Identification of six new susceptibility loci for invasive epithelial ovarian cancer
Open accessAbstract
Genome-wide association studies (GWAS) have identified 12 epithelial ovarian cancer (EOC) susceptibility alleles. The pattern of association at these loci is consistent in BRCA1 and BRCA2 mutation carriers who are at high risk of EOC. After imputation to 1000 Genomes Project data, we assessed associations of 11 million genetic variants with EOC risk from 15,437 cases unselected for family history and 30,845 controls and from 15,252 BRCA1 mutation carriers and 8,211 BRCA2 mutation carriers (3,096 with ovarian cancer), and we combined the results in a meta-analysis. This new study design yielded increased statistical power, leading to the discovery of six new EOC susceptibility loci. Variants at 1p36 (nearest gene, WNT4), 4q26 (SYNPO2), 9q34.2 (ABO) and 17q11.2 (ATAD5) were associated with EOC risk, and at 1p34.3 (RSPO1) and 6p22.1 (GPX6) variants were specifically associated with the serous EOC subtype, all with P < 5 × 10(-8). Incorporating these variants into risk assessment tools will improve clinical risk predictions for BRCA1 and BRCA2 mutation carriers.
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The index SNP for endometriosis at the WNT4 locus on chromosome 1p36.12 is also the index SNP for ovarian cancer and the risk mechanism likely acts through inverse regulation of CDC42 and LINC00339.
“The most strongly associated (index) SNP for endometriosis at the WNT4 locus on chromosome 1p36.12 is also the index SNP for ovarian cancer35 and the risk mechanism likely acts through inverse regulation of CDC42 and LINC00339 (ref. 36).”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [35]
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Self-citation
- Authors
- EMBRACE, Kuchenbaecker, K. B., Collaborators, G. S., Breast Cancer Family Registry, HEBON, KConFab Investigators, Australian Cancer Study (Ovarian Cancer Investigators), Australian Ovarian Cancer Study Group, the Consortium of Investigators of Modifiers of BRCA1 and BRCA2, Ramus, S. J., Tyrer, J., Lee, A., Shen, H. C., Beesley, J., Lawrenson, K., McGuffog, L., Healey, S., Lee, J. M., Spindler, T. J., Lin, Y. G., Pejovic, T., Bean, Y., Li, Q., Coetzee, S., Hazelett, D., Miron, A., Southey, M., Terry, M. B., Goldgar, D. E., Buys, S. S., Janavicius, R., Dorfling, C. M., van Rensburg, E. J., Neuhausen, S. L., Ding, Y. C., Hansen, T. V. O., Jønson, L., Gerdes, A.-M., Ejlertsen, B., Barrowdale, D., Dennis, J., Benitez, J., Osorio, A., Garcia, M. J., Komenaka, I., Weitzel, J. N., Ganschow, P., Peterlongo, P., Bernard, L., Viel, A., Bonanni, B., Peissel, B., Manoukian, S., Radice, P., Papi, L., Ottini, L., Fostira, F., Konstantopoulou, I., Garber, J., Frost, D., Perkins, J., Platte, R., Ellis, S., Godwin, A. K., Schmutzler, R. K., Meindl, A., Engel, C., Sutter, C., Sinilnikova, O. M., Damiola, F., Mazoyer, S., Stoppa-Lyonnet, D., Claes, K., De Leeneer, K., Kirk, J., Rodriguez, G. C., Piedmonte, M., O'Malley, D. M., de la