University of Oulu

Ahearn, T.U., Zhang, H., Michailidou, K. et al. Common variants in breast cancer risk loci predispose to distinct tumor subtypes. Breast Cancer Res 24, 2 (2022). https://doi.org/10.1186/s13058-021-01484-x

Common variants in breast cancer risk loci predispose to distinct tumor subtypes

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Author: Ahearn, Thomas U.1; Zhang, Haoyu1,2; Michailidou, Kyriaki3,4,5;
Milne, Roger L.6,7,8; Bolla, Manjeet K.4; Dennis, Joe4; Dunning, Alison M.9; Lush, Michael4; Wang, Qin4; Andrulis, Irene L.10,11; Anton-Culver, Hoda12; Arndt, Volker13; Aronson, Kristan J.14,15; Auer, Paul L.16,17; Augustinsson, Annelie18; Baten, Adinda19; Becher, Heiko20; Behrens, Sabine21; Benitez, Javier22,23; Bermisheva, Marina24,25; Blomqvist, Carl26,27; Bojesen, Stig E.28,29,30; Bonanni, Bernardo31; Borresen-Dale, Anne-Lise32,33; Brauch, Hiltrud34,35,36; Brenner, Hermann13,37,38; Brooks-Wilson, Angela39,40; Bruening, Thomas41; Burwinkel, Barbara42,43; Buys, Saundra S.44; Canzian, Federico45; Castelao, Jose E.46; Chang-Claude, Jenny21,47; Chanock, Stephen J.1; Chenevix-Trench, Georgia48; Clarke, Christine L.49; Collee, J. Margriet50; Cox, Angela51; Cross, Simon S.52; Czene, Kamila53; Daly, Mary B.54; Devilee, Peter55,56; Dork, Thilo57; Dwek, Miriam58; Eccles, Diana M.59; Evans, D. Gareth60,61; Fasching, Peter A.62; Figueroa, Jonine63,64; Floris, Giuseppe19; Gago-Dominguez, Manuela65,66; Gapstur, Susan M.67; Garcia-Saenz, Jose A.68; Gaudet, Mia M.67; Giles, Graham G.6,7,8; Goldberg, Mark S.69,70; Gonzalez-Neira, Anna22; Alnaes, Grethe I. Grenaker32; Grip, Mervi71; Guenel, Pascal72; Haiman, Christopher A.73; Hall, Per53,74; Hamann, Ute75; Harkness, Elaine F.76,77,78; Heemskerk-Gerritsen, Bernadette A. M.79; Holleczek, Bernd80; Hollestelle, Antoinette79; Hooning, Maartje J.79; Hoover, Robert N.1; Hopper, John L.7; Howell, Anthony81; Jakimovska, Milena82; Jakubowska, Anna83,84; John, Esther M.85,86; Jones, Michael E.87; Jung, Audrey21; Kaaks, Rudolf21; Kauppila, Saila88; Keeman, Renske89; Khusnutdinova, Elza24,90; Kitahara, Cari M.91; Ko, Yon-Dschun92; Koutros, Stella1; Kristensen, Vessela N.33,93,94; Kruger, Ute18; Kubelka-Sabit, Katerina95; Kurian, Allison W.85,86; Kyriacou, Kyriacos5,96; Lambrechts, Diether97,98; Lee, Derrick G.99,100; Lindblom, Annika101,102; Linet, Martha91; Lissowska, Jolanta103; Llaneza, Ana104; Lo, Wing-Yee34,105; MacInnis, Robert J.6,7; Mannermaa, Arto106,107,108; Manoochehri, Mehdi75; Margolin, Sara74,109; Martinez, Maria Elena66; McLean, Catriona110; Meindl, Alfons111; Menon, Usha112; Nevanlinna, Heli113; Newman, William