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Transferability of Type 2 Diabetes Implicated Loci in Multi-Ethnic Cohorts from Southeast Asia
Open accessAbstract
Recent large genome-wide association studies (GWAS) have identified multiple loci which harbor genetic variants associated with type 2 diabetes mellitus (T2D), many of which encode proteins not previously suspected to be involved in the pathogenesis of T2D. Most GWAS for T2D have focused on populations of European descent, and GWAS conducted in other populations with different ancestry offer a unique opportunity to study the genetic architecture of T2D. We performed genome-wide association scans for T2D in 3,955 Chinese (2,010 cases, 1,945 controls), 2,034 Malays (794 cases, 1,240 controls), and 2,146 Asian Indians (977 cases, 1,169 controls). In addition to the search for novel variants implicated in T2D, these multi-ethnic cohorts serve to assess the transferability and relevance of the previous findings from European descent populations in the three major ethnic populations of Asia, comprising half of the world's population. Of the SNPs associated with T2D in previous GWAS, only variants at CDKAL1 and HHEX/IDE/KIF11 showed the strongest association with T2D in the meta-analysis including all three ethnic groups. However, consistent direction of effect was observed for many of the other SNPs in our study and in those carried out in European populations. Close examination of the associations at both the CDKAL1 and HHEX/IDE/KIF11 loci provided some evidence of locus and allelic heterogeneity in relation to the associations with T2D. We also detected variation in linkage disequilibrium between populations for most of these loci that have been previously identified. These factors, combined with limited statistical power, may contribute to the failure to detect associations across populations of diverse ethnicity. These findings highlight the value of surveying across diverse racial/ethnic groups towards the fine-mapping efforts for the casual variants and also of the search for variants, which may be population-specific.
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“Under a mutation-selection balance model, it may be possible for different novel rare variants to have effects in each population, and fine mapping studies sometimes reveal subtle differences in the patterns of association [eg.67,68.”
From Rare and common variants: twenty arguments (2012) · cites this paper as [67]
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BackgroundReplication of Genome-Wide Association Signals in UK Samples Reveals Risk Loci for Type 2 Diabetes
Zeggini, E., Weedon, M. N., Lindgren, C. M., Frayling, T. M., Elliott, K. S., Lango, H., Timpson, N. J., Perry, J. R. B., Rayner, N. W., Freathy, R. M., et al. (2007) · Science · doi:10.1126/science.1142364 · Cited by 2,194 · cited 3×
“It is noteworthy that the variants for which we were able to detect an association in our study were mostly discovered in the earlier wave of genome-wide scans for T2D (including CDKAL1, HHEX/IDE/KIF11, IGFBP2, SLC30A8 and FTO) [5–7,51].”
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Self-citationThe common PPARγ Pro12Ala polymorphism is associated with decreased risk of type 2 diabetes
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Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis
The MAGIC investigators, Voight, B. F., The GIANT Consortium, Scott, L. J., Steinthorsdottir, V., Morris, A. P., Dina, C., Welch, R. P., Zeggini, E., Huth, C., et al. (2010) · Nature Genetics · doi:10.1038/ng.609 · Cited by 1,761 · cited 4×
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“These genome-wide association studies (GWAS) have identified a number of novel loci harboring common variants that are associated with an increased risk of T2D [4–11], adding to the loci previously identified by candidate gene studies (PPARG [12], KCNJ11 [13–14], WFS1 [15–16]) and linkage studies TCF7L2 [17–19]).”
BackgroundMechanisms by which common variants in the TCF7L2 gene increase risk of type 2 diabetes
Lyssenko, V., Lupi, R., Marchetti, P., Guerra, S. D., Orho‐Melander, M., Almgren, P., Sjögren, M., Ling, C., Eriksson, K., Lethagen, Υ.-L., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30706 · Cited by 837 · cited 1×
“These genome-wide association studies (GWAS) have identified a number of novel loci harboring common variants that are associated with an increased risk of T2D [4–11], adding to the loci previously identified by candidate gene studies (PPARG [12], KCNJ11 [13–14], WFS1 [15–16]) and linkage studies TCF7L2 [17–19]).”
