Gene-Environment Interactions Relevant to Estrogen and Risk of Breast Cancer: Can Gene-Environment Interactions Be Detected Only among Candidate SNPs from Genome-Wide Association Studies?

doi:10.3390/cancers13102370

. 2021 May 14;13(10):2370.

doi: 10.3390/cancers13102370.

Gene-Environment Interactions Relevant to Estrogen and Risk of Breast Cancer: Can Gene-Environment Interactions Be Detected Only among Candidate SNPs from Genome-Wide Association Studies?

JooYong Park^{1

2}, Ji-Yeob Choi^{1

2

3

4}, Jaesung Choi³, Seokang Chung¹, Nan Song⁵, Sue K Park^{1

4

6}, Wonshik Han^{4

7}, Dong-Young Noh^{4

7}, Sei-Hyun Ahn⁸, Jong Won Lee⁸, Mi Kyung Kim⁹, Sun Ha Jee¹⁰, Wanqing Wen¹¹, Manjeet K Bolla¹², Qin Wang¹², Joe Dennis¹², Kyriaki Michailidou^{12

13

14}, Mitul Shah¹⁵, Don M Conroy¹⁵, Patricia A Harrington¹⁵, Rebecca Mayes¹⁵, Kamila Czene¹⁶, Per Hall^{16

17}, Lauren R Teras¹⁸, Alpa V Patel¹⁹, Fergus J Couch¹⁹, Janet E Olson²⁰, Elinor J Sawyer²¹, Rebecca Roylance²², Stig E Bojesen^{23

24

25}, Henrik Flyger²⁶, Diether Lambrechts^{27

28}, Adinda Baten²⁹, Keitaro Matsuo^{30

31}, Hidemi Ito³¹, Pascal Guénel³², Thérèse Truong³², Renske Keeman³³, Marjanka K Schmidt^{33

34}, Anna H Wu³⁵, Chiu-Chen Tseng³⁵, Angela Cox³⁶, Simon S Cross³⁷, kConFab Investigators^{38

39}, Irene L Andrulis^{40

41}, John L Hopper⁴², Melissa C Southey^{43

44

45}, Pei-Ei Wu⁴⁶, Chen-Yang Shen^{47

48}, Peter A Fasching^{49

50}, Arif B Ekici⁵¹, Kenneth Muir⁵², Artitaya Lophatananon⁵², Hermann Brenner^{53

54

55}, Volker Arndt⁵³, Michael E Jones⁵⁶, Anthony J Swerdlow^{56

57}, Reiner Hoppe^{58

59}, Yon-Dschun Ko⁶⁰, Mikael Hartman^{61

62

63}, Jingmei Li⁶⁴, Arto Mannermaa^{65

66

67}, Jaana M Hartikainen^{65

66}, Javier Benitez^{68

69}, Anna González-Neira⁶⁹, Christopher A Haiman³⁵, Thilo Dörk⁷⁰, Natalia V Bogdanova^{70

71

72}, Soo Hwang Teo^{73

74}, Nur Aishah Mohd Taib⁷⁵, Olivia Fletcher⁷⁶, Nichola Johnson⁷⁶, Mervi Grip⁷⁷, Robert Winqvist^{78

79}, Carl Blomqvist^{80

81}, Heli Nevanlinna⁸², Annika Lindblom^{83

84}, Camilla Wendt⁸⁵, Vessela N Kristensen^{86

87}, Nbcs Collaborators^{86

87

88

89

90

91

92

93

94

95

96

97}, Rob A E M Tollenaar⁹⁸, Bernadette A M Heemskerk-Gerritsen⁹⁹, Paolo Radice¹⁰⁰, Bernardo Bonanni¹⁰¹, Ute Hamann¹⁰², Mehdi Manoochehri¹⁰², James V Lacey^{103

