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Genome-wide meta-analysis of macronutrient intake of 91,114 European ancestry participants from the cohorts for heart and aging research in genomic epidemiology consortium

Molecular Psychiatry volume 24, pages 1920–1932 (2019)Cite this article

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Abstract

Macronutrient intake, the proportion of calories consumed from carbohydrate, fat, and protein, is an important risk factor for metabolic diseases with significant familial aggregation. Previous studies have identified two genetic loci for macronutrient intake, but incomplete coverage of genetic variation and modest sample sizes have hindered the discovery of additional loci. Here, we expanded the genetic landscape of macronutrient intake, identifying 12 suggestively significant loci (P < 1 × 10−6) associated with intake of any macronutrient in 91,114 European ancestry participants. Four loci replicated and reached genome-wide significance in a combined meta-analysis including 123,659 European descent participants, unraveling two novel loci; a common variant in RARB locus for carbohydrate intake and a rare variant in DRAM1 locus for protein intake, and corroborating earlier FGF21 and FTO findings. In additional analysis of 144,770 participants from the UK Biobank, all identified associations from the two-stage analysis were confirmed except for DRAM1. Identified loci might have implications in brain and adipose tissue biology and have clinical impact in obesity-related phenotypes. Our findings provide new insight into biological functions related to macronutrient intake.

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Acknowledgements

A full list of acknowledgments appears in Supplementary Table 6. We acknowledge the essential role of the Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Consortium for encouraging CHARGE studies to participate in this effort and for the contributions of CHARGE members to the analyses conducted for this research. Dr. Caren Smith is supported by NHLBI K08 HL112845.

Authors contributions

D.I.C., T.T., and A.Y.C. conceived and designed the study. A.E.J., M.G., C.P., G.V.D., R.N.L., M.K.W., S.M., J.S.N., M.K., T.S.A., N.P., D.K.H., C.B., T.H., M.O., A.C.F.-W., D.O.M.-K., L.P., C.E.P., P.S.V., T.V., O.L., S.K., L.M.R., T.L., J.H.Z., M.F.F., J.L., N.M.M., J.A.S., T.H., N.E., M.A.N., T.R., J.H., D.G.H., C.-A.S., A.M., R.L.-G., M.-C.V., C.A.W., F.J.A.R., J.S., I.P.K., F.D., P.M.R., M.K., D.S.S., C.L., W.Z., A.A., P.K., M.G., D.C.R., Q.Q., L.F., U.E., J.B., A.H., Z.P., V.M., N.J.W., S.L.R.K., O.P., A.J., J.E.C., M.C.Z., J.S.V., N.G.F., J.M.O., J.C.L., H.R., A.G.U., O.T.R., J.C.K.-d.J., J.D., J.I.R., K.W.N., R.A.S., M.A.P., M.P., L.A.C., S.T.T., T.I.A.S., V.K., Y.L., Y.S., L.Q., S.B., S.S.R., R.M., A.T., W.H.O., O.H.F., T.P., J.C.F., P.D., L.-P.L., contributed to data collection. J.M., H.S.D., D.I.C., T.T., and A.Y.C. performed quality control and meta-analyses. J.M., A.E.J., C.S., S.X.L. performed additional analyses including look-up in the NH.G.R.I.-E.B.I. G.W.A.S. Catalog, fine-mapping analyses, colocalization analyses for Expression Quantitative Trait loci and Human Atlas of long non-coding R.N.A., L.D. score regression analyses and Mendelian randomization. J.M., H.S.D., S.X.L., A.E.J., M.G., C.P., C.E.S., G.V.D., D.I.C., T.T., and A.Y.C. wrote the manuscript. All authors approved the final version of the manuscript.

Author information

Author notes

  1. These authors contributed equally: Jordi Merino, Hassan S. Dashti.

  2. These authors jointly supervised this work: Daniel I. Chasman, Audrey Y. Chu, Toshiko Tanaka.

Authors and Affiliations

  1. Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA

    Jordi Merino, Hassan S. Dashti & Jose C. Florez

  2. Programs in Metabolism and Medical & Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA

    Jordi Merino, Hassan S. Dashti & Jose C. Florez

  3. Diabetes Unit, Massachusetts General Hospital, Boston, MA, USA

    Jordi Merino & Jose C. Florez

  4. MRC Epidemiology Unit, University of Cambridge, Cambridge, UK

    Sherly X. Li, Jing Hua Zhao, Jian’an Luan, Felix Day, Claudia Langenberg, Nick J. Wareham, Nita G. Forouhi & Robert A. Scott

  5. Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA

    Chloé Sarnowski, Julius S. Ngwa, Josée Dupuis & L. Adrienne Cupples

  6. Biomedical and Translational Informatics Institute, Geisinger Health Weis Center for Research, Danvilla, PA, USA

    Anne E. Justice

  7. Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Anne E. Justice, Misa Graff & Kari E. North

