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New genetic loci link adipose and insulin biology to body fat distribution
Open accessAbstract
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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“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]
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“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]
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“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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“The genetic locus on chromosome 4 harbouring FAM13A has previously been linked to body fat distribution [40], and the chromosome 7 locus harbouring POM121C has been linked to BMI [41].”
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ResultHan, X., Qassim, A., An, J., Marshall, H. N., Zhou, T., Ong, J., Hassall, M., Hysi, P. G., Foster, P. J., Khaw, P. T., et al. (2019) · Human Molecular Genetics · doi:10.1093/hmg/ddz193 · Cited by 30
“The lead SNP rs2152876 in CENPW exhibits a pleiotropic effect, as its proxy SNPs ( R 2 > 0.8) are associated with intraocular pressure (38), height (39), hip circumference (40) and the age onset of menarche (41).”
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“The WC SNPs were obtained from the publicly available Genetic Investigation of Anthropometric Traits (GIANT) consortium [23], Since we could not find significantly associated SNPs in our GWAS analysis.”
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Self-citationMicroRNA-196a links human body fat distribution to adipose tissue extracellular matrix composition
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“We used the index SNPs as reported in the initial genome-wide association study of WHR performed in GIANT [14].”
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“Hundreds of GWAS loci for cardiometabolic traits are colocalized with eQTL in adipose tissue [3–5], and variants at GWAS loci for some cardiometabolic traits, such as waist-to-hip ratio adjusted for body mass index (BMI) and high-density lipoprotein (HDL) cholesterol, are overrepresented in transcriptional regulatory…”
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“61 × 10−10 Waist format 2: Waist hip ratio [55] WHR 2015 143,480 Esophagus—Muscularis 0.”
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“The strongest GWAS signal for BMI is the FTO locus, for WC the MC4R locus and for WHRadjBMI the RSPO3 locus [69].”
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“232,101 (2,565,408 SNPs) and 73,137 (2,738,303 SNPs) European individuals from GIANT Consortium into the study [15].”
BackgroundMethodDiabetic retinopathy risk in patients with unhealthy lifestyle: A Mendelian randomization study
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“Single nucleotide variants (singlenucleotide polymorphisms [SNPs]) for BMI were retrieved from the Neale Lab consortium, and the rest were retrieved from a published meta-analysis of genome-wide association studies (GWAS) datasets summarized by Shungin (10) (datasets: ukb-a-248, ieu-a-79, ieu-a-55, ieu-a-67).”
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“Heterogeneity between depots is controlled at the genetic level with distinct genetic loci influencing local adipose behavior.(7) Proteomics analysis comparing different white adipose”
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“The GWAS data for waist circumference, hip circumference, and waist-to-hip ratio involved 210,088 European participants and adjusted for age, age square, and study-speci fi c covariates as needed [19] (online suppl.”
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“Consistent with the presence of different regulatory mechanisms related to human body shape, GWAS from the GIANT consortium identified several loci with sex-specific effects and most of them have larger effects in women than in men [30, 32].”
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“related traits, including waist-to-hip ratio and various body fat indices (20,21).”
BackgroundThe geometry of clinical labs and wellness states from deeply phenotyped humans
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Self-citationNew insights from monogenic diabetes for “common” type 2 diabetes
Tallapragada, D. S. P., Bhaskar, S., & Chandak, G. R. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00251 · Cited by 30
A Phenome-Wide Mendelian Randomization Study of Pancreatic Cancer Using Summary Genetic Data
Langdon, R., Richmond, R. C., Hemani, G., Zheng, J., Wade, K. H., Carreras‐Torres, R., Johansson, M., Brennan, P., Wootton, R. E., Munafo, M. R., et al. (2019) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-19-0036 · Cited by 30
MTAG: Multi-Trait Analysis of GWASPreprint
Turley, P., Walters, R. K., Maghzian, O., Okbay, A., Lee, J. J., Fontana, M. A., Nguyen-Viet, T. A., Wedow, R., Zacher, M., Furlotte, N. A., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/118810 · Cited by 30
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Hao, R.-H., Zhang, T.-P., Jiang, F., Liu, J.-H., Dong, S., Li, M., Guo, Y., & Yang, T. (2024) · Nature Communications · doi:10.1038/s41467-024-49263-4 · Cited by 30
“As the well accepted indicators of obesity, both BMI and other obesity-related traits were found related to brain 4,18,19 , while the strongest genetic factors appeared to be largely distinct 20,21 .”
