Journal article

Inherited variants in the inner centromere protein (INCENP) gene of the chromosomal passenger complex contribute to the susceptibility of ER-negative breast cancer

Maria Kabisch, Justo Lorenzo Bermejo, Thomas Duennebier, Shibo Ying, Kyriaki Michailidou, Manjeet K Bolla, Qin Wang, Joe Dennis, Mitul Shah, Barbara J Perkins, Kamila Czene, Hatef Darabi, Mikael Eriksson, Stig E Bojesen, Borge G Nordestgaard, Sune F Nielsen, Henrik Flyger, Diether Lambrechts, Patrick Neven, Stephanie Peeters Show all

Carcinogenesis | OXFORD UNIV PRESS | Published : 2015

Grants

Awarded by Cancer Research UK


Awarded by European Community


Awarded by National Institutes of Health


Awarded by Post-Cancer GWAS initiative (GAME-ON initiative)


Awarded by Department of Defence


Awarded by 'Stichting tegen Kanker'


Awarded by NIH


Awarded by Deutsche Krebshilfe e.V.


Awarded by Federal Ministry of Education and Research (BMBF) Germany


Awarded by Academy of Finland


Awarded by Dutch Cancer Society


Awarded by Dutch government


Awarded by Fondo de Investigacion Sanitario


Awarded by National Cancer Institute (USA)


Awarded by CCSG Share Resource by National Institutes of Health


Awarded by Hellenic Cooperative Oncology Group


Awarded by Australian NHMRC


Awarded by Canadian Institutes of Health Research


Awarded by Ministry of Economic Development, Innovation and Export Trade


Awarded by Finnish Cancer Foundation, the Academy of Finland


Awarded by Finnish Cancer Foundation, the Academy of Finland (Center of Excellence)


Awarded by Federal Ministry of Education and Research (BMBF)


