. 2019 Aug 29;9(1):12524.

doi: 10.1038/s41598-019-48804-y.

Two truncating variants in FANCC and breast cancer risk

Thilo Dörk¹, Paolo Peterlongo², Arto Mannermaa^{3

4

5}, Manjeet K Bolla⁶, Qin Wang⁶, Joe Dennis⁶, Thomas Ahearn⁷, Irene L Andrulis^{8

9}, Hoda Anton-Culver¹⁰, Volker Arndt¹¹, Kristan J Aronson¹², Annelie Augustinsson¹³, Laura E Beane Freeman⁷, Matthias W Beckmann¹⁴, Alicia Beeghly-Fadiel¹⁵, Sabine Behrens¹⁶, Marina Bermisheva¹⁷, Carl Blomqvist^{18

19}, Natalia V Bogdanova^{20

21

22}, Stig E Bojesen^{23

24

25}, Hiltrud Brauch^{26

27

28}, Hermann Brenner^{11

27

29}, Barbara Burwinkel^{30

31}, Federico Canzian³², Tsun L Chan^{33

34}, Jenny Chang-Claude^{16

35}, Stephen J Chanock⁷, Ji-Yeob Choi^{36

37}, Hans Christiansen²¹, Christine L Clarke³⁸, Fergus J Couch³⁹, Kamila Czene⁴⁰, Mary B Daly⁴¹, Isabel Dos-Santos-Silva⁴², Miriam Dwek⁴³, Diana M Eccles⁴⁴, Arif B Ekici⁴⁵, Mikael Eriksson⁴⁰, D Gareth Evans^{46

47}, Peter A Fasching^{14

48}, Jonine Figueroa^{7

49

50}, Henrik Flyger⁵¹, Lin Fritschi⁵², Marike Gabrielson⁴⁰, Manuela Gago-Dominguez^{53

54}, Chi Gao^{55

56}, Susan M Gapstur⁵⁷, Montserrat García-Closas^{7

58}, José A García-Sáenz⁵⁹, Mia M Gaudet⁵⁷, Graham G Giles^{60

61

62}, Mark S Goldberg^{63

64}, David E Goldgar⁶⁵, Pascal Guénel⁶⁶, Lothar Haeberle⁶⁷, Christopher A Haiman⁶⁸, Niclas Håkansson⁶⁹, Per Hall^{40

70}, Ute Hamann⁷¹, Mikael Hartman^{72

73}, Jan Hauke^{74

75

76}, Alexander Hein¹⁴, Peter Hillemanns²⁰, Frans B L Hogervorst⁷⁷, Maartje J Hooning⁷⁸, John L Hopper⁶¹, Tony Howell⁷⁹, Dezheng Huo⁸⁰, Hidemi Ito^{81

82}, Motoki Iwasaki⁸³, Anna Jakubowska^{84

85}, Wolfgang Janni⁸⁶, Esther M John⁸⁷, Audrey Jung¹⁶, Rudolf Kaaks¹⁶, Daehee Kang^{36

37

88}, Pooja Middha Kapoor^{16

89}, Elza Khusnutdinova^{17

90}, Sung-Won Kim⁹¹, Cari M Kitahara⁹², Stella Koutros⁷, Peter Kraft^{55

56}, Vessela N Kristensen^{93

94}, Ava Kwong^{33

95

96}, Diether Lambrechts^{97

98}, Loic Le Marchand⁹⁹, Jingmei Li¹⁰⁰, Sara Lindström^{101

102}, Martha Linet⁹², Wing-Yee Lo^{26

103}, Jirong Long¹⁵, Artitaya Lophatananon¹⁰⁴, Jan Lubiński⁸⁴, Mehdi Manoochehri⁷¹, Siranoush Manoukian¹⁰⁵, Sara Margolin^{70

106}, Elena Martinez^{54

107}, Keitaro Matsuo^{81

82}, Dimitris Mavroudis¹⁰⁸, Alfons Meindl¹⁰⁹, Usha Menon¹¹⁰, Roger L Milne^{60

61

111}, Nur Aishah Mohd Taib¹¹², Kenneth Muir^{113

104}, Anna Marie Mulligan^{114

115}, Susan L Neuhausen¹¹⁶, Heli Nevanlinna¹¹⁷, Patrick Neven¹¹⁸, William G Newman^{46