104}, Maria Elena Martinez^{105

106}, Alison M Dunning¹⁵, Paul D P Pharoah^{12

15}, Douglas F Easton^{12

15}, Keun-Young Yoo⁶, Daehee Kang^{1

4

6}

Affiliations

¹ Department of Biomedical Sciences, Seoul National University Graduate School, Seoul 03080, Korea.
² BK21plus Biomedical Science Project, Seoul National University College of Medicine, Seoul 03080, Korea.
³ Institute of Health Policy and Management, Seoul National University Medical Research Center, Seoul 03080, Korea.
⁴ Cancer Research Institute, Seoul National University, Seoul 03080, Korea.
⁵ College of Pharmacy, Chungbuk National University, Cheongju-si 28160, Korea.
⁶ Department of Preventive Medicine, Seoul National University College of Medicine, Seoul 03080, Korea.
⁷ Department of Surgery, Seoul National University College of Medicine, Seoul 03080, Korea.
⁸ Department of Surgery, Medicine and ASAN Medical Center, University of Ulsan College, Seoul 05505, Korea.
⁹ Division of Cancer Epidemiology and Management, National Cancer Center, Goyang-si 10408, Korea.
¹⁰ Department of Epidemiology and Health Promotion, Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul 03722, Korea.
¹¹ Division of Epidemiology, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
¹² Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB2 0SR, UK.
¹³ Biostatistics Unit, The Cyprus Institute of Neurology & Genetics, Nicosia 2371, Cyprus.
¹⁴ Cyprus School of Molecular Medicine, The Cyprus Institute of Neurology & Genetics, Nicosia 23462, Cyprus.
¹⁵ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.
¹⁶ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 171 65 Stockholm, Sweden.
¹⁷ Department of Oncology, Södersjukhuset, 118 83 Stockholm, Sweden.
¹⁸ Department of Population Science, American Cancer Society, Atlanta, GA 30303, USA.
¹⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN 55905, USA.
²⁰ Department of Health Sciences Research, Mayo Clinic, Rochester, MN 55905, USA.
²¹ School of Cancer & Pharmaceutical Sciences, Comprehensive Cancer Centre, Guy's Campus, King's College London, London SE1 9RT, UK.
²² Department of Oncology, UCLH Foundation Trust, London NW1 2PG, UK.
²³ Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, 2730 Herlev, Denmark.
²⁴ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, 2730 Herlev, Denmark.
²⁵ Faculty of Health and Medical Sciences, University of Copenhagen, 2200 Copenhagen, Denmark.
²⁶ Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, 2730 Herlev, Denmark.
²⁷ VIB Center for Cancer Biology, 3001 Leuve, Belgium.
²⁸ Laboratory for Translational Genetics, Department of Human Genetics, University of Leuven, 3000 Leuven, Belgium.
²⁹ Department of Radiotherapy Oncology, KU Leuven-University of Leuven, University Hospitals Leuven, 3000 Leuven, Belgium.
³⁰ Division of Cancer Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya 464-8681, Japan.
³¹ Division of Cancer Epidemiology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan.
³² Center for Research in Epidemiology and Population Health (CESP), Team Exposome and Heredity, INSERM, University Paris-Saclay, 94805 Villejuif, France.
³³ Division of Molecular Pathology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 CX Amsterdam, The Netherlands.
³⁴ Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 CX Amsterdam, The Netherlands.
³⁵ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.
³⁶ Sheffield Institute for Nucleic Acids (SInFoNiA), Department of Oncology and Metabolism, University of Sheffield, Sheffield S10 2TN, UK.
³⁷ Academic Unit of Pathology, Department of Neuroscience, University of Sheffield, Sheffield S10 2TN, UK.
³⁸ Peter MacCallum Cancer Center, Melbourne, VIC 3000, Australia.
³⁹ Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, VIC 3000, Australia.
⁴⁰ Fred A, Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, ON M5G 1X5, Canada.
⁴¹ Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.
⁴² Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, VIC 3010, Australia.
⁴³ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, VIC 3168, Australia.
⁴⁴ Department of Clinical Pathology, The University of Melbourne, Melbourne, VIC 3010, Australia.
⁴⁵ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, VIC 3004, Australia.
⁴⁶ Taiwan Biobank, Institute of Biomedical Sciences, Academia Sinica, Taipei 115, Taiwan.
⁴⁷ Institute of Biomedical Sciences, Academia Sinica, Taipei 115, Taiwan.
⁴⁸ School of Public Health, China Medical University, Taichung 404, Taiwan.
⁴⁹ Department of Medicine Division of Hematology and Oncology, David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA.
⁵⁰ Department of Gynecology and Obstetrics, Comprehensive Cancer Center ER-EMN, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, 91054 Erlangen, Germany.
⁵¹ Institute of Human Genetics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, 91054 Erlangen, Germany.
⁵² Division of Population Health, Health Services Research and Primary Care, School of Health Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester M13 9PL, UK.
⁵³ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
