A genome-wide association study to identify genetic susceptibility loci that modify ductal and lobular postmenopausal breast cancer risk associated with menopausal hormone therapy use: A two-stage design with replication

Breast Cancer Research and Treatment

Volumn 138, Issue 2, 2013, Pages 529-542

  Hein, Rebecca ^a,b   Flesch Janys, Dieter ^c   Dahmen, Norbert ^d   Beckmann, Lars ^a,e   Lindström, Sara ^f   Schoof, Nils ^g   Czene, Kamila ^g   Mittelstraß, Kirstin ^h   Illig, Thomas ^h,i   Seibold, Petra ^a   Behrens, Sabine ^a   Humphreys, Keith ^g   Li, Jingmei ^j   Liu, Jianjun ^j   Olson, Janet E ^k   Wang, Xianshu ^k   Hankinson, Susan E ^f   Truong, Thérèse ^l,m   Menegaux, Florence ^l,m   Dos Santos Silva, Isabel ⁿ   Johnson, Nichola ^o   Chen, Shou Tung ^q   Yu, Jyh Cherng ^r   Ziogas, Argyrios ^s   Kataja, Vesa ^t,u   Kosma, Veli Matti ^t,u   Mannermaa, Arto ^t,u   Anton Culver, Hoda ^v   Shen, Chen Yang ^w,x   Brauch, Hiltrud ^p   Peto, Julian ⁿ   Guénel, Pascal ^l,m   Kraft, Peter ^f   Couch, Fergus J ^k   Easton, Douglas F ^y   Hall, Per ^g   Chang Claude, Jenny ^a   more..

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d Congenics AG ^*  (Germany)

^e INSTITUTE FOR QUALITY AND EFFICIENCY IN HEALTH CARE IQWIG   (Germany)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^g KAROLINSKA INSTITUTE   (Sweden)

^h INSTITUTE OF EPIDEMIOLOGY   (Germany)

ⁱ HANNOVER MEDICAL SCHOOL   (Germany)

^j GENOME INSTITUTE OF SINGAPORE   (Singapore)

^k MAYO CLINIC   (United States)

^l NATIONAL INSTITUTES OF HEALTH   (United States)

^m CENTRE FOR RESEARCH IN EPIDEMIOLOGY AND POPULATION HEALTH   (France)

ⁿ LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^o INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^p UNIVERSITY OF TÜBINGEN   (Germany)

^q CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^r TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^s UNIVERSITY OF CALIFORNIA   (United States)

^t UNIVERSITY OF EASTERN FINLAND   (Finland)

^u KUOPIO UNIVERSITY HOSPITAL   (Finland)

^v UNIVERSITY OF CALIFORNIA   (United States)

^w INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^x Taiwan Biobank   (Taiwan)

^y UNIVERSITY OF CAMBRIDGE   (United Kingdom)

more..

Author keywords

Case only study; Gene environment interaction; Genome wide association study; Menopausal hormone therapy; Polymorphisms; Postmenopausal breast cancer risk

Indexed keywords

THYROID HORMONE RECEPTOR; TUMOR PROTEIN;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER RISK; CHROMOSOME 18; CHROMOSOME 2; CHROMOSOME 7; CONTROLLED STUDY; DELTA NOTCH LIKE EPIDERMAL GROWTH FACTOR LIKE REPEAT CONTAINING GENE; FEMALE; GENE IDENTIFICATION; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HORMONAL THERAPY; HUMAN; MAJOR CLINICAL STUDY; MENOPAUSAL HORMONE THERAPY; POSTMENOPAUSE; PRIORITY JOURNAL; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; SUPPRESSOR OF VARIEGATION ENHANCER OF ZESTE AND TRITHORAX BINDING PROTEIN 1 GENE; THYROID HORMONE RECEPTOR INTERACTOR 12 GENE; TUMOR GENE; TUMOR INVASION;

BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, LOBULAR; CASE-CONTROL STUDIES; CHROMOSOMES, HUMAN; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; GENETIC LOCI; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; POSTMENOPAUSE; PROGESTINS; RISK FACTORS; SEQUENCE ANALYSIS, DNA;

EID: 84879415699     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-013-2443-z     Document Type: Article

References (55)

