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The transcriptional landscape of age in human peripheral blood

Author

Listed:
  • Marjolein J. Peters

    (Erasmus Medical Centre Rotterdam)

  • Roby Joehanes

    (The National Heart, Lung, and Blood Institute’s and Boston University’s Framingham Heart Study
    Population Sciences Branch, National Heart, Lung, and Blood Institute)

  • Luke C. Pilling

    (Epidemiology and Public Health, University of Exeter Medical School)

  • Claudia Schurmann

    (Interfaculty Institute for Genetics and Functional Genomics, University Medicine Greifswald
    The Charles Bronfman Institute for Personalized Medicine, Genetics of Obesity & Related Metabolic Traits Program, Icahn School of Medicine at Mount Sinai)

  • Karen N. Conneely

    (School of Medicine, Emory University)

  • Joseph Powell

    (Centre for Neurogenetics and Statistical Genomics, Queensland Brain Institute, University of Queensland
    The Institute for Molecular Bioscience, University of Queensland)

  • Eva Reinmaa

    (Estonian Genome Center, University of Tartu)

  • George L. Sutphin

    (Nathan Shock Center of Excellence in the Basic Biology of Aging, The Jackson Laboratory)

  • Alexandra Zhernakova

    (University Medical Center Groningen, University of Groningen)

  • Katharina Schramm

    (Institute of Human Genetics, Helmholz Zentrum München - German Research Center for Environmental Health
    Institute of Human Genetics, Technical University Munich)

  • Yana A. Wilson

    (Garvan Institute of Medical Research, Australia and Charles Perkins Centre and School of Molecular Bioscience, The University of Sydney)

  • Sayuko Kobes

    (Phoenix Epidemiology and Clinical Research Branch, National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health)

  • Taru Tukiainen

    (Institute for Molecular Medicine Finland FIMM, University of Helsinki
    National Institute for Health and Welfare)

  • Yolande F. Ramos

    (Leiden University Medical Center)

  • Harald H. H. Göring

    (Texas Biomedical Research Institute)

  • Myriam Fornage

    (Human Genetics, and Environmental Sciences, School of Public Health, University of Texas Health Sciences
    Institute of Molecular Medicine, University of Texas Health Sciences Center at Houston)

  • Yongmei Liu

    (Public Health Sciences, Wake Forest School of Medicine)

  • Sina A. Gharib

    (Computational Medicine Core, Center for Lung Biology, University of Washington)

  • Barbara E. Stranger

    (Section of Genetic Medicine, Institute for Genomics and Systems Biology, University of Chicago)

  • Philip L. De Jager

    (Program in Translational NeuroPsychiatric Genomics, Brigham and Women’s Hospital, Harvard Medical School)

  • Abraham Aviv

    (Center of Human Development and Aging, New Jersey Medical School)

  • Daniel Levy

    (The National Heart, Lung, and Blood Institute’s and Boston University’s Framingham Heart Study
    Population Sciences Branch, National Heart, Lung, and Blood Institute)

  • Joanne M. Murabito

    (The National Heart, Lung, and Blood Institute’s and Boston University’s Framingham Heart Study
    General Internal Medicine Section, Boston University)

  • Peter J. Munson

    (The Mathematical and Statistical Computing Laboratory, Center for Information Technology, National Institutes of Health)

  • Tianxiao Huan

    (The National Heart, Lung, and Blood Institute’s and Boston University’s Framingham Heart Study
    Population Sciences Branch, National Heart, Lung, and Blood Institute)

  • Albert Hofman

    (Erasmus Medical Center)

  • André G. Uitterlinden

    (Erasmus Medical Centre Rotterdam
    Erasmus Medical Center)

  • Fernando Rivadeneira

    (Erasmus Medical Centre Rotterdam
    Erasmus Medical Center)

  • Jeroen van Rooij

    (Erasmus Medical Centre Rotterdam)

  • Lisette Stolk

    (Erasmus Medical Centre Rotterdam)

  • Linda Broer

    (Erasmus Medical Centre Rotterdam)

  • Michael M. P. J. Verbiest

    (Erasmus Medical Centre Rotterdam)