G.60,61; Nodora, Jesse66,114; Offit, Kenneth115; Olsson, Hakan18; Orr, Nick116; Park-Simon, Tjoung-Won57; Patel, Alpa, V67; Peto, Julian117; Pita, Guillermo118; Plaseska-Karanfilska, Dijana82; Prentice, Ross16; Punie, Kevin119,120; Pylkas, Katri121,122; Radice, Paolo123; Rennert, Gad124; Romero, Atocha125; Ruediger, Thomas126; Saloustros, Emmanouil127; Sampson, Sarah128,129; Sandler, Dale P.130; Sawyer, Elinor J.131; Schmutzler, Rita K.132,133,134; Schoemaker, Minouk J.87; Schottker, Ben13,135; Sherman, Mark E.136; Shu, Xiao-Ou137; Smichkoska, Snezhana138; Southey, Melissa C.6,8,139; Spinelli, John J.140,141; Swerdlow, Anthony J.87,142; Tamimi, Rulla M.143; Tapper, William J.59; Taylor, Jack A.130,144; Teras, Lauren R.67; Terry, Mary Beth145; Torres, Diana75,146; Troester, Melissa A.147,148; Vachon, Celine M.149; van Deurzen, Carolien H. M.150; van Veen, Elke M.60,61; Wagner, Philippe18; Weinberg, Clarice R.151; Wendt, Camilla74,109; Wesseling, Jelle89,152; Winqvist, Robert121,122; Wolk, Alicja153,154; Yang, Xiaohong R.1; Zheng, Wei137; Couch, Fergus J.155; Simard, Jacques156; Kraft, Peter157,158; Easton, Douglas F.4,9; Pharoah, Paul D. P.4,9; Schmidt, Marjanka K.89,159; Garcia-Closas, Montserrat1; Chatterjee, Nilanjan160,161
Organizations: 1NCI, Div Canc Epidemiol & Genet, Dept Hlth & Human Serv, Med Ctr Drive,NIH, Rockville, MD 20850 USA.
2Johns Hopkins Bloomberg Sch Publ Hlth, Dept Biostat, Baltimore, MD USA.
3Inst Neurol & Genet, Biostat Unit, Nicosia, Cyprus.
4Univ Cambridge, Ctr Canc Genet Epidemiol, Dept Publ Hlth & Primary Care, Cambridge, England.
5Cyprus Sch Mol Med, Inst Neurol & Genet, Nicosia, Cyprus.
6Canc Council Victoria, Canc Epidemiol Div, Melbourne, Vic, Australia.
7Univ Melbourne, Ctr Epidemiol & Biostat, Melbourne Sch Populat & Global Hlth, Melbourne, Vic, Australia.
8Monash Univ, Sch Clin Sci, Precis Med, Monash Hlth, Clayton, Vic, Australia.
9Univ Cambridge, Ctr Canc Genet Epidemiol, Dept Oncol, Cambridge, England.
10Mt Sinai Hosp, Fred A Litwin Ctr Canc Genet, Lunenfeld Tanenbaum Res Inst, Toronto, ON, Canada.
11Univ Toronto, Dept Mol Genet, Toronto, ON, Canada.
12Univ Calif Irvine, Dept Med, Genet Epidemiol Res Inst, Irvine, CA 92717 USA.
13German Canc Res Ctr, Div Clin Epidemiol & Aging Res, Heidelberg, Germany.
14Queens Univ, Dept Publ Hlth Sci, Kingston, ON, Canada.
15Queens Univ, Canc Res Inst, Kingston, ON, Canada.
16Fred Hutchinson Canc Res Ctr, Canc Prevent Program, 1124 Columbia St, Seattle, WA 98104 USA.
17Univ Wisconsin, Zilber Sch Publ Hlth, Milwaukee, WI 53201 USA.
18Lund Univ, Dept Canc Epidemiol, Clin Sci, Lund, Sweden.
19Univ Hosp Leuven, Leuven Multidisciplinary Breast Ctr, Leuven Canc Inst, Dept Oncol, Leuven, Belgium.