⁵⁴ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), 69120 Heidelberg, Germany.
⁵⁵ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
⁵⁶ Division of Genetics and Epidemiology, The Institute of Cancer Research, London SM2 5NG, UK.
⁵⁷ Division of Breast Cancer Research, The Institute of Cancer Research, London SW7 3RP, UK.
⁵⁸ Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, 70376 Stuttgart, Germany.
⁵⁹ University of Tübingen, 72074 Tübingen, Germany.
⁶⁰ Department of Internal Medicine, Evangelische Kliniken Bonn gGmbH, Johanniter Krankenhaus, 53177 Bonn, Germany.
⁶¹ Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore 117549, Singapore.
⁶² Department of Surgery, Yong Loo Lin School of Medicine, National University of Singapore and National University Health System, Singapore 119228, Singapore.
⁶³ Department of Surgery, National University Health System, Singapore 119228, Singapore.
⁶⁴ Human Genetics Division, Genome Institute of Singapore, Singapore 138672, Singapore.
⁶⁵ Translational Cancer Research Area, University of Eastern Finland, 70210 Kuopio, Finland.
⁶⁶ Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, 70210 Kuopio, Finland.
⁶⁷ Biobank of Eastern Finland, Kuopio University Hospital, 70210 Kuopio, Finland.
⁶⁸ Biomedical Network on Rare Diseases (CIBERER), 28029 Madrid, Spain.
⁶⁹ Human Cancer Genetics Programme, Spanish National Cancer Research Centre (CNIO), 28029 Madrid, Spain.
⁷⁰ Gynaecology Research Unit, Hannover Medical School, 30625 Hannover, Germany.
⁷¹ Department of Radiation Oncology, Hannover Medical School, 30625 Hannover, Germany.
⁷² NN Alexandrov Research Institute of Oncology and Medical Radiology, 223040 Minsk, Belarus.
⁷³ Breast Cancer Research Programme, Cancer Research Malaysia, Subang Jaya 47500, Malaysia.
⁷⁴ Department of Surgery, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia.
⁷⁵ Breast Cancer Research Unit, University Malaya Cancer Research Institute, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia.
⁷⁶ The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London SW7 3RP, UK.
⁷⁷ Department of Surgery, Oulu University Hospital, University of Oulu, 90220 Oulu, Finland.
⁷⁸ Laboratory of Cancer Genetics and Tumor Biology, Cancer and Translational Medicine Research Unit, Biocenter Oulu, University of Oulu, 90570 Oulu, Finland.
⁷⁹ Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre Oulu, Oulu 90570, Finland.
⁸⁰ Department of Oncology, Helsinki University Hospital, University of Helsinki, 00290 Helsinki, Finland.
⁸¹ Department of Oncology, Örebro University Hospital, 70185 Örebro, Sweden.
⁸² Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, 00290 Helsinki, Finland.
⁸³ Department of Molecular Medicine and Surgery, Karolinska Institutet, 171 76 Stockholm, Sweden.
⁸⁴ Department of Clinical Genetics, Karolinska University Hospital, 171 76 Stockholm, Sweden.
⁸⁵ Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, 118 83 Stockholm, Sweden.
⁸⁶ Department of Medical Genetics, Oslo University Hospital and University of Oslo, 0450 Oslo, Norway.
⁸⁷ Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, 0372 Oslo, Norway.
⁸⁸ Department of Research, Vestre Viken Hospital, 3004 Drammen, Norway.
⁸⁹ Department of Tumor Biology, Institute for Cancer Research, Oslo University Hospital, 0450 Oslo, Norway.
⁹⁰ Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital-Radiumhospitalet, 0450 Oslo, Norway.
⁹¹ Section for Breast- and Endocrine Surgery, Department of Cancer, Division of Surgery, Cancer and Transplantation Medicine, Oslo University Hospital-Ullevål, 0450 Oslo, Norway.
⁹² Department of Radiology and Nuclear Medicine, Oslo University Hospital, 0450 Oslo, Norway.
⁹³ Department of Pathology at Akershus University Hospital, 1478 Lørenskog, Norway.
⁹⁴ Department of Oncology, Division of Surgery and Cancer and Transplantation Medicine, University Hospital-Radiumhospitalet, 0405 Oslo, Norway.
⁹⁵ National Advisory Unit on Late Effects after Cancer Treatment, Department of Oncology, Oslo University Hospital, 0405 Oslo, Norway.
⁹⁶ Department of Oncology, Akershus University Hospital, 1478 Lørenskog, Norway.
⁹⁷ Oslo Breast Cancer Research Consortium, Oslo University Hospital, 0405 Oslo, Norway.
⁹⁸ Department of Surgery, Leiden University Medical Center, 2333 ZA Leiden, The Netherlands.
⁹⁹ Department of Medical Oncology, Erasmus MC Cancer Institute, 3015 CN Rotterdam, The Netherlands.
¹⁰⁰ Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, Fondazione IRCCS Istituto Nazionale dei Tumori (INT), 20133 Milan, Italy.
¹⁰¹ Division of Cancer Prevention and Genetics, IEO, European Institute of Oncology IRCCS, 20141 Milan, Italy.
¹⁰² Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
¹⁰³ Department of Computational and Quantitative Medicine, City of Hope, Duarte, CA 91010, USA.
¹⁰⁴ City of Hope Comprehensive Cancer Center, City of Hope, Duarte, CA 91010, USA.
¹⁰⁵ Moores Cancer Center, University of California San Diego, La Jolla, CA 92037, USA.
¹⁰⁶ Herbert Wertheim School of Public Health and Longevity Science, University of California San Diego, La Jolla, CA 92161, USA.

