Altshuler, D., Chanock, S.J., Haynes, R.B., Henderson, B.E., Kaaks, R., Stram, D.O. et al. (2005) A candidate gene approach to searching for low-penetrance breast and prostate cancer genes. Nat. Rev. Cancer, 5, 977-985.
51. Riboli, E., Hunt, K.J., Slimani, N., Ferrari, P., Norat, T., Fahey, M., Charrondiere, U.R., Hemon, B., Casagrande, C., Vignat, J. et al. (2002) European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr., 5, 1113-1124.
52. Anderson, G., Cummings, S., Freedman, L.S., Furberg, C., Henderson, M., Johnson, S.R., Kuller, L., Manson, J., Oberman, A., Prentice, R.L. and Rossouw, J.E. (1998) Design of the Women's Health Initiative Clinical Trial and Observational Study. Control. Clin. Trials, 19, 61-109.
53. Giles, G.G. and English, D.R. (2002) The Melbourne Collaborative Cohort Study. IARC Sci. Publ., 156, 69-70.
54. Colditz, G.A. and Hankinson, S.E. (2005) The Nurses' Health Study: lifestyle and health among women. Nat. Rev. Cancer, 5, 388-396.
55. Rexrode, K., Lee, I., Cook, N., Hennekens, C.H. and Burning, J.E. (2000) Baseline characteristics of participants in the Women's Health Study. J. Womens Health Gend. Based Med., 9, 19-27.
56. Calle, E.E., Rodriguez, C., Jacobs, E.J., Almon, M.L., Chao, A., McCullough, M.L., Feigelson, H.S. and Thun, M.J. (2002) The American Cancer Society Cancer Prevention Study II Nutrition Cohort: rationale, study design, and baseline characteristics. Cancer, 94, 2490-2501.
57. Hayes, R.B., Reding, D., Kopp, W., Subar, A.F., Bhat, N., Rothman, N., Caporaso, N., Ziegler, R.G., Johnson, C.C., Weissfeld, J.L. et al. (2000) Etiologic and early marker studies in the prostate, lung, colorectal and ovarian (PLCO) cancer screening trial. Controlled Clinical Trials, 21, 349-355.
58. Kolonel, L.N., Henderson, B.E., Hankin, J.H., Nomura, A.M.Y., Wilkens, L.R., Pike, M.C., Stram, D.O., Monroe, K.R., Earle, M.E. and Nagamine, F.S. (2000) A Multiethnic Cohort in Hawaii and Los Angeles: Baseline Characteristics. Am. J. Epidemiol., 151, 346-357.
59. Michailidou, K., Hall, P., Gonzalez-Neira, A., Ghoussaini, M., Dennis, J., Milne, R.L., Schmidt, M.K., Chang-Claude, J., Bojesen, S.E., Bolla, M.K. et al. (2013) Large-scale genotyping identifies 41 new loci associated with breast cancer risk. Nat. Genet., 45, 353-361, 361e-2.
60. Gao, X., Starmer, J. and Martin, E.R. (2008) A multiple testing correction method for genetic association studies using correlated single nucleotide polymorphisms. Genet. Epidemiol., 32, 361-369.