20Univ Med Ctr Hamburg Eppendorf, Inst Med Biometry & Epidemiol, Hamburg, Germany.
21German Canc Res Ctr, Div Canc Epidemiol, Heidelberg, Germany.
22Spanish Natl Canc Res Ctr CNIO, Human Canc Genet Programme, Madrid, Spain.
23Biomed Network Rare Dis CIBERER, Madrid, Spain.
24Russian Acad Sci, Inst Biochem & Genet, Ufa Fed Res Ctr, Ufa, Russia.
25St Petersburg State Univ, St Petersburg, Russia.
26Univ Helsinki, Helsinki Univ Hosp, Dept Oncol, Helsinki, Finland.
27Orebro Univ Hosp, Dept Oncol, Orebro, Sweden.
28Univ Copenhagen, Fac Hlth & Med Sci, Copenhagen, Denmark.
29Copenhagen Univ Hosp, Herlev & Gentofte Hosp, Dept Clin Biochem, Herlev, Denmark.
30Copenhagen Univ Hosp, Herlev & Gentofte Hosp, Copenhagen Gen Populat Study, Herlev, Denmark.
31European Inst Oncol IRCCS, Div Canc Prevent & Genet, IEO, Milan, Italy.
32Oslo Univ Hosp, Inst Canc Res, Dept Canc Genet, Radiumhosp, Oslo, Norway.
33Univ Oslo, Fac Med, Inst Clin Med, Oslo, Norway.
34Dr Margarete Fischer Bosch Inst Clin Pharmacol, Stuttgart, Germany.
35Univ Tubingen, iFIT Cluster Excellence, Tubingen, Germany.
36German Canc Consortium DKTK, German Canc Res Ctr DKFZ, Partner Site Tubingen, Tubingen, Germany.
37German Canc Consortium DKTK, German Canc Res Ctr DKFZ, Heidelberg, Germany.
38German Canc Res Ctr, Natl Ctr Tumor Dis NCT, Div Prevent Oncol, Heidelberg, Germany.
39BC Canc Agcy, Genome Sci Ctr, Vancouver, BC, Canada.
40Simon Fraser Univ, Dept Biomed Physiol & Kinesiol, Burnaby, BC, Canada.
41Ruhr Univ Bochum IPA, Inst Prevent & Occupa Tional Med, German Social Accid Insurance, Bochum, Germany.
42German Canc Res Ctr, Mol Epidemiol Grp, C080, Heidelberg, Germany.
43Heidelberg Univ, Univ Womens Clin Heidelberg, Mol Biol Breast Canc, Heidelberg, Germany.
44Huntsman Canc Inst, Dept Med, Salt Lake City, UT USA.
45German Canc Res Ctr, Genom Epidemiol Grp, Heidelberg, Germany.
46Xerencia Xest Integrada Vigo SERGAS, Oncol & Genet Unit, Inst Invest Sanitaria Galicia Sur IISGS, Vigo, Spain.
47Univ Med Ctr Hamburg Eppendorf, Univ Canc Ctr Hamburg UCCH, Canc Epidemiol Grp, Hamburg, Germany.
48QIMR Berghofer Med Res Inst, Dept Genet & Computat Biol, Brisbane, Qld, Australia.
49Univ Sydney, Westmead Inst Med Res, Sydney, NSW, Australia.
50Erasmus MC, Dept Clin Genet, Rotterdam, Netherlands.
51Univ Sheffield, Sheffield Inst Nucle Acids SInFoNiA, Dept Oncol & Metab, Sheffield, S Yorkshire, England.
52Univ Sheffield, Acad Unit Pathol, Dept Neurosci, Sheffield, S Yorkshire, England.
53Karolinska Inst, Dept Med Epidemiol & Biostat, Stockholm, Sweden.
