Meta-Analysis

. 2017 Jun 9:8:15724.

doi: 10.1038/ncomms15724.

Genome-wide association study identifies multiple risk loci for renal cell carcinoma

Ghislaine Scelo¹, Mark P Purdue², Kevin M Brown², Mattias Johansson¹, Zhaoming Wang³, Jeanette E Eckel-Passow⁴, Yuanqing Ye⁵, Jonathan N Hofmann², Jiyeon Choi², Matthieu Foll¹, Valerie Gaborieau¹, Mitchell J Machiela², Leandro M Colli², Peng Li¹, Joshua N Sampson², Behnoush Abedi-Ardekani¹, Celine Besse⁶, Helene Blanche⁷, Anne Boland⁶, Laurie Burdette², Amelie Chabrier¹, Geoffroy Durand¹, Florence Le Calvez-Kelm¹, Egor Prokhortchouk^{8

9}, Nivonirina Robinot¹, Konstantin G Skryabin^{8

9}, Magdalena B Wozniak¹, Meredith Yeager², Gordana Basta-Jovanovic¹⁰, Zoran Dzamic¹¹, Lenka Foretova¹², Ivana Holcatova¹³, Vladimir Janout¹⁴, Dana Mates¹⁵, Anush Mukeriya¹⁶, Stefan Rascu¹⁷, David Zaridze¹⁶, Vladimir Bencko¹⁸, Cezary Cybulski¹⁹, Eleonora Fabianova²⁰, Viorel Jinga¹⁷, Jolanta Lissowska²¹, Jan Lubinski¹⁹, Marie Navratilova¹², Peter Rudnai²², Neonila Szeszenia-Dabrowska²³, Simone Benhamou²⁴, Geraldine Cancel-Tassin^{25

26}, Olivier Cussenot^{25

26}, Laura Baglietto²⁷, Heiner Boeing²⁸, Kay-Tee Khaw²⁹, Elisabete Weiderpass^{30

31

32

33}, Borje Ljungberg³⁴, Raviprakash T Sitaram³⁴, Fiona Bruinsma³⁵, Susan J Jordan^{36

37}, Gianluca Severi^{27

35

38

39}, Ingrid Winship^{40

41}, Kristian Hveem⁴², Lars J Vatten⁴³, Tony Fletcher⁴⁴, Kvetoslava Koppova²⁰, Susanna C Larsson⁴⁵, Alicja Wolk⁴⁵, Rosamonde E Banks⁴⁶, Peter J Selby⁴⁶, Douglas F Easton^{29

47}, Paul Pharoah^{29

47}, Gabriella Andreotti², Laura E Beane Freeman², Stella Koutros², Demetrius Albanes², Satu Männistö⁴⁸, Stephanie Weinstein², Peter E Clark⁴⁹, Todd L Edwards⁵⁰, Loren Lipworth⁵¹, Susan M Gapstur⁵², Victoria L Stevens⁵², Hallie Carol⁵³, Matthew L Freedman⁵³, Mark M Pomerantz⁵³, Eunyoung Cho⁵⁴, Peter Kraft⁵⁵, Mark A Preston⁵⁶, Kathryn M Wilson⁵⁵, J Michael Gaziano⁵⁶, Howard D Sesso^{55

56}, Amanda Black², Neal D Freedman², Wen-Yi Huang², John G Anema⁵⁷, Richard J Kahnoski⁵⁷, Brian R Lane^{57

58}, Sabrina L Noyes⁵⁹, David Petillo⁵⁹, Bin Tean Teh⁵⁹, Ulrike Peters⁶⁰, Emily White⁶⁰, Garnet L Anderson⁶⁰, Lisa Johnson⁶⁰, Juhua Luo⁶¹, Julie Buring^{55

56}, I-Min Lee^{55

56}, Wong-Ho Chow⁵, Lee E Moore², Christopher Wood⁶², Timothy Eisen⁶³, Marc Henrion⁶⁴, James Larkin⁶⁵, Poulami Barman⁴, Bradley C Leibovich⁶⁶, Toni K Choueiri⁵³, G Mark Lathrop⁶⁷, Nathaniel Rothman², Jean-Francois Deleuze^{6

