New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk
Open accessAbstract
Levels of circulating glucose are tightly regulated. To identify new loci influencing glycemic traits, we performed meta-analyses of 21 genome-wide association studies informative for fasting glucose, fasting insulin and indices of beta-cell function (HOMA-B) and insulin resistance (HOMA-IR) in up to 46,186 nondiabetic participants. Follow-up of 25 loci in up to 76,558 additional subjects identified 16 loci associated with fasting glucose and HOMA-B and two loci associated with fasting insulin and HOMA-IR. These include nine loci newly associated with fasting glucose (in or near ADCY5, MADD, ADRA2A, CRY2, FADS1, GLIS3, SLC2A2, PROX1 and C2CD4B) and one influencing fasting insulin and HOMA-IR (near IGF1). We also demonstrated association of ADCY5, PROX1, GCK, GCKR and DGKB-TMEM195 with type 2 diabetes. Within these loci, likely biological candidate genes influence signal transduction, cell proliferation, development, glucose-sensing and circadian regulation. Our results demonstrate that genetic studies of glycemic traits can identify type 2 diabetes risk loci, as well as loci containing gene variants that are associated with a modest elevation in glucose levels but are not associated with overt diabetes.
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Mutations in multiple clock genes in humans contribute to genetic susceptibility to obesity, insulin resistance, and type 2 diabetes.
“mutations in multiple clock genes in humans have been shown to contribute to genetic susceptibility to obesity, IR, and type 2 diabetes [10,26,27,28].”
From Chronotype: A Tool to Screen Eating Habits in Polycystic Ovary Syndrome? (2022) · cites this paper as [28]
The Discussion box (page not provided) identifies CRY2 and MTNR1B as circadian genes associated with fasting glucose in humans. The Results also report a less significant association between a variant in or near CRY2 and type 2 diabetes risk. The paper does not establish that mutations in multiple human clock genes confer susceptibility to obesity or insulin resistance; the body-weight and insulin-sensitivity findings cited in the box concern mice with CRY2 null mutations. (LLM, conf=0.88)
Experimental — accuracy not yet measuredHumans develop impaired glucose tolerance when subjected to circadian misalignment conditions.
“it has already been reported that humans develop impaired glucose tolerance when subjected to circadian misalignment conditions [10,26,27,28].”
From Chronotype: A Tool to Screen Eating Habits in Polycystic Ovary Syndrome? (2022) · cites this paper as [28]
The Discussion box reports impaired glucose tolerance alongside abnormal circadian rhythmicity in mice with CRY2 null mutations, and an association between circadian genes and fasting glucose in humans. It does not report that humans subjected to circadian misalignment develop impaired glucose tolerance; both the population and the condition differ. (LLM, conf=0.86)
Experimental — accuracy not yet measuredGWAS have identified genetic loci associated with many physical diseases, such as obesity, type 2 diabetes mellitus, and heart disease.
“as well as with many physical diseases, such as obesity186, type 2 diabetes mellitus187, and heart disease188.”
From Comorbidity between major depressive disorder and physical diseases: a comprehensive review of epidemiology, mechanisms and management (2023) · cites this paper as [187]
