Beyond GWAS of Colorectal Cancer: Evidence of Interaction with Alcohol Consumption and Putative Causal Variant for the 10q24.2 Region.


Journal

Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology
ISSN: 1538-7755
Titre abrégé: Cancer Epidemiol Biomarkers Prev
Pays: United States
ID NLM: 9200608

Informations de publication

Date de publication:
04 05 2022
Historique:
received: 20 08 2021
revised: 30 10 2021
accepted: 15 02 2022
pubmed: 20 4 2022
medline: 6 5 2022
entrez: 19 4 2022
Statut: ppublish

Résumé

Currently known associations between common genetic variants and colorectal cancer explain less than half of its heritability of 25%. As alcohol consumption has a J-shape association with colorectal cancer risk, nondrinking and heavy drinking are both risk factors for colorectal cancer. Individual-level data was pooled from the Colon Cancer Family Registry, Colorectal Transdisciplinary Study, and Genetics and Epidemiology of Colorectal Cancer Consortium to compare nondrinkers (≤1 g/day) and heavy drinkers (>28 g/day) with light-to-moderate drinkers (1-28 g/day) in GxE analyses. To improve power, we implemented joint 2df and 3df tests and a novel two-step method that modifies the weighted hypothesis testing framework. We prioritized putative causal variants by predicting allelic effects using support vector machine models. For nondrinking as compared with light-to-moderate drinking, the hybrid two-step approach identified 13 significant SNPs with pairwise r2 > 0.9 in the 10q24.2/COX15 region. When stratified by alcohol intake, the A allele of lead SNP rs2300985 has a dose-response increase in risk of colorectal cancer as compared with the G allele in light-to-moderate drinkers [OR for GA genotype = 1.11; 95% confidence interval (CI), 1.06-1.17; OR for AA genotype = 1.22; 95% CI, 1.14-1.31], but not in nondrinkers or heavy drinkers. Among the correlated candidate SNPs in the 10q24.2/COX15 region, rs1318920 was predicted to disrupt an HNF4 transcription factor binding motif. Our study suggests that the association with colorectal cancer in 10q24.2/COX15 observed in genome-wide association study is strongest in nondrinkers. We also identified rs1318920 as the putative causal regulatory variant for the region. The study identifies multifaceted evidence of a possible functional effect for rs1318920.

Sections du résumé

BACKGROUND
Currently known associations between common genetic variants and colorectal cancer explain less than half of its heritability of 25%. As alcohol consumption has a J-shape association with colorectal cancer risk, nondrinking and heavy drinking are both risk factors for colorectal cancer.
METHODS
Individual-level data was pooled from the Colon Cancer Family Registry, Colorectal Transdisciplinary Study, and Genetics and Epidemiology of Colorectal Cancer Consortium to compare nondrinkers (≤1 g/day) and heavy drinkers (>28 g/day) with light-to-moderate drinkers (1-28 g/day) in GxE analyses. To improve power, we implemented joint 2df and 3df tests and a novel two-step method that modifies the weighted hypothesis testing framework. We prioritized putative causal variants by predicting allelic effects using support vector machine models.
RESULTS
For nondrinking as compared with light-to-moderate drinking, the hybrid two-step approach identified 13 significant SNPs with pairwise r2 > 0.9 in the 10q24.2/COX15 region. When stratified by alcohol intake, the A allele of lead SNP rs2300985 has a dose-response increase in risk of colorectal cancer as compared with the G allele in light-to-moderate drinkers [OR for GA genotype = 1.11; 95% confidence interval (CI), 1.06-1.17; OR for AA genotype = 1.22; 95% CI, 1.14-1.31], but not in nondrinkers or heavy drinkers. Among the correlated candidate SNPs in the 10q24.2/COX15 region, rs1318920 was predicted to disrupt an HNF4 transcription factor binding motif.
CONCLUSIONS
Our study suggests that the association with colorectal cancer in 10q24.2/COX15 observed in genome-wide association study is strongest in nondrinkers. We also identified rs1318920 as the putative causal regulatory variant for the region.
IMPACT
The study identifies multifaceted evidence of a possible functional effect for rs1318920.

Identifiants

pubmed: 35438744
pii: 694506
doi: 10.1158/1055-9965.EPI-21-1003
pmc: PMC9081195
mid: NIHMS1783982
doi:

Substances chimiques

COX15 protein, human EC 1.9.3.1
Electron Transport Complex IV EC 1.9.3.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1077-1089

Subventions

Organisme : NCI NIH HHS
ID : R01 CA059045
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES010126
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA182883
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA137088
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA164930
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA206110
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA201407
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA196569
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA206279
Pays : United States
Organisme : NCI NIH HHS
ID : UG1 CA189974
Pays : United States

Informations de copyright

©2022 American Association for Cancer Research.

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Auteurs

Kristina M Jordahl (KM)

Department of Epidemiology, School of Public Health, University of Washington, Seattle, Washington.
Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Anna Shcherbina (A)

Department of Genetics, Stanford University, Stanford, California.
Department of Computer Science, Stanford University, Stanford, California.