BackgroundInvestigation of Genetic Variation Underlying Central Obesity amongst South Asians
Scott, W. R., Zhang, W., Loh, M. C. S., Tan, S.-T., Lehne, B. C., Afzal, U., Peralta, J. M., Saxena, R., Ralhan, S. K., Wander, G. S., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0155478 · Cited by 28
“We found 38 SNPs associated with WHR in men and women [19,22], and 11 SNPs associated in women alone [20,22].”
BackgroundSelf-citationGenetic Determinants of Weight Loss After Bariatric Surgery
Aasbrenn, M., Schnurr, T. M., Have, C. T., Svendstrup, M., Hansen, D. L., Worm, D., Balslev‐Harder, M., Hollensted, M., Grarup, N., Burgdorf, K. S., et al. (2019) · Obesity Surgery · doi:10.1007/s11695-019-03878-5 · Cited by 28
An evolutionary compass for detecting signals of polygenic selection and mutational bias
Uricchio, L. H., Kitano, H. C., Gusev, A., & Zaitlen, N. (2019) · Evolution Letters · doi:10.1002/evl3.97 · Cited by 29
Braunerová, R. T., Kunešová, M., Heinen, M. M., Rutter, H., Hassapidou, M. N., Duleva, V. L., Pudule, I., Petrauskienė, A., Sjöberg, A., Lissner, L., et al. (2021) · Obesity Reviews · doi:10.1111/obr.13208 · Cited by 30
“A recently conducted genome-wide association meta-analysis of traits related to waist and hip circumference confirmed that body fat distribution is a heritable trait associated with loci that are linked to cardiometabolic risks.(36) Loci linked to body fat distribution—in contrast to those linked to overall obesity—ex…”
BackgroundNutrition for precision health: The time is now
Qi, L. (2022) · Obesity · doi:10.1002/oby.23448 · Cited by 29
Self-citationChen, X., Tang, H., Lin, J., & Zeng, R. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.971997 · Cited by 31
“The genetic variants for waist circumference (N = 232,101), hip circumference (N = 213,038), and waist-to-hip ratio traits (N = 212,244) also originated from European population based on the GIANT consortium (18).”
BackgroundLivingstone, K. M., Celis-Morales, C. A., Navas‐Carretero, S., San-Cristóbal, R., Forster, H., O’Donovan, C. B., Woolhead, C., Marsaux, C. F. M., Macready, A. L., Fallaize, R., et al. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515004675 · Cited by 29
Biological clocks and physical functioning in monozygotic female twins
Sillanpää, E., Laakkonen, E. K., Vaara, E. M., Rantanen, T., Kovanen, V., Sipilä, S., Kaprio, J. A., & Ollikainen, M. (2018) · BMC Geriatrics · doi:10.1186/s12877-018-0775-6 · Cited by 29
“The genetic architecture of body composition is better known, in particular of height, overall BMI and regional adiposity [30, 31], and much of their heritability is accounted for identified genes [32].”
BackgroundSelf-citationLemmelä, S., Wigmore, E. M., Benner, C., Havulinna, A. S., Ong, R. M., Kempf, T., Wollert, K. C., Blankenberg, S., Zeller, T., Peters, J. E., et al. (2022) · eLife · doi:10.7554/elife.76272 · Cited by 28
“, 2018), WHR (n=485,486) (Shungin et al., 2015), 669 glucose (n=314,916) (Neale, 2018), type 2 diabetes (n cases=74,124, n controls=824,006) 670 (Mahajan et al.”
Epigenetic developmental mechanisms underlying sex differences in cancer
Rubin, J. B., Abou-Antoun, T., Ippolito, J. E., Llaci, L., Marquez, C., Wong, J. P., & Yang, L. (2024) · Journal of Clinical Investigation · doi:10.1172/jci180071 · Cited by 29
“Experiments examining the effect of sequential X chromosome addition, Y chromosome deletion, and gonadal sex on metabolic substrate utilization confirm that prenatal sex biases are driven by sex chromosome complement during mammalian development (75, 79–83).”
Kouvari, M., Yannakoulia, M., Souliotis, K. N., & Panagiotakos, D. B. (2018) · Angiology · doi:10.1177/0003319718756732 · Cited by 29
“the effect was stronger for females.(24,25) Another study revealed that 11b-hydroxysteroid dehydrogenase type 1 gene expression in adipocytes was higher in males.”
