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Fine-mapping analysis including over 254,000 East Asian and European descendants identifies 136 putative colorectal cancer susceptibility genes

Author

Listed:
  • Zhishan Chen

    (Vanderbilt University Medical Center)

  • Xingyi Guo

    (Vanderbilt University Medical Center
    Vanderbilt University School of Medicine)

  • Ran Tao

    (Vanderbilt University Medical Center
    Vanderbilt University Medical Center)

  • Jeroen R. Huyghe

    (Fred Hutchinson Cancer Center)

  • Philip J. Law

    (Institute of Cancer Research)

  • Ceres Fernandez-Rozadilla

    (University of Edinburgh
    Instituto de Investigacion Sanitaria de Santiago)

  • Jie Ping

    (Vanderbilt University Medical Center)

  • Guochong Jia

    (Vanderbilt University Medical Center)

  • Jirong Long

    (Vanderbilt University Medical Center)

  • Chao Li

    (Vanderbilt University Medical Center)

  • Quanhu Shen

    (Vanderbilt University Medical Center)

  • Yuhan Xie

    (Yale School of Public Health)

  • Maria N. Timofeeva

    (University of Edinburgh
    University of Southern Denmark)

  • Minta Thomas

    (Fred Hutchinson Cancer Center)

  • Stephanie L. Schmit

    (Cleveland Clinic
    Case Comprehensive Cancer Center)

  • Virginia Díez-Obrero

    (Bellvitge Biomedical Research Institute
    Consortium for Biomedical Research in Epidemiology and Public Health
    University of Barcelona
    Catalan Institute of Oncology)

  • Matthew Devall

    (University of Virginia)

  • Ferran Moratalla-Navarro

    (Bellvitge Biomedical Research Institute
    Consortium for Biomedical Research in Epidemiology and Public Health
    University of Barcelona
    Catalan Institute of Oncology)

  • Juan Fernandez-Tajes

    (University of Edinburgh)

  • Claire Palles

    (University of Birmingham)

  • Kitty Sherwood

    (University of Edinburgh)

  • Sarah E. W. Briggs

    (University of Oxford)

  • Victoria Svinti

    (University of Edinburgh)

  • Kevin Donnelly

    (University of Edinburgh)

  • Susan M. Farrington

    (University of Edinburgh)

  • James Blackmur

    (University of Edinburgh)

  • Peter G. Vaughan-Shaw

    (University of Edinburgh)

  • Xiao-Ou Shu

    (Vanderbilt University Medical Center)

  • Yingchang Lu

    (Vanderbilt University Medical Center)

  • Peter Broderick

    (Institute of Cancer Research)

  • James Studd

    (Institute of Cancer Research)

  • Tabitha A. Harrison

    (Fred Hutchinson Cancer Center)

  • David V. Conti

    (University of Southern California)

  • Fredrick R. Schumacher

    (Case Western Reserve University
    Case Western Reserve University)

  • Marilena Melas

    (Nationwide Children’s Hospital)

  • Gad Rennert

    (Clalit National Cancer Control Center
    Lady Davis Carmel Medical Center
    Technion-Israel Institute of Technology)

  • Mireia Obón-Santacana

    (Bellvitge Biomedical Research Institute
    Consortium for Biomedical Research in Epidemiology and Public Health
    Catalan Institute of Oncology)

  • Vicente Martín-Sánchez

    (Consortium for Biomedical Research in Epidemiology and Public Health
    University of León)

  • Jae Hwan Oh

    (National Cancer Center)

  • Jeongseon Kim

    (National Cancer Center)

  • Sun Ha Jee

    (Yonsei University)

  • Keum Ji Jung

    (Yonsei University)

  • Sun-Seog Kweon

    (Chonnam National University Medical School)

  • Min-Ho Shin

    (Chonnam National University Medical School)

  • Aesun Shin

    (Seoul National University
    Seoul National University College of Medicine)