PMID: 34069208
PMCID: PMC8156547
DOI: 10.3390/cancers13102370

Gene-Environment Interactions Relevant to Estrogen and Risk of Breast Cancer: Can Gene-Environment Interactions Be Detected Only among Candidate SNPs from Genome-Wide Association Studies?

JooYong Park et al. Cancers (Basel). 2021.

. 2021 May 14;13(10):2370.

doi: 10.3390/cancers13102370.

Authors

Affiliations

¹ Department of Biomedical Sciences, Seoul National University Graduate School, Seoul 03080, Korea.
² BK21plus Biomedical Science Project, Seoul National University College of Medicine, Seoul 03080, Korea.
³ Institute of Health Policy and Management, Seoul National University Medical Research Center, Seoul 03080, Korea.
⁴ Cancer Research Institute, Seoul National University, Seoul 03080, Korea.
⁵ College of Pharmacy, Chungbuk National University, Cheongju-si 28160, Korea.
⁶ Department of Preventive Medicine, Seoul National University College of Medicine, Seoul 03080, Korea.
⁷ Department of Surgery, Seoul National University College of Medicine, Seoul 03080, Korea.
⁸ Department of Surgery, Medicine and ASAN Medical Center, University of Ulsan College, Seoul 05505, Korea.
⁹ Division of Cancer Epidemiology and Management, National Cancer Center, Goyang-si 10408, Korea.
¹⁰ Department of Epidemiology and Health Promotion, Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul 03722, Korea.
¹¹ Division of Epidemiology, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN 37232, USA.
¹² Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge CB2 0SR, UK.
¹³ Biostatistics Unit, The Cyprus Institute of Neurology & Genetics, Nicosia 2371, Cyprus.
¹⁴ Cyprus School of Molecular Medicine, The Cyprus Institute of Neurology & Genetics, Nicosia 23462, Cyprus.
¹⁵ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.
¹⁶ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 171 65 Stockholm, Sweden.
¹⁷ Department of Oncology, Södersjukhuset, 118 83 Stockholm, Sweden.
¹⁸ Department of Population Science, American Cancer Society, Atlanta, GA 30303, USA.
¹⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN 55905, USA.
²⁰ Department of Health Sciences Research, Mayo Clinic, Rochester, MN 55905, USA.
²¹ School of Cancer & Pharmaceutical Sciences, Comprehensive Cancer Centre, Guy's Campus, King's College London, London SE1 9RT, UK.
²² Department of Oncology, UCLH Foundation Trust, London NW1 2PG, UK.
²³ Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, 2730 Herlev, Denmark.
²⁴ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, 2730 Herlev, Denmark.
²⁵ Faculty of Health and Medical Sciences, University of Copenhagen, 2200 Copenhagen, Denmark.
²⁶ Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, 2730 Herlev, Denmark.
²⁷ VIB Center for Cancer Biology, 3001 Leuve, Belgium.
²⁸ Laboratory for Translational Genetics, Department of Human Genetics, University of Leuven, 3000 Leuven, Belgium.
²⁹ Department of Radiotherapy Oncology, KU Leuven-University of Leuven, University Hospitals Leuven, 3000 Leuven, Belgium.
³⁰ Division of Cancer Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya 464-8681, Japan.
³¹ Division of Cancer Epidemiology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan.
³² Center for Research in Epidemiology and Population Health (CESP), Team Exposome and Heredity, INSERM, University Paris-Saclay, 94805 Villejuif, France.
³³ Division of Molecular Pathology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 CX Amsterdam, The Netherlands.
³⁴ Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, 1066 CX Amsterdam, The Netherlands.