47}, Kenneth Offit^{119

120}, Olufunmilayo I Olopade⁸⁰, Andrew F Olshan¹²¹, Janet E Olson¹²², Håkan Olsson¹³, Sue K Park^{36

37

88}, Tjoung-Won Park-Simon²⁰, Julian Peto⁴², Dijana Plaseska-Karanfilska¹²³, Esther Pohl-Rescigno^{74

75

76}, Nadege Presneau⁴³, Brigitte Rack⁸⁶, Paolo Radice¹²⁴, Muhammad U Rashid^{71

125}, Gad Rennert¹²⁶, Hedy S Rennert¹²⁶, Atocha Romero¹²⁷, Matthias Ruebner⁶⁷, Emmanouil Saloustros¹²⁸, Marjanka K Schmidt^{129

130}, Rita K Schmutzler^{74

75

76}, Michael O Schneider⁶⁷, Minouk J Schoemaker¹³¹, Christopher Scott¹²², Chen-Yang Shen^{132

133}, Xiao-Ou Shu¹⁵, Jacques Simard¹³⁴, Susan Slager¹²², Snezhana Smichkoska¹³⁵, Melissa C Southey^{111

136}, John J Spinelli^{137

138}, Jennifer Stone^{61

139}, Harald Surowy^{30

31}, Anthony J Swerdlow^{131

140}, Rulla M Tamimi^{55

56

141}, William J Tapper¹⁴², Soo H Teo^{112

143}, Mary Beth Terry¹⁴⁴, Amanda E Toland¹⁴⁵, Rob A E M Tollenaar¹⁴⁶, Diana Torres^{71

147}, Gabriela Torres-Mejía¹⁴⁸, Melissa A Troester¹²¹, Thérèse Truong⁶⁶, Shoichiro Tsugane¹⁴⁹, Michael Untch¹⁵⁰, Celine M Vachon¹⁵¹, Ans M W van den Ouweland¹⁵², Elke M van Veen^{46

47}, Joseph Vijai^{119

120}, Camilla Wendt¹⁰⁶, Alicja Wolk^{69

153}, Jyh-Cherng Yu¹⁵⁴, Wei Zheng¹⁵, Argyrios Ziogas¹⁰, Elad Ziv¹⁵⁵; ABCTB Investigators; NBCS Collaborators; Alison M Dunning¹⁵⁶, Paul D P Pharoah^{6