  8. Research International and Scientific Affairs, Academy of Nutrition and Dietetics, Chicago, IL, USA

    Constantina Papoutsakis

  9. Nutrition and Genomics, JM-USDA-HNRCA at Tufts University, Boston, MA, USA

    Caren E. Smith & José M. Ordovás

  10. Department of Dietetics and Nutritional Science, School of Health Science and Education, Harokopio University, Athens, Greece

    George V. Dedoussis & Ioanna P. Kalafati

  11. Departments of Medicine, University of Washington, Seattle, USA

    Rozenn N. Lemaitre

  12. Department of Genetics, Washington University School of Medicine, Saint Louis, MO, USA

    Mary K. Wojczynski, Mary F. Feitosa & Michael A. Province

  13. National Institute for Health and Welfare, Helsinki, Finland

    Satu Männistö, Natalia Pervjakova, Niina Eklund, Paul Knekt, Antti Jula, Harri Rissanen, Markus Perola & Veikko Salomaa

  14. Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA

    Julius S. Ngwa

  15. Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA

    Minjung Kho, Jennifer A. Smith, Wei Zhao & Sharon L. R Kardia

  16. Novo Nordisk Foundation Center for Basic Metabolic Research, Section of Metabolic Genetics, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Tarunveer S. Ahluwalia, Torben Hansen, Oluf Pedersen & Thorkild I. A. Sørensen

  17. Estonian Genome Center, Institute of Genomics, University of Tartu, Tartu, Estonia

    Natalia Pervjakova

  18. Department of Biotechnology, Institute of Molecular and Cell Biology, University of Tartu, Tartu, Estonia

    Natalia Pervjakova

  19. Genomics of Common Disease, Division of Diabetes, Endocrinology and Metabolism, Department of Medicine, Imperial College London, London, UK

    Natalia Pervjakova

  20. Department of Internal Medicine, Wake Forest School of Medicine, Winston Salem, NC, USA

    Denise K. Houston

  21. Human Genomics Laboratory, Pennington Biomedical Research Center, Baton Rouge, LA, USA

    Claude Bouchard & Tuomo Rankinen

  22. Department of Epidemiology and Biostatistics, School of Public Health, Peking University, Peking, China

    Tao Huang

  23. Department of Clinical Sciences, Lund University Diabetes Center, Lund University, Malmö, Sweden

    Marju Orho-Melander, Christina-Alexandra Schulz & Ulrika Ericson

  24. USDA/ARS Children’s Nutrition Research Center, Houston, TX, USA

    Alexis C. Frazier-Wood

  25. Department of Clinical Epidemiology, Leiden University Medical Center, Leiden, The Netherlands

    Dennis O. Mook-Kanamori, Ruifang Li-Gao & Renée de Mutsert

  26. Department of Public Health and Primary Care, Leiden University Medical Center, Leiden, The Netherlands

    Dennis O. Mook-Kanamori

  27. Department of Kinesiology, Faculty of Medicine, Laval University, Québec, Canada

    Louis Pérusse & Angelo Tremblay

  28. Institute of Nutrition and Functional Foods, Québec, Canada

    Louis Pérusse & Marie-Claude Vohl

  29. School of Medicine and Public Health, Faculty of Medicine and Health, The University of Newcastle, Callaghan, Australia

    Craig E. Pennell & Carol A. Wang

  30. Human Genetics Center, University of Texas Health Science Center at Houston, Houston, TX, USA

    Paul S. de Vries

  31. Department of Epidemiology, Erasmus MC University Hospital, Rotterdam, The Netherlands

    Trudy Voortman, Frank J. A. van Rooij, Albert Hofman, André G. Uitterlinden, Jessica C. Kiefte-de Jong & Oscar H. Franco

  32. The Hospital for Sick Children, Translational Medicine, University of Toronto, Toronto, Canada

    Olivia Li, Jean Shin & Zdenka Pausova

  33. William Harvey Research Institute, Queen Mary University of London, London, UK

    Stavroula Kanoni & Panos Deloukas

  34. Division of Preventive Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Lynda M. Rose, Paul M. Ridker & Audrey Y. Chu

  35. Department of Clinical Chemistry, Fimlab Laboratories, Finnish Cardiovascular Research Center - Tampere, Faculty of Medicine and Life Sciences, University of Tampere, Tampere, Finland

    Terho Lehtimäki, Mika Kähönen, Leo-Pekka Lyytikäinen & Daniel I. Chasman

  36. Nutritional Epidemiology, JM-USDA-HNRCA at Tufts University, Boston, MA, USA

    Nicola M. McKeown

  37. Data Tecnica International, Glen Echo, MD, USA

    Mike A. Nalls

  38. Laboratory of Neurogenetics, National Institute on Aging, Bethesda, MD, USA

    Mike A. Nalls & Dena G. Hernandez

  39. Department of Bioinformatics, Shanghai Institute of Hematology, Shanghai, China

    Jinyan Huang

  40. Center for Public Health Genomics, Division of Biostatistics and Epidemiology, University of Virginia, Charlottesville, VA, USA

