Inherited causes of clonal haematopoiesis in 97,691 whole genomes View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2020-10-14

AUTHORS

Alexander G. Bick, Joshua S. Weinstock, Satish K. Nandakumar, Charles P. Fulco, Erik L. Bao, Seyedeh M. Zekavat, Mindy D. Szeto, Xiaotian Liao, Matthew J. Leventhal, Joseph Nasser, Kyle Chang, Cecelia Laurie, Bala Bharathi Burugula, Christopher J. Gibson, Abhishek Niroula, Amy E. Lin, Margaret A. Taub, Francois Aguet, Kristin Ardlie, Braxton D. Mitchell, Kathleen C. Barnes, Arden Moscati, Myriam Fornage, Susan Redline, Bruce M. Psaty, Edwin K. Silverman, Scott T. Weiss, Nicholette D. Palmer, Ramachandran S. Vasan, Esteban G. Burchard, Sharon L. R. Kardia, Jiang He, Robert C. Kaplan, Nicholas L. Smith, Donna K. Arnett, David A. Schwartz, Adolfo Correa, Mariza de Andrade, Xiuqing Guo, Barbara A. Konkle, Brian Custer, Juan M. Peralta, Hongsheng Gui, Deborah A. Meyers, Stephen T. McGarvey, Ida Yii-Der Chen, M. Benjamin Shoemaker, Patricia A. Peyser, Jai G. Broome, Stephanie M. Gogarten, Fei Fei Wang, Quenna Wong, May E. Montasser, Michelle Daya, Eimear E. Kenny, Kari E. North, Lenore J. Launer, Brian E. Cade, Joshua C. Bis, Michael H. Cho, Jessica Lasky-Su, Donald W. Bowden, L. Adrienne Cupples, Angel C. Y. Mak, Lewis C. Becker, Jennifer A. Smith, Tanika N. Kelly, Stella Aslibekyan, Susan R. Heckbert, Hemant K. Tiwari, Ivana V. Yang, John A. Heit, Steven A. Lubitz, Jill M. Johnsen, Joanne E. Curran, Sally E. Wenzel, Daniel E. Weeks, Dabeeru C. Rao, Dawood Darbar, Jee-Young Moon, Russell P. Tracy, Erin J. Buth, Nicholas Rafaels, Ruth J. F. Loos, Peter Durda, Yongmei Liu, Lifang Hou, Jiwon Lee, Priyadarshini Kachroo, Barry I. Freedman, Daniel Levy, Lawrence F. Bielak, James E. Hixson, James S. Floyd, Eric A. Whitsel, Patrick T. Ellinor, Marguerite R. Irvin, Tasha E. Fingerlin, Laura M. Raffield, Sebastian M. Armasu, Marsha M. Wheeler, Ester C. Sabino, John Blangero, L. Keoki Williams, Bruce D. Levy, Wayne Huey-Herng Sheu, Dan M. Roden, Eric Boerwinkle, JoAnn E. Manson, Rasika A. Mathias, Pinkal Desai, Kent D. Taylor, Andrew D. Johnson, Paul L. Auer, Charles Kooperberg, Cathy C. Laurie, Thomas W. Blackwell, Albert V. Smith, Hongyu Zhao, Ethan Lange, Leslie Lange, Stephen S. Rich, Jerome I. Rotter, James G. Wilson, Paul Scheet, Jacob O. Kitzman, Eric S. Lander, Jesse M. Engreitz, Benjamin L. Ebert, Alexander P. Reiner, Siddhartha Jaiswal, Gonçalo Abecasis, Vijay G. Sankaran, Sekar Kathiresan, Pradeep Natarajan