156}, Detlev Schindler¹⁵⁷, Peter Devilee^{158

159}, Douglas F Easton^{6

156}

Collaborators, Affiliations

Affiliations

¹ Gynaecology Research Unit, Hannover Medical School, Hannover, Germany. doerk.thilo@mh-hannover.de.
² Genome Diagnostics Program, IFOM - the FIRC Institute of Molecular Oncology, Milan, Italy.
³ Translational Cancer Research Area, University of Eastern Finland, Kuopio, Finland.
⁴ Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland.
⁵ Imaging Center, Department of Clinical Pathology, Kuopio University Hospital, Kuopio, Finland.
⁶ Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
⁷ Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA.
⁸ Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, ON, Canada.
⁹ Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada.
¹⁰ Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA.
¹¹ Division of Clinical Epidemiology and Aging Research, C070, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹² Department of Public Health Sciences, and Cancer Research Institute, Queen's University, Kingston, ON, Canada.
¹³ Department of Cancer Epidemiology, Clinical Sciences, Lund University, Lund, Sweden.
¹⁴ Department of Gynecology and Obstetrics, Comprehensive Cancer Center ER-EMN, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany.
¹⁵ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA.
¹⁶ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁷ Institute of Biochemistry and Genetics of the Ufa Federal Research Centre of the Russian Academy of Sciences, Ufa, Russia.
¹⁸ Department of Oncology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
¹⁹ Department of Oncology, Örebro University Hospital, Örebro, Sweden.
²⁰ Gynaecology Research Unit, Hannover Medical School, Hannover, Germany.
²¹ Department of Radiation Oncology, Hannover Medical School, Hannover, Germany.
²² N.N. Alexandrov Research Institute of Oncology and Medical Radiology, Minsk, Belarus.
²³ Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
²⁴ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
²⁵ Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
²⁶ Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany.
²⁷ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
²⁸ iFIT Cluster of Excellence, University of Tübingen, Tübingen, Germany.
²⁹ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³⁰ Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³¹ Molecular Biology of Breast Cancer, University Womens Clinic Heidelberg, University of Heidelberg, Heidelberg, Germany.
³² Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³³ Hong Kong Hereditary Breast Cancer Family Registry, Cancer Genetics Centre, Happy Valley, Hong Kong.
³⁴ Department of Pathology, Hong Kong Sanatorium and Hospital, Happy Valley, Hong Kong.
³⁵ Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
³⁶ Department of Biomedical Sciences, Seoul National University Graduate School, Seoul, Korea.
³⁷ Cancer Research Institute, Seoul National University, Seoul, Korea.
³⁸ Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales, Australia.
³⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁴⁰ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
⁴¹ Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, PA, USA.
⁴² Department of Non-Communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK.
⁴³ Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, UK.
⁴⁴ Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, UK.
⁴⁵ Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany.
⁴⁶ Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK.
⁴⁷ Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK.
⁴⁸ David Geffen School of Medicine, Department of Medicine Division of Hematology and Oncology, University of California at Los Angeles, Los Angeles, CA, USA.
⁴⁹ Usher Institute of Population Health Sciences and Informatics, The University of Edinburgh Medical School, Edinburgh, UK.
⁵⁰ Cancer Research UK Edinburgh Centre, Edinburgh, UK.
⁵¹ Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
⁵² School of Public Health, Curtin University, Perth, Western Australia, Australia.
⁵³ Genomic Medicine Group, Galician Foundation of Genomic Medicine, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.
⁵⁴ Moores Cancer Center, University of California San Diego, La Jolla, CA, USA.
⁵⁵ Program in Genetic Epidemiology and Statistical Genetics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁵⁶ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁵⁷ Behavioral and Epidemiology Research Group, American Cancer Society, Atlanta, GA, USA.
⁵⁸ Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK.
⁵⁹ Medical Oncology Department, Hospital Clínico San Carlos, Instituto de Investigación Sanitaria San Carlos (IdISSC), Centro Investigación Biomédica en Red de Cáncer (CIBERONC), Madrid, Spain.
⁶⁰ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
⁶¹ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
⁶² Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Victoria, Australia.
⁶³ Department of Medicine, McGill University, Montréal, QC, Canada.
⁶⁴ Division of Clinical Epidemiology, Royal Victoria Hospital, McGill University, Montréal, QC, Canada.
⁶⁵ Department of Dermatology, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.
⁶⁶ Cancer & Environment Group, Center for Research in Epidemiology and Population Health (CESP), INSERM, University Paris-Sud, University Paris-Saclay, Villejuif, France.
⁶⁷ Department of Gynaecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany.
⁶⁸ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁶⁹ Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁷⁰ Department of Oncology, Södersjukhuset, Stockholm, Sweden.
⁷¹ Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁷² Saw Swee Hock School of Public Health, National University of Singapore, Singapore, Singapore.
⁷³ Department of Surgery, National University Health System, Singapore, Singapore.
⁷⁴ Center for Familial Breast and Ovarian Cancer, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
⁷⁵ Center for Molecular Medicine Cologne (CMMC), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
⁷⁶ Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
⁷⁷ Family Cancer Clinic, The Netherlands Cancer Institute - Antoni van Leeuwenhoek hospital, Amsterdam, The Netherlands.
⁷⁸ Department of Medical Oncology, Family Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, The Netherlands.
⁷⁹ Division of Cancer Sciences, University of Manchester, Manchester, UK.
⁸⁰ Center for Clinical Cancer Genetics, The University of Chicago, Chicago, IL, USA.
⁸¹ Division of Cancer Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan.