³⁵ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.
³⁶ Sheffield Institute for Nucleic Acids (SInFoNiA), Department of Oncology and Metabolism, University of Sheffield, Sheffield S10 2TN, UK.
³⁷ Academic Unit of Pathology, Department of Neuroscience, University of Sheffield, Sheffield S10 2TN, UK.
³⁸ Peter MacCallum Cancer Center, Melbourne, VIC 3000, Australia.
³⁹ Sir Peter MacCallum Department of Oncology, The University of Melbourne, Melbourne, VIC 3000, Australia.
⁴⁰ Fred A, Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, ON M5G 1X5, Canada.
⁴¹ Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.
⁴² Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, VIC 3010, Australia.
⁴³ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, VIC 3168, Australia.
⁴⁴ Department of Clinical Pathology, The University of Melbourne, Melbourne, VIC 3010, Australia.
⁴⁵ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, VIC 3004, Australia.
⁴⁶ Taiwan Biobank, Institute of Biomedical Sciences, Academia Sinica, Taipei 115, Taiwan.
⁴⁷ Institute of Biomedical Sciences, Academia Sinica, Taipei 115, Taiwan.
⁴⁸ School of Public Health, China Medical University, Taichung 404, Taiwan.
⁴⁹ Department of Medicine Division of Hematology and Oncology, David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA.
⁵⁰ Department of Gynecology and Obstetrics, Comprehensive Cancer Center ER-EMN, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, 91054 Erlangen, Germany.
⁵¹ Institute of Human Genetics, Comprehensive Cancer Center Erlangen-EMN, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, 91054 Erlangen, Germany.
⁵² Division of Population Health, Health Services Research and Primary Care, School of Health Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester M13 9PL, UK.
⁵³ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
⁵⁴ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), 69120 Heidelberg, Germany.
⁵⁵ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
⁵⁶ Division of Genetics and Epidemiology, The Institute of Cancer Research, London SM2 5NG, UK.
⁵⁷ Division of Breast Cancer Research, The Institute of Cancer Research, London SW7 3RP, UK.
⁵⁸ Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, 70376 Stuttgart, Germany.
⁵⁹ University of Tübingen, 72074 Tübingen, Germany.
⁶⁰ Department of Internal Medicine, Evangelische Kliniken Bonn gGmbH, Johanniter Krankenhaus, 53177 Bonn, Germany.
⁶¹ Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore 117549, Singapore.
⁶² Department of Surgery, Yong Loo Lin School of Medicine, National University of Singapore and National University Health System, Singapore 119228, Singapore.
⁶³ Department of Surgery, National University Health System, Singapore 119228, Singapore.
⁶⁴ Human Genetics Division, Genome Institute of Singapore, Singapore 138672, Singapore.
⁶⁵ Translational Cancer Research Area, University of Eastern Finland, 70210 Kuopio, Finland.
⁶⁶ Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, 70210 Kuopio, Finland.
⁶⁷ Biobank of Eastern Finland, Kuopio University Hospital, 70210 Kuopio, Finland.
⁶⁸ Biomedical Network on Rare Diseases (CIBERER), 28029 Madrid, Spain.
⁶⁹ Human Cancer Genetics Programme, Spanish National Cancer Research Centre (CNIO), 28029 Madrid, Spain.
⁷⁰ Gynaecology Research Unit, Hannover Medical School, 30625 Hannover, Germany.
⁷¹ Department of Radiation Oncology, Hannover Medical School, 30625 Hannover, Germany.
