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Cited by 1,580Genetic Associations and EpidemiologyAdipokines, Inflammation, and Metabolic DiseasesGenetics and Physical Performance

New genetic loci link adipose and insulin biology to body fat distribution

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The ADIPOGen Consortium, Shungin, Dmitry, The CARDIOGRAMplusC4D Consortium, The CKDGen Consortium, The GEFOS Consortium, The GENIE Consortium, The GLGC, The ICBP +411 more·2015·Nature
DOI 10.1038/nature14132PMC PMC4338562
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Abstract

Body fat distribution is a heritable trait and a well-established predictor of adverse metabolic outcomes, independent of overall adiposity. To increase our understanding of the genetic basis of body fat distribution and its molecular links to cardiometabolic traits, here we conduct genome-wide association meta-analyses of traits related to waist and hip circumferences in up to 224,459 individuals. We identify 49 loci (33 new) associated with waist-to-hip ratio adjusted for body mass index (BMI), and an additional 19 loci newly associated with related waist and hip circumference measures (P < 5 × 10(-8)). In total, 20 of the 49 waist-to-hip ratio adjusted for BMI loci show significant sexual dimorphism, 19 of which display a stronger effect in women. The identified loci were enriched for genes expressed in adipose tissue and for putative regulatory elements in adipocytes. Pathway analyses implicated adipogenesis, angiogenesis, transcriptional regulation and insulin resistance as processes affecting fat distribution, providing insight into potential pathophysiological mechanisms.

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  • Although Gao et al. use the most up-to-date body mass index GWAS data, they do not do the same for waist-hip ratio, despite the most recent GWAS for waist-hip ratio adjusted for body mass index identifying 33 additional variants and being published around the same time.

    “Interestingly, although Gao et al. use the most up-to-date BMI GWAS data, 20 they do not do the same for WHR, despite the most recent GWAS for WHR adjusted for BMI identifying 33 additional variants (as well as confirming the 14 used here from the earlier GWAS) and being published around the same time as the most up-to-date BMI GWAS.”

    From Commentary: Two-sample Mendelian randomization: opportunities and challenges (2016) · cites this paper as [21]

  • In both GWAS, the per allele effect of the genetic instrument on waist-hip ratio adjusted for body mass index is notably stronger in females than males.

    “In both GWAS, the results of the per allele effect of the genetic instrument on WHR adjusted for BMI is notably stronger in females than males.”

    From Commentary: Two-sample Mendelian randomization: opportunities and challenges (2016) · cites this paper as [21]

  • Seven of the 14 waist-hip ratio adjusted for body mass index variants used by Gao et al. were stronger in females compared with males, with 19 of the 44 variants in the more up-to-date GWAS being stronger in females (and one stronger in males).

    “Seven of the 14 WHR adjusted for BMI variants used by Gao and colleagues were stronger in females compared with males ( Table 2 ), with 19 of the 44 variants in the more up-to-date GWAS being stronger in females (and one stronger in males).”

    From Commentary: Two-sample Mendelian randomization: opportunities and challenges (2016) · cites this paper as [21]

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  1. [93]Bult CJ Blake JA Kadin JA Ringwald M Eppig JT Mouse Genome Database Group IEEE International Symposium on Bio-Informatics and Biomedical Engineering 29 32 R. J.