BackgroundAdiponectin and coronary artery disease risk: A bi-directional Mendelian randomization study
Yeung, S. L. A., & Schooling, C. M. (2018) · International Journal of Cardiology · doi:10.1016/j.ijcard.2018.03.132 · Cited by 29
Plasma Cortisol and Risk of Atrial Fibrillation: A Mendelian Randomization Study
Larsson, S. C., Lee, W., Burgess, S., & Allara, E. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgab219 · Cited by 30
“Summary-level GWAS data for systolic blood pressure and waist circumference were obtained respectively from the International Consortium of Blood Pressure (n = 757 601 participants) (14) and Genetic Investigation of ANthropometric Traits consortium (n = 232 101 participants) (15).”
Fernández‐Rhodes, L., Graff, M., Buchanan, V. L., Justice, A. E., Highland, H. M., Guo, X., Zhu, W., Chen, H., Young, K. L., Adhikari, K., et al. (2022) · Human Genetics and Genomics Advances · doi:10.1016/j.xhgg.2022.100099 · Cited by 34
Self-citationCausality of abdominal obesity on cognition: a trans-ethnic Mendelian randomization study
Wang, S., Su, M., Chen, C., Lin, K., Feng, Y. A., Hsiao, P., Pan, Y., & Wu, C. (2022) · International Journal of Obesity · doi:10.1038/s41366-022-01138-8 · Cited by 28
“GWAS for WHRadjBMI was conducted among 210,088 individuals of European descent [26].”
BackgroundAbramova, M. Y., Churnosova, M., Efremova, O., Aristova, I., Reshetnikov, E., Polonikov, A., Churnosov, M. I., & Ponomarenko, I. (2022) · Life · doi:10.3390/life12122018 · Cited by 30
Establishing causal relationships between sleep and adiposity traits using Mendelian randomization
Hayes, B., Vabistsevits, M., Martin, R. M., Lawlor, D. A., Richmond, R. C., & Robinson, T. (2023) · Obesity · doi:10.1002/oby.23668 · Cited by 26
“We identified genetic instruments for HC, WC, adult-BMI, and WHR from GIANT consortium summary data (N = 322,154) [25, 27], for which 52, 41, 68, and 29 independent (defined as R(2) < 0.”
MethodInfluentialBarbitoff, Y. A., Serebryakova, E. A., Nasykhova, Y. A., Predeus, A. V., Polev, D. E., Shuvalova, A. R., Vasiliev, E. V., Петрович, У. С., Sarana, А. М., Scherbak, S. G., et al. (2018) · Genes · doi:10.3390/genes9080415 · Cited by 29
“This variant is also significantly associated with height [33].”
BackgroundQiu, Y., Liu, Q., Luo, Y., Chen, J., Zheng, Q., Xie, Y., & Cao, Y. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1287463 · Cited by 31
Self-citationGenomic Variants Associated with Resistance to High Fat Diet Induced Obesity in a Primate Model
Harris, R. A., Alcott, C. E., Sullivan, E. L., Takahashi, D. L., McCurdy, C. E., Comstock, S. M., Baquero, K. C., Blundell, P., Frias, A. E., Kahr, M. K., et al. (2016) · Scientific Reports · doi:10.1038/srep36123 · Cited by 27
Epigenetic Regulation of PLIN 1 in Obese Women and its Relation to Lipolysis
Bialešová, L., Kulyté, A., Petrus, P., Sinha, I., Laurencikiene, J., Zhao, C., Wright, K. D., Arner, P., & Dahlman, I. A. (2017) · Scientific Reports · doi:10.1038/s41598-017-09232-y · Cited by 30
The impact of abdominal fat on abdominal aorta calcification measured on non-enhanced CT
Goldenberg, L., Saliba, W., Hayeq, H., Hasadia, R., & Zeina, A. (2018) · Medicine · doi:10.1097/md.0000000000013233 · Cited by 27
Multi-Omics Analysis Reveals MicroRNAs Associated With Cardiometabolic Traits
Mens, M. M. J., Maas, S. C. E., Klap, J. M., Weverling, G. J., Klatser, P. R., Brakenhoff, J. P. J., van Meurs, J. B. J., Uitterlinden, A. G., Ikram, M. A., Kavousi, M., et al. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00110 · Cited by 32
Self-citationtRNA Biology in the Pathogenesis of Diabetes: Role of Genetic and Environmental Factors
Arroyo, M. N., Green, J. A., Cnop, M., & Igoillo‐Esteve, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020496 · Cited by 27
Ostinelli, G., Vijay, J., Vohl, M., Grundberg, E., & Tchernof, A. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111220 · Cited by 28
“Obesity is associated with numerous cardiometabolic complications including the metabolic syndrome (Shungin et al., 2015), type 2 diabetes (T2D) and cardiovascular diseases (CVD).”