  • Yoon-Ok Ahn

    (Seoul National University College of Medicine)

  • Dong-Hyun Kim

    (Hallym University College of Medicine)

  • Isao Oze

    (Aichi Cancer Center Research Institute)

  • Wanqing Wen

    (Vanderbilt University Medical Center)

  • Keitaro Matsuo

    (Nagoya University Graduate School of Medicine
    Aichi Cancer Center Research Institute)

  • Koichi Matsuda

    (University of Tokyo)

  • Chizu Tanikawa

    (University of Tokyo)

  • Zefang Ren

    (Sun Yat-sen University)

  • Yu-Tang Gao

    (Shanghai Jiaotong University School of Medicine)

  • Wei-Hua Jia

    (Sun Yat-sen University)

  • John L. Hopper

    (University of Melbourne
    Seoul National University)

  • Mark A. Jenkins

    (University of Melbourne)

  • Aung Ko Win

    (University of Melbourne)

  • Rish K. Pai

    (Mayo Clinic Arizona)

  • Jane C. Figueiredo

    (University of Southern California
    Cedars-Sinai Medical Center)

  • Robert W. Haile

    (Cedars-Sinai Cancer Research Center for Health Equity)

  • Steven Gallinger

    (University of Toronto)

  • Michael O. Woods

    (Memorial University of Newfoundland)

  • Polly A. Newcomb

    (Fred Hutchinson Cancer Center
    University of Washington)

  • David Duggan

    (Translational Genomics Research Institute)

  • Jeremy P. Cheadle

    (Cardiff University)

  • Richard Kaplan

    (Medical Research Council)

  • Rachel Kerr

    (University of Oxford)

  • David Kerr

    (University of Oxford)

  • Iva Kirac

    (Sestre milosrdnice University Hospital Center)

  • Jan Böhm

    (Central Finland Health Care District)

  • Jukka-Pekka Mecklin

    (Central Finland Health Care District)

  • Pekka Jousilahti

    (Finnish Institute for Health and Welfare)

  • Paul Knekt

    (Finnish Institute for Health and Welfare)

  • Lauri A. Aaltonen

    (University of Helsinki
    University of Helsinki)

  • Harri Rissanen

    (Finnish Institute for Health and Welfare)

  • Eero Pukkala

    (Tampere University
    Institute for Statistical and Epidemiological Cancer Research)

  • Johan G. Eriksson

    (University of Helsinki
    National University of Singapore
    University of Helsinki and Helsinki University Hospital)

  • Tatiana Cajuso

    (University of Helsinki
    University of Helsinki)

  • Ulrika Hänninen

    (University of Helsinki
    University of Helsinki)

  • Johanna Kondelin

    (University of Helsinki
    University of Helsinki)

  • Kimmo Palin

    (University of Helsinki
    University of Helsinki)

  • Tomas Tanskanen

    (University of Helsinki
    University of Helsinki)

  • Laura Renkonen-Sinisalo

    (Helsinki University Hospital)

  • Satu Männistö

    (Finnish Institute for Health and Welfare)

  • Demetrius Albanes

    (National Institutes of Health)

  • Stephanie J. Weinstein

    (National Institutes of Health)

  • Edward Ruiz-Narvaez

    (University of Michigan)

  • Julie R. Palmer

    (Boston University School of Medicine
    Slone Epidemiology Center at Boston University)

  • Daniel D. Buchanan

    (University of Melbourne
    Royal Melbourne Hospital
    Victorian Comprehensive Cancer Centre)

  • Elizabeth A. Platz

    (Johns Hopkins Bloomberg School of Public Health)

  • Kala Visvanathan

    (Johns Hopkins Bloomberg School of Public Health)

  • Cornelia M. Ulrich

    (University of Utah)

  • Erin Siegel

    (H. Lee Moffitt Cancer Center and Research Institute)

