Multi-ancestry genome-wide gene-smoking interaction study of 387,272 individuals identifies new loci associated with serum lipids

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Abstract

The concentrations of high- and low-density lipoprotein cholesterol and triglycerides are influenced by smoking, but it is unknown whether genetic associations with lipids may be modified by smoking. We conducted a multi-ancestry genome-wide gene-smoking interaction study in 133,805 individuals with follow-up in an additional 253,467 individuals. Combined meta-analyses identified 13 novel loci, some of which were detected only because the association differed by smoking status. Additionally, we demonstrated the importance of including diverse populations, particularly in studies of interactions with lifestyle factors, where genomic and lifestyle differences by ancestry may contribute to novel findings.

Editorial summary:

A multi-ancestry genome-wide gene-smoking interaction study identifies 13 new loci associated with serum lipids.

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Most cited references 35

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A human phenome-interactome network of protein complexes implicated in genetic disorders.

Kasper Lage, E Olof Karlberg, Zenia Størling … (2007)

We performed a systematic, large-scale analysis of human protein complexes comprising gene products implicated in many different categories of human disease to create a phenome-interactome network. This was done by integrating quality-controlled interactions of human proteins with a validated, computationally derived phenotype similarity score, permitting identification of previously unknown complexes likely to be associated with disease. Using a phenomic ranking of protein complexes linked to human disease, we developed a Bayesian predictor that in 298 of 669 linkage intervals correctly ranks the known disease-causing protein as the top candidate, and in 870 intervals with no identified disease-causing gene, provides novel candidates implicated in disorders such as retinitis pigmentosa, epithelial ovarian cancer, inflammatory bowel disease, amyotrophic lateral sclerosis, Alzheimer disease, type 2 diabetes and coronary heart disease. Our publicly available draft of protein complexes associated with pathology comprises 506 complexes, which reveal functional relationships between disease-promoting genes that will inform future experimentation.

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Exome-wide association study of plasma lipids in >300,000 individuals

Dajiang J Liu, Gina M. Peloso, Haojie Yu … (2017)

We screened DNA sequence variants on an exome-focused genotyping array in >300,000 participants with replication in >280,000 participants and identified 444 independent variants in 250 loci significantly associated with total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), and/or triglycerides (TG). At two loci (JAK2 and A1CF), experimental analysis in mice revealed lipid changes consistent with the human data. We utilized mapped variants to address four clinically relevant questions and found the following: (1) beta-thalassemia trait carriers displayed lower TC and were protected from coronary artery disease; (2) outside of the CETP locus, there was not a predictable relationship between plasma HDL-C and risk for age-related macular degeneration; (3) only some mechanisms of lowering LDL-C seemed to increase risk for type 2 diabetes; and (4) TG-lowering alleles involved in hepatic production of TG-rich lipoproteins (e.g., TM6SF2, PNPLA3) tracked with higher liver fat, higher risk for type 2 diabetes, and lower risk for coronary artery disease whereas TG-lowering alleles involved in peripheral lipolysis (e.g., LPL, ANGPTL4) had no effect on liver fat but lowered risks for both type 2 diabetes and coronary artery disease.

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Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Consortium: Design of prospective meta-analyses of genome-wide association studies from 5 cohorts.

Bruce M. Psaty, Christopher J O'Donnell, Vilmundur Gudnason … (2009)

The primary aim of genome-wide association studies is to identify novel genetic loci associated with interindividual variation in the levels of risk factors, the degree of subclinical disease, or the risk of clinical disease. The requirement for large sample sizes and the importance of replication have served as powerful incentives for scientific collaboration. Methods- The Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium was formed to facilitate genome-wide association studies meta-analyses and replication opportunities among multiple large population-based cohort studies, which collect data in a standardized fashion and represent the preferred method for estimating disease incidence. The design of the Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium includes 5 prospective cohort studies from the United States and Europe: the Age, Gene/Environment Susceptibility-Reykjavik Study, the Atherosclerosis Risk in Communities Study, the Cardiovascular Health Study, the Framingham Heart Study, and the Rotterdam Study. With genome-wide data on a total of about 38 000 individuals, these cohort studies have a large number of health-related phenotypes measured in similar ways. For each harmonized trait, within-cohort genome-wide association study analyses are combined by meta-analysis. A prospective meta-analysis of data from all 5 cohorts, with a properly selected level of genome-wide statistical significance, is a powerful approach to finding genuine phenotypic associations with novel genetic loci. The Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium and collaborating non-member studies or consortia provide an excellent framework for the identification of the genetic determinants of risk factors, subclinical-disease measures, and clinical events.