⁷² NN Alexandrov Research Institute of Oncology and Medical Radiology, 223040 Minsk, Belarus.
⁷³ Breast Cancer Research Programme, Cancer Research Malaysia, Subang Jaya 47500, Malaysia.
⁷⁴ Department of Surgery, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia.
⁷⁵ Breast Cancer Research Unit, University Malaya Cancer Research Institute, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia.
⁷⁶ The Breast Cancer Now Toby Robins Research Centre, The Institute of Cancer Research, London SW7 3RP, UK.
⁷⁷ Department of Surgery, Oulu University Hospital, University of Oulu, 90220 Oulu, Finland.
⁷⁸ Laboratory of Cancer Genetics and Tumor Biology, Cancer and Translational Medicine Research Unit, Biocenter Oulu, University of Oulu, 90570 Oulu, Finland.
⁷⁹ Laboratory of Cancer Genetics and Tumor Biology, Northern Finland Laboratory Centre Oulu, Oulu 90570, Finland.
⁸⁰ Department of Oncology, Helsinki University Hospital, University of Helsinki, 00290 Helsinki, Finland.
⁸¹ Department of Oncology, Örebro University Hospital, 70185 Örebro, Sweden.
⁸² Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, 00290 Helsinki, Finland.
⁸³ Department of Molecular Medicine and Surgery, Karolinska Institutet, 171 76 Stockholm, Sweden.
⁸⁴ Department of Clinical Genetics, Karolinska University Hospital, 171 76 Stockholm, Sweden.
⁸⁵ Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, 118 83 Stockholm, Sweden.
⁸⁶ Department of Medical Genetics, Oslo University Hospital and University of Oslo, 0450 Oslo, Norway.
⁸⁷ Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, 0372 Oslo, Norway.
⁸⁸ Department of Research, Vestre Viken Hospital, 3004 Drammen, Norway.
⁸⁹ Department of Tumor Biology, Institute for Cancer Research, Oslo University Hospital, 0450 Oslo, Norway.
⁹⁰ Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital-Radiumhospitalet, 0450 Oslo, Norway.
⁹¹ Section for Breast- and Endocrine Surgery, Department of Cancer, Division of Surgery, Cancer and Transplantation Medicine, Oslo University Hospital-Ullevål, 0450 Oslo, Norway.
⁹² Department of Radiology and Nuclear Medicine, Oslo University Hospital, 0450 Oslo, Norway.
⁹³ Department of Pathology at Akershus University Hospital, 1478 Lørenskog, Norway.
⁹⁴ Department of Oncology, Division of Surgery and Cancer and Transplantation Medicine, University Hospital-Radiumhospitalet, 0405 Oslo, Norway.
⁹⁵ National Advisory Unit on Late Effects after Cancer Treatment, Department of Oncology, Oslo University Hospital, 0405 Oslo, Norway.
⁹⁶ Department of Oncology, Akershus University Hospital, 1478 Lørenskog, Norway.
⁹⁷ Oslo Breast Cancer Research Consortium, Oslo University Hospital, 0405 Oslo, Norway.
⁹⁸ Department of Surgery, Leiden University Medical Center, 2333 ZA Leiden, The Netherlands.
⁹⁹ Department of Medical Oncology, Erasmus MC Cancer Institute, 3015 CN Rotterdam, The Netherlands.
¹⁰⁰ Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, Fondazione IRCCS Istituto Nazionale dei Tumori (INT), 20133 Milan, Italy.
¹⁰¹ Division of Cancer Prevention and Genetics, IEO, European Institute of Oncology IRCCS, 20141 Milan, Italy.
¹⁰² Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
¹⁰³ Department of Computational and Quantitative Medicine, City of Hope, Duarte, CA 91010, USA.
¹⁰⁴ City of Hope Comprehensive Cancer Center, City of Hope, Duarte, CA 91010, USA.
¹⁰⁵ Moores Cancer Center, University of California San Diego, La Jolla, CA 92037, USA.
¹⁰⁶ Herbert Wertheim School of Public Health and Longevity Science, University of California San Diego, La Jolla, CA 92161, USA.

