The FANCM :p.Arg658* truncating variant is associated with risk of triple-negative breast cancer
Figlioli, Gisella ![ORCID Identifier](/img/uab/orcid.ico)
(The FIRC Institute for Molecular Oncology)
Bogliolo, Massimo ![ORCID Identifier](/img/uab/orcid.ico)
(Institut d'Investigació Biomèdica Sant Pau)
Catucci, Irene (The FIRC Institute for Molecular Oncology)
Caleca, Laura ![ORCID Identifier](/img/uab/orcid.ico)
(Istituto Nazionale dei Tumori, Department of Research)
Viz Lasheras, Sandra ![ORCID Identifier](/img/uab/orcid.ico)
(Universitat Autònoma de Barcelona. Departament de Genètica i de Microbiologia)
Pujol, Roser ![ORCID Identifier](/img/uab/orcid.ico)
(Institut d'Investigació Biomèdica Sant Pau)
Kiiski, Johanna I. (University of Helsinki, Department of Obstetrics and Gynecology)
Muranen, Taru A.
(University of Helsinki, Department of Obstetrics and Gynecology)
Barnes, Daniel R. (University of Cambridge, Department of Public Health and Primary Care)
Dennis, Joe
(University of Cambridge, Department of Public Health and Primary Care)
Michailidou, Kyriaki (The Cyprus Institute of Neurology & Genetics, Department of Electron Microscopy)
Bolla, Manjeet K. (University of Cambridge, Department of Public Health and Primary Care)
Leslie, Goska (University of Cambridge, Department of Public Health and Primary Care)
Aalfs, Cora M. (Amsterdam UMC, Department of Clinical Genetics)
Adank, Muriel A. (The Netherlands Cancer Institute (Amsterdam, Països Baixos))
Adlard, Julian
(Chapel Allerton Hospital)
Agata, Simona (Veneto Institute of Oncology (Pàdua, Itàlia))
Cadoo, Karen (Memorial Sloan Kettering Cancer Center)
Agnarsson, Bjarni A. (University of Iceland, School of Medicine)
Ahearn, Thomas (National Cancer Institute)
Aittomäki, Kristiina (University of Helsinki, Department of Clinical Genetics)
Ambrosone, Christine B. (Roswell Park Cancer Institute)
Andrews, Lesley (Nelune Comprehensive Cancer Care Centre)
Anton-Culver, Hoda (University of California Irvine, Department of Epidemiology)
Antonenkova, Natalia N. (N.N. Alexandrov Research Institute of Oncology and Medical Radiology)
Arndt, Volker
(German Cancer Research Center)
Arnold, Norbert (University Hospital of Schleswig-Holstein, Department of Gynaecology and Obstetrics)
Aronson, Kristan J. (Queen's University, Department of Public Health Sciences)
Arun, Banu K. (University of Texas, Department of Breast Medical Oncology)
Asseryanis, Ella (Medical University of Vienna, Dept of OB/GYN and Comprehensive Cancer Center)
Auber, Bernd
(Institute of Human Genetics)
Auvinen, Päivi (University of Eastern Finland, Translational Cancer Research Area)
Azzollini, Jacopo (Fondazione Istituto Nazionale dei Tumori di Milano, Department of Medical Oncology and Hematology)
Balmaña Gelpí, Judith
(Hospital Universitari Vall d'Hebron)
Barkardottir, Rosa B. (University of Iceland)
Barrowdale, Daniel (University of Cambridge, Department of Public Health and Primary Care)
Barwell, Julian (Leicester General Hospital (Leicester, Regne Unit))
Beane-Freeman, Laura (National Cancer Institute)
Beauparlant, Charles Joly (Centre Hospitalier Universitaire de Québec - Université Laval)
Beckmann, Matthias W. (Friedrich-Alexander-University Erlangen-Nuremberg, Department of Gynecology and Obstetrics)
Behrens, Sabine (German Cancer Research Center)
Benitez, Javier
(Centro Nacional de Investigaciones Oncológicas)
Berger, Raanan (Chaim Sheba Medical Center. The Institute of Oncology)
Bermisheva, Marina (Institute of Biochemistry and Genetics)
Blanco, Amie M. (University of California San Francisco)