⁸² Division of Cancer Epidemiology, Nagoya University Graduate School of Medicine, Nagoya, Japan.
⁸³ Division of Epidemiology, Center for Public Health Sciences, National Cancer Center, Tokyo, Japan.
⁸⁴ Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
⁸⁵ Independent Laboratory of Molecular Biology and Genetic Diagnostics, Pomeranian Medical University, Szczecin, Poland.
⁸⁶ Department of Gynaecology and Obstetrics, University Hospital Ulm, Ulm, Germany.
⁸⁷ Department of Medicine, Division of Oncology, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
⁸⁸ Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Korea.
⁸⁹ Faculty of Medicine, University of Heidelberg, Heidelberg, Germany.
⁹⁰ Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia.
⁹¹ Department of Surgery, Daerim Saint Mary's Hospital, Seoul, Korea.
⁹² Radiation Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA.
⁹³ Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital-Radiumhospitalet, Oslo, Norway.
⁹⁴ Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway.
⁹⁵ Department of Surgery, The University of Hong Kong, Pok Fu Lam, Hong Kong.
⁹⁶ Department of Surgery, Hong Kong Sanatorium and Hospital, Happy Valley, Hong Kong.
⁹⁷ VIB Center for Cancer Biology, VIB, Leuven, Belgium.
⁹⁸ Laboratory for Translational Genetics, Department of Human Genetics, University of Leuven, Leuven, Belgium.
⁹⁹ Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
¹⁰⁰ Human Genetics Division, Genome Institute of Singapore, Singapore, Singapore.
¹⁰¹ Department of Epidemiology, University of Washington School of Public Health, Seattle, WA, USA.
¹⁰² Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
¹⁰³ University of Tübingen, Tübingen, Germany.
¹⁰⁴ 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, UK.
¹⁰⁵ Unit of Medical Genetics, Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy.
¹⁰⁶ Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden.
¹⁰⁷ Department of Family Medicine and Public Health, University of California San Diego, La Jolla, CA, USA.
¹⁰⁸ Department of Medical Oncology, University Hospital of Heraklion, Heraklion, Greece.
¹⁰⁹ Department of Gynecology and Obstetrics, Ludwig Maximilian University of Munich, Munich, Germany.
¹¹⁰ MRC Clinical Trials Unit at UCL, Institute of Clinical Trials & Methodology, University College London, London, UK.
¹¹¹ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.
¹¹² Breast Cancer Research Unit, UM Cancer Research Institute, University of Malaya Medical Centre, Kuala Lumpur, Malaysia.
¹¹³ Division of Health Sciences, Warwick Medical School, University of Warwick, Coventry, UK.
¹¹⁴ Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada.
¹¹⁵ Laboratory Medicine Program, University Health Network, Toronto, ON, Canada.
¹¹⁶ Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, CA, USA.
¹¹⁷ Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
¹¹⁸ Leuven Multidisciplinary Breast Center, Department of Oncology, Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium.
¹¹⁹ Clinical Genetics Research Lab, Department of Cancer Biology and Genetics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹²⁰ Clinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹²¹ Department of Epidemiology, Gillings School of Global Public Health and UNC Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
¹²² Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
¹²³ Research Centre for Genetic Engineering and Biotechnology 'Georgi D. Efremov', Macedonian Academy of Sciences and Arts, Skopje, Republic of Macedonia.
¹²⁴ Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, Fondazione IRCCS Istituto Nazionale dei Tumori (INT), Milan, Italy.
¹²⁵ Department of Basic Sciences, Shaukat Khanum Memorial Cancer Hospital and Research Centre (SKMCH & RC), Lahore, Pakistan.
¹²⁶ Clalit National Cancer Control Center, Carmel Medical Center and Technion Faculty of Medicine, Haifa, Israel.
¹²⁷ Medical Oncology Department, Hospital Universitario Puerta de Hierro, Madrid, Spain.
¹²⁸ Department of Oncology, University Hospital of Larissa, Larissa, Greece.
¹²⁹ Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
¹³⁰ Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek hospital, Amsterdam, The Netherlands.
¹³¹ Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.
¹³² Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.
¹³³ School of Public Health, China Medical University, Taichung, Taiwan.
¹³⁴ Genomics Center, Centre Hospitalier Universitaire de Québec - Université Laval Research Center, Québec City, QC, Canada.
¹³⁵ Ss. Cyril and Methodius University in Skopje, Medical Faculty, University Clinic of Radiotherapy and Oncology, Skopje, Republic of Macedonia.
¹³⁶ Department of Clinical Pathology, The University of Melbourne, Melbourne, Victoria, Australia.
¹³⁷ Population Oncology, BC Cancer, Vancouver, BC, Canada.
¹³⁸ School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada.
¹³⁹ The Curtin UWA Centre for Genetic Origins of Health and Disease, Curtin University and University of Western Australia, Perth, Western Australia, Australia.
¹⁴⁰ Division of Breast Cancer Research, The Institute of Cancer Research, London, UK.
¹⁴¹ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
¹⁴² Faculty of Medicine, University of Southampton, Southampton, UK.
¹⁴³ Cancer Research Malaysia, Subang Jaya, Selangor, Malaysia.
¹⁴⁴ Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA.
¹⁴⁵ Department of Cancer Biology and Genetics, The Ohio State University, Columbus, OH, USA.
¹⁴⁶ Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands.
¹⁴⁷ Institute of Human Genetics, Pontificia Universidad Javeriana, Bogota, Colombia.
¹⁴⁸ Center for Population Health Research, National Institute of Public Health, Mexico, Mexico.
¹⁴⁹ Center for Public Health Sciences, National Cancer Center, Tokyo, Japan.
¹⁵⁰ Department of Gynecology and Obstetrics, Helios Clinics Berlin-Buch, Berlin, Germany.
¹⁵¹ Department of Health Science Research, Division of Epidemiology, Mayo Clinic, Rochester, MN, USA.
¹⁵² Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, The Netherlands.
¹⁵³ Department of Surgical Sciences, Uppsala University, Uppsala, Sweden.
¹⁵⁴ Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan.
¹⁵⁵ Department of Medicine, Institute for Human Genetics, UCSF Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA.
¹⁵⁶ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
¹⁵⁷ Institute of Human Genetics, Biocenter, University of Würzburg, Würzburg, Germany.
¹⁵⁸ Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands.
¹⁵⁹ Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.