PMID: 34069208
PMCID: PMC8156547
DOI: 10.3390/cancers13102370

Abstract

In this study we aim to examine gene-environment interactions (GxEs) between genes involved with estrogen metabolism and environmental factors related to estrogen exposure. GxE analyses were conducted with 1970 Korean breast cancer cases and 2052 controls in the case-control study, the Seoul Breast Cancer Study (SEBCS). A total of 11,555 SNPs from the 137 candidate genes were included in the GxE analyses with eight established environmental factors. A replication test was conducted by using an independent population from the Breast Cancer Association Consortium (BCAC), with 62,485 Europeans and 9047 Asians. The GxE tests were performed by using two-step methods in GxEScan software. Two interactions were found in the SEBCS. The first interaction was shown between rs13035764 of NCOA1 and age at menarche in the GE|2df model (p-2df = 1.2 × 10^-3). The age at menarche before 14 years old was associated with the high risk of breast cancer, and the risk was higher when subjects had homozygous minor allele G. The second GxE was shown between rs851998 near ESR1 and height in the GE|2df model (p-2df = 1.1 × 10^-4). Height taller than 160 cm was associated with a high risk of breast cancer, and the risk increased when the minor allele was added. The findings were not replicated in the BCAC. These results would suggest specificity in Koreans for breast cancer risk.

Keywords: breast cancer; estrogen; gene-environment interaction.

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Conflict of interest statement

The authors declare no conflict of interest.