BackgroundInfluentialSelf-citationDong, S., Zhu, D., Zhou, X., Rong, Y., Zeng, M., Chen, J., Jiang, F., Tuo, X.-M., Feng, Z., Yang, T., et al. (2021) · Diabetes · doi:10.2337/db20-1151 · Cited by 25
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Nielsen, M. B., Çolak, Y., Benn, M., & Nordestgaard, B. G. (2021) · Diabetes · doi:10.2337/db21-0131 · Cited by 27
Lin, Y., Zhu, X., Luo, W., Jiang, B., Lin, Q., Tang, M., Li, X., & Xie, L. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.835524 · Cited by 29
Mendelian randomization highlights the causal association of obesity with periodontal diseases
Dong, J., Gong, Y., Chu, T., Wu, L., Li, S., Deng, H., Hu, R., & Wang, Y. (2022) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.13640 · Cited by 27
Ruskovska, T., Budić-Leto, I., Corral‐Jara, K. F., Ajdžanović, V. Z., Arola‐Arnal, A., Bravo, F. I., Deligiannidou, G.-E., Havlík, J., Janeva, M., Kistanova, E. K., et al. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101649 · Cited by 27
General and Abdominal Obesity Operate Differently as Risk Factors of Fracture Risk in Old Adults
Zhu, X.-W., Liu, K.-Q., Yuan, C., Xia, J., Qian, Y., Xu, L., Gao, J.-H., Rong, X., Chen, G., Karasik, D., et al. (2022) · iScience · doi:10.1016/j.isci.2022.104466 · Cited by 25
Rühlemann, M. C., Degenhardt, F. C., Thingholm, L. B., Wang, J., Skiecevičienė, J., Rausch, P., Hov, J. R., Lieb, W., Karlsen, T. H., Laudes, M., et al. (2017) · Gut Microbes · doi:10.1080/19490976.2017.1356979 · Cited by 27
“928) has previously been reported to be associated with Crohn’s disease(18,19) and obesity-related traits.(20) The second signal is located on chromosome 20 (rs113738363; chr20:48449631; Pmeta D 1.”
Background
Metadata
- 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)
- University of Maryland, Baltimore (US)
- Maastricht University (NL)
- University of Milan (IT)
- Nanyang Technological University (SG)
- Université de Lille (FR)
- University of London (GB)
- Loyola University Chicago (US)
- Institut für Medizinische Informatik, Biometrie und Epidemiologie (DE)
- Wake Forest University Health Sciences (US)
- 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
- Shungin, Dmitry
- Winkler, Thomas W.
- Ferreira, Teresa
- Locke, Adam E.
- Mägi, Reedik
- Strawbridge, Rona J.
- Pers, Tune H.
- Fischer, Krista
- Justice, Anne E.
- Workalemahu, Tsegaselassie
- Wu, Joseph M. W.
- Buchkovich, Martin L.
- Roman, Tamara S.
- Song, Ci
- Gustafsson, Stefan
- Day, Felix R.
- Fall, Tove
- Kutalik, Zoltán
- Luan, Jian’an
- Scherag, André
- Vedantam, Sailaja
- Wood, Andrew R.
- Fehrmann, Rudolf
- Karjalainen, Juha
- Kahali, Bratati
- Schmidt, Ellen M.
- Amin, Najaf
- Anderson, Denise
- Beekman, Marian
- Buyske, Steven
- Ehret, Georg B.
- Feitosa, Mary F.
- Goel, Anuj
- Jackson, Anne U.
- Johnson, Toby
- Kleber, Marcus E.
- Kristiansson, Kati
- Mangino, Massimo
- Palmer, Cameron D.
- Pechlivanis, Sonali
- Peters, Marjolein J.
- Prokopenko, Inga
- Tanaka, Toshiko
- Teumer, Alexander
- Yengo, Loïc
- Zhang, Weihua
- Ärnlöv, Johan
- Arscott, Gillian M.
- Bandinelli, Stefania
- Bellis, Claire
- Bennett, Amanda J.