Hoya, M., Caldes, T., Aittomäki, K., Nevanlinna, H., Collée, J. M., Rookus, M. A., Oosterwijk, J. C., Tihomirova, L., Tung, N., Hamann, U., Isaccs, C., Tischkowitz, M., Imyanitov, E. N., Caligo, M. A., Campbell, I. G., Hogervorst, F. B. L., Olah, E., Diez, O., Blanco, I., Brunet, J., Lazaro, C., Pujana, M. A., Jakubowska, A., Gronwald, J., Lubinski, J., Sukiennicki, G., Barkardottir, R. B., Plante, M., Simard, J., Soucy, P., Montagna, M., Tognazzo, S., Teixeira, M. R., Pankratz, V. S., Wang, X., Lindor, N., Szabo, C. I., Kauff, N., Vijai, J., Aghajanian, C. A., Pfeiler, G., Berger, A., Singer, C. F., Tea, M.-K., Phelan, C. M., Greene, M. H., Mai, P. L., Rennert, G., Mulligan, A. M., Tchatchou, S., Andrulis, I. L., Glendon, G., Toland, A. E., Jensen, U. B., Kruse, T. A., Thomassen, M., Bojesen, A., Zidan, J., Friedman, E., Laitman, Y., Soller, M., Liljegren, A., Arver, B., Einbeigi, Z., Stenmark-Askmalm, M., Olopade, O. I., Nussbaum, R. L., Rebbeck, T. R., Nathanson, K. L., Domchek, S. M., Lu, K. H., Karlan, B. Y., Walsh, C., Lester, J., Hein, A., Ekici, A. B., Beckmann, M. W., Fasching, P. A., Lambrechts, D., Van Nieuwenhuysen, E., Vergote, I., Lambrechts, S., Dicks, E., Doherty, J. A., Wicklund, K. G., Rossing, M. A., Rudolph, A., Chang-Claude, J., Wang-Gohrke, S., Eilber, U., Moysich, K. B., Odunsi, K., Sucheston, L., Lele, S., Wilkens, L. R., Goodman, M. T., Thompson, P. J., Shvetsov, Y. B., Runnebaum, I. B., Dürst, M., Hillemanns, P., Dörk, T., Antonenkova, N., Bogdanova, N., Leminen, A., Pelttari, L. M., Butzow, R., Modugno, F., Kelley, J. L., Edwards, R. P., Ness, R. B., du Bois, A., Heitz, F., Schwaab, I., Harter, P., Matsuo, K., Hosono, S., Orsulic, S., Jensen, A., Kjaer, S. K., Hogdall, E., Hasmad, H. N., Azmi, M. A. N., Teo, S.-H., Woo, Y.-L., Fridley, B. L., Goode, E. L., Cunningham, J. M., Vierkant, R. A., Bruinsma, F., Giles, G. G., Liang, D., Hildebrandt, M. A. T., Wu, X., Levine, D. A., Bisogna, M., Berchuck, A., Iversen, E. S., Schildkraut, J. M., Concannon, P., Weber, R. P., Cramer, D. W., Terry, K. L., Poole, E. M., Tworoger, S. S., Bandera, E. V., Orlow, I., Olson, S. H., Krakstad, C., Salvesen, H. B., Tangen, I. L., Bjorge, L., van Altena, A. M., Aben, K. K. H., Kiemeney, L. A., Massuger, L. F. A. G., Kellar, M., Brooks-Wilson, A., Kelemen, L. E., Cook, L. S., Le, N. D., Cybulski, C., Yang, H., Lissowska, J., Brinton, L. A., Wentzensen, N., Hogdall, C., Lundvall, L., Nedergaard, L., Baker, H., Song, H., Eccles, D., McNeish, I., Paul, J., Carty, K., Siddiqui, N., Glasspool, R., Whittemore, A. S., Rothstein, J. H., McGuire, V., Sieh, W., Ji, B.-T., Zheng, W., Shu, X.-O., Gao, Y.-T., Rosen, B., Risch, H. A., McLaughlin, J. R., Narod, S. A., Monteiro, A. N., Chen, A., Lin, H.-Y., Permuth-Wey, J., Sellers, T. A., Tsai, Y.-Y., Chen, Z., Ziogas, A., Anton-Culver, H., Gentry-Maharaj, A., Menon, U., Harrington, P., Lee, A. W., Wu, A. H., Pearce, C. L., Coetzee, G., Pike, M. C., Dansonka-Mieszkowska, A., Timorek, A., Rzepecka, I. K., Kupryjanczyk, J., Freedman, M., Noushmehr, H., Easton, D. F., Offit, K., Couch, F. J., Gayther, S., Pharoah, P. P., Antoniou, A. C., & Chenevix-Trench, G.