Blomqvist, Carl (Örebro University Hospital, Department of Oncology)
Bogdanova, Natalia V. (Hannover Medical School)
Bojesen, Anders (Aarhus University Hospital (Aarhus, Dinamarca))
Bojesen, Stig E. (University of Copenhagen)
Bonanni, Bernardo
(IEO, European Institute of Oncology)
Borg, Åke (Skåne University Hospital (Suècia))
Brady, Angela F. (London North West University Hospitals)
Brauch, Hiltrud
(German Cancer Research Center)
Brenner, Hermann (German Cancer Research Center)
Brüning, Thomas (Institute of the Ruhr University Bochum)
Burwinkel, Barbara (University of Heidelberg)
Buys, Saundra
(Huntsman Cancer Institute, Department of Medicine)
Caldes, Trinidad (Instituto de Investigación Sanitaria del Hospital Clínico San Carlos)
Caliebe, Almuth (Universitätsklinikum Schleswig-Holstein (Alemanya))
Caligo, Maria
(University Hospital of Pisa (Pisa, Itàlia))
Campa, Daniele
(University of Pisa, Department of Biology)
Campbell, Ian (The University of Melbourne, Department of Oncology)
Canzian, Federico
(German Cancer Research Center)
Castelao, Jose E. (Instituto de Investigación Sanitaria Galicia Sur)
Chang-Claude, Jenny (University Medical Center Hamburg-Eppendorf)
Chanock, Stephen J. (National Cancer Institute)
Claes, Kathleen
(Ghent University, Centre for Medical Genetics)
Clarke, Christine L. (University of Sydney, Westmead Institute for Medical Research)
Collavoli, Anita (University Hospital of Pisa (Pisa, Itàlia))
Conner, Thomas A. (Huntsman Cancer Institute (Salt Lake City, Estats Units d'Amèrica))
Cox, David G. (Cancer Research Center of Lyon)
Cybulski, Cezary (Pomeranian Medical University, Department of Genetics and Pathology)
Czene, Kamila (Karolinska Institutet (Estocolm, Suècia). Department of Medical Epidemiology and Biostatistics)
Daly, Mary B. (Fox Chase Cancer Center, Department of Clinical Genetics)
De la Hoya, Miguel (Instituto de Investigación Sanitaria del Hospital Clínico San Carlos)
Devilee, Peter
(Leiden University Medical Center, Department of Human Genetics)
Diez, Orland
(Hospital Universitari Vall d'Hebron)
Ding, Yuan Chun (Beckman Research Institute of City of Hope (Duarte, Estats Units d'Amèrica). Department of Population Sciences)
Dite, Gillian S. (The University of Melbourne)
Ditsch, Nina (Ludwig Maximilian University of Munich, Department of Gynecology and Obstetrics)
Domchek, Susan M.
(Perelman School of Medicine at the University of Pennsylvania, Department of Medicine)
Dorfling, Cecilia M. (University of Pretoria, Department of Genetics)
dos-Santos-Silva, Isabel (London School of Hygiene and Tropical Medicine, Department of Non-Communicable Disease Epidemiology)
Durda, Katarzyna (Pomeranian Medical University, Department of Genetics and Pathology)
Dwek, Miriam (University of Westminster, Department of Biomedical Sciences)
Eccles, Diana M.
(University of Southampton, Cancer Sciences Academic Unit)
Ekici, Arif B. (Friedrich-Alexander University Erlangen-Nuremberg)
Eliassen, A. Heather (Harvard T.H. Chan School of Public Health, Department of Epidemiology)
Ellberg, Carolina (Lund University, Department of Cancer Epidemiology)
Eriksson, Mikael (Karolinska Institutet (Estocolm, Suècia). Department of Medical Epidemiology and Biostatistics)
Evans, Gareth
(Manchester University NHS Foundation Trust)
Fasching, Peter A. (University of California at Los Angeles, Department of Medicine Division of Hematology and Oncology)
Figueroa, Jonine (Cancer Research UK Edinburgh Centre)
Flyger, Henrik (Copenhagen University Hospital)
Foulkes, William D.
