Variants in genes encoding small GTPases and association with epithelial ovarian cancer susceptibility

Madalene Earp; Jonathan P Tyrer; Stacey J Winham; Hui-Yi Lin; Ganna Chornokur; Joe Dennis; Katja K H Aben; Hoda Anton-Culver; Natalia Antonenkova; Elisa V Bandera; Yukie T Bean; Matthias W Beckmann; Line Bjorge; Natalia Bogdanova; Louise A Brinton; Angela Brooks-Wilson; Fiona Bruinsma; Clareann H Bunker; Ralf Butzow; Ian G Campbell; Karen Carty; Jenny Chang-Claude; Linda S Cook; Daniel W Cramer; Julie M Cunningham; Cezary Cybulski; Agnieszka Dansonka-Mieszkowska; Evelyn Despierre; Jennifer A Doherty; Thilo Dörk; Andreas du Bois; Matthias Dürst; Douglas F Easton; Diana M Eccles; Robert P Edwards; Arif B Ekici; Peter A Fasching; Brooke L Fridley; Aleksandra Gentry-Maharaj; Graham G Giles; Rosalind Glasspool; Marc T Goodman; Jacek Gronwald; Philipp Harter; Alexander Hein; Florian Heitz; Michelle A T Hildebrandt; Peter Hillemanns; Claus K Hogdall; Estrid Høgdall; Satoyo Hosono; Edwin S Iversen; Anna Jakubowska; Allan Jensen; Bu-Tian Ji; Audrey Y Jung; Beth Y Karlan; Melissa Kellar; Lambertus A Kiemeney; Boon Kiong Lim; Susanne K Kjaer; Camilla Krakstad; Jolanta Kupryjanczyk; Diether Lambrechts; Sandrina Lambrechts; Nhu D Le; Shashi Lele; Jenny Lester; Douglas A Levine; Zheng Li; Dong Liang; Jolanta Lissowska; Karen Lu; Jan Lubinski; Lene Lundvall; Leon F A G Massuger; Keitaro Matsuo; Valerie McGuire; John R McLaughlin; Iain McNeish; Usha Menon; Roger L Milne; Francesmary Modugno; Kirsten B Moysich; Roberta B Ness; Heli Nevanlinna; Kunle Odunsi; Sara H Olson; Irene Orlow; Sandra Orsulic; James Paul; Tanja Pejovic; Liisa M Pelttari; Jenny B Permuth; Malcolm C Pike; Elizabeth M Poole; Barry Rosen; Mary Anne Rossing; Joseph H Rothstein; Ingo B Runnebaum; Iwona K Rzepecka; Eva Schernhammer; Ira Schwaab; Xiao-Ou Shu; Yurii B Shvetsov; Nadeem Siddiqui; Weiva Sieh; Honglin Song; Melissa C Southey; Beata Spiewankiewicz; Lara Sucheston-Campbell; Ingvild L Tangen; Soo-Hwang Teo; Kathryn L Terry; Pamela J Thompson; Lotte Thomsen; Shelley S Tworoger; Anne M van Altena; Ignace Vergote; Liv Cecilie Vestrheim Thomsen; Robert A Vierkant; Christine S Walsh; Shan Wang-Gohrke; Nicolas Wentzensen; Alice S Whittemore; Kristine G Wicklund; Lynne R Wilkens; Yin-Ling Woo; Anna H Wu; Xifeng Wu; Yong-Bing Xiang; Hannah Yang; Wei Zheng; Argyrios Ziogas; Alice W Lee; Celeste L Pearce; Andrew Berchuck; Joellen M Schildkraut; Susan J Ramus; Alvaro N A Monteiro; Steven A Narod; Thomas A Sellers; Simon A Gayther; Linda E Kelemen; Georgia Chenevix-Trench; Harvey A Risch; Paul D P Pharoah; Ellen L Goode; Catherine M Phelan

doi:10.1371/journal.pone.0197561

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Variants in genes encoding small GTPases and association with epithelial ovarian cancer susceptibility

Journal article

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Variants in genes encoding small GTPases and association with epithelial ovarian cancer susceptibility

Madalene Earp, Jonathan P Tyrer, Stacey J Winham, Hui-Yi Lin, Ganna Chornokur, Joe Dennis, Katja K H Aben, Hoda Anton-Culver, Natalia Antonenkova, Elisa V Bandera, …