1. Beral V (2003) Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 362(9382):419-427 (Pubitemid 36999703)
2. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 288(3):321-333 (Pubitemid 34761611)
3. Horwitz K, Clarke C (1998) Estrogens and progestins in mammary development and neoplasia. Introduction. J Mammary Gland Biol Neoplasia 3(1):1-2
4. Zumoff B (1998) Does postmenopausal estrogen administration increase the risk of breast cancer? Contributions of animal, biochemical, and clinical investigative studies to a resolution of the controversy. Proc Soc Exp Biol Med 217(1):30-37
5. Poutanen M, Isomaa V, Peltoketo H, Vihko R (1995) Role of 17 beta-hydroxysteroid dehydrogenase type 1 in endocrine and intracrine estradiol biosynthesis. J Steroid Biochem Mol Biol 55(5-6):525-532 (Pubitemid 26019338)
6. Pawlak KJ, Wiebe JP (2007) Regulation of estrogen receptor (ER) levels in MCF-7 cells by progesterone metabolites. J Steroid Biochem Mol Biol 107(3-5):172-179 (Pubitemid 47380373)
7. Wiebe JP (2006) Progesterone metabolites in breast cancer. Endocr Relat Cancer 13(3):717-738 (Pubitemid 44763254)
8. Wiebe JP, Souter L, Zhang G (2006) Dutasteride affects progesterone metabolizing enzyme activity/expression in human breast cell lines resulting in suppression of cell proliferation and detachment. J Steroid Biochem Mol Biol 100(4-5):129-140 (Pubitemid 44175837)
9. Collaborative Group on Hormonal Factors in Breast Cancer (1997) Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Lancet 350(9084):1047-1059 (Pubitemid 27437855)
10. Flesch-Janys D, Slanger T, Mutschelknauss E, Kropp S, Obi N, Vettorazzi E, Braendle W, Bastert G, Hentschel S, Berger J, Chang-Claude J (2008) Risk of different histological types of postmenopausal breast cancer by type and regimen of menopausal hormone therapy. Int J Cancer 123(4):933-941 (Pubitemid 352032424)
11. Chlebowski RT, Anderson GL, Gass M, Lane DS, Aragaki AK, Kuller LH, Manson JE, Stefanick ML, Ockene J, Sarto GE, Johnson KC, Wactawski-Wende J, Ravdin PM, Schenken R, Hendrix SL, Rajkovic A, Rohan TE, Yasmeen S, Prentice RL (2010) Estrogen plus progestin and breast cancer incidence and mortality in postmenopausal women. JAMA 304(15):1684-1692
12. Li CI (2004) Postmenopausal hormone therapy and the risk of breast cancer: the view of an epidemiologist. Maturitas 49(1):44-50 (Pubitemid 39209370)
13. Newcomb PA, Titus-Ernstoff L, Egan KM, Trentham-Dietz A, Baron JA, Storer BE, Willett WC, Stampfer MJ (2002) Postmenopausal estrogen and progestin use in relation to breast cancer risk. Cancer Epidemiol Biomarkers Prev 11(7):593-600 (Pubitemid 34760816)
14. Ross RK, Paganini-Hill A, Wan PC, Pike MC (2000) Effect of hormone replacement therapy on breast cancer risk: estrogen versus estrogen plus progestin. J Natl Cancer Inst 92(4):328-332 (Pubitemid 30117736)
15. Schairer C, Lubin J, Troisi R, Sturgeon S, Brinton L, Hoover R (2000) Menopausal estrogen and estrogen-progestin replacement therapy and breast cancer risk. JAMA 283(4):485-491 (Pubitemid 30062864)
16. Seeger H, Mueck AO (2008) Are the progestins responsible for breast cancer risk during hormone therapy in the postmenopause? Experimental vs. clinical data. J Steroid Biochem Mol Biol 109(1-2):11-15
17. Shah NR, Borenstein J, Dubois RW (2005) Postmenopausal hormone therapy and breast cancer: a systematic review and meta-analysis. Menopause 12(6):668-678 (Pubitemid 41669118)