PMID: 31467304
PMCID: PMC6715680
DOI: 10.1038/s41598-019-48804-y

Two truncating variants in FANCC and breast cancer risk

Thilo Dörk et al. Sci Rep. 2019.

. 2019 Aug 29;9(1):12524.

doi: 10.1038/s41598-019-48804-y.

Authors

Affiliations

¹ Gynaecology Research Unit, Hannover Medical School, Hannover, Germany. doerk.thilo@mh-hannover.de.
² Genome Diagnostics Program, IFOM - the FIRC Institute of Molecular Oncology, Milan, Italy.
³ Translational Cancer Research Area, University of Eastern Finland, Kuopio, Finland.
⁴ Institute of Clinical Medicine, Pathology and Forensic Medicine, University of Eastern Finland, Kuopio, Finland.
⁵ Imaging Center, Department of Clinical Pathology, Kuopio University Hospital, Kuopio, Finland.
⁶ Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
⁷ Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA.
⁸ Fred A. Litwin Center for Cancer Genetics, Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital, Toronto, ON, Canada.
⁹ Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada.
¹⁰ Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, CA, USA.
¹¹ Division of Clinical Epidemiology and Aging Research, C070, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹² Department of Public Health Sciences, and Cancer Research Institute, Queen's University, Kingston, ON, Canada.
¹³ Department of Cancer Epidemiology, Clinical Sciences, Lund University, Lund, Sweden.
¹⁴ Department of Gynecology and Obstetrics, Comprehensive Cancer Center ER-EMN, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany.
¹⁵ Division of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University School of Medicine, Nashville, TN, USA.
¹⁶ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
¹⁷ Institute of Biochemistry and Genetics of the Ufa Federal Research Centre of the Russian Academy of Sciences, Ufa, Russia.
¹⁸ Department of Oncology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
¹⁹ Department of Oncology, Örebro University Hospital, Örebro, Sweden.
²⁰ Gynaecology Research Unit, Hannover Medical School, Hannover, Germany.
²¹ Department of Radiation Oncology, Hannover Medical School, Hannover, Germany.
²² N.N. Alexandrov Research Institute of Oncology and Medical Radiology, Minsk, Belarus.
²³ Copenhagen General Population Study, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
²⁴ Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
²⁵ Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
²⁶ Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany.
²⁷ German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
²⁸ iFIT Cluster of Excellence, University of Tübingen, Tübingen, Germany.
²⁹ Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
³⁰ Molecular Epidemiology Group, C080, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³¹ Molecular Biology of Breast Cancer, University Womens Clinic Heidelberg, University of Heidelberg, Heidelberg, Germany.
³² Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
³³ Hong Kong Hereditary Breast Cancer Family Registry, Cancer Genetics Centre, Happy Valley, Hong Kong.
³⁴ Department of Pathology, Hong Kong Sanatorium and Hospital, Happy Valley, Hong Kong.
³⁵ Cancer Epidemiology Group, University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
³⁶ Department of Biomedical Sciences, Seoul National University Graduate School, Seoul, Korea.
³⁷ Cancer Research Institute, Seoul National University, Seoul, Korea.
³⁸ Westmead Institute for Medical Research, University of Sydney, Sydney, New South Wales, Australia.
³⁹ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁴⁰ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
⁴¹ Department of Clinical Genetics, Fox Chase Cancer Center, Philadelphia, PA, USA.
⁴² Department of Non-Communicable Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK.
⁴³ Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, UK.
⁴⁴ Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, UK.
⁴⁵ Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany.
⁴⁶ Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK.
⁴⁷ Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK.
⁴⁸ David Geffen School of Medicine, Department of Medicine Division of Hematology and Oncology, University of California at Los Angeles, Los Angeles, CA, USA.
⁴⁹ Usher Institute of Population Health Sciences and Informatics, The University of Edinburgh Medical School, Edinburgh, UK.
⁵⁰ Cancer Research UK Edinburgh Centre, Edinburgh, UK.
⁵¹ Department of Breast Surgery, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark.
⁵² School of Public Health, Curtin University, Perth, Western Australia, Australia.
⁵³ Genomic Medicine Group, Galician Foundation of Genomic Medicine, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago, SERGAS, Santiago de Compostela, Spain.