Andre E Kim (AE)

Division of Biostatistics, Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.

Yu-Ru Su (YR)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Yi Lin (Y)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Jun Wang (J)

Division of Biostatistics, Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.

Conghui Qu (C)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Demetrius Albanes (D)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.

Volker Arndt (V)

Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.

James W Baurley (JW)

Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.
BioRealm LLC, Walnut, California.

Sonja I Berndt (SI)

Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.

Stephanie A Bien (SA)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

D Timothy Bishop (DT)

Leeds Institute of Cancer and Pathology, University of Leeds, Leeds, United Kingdom.

Emmanouil Bouras (E)

Department of Hygiene and Epidemiology, University of Ioannina School of Medicine, Ioannina, Greece.

Hermann Brenner (H)

Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Division of Preventive Oncology, German Cancer Research Center (DKFZ) and National Center for Tumor Diseases (NCT), Heidelberg, Germany.
German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Daniel D Buchanan (DD)

Colorectal Oncogenomics Group, Department of Clinical Pathology, The University of Melbourne, Parkville, Victoria, Australia.
University of Melbourne Centre for Cancer Research, Victorian Comprehensive Cancer Centre, Parkville, Victoria, Australia.
Genetic Medicine and Family Cancer Clinic, The Royal Melbourne Hospital, Parkville, Victoria, Australia.

Arif Budiarto (A)

Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.
Computer Science Department, School of Computer Science, Bina Nusantara University, Jakarta, Indonesia.

Peter T Campbell (PT)

Behavioral and Epidemiology Research Group, American Cancer Society, Atlanta, Georgia.

Robert Carreras-Torres (R)

Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.

Graham Casey (G)

Center for Public Health Genomics, University of Virginia, Charlottesville, Virginia.

Tjeng Wawan Cenggoro (TW)

Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.

Andrew T Chan (AT)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.
Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.
Broad Institute of Harvard and MIT, Cambridge, Massachusetts.
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts.
Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts.

David V Conti (DV)

Department of Preventive Medicine and USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California.

Christopher H Dampier (CH)

Center for Public Health Genomics, University of Virginia, Charlottesville, Virginia.

Matthew A Devall (MA)

Center for Public Health Genomics, University of Virginia, Charlottesville, Virginia.

Virginia Díez-Obrero (V)

Colorectal Cancer Group, ONCOBELL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.
Oncology Data Analytics Program, Catalan Institute of Oncology-IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.
Consortium for Biomedical Research in Epidemiology and Public Health (CIBERESP), Madrid, Spain.
Department of Clinical Sciences, Faculty of Medicine, University of Barcelona, Barcelona, Spain.

Niki Dimou (N)

Section of Nutrition and Metabolism, International Agency for Research on Cancer, Lyon, France.

David A Drew (DA)

Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

Jane C Figueiredo (JC)

Department of Medicine, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, California.
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.

Steven Gallinger (S)

Lunenfeld Tanenbaum Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada.

Graham G Giles (GG)

Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Victoria, Australia.
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.
Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.

Stephen B Gruber (SB)

Department of Preventive Medicine and USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California.

Andrea Gsur (A)

Institute of Cancer Research, Department of Medicine I, Medical University Vienna, Vienna, Austria.

Marc J Gunter (MJ)

Nutrition and Metabolism Section, International Agency for Research on Cancer, World Health Organization, Lyon, France.

Heather Hampel (H)

Division of Human Genetics, Department of Internal Medicine, The Ohio State University Comprehensive Cancer Center, Columbus, Ohio.

Sophia Harlid (S)

Department of Radiation Sciences, Oncology Unit, Umeå University, Umeå, Sweden.

Tabitha A Harrison (TA)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Akihisa Hidaka (A)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Michael Hoffmeister (M)

Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Jeroen R Huyghe (JR)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Mark A Jenkins (MA)

Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Victoria, Australia.

Amit D Joshi (AD)

Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts.

Temitope O Keku (TO)

Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, North Carolina.

Susanna C Larsson (SC)

Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

Loic Le Marchand (L)

University of Hawaii Cancer Center, Honolulu, Hawaii.

Juan Pablo Lewinger (JP)

Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.

Li Li (L)

Department of Family Medicine, University of Virginia, Charlottesville, Virginia.

Bharuno Mahesworo (B)

Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.

Victor Moreno (V)

Oncology Data Analytics Program, Catalan Institute of Oncology-IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.
Department of Clinical Sciences, Faculty of Medicine, University of Barcelona, Barcelona, Spain.
CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
ONCOBEL Program, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.

John L Morrison (JL)

Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.

Neil Murphy (N)

Nutrition and Metabolism Section, International Agency for Research on Cancer, World Health Organization, Lyon, France.

Hongmei Nan (H)

Department of Epidemiology, Richard M. Fairbanks School of Public Health, Indianapolis, Indiana.
IU Melvin and Bren Simon Cancer Center, Indiana University, Indianapolis, Indiana.