7}, James D McKay¹, Alexander S Parker⁶⁸, Xifeng Wu⁵, Richard S Houlston^{69

70}, Paul Brennan¹, Stephen J Chanock²

Affiliations

¹ International Agency for Research on Cancer (IARC), 69008 Lyon, France.
² Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department Health and Human Services, Bethesda, Maryland 20892, USA.
³ Department of Computational Biology, St Jude Children's Research Hospital, Memphis, Tennessee 38105, USA.
⁴ Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota 55905, USA.
⁵ Department of Epidemiology, Division of Cancer Prevention and Population Sciences, The University of Texas MD Anderson Cancer Center, Houston, Texas 77230, USA.
⁶ Centre National de Genotypage, Institut de Genomique, Commissariat à l'Energie Atomique et aux Energies Alternatives, 91057 Evry, France.
⁷ Fondation Jean Dausset-Centre d'Etude du Polymorphisme Humain, 75010 Paris, France.
⁸ Center 'Bioengineering' of the Russian Academy of Sciences, Moscow 117312, Russia.
⁹ Kurchatov Scientific Center, Moscow 123182, Russia.
¹⁰ Institute of Pathology, School of Medicine, University of Belgrade, 11000 Belgrade, Serbia.
¹¹ Clinical Center of Serbia (KCS), Clinic of Urology, University of Belgrade-Faculty of Medicine, 11000 Belgrade, Serbia.
¹² Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, 656 53 Brno, Czech Republic.
¹³ 2nd Faculty of Medicine, Institute of Public Health and Preventive Medicine, Charles University, 150 06 Prague 5, Czech Republic.
¹⁴ Department of Preventive Medicine, Faculty of Medicine, Palacky University, 775 15 Olomouc, Czech Republic.
¹⁵ National Institute of Public Health, 050463 Bucharest, Romania.
¹⁶ Russian N.N. Blokhin Cancer Research Centre, Moscow 115478, Russian Federation.
¹⁷ Carol Davila University of Medicine and Pharmacy, Th. Burghele Hospital, 050659 Bucharest, Romania.
¹⁸ First Faculty of Medicine, Institute of Hygiene and Epidemiology, Charles University, 128 00 Prague 2, Czech Republic.
¹⁹ International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, 70-204 Szczecin, Poland.
²⁰ Regional Authority of Public Health in Banska Bystrica, 975 56 Banska Bystrica, Slovakia.
²¹ The M Sklodowska-Curie Cancer Center and Institute of Oncology, 02-034 Warsaw, Poland.
²² National Public Health Center, National Directorate of Environmental Health, 1097 Budapest, Hungary.
²³ Department of Epidemiology, Institute of Occupational Medicine, 91-348 Lodz, Poland.
²⁴ Université Paris Diderot, INSERM, Unité Variabilité Génétique et Maladies Humaines, 75010 Paris, France.
²⁵ CeRePP, Tenon Hospital, 75020 Paris, France.
²⁶ UPMC Univ Paris 06 GRC n°5, 75013 Paris, France.
²⁷ Centre de Recherche en Épidémiologie et Santé des Populations (CESP, Inserm U1018), Université Paris-Saclay, UPS, UVSQ, Gustave Roussy, 94805 Villejuif, France.
²⁸ Department of Epidemiology, German Institute of Human Nutrition (DIfE) Potsdam-Rehbrücke, 14558 Nuthetal, Germany.
²⁹ Department of Public Health and Primary Care, University of Cambridge, Cambridge CB2 0QQ, UK.
³⁰ Department of Community Medicine, Faculty of Health Sciences, University of Tromsø, The Arctic University of Norway, 9037 Tromsø, Norway.
³¹ Department of Research, Cancer Registry of Norway, Institute of Population-Based Cancer Research, 0304 Oslo, Norway.
³² Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 171 77 Stockholm, Sweden.
³³ Genetic Epidemiology Group, Folkhälsan Research Center, 00250 Helsinki, Finland.
³⁴ Department of Surgical and Perioperative Sciences, Urology and Andrology, Umeå University, 901 85 Umeå, Sweden.
³⁵ Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria 3004, Australia.
³⁶ QIMR Berghofer Medical Research Institute, Herston, Queensland 4006, Australia.
³⁷ School of Public Health, The University of Queensland, Brisbane, Queensland 4072, Australia.
³⁸ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Carlton, Victoria 3053, Australia.
³⁹ Human Genetics Foundation (HuGeF), 10126 Torino, Italy.
⁴⁰ Department of Medicine, The University of Melbourne, Melbourne, Victoria 3010, Australia.
⁴¹ Genetic Medicine and Family Cancer Clinic, Royal Melbourne Hospital, Parkville, Victoria 3050, Australia.
⁴² HUNT Research Centre, Department of Public Health and General Practice, Norwegian University of Science and Technology, Levanger 7600, Norway.
⁴³ Department of Public Health and General Practice, Faculty of Medicine, Norwegian University of Science and Technology, Trondheim 7491, Norway.
⁴⁴ London School of Hygiene and Tropical Medicine, University of London, London WC1H 9SH, UK.
⁴⁵ Institute of Environmental Medicine, Karolinska Institutet, 171 77 Stockholm, Sweden.
⁴⁶ Leeds Institute of Cancer and Pathology, University of Leeds, Cancer Research Building, St James's University Hospital, Leeds LS9 7TF, UK.
⁴⁷ Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.
⁴⁸ Department of Health, National Institute for Health and Welfare, 00271 Helsinki, Finland.
⁴⁹ Vanderbilt-Ingram Cancer Center, Department of Urology, Vanderbilt University Medical Center, Nashville, Tennessee 37232, USA.
⁵⁰ Vanderbilt-Ingram Cancer Center, Division of Epidemiology, Department of Medicine, Institute for Medicine and Public Health, Vanderbilt Genetics Institute, Vanderbilt University Medical Center, Nashville, Tennessee 37209, USA.
⁵¹ Vanderbilt-Ingram Cancer Center, Division of Epidemiology, Department of Medicine, Institute for Medicine and Public Health, Vanderbilt University Medical Center, Nashville, Tennessee 37203, USA.
⁵² American Cancer Society, Atlanta, Georgia 30303, USA.
⁵³ Dana-Farber Cancer Institute, Boston, Massachusetts 02215, USA.
⁵⁴ Warren Alpert Medical School of Brown University, Providence, Rhode Island 02903, USA.
⁵⁵ Harvard T.H. Chan School of Public Health, Boston, Massachusetts 02115, USA.
⁵⁶ Brigham and Women's Hospital and VA Boston, Boston, Massachusetts 02115, USA.
⁵⁷ Division of Urology, Spectrum Health, Grand Rapids, Michigan 49503, USA.
⁵⁸ College of Human Medicine, Michigan State University, Grand Rapids, Michigan 49503, USA.
⁵⁹ Van Andel Research Institute, Center for Cancer Genomics and Quantitative Biology, Grand Rapids, Michigan 49503, USA.
⁶⁰ Cancer Prevention Program, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA.
⁶¹ Department of Epidemiology and Biostatistics, School of Public Health Indiana University Bloomington, Bloomington, Indiana 47405, USA.
⁶² Department of Urology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas 77030, USA.
⁶³ Department of Oncology, Cambridge University Hospitals NHS Foundation Trust, Cambridge CB2 0QQ, UK.
⁶⁴ Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, New York 10029, USA.
⁶⁵ Medical Oncology, Royal Marsden NHS Foundation Trust, London SW3 6JJ, UK.
⁶⁶ Department of Urology, Mayo Medical School and Mayo Clinic, Rochester, Minnesota 55902, USA.
⁶⁷ McGill University and Genome Quebec Innovation Centre, Montreal, Quebec, Canada H3A 0G1.
⁶⁸ Department of Health Sciences Research, Mayo Clinic, Jacksonville, Florida 32224, USA.
⁶⁹ Division of Genetics and Epidemiology, The Institute of Cancer Research, London SW7 3RP, UK.
⁷⁰ Division of Molecular Pathology, The Institute of Cancer Research, London SW7 3RP, UK.