  • Mila Jhamai

    (Erasmus Medical Centre Rotterdam)

  • Pascal Arp

    (Erasmus Medical Centre Rotterdam)

  • Andres Metspalu

    (Estonian Genome Center, University of Tartu)

  • Liina Tserel

    (Molecular Pathology, Institute of Biomedicine, University of Tartu)

  • Lili Milani

    (Estonian Genome Center, University of Tartu)

  • Nilesh J. Samani

    (University of Leicester
    National Institute for Health Research Leicester Cardiovascular Biomedical Research Unit, Glenfield Hospital)

  • Pärt Peterson

    (Molecular Pathology, Institute of Biomedicine, University of Tartu)

  • Silva Kasela

    (Institute of Molecular and Cell Biology, Estonian Genome Center, University of Tartu)

  • Veryan Codd

    (University of Leicester
    National Institute for Health Research Leicester Cardiovascular Biomedical Research Unit, Glenfield Hospital)

  • Annette Peters

    (Institute of Epidemiologie II, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health
    Research Unit of Molecular Epidemiology, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health)

  • Cavin K. Ward-Caviness

    (Institute of Epidemiologie II, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health)

  • Christian Herder

    (Institute of Clinical Diabetology, German Diabetes Center, Leibniz Center for Diabetes Research at Heinrich Heine University Düsseldorf)

  • Melanie Waldenberger

    (Institute of Epidemiologie II, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health
    Research Unit of Molecular Epidemiology, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health)

  • Michael Roden

    (Institute of Clinical Diabetology, German Diabetes Center, Leibniz Center for Diabetes Research at Heinrich Heine University Düsseldorf
    University Hospital Düsseldorf, Heinrich Heine University)

  • Paula Singmann

    (Institute of Epidemiologie II, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health
    Research Unit of Molecular Epidemiology, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health)

  • Sonja Zeilinger

    (Institute of Epidemiologie II, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health
    Research Unit of Molecular Epidemiology, Helmholtz Zentrum Muenchen, German Research Center for Environmental Health)

  • Thomas Illig

    (Hannover Unified Biobank, Hannover Medical School)

  • Georg Homuth

    (Interfaculty Institute for Genetics and Functional Genomics, University Medicine Greifswald)

  • Hans-Jörgen Grabe

    (Helios Hospital Stralsund, University Medicine Greifswald)

  • Henry Völzke

    (Institute for Community Medicine, University Medicine Greifswald)

  • Leif Steil

    (Interfaculty Institute for Genetics and Functional Genomics, University Medicine Greifswald)

  • Thomas Kocher

    (Unit of Periodontology, Periodontology and Endodontology, University Medicine Greifswald)

  • Anna Murray

    (Epidemiology and Public Health, University of Exeter Medical School)

  • David Melzer

    (Epidemiology and Public Health, University of Exeter Medical School)

  • Hanieh Yaghootkar

    (Genetics of Complex Traits, University of Exeter Medical School, University of Exeter)

  • Stefania Bandinelli

    (Geriatric Unit, Azienda Sanitaria di Firenze)

  • Eric K. Moses

    (Centre for Genetic Origins of Health and Disease, The University of Western Australia, and Faculty of Health Sciences, Curtin University)

  • Jack W. Kent

    (Texas Biomedical Research Institute)

  • Joanne E. Curran

    (Texas Biomedical Research Institute)

  • Matthew P. Johnson

    (Texas Biomedical Research Institute)

  • Sarah Williams-Blangero

    (Texas Biomedical Research Institute)

  • Harm-Jan Westra

    (University Medical Center Groningen, University of Groningen
    Program in Medical and Population Genetics, Broad Institute of MIT and Harvard
    Brigham and Women’s Hospital and Harvard Medical School
    Partners Center for Personalized Genetic Medicine)

  • Allan F. McRae

    (The Queensland Brain Institute, University of Queensland
    University of Queensland Diamantina Institute, University of Queensland, Princess Alexandra Hospital)

  • Jennifer A. Smith

    (University of Michigan)

  • Sharon L. R. Kardia

    (University of Michigan)