(McGill University, Departments of Human Genetics and Oncology)
Friebel, Tara M. (Dana-Farber Cancer Institute (Boston, Estats Units d'Amèrica))
Friedman, Eitan (Tel Aviv University)
Gabrielson, Marike (Karolinska Institutet (Estocolm, Suècia). Department of Medical Epidemiology and Biostatistics)
Gaddam, Pragna (Memorial Sloan-Kettering Cancer Center (Nova York, Estats Units d'Amèrica))
Gago-Dominguez, Manuela (University of California San Diego)
Gao, Chi (Harvard T.H. Chan School of Public Health (Boston, Estats Units d'Amèrica))
Gapstur, Susan M. (American Cancer Society)
Garber, Judy (Dana-Farber Cancer Institute (Boston, Estats Units d'Amèrica))
García-Closas, Montserrat (National Cancer Institute)
García-Sáenz, José A. (Instituto de Investigación Sanitaria del Hospital Clínico San Carlos)
Gaudet, Mia M. (American Cancer Society)
Gayther, Simon A. (Cedars Sinai Heart Institute (Los Angeles, Estats Units d'Amèrica))
Giles, Graham G. (Monash University, Department of Epidemiology and Preventive Medicine)
Glendon, Gord (Lunenfeld-Tanenbaum Research Institute of Mount Sinai Hospital)
Godwin, Andrew K. (Kansas University Medical Center, Department of Pathology and Laboratory Medicine)
Goldberg, Mark S. (McGill University)
Goldgar, David E. (University of Utah School of Medicine, Department of Dermatology)
Guénel, Pascal (University Paris-Sud, University Paris-Saclay)
Gutierrez-Barrera, Angelica M. (University of Texas, Department of Breast Medical Oncology and Clinical Genetics Program)
Haeberle, Lothar (University Hospital Erlangen (Alemanya))
Haiman, Christopher A. (University of Southern California, Department of Preventive Medicine)
Håkansson, Niclas (Karolinska Institutet, Institute of Environmental Medicine)
Hall, Per (Södersjukhuset, Department of Oncology)
Hamann, Ute (German Cancer Research Center)
Harrington, Patricia A. (University of Cambridge, Department of Oncology)
Hein, Alexander (University Hospital Erlangen (Alemanya))
Heyworth, Jane (The University of Western Australia)
Hillemanns, Peter (Hannover Medical School, Gynaecology Research Unit)
Hollestelle, Antoinette (Erasmus MC Cancer Institute)
Hopper, John L. (The University of Melbourne)
Hosgood, H. Dean (Albert Einstein College of Medicine)
Howell, Anthony (University of Manchester, Division of Cancer Sciences)
Hu, Chunling (Mayo Clinic, Department of Laboratory Medicine and Pathology)
Hulick, Peter J. (The University of Chicago Pritzker School of Medicine)
Hunter, David J. (University of Oxford)
Imyanitov, Evgeny N. (N.N. Petrov Institute of Oncology)
Isaacs, Claudine
(Georgetown University)
Jakimovska, Milena
(Macedonian Academy of Sciences and Arts)
Jakubowska, Anna (Pomeranian Medical University)
James, Paul (Peter MacCallum Cancer Center)
Janavicius, Ramunas (State Research Institute Innovative Medicine Center)
Janni, Wolfgang (University Hospital of Ulm (Alemanya))
John, Esther M. (Stanford University School of Medicine, Department of Medicine)
Jones, Michael E. (The Institute of Cancer Research)
Jung, Audrey (German Cancer Research Center)
Kaaks, Rudolf (German Cancer Research Center)
Karlan, Beth Y. (Cedars Sinai Heart Institute (Los Angeles, Estats Units d'Amèrica))
Khusnutdinova, Elza (Bashkir State Medical University, Department of Medical Genetics)
Kitahara, Cari M. (National Cancer Institute)
Konstantopoulou, Irene
(National Centre for Scientific Research 'Demokritos')
Koutros, Stella (National Cancer Institute)
Kraft, Peter (Harvard T.H. Chan School of Public Health (Boston, Estats Units d'Amèrica))
Lambrechts, Diether (University of Leuven, Department of Human Genetics)
Lazaro, Conxi (Institut d'Investigació Biomèdica de Bellvitge)
Le Marchand, Loic (University of Hawaii Cancer Center, Epidemiology Program)
Lester, Jenny (Cedars Sinai Heart Institute (Los Angeles, Estats Units d'Amèrica))