PMID: 28598434
PMCID: PMC5472706
DOI: 10.1038/ncomms15724

Meta-Analysis

Genome-wide association study identifies multiple risk loci for renal cell carcinoma

Ghislaine Scelo et al. Nat Commun. 2017.

. 2017 Jun 9:8:15724.

doi: 10.1038/ncomms15724.

Authors

Affiliations

¹ International Agency for Research on Cancer (IARC), 69008 Lyon, France.
² Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department Health and Human Services, Bethesda, Maryland 20892, USA.
³ Department of Computational Biology, St Jude Children's Research Hospital, Memphis, Tennessee 38105, USA.
⁴ Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota 55905, USA.
⁵ Department of Epidemiology, Division of Cancer Prevention and Population Sciences, The University of Texas MD Anderson Cancer Center, Houston, Texas 77230, USA.
⁶ Centre National de Genotypage, Institut de Genomique, Commissariat à l'Energie Atomique et aux Energies Alternatives, 91057 Evry, France.
⁷ Fondation Jean Dausset-Centre d'Etude du Polymorphisme Humain, 75010 Paris, France.
⁸ Center 'Bioengineering' of the Russian Academy of Sciences, Moscow 117312, Russia.
⁹ Kurchatov Scientific Center, Moscow 123182, Russia.
¹⁰ Institute of Pathology, School of Medicine, University of Belgrade, 11000 Belgrade, Serbia.
¹¹ Clinical Center of Serbia (KCS), Clinic of Urology, University of Belgrade-Faculty of Medicine, 11000 Belgrade, Serbia.
¹² Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, 656 53 Brno, Czech Republic.
¹³ 2nd Faculty of Medicine, Institute of Public Health and Preventive Medicine, Charles University, 150 06 Prague 5, Czech Republic.
¹⁴ Department of Preventive Medicine, Faculty of Medicine, Palacky University, 775 15 Olomouc, Czech Republic.
¹⁵ National Institute of Public Health, 050463 Bucharest, Romania.
¹⁶ Russian N.N. Blokhin Cancer Research Centre, Moscow 115478, Russian Federation.
¹⁷ Carol Davila University of Medicine and Pharmacy, Th. Burghele Hospital, 050659 Bucharest, Romania.
¹⁸ First Faculty of Medicine, Institute of Hygiene and Epidemiology, Charles University, 128 00 Prague 2, Czech Republic.
¹⁹ International Hereditary Cancer Center, Department of Genetics and Pathology, Pomeranian Medical University, 70-204 Szczecin, Poland.
²⁰ Regional Authority of Public Health in Banska Bystrica, 975 56 Banska Bystrica, Slovakia.
²¹ The M Sklodowska-Curie Cancer Center and Institute of Oncology, 02-034 Warsaw, Poland.
²² National Public Health Center, National Directorate of Environmental Health, 1097 Budapest, Hungary.
²³ Department of Epidemiology, Institute of Occupational Medicine, 91-348 Lodz, Poland.
²⁴ Université Paris Diderot, INSERM, Unité Variabilité Génétique et Maladies Humaines, 75010 Paris, France.
²⁵ CeRePP, Tenon Hospital, 75020 Paris, France.
²⁶ UPMC Univ Paris 06 GRC n°5, 75013 Paris, France.
²⁷ Centre de Recherche en Épidémiologie et Santé des Populations (CESP, Inserm U1018), Université Paris-Saclay, UPS, UVSQ, Gustave Roussy, 94805 Villejuif, France.
²⁸ Department of Epidemiology, German Institute of Human Nutrition (DIfE) Potsdam-Rehbrücke, 14558 Nuthetal, Germany.
²⁹ Department of Public Health and Primary Care, University of Cambridge, Cambridge CB2 0QQ, UK.
³⁰ Department of Community Medicine, Faculty of Health Sciences, University of Tromsø, The Arctic University of Norway, 9037 Tromsø, Norway.
³¹ Department of Research, Cancer Registry of Norway, Institute of Population-Based Cancer Research, 0304 Oslo, Norway.
³² Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, 171 77 Stockholm, Sweden.
³³ Genetic Epidemiology Group, Folkhälsan Research Center, 00250 Helsinki, Finland.
³⁴ Department of Surgical and Perioperative Sciences, Urology and Andrology, Umeå University, 901 85 Umeå, Sweden.