  • Iiris Hovatta

    (University of Helsinki
    National Institute for Health and Welfare)

  • Markus Perola

    (Estonian Genome Center, University of Tartu
    Institute for Molecular Medicine Finland FIMM, University of Helsinki
    National Institute for Health and Welfare)

  • Samuli Ripatti

    (Institute for Molecular Medicine Finland FIMM, University of Helsinki
    National Institute for Health and Welfare
    Wellcome Trust Sanger Institute
    Hjelt Institute, University of Helsinki)

  • Veikko Salomaa

    (National Institute for Health and Welfare)

  • Anjali K. Henders

    (The Institute for Molecular Bioscience, University of Queensland)

  • Nicholas G. Martin

    (QIMR Berghofer Medical Research Institute)

  • Alicia K. Smith

    (Emory University School of Medicine)

  • Divya Mehta

    (Max-Planck Institute of Psychiatry)

  • Elisabeth B. Binder

    (Max-Planck Institute of Psychiatry)

  • K Maria Nylocks

    (Emory University School of Medicine)

  • Elizabeth M. Kennedy

    (School of Medicine, Emory University)

  • Torsten Klengel

    (Max-Planck Institute of Psychiatry)

  • Jingzhong Ding

    (Wake Forest School of Medicine)

  • Astrid M. Suchy-Dicey

    (University of Washington)

  • Daniel A. Enquobahrie

    (University of Washington)

  • Jennifer Brody

    (Cardiovascular Health Research Unit, University of Washington)

  • Jerome I. Rotter

    (Institute for Translational Genomics and Population Sciences, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center)

  • Yii-Der I. Chen

    (Institute for Translational Genomics and Population Sciences, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center)

  • Jeanine Houwing-Duistermaat

    (Leiden University Medical Center)

  • Margreet Kloppenburg

    (Leiden University Medical Center
    Leiden University Medical Center)

  • P. Eline Slagboom

    (Leiden University Medical Center)

  • Quinta Helmer

    (Leiden University Medical Center)

  • Wouter den Hollander

    (Leiden University Medical Center)

  • Shannon Bean

    (Nathan Shock Center of Excellence in the Basic Biology of Aging, The Jackson Laboratory)

  • Towfique Raj

    (Harvard Medical School)

  • Noman Bakhshi

    (Garvan Institute of Medical Research, Australia and Charles Perkins Centre and School of Molecular Bioscience, The University of Sydney)

  • Qiao Ping Wang

    (Garvan Institute of Medical Research, Australia and Charles Perkins Centre and School of Molecular Bioscience, The University of Sydney)

  • Lisa J. Oyston

    (Garvan Institute of Medical Research, Australia and Charles Perkins Centre and School of Molecular Bioscience, The University of Sydney)

  • Bruce M. Psaty

    (Cardiovascular Health Research Unit, University of Washington
    Cardiovascular Health Research Unit, University of Washington
    Cardiovascular Health Research Unit, University of Washington
    Group Health Research Institute, Group Health Cooperative)

  • Russell P. Tracy

    (University of Vermont College of Medicine)

  • Grant W. Montgomery

    (QIMR Berghofer Medical Research Institute)

  • Stephen T. Turner

    (Mayo Clinic)

  • John Blangero

    (Texas Biomedical Research Institute)

  • Ingrid Meulenbelt

    (Leiden University Medical Center)

  • Kerry J. Ressler

    (Emory University School of Medicine)

  • Jian Yang

    (The Queensland Brain Institute, University of Queensland
    University of Queensland Diamantina Institute, University of Queensland, Princess Alexandra Hospital)

  • Lude Franke

    (University Medical Center Groningen, University of Groningen)

  • Johannes Kettunen

    (Institute for Molecular Medicine Finland FIMM, University of Helsinki
    National Institute for Health and Welfare
    Computational Medicine, Institute of Health Sciences, Faculty of Medicine, University of Oulu)

  • Peter M. Visscher

    (The Queensland Brain Institute, University of Queensland
    University of Queensland Diamantina Institute, University of Queensland, Princess Alexandra Hospital)