PloS one, Vol.13(7), pp.e0197561-e0197561

2018

DOI: https://doi.org/10.1371/journal.pone.0197561

PMCID: PMC6034790

PMID: 29979793

Abstract

A Kinase Anchor Proteins - genetics

Carcinoma, Ovarian Epithelial - genetics

Carcinoma, Ovarian Epithelial - pathology

Female

Genetic Association Studies

Genetic Predisposition to Disease

Genotype

Humans

Monomeric GTP-Binding Proteins - genetics

Polymorphism, Single Nucleotide - genetics

Quantitative Trait Loci - genetics

Rho Guanine Nucleotide Exchange Factors - genetics

Risk Factors

Epithelial ovarian cancer (EOC) is the fifth leading cause of cancer mortality in American women. Normal ovarian physiology is intricately connected to small GTP binding proteins of the Ras superfamily (Ras, Rho, Rab, Arf, and Ran) which govern processes such as signal transduction, cell proliferation, cell motility, and vesicle transport. We hypothesized that common germline variation in genes encoding small GTPases is associated with EOC risk. We investigated 322 variants in 88 small GTPase genes in germline DNA of 18,736 EOC patients and 26,138 controls of European ancestry using a custom genotype array and logistic regression fitting log-additive models. Functional annotation was used to identify biofeatures and expression quantitative trait loci that intersect with risk variants. One variant, ARHGEF10L (Rho guanine nucleotide exchange factor 10 like) rs2256787, was associated with increased endometrioid EOC risk (OR = 1.33, p = 4.46 x 10-6). Other variants of interest included another in ARHGEF10L, rs10788679, which was associated with invasive serous EOC risk (OR = 1.07, p = 0.00026) and two variants in AKAP6 (A-kinase anchoring protein 6) which were associated with risk of invasive EOC (rs1955513, OR = 0.90, p = 0.00033; rs927062, OR = 0.94, p = 0.00059). Functional annotation revealed that the two ARHGEF10L variants were located in super-enhancer regions and that AKAP6 rs927062 was associated with expression of GTPase gene ARHGAP5 (Rho GTPase activating protein 5). Inherited variants in ARHGEF10L and AKAP6, with potential transcriptional regulatory function and association with EOC risk, warrant investigation in independent EOC study populations.

