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Multiple independent variants at the TERT locus are associated with telomere length and risks of breast and ovarian cancer

Nature Genetics volume 45, pages 371–384 (2013)Cite this article

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Abstract

TERT-locus SNPs and leukocyte telomere measures are reportedly associated with risks of multiple cancers. Using the Illumina custom genotyping array iCOGs, we analyzed ∼480 SNPs at the TERT locus in breast (n = 103,991), ovarian (n = 39,774) and BRCA1 mutation carrier (n = 11,705) cancer cases and controls. Leukocyte telomere measurements were also available for 53,724 participants. Most associations cluster into three independent peaks. The minor allele at the peak 1 SNP rs2736108 associates with longer telomeres (P = 5.8 × 10−7), lower risks for estrogen receptor (ER)-negative (P = 1.0 × 10−8) and BRCA1 mutation carrier (P = 1.1 × 10−5) breast cancers and altered promoter assay signal. The minor allele at the peak 2 SNP rs7705526 associates with longer telomeres (P = 2.3 × 10−14), higher risk of low-malignant-potential ovarian cancer (P = 1.3 × 10−15) and greater promoter activity. The minor alleles at the peak 3 SNPs rs10069690 and rs2242652 increase ER-negative (P = 1.2 × 10−12) and BRCA1 mutation carrier (P = 1.6 × 10−14) breast and invasive ovarian (P = 1.3 × 10−11) cancer risks but not via altered telomere length. The cancer risk alleles of rs2242652 and rs10069690, respectively, increase silencing and generate a truncated TERT splice variant.

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Figure 1: Association results for all SNPs with seven phenotypes.
Figure 2: Associated signals within the TERT gene.
Figure 3: Open chromatin signatures around rs10069690.
Figure 4: TERT promoter and PRE activity.

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Acknowledgements

We thank all the individuals who took part in these studies and all the researchers, clinicians, technicians and administrative staff who have enabled this work to be carried out. COGS is funded through a grant from the European Commission's Seventh Framework Programme (agreement 223175–HEALTH-F2-2009-223175). BCAC is funded by Cancer Research UK (C1287/A10118 and C1287/A12014). BCAC meetings have been funded by the European Union Cooperation in Science and Technology (COST) programme (BM0606). Telomere length measurement and analysis were funded by Cancer Research UK project grant C1287/A9540 and Chief Physician Johan Boserup and Lise Boserup's Fund. CIMBA data management and analysis were supported by Cancer Research UK grants C12292/A11174 and C1287/A10118. OCAC is supported by a grant from the Ovarian Cancer Research Fund thanks to the family and friends of Kathryn Sladek Smith (PPD/RPCI.07). Genotyping of the iCOGS array was funded by the European Union (HEALTH-F2-2009-223175), Cancer Research UK (C1287/A10710), the Canadian Institutes of Health Research (CIHR) for the CIHR Team in Familial Risks of Breast Cancer program (J.S. and D.E.) and the Ministry of Economic Development, Innovation and Export Trade of Quebec (grant PSR-SIIRI-701; J.S., D.E. and P. Hall). Scientific development and funding of the OCAC portion of this project were supported by Genetic Associations and Mechanisms in Oncology (GAME-ON; U19-CA148112). CIMBA genotyping was supported by US National Institutes of Health (NIH) grant CA128978, a National Cancer Institute (NCI) Specialized Program of Research Excellence (SPORE) in Breast Cancer (CA116201), a US Department of Defense Ovarian Cancer Idea award (W81XWH-10-1-0341) and grants from the Breast Cancer Research Foundation and the Komen Foundation for the Cure. This study made use of data generated by The Wellcome Trust Case Control Consortium (funding was provided by Wellcome Trust award 076113) and the TCGA Pilot Project established by NCI and the National Human Genome Research Institute.

Author information

Author notes

  1. Stig E Bojesen, Karen A Pooley, Sharon E Johnatty, Jonathan Beesley, Kyriaki Michailidou, Jonathan P Tyrer and Andrew Berchuck: These authors contributed equally to this work.

  2. Douglas F Easton, Andrew Berchuck, Antonis C Antoniou, Georgia Chenevix-Trench and Alison M Dunning: These authors jointly directed this work.

Authors and Affiliations

  1. Copenhagen General Population Study, Herlev Hospital, Copenhagen University Hospital, University of Copenhagen, Copenhagen, Denmark

    Stig E Bojesen, Maren Weischer, Sune F Nielsen & Børge G Nordestgaard

  2. Department of Clinical Biochemistry, Herlev Hospital, Copenhagen University Hospital, University of Copenhagen, Copenhagen, Denmark

    Stig E Bojesen, Maren Weischer, Sune F Nielsen & Børge G Nordestgaard

  3. Department of Public Health and Primary Care, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK

    Karen A Pooley, Kyriaki Michailidou, Manjeet K Bolla, Qin Wang, Joe Dennis, Lesley McGuffog, Daniel Barrowdale, Andrew Lee, Michael Lush, Judith Brown, Robert Luben, Susan Peock, Debra Frost, Elena Fineberg, Radka Platte, Steve D Ellis, Karoline B Kuchenbaecker, Ed Dicks, Douglas F Easton & Antonis C Antoniou

  4. Department of Genetics, Queensland Institute of Medical Research, Brisbane, Queensland, Australia

    Sharon E Johnatty, Jonathan Beesley, Yi Lu, Xiaoqing Chen, Sue Healey, Amanda B Spurdle & Georgia Chenevix-Trench