⁵⁴ Moores Cancer Center, University of California San Diego, La Jolla, CA, USA.
⁵⁵ Program in Genetic Epidemiology and Statistical Genetics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁵⁶ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁵⁷ Behavioral and Epidemiology Research Group, American Cancer Society, Atlanta, GA, USA.
⁵⁸ Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK.
⁵⁹ Medical Oncology Department, Hospital Clínico San Carlos, Instituto de Investigación Sanitaria San Carlos (IdISSC), Centro Investigación Biomédica en Red de Cáncer (CIBERONC), Madrid, Spain.
⁶⁰ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
⁶¹ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
⁶² Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Victoria, Australia.
⁶³ Department of Medicine, McGill University, Montréal, QC, Canada.
⁶⁴ Division of Clinical Epidemiology, Royal Victoria Hospital, McGill University, Montréal, QC, Canada.
⁶⁵ Department of Dermatology, Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.
⁶⁶ Cancer & Environment Group, Center for Research in Epidemiology and Population Health (CESP), INSERM, University Paris-Sud, University Paris-Saclay, Villejuif, France.
⁶⁷ Department of Gynaecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Comprehensive Cancer Center Erlangen-EMN, Erlangen, Germany.
⁶⁸ Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁶⁹ Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
⁷⁰ Department of Oncology, Södersjukhuset, Stockholm, Sweden.
⁷¹ Molecular Genetics of Breast Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁷² Saw Swee Hock School of Public Health, National University of Singapore, Singapore, Singapore.
⁷³ Department of Surgery, National University Health System, Singapore, Singapore.
⁷⁴ Center for Familial Breast and Ovarian Cancer, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
⁷⁵ Center for Molecular Medicine Cologne (CMMC), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
⁷⁶ Center for Integrated Oncology (CIO), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
⁷⁷ Family Cancer Clinic, The Netherlands Cancer Institute - Antoni van Leeuwenhoek hospital, Amsterdam, The Netherlands.
⁷⁸ Department of Medical Oncology, Family Cancer Clinic, Erasmus MC Cancer Institute, Rotterdam, The Netherlands.
⁷⁹ Division of Cancer Sciences, University of Manchester, Manchester, UK.
⁸⁰ Center for Clinical Cancer Genetics, The University of Chicago, Chicago, IL, USA.
⁸¹ Division of Cancer Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan.
⁸² Division of Cancer Epidemiology, Nagoya University Graduate School of Medicine, Nagoya, Japan.
⁸³ Division of Epidemiology, Center for Public Health Sciences, National Cancer Center, Tokyo, Japan.
⁸⁴ Department of Genetics and Pathology, Pomeranian Medical University, Szczecin, Poland.
⁸⁵ Independent Laboratory of Molecular Biology and Genetic Diagnostics, Pomeranian Medical University, Szczecin, Poland.
⁸⁶ Department of Gynaecology and Obstetrics, University Hospital Ulm, Ulm, Germany.
⁸⁷ Department of Medicine, Division of Oncology, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA, USA.
⁸⁸ Department of Preventive Medicine, Seoul National University College of Medicine, Seoul, Korea.
⁸⁹ Faculty of Medicine, University of Heidelberg, Heidelberg, Germany.
⁹⁰ Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia.
⁹¹ Department of Surgery, Daerim Saint Mary's Hospital, Seoul, Korea.
⁹² Radiation Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA.
⁹³ Department of Cancer Genetics, Institute for Cancer Research, Oslo University Hospital-Radiumhospitalet, Oslo, Norway.
⁹⁴ Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway.
⁹⁵ Department of Surgery, The University of Hong Kong, Pok Fu Lam, Hong Kong.
⁹⁶ Department of Surgery, Hong Kong Sanatorium and Hospital, Happy Valley, Hong Kong.
⁹⁷ VIB Center for Cancer Biology, VIB, Leuven, Belgium.
⁹⁸ Laboratory for Translational Genetics, Department of Human Genetics, University of Leuven, Leuven, Belgium.
⁹⁹ Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
¹⁰⁰ Human Genetics Division, Genome Institute of Singapore, Singapore, Singapore.
¹⁰¹ Department of Epidemiology, University of Washington School of Public Health, Seattle, WA, USA.
¹⁰² Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
¹⁰³ University of Tübingen, Tübingen, Germany.
¹⁰⁴ 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, UK.
¹⁰⁵ Unit of Medical Genetics, Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy.
¹⁰⁶ Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden.
¹⁰⁷ Department of Family Medicine and Public Health, University of California San Diego, La Jolla, CA, USA.
¹⁰⁸ Department of Medical Oncology, University Hospital of Heraklion, Heraklion, Greece.