54Fox Chase Canc Ctr, Dept Clin Genet, 7701 Burholme Ave, Philadelphia, PA 19111 USA.
55Leiden Univ Med Ctr, Dept Human Genet, Leiden, Netherlands.
56Leiden Univ Med Ctr, Dept Pathol, Leiden, Netherlands.
57Hannover Med Sch, Gynaecol Res Unit, Hannover, Germany.
58Univ Westminster, Sch Life Sci, London, England.
59Univ Southampton, Fac Med, Southampton, Hants, England.
60Manchester Univ NHS Fdn Trust, Manchester Acad Hlth Sci Ctr, Manchester Ctr Genom Med, North West Genom Lab Hub, Manchester, Lancs, England.
61Univ Manchester, Manchester Acad Hlth Sci Ctr, Fac Biol Med & Hlth, Sch Biol Sci,Div Evolut & Genom Sci, Manchester, Lancs, England.
62Friedrich Alexander Univ Erlangen Nuremberg, Univ Hosp Erlangen, Dept Gynecol & Obstet, Comprehens Canc Ctr Erlangen EMN, Erlangen, Germany.
63Univ Edinburgh, Usher Inst Populat Hlth Sci & Informat, Edinburgh, Midlothian, Scotland.
64Univ Edinburgh, Canc Res UK Edinburgh Ctr, Edinburgh, Midlothian, Scotland.
65Complejo Hosp Univ Santiago, Inst Invest Sanitaria Santiago de Compostela IDIS, Fdn Publ Galega Med Xenom, SERGAS, Santiago De Compostela, Spain.
66Univ Calif San Diego, Moores Canc Ctr, La Jolla, CA 92093 USA.
67Amer Canc Soc, Behav & Epidemiol Res Grp, Atlanta, GA 30329 USA.
68Hosp Clin San Carlos, Ctr Invest Biomed Red Canc CIBERONC, Inst Invest Sanitaria San Carlos IdISSC, Med Oncol Dept, Madrid, Spain.
69McGill Univ, Royal Victoria Hosp, Div Clin Epidemiol, Montreal, PQ, Canada.
70McGill Univ, Dept Med, Montreal, PQ, Canada.
71Univ Oulu, Oulu Univ Hosp, Dept Surg, Oulu, Finland.
72Univ Paris Saclay, Ctr Res Epidemiol & Populat Hlth CESP, INSERM, Team Exposome & Hered, Villejuif, France.
73Univ Southern Calif, Dept Prevent Med, Keck Sch Med, Los Angeles, CA 90007 USA.
74Soder Sjukhuset, Dept Oncol, Stockholm, Sweden.
75German Canc Res Ctr, Mol Genet Breast Canc, Heidelberg, Germany.
76Univ Manchester, Manchester Acad Hlth Sci Ctr, Fac Biol Med & Hlth, Div Informat Imaging & Data Sci, Manchester, Lancs, England.
77Manchester Univ NHS Fdn Trust, Wythenshawe Hosp, Nightingale & Genesis Prevent Ctr, Manchester, Lancs, England.
78Manchester Univ NHS Fdn Trust, Manchester Acad Hlth Sci Ctr, NIHR Manchester Biomed Res Unit, Manchester, Lancs, England.
79Erasmus MC Canc Inst, Dept Med Oncol, Rotterdam, Netherlands.
80Saarland Canc Registry, Saarbrucken, Germany.
81Univ Manchester, Div Canc Sci, Manchester, Lancs, England.
82MASA, Res Ctr Genet Engn & Biotechnol Georgi D Efremov, Skopje, North Macedonia.
83Pomeranian Med Univ, Dept Genet & Pathol, Szczecin, Poland.
84Pomeranian Med Univ, Independent Lab Mol Biol & Genet Diagnost, Szczecin, Poland.
85Stanford Univ, Dept Epidemiol & Populat Hlth, Sch Med, Stanford, CA 94305 USA.