  5. Department of Oncology, Centre for Cancer Genetic Epidemiology, University of Cambridge, Cambridge, UK

    Jonathan P Tyrer, Melanie J Maranian, Maya Ghoussaini, Shahana Ahmed, Caroline Baynes, Mitul Shah, Honglin Song, Catherine S Healey, Craig Luccarini, Paul D P Pharoah, Douglas F Easton & Alison M Dunning

  6. School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland, Australia

    Stacey L Edwards, Kristine M Hillman & Juliet D French

  7. Cancer Research Unit, Children's Medical Research Institute, Westmead, New South Wales, Australia

    Hilda A Pickett, Michael D Stutz & Roger R Reddel

  8. Sydney Medical School, University of Sydney, Sydney, New South Wales, Australia

    Hilda A Pickett, Michael D Stutz & Roger R Reddel

  9. Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA

    Howard C Shen, Kate Lawrenson, Rod Karevan, Christopher A Haiman, Anna H Wu, Brian E Henderson, Fredrick Schumacher, Susan J Ramus, Celeste L Pearce, Malcolm C Pike, Chiu-Chen Tseng, Daniel O Stram, David van den Berg & Simon A Gayther

  10. University of Queensland, UQ Centre for Clinical Research (UQCCR) Royal Brisbane and Women's Hospital, Herston, Queensland, Australia

    Chanel E Smart, Rebecca L Johnston & Sunil R Lakhani

  11. Division of Cancer Epidemiology and Genetics, Clinical Genetics Branch, National Cancer Institute, US National Institutes of Health, Rockville, Maryland, USA

    Phuong L Mai, Sharon A Savage & Mark H Greene

  12. Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA

    Nicholas Woods, Catherine M Phelan, Jenny Permuth-Wey, Thomas A Sellers & Alvaro N A Monteiro

  13. McGill University and Génome Québec Innovation Centre, Montréal, Quebec, Canada

    Daniel C Tessier, Daniel Vincent & Françis Bacot

  14. Department of Obstetrics and Gynaecology, Division of Gynecologic Oncology, University Hospitals Leuven, Leuven, Belgium

    Ignace Vergote, Sandrina Lambrechts & Evelyn Despierre

  15. Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium

    Ignace Vergote, Sandrina Lambrechts & Evelyn Despierre

  16. Department of Epidemiology and Public Health, Yale University School of Public Health and School of Medicine, New Haven, Connecticut, USA

    Harvey A Risch

  17. Centro Nacional de Genotipación, Human Cancer Genetics Program, Spanish National Cancer Research Centre (CNIO), Madrid, Spain

    Anna González-Neira, Guillermo Pita, Nuria Álvarez & Javier Benitez

  18. Department of Epidemiology, University of Washington, Seattle, Washington, USA

    Mary Anne Rossing

  19. Division of Public Health Sciences, Program in Epidemiology, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA

    Mary Anne Rossing

  20. Section of Biostatistics and Epidemiology, The Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire, USA

    Jennifer A Doherty

  21. Department of Health Science Research, Division of Biomedical Statistics and Informatics, Mayo Clinic, Rochester, Minnesota, USA

    Melissa C Larson, Sebastian M Armasu & Robert A Vierkant

  22. Kansas IDeA Network of Biomedical Research Excellence Bioinformatics Core, The University of Kansas Cancer Center, Kansas City, Kansas, USA

    Brooke L Fridley

  23. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

    Nils Schoof, Mikael Hartman, Kamila Czene, Keith Humphreys & Per Hall

  24. Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany

    Jenny Chang-Claude, Rebecca Hein, Anja Rudolph & Stefan Nickels

  25. Department of Health Science Research, Division of Epidemiology, Mayo Clinic, Rochester, Minnesota, USA

    Mine S Cicek & Ellen L Goode

  26. Department of Non-communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK

    Julian Peto, Isabel Dos Santos Silva & Lorna Gibson

  27. Department of Medical Oncology, Mayo Clinic, Rochester, Minnesota, USA

    Kimberly R Kalli

  28. Division of Molecular Pathology, Netherlands Cancer Institute, Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands

    Annegien Broeks, Marjanka K Schmidt, Linde M Braaf & Matti A Rookus

  29. Division of Psychosocial Research and Epidemiology, Netherlands Cancer Institute, Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands

    Marjanka K Schmidt

  30. Department of Obstetrics and Gynecology, Mayo Clinic, Rochester, Minnesota, USA

    Boris Winterhoff, Lisa Rogmann & Attila Teoman

  31. Department of Obstetrics and Gynecology, Helsinki University Central Hospital, University of Helsinki, Helsinki, Finland

    Heli Nevanlinna, Ralf Butzow, Liisa M Pelttari, Arto Leminen & Taru A Muranen

  32. Division of Hematology and Oncology, Department of Medicine, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, California, USA

    Gottfried E Konecny & Peter A Fasching

  33. Department of Oncology, Laboratory for Translational Genetics, University of Leuven, Leuven, Belgium

    Diether Lambrechts & Els Wauters

  34. Vesalius Research Center (VRC), VIB, Leuven, Belgium

    Diether Lambrechts & Els Wauters

  35. Institut National de la Santé et de la Recherche Médicale (INSERM) U1018, CESP (Center for Research in Epidemiology and Population Health), Environmental Epidemiology of Cancer, Villejuif, France