Awarded by NIH grant


Awarded by California Breast Cancer Research Fund


Awarded by California Department of Public Health


Awarded by Lon V Smith Foundation


Awarded by Norwegian Research council



Awarded by National Institute for Health Research


Funding Acknowledgements

The results shown in this article are in part based upon data generated by the TCGA Research Network: http://cancergenome.nih.gov; the ENCODE Consortium and the ENCODE production laboratory(s): http://genome.ucsc.edu/ENCODE; the Gene Expression Omnibus contributors: http://www.ncbi.nlm.nih.gov/geo and the 1000 Genomes Project Consortium: http://www.1000genomes.org/home.BCAC: 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: This study would not have been possible without the contributions of the following: PH (COGS); DFE, PP, KM, MKB, QW (BCAC), Andrew Berchuck (OCAC), Rosalind A. Eeles, DFE, Ali Amin Al Olama, Zsofia Kote-Jarai, Sara Benlloch (PRACTICAL), GCT, Antonis Antoniou, Lesley McGuffog, FJC and Ken Offit (CIMBA), JD, AMD, Andrew Lee, and Ed Dicks, CL and the staff of the Centre for Genetic Epidemiology Laboratory, JB, AGN and the staff of the CNIO genotyping unit, JS and DCT, FB, DV, Sylvie LaBoissiere and Frederic Robidoux and the staff of the McGill University and Genome Quebec Innovation Centre, SEB, SFN, BGN, and the staff of the Copenhagen DNA laboratory, and Julie M. Cunningham, Sharon A. Windebank, Christopher A. Hilker, Jeffrey Meyer and the staff of Mayo Clinic Genotyping Core Facility. SEARCH: The SEARCH and EPIC teams. pKARMA: The Swedish Medical Research Counsel. CGPS: Staff and participants of the Copenhagen General Population Study. For the excellent technical assistance: Dorthe Uldall Andersen, Maria Birna Arnadottir, Anne Bank, Dorthe Kjeldgard Hansen. The Danish Breast Cancer Group (DBCG) is acknowledged for the tumor information. LMBC: Gilian Peuteman, Dominiek Smeets, Thomas Van Brussel and Kathleen Corthouts. MARIE: Judith Heinz, Nadia Obi, Alina Vrieling, Sabine Behrens, Ursula Eilber, Muhabbet Celik, Til Olchers, Stefan Nickels. BBCS: Eileen Williams, Elaine Ryder-Mills, Kara Sargus. HEBCS: Kirsimari Aaltonen, Karl von Smitten, Sofia Khan, Tuomas Heikkinen, Irja Erkkila. ABCS: Sten Cornelissen, Richard van Hien, Linde Braaf, FBLH, Senno Verhoef, Laura van 't Veer, Emiel Rutgers, Ellen van der Schoot, Femke Atsma. SASBAC: The Swedish Medical Research Counsel. BSUCH: Medical Faculty Mannheim, Germany (PB). CNIO-BCS: Guillermo Pita, Charo Alonso, Daniel Herrero, Nuria Alvarez, MPZ, Primitiva Menendez, the Human Genotyping-CEGEN Unit (CNIO). SBCS: Sue Higham, Helen Cramp, Ian Brock, Sabapathy Balasubramanian and Dan Connley. OFBCR: Teresa Selander, Nayana Weerasooriya. BIGGS: Niall McInerney, Gabrielle Colleran, Andrew Rowan, Angela Jones. kConFab/AOCS: We wish to thank Heather Thorne, Eveline Niedermayr, all the kConFab research nurses and staff, the heads and staff of the Family Cancer Clinics, and the Clinical Follow Up Study (which has received funding from the National Health and Medical Research Council, the National Breast Cancer Foundation, Cancer Australia and the National Institute of Health (USA) for their contributions to this resource, and the many families who contribute to kConFab. RBCS: Petra Bos, Jannet Blom, Ellen Crepin, Anja Nieuwlaat, Annette Heemskerk, the Erasmus MC Family Cancer Clinic. ABCFS: Maggie Angelakos, Judi Maskiell, Gillian Dite. TNBCC: Robert Pilarski and Charles Shapiro were instrumental in the formation of the OSU Breast Cancer Tissue Bank. We thank the Human Genetics Sample Bank for processing of samples and providing OSU Columbus area control samples. BBCC: Silke Landrith, Alexander Hein, Sonja Oeser, Michael Schneider.ESTHER: Hartwig Ziegler, Sonja Wolf, Volker Hermann. UKBGS: We thank Breakthrough Breast Cancer and the Institute of Cancer Research for support and funding of the Breakthrough Generations Study, and the study participants, study staff, and the doctors, nurses and other health care providers and health information sources who have contributed to the study. We acknowledge National Health Service (NHS) funding to the Royal Marsden/ICR NIHR Biomedical Research Centre. PBCS: Louise Brinton, Mark Sherman, Neonila Szeszenia-Dabrowska, Beata Peplonska, Witold Zatonski, Pei Chao, Michael Stagner. MTLGEBCS: We would like to thank Martine Tranchant (CHU de Quebec Research Center), Marie-France Valois, Annie Turgeon and Lea Heguy (McGill University Health Centre, Royal Victoria Hospital; McGill University) for DNA extraction, sample management and skillful technical assistance. J.S. is Chairholder of the Canada Research Chair in Oncogenetics. OBCS: Meeri Otsukka, Kari Mononen. GENICA: The GENICA