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Variants in KCNQ1 are associated with susceptibility to type 2 diabetes mellitus
Yasuda, K., Miyake, K., Horikawa, Y., Hara, K., Osawa, H., Furuta, H., Hirota, Y., Mori, H., Jonsson, A., Sato, Y., et al. (2008) · Nature Genetics · doi:10.1038/ng.207 · Cited by 776 · cited 2×
“These genome-wide association studies (GWAS) have identified a number of novel loci harboring common variants that are associated with an increased risk of T2D [4–11], adding to the loci previously identified by candidate gene studies (PPARG [12], KCNJ11 [13–14], WFS1 [15–16]) and linkage studies TCF7L2 [17–19]).”
BackgroundGloyn, A. L., Weedon, M. N., Owen, K. R., Turner, M. J., Knight, B. A., Hitman, G., Walker, M., Levy, J. C., Sampson, M., Halford, S., et al. (2003) · Diabetes · doi:10.2337/diabetes.52.2.568 · Cited by 754
Unoki, H., Takahashi, A., Kawaguchi, T., Hara, K., Horikoshi, M., Andersen, G., Ng, D. P. K., Holmkvist, J., Borch-Johnsen, K., Jørgensen, T., et al. (2008) · Nature Genetics · doi:10.1038/ng.208 · Cited by 725 · cited 2×
“These genome-wide association studies (GWAS) have identified a number of novel loci harboring common variants that are associated with an increased risk of T2D [4–11], adding to the loci previously identified by candidate gene studies (PPARG [12], KCNJ11 [13–14], WFS1 [15–16]) and linkage studies TCF7L2 [17–19]).”
BackgroundSelf-citationFoong, A. W. P., Saw, S., Loo, J.-L., Shen, S. Y., Loon, S., Rosman, M., Aung, T., Tan, D. T. H., Tai, E. S., & Wong, T. Y. (2007) · Ophthalmic Epidemiology · doi:10.1080/09286580600878844 · Cited by 432 · cited 1×
“Details of the study participants and methods have been published previously [56].”
MethodSelf-citationCommon variants in WFS1 confer risk of type 2 diabetes
Sandhu, M. S., Weedon, M. N., Fawcett, K. A., Wasson, J., Debenham, S. L., Daly, A., Allen, H. L., Frayling, T. M., Neumann, R. J., Sherva, R., et al. (2007) · Nature Genetics · doi:10.1038/ng2067 · Cited by 378 · cited 1×
“These genome-wide association studies (GWAS) have identified a number of novel loci harboring common variants that are associated with an increased risk of T2D [4–11], adding to the loci previously identified by candidate gene studies (PPARG [12], KCNJ11 [13–14], WFS1 [15–16]) and linkage studies TCF7L2 [17–19]).”
BackgroundNg, M. C. Y., Park, K. S., Oh, B., Tam, C. H. T., Cho, Y. M., Shin, H. D., Lam, V. K. L., Ma, R. C. W., So, W. Y., Cho, Y. S., et al. (2008) · Diabetes · doi:10.2337/db07-1583 · Cited by 362
Tsai, F., Yang, C.-F., Chen, C., Chuang, L., Lu, C.-H., Chang, C., Wang, T.-Y., Chen, R.-H., Shiu, C.-F., Liu, Y.-M., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000847 · Cited by 348 · cited 3×
“Based on the allele frequencies observed in our studies and the sample sizes available, we had at least 80% power to detect the associations for only 8 (TCF7L2, HNF1B, UBE2E2, CDKAL1, SLC30A8, HHEX, KCNQ1 and SRR) of the 36 variants in the Chinese (the ethnic group with the largest sample size), 1 in the Malays (SRR)…”
BackgroundLavanya, R., Jeganathan, V. S. E., Zheng, Y., Raju, P., Cheung, N., Tai, E. S., Wang, J. J., Lamoureux, E. L., Mitchell, P. L. R., Young, T. L., et al. (2009) · Ophthalmic Epidemiology · doi:10.3109/09286580903144738 · Cited by 320 · cited 1×
“Detailed methodology has been published [57].”