  • Stefanie Brezina

    (Medical University Vienna)

  • Andrea Gsur

    (Medical University Vienna)

  • Peter T. Campbell

    (Albert Einstein College of Medicine)

  • Jenny Chang-Claude

    (German Cancer Research Center
    University Cancer Centre Hamburg)

  • Michael Hoffmeister

    (German Cancer Research Center)

  • Hermann Brenner

    (German Cancer Research Center
    German Cancer Research Center and National Center for Tumor Diseases
    German Cancer Research Center)

  • Martha L. Slattery

    (University of Utah)

  • John D. Potter

    (Fred Hutchinson Cancer Center
    Massey University)

  • Kostas K. Tsilidis

    (Imperial College London
    University of Ioannina School of Medicine)

  • Matthias B. Schulze

    (German Institute of Human Nutrition Potsdam-Rehbruecke
    University of Potsdam)

  • Marc J. Gunter

    (World Health Organization)

  • Neil Murphy

    (World Health Organization)

  • Antoni Castells

    (University of Barcelona)

  • Sergi Castellví-Bel

    (University of Barcelona)

  • Leticia Moreira

    (University of Barcelona)

  • Volker Arndt

    (German Cancer Research Center)

  • Anna Shcherbina

    (Stanford University)

  • D. Timothy Bishop

    (University of Leeds)

  • Graham G. Giles

    (University of Melbourne
    Cancer Council Victoria
    Monash University)

  • Melissa C. Southey

    (Cancer Council Victoria
    Monash University
    University of Melbourne)

  • Gregory E. Idos

    (City of Hope National Medical Center)

  • Kevin J. McDonnell

    (Clalit National Cancer Control Center
    Technion-Israel Institute of Technology
    City of Hope National Medical Center)

  • Zomoroda Abu-Ful

    (Lady Davis Carmel Medical Center)

  • Joel K. Greenson

    (Clalit National Cancer Control Center
    Technion-Israel Institute of Technology
    University of Michigan)

  • Katerina Shulman

    (Lady Davis Carmel Medical Center)

  • Flavio Lejbkowicz

    (Clalit National Cancer Control Center
    Lady Davis Carmel Medical Center
    Lady Davis Carmel Medical Center)

  • Kenneth Offit

    (Memorial Sloan-Kettering Cancer Center
    Weill Cornell Medical College)

  • Yu-Ru Su

    (Kaiser Permanente Washington Health Research Institute)

  • Robert Steinfelder

    (Fred Hutchinson Cancer Center)

  • Temitope O. Keku

    (University of North Carolina)

  • Bethany Guelpen

    (Umeå University
    Umeå University)

  • Thomas J. Hudson

    (Ontario Institute for Cancer Research)

  • Heather Hampel

    (Ohio State University Comprehensive Cancer Center)

  • Rachel Pearlman

    (Ohio State University Comprehensive Cancer Center)

  • Sonja I. Berndt

    (National Institutes of Health)

  • Richard B. Hayes

    (New York University School of Medicine)

  • Marie Elena Martinez

    (University of California San Diego
    University of California San Diego Moores Cancer Center)

  • Sushma S. Thomas

    (Fred Hutchinson Cancer Center)

  • Paul D. P. Pharoah

    (University of Cambridge)

  • Susanna C. Larsson

    (Karolinska Institutet)

  • Yun Yen

    (Taipei Medical University)

  • Heinz-Josef Lenz

    (University of Southern California)

  • Emily White

    (Fred Hutchinson Cancer Center
    University of Washington School of Public Health)

  • Li Li

    (Case Western Reserve University)

  • Kimberly F. Doheny

    (Johns Hopkins University School of Medicine)

  • Elizabeth Pugh

    (Johns Hopkins University School of Medicine)

  • Tameka Shelford

    (Johns Hopkins University School of Medicine)