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Author and article information

Journal

Journal ID (nlm-journal-id): 9216904

Journal ID (pubmed-jr-id): 2419

Journal ID (nlm-ta): Nat Genet

Journal ID (iso-abbrev): Nat. Genet.

Title: Nature genetics

ISSN (Print): 1061-4036

ISSN (Electronic): 1546-1718

Publication date Nihms-submitted: 12 February 2019

Publication date (Electronic): 29 March 2019

Publication date (Print): April 2019

Publication date PMC-release: 29 September 2019

Volume: 51

Issue: 4

Pages: 636-648

Affiliations

[1. ]Center for Research on Genomics and Global Health, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland, USA.

[2. ]Division of Biostatistics, Washington University School of Medicine, St. Louis, Missouri, USA.

[3. ]Human Genetics Center, Department of Epidemiology, Human Genetics, and Environmental Sciences, School of Public Health, The University of Texas Health Science Center at Houston, Houston, Texas, USA.

[4. ]Department of Genetic Epidemiology, University of Regensburg, Regensburg, Germany.

[5. ]Division of Statistical Genomics, Department of Genetics, Washington University School of Medicine, St. Louis, Missouri, USA.

[6. ]Clinical Pharmacology, William Harvey Research Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, UK.

[7. ]Division of Preventive Medicine, Brigham and Women's Hospital, Boston, Massachusetts, USA.

[8. ]Harvard Medical School, Boston, Massachusetts, USA.

[9. ]Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts, USA.

[10. ]The Institute for Translational Genomics and Population Sciences, Department of Pediatrics, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, California, USA.

[11. ]WHI CCC, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA.

[12. ]The Charles Bronfman Institute for Personalized Medicine, The Icahn School of Medicine at Mount Sinai, New York, New York, USA.

[13. ]Singapore Eye Research Institute, Singapore National Eye Centre, Singapore, Singapore, Singapore.

[14. ]Centre for Quantitative Medicine, Academic Medicine Research Institute, Ophthalmology & Visual Sciences Academic Clinical Program (Eye ACP), Duke-NUS Medical School, Singapore, Singapore, Singapore.

[15. ]Department of Ophthalmology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore, Singapore.

[16. ]Saw Swee Hock School of Public Health, National University of Singapore and National University Health System, Singapore, Singapore.

[17. ]Department of Epidemiology, Erasmus University Medical Center, Rotterdam, The Netherlands.

[18. ]Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh, United Kingdom.

[19. ]Jackson Heart Study, Department of Medicine, University of Mississippi Medical Center, Jackson, Mississippi, USA.

[20. ]Epidemiology and Biostatistics, University of Georgia at Athens College of Public Health, Athens, Georgia, USA.

[21. ]Brown Foundation Institute of Molecular Medicine, The University of Texas Health Science Center at Houston, Houston, Texas, US.

[22. ]Internal Medicine, Gerontology and Geriatrics, Leiden University Medical Center, Leiden, Netherlands.

[23. ]Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), Institut Pasteur, Paris, France.

[24. ]Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, USA.

[25. ]Cardiovascular Health Research Unit, Biostatistics and Medicine, University of Washington, Seattle, Washington, USA.

[26. ]Center on Diabetes, Obesity, and Metabolism, Gerontology and Geriatric Medicine, Wake Forest University Health Sciences, Winston-Salem, North Carolina, USA.

[27. ]Genome Institute of Singapore, Agency for Science Technology and Research, Singapore, Singapore.

[28. ]Clinical and Translational Epidemiology Unit, Massachusetts General Hospital, Boston, Massachusetts, USA.

[29. ]Department of Medicine, Harvard Medical School, Boston, Massachusetts, USA.

[30. ]Human Genomics Laboratory, Pennington Biomedical Research Center, Baton Rouge, Louisiana, USA.

[31. ]Icelandic Heart Association, Kopavogur, Iceland.

[32. ]Faculty of Medicine, University of Iceland, Reykjavik, Iceland.

[33. ]Health Disparities Research Section, Laboratory of Epidemiology and Population Sciences, National Institute on Aging, National Institutes of Health, Baltimore, Maryland, USA.

[34. ]Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, Michigan, USA.

[35. ]Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina, USA.

[36. ]Estonian Genome Center, Institute of Genomics, University of Tartu, Tartu, Estonia.