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Title: Variants in genes encoding small GTPases and association with epithelial ovarian cancer susceptibility
Creators: Madalene Earp - Department of Health Sciences Research, Mayo Clinic, Rochester, MN, United States of America
Jonathan P Tyrer - Department of Oncology, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom
Stacey J Winham - Department of Health Sciences Research, Mayo Clinic, Rochester, MN, United States of America
Hui-Yi Lin - School of Public Health, Louisiana State University Health Sciences Center, New Orleans, LA, United States of America
Ganna Chornokur - Division of Population Sciences, Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United States of America
Joe Dennis - Department of Oncology, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom
Katja K H Aben - Radboud University Medical Center, Radboud Institute for Health Sciences, Nijmegen, The Netherlands
Hoda Anton-Culver - Genetic Epidemiology Research Institute, UCI Center for Cancer Genetics Research and Prevention, School of Medicine, Department of Epidemiology, University of California Irvine, Irvine, CA, United States of America
Natalia Antonenkova - Byelorussian Institute for Oncology and Medical Radiology Aleksandrov N.N., Minsk, Belarus
Elisa V Bandera - Cancer Prevention and Control, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, United States of America
Yukie T Bean - Knight Cancer Institute, Oregon Health & Science University, Portland, OR, United States of America
Matthias W Beckmann - University Breast Center Franconia, Department of Gynecology and Obstetrics, University Hospital Erlangen, Erlangen, Germany
Line Bjorge - Centre for Cancer Biomarkers, Department of Clinical Medicine, University of Bergen, Bergen, Norway
Natalia Bogdanova - Gynaecology Research Unit, Hannover Medical School, Hannover, Germany
Louise A Brinton - Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America
Angela Brooks-Wilson - Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada
Fiona Bruinsma - Cancer Epidemiology & Intelligence Division, The Cancer Council Victoria, Melbourne, Australia
Clareann H Bunker - Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Pittsburgh, PA, United States of America
Ralf Butzow - Department of Obstetrics and Gynecology, University of Helsinki and Helsinki University Central Hospital, Helsinki, Finland
Ian G Campbell - Department of Pathology, University of Melbourne, Melbourne, Victoria, Australia
Karen Carty - Department of Gynaecological Oncology, Glasgow Royal Infirmary, Glasgow, United Kingdom
Jenny Chang-Claude - University Cancer Center Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Linda S Cook - Division of Epidemiology and Biostatistics, University of New Mexico, Albuquerque, NM, United States of America
Daniel W Cramer - Obstetrics and Gynecology Center, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, United States of America
Julie M Cunningham - Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, United States of America
Cezary Cybulski - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Agnieszka Dansonka-Mieszkowska - Department of Pathology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Evelyn Despierre - Division of Gynecologic Oncology, Department of Obstetrics and Gynecology and Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium
Jennifer A Doherty - Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, United States of America
Thilo Dörk - Gynaecology Research Unit, Hannover Medical School, Hannover, Germany
Andreas du Bois - Department of Gynaecology and Gynaecologic Oncology, Kliniken Essen-Mitte/ Evang. Huyssens-Stiftung/ Knappschaft GmbH, Essen, Germany
Matthias Dürst - Department of Gynecology, Friedrich Schiller University, Jena, Germany
Douglas F Easton - Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom
Diana M Eccles - Wessex Clinical Genetics Service, Princess Anne Hospital, Southampton, United Kingdom
Robert P Edwards - Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States of America
Arif B Ekici - Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany
Peter A Fasching - David Geffen School of Medicine, Department of Medicine Division of Hematology and Oncology, University of California at Los Angeles, CA, United States of America
Brooke L Fridley - Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, United States of America
Aleksandra Gentry-Maharaj - Gynaecological Cancer Research Centre, Department of Women's Cancer, Institute for Women's Health, University College London, London, United Kingdom
Graham G Giles - Centre for Epidemiology and Biostatistics, School of Population and Global Health, University of Melbourne, Melbourne, VIC, Australia
Rosalind Glasspool - CRUK Clinical Trials Unit, The Beatson West of Scotland Cancer Centre, Glasgow, United Kingdom
Marc T Goodman - Samuel Oschin Comprehensive Cancer Institute, Cedars Sinai Medical Center, Los Angeles, CA, United States of America
Jacek Gronwald - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Philipp Harter - Department of Gynaecology and Gynaecologic Oncology, Kliniken Essen-Mitte/ Evang. Huyssens-Stiftung/ Knappschaft GmbH, Essen, Germany
Alexander Hein - University Breast Center Franconia, Department of Gynecology and Obstetrics, University Hospital Erlangen, Erlangen, Germany
Florian Heitz - Department of Gynaecology and Gynaecologic Oncology, Kliniken Essen-Mitte/ Evang. Huyssens-Stiftung/ Knappschaft GmbH, Essen, Germany
Michelle A T Hildebrandt - Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, United States of America
Peter Hillemanns - Gynaecology Research Unit, Hannover Medical School, Hannover, Germany
Claus K Hogdall - Department of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Estrid Høgdall - Molecular Unit, Department of Pathology, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark
Satoyo Hosono - Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Aichi, Japan
Edwin S Iversen - Department of Statistics, Duke University, Durham, NC, United States of America