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Authors
The ADIPOGen Consortium, Shungin, D., The CARDIOGRAMplusC4D Consortium, The CKDGen Consortium, The GEFOS Consortium, The GENIE Consortium, The, G. L. G. C., The, I. C. B. P., The International Endogene Consortium, Study, T. L. C., The MAGIC Investigators, The MuTHER Consortium, The PAGE Consortium, The ReproGen Consortium, Winkler, T. W., Croteau-Chonka, D. C., Ferreira, T., Locke, A. E., Mägi, R., Strawbridge, R. J., Pers, T. H., Fischer, K., Justice, A. E., Workalemahu, T., Wu, J. M. W., Buchkovich, M. L., Heard-Costa, N. L., Roman, T. S., Drong, A. W., Song, C., Gustafsson, S., Day, F. R., Esko, T., Fall, T., Kutalik, Z., Luan, J., Randall, J. C., Scherag, A., Vedantam, S., Wood, A. R., Chen, J., Fehrmann, R., Karjalainen, J., Kahali, B., Liu, C.-T., Schmidt, E. M., Absher, D., Amin, N., Anderson, D., Beekman, M., Bragg-Gresham, J. L., Buyske, S., Demirkan, A., Ehret, G. B., Feitosa, M. F., Goel, A., Jackson, A. U., Johnson, T., Kleber, M. E., Kristiansson, K., Mangino, M., Mateo Leach, I., Medina-Gomez, C., Palmer, C. D., Pasko, D., Pechlivanis, S., Peters, M. J., Prokopenko, I., Stančáková, A., Ju Sung, Y., Tanaka, T., Teumer, A., Van Vliet-Ostaptchouk, J. V., Yengo, L., Zhang, W., Albrecht, E., Ärnlöv, J., Arscott, G. M., Bandinelli, S., Barrett, A., Bellis, C., Bennett, A. J., Berne, C., Blüher, M., Böhringer, S., Bonnet, F., Böttcher, Y., Bruinenberg, M., Carba, D. B., Caspersen, I. H., Clarke, R., Warwick Daw, E., Deelen, J., Deelman, E., Delgado, G., Doney, A. S. F., Eklund, N., Erdos, M. R., Estrada, K., Eury, E., Friedrich, N., Garcia, M. E., Giedraitis, V., Gigante, B., Go, A. S., Golay, A., Grallert, H., Grammer, T. B., Gräßler, J., Grewal, J., Groves, C. J., Haller, T., Hallmans, G., Hartman, C. A., Hassinen, M., Hayward, C., Heikkilä, K., Herzig, K.-H., Helmer, Q., Hillege, H. L., Holmen, O., Hunt, S. C., Isaacs, A., Ittermann, T., James, A. L., Johansson, I., Juliusdottir, T., Kalafati, I.-P., Kinnunen, L., Koenig, W., Kooner, I. K., Kratzer, W., Lamina, C., Leander, K., Lee, N. R., Lichtner, P., Lind, L., Lindström, J., Lobbens, S., Lorentzon, M., Mach, F., Magnusson, P. K. E., Mahajan, A., McArdle, W. L., Menni, C., Merger, S., Mihailov, E., Milani, L., Mills, R., Moayyeri, A., Monda, K. L., Mooijaart, S. P., Mühleisen, T. W., Mulas, A., Müller, G., Müller-Nurasyid, M., Nagaraja, R., Nalls, M. A., Narisu, N., Glorioso, N., Nolte, I. M., Olden, M., Rayner, N. W., Renstrom, F., Ried, J. S., Robertson, N. R., Rose, L. M., Sanna, S., Scharnagl, H., Scholtens, S., Sennblad, B., Seufferlein, T., Sitlani, C. M., Vernon Smith, A., Stirrups, K., Stringham, H. M., Sundström, J., Swertz, M. A., Swift, A. J., Syvänen, A.-C., Tayo, B. O., Thorand, B., Thorleifsson, G., Tomaschitz, A., Troffa, C., van Oort, F. V. A., Verweij, N., Vonk, J. M., Waite, L. L., Wennauer, R., Wilsgaard, T., Wojczynski, M. K., Wong, A., Zhang, Q., Hua Zhao, J., Brennan, E. P., Choi, M., Eriksson, P., Folkersen, L., Franco-Cereceda, A., Gharavi, A. G., Hedman, Å. K., Hivert, M.-F., Huang, J., Kanoni, S., Karpe, F., Keildson, S., Kiryluk, K., Liang, L., Lifton, R. P., Ma, B., McKnight, A. J., McPherson, R., Metspalu, A., Min, J. L., Moffatt, M. F., Montgomery, G. W., Murabito, J. M., Nicholson, G., Nyholt, D. R., Olsson, C., Perry, J. R. B., Reinmaa, E., Salem, R. M., Sandholm, N., Schadt, E. E., Scott, R. A., Stolk, L., Vallejo, E. E., Westra, H.