18. Rusner C, Bandemer-Greulich U, Engel J, Stegmaier C, Zawinell A, Holleczek B, Katalinic A, Kuss O, Schmidt-Pokrzywniak A, Schubert-Fritschle G, Tillack A, Stang A (2012) Population-based hormone receptor-specific incidence trends of breast cancer in Germany. Maturitas 73(2):152-157
19. Sprague BL, Trentham-Dietz A, Cronin KA (2012) A sustained decline in postmenopausal hormone use: results from the National Health and Nutrition Examination Survey, 1999-2010. Obstet Gynecol 120(3):595-603
20. Canfell K, Banks E, Clements M, Kang YJ, Moa A, Armstrong B (2003) Beral V (2009) Sustained lower rates of HRT prescribing and breast cancer incidence in Australia since. Breast Cancer Res Treat 117(3):671-673
21. Hemminki E, Kyyronen P, Pukkala E (2008) Postmenopausal hormone drugs and breast and colon cancer: nordic countries 1995-2005. Maturitas 61(4):299-304
22. Barnes KM, Dickstein B, Cutler GB Jr, Fojo T, Bates SE (1996) Steroid treatment, accumulation, and antagonism of P-glycoprotein in multidrug-resistant cells. Biochemistry 35(15):4820-4827 (Pubitemid 26126700)
23. Kim WY, Benet LZ (2004) P-glycoprotein (P-gp/MDR1)-mediated efflux of sex-steroid hormones and modulation of P-gp expression in vitro. Pharm Res 21(7):1284-1293 (Pubitemid 38954215)
24. Campa D, Kaaks R, Le ML, Haiman CA, Travis RC, Berg CD, Buring JE, Chanock SJ, Diver WR, Dostal L, Fournier A, Hankinson SE, Henderson BE, Hoover RN, Isaacs C, Johansson M, Kolonel LN, Kraft P, Lee IM, McCarty CA, Overvad K, Panico S, Peeters PH, Riboli E, Sanchez MJ, Schumacher FR, Skeie G, Stram DO, Thun MJ, Trichopoulos D, Zhang S, Ziegler RG, Hunter DJ, Lindstrom S, Canzian F (2011) Interactions between genetic variants and breast cancer risk factors in the breast and prostate cancer cohort consortium. J Natl Cancer Inst 103(16):1252-1263
25. Kawase T, Matsuo K, Suzuki T, Hiraki A, Watanabe M, Iwata H, Tanaka H, Tajima K (2009) FGFR2 intronic polymorphisms interact with reproductive risk factors of breast cancer: results of a case control study in Japan. Int J Cancer 125(8):1946-1952
26. Milne RL, Gaudet MM, Spurdle AB, Fasching PA, Couch FJ, Benitez J, rias Perez JI, Zamora MP, Malats N, Dos SS, I, Gibson LJ, Fletcher O, Johnson N, nton-Culver H, Ziogas A, Figueroa J, Brinton L, Sherman ME, Lissowska J, Hopper JL, Dite GS, Apicella C, Southey MC, Sigurdson AJ, Linet MS, Schonfeld SJ, Freedman DM, Mannermaa A, Kosma VM, Kataja V, Auvinen P, Andrulis IL, Glendon G, Knight JA, Weerasooriya N, Cox A, Reed MW, Cross SS, Dunning AM, Ahmed S, Shah M, Brauch H, Ko YD, Bruning T, Lambrechts D, Reumers J, Smeets A, Wang-Gohrke S, Hall P, Czene K, Liu J, Irwanto AK, Chenevix-Trench G, Holland H, Giles GG, Baglietto L, Severi G, Bojensen SE, Nordestgaard BG, Flyger H, John EM, West DW, Whittemore AS, Vachon C, Olson JE, Fredericksen Z, Kosel M, Hein R, Vrieling A, Flesch-Janys D, Heinz J, Beckmann MW, Heusinger K, Ekici AB, Haeberle L, Humphreys MK, Morrison J, Easton DF, Pharoah PD, Garcia-Closas M, Goode EL, Chang-Claude J (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(6): R110
27. Prentice RL, Huang Y, Hinds DA, Peters U, Pettinger M, Cox DR, Beilharz E, Chlebowski RT, Rossouw JE, Caan B, Ballinger DG (2009) Variation in the FGFR2 gene and the effects of postmenopausal hormone therapy on invasive breast cancer. Cancer Epidemiol Biomarkers Prev 18(11):3079-3085
28. Rebbeck TR, DeMichele A, Tran TV, Panossian S, Bunin GR, Troxel AB, Strom BL (2009) Hormone-dependent effects of FGFR2 and MAP3K1 in breast cancer susceptibility in a population-based sample of post-menopausal African-American and European-American women. Carcinogenesis 30(2):269-274