Anna Jakubowska - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Allan Jensen - Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark
Bu-Tian Ji - Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America
Audrey Y Jung - Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Beth Y Karlan - Women's Cancer Program, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, United States of America
Melissa Kellar - Knight Cancer Institute, Oregon Health & Science University, Portland, OR, United States of America
Lambertus A Kiemeney - Radboud University Medical Center, Radboud Institute for Health Sciences, Nijmegen, The Netherlands
Boon Kiong Lim - Department of Obstetrics and Gynaecology, University Malaya Medical Centre, University Malaya, Kuala Lumpur, Malaysia
Susanne K Kjaer - Department of Gynecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Camilla Krakstad - Department of Gynecology and Obstetrics, Haukeland University Hospital, Bergen, Norway
Jolanta Kupryjanczyk - Department of Pathology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Diether Lambrechts - Vesalius Research Center, VIB, University of Leuven, Leuven, Belgium
Sandrina Lambrechts - Division of Gynecologic Oncology; Leuven Cancer Institute, University Hospitals Leuven, KU Leuven, Leuven, Belgium
Nhu D Le - Cancer Control Research, BC Cancer Agency, Vancouver, BC, Canada
Shashi Lele - Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, United States of America
Jenny Lester - Women's Cancer Program, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, United States of America
Douglas A Levine - Gynecology Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY, United States of America
Zheng Li - Department of Gynecologic Oncology, The Third Affiliated Hospital of Kunming Medical University (Yunnan Tumor Hospital), Kunming, China
Dong Liang - College of Pharmacy and Health Sciences, Texas Southern University, Houston, TX, United States of America
Jolanta Lissowska - Department of Cancer Epidemiology and Prevention, M. Sklodowska-Curie Memorial Cancer Center & Institute of Oncology, Warsaw, Poland
Karen Lu - Department of Gynecologic Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, United States of America
Jan Lubinski - International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland
Lene Lundvall - Department of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Leon F A G Massuger - Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Nijmegen, The Netherlands
Keitaro Matsuo - Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Aichi, Japan
Valerie McGuire - Department of Health Research and Policy, Stanford University School of Medicine, Stanford, CA, United States of America
John R McLaughlin - Public Health Ontario, Toronto, ON, Canada
Iain McNeish - Public Health Ontario, Toronto, ON, Canada
Usha Menon - Gynaecological Cancer Research Centre, Department of Women's Cancer, Institute for Women's Health, University College London, London, United Kingdom
Roger L Milne - Centre for Epidemiology and Biostatistics, School of Population and Global Health, University of Melbourne, Melbourne, VIC, Australia
Francesmary Modugno - Womens Cancer Research Program, Magee-Womens Research Institute and University of Pittsburgh Cancer Institute, Pittsburgh, PA, United States of America
Kirsten B Moysich - Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, United States of America
Roberta B Ness - The University of Texas School of Public Health, Houston, TX, United States of America
Heli Nevanlinna - Department of Obstetrics and Gynecology, University of Helsinki and Helsinki University Central Hospital, Helsinki, Finland
Kunle Odunsi - Department of Gynecologic Oncology, Roswell Park Cancer Institute, Buffalo, NY, United States of America
Sara H Olson - Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, United States of America
Irene Orlow - Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, United States of America
Sandra Orsulic - Women's Cancer Program, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, United States of America
James Paul - CRUK Clinical Trials Unit, The Beatson West of Scotland Cancer Centre, Glasgow, United Kingdom
Tanja Pejovic - Knight Cancer Institute, Oregon Health & Science University, Portland, OR, United States of America
Liisa M Pelttari - Department of Obstetrics and Gynecology, University of Helsinki and Helsinki University Central Hospital, Helsinki, Finland
Jenny B Permuth - Division of Population Sciences, Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United States of America
Malcolm C Pike - Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY, United States of America
Elizabeth M Poole - Department of Epidemiology, Harvard School of Public Health, Boston, MA, United States of America
Barry Rosen - Department of Gynecology-Oncology, Princess Margaret Hospital, and Department of Obstetrics and Gynecology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
Mary Anne Rossing - Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, United States of America
Joseph H Rothstein - Department of Population Health Science and Policy, Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, United States of America
Ingo B Runnebaum - Department of Gynecology, Friedrich Schiller University, Jena, Germany
Iwona K Rzepecka - Department of Pathology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
Eva Schernhammer - Department of Epidemiology, Harvard School of Public Health, Boston, MA, United States of America
Ira Schwaab - Institut für Humangenetik Wiesbaden, Wiesbaden, Germany
Xiao-Ou Shu - Epidemiology Center and Vanderbilt, Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, United States of America
Yurii B Shvetsov - Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, United States of America
Nadeem Siddiqui - Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, United States of America
Weiva Sieh - Department of Population Health Science and Policy, Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, United States of America