Self-citationOmori, S., Tanaka, Y., Takahashi, A., Hirose, H., Kashiwagi, A., Kaku, K., Kawamori, R., Nakamura, Y., & Maeda, S. (2007) · Diabetes · doi:10.2337/db07-0979 · Cited by 279 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultGrarup, N., Rose, C. S., Galijatovic, E. A. A., Andersen, G., Nielsen, A. L., Albrechtsen, A., Clausen, J. O., Rasmussen, S. S., Jørgensen, T., Sandbæk, A., et al. (2007) · Diabetes · doi:10.2337/db07-0856 · Cited by 263 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultGroves, C. J., Zeggini, E., Minton, J. A. L., Frayling, T. M., Weedon, M. N., Rayner, N. W., Hitman, G. A., Walker, M., Wiltshire, S., Hattersley, A. T., et al. (2006) · Diabetes · doi:10.2337/db06-0355 · Cited by 252
Wu, Y., Li, H., Loos, R. J. F., Yu, Z., Ye, X., Chen, L., Pan, A., Hu, F. B., & Lin, X. (2008) · Diabetes · doi:10.2337/db08-0047 · Cited by 240 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultTakeuchi, F., Serizawa, M., Yamamoto, K., Fujisawa, T., Nakashima, E., Ohnaka, K., Ikegami, H., Sugiyama, T., Katsuya, T., Miyagishi, M., et al. (2009) · Diabetes · doi:10.2337/db08-1494 · Cited by 235 · cited 6×
“discovered in a Japanese study [20] conferred a protective effect”
BackgroundResultInfluentialHorikoshi, M., Hara, K., Ito, C., Shojima, N., Nagai, R., Ueki, K., Froguel, P., & Kadowaki, T. (2007) · Diabetologia · doi:10.1007/s00125-007-0827-5 · Cited by 211 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultTan, C., Emmanuel, S. C., Tan, B. Y., & Jacob, E. B. (1999) · Diabetes Care · doi:10.2337/diacare.22.2.241 · Cited by 210
Hughes, K., Aw, T. C., Kuperan, P., & Choo, M. H. (1997) · Journal of Epidemiology & Community Health · doi:10.1136/jech.51.4.394 · Cited by 206 · cited 1×
“The Singapore Prospective Study Program (SP2) includes 6,968 participants from one of four previous cross-sectional studies: Thyroid and Heart Study 1982–1984 [52], National Health Survey 1992 [53], National University of Singapore Heart Study 1993–1995 [54] or National Health Survey 1998 [55].”
MethodHughes, K., Yeo, P. P., Lun, K. C., Thai, A. C., Sothy, S. P., Wang, K. W., Cheah, J. S., Phoon, W. O., & Lim, P. (1990) · Journal of Epidemiology & Community Health · doi:10.1136/jech.44.1.29 · Cited by 180 · cited 1×
“The Singapore Prospective Study Program (SP2) includes 6,968 participants from one of four previous cross-sectional studies: Thyroid and Heart Study 1982–1984 [52], National Health Survey 1992 [53], National University of Singapore Heart Study 1993–1995 [54] or National Health Survey 1998 [55].”
MethodHu, C., Zhang, R., Wang, C., Wang, J., Ma, X., Lu, J., Qin, W., Hou, X., Wang, C., Bao, Y., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007643 · Cited by 178 · cited 2×
“However, replication efforts for the more recently identified SNPs have been less successful [32,46–48].”
BackgroundResultLee, Y., Kang, E. S., Kim, S. H., Han, S. J., Kim, C. H., Kim, H. J., Ahn, C. W., Soo, B., Nam, M., Nam, C. M., et al. (2008) · Journal of Human Genetics · doi:10.1007/s10038-008-0341-8 · Cited by 174 · cited 2×
“Of these, only the association at KCNQ1 has been extensively replicated [11,20–21,23–30].”
