Cited by 1,017Genetic Associations and EpidemiologyMetabolomics and Mass Spectrometry StudiesNutrition, Genetics, and Disease

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Human metabolic individuality in biomedical and pharmaceutical research

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CARDIoGRAM, Suhre, Karsten, Shin, So-Youn, Petersen, Ann-Kristin, Mohney, Robert P., Meredith, David, Wägele, Brigitte, Altmaier, Elisabeth, Deloukas, Panos, Erdmann, Jeanette, Grundberg, Elin, Hammond, Christopher J., de Angelis, Martin Hrabé, Kastenmüller, Gabi, Köttgen, Anna, Kronenberg, Florian, Mangino, Massimo, Meisinger, Christa, Meitinger, Thomas, Mewes, Hans-Werner, Milburn, Michael V., Prehn, Cornelia, Raffler, Johannes, Ried, Janina S., Römisch-Margl, Werner, Samani, Nilesh J., Small, Kerrin S., -Erich Wichmann, H., Zhai, Guangju, Illig, Thomas, Spector, Tim D., Adamski, Jerzy, Soranzo, Nicole, Gieger, Christian·2011·Nature

DOI 10.1038/nature10354PMC PMC3832838

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Abstract

Genome-wide association studies (GWAS) have identified many risk loci for complex diseases, but effect sizes are typically small and information on the underlying biological processes is often lacking. Associations with metabolic traits as functional intermediates can overcome these problems and potentially inform individualized therapy. Here we report a comprehensive analysis of genotype-dependent metabolic phenotypes using a GWAS with non-targeted metabolomics. We identified 37 genetic loci associated with blood metabolite concentrations, of which 25 show effect sizes that are unusually high for GWAS and account for 10-60% differences in metabolite levels per allele copy. Our associations provide new functional insights for many disease-related associations that have been reported in previous studies, including those for cardiovascular and kidney disorders, type 2 diabetes, cancer, gout, venous thromboembolism and Crohn's disease. The study advances our knowledge of the genetic basis of metabolic individuality in humans and generates many new hypotheses for biomedical and pharmaceutical research.