[37. ]CNRS UMR 8199, European Genomic Institute for Diabetes (EGID), Institut Pasteur de Lille, University of Lille, Lille, France.

[38. ]Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Stockholm, Sweden.

[39. ]Department of Biostatistics and Data Science, Division of Public Health Sciences, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.

[40. ]Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK.

[41. ]Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina, Greece.

[42. ]Molecular Genetics and Genomics Program, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.

[43. ]Division of Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, Oxfordshire, UK.

[44. ]Wellcome Centre for Human Genetics, University of Oxford, Oxford, Oxfordshire, UK.

[45. ]University of Groningen, University Medical Center Groningen, Department of Cardiology, Groningen, The Netherlands.

[46. ]Centre for Cognitive Ageing and Cognitive Epidemiology, The University of Edinburgh, Edinburgh, UK.

[47. ]Medical Genetics Section, University of Edinburgh Centre for Genomic and Experimental Medicine and MRC Institute of Genetics and Molecular Medicine, The University of Edinburgh, Edinburgh, UK.

[48. ]Postgraduate Programme in Epidemiology, Federal University of Pelotas, Pelotas, RS, Brazil.

[49. ]Medical Research Council Integrative Epidemiology Unit, University of Bristol, Bristol, UK.

[50. ]Department of Occupational and Environmental Health and State Key Laboratory of Environmental Health for Incubating, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China.

[51. ]Laboratory of Genetics and Molecular Cardiology, Heart Institute (InCor), University of São Paulo Medical School, São Paulo, SP, Brazil.

[52. ]Endocrinology and Metabolism, Tri-Service General Hospital, Taipei, Taiwan.

[53. ]School of Medicine, National Defense Medical Center, Taipei, Taiwan.

[54. ]Department of Biostatistics and Center for Statistical Genetics, University of Michigan, Ann Arbor, Michigan, USA.

[55. ]Department of Public Health, Faculty of Medicine, University of Kelaniya, Ragama, Sri Lanka.

[56. ]Foundation for Research in Health Exercise and Nutrition, Kuopio Research Institute of Exercise Medicine, Kuopio, Finland.

[57. ]Research Unit of Molecular Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.

[58. ]Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.

[59. ]Unit of Cardiovascular Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

[60. ]Ophthalmology, Taichung Veterans General Hospital, Taichung, Taiwan.

[61. ]MRC Epidemiology Unit, University of Cambridge, Cambridge, UK.

[62. ]Department of Clinical Chemistry, Fimlab Laboratories, Tampere, Finland.

[63. ]Department of Clinical Chemistry, Finnish Cardiovascular Research Center - Tampere, Faculty of Medicine and Technology, Tampere University, Tampere, Finland.

[64. ]Laboratory for Statistical Analysis, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.

[65. ]University of Groningen, University Medical Center Groningen, Department of Epidemiology, Groningen, The Netherlands.

[66. ]DZHK (German Centre for Cardiovascular Health), Partner Site Greifswald, Greifswald, Germany.

[67. ]Institute of Clinical Chemistry and Laboratory Medicine, University Medicine Greifswald, Greifswald, Germany.

[68. ]Human Genetics, Wellcome Trust Sanger Institute, Hinxton, UK.

[69. ]Department of Cardiovascular Sciences, University of Leicester, Leicester, UK.

[70. ]NIHR Leicester Biomedical Research Centre, Glenfield Hospital, Leicester, UK.

[71. ]Institute for Maternal and Child Health - IRCCS "Burlo Garofolo", Trieste, Italy.

[72. ]Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, Columbia University Medical Center, New York, New York, USA.

[73. ]Division of Sleep and Circadian Disorders, Brigham and Women's Hospital, Boston, Massachusetts, USA.

[74. ]Institute of Clinical Medicine, Internal Medicine, University of Eastern Finland, Kuopio, Finland.

[75. ]Department of Gene Diagnostics and Therapeutics, Research Institute, National Center for Global Health and Medicine, Tokyo, Japan.

[76. ]Department of Public Health Sciences, Loyola University Chicago, Maywood, Illinois, USA.

[77. ]Department of Clinical Sciences, Genetic and Molecular Epidemiology Unit, Lund University Diabetes Centre, Skåne University Hospital, Malmö, Sweden.

[78. ]Cardiovascular Center and Division of Cardiology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan.

[79. ]National Taiwan University College of Medicine, Taipei, Taiwan.

[80. ]Department of Population Quantitative and Health Sciences, Case Western Reserve University, Cleveland, Ohio, USA.