BackgroundResultSingapore Genome Variation Project: A haplotype map of three Southeast Asian populationsPreprint
Teo, Y., Sim, X., Ong, R. T., Tan, A. K. S., Chen, J., Tantoso, E., Small, K. S., Ku, C., Lee, E. J. D., Seielstad, M. T., et al. (2009) · Genome Research · doi:10.1101/gr.095000.109 · Cited by 173 · cited 4×
“Found at: doi:10.1371/journal.pgen.1001363.s001 (0.42 MB TIF) Figure S2 Principal components analysis (PCA) plots of genetic diversity for each of the case control study and when superimposed against the Singapore Genome Variation Project (SGVP) populations.”
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“While the direction and magnitude of the effects sizes were similar in our populations and previous reports [24,49–50], statistical significance was only observed in the Indian GWAS.”
ResultReplication of Genome-Wide Association Studies of Type 2 Diabetes Susceptibility in Japan
Horikawa, Y., Miyake, K., Yasuda, K., Enya, M., Hirota, Y., Yamagata, K., Hinokio, Y., Oka, Y., Iwasaki, N., Iwamoto, Y., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0452 · Cited by 150 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultReplication Study of Candidate Genes Associated With Type 2 Diabetes Based On Genome-Wide Screening
Tabara, Y., Osawa, H., Kawamoto, R., Onuma, H., Shimizu, I., Miki, T., Kohara, K., & Makino, H. (2008) · Diabetes · doi:10.2337/db07-1785 · Cited by 144 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
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Wen, J., Rönn, T., Olsson, A., Yang, Z., Lu, B., Du, Y., Groop, L., Ling, C., & Ren-ming, H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009153 · Cited by 124 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultHu, C., Wang, C., Zhang, R., Ma, X., Wang, J., Lu, J., Qin, W., Bao, Y., Xiang, K., & Jia, W. (2009) · Diabetologia · doi:10.1007/s00125-009-1335-6 · Cited by 123 · cited 1×
“Of these, only the association at KCNQ1 has been extensively replicated [11,20–21,23–30].”
BackgroundFranks, P. W., Rolandsson, O., Debenham, S. L., Fawcett, K. A., Payne, F., Dina, C., Froguel, P., Mohlke, K. L., Willer, C. J., Olsson, T., et al. (2007) · Diabetologia · doi:10.1007/s00125-007-0887-6 · Cited by 115
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Hertel, J. K., Johansson, S., Ræder, H., Midthjell, K., Lyssenko, V., Groop, L., Molven, A., & Njølstad, P. R. (2008) · Diabetologia · doi:10.1007/s00125-008-0982-3 · Cited by 97 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultLin, Y., Li, P., Li, C., Zhang, B., Tang, X., Zhang, X., Li, Y., Yang, X. Q., Yang, Y., Wang, L., et al. (2010) · BMC Medical Genetics · doi:10.1186/1471-2350-11-97 · Cited by 87 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultLiu, Y., Zhou, D., Zhang, D., Chen, Z., Zhao, T., Zhang, Z., Ning, M., Hu, X., Yang, Y., Zhang, Z., et al. (2009) · Diabetologia · doi:10.1007/s00125-009-1375-y · Cited by 85 · cited 1×
“Of these, only the association at KCNQ1 has been extensively replicated [11,20–21,23–30].”
BackgroundGenetic Variation in KCNQ1 Associates With Fasting Glucose andβ-Cell Function
Tan, J. T., Nurbaya, S., Gardner, D. S.-L., Ye, S., Tai, E. S., & Ng, D. P. K. (2009) · Diabetes · doi:10.2337/db08-1138 · Cited by 82 · cited 1×
“Of these, only the association at KCNQ1 has been extensively replicated [11,20–21,23–30].”