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References

1. Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I., Jemal A., Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021 doi: 10.3322/caac.21660. - DOI - PubMed
1. Kang S.Y., Kim Y.S., Kim Z., Kim H.Y., Kim H.J., Park S., Bae S.Y., Yoon K.H., Lee S.B., Lee S.K., et al. Breast Cancer Statistics in Korea in 2017: Data from a Breast Cancer Registry. J. Breast Cancer. 2020;23:115–128. doi: 10.4048/jbc.2020.23.e24. - DOI - PMC - PubMed
1. Kluttig A., Schmidt-Pokrzywniak A. Established and Suspected Risk Factors in Breast Cancer Aetiology. Breast Care. 2009;4:82–87. doi: 10.1159/000211368. - DOI - PMC - PubMed
1. Key T.J., Verkasalo P.K., Banks E. Epidemiology of breast cancer. Lancet Oncol. 2001;2:133–140. doi: 10.1016/S1470-2045(00)00254-0. - DOI - PubMed
1. Rojas K., Stuckey A. Breast Cancer Epidemiology and Risk Factors. Clin. Obstet. Gynecol. 2016;59:651–672. doi: 10.1097/GRF.0000000000000239. - DOI - PubMed

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[1] Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I., Jemal A., Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021 doi: 10.3322/caac.21660. - DOI - PubMed

[2] Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I., Jemal A., Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021 doi: 10.3322/caac.21660. - DOI - PubMed

[3] Kang S.Y., Kim Y.S., Kim Z., Kim H.Y., Kim H.J., Park S., Bae S.Y., Yoon K.H., Lee S.B., Lee S.K., et al. Breast Cancer Statistics in Korea in 2017: Data from a Breast Cancer Registry. J. Breast Cancer. 2020;23:115–128. doi: 10.4048/jbc.2020.23.e24. - DOI - PMC - PubMed

[4] Kang S.Y., Kim Y.S., Kim Z., Kim H.Y., Kim H.J., Park S., Bae S.Y., Yoon K.H., Lee S.B., Lee S.K., et al. Breast Cancer Statistics in Korea in 2017: Data from a Breast Cancer Registry. J. Breast Cancer. 2020;23:115–128. doi: 10.4048/jbc.2020.23.e24. - DOI - PMC - PubMed

[5] Kluttig A., Schmidt-Pokrzywniak A. Established and Suspected Risk Factors in Breast Cancer Aetiology. Breast Care. 2009;4:82–87. doi: 10.1159/000211368. - DOI - PMC - PubMed

[6] Kluttig A., Schmidt-Pokrzywniak A. Established and Suspected Risk Factors in Breast Cancer Aetiology. Breast Care. 2009;4:82–87. doi: 10.1159/000211368. - DOI - PMC - PubMed

[7] Key T.J., Verkasalo P.K., Banks E. Epidemiology of breast cancer. Lancet Oncol. 2001;2:133–140. doi: 10.1016/S1470-2045(00)00254-0. - DOI - PubMed

[8] Key T.J., Verkasalo P.K., Banks E. Epidemiology of breast cancer. Lancet Oncol. 2001;2:133–140. doi: 10.1016/S1470-2045(00)00254-0. - DOI - PubMed

[9] Rojas K., Stuckey A. Breast Cancer Epidemiology and Risk Factors. Clin. Obstet. Gynecol. 2016;59:651–672. doi: 10.1097/GRF.0000000000000239. - DOI - PubMed

[10] Rojas K., Stuckey A. Breast Cancer Epidemiology and Risk Factors. Clin. Obstet. Gynecol. 2016;59:651–672. doi: 10.1097/GRF.0000000000000239. - DOI - PubMed

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Gene-Environment Interactions Relevant to Estrogen and Risk of Breast Cancer: Can Gene-Environment Interactions Be Detected Only among Candidate SNPs from Genome-Wide Association Studies?

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Gene-Environment Interactions Relevant to Estrogen and Risk of Breast Cancer: Can Gene-Environment Interactions Be Detected Only among Candidate SNPs from Genome-Wide Association Studies?

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