-J., Zondervan, K. T., Amouyel, P., Arveiler, D., Bakker, S. J. L., Beilby, J., Bergman, R. N., Blangero, J., Brown, M. J., Burnier, M., Campbell, H., Chakravarti, A., Chines, P. S., Claudi-Boehm, S., Collins, F. S., Crawford, D. C., Danesh, J., de Faire, U., de Geus, E. J. C., Dörr, M., Erbel, R., Eriksson, J. G., Farrall, M., Ferrannini, E., Ferrières, J., Forouhi, N. G., Forrester, T., Franco, O. H., Gansevoort, R. T., Gieger, C., Gudnason, V., Haiman, C. A., Harris, T. B., Hattersley, A. T., Heliövaara, M., Hicks, A. A., Hingorani, A. D., Hoffmann, W., Hofman, A., Homuth, G., Humphries, S. E., Hyppönen, E., Illig, T., Jarvelin, M.-R., Johansen, B., Jousilahti, P., Jula, A. M., Kaprio, J., Kee, F., Keinanen-Kiukaanniemi, S. M., Kooner, J. S., Kooperberg, C., Kovacs, P., Kraja, A. T., Kumari, M., Kuulasmaa, K., Kuusisto, J., Lakka, T. A., Langenberg, C., Le Marchand, L., Lehtimäki, T., Lyssenko, V., Männistö, S., Marette, A., Matise, T. C., McKenzie, C. A., McKnight, B., Musk, A. W., Möhlenkamp, S., Morris, A. D., Nelis, M., Ohlsson, C., Oldehinkel, A. J., Ong, K. K., Palmer, L. J., Penninx, B. W., Peters, A., Pramstaller, P. P., Raitakari, O. T., Rankinen, T., Rao, D. C., Rice, T. K., Ridker, P. M., Ritchie, M. D., Rudan, I., Salomaa, V., Samani, N. J., Saramies, J., Sarzynski, M. A., Schwarz, P. E. H., Shuldiner, A. R., Staessen, J. A., Steinthorsdottir, V., Stolk, R. P., Strauch, K., Tönjes, A., Tremblay, A., Tremoli, E., Vohl, M.-C., Völker, U., Vollenweider, P., Wilson, J. F., Witteman, J. C., Adair, L. S., Bochud, M., Boehm, B. O., Bornstein, S. R., Bouchard, C., Cauchi, S., Caulfield, M. J., Chambers, J. C., Chasman, D. I., Cooper, R. S., Dedoussis, G., Ferrucci, L., Froguel, P., Grabe, H.-J., Hamsten, A., Hui, J., Hveem, K., Jöckel, K.-H., Kivimaki, M., Kuh, D., Laakso, M., Liu, Y., März, W., Munroe, P. B., Njølstad, I., Oostra, B. A., Palmer, C. N. A., Pedersen, N. L., Perola, M., Pérusse, L., Peters, U., Power, C., Quertermous, T., Rauramaa, R., Rivadeneira, F., Saaristo, T. E., Saleheen, D., Sinisalo, J., Eline Slagboom, P., Snieder, H., Spector, T. D., Thorsteinsdottir, U., Stumvoll, M., Tuomilehto, J., Uitterlinden, A. G., Uusitupa, M., van der Harst, P., Veronesi, G., Walker, M., Wareham, N. J., Watkins, H., Wichmann, H.-E., Abecasis, G. R., Assimes, T. L., Berndt, S. I., Boehnke, M., Borecki, I. B., Deloukas, P., Franke, L., Frayling, T. M., Groop, L. C., Hunter, D. J., Kaplan, R. C., O’Connell, J. R., Qi, L., Schlessinger, D., Strachan, D. P., Stefansson, K., van Duijn, C. M., Willer, C. J., Visscher, P. M., Yang, J., Hirschhorn, J. N., Carola Zillikens, M., McCarthy, M. I., Speliotes, E. K., North, K. E., Fox, C. S., Barroso, I., Franks, P. W., Ingelsson, E., Heid, I. M., Loos, R. J. F., Cupples, L. A., Morris, A. P., Lindgren, C. M., & Mohlke, K. L.
Affiliations
  • Lund University (SE)
  • University of Regensburg (DE)
  • Brigham and Women's Hospital (US)
  • University Medical Center Groningen (NL)
  • University of Michigan (US)
  • Centre for Human Genetics (GB)
  • Boston Children's Hospital (US)
  • University of North Carolina at Chapel Hill (US)
  • Harvard University (US)
  • Broad Institute (US)
  • Boston University (US)
  • Uppsala University (SE)
  • University of Cambridge (GB)
  • SIB Swiss Institute of Bioinformatics (CH)
  • University of Exeter (GB)
  • Rutgers, The State University of New Jersey (US)
  • The Kids Research Institute Australia (AU)
  • Johns Hopkins University (US)
  • Washington University in St. Louis (US)
  • King's College London (GB)
  • Heidelberg University (DE)