BackgroundSelf-citationTan, J. T., Ng, D. P. K., Yaakub, S. N., Ye, S., Lim, X. L., Leong, H., Seet, L. T., Siew, W. F., Kon, W. Y. C., Wong, T. Y., et al. (2009) · Endocrine Reviews · doi:10.1210/edrv.30.7.9999 · Cited by 77
Self-citationTan, J. T., Ng, D. P. K., Yaakub, S. N., Ye, S., Lim, X. L., Leong, H., Seet, L. T., Siew, W. F., Kon, W. Y. C., Wong, T. Y., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0688 · Cited by 76 · cited 1×
“We have previously shown that SNPs associated with T2D in European populations also show similar associations in populations of Asian ethnicity [24].”
BackgroundSelf-citationHerder, C., Rathmann, W., Straßburger, K., Finner, H., Grallert, H., Huth, C., Meisinger, C., Gieger, C., Martin, S., Giani, G., et al. (2008) · Hormone and Metabolic Research · doi:10.1055/s-2008-1078730 · Cited by 71 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultGenome-wide comparisons of variation in linkage disequilibriumPreprint
Teo, Y. Y., Fry, A. E., Bhattacharya, K., Small, K. S., Kwiatkowski, D. P., & Clark, T. G. (2009) · Genome Research · doi:10.1101/gr.092189.109 · Cited by 71 · cited 1×
“The varLD algorithm [64–65] was used to assess regional patterns of LD variation between two populations.”
MethodSelf-citationFurukawa, Y., Shimada, T., Furuta, H., Matsuno, S., Kusuyama, A., Doi, A., Nishi, M., Sasaki, H., Sanke, T., & Nanjo, K. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1029 · Cited by 64 · cited 1×
“Many of these studies, conducted in individuals of Han Chinese, Japanese, Asian Indians, exhibited replication for many of the index SNPs that emerged from the first wave of T2D GWAS [4–7] with consistent direction of effect [20,23–24,30–45].”
ResultvarLD: a program for quantifying variation in linkage disequilibrium patterns between populations
Ong, R. T., & Teo, Y. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq125 · Cited by 59
Self-citationQi, Q., Li, H., Loos, R. J. F., Liu, C., Wu, Y., Hu, F. B., Wu, H., Lu, L., Yu, Z., & Xu, L. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp294 · Cited by 53 · cited 1×
“Of these, only the association at KCNQ1 has been extensively replicated [11,20–21,23–30].”
BackgroundPositive association between variations in CDKAL1 and type 2 diabetes in Han Chinese individuals
Liu, Y., Yu, L., Zhang, D., Chen, Z., Zhou, D., Zhao, T., Li, S., Wang, T., Hu, X., Feng, G., et al. (2008) · Diabetologia · doi:10.1007/s00125-008-1141-6 · Cited by 45
Sanghera, D. K., Been, L. F., Ortega, L., Wander, G. S., Mehra, N. K., Aston, C. E., Mulvihill, J. J., & Ralhan, S. K. (2009) · Journal of Human Genetics · doi:10.1038/jhg.2009.7 · Cited by 42 · cited 1×
“However, replication efforts for the more recently identified SNPs have been less successful [32,46–48].”