ABSTRACT

Age is the dominant risk factor for most chronic human diseases, but the mechanisms through which ageing confers this risk are largely unknown1. The age-related acquisition of somatic mutations that lead to clonal expansion in regenerating haematopoietic stem cell populations has recently been associated with both haematological cancer2–4 and coronary heart disease5—this phenomenon is termed clonal haematopoiesis of indeterminate potential (CHIP)6. Simultaneous analyses of germline and somatic whole-genome sequences provide the opportunity to identify root causes of CHIP. Here we analyse high-coverage whole-genome sequences from 97,691 participants of diverse ancestries in the National Heart, Lung, and Blood Institute Trans-omics for Precision Medicine (TOPMed) programme, and identify 4,229 individuals with CHIP. We identify associations with blood cell, lipid and inflammatory traits that are specific to different CHIP driver genes. Association of a genome-wide set of germline genetic variants enabled the identification of three genetic loci associated with CHIP status, including one locus at TET2 that was specific to individuals of African ancestry. In silico-informed in vitro evaluation of the TET2 germline locus enabled the identification of a causal variant that disrupts a TET2 distal enhancer, resulting in increased self-renewal of haematopoietic stem cells. Overall, we observe that germline genetic variation shapes haematopoietic stem cell function, leading to CHIP through mechanisms that are specific to clonal haematopoiesis as well as shared mechanisms that lead to somatic mutations across tissues. More... »