Network: Dr Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, and University of Tubingen, Germany; (HBra, Wing-Yee Lo, Christina Justenhoven), Department of Internal Medicine, Evangelische Kliniken Bonn gGmbH, Johanniter Krankenhaus, Bonn, Germany (YDK, Christian Baisch), Institute of Pathology, University of Bonn, Germany (Hans-Peter Fischer), Molecular Genetics of Breast Cancer, Deutsches Krebsforschungszentrum (DKFZ), Heidelberg, Germany (UH) and Institute for Prevention and Occupational Medicine of the German Social Accident Insurance, Institute of the Ruhr University Bochum (IPA), Bochum, Germany (TB, Beate Pesch, Sylvia Rabstein, Anne Lotz); Institute of Occupational Medicine and Maritime Medicine, University Medical Center Hamburg-Eppendorf, Germany (Volker Harth). MBCSG: Siranoush Manoukian, Bernard Peissel and Daniela Zaffaroni of the Fondazione IRCCS Istituto Nazionale dei Tumori (INT); Bernardo Bonanni, Monica Barile and Irene Feroce of the Istituto Europeo di Oncologia (IEO) and Loris Bernard the personnel of the Cogentech Cancer Genetic Test Laboratory. HMBCS: Peter Hillemanns, Hans Christiansen and Johann H. Karstens. KBCP: Eija Myohanen, Helena Kemilainen. ORIGO: We thank E. Krol-Warmerdam and J. Blom for patient accrual, administering questionnaires and managing clinical information. The LUMC survival data were retrieved from the Leiden hospital-based cancer registry system (ONCDOC) with the help of Dr J. Molenaar. NBHS: We thank study participants and research staff for their contributions and commitment to this study. SKKDKFZS: We thank all study participants, clinicians, family doctors, researchers and technicians for their contributions and commitment to this study. CTS: The CTS Steering Committee includes Leslie Bernstein, Susan Neuhausen, James Lacey, Sophia Wang, Huiyan Ma, Yani Lu and Jessica Clague DeHart at the Beckman Research Institute of City of Hope, Dennis Deapen, Rich Pinder, Eunjung Lee and Fred Schumacher at the University of Southern California, Pam Horn-Ross, Peggy Reynolds, Christina Clarke Dur and David Nelson at the Cancer Prevention Institute of California, and HAC, Argyrios Ziogas, and Hannah Park at the University of California Irvine. NBCS: NBCS includes the following clinical collaborators: Prof. Per Eystein Lonning, MD (Section of Oncology, Institute of Medicine, University of Bergen and Department of Oncology, Haukeland University Hospital, Bergen, Norway), Prof. Em. Sophie D.Fossa, MD (National Resource Centre for Longterm Studies after Cancer, Rikshospitalet-Radiumhospitalet Cancer Clinic Montebello, Oslo, Norway), Head physician Tone Ikdahl, MD (Department of Oncology, Oslo University Hospital, Oslo, Norway), Dr Lars Ottestad, MD (Department of Genetics and Department of Oncology, Oslo University Hospital Radiumhospitalet), Dr Marit Muri Holmen, MD (Department of Radiology, Oslo University Hospital Radiumhospitalet, Oslo, Norway), Dr Vilde Haakensen, MD (Department of Genetics and Department of Oncology, Oslo University Hospital Radiumhospitalet and Institute for Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway), Prof. Bjorn Naume, MD (Division of Cancer Medicine and Radiotherapy, Department of Oncology, Oslo University Hospital Radiumhospitalet, Oslo, Norway), Associate Prof. Aslaug Helland, MD (Department of Genetics, Institute for Cancer Research and Department of Oncology, Oslo University Hospital Radiumhospitalet, Oslo, Norway and Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway), Prof. Inger Torhild Gram, MD (Department of Community Medicine, Faculty of Health Sciences, University of Tromso and Norwegian Centre for Integrated Care and Telemedicine, University Hospital of North Norway, Tromso, Norway), Prof. Em. Rolf Karesen, MD (Department of Breast and Endocrine Surgery, Institute for Clinical Medicine, Ullevaal Hospital, Oslo University Hospital and Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway), Dr Ellen Schlichting, MD (Department for Breast and Endocrine Surgery, Oslo University Hospital Ullevaal, Oslo, Norway), Prof. Toril Sauer, MD (Department of Pathology at Akershus University Hospital, Lorenskog, Norway), Dr Olav Engebraten, MD (Institute for Clinical Medicine, Faculty of Medicine, University of Oslo and Department of Oncology, Oslo University Hospital, Oslo, Norway), Dr Margit Riis, MD (Department of Surgery, Akershus University Hospital and Department of Clinical Molecular Biology (EpiGen), Institute of Clinical Medicine, Akershus University Hospital, University of Oslo, Lorenskog, Norway).This work was supported by the following: BCAC: Cancer Research UK [C1287/A10118, C1287/A12014] and by the European Community's Seventh Framework Programme under