¹⁰⁹ Department of Gynecology and Obstetrics, Ludwig Maximilian University of Munich, Munich, Germany.
¹¹⁰ MRC Clinical Trials Unit at UCL, Institute of Clinical Trials & Methodology, University College London, London, UK.
¹¹¹ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.
¹¹² Breast Cancer Research Unit, UM Cancer Research Institute, University of Malaya Medical Centre, Kuala Lumpur, Malaysia.
¹¹³ Division of Health Sciences, Warwick Medical School, University of Warwick, Coventry, UK.
¹¹⁴ Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada.
¹¹⁵ Laboratory Medicine Program, University Health Network, Toronto, ON, Canada.
¹¹⁶ Department of Population Sciences, Beckman Research Institute of City of Hope, Duarte, CA, USA.
¹¹⁷ Department of Obstetrics and Gynecology, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.
¹¹⁸ Leuven Multidisciplinary Breast Center, Department of Oncology, Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium.
¹¹⁹ Clinical Genetics Research Lab, Department of Cancer Biology and Genetics, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹²⁰ Clinical Genetics Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY, USA.
¹²¹ Department of Epidemiology, Gillings School of Global Public Health and UNC Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
¹²² Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
¹²³ Research Centre for Genetic Engineering and Biotechnology 'Georgi D. Efremov', Macedonian Academy of Sciences and Arts, Skopje, Republic of Macedonia.
¹²⁴ Unit of Molecular Bases of Genetic Risk and Genetic Testing, Department of Research, Fondazione IRCCS Istituto Nazionale dei Tumori (INT), Milan, Italy.
¹²⁵ Department of Basic Sciences, Shaukat Khanum Memorial Cancer Hospital and Research Centre (SKMCH & RC), Lahore, Pakistan.
¹²⁶ Clalit National Cancer Control Center, Carmel Medical Center and Technion Faculty of Medicine, Haifa, Israel.
¹²⁷ Medical Oncology Department, Hospital Universitario Puerta de Hierro, Madrid, Spain.
¹²⁸ Department of Oncology, University Hospital of Larissa, Larissa, Greece.
¹²⁹ Division of Molecular Pathology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.
¹³⁰ Division of Psychosocial Research and Epidemiology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek hospital, Amsterdam, The Netherlands.
¹³¹ Division of Genetics and Epidemiology, The Institute of Cancer Research, London, UK.
¹³² Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.
¹³³ School of Public Health, China Medical University, Taichung, Taiwan.
¹³⁴ Genomics Center, Centre Hospitalier Universitaire de Québec - Université Laval Research Center, Québec City, QC, Canada.
¹³⁵ Ss. Cyril and Methodius University in Skopje, Medical Faculty, University Clinic of Radiotherapy and Oncology, Skopje, Republic of Macedonia.
¹³⁶ Department of Clinical Pathology, The University of Melbourne, Melbourne, Victoria, Australia.
¹³⁷ Population Oncology, BC Cancer, Vancouver, BC, Canada.
¹³⁸ School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada.
¹³⁹ The Curtin UWA Centre for Genetic Origins of Health and Disease, Curtin University and University of Western Australia, Perth, Western Australia, Australia.
¹⁴⁰ Division of Breast Cancer Research, The Institute of Cancer Research, London, UK.
¹⁴¹ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
¹⁴² Faculty of Medicine, University of Southampton, Southampton, UK.
¹⁴³ Cancer Research Malaysia, Subang Jaya, Selangor, Malaysia.
¹⁴⁴ Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA.
¹⁴⁵ Department of Cancer Biology and Genetics, The Ohio State University, Columbus, OH, USA.
¹⁴⁶ Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands.
¹⁴⁷ Institute of Human Genetics, Pontificia Universidad Javeriana, Bogota, Colombia.
¹⁴⁸ Center for Population Health Research, National Institute of Public Health, Mexico, Mexico.
¹⁴⁹ Center for Public Health Sciences, National Cancer Center, Tokyo, Japan.
¹⁵⁰ Department of Gynecology and Obstetrics, Helios Clinics Berlin-Buch, Berlin, Germany.
¹⁵¹ Department of Health Science Research, Division of Epidemiology, Mayo Clinic, Rochester, MN, USA.
¹⁵² Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, The Netherlands.
¹⁵³ Department of Surgical Sciences, Uppsala University, Uppsala, Sweden.
¹⁵⁴ Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan.
¹⁵⁵ Department of Medicine, Institute for Human Genetics, UCSF Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, CA, USA.
¹⁵⁶ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
¹⁵⁷ Institute of Human Genetics, Biocenter, University of Würzburg, Würzburg, Germany.
¹⁵⁸ Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands.
¹⁵⁹ Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.