[81. ]Survey Research Center, Institute for Social Research, University of Michigan, Ann Arbor, Michigan, USA.

[82. ]Division of Epidemiology, Department of Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.

[83. ]SKLORG & Department of Epidemiology, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China.

[84. ]Division of General Internal Medicine, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

[85. ]MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London, London, UK.

[86. ]Department of Cardiology, Ealing Hospital, Middlesex, UK.

[87. ]McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

[88. ]Ophthalmology & Visual Sciences Academic Clinical Program (Eye ACP), Duke-NUS Medical School, Singapore, Singapore, Singapore.

[89. ]Section of Cardiovascular Research, Baylor College of Medicine, Houston, Texas, USA.

[90. ]Houston Methodist Debakey Heart and Vascular Center, Houston, Texas, USA.

[91. ]Departments of Medicine and Epidemiology, Columbia University Medical Center, New York, New York, USA.

[92. ]Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas, USA.

[93. ]Section of Genomic Pediatrics, Department of Pediatrics, Medicine and Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.

[94. ]NIHR Barts Cardiovascular Biomedical Research Centre, Queen Mary University of London, London, London, UK.

[95. ]Centre for Genomic & Experimental Medicine, Institute of Genetics & Molecular Medicine, University of Edinburgh, Edinburgh, United Kingdom.

[96. ]The Danish Aging Research Center, Institute of Public Health, University of Southern Denmark, Odense, Denmark.

[97. ]A full list of authors can be found in the Supplementary Note.

[98. ]Ninewells Hospital & Medical School, University of Dundee, Dundee, Scotland, UK.

[99. ]Cardiovascular Division, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri, USA.

[100. ]Department of Medicine, Faculty of Medicine, University of Kelaniya, Ragama, Sri Lanka.

[101. ]Department of Genetics, University of North Carolina, Chapel Hill, North Carolina, USA.

[102. ]Department of Family Medicine and Epidemiology, Alpert Medical School of Brown University, Providence, Rhode Island, USA.

[103. ]Cardiovascular Health Research Unit, Medicine and Epidemiology, University of Washington, Seattle, Washington, USA.

[104. ]UWI Solutions for Developing Countries, University of the West Indies, Kingston, Jamaica.

[105. ]Braun School of Public Health, Hebrew University-Hadassah Medical Center, Jerusalem, Israel.

[106. ]Department of Medical Sciences, University of Trieste, Trieste, Italy.

[107. ]Department of Genetics, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

[108. ]Computational Medicine Core, Center for Lung Biology, UW Medicine Sleep Center, Medicine, University of Washington, Seattle, Washington, USA.

[109. ]Department Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.

[110. ]Laboratory of Epidemiology and Population Sciences, National Institute on Aging, National Institutes of Health, Bethesda, Maryland, USA.

[111. ]Institute of Biomedicine, School of Medicine, University of Eastern Finland, Kuopio Campus, Finland.

[112. ]Department of Paediatrics, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.

[113. ]Khoo Teck Puat – National University Children's Medical Institute, National University Health System, Singapore, Singapore.

[114. ]Laboratory of Genome Technology, Human Genome Center, Institute of Medical Science, The University of Tokyo, Minato-ku, Japan.

[115. ]Department of Radiology and Nuclear Medicine, Erasmus University Medical Center, Rotterdam, The Netherlands.

[116. ]Department of Neurology, Erasmus University Medical Center, Rotterdam, The Netherlands.

[117. ]Hebrew SeniorLife, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA.

[118. ]Framingham Heart Study, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland, USA.

[119. ]Collaborative Health Studies Coordinating Center, University of Washington, Seattle, Washington, USA.

[120. ]Department of Ophthalmology, Medical Faculty Mannheim, University Heidelberg, Mannheim, Germany, Germany.

[121. ]Beijing Institute of Ophthalmology, Beijing Ophthalmology and Visual Science Key Lab, Beijing Tongren Eye Center, Capital Medical University, Beijing, China, China.

[122. ]Department of Clinical Gene Therapy, Osaka University Graduate School of Medicine, Suita, Japan.

[123. ]Department of Geriatric and General Medicine, Osaka University Graduate School of Medicine, Suita, Japan.

[124. ]Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen 2200, Denmark.

[125. ]Department of Environmental Medicine and Public Health, The Icahn School of Medicine at Mount Sinai, New York, New York, USA.

[126. ]Duke-NUS Medical School, Singapore, Singapore.

[127. ]Department of Public Health, Department of Medicine, University of Split, Split, Croatia.