  • G. Gregory Neely

    (Garvan Institute of Medical Research, Australia and Charles Perkins Centre and School of Molecular Bioscience, The University of Sydney)

  • Ron Korstanje

    (Nathan Shock Center of Excellence in the Basic Biology of Aging, The Jackson Laboratory)

  • Robert L. Hanson

    (Phoenix Epidemiology and Clinical Research Branch, National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health)

  • Holger Prokisch

    (Institute of Human Genetics, Helmholz Zentrum München - German Research Center for Environmental Health
    Institute of Human Genetics, Technical University Munich)

  • Luigi Ferrucci

    (Clinical Research Branch, National Institute on Aging)

  • Tonu Esko

    (Estonian Genome Center, University of Tartu
    Program in Medical and Population Genetics, Broad Institute of MIT and Harvard
    Children's Hospital Boston
    Harvard Medical School)

  • Alexander Teumer

    (Interfaculty Institute for Genetics and Functional Genomics, University Medicine Greifswald)

  • Joyce B. J. van Meurs

    (Erasmus Medical Centre Rotterdam)

  • Andrew D. Johnson

    (The National Heart, Lung, and Blood Institute’s and Boston University’s Framingham Heart Study
    Population Sciences Branch, National Heart, Lung, and Blood Institute)

Abstract

Disease incidences increase with age, but the molecular characteristics of ageing that lead to increased disease susceptibility remain inadequately understood. Here we perform a whole-blood gene expression meta-analysis in 14,983 individuals of European ancestry (including replication) and identify 1,497 genes that are differentially expressed with chronological age. The age-associated genes do not harbor more age-associated CpG-methylation sites than other genes, but are instead enriched for the presence of potentially functional CpG-methylation sites in enhancer and insulator regions that associate with both chronological age and gene expression levels. We further used the gene expression profiles to calculate the ‘transcriptomic age’ of an individual, and show that differences between transcriptomic age and chronological age are associated with biological features linked to ageing, such as blood pressure, cholesterol levels, fasting glucose, and body mass index. The transcriptomic prediction model adds biological relevance and complements existing epigenetic prediction models, and can be used by others to calculate transcriptomic age in external cohorts.

Suggested Citation

  • Marjolein J. Peters & Roby Joehanes & Luke C. Pilling & Claudia Schurmann & Karen N. Conneely & Joseph Powell & Eva Reinmaa & George L. Sutphin & Alexandra Zhernakova & Katharina Schramm & Yana A. Wil, 2015. "The transcriptional landscape of age in human peripheral blood," Nature Communications, Nature, vol. 6(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms9570
    DOI: 10.1038/ncomms9570
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    Cited by:

    1. Anna Halama & Shaza Zaghlool & Gaurav Thareja & Sara Kader & Wadha Al Muftah & Marjonneke Mook-Kanamori & Hina Sarwath & Yasmin Ali Mohamoud & Nisha Stephan & Sabine Ameling & Maja Pucic Baković & Jan, 2024. "A roadmap to the molecular human linking multiomics with population traits and diabetes subtypes," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    2. Paul R. H. J. Timmers & James F. Wilson & Peter K. Joshi & Joris Deelen, 2020. "Multivariate genomic scan implicates novel loci and haem metabolism in human ageing," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    3. Jian Lu & Raheel Ahmad & Thomas Nguyen & Jeffrey Cifello & Humza Hemani & Jiangyuan Li & Jinguo Chen & Siyi Li & Jing Wang & Achouak Achour & Joseph Chen & Meagan Colie & Ana Lustig & Christopher Dunn, 2022. "Heterogeneity and transcriptome changes of human CD8+ T cells across nine decades of life," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Ruiyang Li & Wenben Chen & Mingyuan Li & Ruixin Wang & Lanqin Zhao & Yuanfan Lin & Xinwei Chen & Yuanjun Shang & Xueer Tu & Duoru Lin & Xiaohang Wu & Zhenzhe Lin & Andi Xu & Xun Wang & Dongni Wang & X, 2023. "LensAge index as a deep learning-based biological age for self-monitoring the risks of age-related diseases and mortality," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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