    Pascal Guénel & Thérèse Truong

  36. University Paris–Sud, Unité Mixte de Recherche Scientifique (UMRS) 1018, Villejuif, France

    Pascal Guénel & Thérèse Truong

  37. Genetic and Molecular Epidemiology Group, Human Cancer Genetics Program, CNIO, Madrid, Spain

    Roger L Milne

  38. Department of Laboratory Medicine and Pathology, Division of Experimental Pathology, Mayo Clinic, Rochester, Minnesota, USA

    Joaquin J Garcia, Vijayalakshmi Shridhar, Xianshu Wang, Julie M Cunningham & Fergus J Couch

  39. Department of Oncology, Cancer Research UK/Yorkshire Cancer Research Sheffield Cancer Research Centre, University of Sheffield, Sheffield, UK

    Angela Cox & Sabapathy P Balasubramanian

  40. Department of Obstetrics and Gynecology, University of Heidelberg, Heidelberg, Germany

    Barbara Burwinkel, Frederik Marme, Andreas Schneeweiss & Christof Sohn

  41. Molecular Epidemiology Group, DKFZ, Heidelberg, Germany

    Barbara Burwinkel

  42. National Center for Tumor Diseases, University of Heidelberg, Heidelberg, Germany

    Frederik Marme & Andreas Schneeweiss

  43. Primärmedizinische Versorgung (PMV) Research Group at the Department of Child and Adolescent Psychiatry and Psychotherapy, University of Cologne, Cologne, Germany

    Rebecca Hein

  44. Division of Cancer Studies, National Institute for Health Research (NIHR) Comprehensive Biomedical Research Centre, Guy's & St. Thomas' National Health Service (NHS) Foundation Trust in partnership with King's College London, London, UK

    Elinor J Sawyer

  45. Department of Obstetrics and Gynecology, University of Ulm, Ulm, Germany

    Shan Wang-Gohrke & Helmut Deissler

  46. Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada

    Irene L Andrulis

  47. Ontario Cancer Genetics Network, Fred A. Litwin Center for Cancer Genetics, Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada

    Irene L Andrulis

  48. Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, New York, USA

    Kirsten B Moysich & Kunle Odunsi

  49. Centre for Molecular, Environmental, Genetic and Analytic Epidemiology, University of Melbourne, Melbourne, Victoria, Australia

    John L Hopper, Graham G Giles, Carmel Apicella, Gianluca Severi & Laura Baglietto

  50. Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden

    Annika Lindblom

  51. Cancer Epidemiology Centre, The Cancer Council Victoria, Melbourne, Victoria, Australia

    Graham G Giles, Gianluca Severi & Laura Baglietto

  52. Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Victoria, Australia

    Graham G Giles

  53. Division of Clinical Epidemiology and Aging Research, DKFZ, Heidelberg, Germany

    Hermann Brenner, Heiko Müller & Volker Arndt

  54. Cancer Genomics Laboratory, Centre Hospitalier Universitaire de Québec and Laval University, Quebec City, Quebec, Canada

    Jacques Simard, Martine Dumont & Penny Soucy

  55. Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii, USA

    Galina Lurie, Michael E Carney, Lynne R Wilkens & Loic Le Marchand

  56. Department of Gynecology and Obstetrics, University Breast Center for Franconia Erlangen University Hospital, Erlangen, Germany

    Peter A Fasching, Matthias W Beckmann & Michael P Lux

  57. Department of Preventive and Predictive Medicine, Unit of Molecular Bases of Genetic Risk and Genetic Testing, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Istituto Nazionale Tumori (INT), Milan, Italy

    Paolo Radice & Paolo Peterlongo

  58. Istituto Fondazione Italiana per la Ricerca sul Cancro di Oncologia Molecolare, Milan, Italy

    Paolo Radice, Filomena Ficarazzi & Paolo Peterlongo

  59. Division of Genetics and Epidemiology, The Institute of Cancer Research, Sutton, UK

    Anthony Swerdlow & Michael Jones

  60. Division of Breast Cancer Research, The Institute of Cancer Research, Sutton, UK

    Anthony Swerdlow

  61. Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California, USA

    Marc T Goodman

  62. Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany

    Hiltrud Brauch

  63. Faculty of Medicine, University of Tübingen, Tübingen, Germany

    Hiltrud Brauch

  64. Division of Breast Cancer Research, Breakthrough Breast Cancer Research Centre, The Institute of Cancer Research, London, UK

    Montserrat Garcia-Closas, Olivia Fletcher, Alan Ashworth & Nick Orr

  65. Clinics of Obstetrics and Gynaecology, Hannover Medical School, Hannover, Germany

    Peter Hillemanns

  66. Department of Clinical Genetics, Laboratory of Cancer Genetics and Tumor Biology, University of Oulu, Oulu University Hospital, Oulu, Finland

    Robert Winqvist & Katri Pylkäs

  67. Biocenter Oulu, University of Oulu, Oulu, Finland

    Robert Winqvist & Katri Pylkäs

  68. Department of Gynecology, Jena University Hospital, Jena, Germany

    Matthias Dürst & Ingo Runnebaum

  69. Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands

    Peter Devilee

  70. Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands

    Peter Devilee

  71. Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland

    Anna Jakubowska, Jan Lubinski, Katarzyna Durda, Katarzyna Jaworska, Aleksandra Toloczko-Grabarek, Jacek Gronwald & Tomasz Byrski

  72. Department of Clinical Pathology, Imaging Center, Kuopio University Hospital, Kuopio, Finland

    Arto Mannermaa, Jaana M Hartikainen & Veli-Matti Kosma

  73. School of Medicine, Institute of Clinical Medicine, Pathology and Forensic Medicine, Biocenter Kuopio, Cancer Center of Eastern Finland, University of Eastern Finland, Kuopio, Finland