- Blüher, Matthias
- Böhringer, Stefan
- Bonnet, Fabrice
- Böttcher, Yvonne
- Carba, Delia B.
- Caspersen, Ida H.
- Deelen, Joris
- Deelman, Ewa
- Doney, Alex S. F.
- Erdos, Michael R.
- Estrada, Karol
- Giedraitis, Vilmantas
- Gigante, Bruna
- Go, Alan S.
- Golay, Alain
- Grallert, Harald
- Grewal, Jagvir
- Groves, Christopher J.
- Haller, Toomas
- Hartman, Catharina A.
- Hayward, Caroline
- Herzig, Karl-Heinz
- Hillege, Hans L.
- Hunt, Steven C.
- Isaacs, Aaron
- Ittermann, Till
- Johansson, Ingegerd
- Kalafati, Ioanna-Panagiota
- Kinnunen, Leena
- Kratzer, Wolfgang
- Lamina, Claudia
- Leander, Karin
- Lichtner, Peter
- Lind, Lars
- Lindström, Jaana
- Lorentzon, Mattias
- Mach, François
- Magnusson, Patrik K. E.
- Mahajan, Anubha
- Menni, Cristina
- Merger, Sigrun
- Milani, Lili
- Mills, Rebecca
- Moayyeri, Alireza
- Mooijaart, Simon P.
- Mulas, Antonella
- Müller, Gabriele
- Nagaraja, Ramaiah
- Narisu, Narisu
- Nolte, Ilja M.
- Olden, Matthias
- Rayner, Nigel W.
- Rose, Lynda M.
- Sanna, Serena
- Scharnagl, Hubert
- Scholtens, Salome
- Sennblad, Bengt
- Seufferlein, Thomas
- Sitlani, Colleen M.
- Stirrups, Kathleen
- Stringham, Heather M.
- Sundström, Johan
- Swertz, Morris A.
- Tayo, Bamidele O.
- Thorand, Barbara
- Tomaschitz, Andreas
- Verweij, Niek
- Vonk, Judith M.
- Wilsgaard, Tom
- Wojczynski, Mary K.
- Wong, Andrew
- Brennan, Eoin P.
- Choi, Murim
- Eriksson, Per
- Folkersen, Lasse
- Gharavi, Ali G.
- Hedman, Åsa K.
- Hivert, Marie-France
- Huang, Jinyan
- Kanoni, Stavroula
- Karpe, Fredrik
- Kiryluk, Krzysztof
- Liang, Liming
- Lifton, Richard P.
- Ma, Baoshan
- McKnight, Amy J.
- McPherson, Ruth
- Metspalu, Andres
- Min, Josine L.
- Moffatt, Miriam F.
- Montgomery, Grant W.
- Murabito, Joanne M.
- Nyholt, Dale R.
- Olsson, Christian
- Perry, John R. B.
- Salem, Rany M.
- Sandholm, Niina
- Vallejo, Edgar E.
- Westra, Harm-Jan
- Zondervan, Krina T.
- Amouyel, Philippe
- Bakker, Stephan J. L.
- Beilby, John
- Bergman, Richard N.
- Blangero, John
- Brown, Morris J.
- Burnier, Michel
- Chakravarti, Aravinda
- Collins, Francis S.
- Crawford, Dana C.
- Danesh, John
- Dörr, Marcus
- Eriksson, Johan G.
- Farrall, Martin
- Ferrannini, Ele
- Ferrières, Jean
- Forouhi, Nita G.
- Franco, Oscar H.
- Gansevoort, Ron T.
- Gieger, Christian
- Gudnason, Vilmundur
- Haiman, Christopher A.
- Harris, Tamara B.
- Hattersley, Andrew T.
- Hicks, Andrew A.
- Hingorani, Aroon D.
- Hoffmann, Wolfgang
- Homuth, Georg
- Humphries, Steve E.
- Hyppönen, Elina
- Johansen, Berit
- Kaprio, Jaakko
- Kee, Frank
- Keinanen-Kiukaanniemi, Sirkka M.
- Kooner, Jaspal S.
- Kooperberg, Charles
- Kovacs, Peter
- Kuulasmaa, Kari
- Lakka, Timo A.
- Langenberg, Claudia
- Lehtimäki, Terho
- Lyssenko, Valeriya
- Männistö, Satu
- Marette, André
- Matise, Tara C.
- Musk, Arthur W.
- Morris, Andrew D.
- Nelis, Mari
- Ohlsson, Claes
- Oldehinkel, Albertine J.