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Nettleton, J. A., Hivert, M.-F., Lemaitre, R. N., McKeown, N. M., Mozaffarian, D., Tanaka, T., Wojczynski, M. K., Hruby, A., Djoussé, L., Ngwa, J. S., et al. (2013) · American Journal of Epidemiology · doi:10.1093/aje/kws297 · Cited by 89 · see citing works
Self-citationMinutes, days and years: molecular interactions among different scales of biological timing
Golombek, D. A., Bussi, I. L., & Agostino, P. V. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0465 · Cited by 80 · see citing works
Xie, W., Wood, A. R., Lyssenko, V., Weedon, M. N., Knowles, J. W., Alkayyali, S., Assimes, T. L., Quertermous, T., Abbasi, F., Paananen, J., et al. (2013) · Diabetes · doi:10.2337/db12-0876 · Cited by 83 · see citing works
Self-citationChronobiology and obesity: Interactions between circadian rhythms and energy regulation
Summa, K. C., & Turek, F. W. (2014) · Advances in Nutrition · doi:10.3945/an.113.005132 · Cited by 82 · see citing works
Rees, S. D., Hydrie, M. Z. I., O'Hare, J. P., Kumar, S., Shera, A. S., Basit, A., Barnett, A. H., & Kelly, M. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024710 · Cited by 78 · see citing works
Vasan, S. K., Noordam, R., Gowri, M. S., Neville, M. J., Karpe, F., & Christodoulides, C. (2019) · Diabetologia · doi:10.1007/s00125-019-4947-5 · Cited by 76 · see citing works
Self-citationNervous glucose sensing regulates postnatal β cell proliferation and glucose homeostasis
Tarussio, D., Metref, S., Seyer, P., Mounien, L., Vallois, D., Magnan, C., Foretz, M., & Thorens, B. (2014) · Journal of Clinical Investigation · doi:10.1172/jci69154 · Cited by 71 · see citing works
Jordan, D. M., Verbanck, M., & Do, R. (2019) · Genome Biology · doi:10.1186/s13059-019-1844-7 · Cited by 73 · see citing works
- Authors
- DIAGRAM Consortium, Dupuis, J., GIANT Consortium, Global BPgen Consortium, Anders Hamsten on behalf of Procardis Consortium, the MAGIC investigators, Langenberg, C., Prokopenko, I., Saxena, R., Soranzo, N., Jackson, A. U., Wheeler, E., Glazer, N. L., Bouatia-Naji, N., Gloyn, A. L., Lindgren, C. M., Mägi, R., Morris, A. P., Randall, J., Johnson, T., Elliott, P., Rybin, D., Thorleifsson, G., Steinthorsdottir, V., Henneman, P., Grallert, H., Dehghan, A., Hottenga, J. J., Franklin, C. S., Navarro, P., Song, K., Goel, A., Perry, J. R. B., Egan, J. M., Lajunen, T., Grarup, N., Sparsø, T., Doney, A., Voight, B. F., Stringham, H. M., Li, M., Kanoni, S., Shrader, P., Cavalcanti-Proença, C., Kumari, M., Qi, L., Timpson, N. J., Gieger, C., Zabena, C., Rocheleau, G., Ingelsson, E., An, P., O'Connell, J., Luan, J., Elliott, A., McCarroll, S. A., Payne, F., Roccasecca, R. M., Pattou, F., Sethupathy, P., Ardlie, K., Ariyurek, Y., Balkau, B., Barter, P., Beilby, J. P., Ben-Shlomo, Y., Benediktsson, R., Bennett, A. J., Bergmann, S., Bochud, M., Boerwinkle, E., Bonnefond, A., Bonnycastle, L. L., Borch-Johnsen, K., Böttcher, Y., Brunner, E., Bumpstead, S. J., Charpentier, G., Chen, Y.-D. I., Chines, P., Clarke, R., Coin, L. J. M., Cooper, M. N., Cornelis, M., Crawford, G., Crisponi, L., Day, I. N. M., de Geus, E. J. C., Delplanque, J., Dina, C., Erdos, M. R., Fedson, A. C., Fischer-Rosinsky, A., Forouhi, N. G., Fox, C. S., Frants, R., Franzosi, M. G., Galan, P., Goodarzi, M. O., Graessler, J., Groves, C. J., Grundy, S., Gwilliam, R., Gyllensten, U., Hadjadj, S., Hallmans, G., Hammond, N., Han, X., Hartikainen, A.