86Stanford Univ, Stanford Canc Inst, Dept Med, Div Oncol,Sch Med, Stanford, CA 94305 USA.
87Inst Canc Res, Div Genet & Epidemiol, London, England.
88Univ Oulu, Oulu Univ Hosp, Depart Ment Pathol, Oulu, Finland.
89Antoni Van Leeuwenhoek Hosp, Div Mol Pathol, Netherlands Canc Inst, Amsterdam, Netherlands.
90Bashkir State Univ, Dept Genet & Fundamental Med, Ufa, Russia.
91NCI, Radiat Epidemiol Branch, Div Canc Epidemiol & Genet, Bethesda, MD 20892 USA.
92Johanniter Krankenhaus, Dept Internal Med, Johanniter Kliniken Bonn, Bonn, Germany.
93Oslo Univ Hosp, Dept Med Genet, Oslo, Norway.
94Univ Oslo, Oslo, Norway.
95Clin Hosp Acibadem Sistina, Dept Histopathol & Cytol, Skopje, North Macedonia.
96Cyprus Inst Neurol & Genet, Canc Genet Therapeut & Ultrastruct Pathol, Nicosia, Cyprus.
97Univ Leuven, Dept Human Genet, Lab Translat Genet, Leuven, Belgium.
98VIB Ctr Canc Biol, Leuven, Belgium.
99BC Canc, Canc Control Res, Vancouver, BC, Canada.
100St Francis Xavier Univ, Dept Math & Stat, Antigonish, NS, Canada.
101Karolinska Inst, Dept Mol Med & Surg, Stockholm, Sweden.
102Karolinska Univ Hosp, Dept Clin Genet, Stockholm, Sweden.
103M Sklodowska Curie Natl Res Inst Oncol, Dept Canc Epidemiol Ogy & Prevent, Warsaw, Poland.
104Hosp Univ Cent Asturias, Gen & Gastroenterol Surg Serv, Oviedo, Spain.
105Univ Tubingen, Tubingen, Germany.
106Univ Eastern Finland, Inst Clin Med Pathol & Forens Med, Kuopio, Finland.
107Univ Eastern Finland, Translat Canc Res Area, Kuopio, Finland.
108Kuopio Univ Hosp, Biobank Eastern Finland, Kuopio, Finland.
109Karolinska Inst, Dept Clin Sci & Educ, Sodersjukhuset Stockholm, Stockholm, Sweden.
110Alfred Hosp, Anat Pathol, Melbourne, Vic, Australia.
111Univ Munich, Dept Gynecol & Obstet, Campus Grosshadern, Munich, Germany.
112UCL, Inst Clin Trials & Methodol, London, England.
113Univ Helsinki, Helsinki Univ Hosp, Dept Obstet & Gynecol, Helsinki, Finland.
114Univ Calif San Diego, Herbert Wertheim Sch Publ Hlth & Human Longev Sci, La Jolla, CA 92093 USA.
115Mem Sloan Kettering Canc Ctr, Dept Canc Biol & Genet, Clin Genet Res Lab, 1275 York Ave, New York, NY 10021 USA.
116Queens Univ Belfast, Ctr Canc Res & Cell Biol, Belfast, North Ireland.
117Sch Hyg & Trop Med, Dept Noncommunicable Dis Epidemiol, London, England.
118Spanish Natl Canc Res Ctr, Human Genotyping CEGEN Unit, Human Canc Genet Program, Madrid, Spain.
119Univ Hosp Leuven, Leuven Canc Inst, Dept Gen Med Oncol, Leuven, Belgium.
120Univ Hosp Leuven, Multidisciplinary Breast Ctr, Leuven Canc Inst, Leuven, Belgium.
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154Uppsala Univ, Dept Surg Sci, Uppsala, Sweden.
155Mayo Clin, Dept Lab Med & Pathol, Rochester, MN USA.
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157Harvard TH Chan Sch Publ Hlth, Program Genet Epidemiol & Stat Genet, Boston, MA USA.