Lesueur, Fabienne
(Mines ParisTech)
Lilyquist, Jenna (Mayo Clinic, Department of Health Sciences Research)
Loud, Jennifer T. (National Cancer Institute, Clinical Genetics Branch, Division of Cancer Epidemiology and Genetics)
Lu, Karen H. (University of Texas MD Anderson Cancer Center, Department of Gynecologic Oncology)
Luben, Robert N. (University of Cambridge, Department of Public Health and Primary Care)
Lubinski, Jan
(Pomeranian Medical University, Department of Genetics and Pathology)
Mannermaa, Arto (Kuopio University Hospital ( Finlàndia))
Manoochehri, Mehdi (German Cancer Research Center)
Manoukian, Siranoush (Istituto Nazionale dei Tumori di Milano)
Margolin, Sara (Karolinska Institutet, Department of Clinical Science and Education)
Martens, John W. M. (Erasmus MC Cancer Institute)
Maurer, Tabea (University Medical Center Hamburg-Eppendorf)
Mavroudis, Dimitrios (University Hospital of Heraklion, Department of Medical Oncology)
Mebirouk, Noura (Mines ParisTech)
Meindl, Alfons (Ludwig Maximilian University of Munich, Department of Gynecology and Obstetrics)
Menon, Usha
(University College London)
Miller, Austin
(Roswell Park Cancer Institute)
Montagna, Marco (Veneto Institute of Oncology (Pàdua, Itàlia))
Nathanson, Katherine L.
(University of Pennsylvania, Department of Medicine)
Neuhausen, Susan L. (Beckman Research Institute of City of Hope (Duarte, Estats Units d'Amèrica). Department of Population Sciences)
Newman, William G. (Manchester University NHS Foundation Trust)
Nguyen-Dumont, Tu (The University of Melbourne, Department of Clinical Pathology)
Nielsen, Finn Cilius (Copenhagen University Hospital)
Nielsen, Sarah (The University of Chicago, Center for Clinical Cancer Genetics)
Nikitina-Zake, Liene (Latvian Biomedical Research and Study Centre)
Offit, Kenneth (Memorial Sloan-Kettering Cancer Center, Clinical Genetics Service, Department of Medicine)
Olah, Edith (National Institute of Oncology, Department of Molecular Genetics)
Olopade, Olufunmilayo I. (The University of Chicago)
Olshan, Andrew F. (University of North Carolina at Chapel Hill, Department of Epidemiology)
Olson, Janet E. (Mayo Clinic, Department of Health Sciences Research)
Olsson, Håkan (Lund University, Department of Cancer Epidemiology, Clinical Sciences)
Osorio, Ana
(Spanish Network on Rare Diseases)
Ottini, Laura (University La Sapienza, Department of Molecular Medicine)
Peissel, Bernard (Istituto Nazionale dei Tumori di Milano)
Peixoto, Ana (Portuguese Oncology Institute, Department of Genetics)
Peto, Julian
(London School of Hygiene and Tropical Medicine, Department of Non-Communicable Disease Epidemiology)
Plaseska-Karanfilska, Dijana (Macedonian Academy of Sciences and Arts)
Pocza, Timea (National Institute of Oncology, Department of Molecular Genetics)
Presneau, Nadege (University of Westminster, Department of Biomedical Sciences)
Pujana, Miquel Angel (Institut d'Investigació Biomèdica de Bellvitge)
Punie, Kevin
(University Hospitals Leuven (Bèlgica))
Rack, Brigitte (University Hospital of Ulm (Alemanya))
Rantala, Johanna (Karolinska Institutet, Clinical Genetics)
Rashid, Muhammad U. (Shaukat Khanum Memorial Cancer Hospital and Research Centre, Department of Basic Sciences)
Rau-Murthy, Rohini (Memorial Sloan-Kettering Cancer Center, Department of Medicine)
Rennert, Gad
(Clalit National Cancer Control Center)
Lejbkowicz, Flavio (Clalit National Cancer Control Center)
Rhenius, Valerie (University of Cambridge. Centre for Cancer Genetic Epidemiology)
Romero, Atocha
(Hospital Universitario Puerta de Hierro Majadahonda (Madrid))
Rookus, Matti A. (The Netherlands Cancer Institute, Department of Epidemiology)
Ross, Eric A. (Fox Chase Cancer Center)
Rossing, Maria (Copenhagen University Hospital)