-L., Hassanali, N., Hayward, C., Heath, S. C., Hercberg, S., Herder, C., Hicks, A. A., Hillman, D. R., Hingorani, A. D., Hofman, A., Hui, J., Hung, J., Isomaa, B., Johnson, P. R. V., Jørgensen, T., Jula, A., Kaakinen, M., Kaprio, J., Kesaniemi, Y. A., Kivimaki, M., Knight, B., Koskinen, S., Kovacs, P., Kyvik, K. O., Lathrop, G. M., Lawlor, D. A., Le Bacquer, O., Lecoeur, C., Li, Y., Lyssenko, V., Mahley, R., Mangino, M., Manning, A. K., Martínez-Larrad, M. T., McAteer, J. B., McCulloch, L. J., McPherson, R., Meisinger, C., Melzer, D., Meyre, D., Mitchell, B. D., Morken, M. A., Mukherjee, S., Naitza, S., Narisu, N., Neville, M. J., Oostra, B. A., Orrù, M., Pakyz, R., Palmer, C. N. A., Paolisso, G., Pattaro, C., Pearson, D., Peden, J. F., Pedersen, N. L., Perola, M., Pfeiffer, A. F. H., Pichler, I., Polasek, O., Posthuma, D., Potter, S. C., Pouta, A., Province, M. A., Psaty, B. M., Rathmann, W., Rayner, N. W., Rice, K., Ripatti, S., Rivadeneira, F., Roden, M., Rolandsson, O., Sandbaek, A., Sandhu, M., Sanna, S., Sayer, A. A., Scheet, P., Scott, L. J., Seedorf, U., Sharp, S. J., Shields, B., Sigurðsson, G., Sijbrands, E. J. G., Silveira, A., Simpson, L., Singleton, A., Smith, N. L., Sovio, U., Swift, A., Syddall, H., Syvänen, A.-C., Tanaka, T., Thorand, B., Tichet, J., Tönjes, A., Tuomi, T., Uitterlinden, A. G., van Dijk, K. W., van Hoek, M., Varma, D., Visvikis-Siest, S., Vitart, V., Vogelzangs, N., Waeber, G., Wagner, P. J., Walley, A., Walters, G. B., Ward, K. L., Watkins, H., Weedon, M. N., Wild, S. H., Willemsen, G., Witteman, J. C. M., Yarnell, J. W. G., Zeggini, E., Zelenika, D., Zethelius, B., Zhai, G., Zhao, J. H., Zillikens, M. C., Borecki, I. B., Loos, R. J. F., Meneton, P., Magnusson, P. K. E., Nathan, D. M., Williams, G. H., Hattersley, A. T., Silander, K., Salomaa, V., Smith, G. D., Bornstein, S. R., Schwarz, P., Spranger, J., Karpe, F., Shuldiner, A. R., Cooper, C., Dedoussis, G. V., Serrano-Ríos, M., Morris, A. D., Lind, L., Palmer, L. J., Hu, F. B., Franks, P. W., Ebrahim, S., Marmot, M., Kao, W. H. L., Pankow, J. S., Sampson, M. J., Kuusisto, J., Laakso, M., Hansen, T., Pedersen, O., Pramstaller, P. P., Wichmann, H. E., Illig, T., Rudan, I., Wright, A. F., Stumvoll, M., Campbell, H., & Wilson, J. F.
- Affiliations
- Boston University (US)
- Addenbrooke's Hospital (GB)
- University of Oxford (GB)
- Broad Institute (US)
- St Thomas' Hospital (GB)
- University of Michigan (US)
- University of Washington (US)
- Centre National de la Recherche Scientifique (FR)
- Centre for Human Genetics (GB)
- SIB Swiss Institute of Bioinformatics (CH)
- Leiden University Medical Center (NL)
- Erasmus MC (NL)
- Vrije Universiteit Amsterdam (NL)
- Institute of Genetics and Cancer (GB)
- GlaxoSmithKline (United States) (US)
- University of Exeter (GB)
- National Institute on Aging (US)
- University of Oulu (FI)
- Ninewells Hospital (GB)
- Johns Hopkins University (US)
- Harokopio University of Athens (GR)
- Harvard University (US)
- Helmholtz Munich (DE)
- Hospital Clínico San Carlos (ES)
- Karolinska Institutet (SE)
- Uppsala University (SE)
- University of Maryland, Baltimore (US)
- Massachusetts General Hospital (US)
- Wellcome Sanger Institute (GB)
- Inserm (FR)
- The Heart Research Institute (AU)
- The University of Western Australia (AU)
- Centre Hospitalier Universitaire Vaudois (CH)
- National Human Genome Research Institute (US)
- University College London (GB)
- Cedars-Sinai Medical Center (US)
- University of Bristol (GB)
- Framingham Heart Study (US)
- Brigham and Women's Hospital (US)
- Mario Negri Institute for Pharmacological Research (IT)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Eurac Research (IT)
- Sir Charles Gairdner Hospital (AU)