³⁵ Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Victoria 3004, Australia.
³⁶ QIMR Berghofer Medical Research Institute, Herston, Queensland 4006, Australia.
³⁷ School of Public Health, The University of Queensland, Brisbane, Queensland 4072, Australia.
³⁸ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Carlton, Victoria 3053, Australia.
³⁹ Human Genetics Foundation (HuGeF), 10126 Torino, Italy.
⁴⁰ Department of Medicine, The University of Melbourne, Melbourne, Victoria 3010, Australia.
⁴¹ Genetic Medicine and Family Cancer Clinic, Royal Melbourne Hospital, Parkville, Victoria 3050, Australia.
⁴² HUNT Research Centre, Department of Public Health and General Practice, Norwegian University of Science and Technology, Levanger 7600, Norway.
⁴³ Department of Public Health and General Practice, Faculty of Medicine, Norwegian University of Science and Technology, Trondheim 7491, Norway.
⁴⁴ London School of Hygiene and Tropical Medicine, University of London, London WC1H 9SH, UK.
⁴⁵ Institute of Environmental Medicine, Karolinska Institutet, 171 77 Stockholm, Sweden.
⁴⁶ Leeds Institute of Cancer and Pathology, University of Leeds, Cancer Research Building, St James's University Hospital, Leeds LS9 7TF, UK.
⁴⁷ Department of Oncology, University of Cambridge, Cambridge CB1 8RN, UK.
⁴⁸ Department of Health, National Institute for Health and Welfare, 00271 Helsinki, Finland.
⁴⁹ Vanderbilt-Ingram Cancer Center, Department of Urology, Vanderbilt University Medical Center, Nashville, Tennessee 37232, USA.
⁵⁰ Vanderbilt-Ingram Cancer Center, Division of Epidemiology, Department of Medicine, Institute for Medicine and Public Health, Vanderbilt Genetics Institute, Vanderbilt University Medical Center, Nashville, Tennessee 37209, USA.
⁵¹ Vanderbilt-Ingram Cancer Center, Division of Epidemiology, Department of Medicine, Institute for Medicine and Public Health, Vanderbilt University Medical Center, Nashville, Tennessee 37203, USA.
⁵² American Cancer Society, Atlanta, Georgia 30303, USA.
⁵³ Dana-Farber Cancer Institute, Boston, Massachusetts 02215, USA.
⁵⁴ Warren Alpert Medical School of Brown University, Providence, Rhode Island 02903, USA.
⁵⁵ Harvard T.H. Chan School of Public Health, Boston, Massachusetts 02115, USA.
⁵⁶ Brigham and Women's Hospital and VA Boston, Boston, Massachusetts 02115, USA.
⁵⁷ Division of Urology, Spectrum Health, Grand Rapids, Michigan 49503, USA.
⁵⁸ College of Human Medicine, Michigan State University, Grand Rapids, Michigan 49503, USA.
⁵⁹ Van Andel Research Institute, Center for Cancer Genomics and Quantitative Biology, Grand Rapids, Michigan 49503, USA.
⁶⁰ Cancer Prevention Program, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA.
⁶¹ Department of Epidemiology and Biostatistics, School of Public Health Indiana University Bloomington, Bloomington, Indiana 47405, USA.
⁶² Department of Urology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas 77030, USA.
⁶³ Department of Oncology, Cambridge University Hospitals NHS Foundation Trust, Cambridge CB2 0QQ, UK.
⁶⁴ Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, New York 10029, USA.
⁶⁵ Medical Oncology, Royal Marsden NHS Foundation Trust, London SW3 6JJ, UK.
⁶⁶ Department of Urology, Mayo Medical School and Mayo Clinic, Rochester, Minnesota 55902, USA.
⁶⁷ McGill University and Genome Quebec Innovation Centre, Montreal, Quebec, Canada H3A 0G1.
⁶⁸ Department of Health Sciences Research, Mayo Clinic, Jacksonville, Florida 32224, USA.
⁶⁹ Division of Genetics and Epidemiology, The Institute of Cancer Research, London SW7 3RP, UK.
⁷⁰ Division of Molecular Pathology, The Institute of Cancer Research, London SW7 3RP, UK.