Rudaitis, Vilius (Vilnius University, Institute of Clinical Medicine)
Ruebner, Matthias (University Hospital Erlangen. Friedrich-Alexander University Erlangen-Nuremberg, Department of Gynaecology and Obstetrics)
Saloustros, Emmanouil
(General University Hospital of Larissa (Grècia))
Sanden, Kristin (University of Wisconsin, Cancer Center at ProHealth Care)
Santamariña, Marta (Instituto de Investigación Sanitaria de Santiago (IDIS))
Scheuner, Maren T. (University of California San Francisco, Cancer Genetics and Prevention Program)
Schmutzler, Rita K. (University of Cologne, Center for Molecular Medicine Cologne)
Schneider, Michael (University Hospital Erlangen (Alemanya))
Scott, Christopher
(Mayo Clinic, Department of Health Sciences Research)
Senter, Leigha (The Ohio State University, Department of Internal Medicine)
Shah, Mitul (University of Cambridge, Department of Oncology)
Sharma, Priyanka (University of Kansas Medical Center, Department of Internal Medicine)
Shu, Xiao-Ou (Vanderbilt University School of Medicine, Department of Medicine)
Simard, Jacques (Université Laval)
Singer, Christian F. (Medical University of Vienna)
Sohn, Christof (University of Heidelberg)
Soucy, Penny (Université Laval)
Southey, Melissa C. (The University of Melbourne, Department of Clinical Pathology)
Spinelli, John J. (University of British Columbia, School of Population and Public Health)
Steele, Linda (Beckman Research Institute of City of Hope (Duarte, Estats Units d'Amèrica). Department of Population Sciences)
Stoppa-Lyonnet, Dominique
(Université Paris Descartes)
Tapper, William J. (University of Southampton)
Teixeira, Manuel R. (University of Porto)
Terry, Mary Beth (Columbia University, Department of Epidemiology)
Thomassen, Mads (Odense University Hospital (Dinamarca))
Thompson, Jennifer (NorthShore University HealthSystem, Center for Medical Genetics)
Thull, Darcy L. (University of Pittsburgh School of Medicine, Department of Medicine)
Tischkowitz, Marc (University of Cambridge, Department of Medical Genetics)
Tollenaar, Rob A. E. M. (Leiden University Medical Center, Department of Surgery)
Torres, Diana (Pontificia Universidad Javeriana)
Troester, Melissa A. (University of North Carolina at Chapel Hill)
Truong, Thérèse (University Paris-Sud)
Tung, Nadine (Beth Israel Deaconess Medical Center, Department of Medical Oncology)
Untch, Michael (Helios Clinics Berlin-Buch, Department of Gynecology and Obstetrics)
Vachon, Celine M. (Mayo Clinic, Department of Health Sciences Research)
van Rensburg, Elizabeth J. (University of Pretoria, Department of Genetics)
van Veen, Elke M. (Manchester University NHS Foundation Trust)
Vega, Ana (Instituto de Investigación Sanitaria de Santiago (IDIS))
Viel, Alessandra
(Centro di Riferimento Oncologico di Aviano)
Wappenschmidt, Barbara (University of Cologne, Center for Molecular Medicine Cologne)
Weitzel, Jeffrey N. (City of Hope, Clinical Cancer Genetics)
Wendt, Camilla (Karolinska Institutet (Estocolm, Suècia))
Wieme, Greet
(Ghent University, Centre for Medical Genetics)
Wolk, Alicja (Uppsala University, Department of Surgical Sciences)
Yang, Xiaohong R. (National Cancer Institute)
Zheng, Wei
(Vanderbilt University School of Medicine)
Ziogas, Argyrios
(University of California Irvine, Department of Epidemiology)
Zorn, Kristin K. (University of Pittsburgh School of Medicine)
Dunning, Alison M. (University of Cambridge, Department of Oncology)
Lush, Michael (University of Cambridge, Department of Public Health and Primary Care)
Wang, Qin (University of Cambridge, Department of Public Health and Primary Care)
McGuffog, Lesley (University of Cambridge, Department of Public Health and Primary Care)
Parsons, Michael T. (QIMR Berghofer Medical Research Institute, Department of Genetics and Computational Biology)
Pharoah, Paul D. P.