- Glostrup Hospital (DK)
- University of Copenhagen (DK)
- University of Helsinki (FI)
- Finnish Institute for Health and Welfare (FI)
- University of Southern Denmark (DK)
- Lund University (SE)
- University of California, San Francisco (US)
- Queen Elizabeth II Medical Centre (AU)
- Churchill Hospital (GB)
- University of Dundee (GB)
- Oulu University Hospital (FI)
- Washington University in St. Louis (US)
- Group Health Cooperative (US)
- Deutsches Diabetes-Zentrum e.V. (DE)
- Aarhus University (DK)
- University of Cambridge (GB)
- Southampton General Hospital (GB)
- The University of Texas MD Anderson Cancer Center (US)
- University of Münster (DE)
- National Institutes of Health (US)
- Leipzig University (DE)
- Folkhälsans Forskningscentrum (FI)
- deCODE Genetics (Iceland) (IS)
- Queen's University Belfast (GB)
- Technische Universität Dresden (DE)
- London School of Hygiene & Tropical Medicine (GB)
- University of Minnesota (US)
- National Health Service (GB)
- Kuopio University Hospital (FI)
- University of Edinburgh (GB)
- ORCID
- Dupuis, Josée
- Langenberg, Claudia
- Prokopenko, Inga
- Saxena, Richa
- Soranzo, Nicole
- Wheeler, Eleanor
- Glazer, Nicole L
- Gloyn, Anna L
- Lindgren, Cecilia M
- Mägi, Reedik
- Morris, Andrew P
- Johnson, Toby
- Elliott, Paul
- Rybin, Denis
- Henneman, Peter
- Grallert, Harald
- Dehghan, Abbas
- Hottenga, Jouke Jan
- Navarro, Pau
- Goel, Anuj
- Perry, John R B
- Egan, Josephine M
- Lajunen, Taina
- Grarup, Niels
- Doney, Alex
- Voight, Benjamin F
- Stringham, Heather M
- Li, Man
- Kanoni, Stavroula
- Qi, Lu
- Timpson, Nicholas J
- Gieger, Christian
- Rocheleau, Ghislain
- Ingelsson, Erik
- An, Ping
- Luan, Jian'an
- McCarroll, Steven A
- Payne, Felicity
- Pattou, François
- Sethupathy, Praveen
- Ardlie, Kristin
- Balkau, Beverley
- Beilby, John P
- Benediktsson, Rafn
- Bennett, Amanda J
- Bochud, Murielle
- Boerwinkle, Eric
- Bonnefond, Amélie
- Bonnycastle, Lori L
- Brunner, Eric
- Charpentier, Guillaume
- Chen, Yii-Der Ida
- Clarke, Robert
- Coin, Lachlan J M
- Cooper, Matthew N
- Cornelis, Marilyn
- Crisponi, Laura
- Erdos, Michael R
- Forouhi, Nita G
- Fox, Caroline S
- Galan, Pilar
- Goodarzi, Mark O
- Grundy, Scott
- Gyllensten, Ulf
- Hadjadj, Samy
- Hallmans, Göran
- Han, Xijing
- Hayward, Caroline
- Heath, Simon C
- Herder, Christian
- Hicks, Andrew A
- Hillman, David R
- Hingorani, Aroon D
- Hui, Jennie
- Jørgensen, Torben
- Jula, Antti
- Kaakinen, Marika
- Kaprio, Jaakko
- Kovacs, Peter
- Kyvik, Kirsten Ohm
- Lawlor, Debbie A
- Li, Yun
- Lyssenko, Valeriya
- Mahley, Robert
- Mangino, Massimo
- Manning, Alisa K
- McCulloch, Laura J
- McPherson, Ruth
- Meisinger, Christa
- Melzer, David
- Meyre, David
- Mitchell, Braxton D
- Mukherjee, Sutapa
- Naitza, Silvia
- Narisu, Narisu
- Neville, Matthew J
- Orrù, Marco
- Paolisso, Giuseppe
- Pattaro, Cristian
- Pearson, Daniel
- Pedersen, Nancy L
- Pfeiffer, Andreas F H
- Pichler, Irene
- Potter, Simon C
- Province, Michael A
- Psaty, Bruce M
- Rathmann, Wolfgang
- Rayner, Nigel W
- Rice, Kenneth
- Ripatti, Samuli
- Rivadeneira, Fernando
- Roden, Michael
- Rolandsson, Olov
- Sandhu, Manjinder
- Sanna, Serena
- Sayer, Avan Aihie
- Scheet, Paul
- Scott, Laura J
- Seedorf, Udo
- Sharp, Stephen J
- Shields, Beverley
- Sijbrands, Eric J G
- Silveira, Angela
- Simpson, Laila
- Singleton, Andrew
- Smith, Nicholas L
- Sovio, Ulla
- Syddall, Holly
- Syvänen, Ann-Christine
- Tanaka, Toshiko
- Thorand, Barbara
- Tönjes, Anke
- Uitterlinden, André G
- Vogelzangs, Nicole
- Waeber, Gérard
- Walley, Andrew