    Arto Mannermaa, Jaana M Hartikainen, Veli-Matti Kosma & Vesa Kataja

  74. Department of Pathology, Helsinki University Central Hospital, Helsinki, Finland

    Ralf Butzow

  75. Department of Obstetrics and Gynaecology, Hannover Medical School, Hannover, Germany

    Natalia V Bogdanova & Thilo Dörk

  76. Department of Radiation Oncology, Hannover Medical School, Hannover, Germany

    Natalia V Bogdanova & Qiuyin Cai

  77. Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA

    Wei Zheng, Xiao-Ou Shu, William Blot, Gong Yang, Jirong Long, Martha Shrubsole, Sandra Deming-Halverson, Hui Cai & Lisa B Signorello

  78. Department of Epidemiology, University of California–Irvine, Irvine, California, USA

    Hoda Anton-Culver

  79. Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

    Clareann H Bunker

  80. Department of Genetics, Institute for Cancer Research, Oslo University Hospital, Radiumhospitalet, Oslo, Norway

    Vessela Kristensen

  81. Faculty of Medicine (Faculty Division Ahus), Universitetet i Oslo, Oslo, Norway

    Vessela Kristensen

  82. The University of Texas School of Public Health, Houston, Texas, USA

    Roberta B Ness

  83. Warwick Medical School, Warwick University, Coventry, UK

    Kenneth Muir, Artitaya Lophatananon & Sarah Stewart-Brown

  84. Institute of Population Health, University of Manchester, Manchester, UK

    Kenneth Muir & Artitaya Lophatananon

  85. Maggee Women's Hospital, Pittsburgh, Pennsylvania, USA

    Robert Edwards

  86. Department of Gynecology and Obstetrics, Division of Tumor Genetics, Klinikum Rechts der Isar, Technical University Munich, Munich, Germany

    Alfons Meindl

  87. Department of Gynecology and Gynecologic Oncology, Dr. Horst Schmidt Klinik Wiesbaden, Wiesbaden, Germany

    Florian Heitz, Andreas du Bois & Philipp Harter

  88. Department of Gynecology and Gynecologic Oncology, Kliniken Essen-Mitte, Essen, Germany

    Florian Heitz, Andreas du Bois & Philipp Harter

  89. Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan

    Keitaro Matsuo, Satoyo Hosono, Hidemi Ito & Kazuo Tajima

  90. Cancer Research Initiatives Foundation, Sime Darby Medical Centre, Subang Jaya, Malaysia

    Soo-Hwang Teo

  91. Breast Cancer Research Unit, University Malaya Cancer Research Institute, University Malaya Medical Centre, Kuala Lumpur, Malaysia

    Soo-Hwang Teo, Cheng Har Yip & Yew-Ching Teh

  92. Institut für Humangenetik Wiesbaden, Wiesbaden, Germany

    Ira Schwaab

  93. International Epidemiology Institute, Rockville, Maryland, USA

    William Blot & Lisa B Signorello

  94. Seoul National University College of Medicine, Seoul, Korea

    Daehee Kang, Dong-Young Noh & Keun-Young Yoo

  95. Department of Gynecologic Oncology, Aichi Cancer Center Central Hospital, Nagoya, Japan

    Toru Nakanishi

  96. Department of Surgery, Yong Loo Lin School of Medicine, National University of Singapore, Singapore

    Mikael Hartman & Philip Tsau-Choong Iau

  97. Saw Swee Hock School of Public Health, National University of Singapore, Singapore

    Mikael Hartman, Hui Miao & Yik Ying Teo

  98. Department of Pathology and Molecular Diagnostic, Aichi Cancer Center Central Hospital, Nagoya, Japan

    Yasushi Yatabe

  99. Molecular Genetics of Breast Cancer, DKFZ, Heidelberg, Germany

    Ute Hamann

  100. Women's Cancer Program, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California, USA

    Beth Y Karlan & Jenny Lester

  101. Research Division, National Cancer Institute, Bangkok, Thailand

    Suleeporn Sangrajrang

  102. Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark

    Susanne Krüger Kjaer, Allan Jensen & Estrid Høgdall

  103. Department of Obstetrics and Gynecology, The Juliane Marie Centre, Rigshospitalet, Copenhagen, Denmark

    Susanne Krüger Kjaer & Claus K Høgdall

  104. International Agency for Research on Cancer, Lyon, France

    Valerie Gaborieau & James McKay

  105. Faculty of Medicine, University of Southampton, University Hospital Southampton, Southampton, UK

    Diana Eccles

  106. Department of Pathology, Molecular Unit, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark

    Estrid Høgdall

  107. Colleague of Public Health, China Medical University, Taichong, Taiwan

    Chen-Yang Shen

  108. Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan

    Chen-Yang Shen & Chia-Ni Hsiung

  109. Department of Obstetrics and Gynaecology, Faculty of Medicine, University Malaya Medical Centre, University Malaya, Kuala Lumpur, Malaysia

    Yin Ling Woo, Mat Adenan Noor Azmi & Siti Zawiah Omar

  110. Department of Breast Surgery, Herlev Hospital, Copenhagen University Hospital, Copenhagen, Denmark

    Henrik Flyger

  111. Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota, USA

    Celine Vachon, Janet E Olson, Curtis Olswold, Susan Slager, Vernon S Pankratz & Fergus J Couch