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Additional file 8 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
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Additional file 10 of The metabolome as a link in the genotype-phenotype map for peroxide resistance in the fruit fly, Drosophila melanogaster
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Additional file 17 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
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Additional file 3 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640706
Additional file 1 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24571894
Additional file 12 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P. E., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640733
Additional file 1 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
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Additional file 2 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.24572257
Additional file 8 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.26671524
Additional file 4 of The metabolome as a link in the genotype-phenotype map for peroxide resistance in the fruit fly, Drosophila melanogaster
Harrison, B. R., Wang, L., Gajda, E., Hoffman, E. V., Chung, B. Y., Pletcher, S. D., Raftery, D., & Promislow, D. E. L. (2020) · Figshare · doi:10.6084/m9.figshare.12246677
Additional file 14 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640739
Additional file 2 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.25052495
Additional file 6 of The metabolome as a link in the genotype-phenotype map for peroxide resistance in the fruit fly, Drosophila melanogaster
Harrison, B. R., Wang, L., Gajda, E., Hoffman, E. V., Chung, B. Y., Pletcher, S. D., Raftery, D., & Promislow, D. E. L. (2020) · Figshare · doi:10.6084/m9.figshare.12246692
Additional file 5 of The metabolome as a link in the genotype-phenotype map for peroxide resistance in the fruit fly, Drosophila melanogaster
Harrison, B. R., Wang, L., Gajda, E., Hoffman, E. V., Chung, B. Y., Pletcher, S. D., Raftery, D., & Promislow, D. E. L. (2020) · Figshare · doi:10.6084/m9.figshare.12246683
Additional file 5 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.26671515
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Additional file 4 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640709
Additional file 9 of The metabolome as a link in the genotype-phenotype map for peroxide resistance in the fruit fly, Drosophila melanogaster
Harrison, B. R., Wang, L., Gajda, E., Hoffman, E. V., Chung, B. Y., Pletcher, S. D., Raftery, D., & Promislow, D. E. L. (2020) · Figshare · doi:10.6084/m9.figshare.12246713
Additional file 6 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.26671518
Additional file 9 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640724
Additional file 3 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.26671509
Additional file 9 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.26671527
Additional file 7 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640718
Additional file 3 of Causal relationships between genetically determined metabolites and human intelligence: a Mendelian randomization study
Yang, J., Zhao, B., Qian, L., Gao, F., Fan, Y., He, X., Ma, Q., Yang, L., Yan, B., Wang, W., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13843850
Additional file 2 of Causal relationships between genetically determined metabolites and human intelligence: a Mendelian randomization study
Yang, J., Zhao, B., Qian, L., Gao, F., Fan, Y., He, X., Ma, Q., Yang, L., Yan, B., Wang, W., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13843847
Additional file 6 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640715
Additional file 11 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640730
Additional file 1 of Causal relationships of metabolites with allergic diseases: a trans-ethnic Mendelian randomization study
Tu, J., Wen, J., Luo, Q., Li, X., Wang, D., & Ye, J. (2024) · Figshare · doi:10.6084/m9.figshare.26683378
Additional file 7 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.26671521
Additional file 5 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640712
Additional file 1 of Bidirectional modulation of TCA cycle metabolites and anaplerosis by metformin and its combination with SGLT2i
Harada, M., Adam, J., Covic, M., Ge, J., Brandmaier, S., Muschet, C., Huang, J., Han, S., Rommel, M., Rotter, M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26027587
Self-citation
Additional file 15 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640742
Additional file 2 of Integrated analysis of gut metabolome, microbiome, and exfoliome data in an equine model of intestinal injury
Whitfield-Cargile, C. M., Chung, H. C., Coleman, M. C., Cohen, N. D., Chamoun-Emanuelli, A. M., Ivanov, I. V., Goldsby, J. S., Davidson, L. A., Gaynanova, I., Ni, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26706495
Additional file 4 of Exploring the causal role of multiple metabolites on ovarian cancer: a two sample Mendelian randomization study
Liu, S., Ding, D., Liu, F., Guo, Y., Xie, L., & Han, F. (2024) · Figshare · doi:10.6084/m9.figshare.26671512
Additional file 8 of The metabolome as a link in the genotype-phenotype map for peroxide resistance in the fruit fly, Drosophila melanogaster
Harrison, B. R., Wang, L., Gajda, E., Hoffman, E. V., Chung, B. Y., Pletcher, S. D., Raftery, D., & Promislow, D. E. L. (2020) · Figshare · doi:10.6084/m9.figshare.12246707
Additional file 13 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640736
Additional file 10 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640727
Additional file 16 of Circulating metabolites may illustrate relationship of alcohol consumption with cardiovascular disease
Li, Y., Wang, M., Liu, X., Rong, J., Miller, P., Joehanes, R., Huan, T., Guo, X., Rotter, J. I., Smith, J. A., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26640745
Additional file 2 of Causal relationships of metabolites with allergic diseases: a trans-ethnic Mendelian randomization study
Tu, J., Wen, J., Luo, Q., Li, X., Wang, D., & Ye, J. (2024) · Figshare · doi:10.6084/m9.figshare.26683381
Long-Term Mortality After Tuberculosis Among People With Disabilities in Korea
Min, J., Kim, S. Y., Park, J. E., Kim, Y.-Y., Yang, H. S., Park, B. H., Jeon, S. W., Kim, Y. J., Yang, B., Yeob, K. E., et al. (2025) · Journal of Korean Medical Science · doi:10.3346/jkms.2026.41.e33
Use of Mendelian Randomization to Unveil Metabolic Markers in Helicobacter pylori Infection
Hoang, T., & Kim, J. (2025) · Journal of Korean Medical Science · doi:10.3346/jkms.2026.41.e13