- Affiliations
- University of Cambridge (GB)
- University of Southern California (US)
- QIMR Berghofer Medical Research Institute (AU)
- Oregon Health & Science University (US)
- Universidade de São Paulo (BR)
- University of Utah (US)
- Case Western Reserve University (US)
- The University of Melbourne (AU)
- City of Hope (US)
- Copenhagen University Hospital (DK)
- Spanish National Cancer Research Centre (ES)
- City Of Hope National Medical Center (US)
- IFOM (IT)
- Cogentech S.R.L. Società Benefit a Socio Unico soggetta all’attività di direzione e coordinamento di IFOM - Istituto Fondazione di Oncologia Molecolare ETS (Italy) (IT)
- National Centre of Scientific Research "Demokritos" (GR)
- Dana-Farber Cancer Institute (US)
- University of Cologne (DE)
- TUM Klinikum (DE)
- Heidelberg University (DE)
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Ghent University (BE)
- Roswell Park Comprehensive Cancer Center (US)
- Hospital Clínico San Carlos (ES)
- University of Helsinki (FI)
- Endeavor Health (US)
- German Cancer Research Center (DE)
- The Netherlands Cancer Institute (NL)
- University of Pisa (IT)
- Latvian Biomedical Research and Study Centre (LV)
- Beth Israel Deaconess Medical Center (US)
- Universitat Autònoma de Barcelona (ES)
- Institut d'Investigació Biomédica de Bellvitge (ES)
- Institut Català d'Oncologia (ES)
- Peter MacCallum Cancer Centre (AU)
- University of Iceland (IS)
- Centre hospitalier universitaire de Québec (CA)
- Istituto Oncologico Veneto (IT)
- Universidade do Porto (PT)
- Mayo Clinic (US)
- National Institutes of Health (US)
- Memorial Sloan Kettering Cancer Center (US)
- Comprehensive Cancer Center Vienna (AT)
- University of Toronto (CA)
- Mount Sinai Hospital (CA)
- Odense University Hospital (DK)
- University Health Network (CA)
- Sheba Medical Center (IL)
- Lund University (SE)
- Karolinska University Hospital (SE)
- Sahlgrenska University Hospital (SE)
- Linköping University (SE)
- University of California, San Francisco (US)
- The University of Texas MD Anderson Cancer Center (US)
- Cedars-Sinai Medical Center (US)
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Dartmouth College (US)
- University of California, Los Angeles (US)
- Fred Hutch Cancer Center (US)
- Universität Ulm (DE)
- Medizinische Hochschule Hannover (DE)
- Helsinki University Hospital (FI)
- University of Pittsburgh (US)
- Kyushu University (JP)
- Helios Dr. Horst Schmidt Kliniken Wiesbaden (DE)
- Danish Cancer Society (DK)
- University Malaya Medical Centre (MY)
- Cancer Research Malaysia (MY)
- University of Kansas Medical Center (US)
- Cancer Council Victoria (AU)
- Duke University (US)
- Duke Cancer Institute (US)
- Brigham and Women's Hospital (US)
- Radboud University Medical Center (NL)
- Haukeland University Hospital (NO)
- BC Cancer Agency (CA)
- Medical University of South Carolina (US)
- University of Copenhagen (DK)
- Princess Anne Hospital (GB)
- National Cancer Institute (US)
- Beatson West of Scotland Cancer Centre (GB)
- Vanderbilt University (US)
- Shanghai Cancer Institute (CN)
- Yale University (US)
- Moffitt Cancer Center (US)
- University of California, Irvine (US)