  112. Department of Surgery, Gynecology Service, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

    Douglas A Levine

  113. Department of Community and Family Medicine, Duke University Medical Center, Durham, North Carolina, USA

    Rachel Palmieri Weber & Joellen M Schildkraut

  114. Department of Cancer Epidemiology/Clinical Cancer Registry, University Clinic Hamburg–Eppendorf, Hamburg, Germany

    Dieter Flesch-Janys

  115. Institute for Medical Biometrics and Epidemiology, University Clinic Hamburg–Eppendorf, Hamburg, Germany

    Dieter Flesch-Janys

  116. Department of Statistical Science, Duke University, Durham, North Carolina, USA

    Edwin Iversen

  117. Cancer Prevention, Detection and Control Research Program, Duke Cancer Institute, Durham, North Carolina, USA

    Edwin Iversen & Joellen M Schildkraut

  118. Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA

    Daniel W Cramer, Kathryn L Terry & Allison F Vitonis

  119. Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA

    Daniel W Cramer, Kathryn L Terry, Elizabeth M Poole & Shelley S Tworoger

  120. Sanquin Research, Amsterdam, The Netherlands

    C Ellen van der Schoot

  121. Channing Division of Network Medicine, Harvard Medical School and Brigham and Women's Hospital, Boston, Massachusetts, USA

    Elizabeth M Poole & Shelley S Tworoger

  122. Netherlands Cancer Institute, Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands

    Frans B L Hogervorst

  123. Division of Human Genetics, Genome Institute of Singapore, Singapore

    Jianjun Liu & Jingmei Li

  124. The Cancer Institute of New Jersey, Robert Wood Johnson Medical School, New Brunswick, New Jersey, USA

    Elisa V Bandera & Lorna Rodriguez-Rodriguez

  125. Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

    Sara H Olson, Irene Orlow & Malcolm C Pike

  126. Department of Oncology, University of Helsinki and Helsinki University Central Hospital, Helsinki, Finland

    Carl Blomqvist

  127. Department of Clinical Genetics, Helsinki University Central Hospital, University of Helsinki, Helsinki, Finland

    Kristiina Aittomäki

  128. Department of Gynecology and Obstetrics, Haukeland University Hospital, Bergen, Norway

    Helga B Salvesen, Elisabeth Wik, Camilla Krakstad & Mari K Halle

  129. Department of Clinical Medicine, University of Bergen, Bergen, Norway

    Helga B Salvesen, Elisabeth Wik, Camilla Krakstad & Mari K Halle

  130. Department of Oncology, Laboratory of Experimental Oncology, Leuven, KU Leuven, Belgium

    Barbara Brouwers

  131. Department of General Medical Oncology, University Hospitals Leuven, Leuven Cancer Institute, Leuven, Belgium

    Barbara Brouwers & Hans Wildiers

  132. Comprehensive Cancer Center The Netherlands, Utrecht, The Netherlands

    Lambertus A Kiemeney & Katja K Aben

  133. Department of Epidemiology, Biostatistics and Health Technology Assessment, Radboud University Medical Centre, Nijmegen, The Netherlands

    Lambertus A Kiemeney & Katja K Aben

  134. Department of Urology, Radboud University Medical Centre, Nijmegen, The Netherlands

    Lambertus A Kiemeney

  135. Université Paris Sorbonne Cité, Unité Mixte de Recherche (UMR) S775, INSERM, Paris, France

    Claire Mulot & Pierre Laurent-Puig

  136. Department of Gynecology, Radboud University Medical Centre, Nijmegen, The Netherlands

    Anne Mvan Altena & Leon F A G Massuger

  137. Human Genetics Group, CNIO, Madrid, Spain

    Javier Benitez

  138. Biomedical Network on Rare Diseases (CIBERER), Madrid, Spain

    Javier Benitez

  139. Department of Obstetrics and Gynecology, Oregon Health and Science University, Portland, Oregon, USA

    Tanja Pejovic

  140. Knight Cancer Institute, Oregon Health and Science University, Portland, Oregon, USA

    Tanja Pejovic

  141. Servicio de Cirugía General y Especialidades, Hospital Monte Naranco, Oviedo, Spain

    Jose Ignacio Arias Perez

  142. Department of Biochemistry and Molecular Biology, Oregon Health and Science University, Portland, Oregon, USA

    Maureen Hoatlin

  143. Servicio de Oncología Médica, Hospital Universitario La Paz, Madrid, Spain

    M Pilar Zamora

  144. Division of Epidemiology and Biostatistics, University of New Mexico, Albuquerque, New Mexico, USA

    Linda S Cook

  145. Department of Population Health Research, Alberta Health Services–Cancer Care, Calgary, Alberta, Canada

    Linda E Kelemen

  146. Department of Medical Genetics, University of Calgary, Calgary, Alberta, Canada

    Linda E Kelemen

  147. Department of Oncology, University of Calgary, Calgary, Alberta, Canada

    Linda E Kelemen

  148. Cancer Control Research, British Columbia Cancer Agency, Vancouver, British Columbia, Canada

    Nhu D Le

  149. Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, British Columbia, Canada

    Angela Brooks-Wilson

  150. Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada

    Angela Brooks-Wilson

  151. Welcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK

    Ian Tomlinson

  152. Oxford Biomedical Research Centre, University of Oxford, Oxford, UK

    Ian Tomlinson

  153. School of Medicine, National University of Ireland, Galway, Ireland

    Michael J Kerin & Nicola Miller

  154. Department of Genetics and Pathology, International Hereditary Cancer Center, Pomeranian Medical Academy, Szczecin, Poland

    Cezary Cybulski

  155. Department of Surgical Gynecology and Gynecological Oncology of Adults and Adolescents, Pomeranian Medical University, Szczecin, Poland