  • Andrew T. Chan

    (Broad Institute of Harvard and MIT
    Brigham and Women’s Hospital and Harvard Medical School
    Massachusetts General Hospital and Harvard Medical School
    Harvard University)

  • Marcia Cruz-Correa

    (University of Puerto Rico)

  • Annika Lindblom

    (Karolinska University Hospital
    Karolinska Institutet)

  • David J. Hunter

    (Harvard University
    University of Oxford)

  • Amit D. Joshi

    (Massachusetts General Hospital and Harvard Medical School
    Harvard University)

  • Clemens Schafmayer

    (University Hospital Rostock)

  • Peter C. Scacheri

    (Case Western Reserve University)

  • Anshul Kundaje

    (Stanford University
    Stanford University)

  • Robert E. Schoen

    (University of Pittsburgh Medical Center)

  • Jochen Hampe

    (Technische Universität Dresden)

  • Zsofia K. Stadler

    (Weill Cornell Medical College
    Memorial Sloan-Kettering Cancer Center)

  • Pavel Vodicka

    (Institute of Experimental Medicine of the Czech Academy of Sciences
    Charles University
    Charles University)

  • Ludmila Vodickova

    (Institute of Experimental Medicine of the Czech Academy of Sciences
    Charles University
    Charles University)

  • Veronika Vymetalkova

    (Institute of Experimental Medicine of the Czech Academy of Sciences
    Charles University
    Charles University)

  • Christopher K. Edlund

    (University of Southern California)

  • W. James Gauderman

    (University of Southern California)

  • David Shibata

    (University of Tennessee Health Science Center)

  • Amanda Toland

    (Ohio State University)

  • Sanford Markowitz

    (Case Western Reserve University and University Hospitals of Cleveland)

  • Andre Kim

    (University of Southern California)

  • Stephen J. Chanock

    (National Institutes of Health)

  • Franzel Duijnhoven

    (Wageningen University and Research)

  • Edith J. M. Feskens

    (Wageningen University and Research)

  • Lori C. Sakoda

    (Fred Hutchinson Cancer Center
    Kaiser Permanente Northern California)

  • Manuela Gago-Dominguez

    (Servicio Galego de Saude
    Instituto de Investigación Sanitaria de Santiago de Compostela)

  • Alicja Wolk

    (Karolinska Institutet)

  • Barbara Pardini

    (Candiolo Cancer Institute FPO-IRCCS
    Candiolo Cancer Institute FPO-IRCCS)

  • Liesel M. FitzGerald

    (Cancer Council Victoria
    University of Tasmania)

  • Soo Chin Lee

    (National University of Singapore)

  • Shuji Ogino

    (Harvard University
    Broad Institute of MIT and Harvard
    Dana-Farber Harvard Cancer Center
    Harvard Medical School)

  • Stephanie A. Bien

    (Fred Hutchinson Cancer Center)

  • Charles Kooperberg

    (Fred Hutchinson Cancer Center)

  • Christopher I. Li

    (Fred Hutchinson Cancer Center)

  • Yi Lin

    (Fred Hutchinson Cancer Center)

  • Ross Prentice

    (Fred Hutchinson Cancer Center
    University of Washington)

  • Conghui Qu

    (Fred Hutchinson Cancer Center)

  • Stéphane Bézieau

    (Centre Hospitalier Universitaire Nantes)

  • Taiki Yamaji

    (National Cancer Center)

  • Norie Sawada

    (National Cancer Center)

  • Motoki Iwasaki

    (National Cancer Center
    National Cancer Center)

  • Loic Marchand

    (University of Hawaii)

  • Anna H. Wu

    (University of Southern California)

  • Chenxu Qu

    (University of Southern California)

  • Caroline E. McNeil

    (University of Southern California)

  • Gerhard Coetzee

    (Van Andel Research Institute)

  • Caroline Hayward

    (University of Edinburgh)

  • Ian J. Deary

    (University of Edinburgh)