    Ani Manichaikul

  41. School of Nutrition, Laval University, Québec, Canada

    Marie-Claude Vohl

  42. Division of Cardiovascular Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Paul M. Ridker

  43. New York Academy of Medicine, New York, NY, USA

    David S. Siscovick

  44. Department of Nutrition, Exercise, and Sports, Faculty of Science, University of Copenhagen, Copenhagen, Denmark

    Arne Astrup

  45. Laboratory of Epidemiology and Population Sciences, National Institute on Aging, Bethesda, MD, USA

    Melissa Garcia

  46. Division of Biostatistics, Washington University School of Medicine, St. Louis, MO, USA

    D. C. Rao & Yun J. Sung

  47. Department of Epidemiology & Population Health, Albert Einstein College of Medicine, Bronx, NY, USA

    Qibin Qi

  48. Translational Gerontology Branch, National Institute on Aging, Baltimore, MD, USA

    Luigi Ferrucci & Toshiko Tanaka

  49. South Texas Diabetes and Obesity Institute, University of Texas Rio Grande Valley, Brownsville, TX, USA

    John Blangero & Joanne E. Curran

  50. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Albert Hofman

  51. Departments of Physiology and Nutritional Sciences, University of Toronto, Toronto, Canada

    Zdenka Pausova

  52. Department of Food and Environmental Sciences, Division of Nutrition, Helsinki, Finland

    Vera Mikkilä

  53. Department of Internal Medicine, Erasmus MC University Hospital, Rotterdam, The Netherlands

    M. Carola Zillikens & André G. Uitterlinden

  54. Division of Medicine, Turku University Hospital, Turku, Finland

    Jorma S. Viikari

  55. Department of Medicine, University of Turku, Turku, Finland

    Jorma S. Viikari

  56. Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain

    José M. Ordovás

  57. IMDEA Food Institute, CEI UAM + CSIC, Madrid, Spain

    José M. Ordovás

  58. Division of Nephrology and Hypertension, Mayo Clinic, Rochester, MN, USA

    John C. Lieske & Stephen T. Turner

  59. Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku, Finland

    Olli T. Raitakari

  60. Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, Turku, Finland

    Olli T. Raitakari

  61. Global Public Health, Leiden University College, The Hague, The Netherlands

    Jessica C. Kiefte-de Jong

  62. Institute for Translational Genomics and Population Sciences, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA

    Jerome I. Rotter

  63. Departments of Pediatrics and Medicine, Division of Genomic Outcomes, Harbor-UCLA Medical Center, Torrance, CA, USA

    Jerome I. Rotter

  64. Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, NC, USA

    Kari E. North

  65. NHLBI Framingham Heart Study, Framingham, MA, USA

    L. Adrienne Cupples

  66. Department of Public Health, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Thorkild I. A. Sørensen

  67. Department of Epidemiology and Prevention, Wake Forest School of Medicine, Winston Salem, NC, USA

    Yongmei Liu

  68. Department of Epidemiology, Tulane University, New Orleans, LA, USA

    Lu Qi

  69. Geriatric Unit, Azienda Sanitaria Firenze-ASF, Florence, Italy

    Stefania Bandinelli

  70. Department of Public Health Sciences, Center for Public Health Genomics, University of Virginia, Charlottesville, VA, USA

    Stephen S. Rich

  71. Telethon Kids Institute, The University of Western Australia, Perth, Western Australia, Australia

    Wendy H. Oddy

  72. Menzies Institute for Medical Research, University of Tasmania, Tasmania, Australia

    Wendy H. Oddy

  73. Rotman Research Institute, University of Toronto, Toronto, Canada

    Tomas Paus

  74. Department of Psychiatry and Psychology, University of Toronto, Toronto, Canada

    Tomas Paus

  75. Child Mind Institute, New York, NY, USA

    Tomas Paus

  76. Princess Al-Jawhara Al-Brahim Centre of Excellence in Research of Hereditary Disorders (PACER-HD), King Abdulaziz University, Jeddah, Saudi Arabia

    Panos Deloukas

  77. Division of Genetics, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Daniel I. Chasman

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  1. Jordi Merino
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Corresponding author

Correspondence to Toshiko Tanaka.

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Conflict of interest

MANs’ participation is supported by a consulting contract between Data Tecnica International and the National Institute on Aging, NIH, Bethesda, MD, USA, as a possible conflict of interest. Dr. Nalls also consults for Illumina Inc, the Michael J. Fox Foundation and University of California Healthcare among others. AYC is currently employed by Merck Research Laboratories.

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Merino, J., Dashti, H.S., Li, S.X. et al. Genome-wide meta-analysis of macronutrient intake of 91,114 European ancestry participants from the cohorts for heart and aging research in genomic epidemiology consortium. Mol Psychiatry 24, 1920–1932 (2019). https://doi.org/10.1038/s41380-018-0079-4

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