    Janusz Menkiszak

  156. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland, USA

    Nicolas Wentzensen, Hannah P Yang, Jonine Figueroa & Stephen J Chanock

  157. Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada

    Anna Marie Mulligan

  158. Laboratory Medicine Program, University Health Network, Toronto, Ontario, Canada

    Anna Marie Mulligan

  159. Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada

    Gord Glendon & John R McLaughlin

  160. Department of Radiation Oncology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark

    Svend Aage Engelholm

  161. Division of Epidemiology, Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada

    Julia A Knight

  162. Prosserman Centre for Health Research, Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada

    Julia A Knight

  163. Gynecological Oncology Unit, The Royal Marsden Hospital, London, UK

    Martin Gore

  164. Department of Pathology, Genetic Epidemiology Laboratory, The University of Melbourne, Melbourne, Victoria, Australia

    Helen Tsimiklis & Melissa C Southey

  165. Department of Medical Oncology, Family Cancer Clinic, Erasmus University Medical Center, Rotterdam, The Netherlands

    Agnes Jager, John W M Martens, Mieke Kriege, Antoinette Hollestelle, Caroline Seynaeve & Maartje J Hooning

  166. Department of Clinical Genetics, Family Cancer Clinic, Erasmus University Medical Center, Rotterdam, The Netherlands

    Ans M Wvan den Ouweland & J Margriet Collée

  167. Department of Surgery and Cancer, Imperial College London, London, UK

    Robert Brown & James M Flanagan

  168. The Beatson West of Scotland Cancer Centre, Glasgow, UK

    James Paul

  169. Department of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden

    Sara Margolin

  170. Department of Gynecological Oncology, Glasgow Royal Infirmary, Glasgow, UK

    Nadeem Siddiqui

  171. Department of Health Research and Policy, Stanford University School of Medicine, Stanford, California, USA

    Alice S Whittemore, Valerie McGuire & Weiva Sieh

  172. Saarland Cancer Registry, Saarbrücken, Germany

    Christa Stegmaier

  173. Department of Environmental and Occupational Health, Faculty of Medicine, University of Montreal, Montreal, Quebec, Canada

    France Labrèche

  174. Department of Epidemiology, Shanghai Cancer Institute, Shanghai, China

    Yu-Tang Gao

  175. Department of Medicine, McGill University, Montréal, Quebec, Canada

    Mark S Goldberg

  176. Division of Clinical Epidemiology, McGill University Health Centre, Royal Victoria Hospital, Montréal, Quebec, Canada

    Mark S Goldberg

  177. Dalla Lana School of Public Health, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada

    John R McLaughlin

  178. Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander University Erlangen–Nuremberg, Erlangen, Germany

    Arndt Hartmann

  179. Institute of Human Genetics, Friedrich Alexander University Erlangen–Nuremberg, Erlangen, Germany

    Arif B Ekici

  180. Department of Preventive and Predictive Medicine, Unit of Medical Genetics, Fondazione IRCCS INT, Milan, Italy

    Bernard Peissel, Daniela Zaffaroni & Siranoush Manoukian

  181. Cogentech Cancer Genetic Test Laboratory, Milan, Italy

    Filomena Ficarazzi & Loris Bernard

  182. Division of Cancer Prevention and Genetics, Istituto Europeo di Oncologia, Milan, Italy

    Monica Barile & Bernardo Bonanni

  183. Department of Epidemiology, Center for Cancer Genetics Research and Prevention, School of Medicine, University of California–Irvine, Irvine, California, USA

    Argyrios Ziogas

  184. Gynaecological Cancer Research Centre, University College London Elizabeth Garrett Anderson Institute for Women's Health, London, UK

    Aleksandra Gentry-Maharaj & Usha Menon

  185. Institute for Prevention and Occupational Medicine of the German Social Accident Insurance, Institute of the Ruhr–Universität Bochum, Bochum, Germany

    Thomas Brüning

  186. Department of Internal Medicine, Evangelische Kliniken Bonn, Johanniter Krankenhaus, Bonn, Germany

    Yon-Dschun Ko

  187. Department of Cancer Epidemiology and Prevention, M. Sklodowska-Curie Memorial Cancer Center & Institute of Oncology, Warsaw, Poland

    Jolanta Lissowska

  188. Department of Molecular Pathology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland

    Jolanta Kupryjanczyk, Agnieszka Dansonka-Mieszkowska & Iwona K Rzepecka

  189. Department of Oncology, Oulu University Hospital, University of Oulu, Oulu, Finland

    Arja Jukkola-Vuorinen

  190. Department of Gynecologic Oncology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland

    Mariusz Bidzinski

  191. Department of Pathology, Oulu University Hospital, University of Oulu, Oulu, Finland

    Saila Kauppila

  192. Department of Surgical Oncology, Leiden University Medical Center, Leiden, The Netherlands

    Rob A E M Tollenaar

  193. Postgraduate School of Molecular Medicine, Warsaw Medical University, Warsaw, Poland

    Katarzyna Jaworska

  194. N.N. Alexandrov Research Institute of Oncology and Medical Radiology, Minsk, Belarus

    Natalia N Antonenkova

  195. Ministry of Public Health, Bangkok, Thailand

    Pornthep Siriwanarangsan

  196. Department of Gynecology and Obstetrics, Ludwig-Maximilians-Universität, Munich, Germany

    Nina Ditsch

  197. Insitute of Human Genetics, Technische Universität, Munich, Germany

    Peter Lichtner

  198. Department of Gynaecology and Obstetrics, Centre of Familial Breast and Ovarian Cancer, University Hospital of Cologne, Cologne, Germany