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Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 1.3 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe2022080953405
Language: English
Published: Springer Nature, 2022
Publish Date: 2022-08-09
Description:

Abstract

Background: Genome-wide association studies (GWAS) have identified multiple common breast cancer susceptibility variants. Many of these variants have differential associations by estrogen receptor (ER) status, but how these variants relate with other tumor features and intrinsic molecular subtypes is unclear.

Methods: Among 106,571 invasive breast cancer cases and 95,762 controls of European ancestry with data on 173 breast cancer variants identified in previous GWAS, we used novel two-stage polytomous logistic regression models to evaluate variants in relation to multiple tumor features (ER, progesterone receptor (PR), human epidermal growth factor receptor 2 (HER2) and grade) adjusting for each other, and to intrinsic-like subtypes.

Results: Eighty-five of 173 variants were associated with at least one tumor feature (false discovery rate < 5%), most commonly ER and grade, followed by PR and HER2. Models for intrinsic-like subtypes found nearly all of these variants (83 of 85) associated at p < 0.05 with risk for at least one luminal-like subtype, and approximately half (41 of 85) of the variants were associated with risk of at least one non-luminal subtype, including 32 variants associated with triple-negative (TN) disease. Ten variants were associated with risk of all subtypes in different magnitude. Five variants were associated with risk of luminal A-like and TN subtypes in opposite directions.

Conclusion: This report demonstrates a high level of complexity in the etiology heterogeneity of breast cancer susceptibility variants and can inform investigations of subtype-specific risk prediction.

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Series: Breast cancer research
ISSN: 1465-5411
ISSN-E: 1465-542X
ISSN-L: 1465-5411
Volume: 24
Issue: 1
Article number: 2
DOI: 10.1186/s13058-021-01484-x
OADOI: https://oadoi.org/10.1186/s13058-021-01484-x
Type of Publication: A1 Journal article – refereed
Field of Science: 3122 Cancers
Subjects:
Funding: Open Access funding provided by the National Institutes of Health (NIH) This project has been funded in part with Federal funds from the National Cancer Institute Intramural Research Program, National Institutes of Health. Dr. Nilanjan Chatterjee was supported by NHGRI Institute (1K99 CA256513). OncoArray genotyping was funded by the government of Canada through Genome Canada and the Canadian Institutes of Health Research (GPH-129344), the Ministere de l'Economie, de la Science et de l'Innovation du Quebec through Genome Quebec, the Quebec Breast Cancer Foundation for the PERSPECTIVE project, the US National Institutes of Health (NIH) (1 U19 CA 148065 for the Discovery, Biology and Risk of Inherited Variants in Breast Cancer (DRIVE) project and X01HG007492 to the Center for Inherited Disease Research (CIDR) under contract HHSN268201200008I), Cancer Research UK (C1287/A16563), the Odense University Hospital Research Foundation (Denmark), the National R&D Program for Cancer Control-Ministry of Health and Welfare (Republic of Korea) (1420190), the Italian Association for Cancer Research (AIRC; IG16933), the Breast Cancer Research Foundation, the National Health and Medical Research Council (Australia) and German Cancer Aid (110837). iCOGS genotyping was funded by the European Union and C12292/A11174]), NIH grants (CA128978, CA116167 and CA176785) and the Post-Cancer GWAS initiative (1U19 CA148537, 1U19 CA148065 and 1U19 CA148112 (GAME-ON initiative)), an NCI Specialized Program of Research Excellence (SPORE) in Breast Cancer (CA116201), the Canadian Institutes of Health Research (CIHR) for the CIHR Team in Familial Risks of Breast Cancer, the Ministere de l'Economie, Innovation et Exportation du Quebec Research Foundation and the Ovarian Cancer Research Fund. A full description of the funding is provided in the Additional file 4: Funding and Acknowledgement.
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