[128. ]Fred Hutchinson Cancer Research Center, University of Washington School of Public Health, Seattle, Washington, USA.

[129. ]Sticht Center for Healthy Aging and Alzheimer's Prevention, Department of Internal Medicine, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.

[130. ]RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.

[131. ]Department of Clinical Physiology and Nuclear Medicine, Kuopio University Hospital, Kuopio, Finland.

[132. ]Institute of Clinical Sciences, Department of Molecular Sciences, Imperial College London, London, UK.

[133. ]Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, USA.

[134. ]Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.

[135. ]Epidemiology, Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

[136. ]Translational Laboratory in Genetic Medicine, Agency for Science, Technology and Research, Singapore.

[137. ]Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.

[138. ]Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.

[139. ]Department of Biostatistics, University of Washington, Seattle, Washington, USA.

[140. ]Center for Public Health Genomics, University of Virginia, Charlottesville, Virginia, USA.

[141. ]Tropical Metabolism Research Unit, Caribbean Institute for Health Research, University of the West Indies, Mona, Jamaica.

[142. ]Institute of Human Genetics, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.

[143. ]Institute of Human Genetics, Technische Universität München, Munich, Germany.

[144. ]Technische Universität München, Munich, Germany.

[145. ]Department of Psychiatry, Amsterdam Neuroscience and Amsterdam Public Health Research Institute, Amsterdam UMC, Vrije Universiteit, Amsterdam, The Netherlands.

[146. ]Laboratory for Genotyping Development, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.

[147. ]Department of Biostatistics, University of Liverpool, Liverpool, UK.

[148. ]The Institute of Medical Sciences, Aberdeen Biomedical Imaging Centre, University of Aberdeen, Aberdeen, United Kingdom.

[149. ]Data Tecnica International, Glen Echo, MD, USA.

[150. ]Laboratory of Neurogenetics, National Institute on Aging, Bethesda, MD, USA.

[151. ]Division of Endocrinology, Diabetes, and Nutrition, University of Maryland School of Medicine, Baltimore, Maryland, USA.

[152. ]Program for Personalized and Genomic Medicine, University of Maryland School of Medicine, Baltimore, Maryland, USA.

[153. ]Biochemistry, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.

[154. ]Epidemiology Branch, Division of Cardiovascular Sciences, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland,.

[155. ]Chair of Epidemiology, Faculty of Medicine, IBE, LMU, Munich, Germany.

[156. ]Psychiatric Hospital "Sveti Ivan", Zagreb, Croatia.

[157. ]Gen-info Ltd, Zagreb, Croatia.

[158. ]School of Public Health, Imperial College London, London, UK.

[159. ]Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku, Finland.

[160. ]Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, Turku, Finland.

[161. ]Department of Biobank Research, Umeå University, Umeå, Västerbotten, Sweden.

[162. ]Department of Epidemiology and Medicine, University of Iowa, Iowa City, Iowa, USA.

[163. ]Clinical Epidemiology, Leiden University Medical Center, Leiden, Netherlands.

[164. ]Centre for Global Health Research, Usher Institute of Population Health Sciences and Informatics, University of Edinburgh, Edinburgh, United Kingdom.

[165. ]Institute for Community Medicine, University Medicine Greifswald, Greifswald, Germany.

[166. ]Division of Epidemiology & Community Health, School of Public Health, University of Minnesota, Minneapolis, Minnesota, USA.

[167. ]National Heart and Lung Institute, Imperial College London, London, UK.

[168. ]Division of Research, Kaiser Permanente Northern California, Oakland, California, USA.

[169. ]Alzheimer Scotland Dementia Research Centre, The University of Edinburgh, Edinburgh, UK.

[170. ]Chair of Genetic Epidemiology, IBE, Faculty of Medicine, LMU, Munich, Germany.

[171. ]Institute of Genetic Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.

[172. ]Department of Genetics, Stanford University, Stanford, California, USA.

[173. ]Department of Statistics and Applied Probability, National University of Singapore, Singapore, Singapore.

[174. ]Life Sciences Institute, National University of Singapore, Singapore, Singapore.

[175. ]NUS Graduate School for Integrative Science and Engineering, National University of Singapore, Singapore, Singapore.

[176. ]Department of Social and Behavioral Sciences, Harvard TH Chan School of Public Health, Boston, Massachusetts, USA.

[177. ]Division of Nephrology and Hypertension, Mayo Clinic, Rochester, Minnesota, USA.