grant agreement number 223175 (grant number HEALTH-F2-2009-223175) (COGS). iCOGS: the European Community's Seventh Framework Programme under grant agreement no 223175 (HEALTH-F2-2009-223175) (COGS), Cancer Research UK (C1287/A10118, C1287/A 10710, C12292/A11174, C1281/A12014, C5047/A8384, C5047/A15007, C5047/A10692), the National Institutes of Health (CA128978) and Post-Cancer GWAS initiative (1U19 CA148537, 1U19 CA148065 and 1U19 CA148112-the GAME-ON initiative), the Department of Defence (W81XWH-10-1-0341), the Canadian Institutes of Health Research (CIHR) for the CIHR Team in Familial Risks of Breast Cancer, Komen Foundation for the Cure, the Breast Cancer Research Foundation, and the Ovarian Cancer Research Fund. SEARCH: Cancer Research UK [C490/A10124] and UK National Institute for Health Research Biomedical Research Centre at the University of Cambridge. pKARMA: Marit and Hans Rausings Initiative Against Breast Cancer. CGPS: Chief Physician Johan Boserup and Lise Boserup Fund, the Danish Medical Research Council and Herlev Hospital. LMBC: 'Stichting tegen Kanker' (232-2008 and 196-2010). D.L. is supported by the FWO and the KULPFV/10/016-SymBioSysII. MCBCS: NIH grants CA128978, CA116167, CA176785 an NIH Specialized Program of Research Excellence (SPORE) in Breast Cancer [CA116201], and the Breast Cancer Research Foundation and a generous gift from the David F. and Margaret T. Grohne Family Foundation and the Ting Tsung and Wei Fong Chao Foundation. MARIE: Deutsche Krebshilfe e.V. [70-2892-BR I], the Hamburg Cancer Society, the German Cancer Research Center and the genotype work in part by the Federal Ministry of Education and Research (BMBF) Germany [01KH0402]. BBCS: Cancer Research UK and Breakthrough Breast Cancer and acknowledges NHS funding to the NIHR Biomedical Research Centre, and the National Cancer Research Network (NCRN). HEBCS: Helsinki University Central Hospital Research Fund, Academy of Finland (266528), the Finnish Cancer Society, The Nordic Cancer Union and the Sigrid Juselius Foundation. ABCS: Dutch Cancer Society [grants NKI 2007-3839 and 2009 4363]; BBMRI-NL, which is a Research Infrastructure financed by the Dutch government (NWO 184.021.007); and the Dutch National Genomics Initiative. SASBAC: Agency for Science, Technology and Research of Singapore (A*STAR), the United States National Institute of Health (NIH) and the Susan G. Komen Breast Cancer Foundation. CECILE: Fondation de France, Institut National du Cancer (INCa), Ligue Nationale contre le Cancer, Ligue contre le Cancer Grand Ouest, Agence Nationale de Securite Sanitaire (ANSES), Agence Nationale de la Recherche (ANR). BSUCH: Dietmar-Hopp Foundation, the Helmholtz Society and the German Cancer Research Center (DKFZ). CNIO-BCS: Genome Spain Foundation, the Red Tematica de Investigacion Cooperativa en Cancer and grants from the Asociacion Espanola Contra el Cancer and the Fondo de Investigacion Sanitario (PI11/00923 and PI081120). The Human Genotyping-CEGEN Unit (CNIO) is supported by the Instituto de Salud Carlos III. SBCS: Yorkshire Cancer Research S295, S299, S305PA and Sheffield Experimental Cancer Medicine Centre. Ontario Familial Breast Cancer Registry (OFBCR): UM1 CA164920 from the National Cancer Institute (USA).The content of this manuscript does not necessarily reflect the views or policies of the National Cancer Institute or any of the collaborating centers in the Breast Cancer Family Registry (BCFR), nor does mention of trade names, commercial products or organizations imply endorsement by the USA Government or the BCFR. BIGGS ES: NIHR Comprehensive Biomedical Research Centre, Guy's and St. Thomas' NHS Foundation Trust in partnership with King's College London, UK. I. T. is supported by the Oxford Biomedical Research Centre. kConFab: National Breast Cancer Foundation, and previously by the National Health and Medical Research Council (NHMRC), the Queensland Cancer Fund, the Cancer Councils of New South Wales, Victoria, Tasmania and South Australia, and the Cancer Foundation of Western Australia. MEC: NIH grants CA63464, CA54281, CA098758 and CA132839. Financial support for KARBAC was provided through the regional agreement on medical training and clinical research (ALF) between Stockholm County Council and Karolinska Institutet, the Swedish Cancer Society, The Gustav V Jubilee foundation and Bert von Kantzows foundation. RBCS: Dutch Cancer Society (DDHK 2004-3124, DDHK 2009-4318). The Australian Breast Cancer Family Study (ABCFS) was supported by grant UM1 CA164920 from the National Cancer Institute (USA). The content of this manuscript does not necessarily reflect the views or policies of the National Cancer Institute or any of the collaborating centers