- Walters, G Bragi
- Watkins, Hugh
- Weedon, Michael N
- Wild, Sarah H
- Willemsen, Gonneke
- Zeggini, Eleftheria
- Zethelius, Björn
- Zhai, Guangju
- Zhao, Jing Hua
- Zillikens, M Carola
- Borecki, Ingrid B
- Loos, Ruth J F
- Meneton, Pierre
- Magnusson, Patrik K E
- Williams, Gordon H
- Hattersley, Andrew T
- Salomaa, Veikko
- Smith, George Davey
- Bornstein, Stefan R
- Schwarz, Peter
- Spranger, Joachim
- Karpe, Fredrik
- Shuldiner, Alan R
- Cooper, Cyrus
- Dedoussis, George V
- Morris, Andrew D
- Lind, Lars
- Palmer, Lyle J
- Hu, Frank B
- Franks, Paul W
- Ebrahim, Shah
- Marmot, Michael
- Kao, W H Linda
- Pankow, James S
- Laakso, Markku
- Hansen, Torben
- Pedersen, Oluf
- Pramstaller, Peter Paul
- Wichmann, H Erich
- Rudan, Igor
- Wilson, James F
- Venue
- Nature Genetics
- Published
- 2010-01-17
- Volume
- 42
- Issue
- 2
- Pages
- 105-116
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC3018764
- OpenAlex
- W2159422401
- Cited by
- 2,166
- References
- 78
- Citations by year
- 2026: 31 · 2025: 55 · 2024: 88 · 2023: 96 · 2022: 98 · 2021: 107 · 2020: 132 · 2019: 121 · 2018: 137 · 2017: 144 · 2016: 164 · 2015: 162 · 2014: 155 · 2013: 182 · 2012: 193
- FWCI
- 120.76
- Type
- journal article
- Language
- en
- Update notices
- erratum (2010-05-01)
- Open access
- green
- research.vu.nl
- Licence
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- VU Research Portal (publishedVersion, other-oa)
- PubMed Central (acceptedVersion)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- SERVAL (Université de Lausanne) (acceptedVersion, other-oa)
- IRIS (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- HAL (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion)
- ePrints Soton (University of Southampton) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università degli Studi della Campania "Luigi Vanvitelli" (submittedVersion)
- UnissResearch (Università degli Studi di Sassari) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Research Portal (Queen's University Belfast) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion)
- Spiral (Imperial College London) (submittedVersion)
- OPUS (Augsburg University) (submittedVersion)
- Open Research (University of Surrey) (submittedVersion)
- Hirsla (Landspítali University Hospital) (submittedVersion)
- STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (081682, 077011, 064890, 088885, 077016, 090532, 091746, 089061)
- National Institute for Health and Care Research (NF-SI-0508-10082)
- British Heart Foundation (RG/07/008/23674)
- Economic and Social Research Council (ES/G007438/1)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK072193, R01DK078616, K24DK080140, R01DK029867, P30DK040561)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Keywords
- fasting blood glucose, type 2 diabetes risk, genetic loci, glycemic traits, fasting insulin, insulin resistance, beta-cell function, HOMA-IR, HOMA-β, ADCY5, Prox1, glucokinase, GCKR, insulin-like growth factor I, circadian regulation, glucose detection, signal transduction
- MeSH terms
- Delta-5 Fatty Acid Desaturase, Adolescent, Adult, Alleles, Blood Glucose, Child, Diabetes Mellitus, Type 2, Fasting, Gene Expression Regulation, Homeostasis, Humans, Meta-Analysis as Topic, Reproducibility of Results, Quantitative Trait, Heritable, Genetic Predisposition to Disease, Polymorphism, Single Nucleotide, Databases, Genetic, Quantitative Trait Loci, Genome-Wide Association Study, Genetic Loci, DNA Copy Number Variations
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