  • University of Eastern Finland (FI)
  • Erasmus MC (NL)
  • National Institute on Aging (US)
  • Universitätsmedizin Greifswald (DE)
  • Centre National de la Recherche Scientifique (FR)
  • Azienda Sanitaria di Firenze (IT)
  • Helmholtz Munich (DE)
  • Dalarna University (SE)
  • University of Oxford (GB)
  • Texas Biomedical Research Institute (US)
  • Inserm (FR)
  • Leiden University Medical Center (NL)
  • University of Southern California (US)
  • University of Helsinki (FI)
  • National Institutes of Health (US)
  • Kaiser Permanente (US)
  • University Hospital of Geneva (CH)
  • University Hospital Carl Gustav Carus (DE)
  • Western General Hospital (GB)
  • University of Utah (US)
  • Norwegian University of Science and Technology (NO)
  • The University of Western Australia (AU)
  • University Hospital Ulm (DE)
  • Harokopio University of Athens (GR)
  • Innsbruck Medical University (AT)
  • Ealing Hospital NHS Trust (GB)
  • Karolinska Institutet (SE)
  • University of Bristol (GB)
  • University of Bonn (DE)
  • University of Sassari (IT)
  • Medical University of Graz (AT)
  • Institute of Genetic and Biomedical Research (IT)
  • University of Washington (US)
  • Science for Life Laboratory (SE)
  • MRC Unit for Lifelong Health and Ageing (GB)
  • University College Dublin (IE)
  • Seoul National University (KR)
  • Shanghai Jiao Tong University (CN)
  • Queen Mary University of London (GB)
  • Howard Hughes Medical Institute (US)
  • Queen's University Belfast (GB)
  • QIMR Berghofer Medical Research Institute (AU)
  • National Heart, Lung, and Blood Institute (US)
  • Helsinki University Hospital (FI)
  • Université de Strasbourg (FR)
  • Cedars-Sinai Medical Center (US)
  • Centre Hospitalier Universitaire Vaudois (CH)
  • Vanderbilt University (US)
  • University of Pisa (IT)
  • Essen University Hospital (DE)
  • University of the West Indies (JM)
  • University of Iceland (IS)
  • Eurac Research (IT)
  • University College London (GB)
  • University of South Australia (AU)
  • Finnish Institute for Health and Welfare (FI)
  • Imperial College Healthcare NHS Trust (GB)
  • Tampere University (FI)
  • Steno Diabetes Centers (DK)
  • Sir Charles Gairdner Hospital (AU)
  • University of Dundee (GB)
  • University of Toronto (CA)
  • Vrije Universiteit Amsterdam (NL)
  • Ontario Institute for Cancer Research (CA)
  • Pennington Biomedical Research Center (US)
  • Pennsylvania State University (US)
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  • University of Milan (IT)
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  • Université de Lille (FR)
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  • Institut für Medizinische Informatik, Biometrie und Epidemiologie (DE)
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  • Finnish Diabetes Association (FI)
  • deCODE Genetics (Iceland) (IS)
  • University of Insubria (IT)
  • Albert Einstein College of Medicine (US)
  • The University of Queensland (AU)
Corresponding author
  • Lindgren, Cecilia M.
  • Mohlke, Karen L
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2015-02-11
Volume
518
Issue
7538
Pages
187-196
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/nature14132
PMC
PMC4338562
OpenAlex
W2047783882
Cited by
1,580
References
101
Citations by year
2026: 56 · 2025: 120 · 2024: 129 · 2023: 177 · 2022: 158 · 2021: 167 · 2020: 122 · 2019: 142 · 2018: 161 · 2017: 156 · 2016: 118 · 2015: 71 · 2014: 1
FWCI
21.79
Type
journal article
Language
en
Open access