[178. ]Department of Internal Medicine, Erasmus University Medical Center, Rotterdam, The Netherlands.

[179. ]Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China, China.

[180. ]Jackson Heart Study, School of Public Health, Jackson State University, Jackson, Mississippi, USA.

[181. ]Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.

[182. ]Division of Cancer Control and Population Sciences, UPMC Hillman Cancer, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.

[183. ]Behavioral Epidemiology Section, Laboratory of Epidemiology and Population Sciences, National Institute on Aging, National Institutes of Health, Baltimore, Maryland, USA.

[184. ]Imperial College Healthcare NHS Trust, London, UK.

[185. ]Psychology, The University of Edinburgh, Edinburgh, UK.

[186. ]Broad Institute of the Massachusetts Institute of Technology and Harvard University, Boston, Massachusetts, USA.

[187. ]Harvard T. H. Chan School of Public Health, Department of Nutrition, Harvard University, Boston, Massachusetts, USA.

[188. ]Department of Public Health & Clinical Medicine, Umeå University, Umeå, Västerbotten, Sweden.

[189. ]OCDEM, Radcliffe Department of Medicine, University of Oxford, Oxford, UK.

[190. ]Nephrology, Internal Medicine, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.

[191. ]Department of Genomics of Common Disease, Imperial College London, London, United Kingdom.

[192. ]German Center for Diabetes Research (DZD e.V.), Neuherberg, Germany.

[193. ]Division of Cardiology, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan.

[194. ]Department of Human Genetics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.

[195. ]Endocrinology and Metabolism, Internal Medicine, Taichung Veterans General Hospital, Taichung, Taiwan.

[196. ]School of Medicine, Chung Shan Medical University, Taichung, Taiwan.

[197. ]School of Medicine, National Yang-Ming University, Taipei, Taiwan.

[198. ]University of Groningen, University Medical Center Groningen, Department of Psychiatry, Groningen, The Netherlands.

[199. ]University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, The Netherlands.

[200. ]Public Health Sciences, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.

[201. ]Institute of Translational Genomics, Helmholtz Zentrum München, Neuherberg, Germany.

[202. ]Public Health Sciences, Epidemiology and Prevention, Wake Forest University Health Sciences, Winston-Salem, North Carolina, USA.

[203. ]Cardiovascular Health Research Unit, Epidemiology, Medicine and Health Services, University of Washington, Seattle, Washington, USA.

[204. ]Kaiser Permanente Washington Health Research Institute, Seattle, Washington, USA.

[205. ]Public Health and Primary Care, Leiden University Medical Center, Leiden, Leiden.

[206. ]Brown Foundation Institute of Molecular Medicine, The University of Texas Health Science Center at Houston, Houston, Texas, USA.

[207. ]Epidemiology, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana, USA.

[208. ]Cardiology, Medicine, University of Mississippi Medical Center, Jackson, Mississippi, USA.

[209. ]Nuffield Department of Population Health, University of Oxford, Oxford, UK.

[210. ]The Mindich Child Health Development Institute, The Icahn School of Medicine at Mount Sinai, New York, New York, USA.

[211. ]Psychiatry, Washington University School of Medicine, St. Louis, Missouri, USA.

[212. ]Biostatistics, Preventive Medicine, University of Southern California, Los Angeles, California, USA.

[213. ]These authors constitute the writing group.

Author notes

Correspondence to: Amy R Bentley ( amy.bentley@ 123456nih.gov ), Charles N Rotimi ( rotimic@ 123456nih.gov ), and L Adrienne Cupples ( adrienne@ 123456bu.edu ), 1. Center for Research on Genomics and Global Health, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892; (301) 451-2302, 2. Department of Biostatistics, Boston University, Boston, MA and Framingham Heart Study, Framingham, MA 02118; (617) 638-5176

[*]

These authors contributed equally to this work.

[**]

These authors jointly directed this work.

Article

Manuscript ID: NIHMS1521094

DOI: 10.1038/s41588-019-0378-y

PMC ID: 6467258

PubMed ID: 30926973

SO-VID: c333431e-1f7b-437d-b2cc-4c075bef3e21

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Multi-ancestry genome-wide gene-smoking interaction study of 387,272 individuals identifies new loci associated with serum lipids

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Most cited references 35

A human phenome-interactome network of protein complexes implicated in genetic disorders.

Exome-wide association study of plasma lipids in >300,000 individuals

Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Consortium: Design of prospective meta-analyses of genome-wide association studies from 5 cohorts.

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