- Ong, Ken K.
- Palmer, Lyle J.
- Penninx, Brenda W.
- Peters, Annette
- Pramstaller, Peter P.
- Raitakari, Olli T.
- Rao, D. C.
- Rice, Treva K.
- Ridker, Paul M.
- Ritchie, Marylyn D.
- Rudan, Igor
- Salomaa, Veikko
- Samani, Nilesh J.
- Sarzynski, Mark A.
- Schwarz, Peter E. H.
- Shuldiner, Alan R.
- Staessen, Jan A.
- Stolk, Ronald P.
- Strauch, Konstantin
- Tönjes, Anke
- Tremblay, Angelo
- Tremoli, Elena
- Vohl, Marie-Claude
- Völker, Uwe
- Wilson, James F.
- Adair, Linda S.
- Bochud, Murielle
- Boehm, Bernhard O.
- Bornstein, Stefan R.
- Bouchard, Claude
- Cauchi, Stéphane
- Caulfield, Mark J.
- Chambers, John C.
- Chasman, Daniel I.
- Cooper, Richard S.
- Dedoussis, George
- Ferrucci, Luigi
- Froguel, Philippe
- Grabe, Hans-Jörgen
- Hamsten, Anders
- Hui, Jennie
- Hveem, Kristian
- Jöckel, Karl-Heinz
- Kuh, Diana
- Laakso, Markku
- März, Winfried
- Munroe, Patricia B.
- Njølstad, Inger
- Pedersen, Nancy L.
- Perola, Markus
- Peters, Ulrike
- Power, Chris
- Quertermous, Thomas
- Rivadeneira, Fernando
- Saleheen, Danish
- Sinisalo, Juha
- Snieder, Harold
- Spector, Tim D.
- Tuomilehto, Jaakko
- Uitterlinden, André G.
- Uusitupa, Matti
- Veronesi, Giovanni
- Walker, Mark
- Wareham, Nicholas J.
- Watkins, Hugh
- Wichmann, H-Erich
- Assimes, Themistocles L.
- Berndt, Sonja I.
- Boehnke, Michael
- Borecki, Ingrid B.
- Deloukas, Panos
- Franke, Lude
- Frayling, Timothy M.
- Kaplan, Robert C.
- O’Connell, Jeffrey R.
- Qi, Lu
- Strachan, David P.
- Willer, Cristen J.
- Visscher, Peter M.
- Yang, Jian
- Hirschhorn, Joel N.
- McCarthy, Mark I.
- Speliotes, Elizabeth K.
- North, Kari E.
- Fox, Caroline S.
- Barroso, Inês
- Franks, Paul W.
- Ingelsson, Erik
- Heid, Iris M.
- Loos, Ruth J. F.
- Cupples, L. Adrienne
- Morris, Andrew P.
- Lindgren, Cecilia M.
- Mohlke, Karen L
- Venue
- Nature
- Published
- 2015-02-11
- Volume
- 518
- Issue
- 7538
- Pages
- 187-196
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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
- FWCI
- 21.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Research Explorer (The University of Manchester) (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
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- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
- VU Research Portal (publishedVersion, other-oa)
- PubMed Central (acceptedVersion)
- IRIS (submittedVersion)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- Civil War Book Review (submittedVersion)
- ScholarWorks @ UTRGV (The University of Texas Rio Grande Valley) (submittedVersion)
- UNSWorks (UNSW Sydney) (submittedVersion, cc-by-nc-nd)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- HAL (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Digital Access to Libraries (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- DR-NTU (Nanyang Technological University) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- IrInSubria (University of Insubria) (submittedVersion)
- UnissResearch (Università degli Studi di Sassari) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
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- Lund University Publications (Lund University) (submittedVersion)
- Open Research Exeter (University of Exeter) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
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- Queen Mary Research Online (Queen Mary University of London) (submittedVersion)
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- SERVAL (Université de Lausanne) (submittedVersion, other-oa)
- Spiral (Imperial College London) (submittedVersion)
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- Open Research (University of Surrey) (submittedVersion)
- UNSWorks (University of New South Wales, Sydney, Australia) (submittedVersion, cc-by-nc-nd)
- UniSA Research Outputs Repository (University of South Australia) (submittedVersion)
- STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
- BCU Open Access Repository (Birmingham City University) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Newcastle University ePrints (Newcastle Univesity)
- 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 › Endocrinology, Diabetes and Metabolism › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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