    Rita K Schmutzler, Kerstin Rhiem & Barbara Wappenschmidt

  199. Centre for Molecular Medicine Cologne (CMMC), University Hospital of Cologne, Cologne, Germany

    Rita K Schmutzler, Kerstin Rhiem & Barbara Wappenschmidt

  200. Department of Breast Oncology, Aichi Cancer Center Hospital, Nagoya, Japan

    Hiroji Iwata

  201. Singapore Eye Research Institute, National University of Singapore, Singapore

    M Kamran Ikram

  202. Shanghai Center for Disease Control and Prevention, Shanghai, China

    Wei Lu

  203. Division of Oncology, Wexner Medical Center, The Ohio State University, Columbus, Ohio, USA

    Charles Shapiro

  204. Roswell Park Cancer Institute, Buffalo, New York, USA

    Foluso Ademuyiwa

  205. Department of Medical Oncology, Papageorgiou Hospital, Aristotle University of Thessaloniki School of Medicine, Thessaloniki, Greece

    George Fountzilas

  206. Department of Surgery, Tri-Service General Hospital, Taipei, Taiwan

    Jyh-Cherng Yu

  207. Cancer Center, Kaohsiung Medical University Chung-Ho Memorial Hospital, Kaohsiung, Taiwan

    Ming-Feng Hou

  208. Department of Surgery, Kaohsiung Medical University Chung-Ho Memorial Hospital, Kaohsiung, Taiwan

    Ming-Feng Hou

  209. Department of Tumour Biology, Institut Curie, Paris, France

    Dominique Stoppa-Lyonnet, Bruno Buecher & Virginie Caux-Moncoutier

  210. Institut Curie, INSERM U830, Paris, France

    Dominique Stoppa-Lyonnet

  211. Université Paris Descartes, Sorbonne Paris Cité, Paris, France

    Dominique Stoppa-Lyonnet

  212. Basser Research Center, Abramson Cancer Center, The University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA

    Timothy R Rebbeck, Katherine L Nathanson & Susan M Domchek

  213. Center for Clinical Epidemiology and Biostatistics, The University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA

    Timothy R Rebbeck

  214. Gynecologic Oncology Group Statistical and Data Center, Roswell Park Cancer Institute, Buffalo, New York, USA

    Marion Piedmonte

  215. Department of Obstetrics and Gynecology, Comprehensive Cancer Center, Medical University of Vienna, Vienna, Austria

    Christian F Singer, Daphne Gschwantler Kaulich & Muy-Kheng Tea

  216. The Susanne Levy Gertner Oncogenetics Unit, Sheba Medical Center, Tel-Hashomer, Israel

    Eitan Friedman, Shani Shimon Paluch & Yael Laitman

  217. Institute of Oncology, Sheba Medical Center, Tel-Hashomer, Israel

    Eitan Friedman, Shani Shimon Paluch & Yael Laitman

  218. Department of Clinical Genetics, Odense University Hospital, Odense, Denmark

    Mads Thomassen & Torben A Kruse

  219. Clinical Genetics Service, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

    Kenneth Offit & Mark Robson

  220. Center for Genomic Medicine, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark

    Thomas V O Hansen

  221. Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, California, USA

    Susan L Neuhausen

  222. Department of Biological Sciences, Center for Translational Cancer Research, University of Delaware, Newark, Delaware, USA

    Csilla I Szabo

  223. Genetic Counseling Unit, Hereditary Cancer Program, l'Institut d'Investigació Biomèdica de Bellvitge–Catalan Institute of Oncology, Barcelona, Spain

    Ignacio Blanco

  224. Center for Cancer Genetics and Prevention, Dana-Farber Cancer Institute, Boston, Massachusetts, USA

    Judy Garber

  225. Women's College Research Institute, University of Toronto, Toronto, Ontario, Canada

    Steven A Narod

  226. Clinical Cancer Genetics, City of Hope, Duarte, California, USA

    Jeffrey N Weitzel

  227. Immunology and Molecular Oncology Unit, Istituto Oncologico Veneto (IOV), IRCCS, Padua, Italy

    Marco Montagna

  228. Department of Molecular Genetics, National Institute of Oncology, Budapest, Hungary

    Edith Olah

  229. Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, Kansas, USA

    Andrew K Godwin

  230. Molecular Diagnostics Laboratory, Institute of Radioisotopes and Radiodiagnostic Products, National Centre for Scientific Research Demokritos, Aghia Paraskevi Attikis, Athens, Greece

    Drakoulis Yannoukakos

  231. Department of Dermatology, University of Utah School of Medicine, Salt Lake City, Utah, USA

    David E Goldgar

  232. Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, Utah, USA

    David E Goldgar

  233. Molecular Oncology Laboratory, Hospital Clinico San Carlos, Madrid, Spain

    Trinidad Caldes

  234. N.N. Petrov Institute of Oncology, St. Petersburg, Russia

    Evgeny N Imyanitov

  235. Latvian Biomedical Research and Study Centre, Riga, Latvia

    Laima Tihomirova

  236. Department of Breast Medical Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas, USA

    Banu K Arun

  237. Clinical Cancer Genetics, University of Texas MD Anderson Cancer Center, Houston, Texas, USA

    Banu K Arun

  238. Victorian Breast Cancer Research Consortium Cancer Genetics Laboratory, Peter MacCallum Cancer Center, Melbourne, Victoria, Australia