BackgroundOmori, S., Tanaka, Y., Horikoshi, M., Takahashi, A., Hara, K., Hirose, H., Kashiwagi, A., Kaku, K., Kawamori, R., Kadowaki, T., et al. (2009) · Diabetologia · doi:10.1007/s00125-009-1397-5 · Cited by 33
HHEX gene polymorphisms are associated with type 2 diabetes in the Dutch Breda cohort
van Vliet‐Ostaptchouk, J. V., Onland‐Moret, N. C., van Haeften, T. W., Franke, L., Elbers, C. C., Shiri‐Sverdlov, R., van der Schouw, Y. T., Hofker, M. H., & Wijmenga, C. (2008) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5202008 · Cited by 33
Schleinitz, D., Tönjes, A., Böttcher, Y., Dietrich, K., Enigk, B., Koriath, M., Scholz, G. H., Blüher, M., Zeggini, E., McCarthy, M. I., et al. (2009) · Hormone and Metabolic Research · doi:10.1055/s-0029-1233480 · Cited by 24
Zhou, J., Yang, J., Zhao, L., & Xin, Z. (2010) · PubMed · Cited by 24
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Sorted by citations
Rare and common variants: twenty arguments
Gibson, G. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3118 · Cited by 1,278
The genetic architecture of type 2 diabetes
Fuchsberger, C., Flannick, J., Teslovich, T. M., Mahajan, A., Agarwala, V., Gaulton, K. J., Ma, C., Fontanillas, P., Moutsianas, L., McCarthy, D. J., et al. (2016) · Nature · doi:10.1038/nature18642 · Cited by 1,051
Self-citationGenetics of Type 2 Diabetes—Pitfalls and Possibilities
Prasad, R., & Groop, L. (2015) · Genes · doi:10.3390/genes6010087 · Cited by 458
Volgman, A. S., Palaniappan, L. S., Aggarwal, N. T., Gupta, M., Khandelwal, A., Krishnan, A. V., Lichtman, J. H., Mehta, L. S., Patel, H. N., Shah, K. S., et al. (2018) · Circulation · doi:10.1161/cir.0000000000000580 · Cited by 552
Epidemiology and determinants of type 2 diabetes in south Asia
Hills, A. P., Arena, R., Khunti, K., Yajnik, C. S., Jayawardena, R., Henry, C. J., Street, S. J., Soares, M. J., & Misra, A. (2018) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(18)30204-3 · Cited by 290
Metadata
- Authors
- Sim, X., Ong, R. T.-H., Suo, C., Tay, W.-T., Liu, J., Ng, D. P.-K., Boehnke, M., Chia, K.-S., Wong, T.-Y., Seielstad, M., Teo, Y.-Y., & Tai, E.-S.
- Affiliations
- National University of Singapore (SG)
- Agency for Science, Technology and Research (SG)
- Singapore National Eye Center (SG)
- University of Michigan (US)
- The University of Melbourne (AU)
- Corresponding author
- Teo, Yik-Ying
- Tai, E-Shyong
- ORCID
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-04-07
- Volume
- 7
- Issue
- 4
- Pages
- e1001363
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3072366
- OpenAlex
- W2025086473
- Cited by
- 152
- References
- 67
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 9 · 2020: 9 · 2019: 5 · 2018: 14 · 2017: 9 · 2016: 15 · 2015: 12 · 2014: 19 · 2013: 19 · 2012: 17
- FWCI
- 12.17
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Figshare (submittedVersion, cc-by)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Funders
- National Research Foundation (03/1/27/18/216)
- National University of Singapore
- National Research Foundation Singapore (NRF-RF-2010-05)
- Genome Institute of Singapore
- Medical Research Council
- National Medical Research Council (09/1/35/19/616, NMRC/STaR/0003/2008, 03/1/27/18/216, 08/1/35/19/550, 0796/2003, STAR/0003/2008)
- Biomedical Research Council (08/1/35/19/550, 03/1/27/18/216, 0796/2003, 09/1/35/19/616)
- National Human Genome Research Institute (R56HG000376, R01HG000376)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
- Keywords
- type 2 diabetes, genetic susceptibility loci, multi-ethnic cohort, Chinese, Malay language, Asian Indians, CDKAL1, population-specific variants, allelic heterogeneity, linkage disequilibrium, fine mapping, genetic architecture
- MeSH terms
- Adult, Aged, Asia, Southeastern, Diabetes Mellitus, Type 2, Female, Humans, Male, Middle Aged, tRNA Methyltransferases, Linkage Disequilibrium, Case-Control Studies, Kinesins, Genetic Predisposition to Disease, Polymorphism, Single Nucleotide, Cyclin-Dependent Kinase 5, Genome-Wide Association Study, Genetic Loci
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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