Licence
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Funders
  • McKnight Foundation
  • Pennsylvania State University (16802)
  • Wellcome Trust (098017, 098381, 098498, 085235, 097117, WT098017, 100574, 084766, WT098381, WT100574, WT097117, WT084766, WT098498, WT085235)
  • Cancer Research UK (CRUK_14136, 14136)
  • National Institute for Health and Care Research (NF-SI-0512-10165, NF-SI-0513-10109, NF-SI-0611-10170, NF-SI-0512-10113, NF-SI-0508-10082, NF-SI-0507-10380, NF-SI-0611-10099, NF-SI-0512-10114, NF-SI-0611-10219, NF-SI-0513-10085, NF-SI-0514-10027, NF-SI-0512-10135)
  • British Heart Foundation (BHF_FS/14/55/30806, FS/14/55/30806, BHF_RG/13/2/30098, RG/08/008/25291, BHF_RG/10/12/28456, BHF_RG/08/008/25291, RG/10/12/28456, BHF_RG/08/014/24067, RG/13/2/30098, RG/07/008/23674, RG/08/014/24067)
  • Diabetes UK (DUK_12/0004470, 12/0004470)
  • University of Leicester
  • University of Warwick
  • European Commission (259679)
  • Vrije Universiteit Amsterdam
  • Bundesministerium für Bildung und Forschung (01EO1001)
  • Lundbeckfonden (R190 2014-3904)
  • Turun Yliopisto
  • Novo Nordisk Fonden (NNF14OC0010513, NNF12OC1016467, NNF13OC0005785, NNF15OC0016416, NNF14OC0011039, NNF13OC0005781, NNF12OC1016167, NNF11OC1014855)
  • Turun Yliopistollinen Keskussairaala
  • National Institutes of Health (1r01hl120393-01a1)
  • Medical Research Council (MC_U106179472, MR/K013351/1, MR/K006584/1, MC_UU_12015/5, MR/N01104X/1, MC_PC_U127561128, MR/L003120/1, MR/K011480/1, MC_UP_A100_1003, MC_UU_12015/2, G0601261, MC_UP_A620_1014, G0601463, MC_UU_12011/1, MC_UU_12015/1, G1000143, G1001799)
  • Economic and Social Research Council (ES/J023299/1, ES/F02679X/1)
  • National Institute on Aging (U01AG049505, R01AG025941, R01AG033193, R01AG041517)
  • National Heart, Lung, and Blood Institute (R00HL094535, R01-HL120393, R01HL105756, K01HL116770, R01HL117078, R01HL117626, T32HL069768, T32HL007055, R01HL109946)
  • National Institute on Drug Abuse (R21DA027040)
  • National Human Genome Research Institute (Z01HG000024, U01HG007416, U01HG007417, U01HG007419, U01HG007376)
  • National Cancer Institute (UM1CA182913, UM1CA182910, P30CA071789)
  • National Institute of General Medical Sciences (T32GM007092, T32GM067553, P30GM103341)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R01DK078150, R01DK072193, R01DK089256, U01DK062370, R01DK107437, K23DK080145, P30DK079637, P30DK072488, P60DK020541, R01DK075787, P30DK020572, P30DK056341, R01DK093757, P30DK020541, P30DK040561, R01DK062370)
  • NIH Clinical Center
  • National Institute on Minority Health and Health Disparities (P20MD006899)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD083211)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Physical Performance
Keywords
body fat distribution, waist-to-hip ratio, waist circumference, hip circumference, genetic loci, adipose tissue, adipogenesis, angiogenesis, insulin resistance, transcriptional regulation, sexual dimorphism, abdominal fat, cardiometabolic traits, regulatory elements
MeSH terms
Adipose Tissue, Age Factors, Europe, Female, Humans, Insulin, Insulin Resistance, Male, Models, Biological, Obesity, Sex Characteristics, Transcription, Genetic, Genome, Human, Body Mass Index, Adipocytes, Neovascularization, Physiologic, Polymorphism, Single Nucleotide, Quantitative Trait Loci, Epigenesis, Genetic, Racial Groups, Waist-Hip Ratio, Adipogenesis, Body Fat Distribution, Genome-Wide Association Study

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