29. Travis RC, Reeves GK, Green J, Bull D, Tipper SJ, Baker K, Beral V, Peto R, Bell J, Zelenika D, Lathrop M (2010) Gene-environment interactions in 7610 women with breast cancer: prospective evidence from the Million Women Study. Lancet 375(9732):2143-2151
30. Hein R, Abbas S, Seibold P, Salazar R, Flesch-Janys D, Chang-Claude J (2012) Polymorphism Thr160Thr in SRD5A1, involved in the progesterone metabolism, modifies postmenopausal breast cancer risk associated with menopausal hormone therapy. Breast Cancer Res Treat 131(2):653-661
31. The MARIE-GENICA Consortium on Genetic Susceptibility for Menopausal Hormone Therapy Related Breast Cancer Risk (2010) Postmenopausal estrogen monotherapy-associated breast cancer risk is modified by CYP17A1-34-T > C polymorphism. Breast Cancer Res Treat 120(3):737-744
32. The MARIE-GENICA Consortium6 on Genetic Susceptibility for Menopausal Hormone Therapy7 Related Breast Cancer Risk (2010) Genetic polymorphisms in phase I and phase II enzymes and breast cancer risk associated with menopausal hormone therapy in postmenopausal women. Breast Cancer Res Treat 119(2):463-474
33. The MARIE-GENICA Consortium on Genetic Susceptibility for Menopausal Hormone Therapy Related Breast Cancer Risk (2010) Polymorphisms in the BRCA1 and ABCB1 genes modulate menopausal hormone therapy associated breast cancer risk in postmenopausal women. Breast Cancer Res Treat 120(3):727-736
34. The MARIE-GENICA Consortium on Genetic Susceptibility for Menopausal Hormone Therapy Related Breast Cancer Risk (2010) Polymorphisms in genes of the steroid receptor superfamily modify postmenopausal breast cancer risk associated with menopausal hormone therapy. Int J Cancer 126(12):2935-2946
35. Nickels S, Truong T, Hein R, et al. (2013) Evidence of gene-environment interactions between common breast cancer susceptibility Loci and Established Environmental Risk Factors. PLoS Genet (accepted for publication)
36. Piegorsch WW, Weinberg CR, Taylor JA (1994) Non-hierarchical logistic models and case-only designs for assessing susceptibility in population-based case-control studies. Stat Med 13(2):153-162 (Pubitemid 24017109)
37. Wedren S, Lovmar L, Humphreys K, Magnusson C, Melhus H, Syvanen AC, Kindmark A, Landegren U, Fermer ML, Stiger F, Persson I, Baron J, Weiderpass E (2004) Oestrogen receptor alpha gene haplotype and postmenopausal breast cancer risk: a case control study. Breast Cancer Res 6(4):R437-R449
38. Magnusson C, Baron JA, Correia N, Bergstrom R, Adami HO, Persson I (1999) Breast-cancer risk following long-term oestrogen- and oestrogen-progestin- replacement therapy. Int J Cancer 81(3):339-344 (Pubitemid 29165190)
39. Hunter DJ, Kraft P, Jacobs KB, Cox DG, Yeager M, Hankinson SE, Wacholder S, Wang Z, Welch R, Hutchinson A, Wang J, Yu K, Chatterjee N, Orr N, Willett WC, Colditz GA, Ziegler RG, Berg CD, Buys SS, McCarty CA, Feigelson HS, Calle EE, Thun MJ, Hayes RB, Tucker M, Gerhard DS, Fraumeni JF Jr, Hoover RN, Thomas G, Chanock SJ (2007) A genome-wide association study identifies alleles in FGFR2 associated with risk of sporadic postmenopausal breast cancer. Nat Genet 39(7):870-874 (Pubitemid 47014500)
40. de Bakker PI, Yelensky R, Pe'er I, Gabriel SB, Daly MJ, Altshuler D (2005) Efficiency and power in genetic association studies. Nat Genet 37(11):1217-1223 (Pubitemid 41568704)