PMID: 31467304
PMCID: PMC6715680
DOI: 10.1038/s41598-019-48804-y

Abstract

Fanconi anemia (FA) is a genetically heterogeneous disorder with 22 disease-causing genes reported to date. In some FA genes, monoallelic mutations have been found to be associated with breast cancer risk, while the risk associations of others remain unknown. The gene for FA type C, FANCC, has been proposed as a breast cancer susceptibility gene based on epidemiological and sequencing studies. We used the Oncoarray project to genotype two truncating FANCC variants (p.R185X and p.R548X) in 64,760 breast cancer cases and 49,793 controls of European descent. FANCC mutations were observed in 25 cases (14 with p.R185X, 11 with p.R548X) and 26 controls (18 with p.R185X, 8 with p.R548X). There was no evidence of an association with the risk of breast cancer, neither overall (odds ratio 0.77, 95%CI 0.44-1.33, p = 0.4) nor by histology, hormone receptor status, age or family history. We conclude that the breast cancer risk association of these two FANCC variants, if any, is much smaller than for BRCA1, BRCA2 or PALB2 mutations. If this applies to all truncating variants in FANCC it would suggest there are differences between FA genes in their roles on breast cancer risk and demonstrates the merit of large consortia for clarifying risk associations of rare variants.

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Conflict of interest statement

The authors declare no competing interests.

References

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Two truncating variants in FANCC and breast cancer risk

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Two truncating variants in FANCC and breast cancer risk

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Abstract

Conflict of interest statement

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