Rami Nassir (R)

Department of Pathology, School of Medicine, Umm Al-Qura'a University, Saudi Arabia.

Polly A Newcomb (PA)

Department of Epidemiology, School of Public Health, University of Washington, Seattle, Washington.
Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Mireia Obón-Santacana (M)

Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO-IDIBELL), Avda Gran Via Barcelona 199-203, 08908L'Hospitalet de Llobregat, Barcelona, Spain.

Shuji Ogino (S)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts.
Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital, Boston, Massachusetts.
Harvard Medical School, Boston, Massachusetts.
Broad Institute of MIT and Harvard, Cambridge, Massachusetts.

Jennifer Ose (J)

Huntsman Cancer Institute, University of Utah, Salt Lake City, Utah.
Department of Population Health Sciences, University of Utah, Salt Lake City, Utah.

Rish K Pai (RK)

Department of Laboratory Medicine and Pathology, Mayo Clinic Arizona, Scottsdale, Arizona.

Julie R Palmer (JR)

Slone Epidemiology Center at Boston University, Boston, Massachusetts.

Nikos Papadimitriou (N)

Section of Nutrition and Metabolism, International Agency for Research on Cancer, Lyon, France.

Bens Pardamean (B)

Bioinformatics and Data Science Research Center, Bina Nusantara University, Jakarta, Indonesia.

Anita R Peoples (AR)

Department of Population Health Sciences, University of Utah, Salt Lake City, Utah.
Huntsman Cancer Institute, Salt Lake City, Utah.

Paul D P Pharoah (PDP)

Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.

Elizabeth A Platz (EA)

Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland.

John D Potter (JD)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Ross L Prentice (RL)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Gad Rennert (G)

Department of Community Medicine and Epidemiology, Lady Davis Carmel Medical Center, Haifa, Israel.
Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel.
Clalit National Cancer Control Center, Haifa, Israel.

Edward Ruiz-Narvaez (E)

Department of Nutritional Sciences, University of Michigan School of Public Health, Ann Arbor, Michigan.

Lori C Sakoda (LC)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.
Division of Research, Kaiser Permanente Northern California, Oakland, California.

Peter C Scacheri (PC)

Department of Genetics and Genome Sciences, Case Western Reserve University, Cleveland, Ohio.

Stephanie L Schmit (SL)

Genomic Medicine Institute, Cleveland Clinic, Cleveland, Ohio.
Population and Cancer Prevention Program, Case Comprehensive Cancer Center, Cleveland, Ohio.

Robert E Schoen (RE)

Department of Medicine and Epidemiology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania.

Martha L Slattery (ML)

Department of Internal Medicine, University of Utah, Salt Lake City, Utah.

Mariana C Stern (MC)

Department of Preventive Medicine and USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California.

Catherine M Tangen (CM)

SWOG Statistical Center, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Stephen N Thibodeau (SN)

Division of Laboratory Genetics, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota.

Duncan C Thomas (DC)

Department of Preventive Medicine and USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California.

Yu Tian (Y)

Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
School of Public Health, Capital Medical University, Beijing, China.

Konstantinos K Tsilidis (KK)

Department of Hygiene and Epidemiology, University of Ioannina School of Medicine, Ioannina, Greece.
Department of Epidemiology and Biostatistics, Imperial College London, School of Public Health, London, United Kingdom.

Cornelia M Ulrich (CM)

Department of Population Health Sciences, University of Utah, Salt Lake City, Utah.
Huntsman Cancer Institute, Salt Lake City, Utah.

Franzel J B van Duijnhoven (FJB)

Division of Human Nutrition and Health, Wageningen University & Research, Wageningen, the Netherlands.

Bethany Van Guelpen (B)

Department of Radiation Sciences, Oncology Unit, Umeå University, Umeå, Sweden.
Wallenberg Centre for Molecular Medicine, Umeå University, Umeå, Sweden.

Kala Visvanathan (K)

Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland.

Pavel Vodicka (P)

Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic.
Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.
Faculty of Medicine and Biomedical Center in Pilsen, Charles University, Pilsen, Czech Republic.

Emily White (E)

Department of Epidemiology, School of Public Health, University of Washington, Seattle, Washington.
Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Alicja Wolk (A)

Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

Michael O Woods (MO)

Memorial University of Newfoundland, Discipline of Genetics, St. John's, Canada.

Anna H Wu (AH)

Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.

Natalia Zemlianskaia (N)

Department of Preventive Medicine and USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California.

Jenny Chang-Claude (J)

Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
University Medical Centre Hamburg-Eppendorf, University Cancer Centre Hamburg (UCCH), Hamburg, Germany.

W James Gauderman (WJ)

Department of Preventive Medicine and USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, California.

Li Hsu (L)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.
Department of Biostatistics, University of Washington, Seattle, Washington.

Anshul Kundaje (A)

Department of Genetics, Stanford University, Stanford, California.
Department of Computer Science, Stanford University, Stanford, California.

Ulrike Peters (U)

Department of Epidemiology, School of Public Health, University of Washington, Seattle, Washington.
Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

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