41. Skol AD, Scott LJ, Abecasis GR, Boehnke M (2006) Joint analysis is more efficient than replication-based analysis for two-stage genome-wide association studies. Nat Genet 38(2):209-213 (Pubitemid 43177235)
42. R Development Core Team R: A Language and Environment for Statistical Computing [Version 2.12.2.] (2011) R Foundation for Statistical Computing
43. Sun P, Xia S, Lal B, Eberhart CG, Quinones-Hinojosa A, Maciaczyk J, Matsui W, Dimeco F, Piccirillo SM, Vescovi AL, Laterra J (2009) DNER, an epigenetically modulated gene, regulates glioblastoma-derived neurosphere cell differentiation and tumor propagation. Stem Cells 27(7):1473-1486
44. Park JR, Jung JW, Seo MS, Kang SK, Lee YS, Kang KS (2010) DNER modulates adipogenesis of human adipose tissue-derived mesenchymal stem cells via regulation of cell proliferation. Cell Prolif 43(1):19-28
45. Thomas G, Jacobs KB, Kraft P, Yeager M, Wacholder S, Cox DG, Hankinson SE, Hutchinson A, Wang Z, Yu K, Chatterjee N, Garcia-Closas M, Gonzalez-Bosquet J, Prokunina-Olsson L, Orr N, Willett WC, Colditz GA, Ziegler RG, Berg CD, Buys SS, McCarty CA, Feigelson HS, Calle EE, Thun MJ, Diver R, Prentice R, Jackson R, Kooperberg C, Chlebowski R, Lissowska J, Peplonska B, Brinton LA, Sigurdson A, Doody M, Bhatti P, Alexander BH, Buring J, Lee IM, Vatten LJ, Hveem K, Kumle M, Hayes RB, Tucker M, Gerhard DS, Fraumeni JF, Jr., Hoover RN, Chanock SJ, Hunter DJ (2009) A multistage genome-wide association study in breast cancer identifies two new risk alleles at 1p11.2 and 14q24.1 (RAD51L1). Nat Genet 41(5): 579-584
46. Collado M, Serrano M (2010) The TRIP from ULF to ARF. Cancer Cell 17(4):317-318
47. Minakuchi M, Kakazu N, Gorrin-Rivas MJ, Abe T, Copeland TD, Ueda K, Adachi Y (2001) Identification and characterization of SEB, a novel protein that binds to the acute undifferentiated leukemia-associated protein SET. Eur J Biochem 268(5):1340-1351 (Pubitemid 32231887)
48. Aschard H, Lutz S, Maus B, Duell EJ, Fingerlin TE, Chatterjee N, Kraft P, Van SK (2012) Challenges and opportunities in genome-wide environmental interaction (GWEI) studies. Hum Genet 131(10):1591-1613
49. Dempfle A, Scherag A, Hein R, Beckmann L, Chang-Claude J, Schafer H (2008) Gene-environment interactions for complex traits: definitions, methodological requirements and challenges. Eur J Hum Genet 16(10):1164-1172
50. Hein R, Beckmann L, Chang-Claude J (2008) Sample size requirements for indirect association studies of gene-environment interactions (G × E). Genet Epidemiol 32(3):235-245 (Pubitemid 351550370)
51. Lindstrom S, Yen YC, Spiegelman D, Kraft P (2009) The impact of gene-environment dependence and misclassification in genetic association studies incorporating gene-environment interactions. Hum Hered 68(3):171-181
52. Morimoto LM, White E, Newcomb PA (2003) Selection bias in the assessment of gene-environment interaction in case-control studies. Am J Epidemiol 158(3):259-263 (Pubitemid 36944419)
53. Wacholder S, Chatterjee N, Hartge P (2002) Joint effect of genes and environment distorted by selection biases: implications for hospital-based case-control studies. Cancer Epidemiol Biomarkers Prev 11(9):885-889 (Pubitemid 35014892)
54. Gauderman WJ (2002) Sample size requirements for matched case-control studies of gene-environment interaction. Stat Med 21(1):35-50 (Pubitemid 34065703)
55. Kraft P (2008) Curses - winner's and otherwise - in genetic epidemiology. Epidemiology 19(5):649-651