(University of Cambridge. Centre for Cancer Genetic Epidemiology)
Fostira, Florentia (National Centre for Scientific Research 'Demokritos')
Toland, Amanda E. (The Ohio State University, Department of Cancer Biology and Genetics)
Andrulis, Irene L. (University of Toronto, Department of Molecular Genetics)
Ramus, Susan J. (The Kinghorn Cancer Centre, Garvan Institute of Medical Research)
Swerdlow, Anthony J. (The Institute of Cancer Research)
Greene, Mark H.
(National Cancer Institute, Clinical Genetics Branch)
Chung, Wendy (Columbia University, Departments of Pediatrics and Medicine)
Milne, Roger L.
(Monash University)
Chenevix-Trench, Georgia (QIMR Berghofer Medical Research Institute, Department of Genetics and Computational Biology)
Dörk, Thilo (Hannover Medical School)
Schmidt, Marjanka K. (The Netherlands Cancer Institute (Amsterdam, Països Baixos))
Easton, Douglas F. (University of Cambridge, Department of Oncology)
Radice, Paolo (Istituto Nazionale dei Tumori)
Hahnen, Eric
(University of Cologne)
Antoniou, Antonis C. (University of Cambridge, Department of Public Health and Primary Care)
Couch, Fergus J. (Mayo Clinic, Department of Laboratory Medicine and Pathology)
Nevanlinna, Heli
(University of Helsinki, Department of Obstetrics and Gynecology)
Surrallés i Calonge, Jordi
(Institut d'Investigació Biomèdica Sant Pau)
Peterlongo, Paolo
(The FIRC Institute for Molecular Oncology)
Date: |
2019 |
Abstract: |
Breast cancer is a common disease partially caused by genetic risk factors. Germline pathogenic variants in DNA repair genes BRCA1, BRCA2, PALB2, ATM, and CHEK2 are associated with breast cancer risk. FANCM, which encodes for a DNA translocase, has been proposed as a breast cancer predisposition gene, with greater effects for the ER-negative and triple-negative breast cancer (TNBC) subtypes. We tested the three recurrent protein-truncating variants FANCM :p. Arg658*, p. Gln1701*, and p. Arg1931* for association with breast cancer risk in 67,112 cases, 53,766 controls, and 26,662 carriers of pathogenic variants of BRCA1 or BRCA2. These three variants were also studied functionally by measuring survival and chromosome fragility in FANCM −/− patient-derived immortalized fibroblasts treated with diepoxybutane or olaparib. We observed that FANCM :p. Arg658* was associated with increased risk of ER-negative disease and TNBC (OR = 2. 44, P = 0. 034 and OR = 3. 79; P = 0. 009, respectively). In a country-restricted analysis, we confirmed the associations detected for FANCM :p. Arg658* and found that also FANCM :p. Arg1931* was associated with ER-negative breast cancer risk (OR = 1. 96; P = 0. 006). The functional results indicated that all three variants were deleterious affecting cell survival and chromosome stability with FANCM :p. Arg658* causing more severe phenotypes. In conclusion, we confirmed that the two rare FANCM deleterious variants p. Arg658* and p. Arg1931* are risk factors for ER-negative and TNBC subtypes. Overall our data suggest that the effect of truncating variants on breast cancer risk may depend on their position in the gene. Cell sensitivity to olaparib exposure, identifies a possible therapeutic option to treat FANCM -associated tumors. |
Grants: |
Ministerio de Ciencia e Innovación CB06-07-0023 Ministerio de Ciencia e Innovación RTI2018-098419-B-I00 European Commission 305421
|
Rights: |
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Language: |
Anglès |
Document: |
Article ; recerca ; Versió publicada |
Subject: |
Cancer genetics |
Published in: |
NPJ breast cancer, Vol. 5 (November 2019) , art. 38, ISSN 2374-4677 |
DOI: 10.1038/s41523-019-0127-5
PMID: 31700994
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