PAGES

763-768

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  • Journal

    TITLE

    Nature

    ISSUE

    7831

    VOLUME

    586

    Author Affiliations

  • Division of Genetic Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
  • Center for Statistical Genetics, Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, MI, USA
  • Division of Hematology/Oncology, Boston Children’s Hospital and Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA
  • Department of Systems Biology, Harvard Medical School, Boston, MA, USA
  • Health Sciences and Technology Program, Harvard Medical School, Boston, MA, USA
  • Yale School of Medicine, New Haven, CT, USA
  • Medical Scientist Training Program, University of Colorado Anschutz Medical Campus, Aurora, CO, USA
  • Broad Institute of MIT and Harvard, Cambridge, MA, USA
  • Department of Epidemiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
  • Department of Biostatistics, University of Washington, Seattle, WA, USA
  • Department of Human Genetics, University of Michigan, Ann Arbor, MI, USA
  • Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA
  • Division of Cardiovascular Medicine, Department of Medicine, Brigham and Women’s Hospital, Boston, MA, USA
  • Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
  • Geriatrics Research and Education Clinical Center, Baltimore Veterans Administration Medical Center, Baltimore, MD, USA
  • Colorado Center for Personalized Medicine, School of Medicine, University of Colorado, Aurora, CO, USA
  • Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA
  • Human Genetics Center, School of Public Health, University of Texas Health Science Center at Houston, Houston, TX, USA
  • Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA, USA
  • Kaiser Permanente Washington Health Research Institute, Seattle, WA, USA
  • Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital, Boston, MA, USA
  • Department of Biochemistry, Wake Forest School of Medicine, Winston-Salem, NC, USA
  • Departments of Medicine and Epidemiology, Boston University School of Medicine, Boston, MA, USA
  • Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, USA
  • Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA
  • Tulane University Translational Science Institute, New Orleans, LA, USA
  • Fred Hutchinson Cancer Research Center, Division of Public Health Sciences, Seattle, WA, USA
  • Seattle Epidemiologic Information and Research Center, Department of Veterans Affairs, Office of Research and Development, Seattle, WA, USA
  • College of Public Health, University of Kentucky, Lexington, KY, USA
  • Department of Medicine, University of Colorado, Aurora, CO, USA
  • Departments of Medicine and Population Health Science, University of Mississippi Medical Center, Jackson, MS, USA
  • Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA
  • Institute for Translational Genomics and Population Sciences, Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA
  • Department of Medicine, University of Washington, Seattle, WA, USA
  • Department of Laboratory Medicine, University of California, San Francisco, San Francisco, CA, USA
  • Department of Human Genetics and South Texas Diabetes and Obesity Institute, University of Texas Rio Grande Valley School of Medicine, Brownsville, TX, USA
  • Center for Individualized and Genomic Medicine Research, Department of Internal Medicine, Henry Ford Health System, Detroit, MI, USA
  • Division of Genetics, Genomics and Precision Medicine, University of Arizona, Tucson, AZ, USA
  • Department of Epidemiology and International Health Institute, Brown University School of Public Health, Providence, RI, USA
  • Medical Genetics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Los Angeles, CA, USA
  • Division of Cardiology, Vanderbilt University Medical Center, Nashville, TN, USA
  • Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, USA
  • Division of Biomedical Informatics and Personalized Medicine, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO, USA
  • Institute for Genomic Health, Icahn School of Medicine at Mount Sinai, New York, NY, USA
  • Department of Epidemiology, University of North Carolina, Chapel Hill, NC, USA
  • Laboratory of Epidemiology, Demography, and Biometry, Intramural Research Program, National Institute on Aging, Bethesda, MD, USA
  • Division of Sleep Medicine, Department of Medicine, Harvard Medical School, Boston, MA, USA
  • Cardiovascular Health Research Unit, Department of Medicine, University of Washington, Seattle, WA, USA
  • Departments of Biostatistics and Epidemiology, Boston University School of Public Health, Boston, MA, USA
  • Department of Medicine, University of California, San Francisco, San Francisco, CA, USA
  • GeneSTAR Research Program, Department of Medicine, Johns Hopkins School of Medicine, Baltimore, MD, USA
  • Survey Research Center, Institute for Social Research, University of Michigan, Ann Arbor, MI, USA
  • Department of Epidemiology, University of Alabama at Birmingham, Birmingham, AL, USA
  • Department of Biostatistics, University of Alabama at Birmingham, Birmingham, AL, USA
  • Division of Cardiovascular Diseases, Mayo Clinic, Rochester, MN, USA
  • Cardiovascular Research Center, Massachusetts General Hospital, Boston, MA, USA
  • Department of Environmental and Occupational Health, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, USA
  • Departments of Human Genetics and Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, USA
  • Division of Biostatistics, Washington University School of Medicine, St Louis, MO, USA
  • Division of Cardiology, University of Illinois at Chicago, Chicago, IL, USA
  • Department of Epidemiology and Population Health, Albert Einstein College of Medicine, New York, NY, USA
  • Department of Pathology and Laboratory Medicine, Larner College of Medicine, University of Vermont, Burlington, VT, USA
  • Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA
  • Division of Cardiology, Department of Medicine, Duke University Medical Center, Durham, NC, USA
  • Department of Preventive Medicine, Northwestern Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
  • Division of Sleep and Circadian Disorders, Department of Medicine, Brigham and Women’s Hospital, Boston, MA, USA
  • Department of Internal Medicine, Section on Nephrology, Wake Forest School of Medicine, Winston-Salem, NC, USA
  • Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD, USA
  • Department of Epidemiology, Human Genetics and Environmental Sciences, University of Texas Health Science Center at Houston School of Public Health, Houston, TX, USA
  • Department of Medicine, School of Medicine, University of North Carolina, Chapel Hill, NC, USA
  • Center for Genes Environment and Health, National Jewish Health, Denver, CO, USA
  • Department of Genetics, University of North Carolina, Chapel Hill, NC, USA
  • Department of Genome Science, University of Washington, Seattle, WA, USA
  • Instituto de Medicina Tropical, Faculdade de Medicina da Universidade de São Paulo, São Paulo, Brazil
  • Division of Pulmonary and Critical Care Medicine, Department of Medicine, Brigham and Women’s Hospital, Boston, MA, USA
  • Division of Endocrinology and Metabolism, Department of Internal Medicine, Taichung Veterans General Hospital, Taichung, Taiwan
  • Department of Biomedical Informatics, Vanderbilt University Medical Center, Nashville, TN, USA
  • Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, USA
  • Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA
  • Department of Medicine, Weill Cornell Medical School, New York, NY, USA
  • Department of Pediatrics, Harbor-UCLA Medical Center, Torrance, CA, USA
  • Joseph J. Zilber School of Public Health, University of Wisconsin-Milwaukee, Milwaukee, WI, USA
  • Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA
  • Computational Biology and Bioinformatics Program, Yale University, New Haven, CT, USA
  • Department of Public Health Sciences, Center for Public Health Genomics, University of Virginia, Charlottesville, VA, USA
  • Department of Cardiology, Beth Israel Deaconess Medical Center, Boston, MA, USA
  • Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI, USA
  • Department of Biology, MIT, Cambridge, MA, USA
  • Harvard Society of Fellows, Harvard University, Cambridge, MA, USA
  • Howard Hughes Medical Institute, Boston, MA, USA
  • Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA
  • Regeneron Pharmaceuticals, Tarrytown, NY, USA
  • Verve Therapeutics, Cambridge, MA, USA
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/s41586-020-2819-2

    DOI

    http://dx.doi.org/10.1038/s41586-020-2819-2

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1131656433

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/33057201


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