  • Sarah E. Harris

    (University of Edinburgh)

  • Evropi Theodoratou

    (University of Edinburgh)

  • Stuart Reid

    (University of Edinburgh)

  • Marion Walker

    (University of Edinburgh)

  • Li Yin Ooi

    (University of Edinburgh
    National University Health System)

  • Ken S. Lau

    (Vanderbilt University School of Medicine)

  • Hongyu Zhao

    (Yale School of Public Health
    Yale School of Medicine
    Yale University)

  • Li Hsu

    (Fred Hutchinson Cancer Center
    University of Washington)

  • Qiuyin Cai

    (Vanderbilt University Medical Center)

  • Malcolm G. Dunlop

    (University of Edinburgh)

  • Stephen B. Gruber

    (City of Hope National Medical Center)

  • Richard S. Houlston

    (Institute of Cancer Research)

  • Victor Moreno

    (Bellvitge Biomedical Research Institute
    Consortium for Biomedical Research in Epidemiology and Public Health
    University of Barcelona
    Catalan Institute of Oncology)

  • Graham Casey

    (University of Virginia)

  • Ulrike Peters

    (Fred Hutchinson Cancer Center
    University of Washington)

  • Ian Tomlinson

    (University of Edinburgh
    University of Birmingham)

  • Wei Zheng

    (Vanderbilt University Medical Center)

Abstract

Genome-wide association studies (GWAS) have identified more than 200 common genetic variants independently associated with colorectal cancer (CRC) risk, but the causal variants and target genes are mostly unknown. We sought to fine-map all known CRC risk loci using GWAS data from 100,204 cases and 154,587 controls of East Asian and European ancestry. Our stepwise conditional analyses revealed 238 independent association signals of CRC risk, each with a set of credible causal variants (CCVs), of which 28 signals had a single CCV. Our cis-eQTL/mQTL and colocalization analyses using colorectal tissue-specific transcriptome and methylome data separately from 1299 and 321 individuals, along with functional genomic investigation, uncovered 136 putative CRC susceptibility genes, including 56 genes not previously reported. Analyses of single-cell RNA-seq data from colorectal tissues revealed 17 putative CRC susceptibility genes with distinct expression patterns in specific cell types. Analyses of whole exome sequencing data provided additional support for several target genes identified in this study as CRC susceptibility genes. Enrichment analyses of the 136 genes uncover pathways not previously linked to CRC risk. Our study substantially expanded association signals for CRC and provided additional insight into the biological mechanisms underlying CRC development.

Suggested Citation

  • Zhishan Chen & Xingyi Guo & Ran Tao & Jeroen R. Huyghe & Philip J. Law & Ceres Fernandez-Rozadilla & Jie Ping & Guochong Jia & Jirong Long & Chao Li & Quanhu Shen & Yuhan Xie & Maria N. Timofeeva & Mi, 2024. "Fine-mapping analysis including over 254,000 East Asian and European descendants identifies 136 putative colorectal cancer susceptibility genes," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47399-x
    DOI: 10.1038/s41467-024-47399-x
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    References listed on IDEAS

    as
    1. Philip J. Law & Maria Timofeeva & Ceres Fernandez-Rozadilla & Peter Broderick & James Studd & Juan Fernandez-Tajes & Susan Farrington & Victoria Svinti & Claire Palles & Giulia Orlando & Amit Sud & Am, 2019. "Association analyses identify 31 new risk loci for colorectal cancer susceptibility," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    2. Robin Andersson & Claudia Gebhard & Irene Miguel-Escalada & Ilka Hoof & Jette Bornholdt & Mette Boyd & Yun Chen & Xiaobei Zhao & Christian Schmidl & Takahiro Suzuki & Evgenia Ntini & Erik Arner & Eivi, 2014. "An atlas of active enhancers across human cell types and tissues," Nature, Nature, vol. 507(7493), pages 455-461, March.
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