Authors: CARDIoGRAM, Suhre, K., Shin, S.-Y., Petersen, A.-K., Mohney, R. P., Meredith, D., Wägele, B., Altmaier, E., Deloukas, P., Erdmann, J., Grundberg, E., Hammond, C. J., de Angelis, M. H., Kastenmüller, G., Köttgen, A., Kronenberg, F., Mangino, M., Meisinger, C., Meitinger, T., Mewes, H.-W., Milburn, M. V., Prehn, C., Raffler, J., Ried, J. S., Römisch-Margl, W., Samani, N. J., Small, K. S., -Erich Wichmann, H., Zhai, G., Illig, T., Spector, T. D., Adamski, J., Soranzo, N., & Gieger, C.
Affiliations: Helmholtz Munich (DE)
Wellcome Sanger Institute (GB)
Oxford Brookes University (GB)
St Thomas' Hospital (GB)
King's College London (GB)
University Medical Center Freiburg (DE)
Innsbruck Medical University (AT)
TUM Klinikum (DE)
Corresponding author: Suhre, Karsten
Soranzo, Nicole
ORCID: Suhre, Karsten
Shin, So-Youn
Mohney, Robert P.
Meredith, David
Deloukas, Panos
Erdmann, Jeanette
Grundberg, Elin
Hammond, Christopher J.
Kastenmüller, Gabi
Köttgen, Anna
Kronenberg, Florian
Mangino, Massimo
Meisinger, Christa
Meitinger, Thomas
Mewes, Hans-Werner
Prehn, Cornelia
Raffler, Johannes
Samani, Nilesh J.
Small, Kerrin S.
Zhai, Guangju
Spector, Tim D.
Adamski, Jerzy
Soranzo, Nicole
Gieger, Christian
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2011-08-31
Volume: 477
Issue: 7362
Pages: 54-60
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature10354
PMC: PMC3832838
OpenAlex: W2166711199
Cited by: 1,017
References: 52
Citations by year: 2026: 31 · 2025: 34 · 2024: 53 · 2023: 55 · 2022: 69 · 2021: 63 · 2020: 73 · 2019: 48 · 2018: 69 · 2017: 68 · 2016: 84 · 2015: 82 · 2014: 89 · 2013: 88 · 2012: 95
FWCI: 57.27
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
IRIS (submittedVersion)
Research Portal (King's College London) (submittedVersion)
Leicester Research Archive (University of Leicester) (submittedVersion)
mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
mediaTUM (Technical University of Munich) (submittedVersion, other-oa)
Site cant be reached (submittedVersion)
Explore Bristol Research (submittedVersion)
SERVAL (Université de Lausanne) (submittedVersion)
OPUS (Augsburg University) (submittedVersion)
Funders: Wellcome Trust (091746/Z/10/Z, 091746)
Cancer Research UK
British Heart Foundation
National Institutes of Health (n01ag12100-57-0-2, n01hc55021-47-0-1, n01hc55020-39-0-0, n01hc55016-37-0-0, n01hc055022-024, n01hc55019-35-0-1, n01hc55018-38-0-1, n01hc55015-48-0-1)
Canadian Institutes of Health Research (MOP--82810, #MOP77682, MOP172605)
Biotechnology and Biological Sciences Research Council
National Institute on Aging (N01-AG12100)
National Heart, Lung, and Blood Institute (N01-HC55022, N01-HC-55018, N01 HC 55020, N01 HC 55019, R01HL087676, R01HL103931, R01HL087647, HL087647, N01-HC55016, P01HL076491, P01HL098055, P01HL087018, N01‐HC‐55015, N01-HC55021, R01HL089650)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK080732)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Nutrition, Genetics, and Disease
Keywords: blood metabolites, genetic loci, untargeted metabolomics, endophenotypes, type 2 diabetes, cardiovascular disease, kidney disease, cancer, gout, venous thromboembolism, Crohn's disease, gene-environment interaction, TwinsUK
MeSH terms: Adolescent, Adult, Aged, Aged, 80 and over, Blood, Child, Chronic Disease, Coronary Artery Disease, Diabetes Mellitus, Drug Industry, Female, Genotype, Humans, Male, Metabolism, Middle Aged, Pharmacogenetics, Risk Factors, Genetic Variation, Biomedical Research, Renal Insufficiency, Venous Thromboembolism, Genome-Wide Association Study, Metabolomics, Young Adult, Genetic Loci

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