in the Breast Cancer Family Registry (BCFR), nor does mention of trade names, commercial products or organizations imply endorsement by the USA Government or the BCFR. The ABCFS was also supported by the NHMRC of Australia, the New South Wales Cancer Council, the Victorian Health Promotion Foundation (Australia) and the Victorian Breast Cancer Research Consortium. J.L.H. is a NHMRC Australia Fellow and a Victorian Breast Cancer Research Consortium Group Leader. M.C.S. is a NHMRC senior research fellow and a Victorian Breast Cancer Research Consortium Group Leader. TNBCC: Specialized Program of Research Excellence (SPORE) in Breast Cancer (CA116201), a grant from the Breast Cancer Research Foundation, a generous gift from the David F. and Margaret T. Grohne Family Foundation and the Ting Tsung and Wei Fong Chao Foundation, the Stefanie Spielman Breast Cancer fund and the OSU Comprehensive Cancer Center, DBBR (a CCSG Share Resource by National Institutes of Health Grant P30 CA016056), the Hellenic Cooperative Oncology Group research grant (HR R_BG/04) and the Greek General Secretary for Research and Technology (GSRT) Program, Research Excellence II, the European Union (European Social Fund - ESF) and Greek national funds through the Operational Program 'Education and Lifelong Learning' of the National Strategic Reference Framework (NSRF)-ARISTEIA. MCCS cohort recruitment was funded by VicHealth and Cancer Council Victoria. The MCCS was further supported by Australian NHMRC grants 209057, 251553 and 504711 and by infrastructure provided by Cancer Council Victoria. BBCC: ELAN-Fond of the University Hospital of Erlangen. ESTHER: Baden Wurttemberg Ministry of Science, Research and Arts. Additional cases were recruited in the context of the VERDI study, which was supported by a grant from the German Cancer Aid (Deutsche Krebshilfe). UKBGS: Breakthrough Breast Cancer and the Institute of Cancer Research (ICR), London. ICR acknowledges NHS funding to the NIHR Biomedical Research Centre. PBCS: Intramural Research Funds of the National Cancer Institute, Department of Health and Human Services, USA.MTLGEBCS: Quebec Breast Cancer Foundation, the Canadian Institutes of Health Research for the 'CIHR Team in Familial Risks of Breast Cancer' program-grant # CRN-87521 and the Ministry of Economic Development, Innovation and Export Trade-grant # PSR-SIIRI-701. OBCS: Finnish Cancer Foundation, the Academy of Finland (grant number 250083, 122715 and Center of Excellence grant number 251314), the Finnish Cancer Foundation, the Sigrid Juselius Foundation, the University of Oulu, the University of Oulu Support Foundation and the special Governmental EVO funds for Oulu University Hospital-based research activities. GENICA: Federal Ministry of Education and Research (BMBF) Germany grants 01KW9975/5, 01KW9976/8, 01KW9977/0 and 01KW0114, the Robert Bosch Foundation, Stuttgart, Deutsches Krebsforschungszentrum (DKFZ), Heidelberg, the Institute for Prevention and Occupational Medicine of the German Social Accident Insurance, Institute of the Ruhr University Bochum (IPA), Bochum, as well as the Department of Internal Medicine, Evangelische Kliniken Bonn gGmbH, Johanniter Krankenhaus, Bonn, Germany. MBCSG: Italian Association for Cancer Research (AIRC) and by funds from the Italian citizens who allocated the 5/1000 share of their tax payment in support of the Fondazione IRCCS Istituto Nazionale Tumori, according to Italian laws (INT-Institutional strategic projects '5 x 1000'). HMBCS: Friends of Hannover Medical School and by the Rudolf Bartling Foundation. KBCP: Government Funding (EVO) of Kuopio University Hospital grants, Cancer Fund of North Savo, the Finnish Cancer Organizations and by the strategic funding of the University of Eastern Finland. ORIGO: Dutch Cancer Society (RUL 1997-1505) and the Biobanking and Biomolecular Resources Research Infrastructure (BBMRI-NL CP16). The SZBCS was supported by grant PBZ_KBN_122/P05/2004. NBHS: NIH grant R01CA100374. Biological sample preparation was conducted the Survey and Biospecimen Shared Resource, which is supported by P30 CA68485. SKKDKFZS: DKFZ. CTS: California Breast Cancer Act of 1993 and the California Breast Cancer Research Fund (contract 97-10500) and is currently funded through the National Institutes of Health (R01 CA77398). Collection of cancer incidence data was supported by the California Department of Public Health as part of the statewide cancer reporting program mandated by California Health and Safety Code Section 103885. HAC receives support from the Lon V Smith Foundation (LVS39420). NBCS: Norwegian Research council, 155218/V40, 175240/S10 to ALBD, FUGE-NFR 181600/V11 to VNK and a Swizz Bridge Award to ALBD.