Honglin Song - School of Public Health, Louisiana State University Health Sciences Center, New Orleans, LA, United States of America
Melissa C Southey - Department of Pathology, University of Melbourne, Melbourne, Victoria, Australia
Beata Spiewankiewicz - Department of Gynecologic Oncology, Institute of Oncology, Warsaw, Poland
Lara Sucheston-Campbell - Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, United States of America
Ingvild L Tangen - Department of Gynecology and Obstetrics, Haukeland University Hospital, Bergen, Norway
Soo-Hwang Teo - University Malaya Medical Centre, University Malaya, Kuala Lumpur, Malaysia
Kathryn L Terry - Department of Epidemiology, University of Michigan, Ann Arbor, MI, United States of America
Pamela J Thompson - Samuel Oschin Comprehensive Cancer Institute, Cedars Sinai Medical Center, Los Angeles, CA, United States of America
Lotte Thomsen - Department of Pathology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
Shelley S Tworoger - Department of Epidemiology, Harvard School of Public Health, Boston, MA, United States of America
Anne M van Altena - Department of Obstetrics and Gynecology, Radboud University Medical Center, Nijmegan, The Netherlands
Ignace Vergote - Division of Gynecologic Oncology; Leuven Cancer Institute, University Hospitals Leuven, KU Leuven, Leuven, Belgium
Liv Cecilie Vestrheim Thomsen - Department of Gynecology and Obstetrics, Haukeland University Hospital, Bergen, Norway
Robert A Vierkant - Department of Health Sciences Research, Mayo Clinic, Rochester, MN, United States of America
Christine S Walsh - Women's Cancer Program, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, United States of America
Shan Wang-Gohrke - German Cancer Consortium (DKTK) and German Cancer Research Center (DKFZ), Heidelberg, Germany
Nicolas Wentzensen - Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America
Alice S Whittemore - Department of Health Research and Policy, Department of Biomedical Data Science, Stanford University School of Medicine, Stanford, CA, United States of America
Kristine G Wicklund - Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, United States of America
Lynne R Wilkens - Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, United States of America
Yin-Ling Woo - Cancer Research Malaysia, Subang Jaya Selangor, Malaysia
Anna H Wu - Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States of America
Xifeng Wu - Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, United States of America
Yong-Bing Xiang - Department of Epidemiology, Shanghai Cancer Institute, Shanghai, China
Hannah Yang - Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, United States of America
Wei Zheng - Vanderbilt Epidemiology Center, Vanderbilt University School of Medicine, Nashville, TN, United States of America
Argyrios Ziogas - Genetic Epidemiology Research Institute, UCI Center for Cancer Genetics Research and Prevention, School of Medicine, Department of Epidemiology, University of California Irvine, Irvine, CA, United States of America
Alice W Lee - Department of Health Science, California State University, Fullerton, Fullerton, CA, United States of America
Celeste L Pearce - Department of Epidemiology, University of Michigan, Ann Arbor, MI, United States of America
Andrew Berchuck - Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC, United States of America
Joellen M Schildkraut - Department of Public Health Sciences, The University of Virginia, Charlottesville, VA, United States of America
Susan J Ramus - The Garvan Institute, Sydney, New South Wales, Australia
Alvaro N A Monteiro - Division of Population Sciences, Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United States of America
Steven A Narod - Women's College Research Institute, University of Toronto, Toronto, Ontario, Canada
Thomas A Sellers - Division of Population Sciences, Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United States of America
Simon A Gayther - Center for Cancer Prevention and Translational Genomics, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, United States of America
Linda E Kelemen - Department of Public Health Sciences, Medical University of South Carolina and Hollings Cancer Center, Charleston, SC, United States of America
Georgia Chenevix-Trench - Department of Genetics, QIMR Berghofer Medical Research Institute, Brisbane, Australia
Harvey A Risch - Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, CT, United States of America
Paul D P Pharoah - Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Worts Causeway, Cambridge, United Kingdom
Ellen L Goode - Department of Health Sciences Research, Mayo Clinic, Rochester, MN, United States of America
Catherine M Phelan - Division of Population Sciences, Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United States of America
Publication Details: PloS one, Vol.13(7), pp.e0197561-e0197561
Date published: 2018
Grant note: R03 CA113148 / NCI NIH HHS UM1 CA182910 / NCI NIH HHS R01 CA058860 / NCI NIH HHS C490/A10119 / Cancer Research UK UL1 TR001881 / NCATS NIH HHS K22 CA138563 / NCI NIH HHS 10119 / Cancer Research UK G0601891 / Medical Research Council R03 CA115195 / NCI NIH HHS K07 CA095666 / NCI NIH HHS R01 CA112523 / NCI NIH HHS P30 CA071789 / NCI NIH HHS R01 CA114343 / NCI NIH HHS R01 CA149429 / NCI NIH HHS U01 CA069417 / NCI NIH HHS R01 CA058598 / NCI NIH HHS U19 CA148112 / NCI NIH HHS C490/A10124 / Cancer Research UK C490/A6187 / Cancer Research UK R01 CA067262 / NCI NIH HHS R01 CA080742 / NCI NIH HHS P50 CA105009 / NCI NIH HHS UL1 TR000124 / NCATS NIH HHS R01 CA083918 / NCI NIH HHS R01 CA074850 / NCI NIH HHS R01 CA054419 / NCI NIH HHS R01 CA136924 / NCI NIH HHS R01 CA050385 / NCI NIH HHS K07 CA143047 / NCI NIH HHS P30 CA008748 / NCI NIH HHS MOP-86727 / CIHR UM1 CA186107 / NCI NIH HHS P50 CA136393 / NCI NIH HHS R01 CA087538 / NCI NIH HHS R01 CA122443 / NCI NIH HHS R01 CA049449 / NCI NIH HHS R01 CA126841 / NCI NIH HHS G0501974 / Medical Research Council U01 AR067166 / NIAMS NIH HHS
Academic Unit: Cancer Epidemiology and Health Outcomes
Language: English
Resource Type: Journal article
Identifiers: 991031665379904646