PMID: 28598434
PMCID: PMC5472706
DOI: 10.1038/ncomms15724

Abstract

Previous genome-wide association studies (GWAS) have identified six risk loci for renal cell carcinoma (RCC). We conducted a meta-analysis of two new scans of 5,198 cases and 7,331 controls together with four existing scans, totalling 10,784 cases and 20,406 controls of European ancestry. Twenty-four loci were tested in an additional 3,182 cases and 6,301 controls. We confirm the six known RCC risk loci and identify seven new loci at 1p32.3 (rs4381241, P=3.1 × 10^-10), 3p22.1 (rs67311347, P=2.5 × 10^-8), 3q26.2 (rs10936602, P=8.8 × 10^-9), 8p21.3 (rs2241261, P=5.8 × 10^-9), 10q24.33-q25.1 (rs11813268, P=3.9 × 10^-8), 11q22.3 (rs74911261, P=2.1 × 10^-10) and 14q24.2 (rs4903064, P=2.2 × 10^-24). Expression quantitative trait analyses suggest plausible candidate genes at these regions that may contribute to RCC susceptibility.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing financial interests.

Figures

**Figure 1. Overview of the study design.**
The six genotyping scans contributing to the meta-analysis are detailed on the left, with number of cases and controls and arrays used for the genotyping. The meta-analysis was performed after imputations on 7,437,091 SNPs. Boxes in italic bold represent genotype data newly generated for this study.

**Figure 2. Plots of eQTL association between rs4903064 and DPF3 expression.**
(a) TCGA-KIRC normal, (b) TCGA-KIRC tumour, (c) IARC normal, and (d) IARC tumour sample data sets. Box boundaries designate the twenty-fifth and seventy-fifth percentiles, black line in the centre of boxes represent the median, whiskers extend to the minimum of either the data range or 1.5 times the interquartile range and statistical outliers are plotted as points.

See this image and copyright information in PMC

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Genome-wide association study identifies multiple risk loci for renal cell carcinoma

Affiliations

Genome-wide association study identifies multiple risk loci for renal cell carcinoma

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical

Molecular Biology Databases