- The Maria Sklodowska-Curie National Research Institute of Oncology (PL)
- Corresponding author
- Kuchenbaecker, Karoline B
- Ramus, Susan J
- Tyrer, Jonathan
- ORCID
- Kuchenbaecker, Karoline B
- Ramus, Susan J
- Tyrer, Jonathan
- Lee, Andrew
- Lawrenson, Kate
- Lin, Yvonne G
- Pejovic, Tanja
- Li, Qiyuan
- Coetzee, Simon
- Hazelett, Dennis
- Southey, Melissa
- Terry, Mary Beth
- Buys, Saundra S
- Neuhausen, Susan L
- Ding, Yuan Chun
- Hansen, Thomas V O
- Gerdes, Anne-Marie
- Ejlertsen, Bent
- Barrowdale, Daniel
- Dennis, Joe
- Benitez, Javier
- Komenaka, Ian
- Weitzel, Jeffrey N
- Ganschow, Pamela
- Peterlongo, Paolo
- Viel, Alessandra
- Bonanni, Bernardo
- Peissel, Bernard
- Manoukian, Siranoush
- Radice, Paolo
- Papi, Laura
- Ottini, Laura
- Konstantopoulou, Irene
- Garber, Judy
- Godwin, Andrew K
- Meindl, Alfons
- Engel, Christoph
- Sutter, Christian
- Damiola, Francesca
- Mazoyer, Sylvie
- Claes, Kathleen
- Rodriguez, Gustavo C
- Nevanlinna, Heli
- Collée, J Margriet
- Rookus, Matti A
- Tung, Nadine
- Hamann, Ute
- Tischkowitz, Marc
- Caligo, Maria A
- Campbell, Ian G
- Blanco, Ignacio
- Brunet, Joan
- Jakubowska, Anna
- Gronwald, Jacek
- Barkardottir, Rosa B
- Plante, Marie
- Simard, Jacques
- Montagna, Marco
- Tognazzo, Silvia
- Teixeira, Manuel R
- Pankratz, Vernon S
- Wang, Xianshu
- Lindor, Noralane
- Kauff, Noah
- Vijai, Joseph
- Aghajanian, Carol A
- Pfeiler, Georg
- Singer, Christian F
- Greene, Mark H
- Rennert, Gad
- Mulligan, Anna Marie
- Andrulis, Irene L
- Glendon, Gord
- Toland, Amanda Ewart
- Jensen, Uffe Birk
- Bojesen, Anders
- Friedman, Eitan
- Laitman, Yael
- Soller, Maria
- Liljegren, Annelie
- Einbeigi, Zakaria
- Olopade, Olufunmilayo I
- Nussbaum, Robert L
- Rebbeck, Timothy R
- Nathanson, Katherine L
- Domchek, Susan M
- Lu, Karen H
- Karlan, Beth Y
- Walsh, Christine
- Hein, Alexander
- Ekici, Arif B
- Beckmann, Matthias W
- Fasching, Peter A
- Lambrechts, Diether
- Vergote, Ignace
- Lambrechts, Sandrina
- Dicks, Ed
- Doherty, Jennifer A
- Wicklund, Kristine G
- Rudolph, Anja
- Moysich, Kirsten B
- Odunsi, Kunle
- Wilkens, Lynne R
- Goodman, Marc T
- Shvetsov, Yurii B
- Dürst, Matthias
- Hillemanns, Peter
- Dörk, Thilo
- Bogdanova, Natalia
- Pelttari, Liisa M
- Modugno, Francesmary
- Heitz, Florian
- Harter, Philipp
- Matsuo, Keitaro
- Hosono, Satoyo
- Jensen, Allan
- Teo, Soo-Hwang
- Woo, Yin-Ling
- Fridley, Brooke L
- Goode, Ellen L
- Cunningham, Julie M
- Vierkant, Robert A
- Giles, Graham G
- Liang, Dong
- Hildebrandt, Michelle A T
- Wu, Xifeng
- Levine, Douglas A
- Berchuck, Andrew
- Schildkraut, Joellen M
- Concannon, Patrick
- Weber, Rachel Palmieri
- Cramer, Daniel W
- Terry, Kathryn L
- Poole, Elizabeth M
- Tworoger, Shelley S
- Bandera, Elisa V
- Orlow, Irene
- Olson, Sara H
- Krakstad, Camilla
- Tangen, Ingvild L
- Aben, Katja K H
- Kiemeney, Lambertus A
- Massuger, Leon F A G
- Brooks-Wilson, Angela
- Cook, Linda S
- Le, Nhu D
- Cybulski, Cezary
- Yang, Hannah
- Lissowska, Jolanta
- Brinton, Louise A
- Wentzensen, Nicolas
- Nedergaard, Lotte
- Song, Honglin
- Eccles, Diana
- Paul, James
- Carty, Karen
- Siddiqui, Nadeem
- Glasspool, Rosalind
- Whittemore, Alice S
- Rothstein, Joseph H
- McGuire, Valerie