    Ian Campbell

  239. Department of Human Genetics, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

    Arjen R Mensenkamp

  240. Department of Clinical Genetics, Leiden University Medical Center, Leiden, The Netherlands

    Christi J van Asperen

  241. Department of Clinical Genetics, Maastricht University Medical Center, Maastricht, The Netherlands

    Kees E P van Roozendaal

  242. Department of Clinical Genetics, VU University Medical Centre, Amsterdam, The Netherlands

    Hanne Meijers-Heijboer

  243. Department of Genetics, University of Groningen, University Medical Center, Groningen, The Netherlands

    Jan C Oosterwijk

  244. Department of Medical Genetics, University Medical Center Utrecht, Utrecht, The Netherlands

    Rob B van der Luijt

  245. Department of Clinical Genetics, Academic Medical Center, Amsterdam, The Netherlands

    Theo A Mvan Os

  246. Genetic Medicine, Manchester Academic Health Sciences Centre, Central Manchester University Hospitals NHS Foundation Trust, Manchester, UK

    D Gareth Evans

  247. Leicestershire Clinical Genetics Service, University Hospitals of Leicester NHS Trust, Leicester, UK

    Julian Barwell

  248. Oxford Regional Genetics Service, Churchill Hospital, Oxford, UK

    Lisa Walker

  249. Academic Unit of Clinical and Molecular Oncology, Trinity College Dublin and St James' Hospital, Dublin, Ireland

    M John Kennedy

  250. Laboratory Medicine at Southern General Hospital, Glasgow, UK

    Rosemarie Davidson

  251. West Midlands Regional Genetics Service, Birmingham Women's Hospital Healthcare NHS Trust, Edgbaston, Birmingham, UK

    Trevor Cole

  252. INSERM U946, Fondation Jean Dausset, Paris, France

    Brigitte Bressac-de Paillerets

  253. Service de Génétique, Institut de Cancérologie Gustave Roussy, Villejuif, France

    Brigitte Bressac-de Paillerets

  254. INSERM U1052, Centre National de Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 5286, Université Lyon 1, Centre de Recherche en Cancérologie de Lyon, Lyon, France

    Francesca Damiola, Olga M Sinilnikova & Sylvie Mazoyer

  255. Centre de Génétique, Centre Hôspitalier Universitaire Dijon, Université de Bourgogne, Dijon, France

    Laurence Faivre

  256. Centre Georges François Leclerc, Dijon, France

    Laurence Faivre

  257. Centre Antoine Lacassagne, Nice, France

    Marc Frenay

  258. Unité Mixte de Génétique Constitutionnelle des Cancers Fréquents, Hospices Civils de Lyon, Centre Léon Bérard, Lyon, France

    Olga M Sinilnikova & Sophie Giraud

  259. Département de Médecine, Consultation de Génétique, Institut de Cancérologie Gustave Roussy, Villejuif, France

    Olivier Caron

  260. Unité de Prévention et d'Epidémiologie Génétique, Centre Léon Bérard, Lyon, France

    Valérie Bonadona

  261. Université Lyon 1, CNRS UMR 5558, Lyon, France

    Valérie Bonadona

  262. Department of Molecular Medicine, Sapienza University, Rome, Italy

    Giuseppe Giannini

  263. Department of Experimental Oncology, Istituto Europeo di Oncologia, Milan, Italy

    Loris Bernard

  264. Cancer Bioimmunotherapy Unit, Centro di Riferimento Oncologico, IRCCS, Aviano, Italy

    Riccardo Dolcetti

  265. Department of Gynecology and Obstetrics, University Hospital of Schleswig-Holstein and University Kiel, Kiel, Germany

    Norbert Arnold

  266. Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany

    Christoph Engel

  267. Department of Obstetrics and Gynecology, University Medical Center, Heinrich–Heine University, Düsseldorf, Germany

    Dieter Niederacher

  268. Institute of Human Genetics, University Hospital of Schleswig-Holstein, University Kiel, Kiel, Germany

    Hansjoerg Plendl

  269. Department of Human Genetics, University of Heidelberg, Heidelberg, Germany

    Christian Sutter

  270. Department of Oncology, Lund University, Lund, Sweden

    Åke Borg

  271. Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden

    Beatrice Melin

  272. Department of Clinical Genetics, Karolinska University Hospital, Stockholm, Sweden

    Johanna Rantala

  273. Department of Clinical Genetics, University and Regional Laboratories, Lund University Hospital, Lund, Sweden

    Maria Soller

  274. Department of Medicine, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Katherine L Nathanson & Susan M Domchek

  275. Division of Gynecologic Oncology, North Shore University Health System, University of Chicago, Evanston, Illinois, USA

    Gustavo C Rodriguez

  276. Department of Obstetrics and Gynecology, Ohio State University College of Medicine, Columbus, Ohio, USA

    Ritu Salani

  277. Department of Clinical Genetics, Vejle Hospital, Vejle, Denmark

    Anne-Bine Skytte

  278. Department of Clinical Genetics, Aarhus University Hospital, Aarhus, Denmark

    Uffe Birk Jensen

  279. Department of Clinical Genetics, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark

    Anne-Marie Gerdes

  280. Department of Oncology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark

    Bent Ejlertsen

  281. Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno, Czech Republic

    Lenka Foretova

  282. Pathology Queensland, The Royal Brisbane and Women's Hospital, Herston, Brisbane, Queensland, Australia

    Sunil R Lakhani

  283. Duke Cancer Institute, Duke University Medical Center, Durham, North Carolina, USA

    Andrew Berchuck

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