- Sieh, Weiva
- Ji, Bu-Tian
- Zheng, Wei
- Shu, Xiao-Ou
- Gao, Yu-Tang
- Rosen, Barry
- Risch, Harvey A
- McLaughlin, John R
- Narod, Steven A
- Monteiro, Alvaro N
- Lin, Hui-Yi
- Sellers, Thomas A
- Tsai, Ya-Yu
- Chen, Zhihua
- Ziogas, Argyrios
- Menon, Usha
- Lee, Alice W
- Wu, Anna H
- Pike, Malcolm C
- Rzepecka, Iwona K
- Noushmehr, Houtan
- Easton, Douglas F
- Couch, Fergus J
- Gayther, Simon
- Antoniou, Antonis C
- Venue
- Nature Genetics
- Published
- 2015-01-12
- Volume
- 47
- Issue
- 2
- Pages
- 164-171
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC4445140
- OpenAlex
- W2095936660
- Cited by
- 250
- References
- 61
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 16 · 2023: 21 · 2022: 9 · 2021: 22 · 2020: 22 · 2019: 27 · 2018: 27 · 2017: 36 · 2016: 27 · 2015: 28 · 2014: 1
- FWCI
- 4.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- Research Explorer (The University of Manchester) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- PubMed Central (acceptedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (acceptedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Creighton Digital Repository (CDR) (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- UCL Discovery (University College London) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Florence Research (University of Florence) (submittedVersion, other-oa)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Minerva Access (University of Melbourne) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Lirias (KU Leuven) (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- UpSpace Institutional Repository (University of Pretoria) (submittedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion)
- Hirsla (Landspítali University Hospital) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion)
- Funders
- Ovarian Cancer Research Fund
- Wellcome Trust (076113)
- Francis Crick Institute (10124)
- Cancer Research UK (11174, C1287‐A10118, 12677, 16561, 16565, C12292/A11174, 17523, 16563, 10124, 15960)
- Norges Forskningsråd
- National Institutes of Health (UL1TR000005, 1rc4ca153828-01)
- National Cancer Institute (R01CA140323, UG1CA189867, RC4-CA153828, UM1CA164920, U10CA037517, U10CA180868, U10CA027469, UG1CA233180, R01CA087538, R01CA126841, U19CA148112, U10CA180850, U10CA180838, U10CA180867, U01CA116167, R01CA176785, UM1CA182910, P30CA015083, P30CA071789, P30CA076292, P50CA159981, U24CA196067, P50CA136393, R25CA174664, P50CA116201, U10CA180822)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Keywords
- epithelial ovarian cancer, cancer susceptibility loci, BRCA1 mutation carriers, BRCA2 mutation carriers, genetic risk variants, serous ovarian cancer, Wnt4, Turku, ATAD5, RSPO1, risk prediction, 1p36, 17q11.2
- MeSH terms
- Carcinoma, Ovarian Epithelial, Adolescent, Adult, Alleles, Female, Genotype, Heterozygote, Humans, Mutation, Neoplasms, Glandular and Epithelial, Ovarian Neoplasms, Risk, Genes, Reporter, BRCA1 Protein, Genetic Predisposition to Disease, Polymorphism, Single Nucleotide, BRCA2 Protein, Quantitative Trait Loci, Genome-Wide Association Study, Young Adult
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