Recent progress in genetic and epigenetic research on type 2 diabetes

Experimental and Molecular Medicine

Volumn 48, Issue 3, 2016, Pages

  Kwak, Soo Heon ^a   Park, Kyong Soo ^a,b,c  

^a Seoul National University Hospital   (South Korea)

^b Seoul National University   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; MICRORNA; NOTCH2 RECEPTOR; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR PAX4;

ADAMTS9 GENE; CAMK1D GENE; CDC123 GENE; CDKAL1 GENE; CDKN2A GENE; CDKN2B GENE; DIABETOGENESIS; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; FITM2 GENE; FTO GENE; GCC1 GENE; GENE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOCUS; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC VARIABILITY; GENETICS; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; GLIS3 GENE; HEREDITY; HISTONE MODIFICATION; HNF4A GENE; HUMAN; IGF2BP2 GENE; JAZF1 GENE; KCNJ11 GENE; KCNK16 GENE; LGR5 GENE; MAEA GENE; NON INSULIN DEPENDENT DIABETES MELLITUS; NOTCH2 GENE; PAX4 GENE; PEPD GENE; PPARG GENE; PSMD6 GENE; R3HDML GENE; REVIEW; SEQUENCE ANALYSIS; TCF7L2 GENE; THADA GENE; TSPAN8 GENE; ZFAND GENE; ANIMAL; ENVIRONMENTAL EXPOSURE; GENETIC ASSOCIATION STUDY; GENETIC EPIGENESIS; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; QUANTITATIVE TRAIT; QUANTITATIVE TRAIT LOCUS;

ANIMALS; DIABETES MELLITUS, TYPE 2; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; EPIGENOMICS; GENE-ENVIRONMENT INTERACTION; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HUMANS; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE;

EID: 84978658427     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2016.7     Document Type: Review

References (64)

1. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014; 103: 137-149.
2. Hemminki K, Li X, Sundquist K, Sundquist J. Familial risks for type 2 diabetes in Sweden. Diabetes Care 2010; 33: 293-297.
3. Meigs JB, Cupples LA, Wilson PW. Parental transmission of type 2 diabetes: the Framingham Offspring Study. Diabetes 2000; 49: 2201-2207.
4. Collins FS, Varmus H. A new initiative on precision medicine. N Engl JMed 2015; 372: 793-795.
5. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, Serre D, et al. A genomewide association study identifies novel risk loci for type 2 diabetes. Nature 2007; 445: 881-885.
6. 1000 Genomes Project Consortium, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, et al. A global reference for human genetic variation. Nature 2015; 526: 68-74.
7. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011; 43: 491-498.
8. McCarthy MI. Genomics, type 2 diabetes, and obesity. N Engl JMed 2010; 363: 2339-2350.
9. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, et al. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 2007; 316: 1341-1345.
10. Zeggini E, Weedon MN, Lindgren CM, Frayling TM, Elliott KS, Lango H, et al. Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 2007; 316: 1336-1341.
11. Diabetes Genetics Initiative of Broad Institute of Harvard and MIT, Lund University, Novartis Institutes of BioMedical Research, Saxena R, Voight BF, Lyssenko V, et al. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 2007; 316: 1331-1336.
12. Zeggini E, Scott LJ, Saxena R, Voight BF, Marchini JL, Hu T, et al. Metaanalysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 2008; 40: 638-645.
13. Voight BF, Scott LJ, Steinthorsdottir V, Morris AP, Dina C, Welch RP, et al. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat Genet 2010; 42: 579-U155.
14. Unoki H, Takahashi A, Kawaguchi T, Hara K, Horikoshi M, Andersen G, et al. SNPs in KCNQ1 are associated with susceptibility to type 2 diabetes in East Asian and European populations. Nat Genet 2008; 40: 1098-1102.
15. Yasuda K, Miyake K, Horikawa Y, Hara K, Osawa H, Furuta H, et al. Variants in KCNQ1 are associated with susceptibility to type 2 diabetes mellitus. Nat Genet 2008; 40: 1092-1097.
16. Cho YS, Chen CH, Hu C, Long J, Ong RT, Sim X, et al. Meta-Analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in east Asians. Nat Genet 2012; 44: 67-72.
17. Go MJ, Hwang JY, Park TJ, Kim YJ, Oh JH, Kim YJ, et al. Genome-wide association study identifies two novel Loci with sex-specific effects for type 2 diabetes mellitus and glycemic traits in a korean population. Diabetes Metab J 2014; 38: 375-387.
18. Kooner JS, Saleheen D, Sim X, Sehmi J, Zhang W, Frossard P, et al. Genome-wide association study in individuals of South Asian ancestry identifies six new type 2 diabetes susceptibility loci. Nat Genet 2011; 43: 984-989.
19. Palmer ND, McDonough CW, Hicks PJ, Roh BH, Wing MR, An SS, et al. A genome-wide association search for type 2 diabetes genes in African Americans. PLoS ONE 2012; 7: e29202.
20. SIGMA Type 2 Diabetes Consortium, Williams AL, Jacobs SB, Moreno-Macias H, Huerta-Chagoya A, Churchhouse C, et al. Sequence variants in SLC16A11 are a common risk factor for type 2 diabetes in Mexico. Nature 2014; 506: 97-101.
21. Palmer ND, Ng MC, Hicks PJ, Mudgal P, Langefeld CD, Freedman BI, et al. Evaluation of candidate nephropathy susceptibility genes in a genome-wide association study of African American diabetic kidney disease. PLoS ONE 2014; 9: e88273.
22. Voight BF, Kang HM, Ding J, Palmer CD, Sidore C, Chines PS, et al. The metabochip, a custom genotyping array for genetic studies of metabolic, cardiovascular, and anthropometric traits. PLoS Genet 2012; 8: e1002793.
23. Morris AP, Voight BF, Teslovich TM, Ferreira T, Segre AV, Steinthorsdottir V, et al. Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat Genet 2012; 44: 981-990.
24. Moltke I, Grarup N, Jorgensen ME, Bjerregaard P, Treebak JT, Fumagalli M, et al. A common Greenlandic TBC1D4 variant confers muscle insulin resistance and type 2 diabetes. Nature 2014; 512: 190-193.
25. DIAbetes Genetics Replication And Meta-Analysis (DIAGRAM) Consortium, Asian Genetic Epidemiology Network Type 2 Diabetes (AGEN-T2D) Consortium, South Asian Type 2 Diabetes (SAT2D) Consortium, Mexican American Type 2 Diabetes (MAT2D) Consortium, Type 2 Diabetes Genetic Exploration by Nex-generation sequencing in muylti-Ethnic Samples (T2D-GENES) Consortium, Mahajan A, et al. Genome-wide trans-Ancestry meta-Analysis provides insight into the genetic architecture of type 2 diabetes susceptibility. Nat Genet 2014; 46: 234-244.
26. Bonnefond A, Clement N, Fawcett K, Yengo L, Vaillant E, Guillaume JL, et al. Rare MTNR1B variants impairing melatonin receptor 1B function contribute to type 2 diabetes. Nat Genet 2012; 44: 297-301.
27. Majithia AR, Flannick J, Shahinian P, Guo M, Bray MA, Fontanillas P, et al. Rare variants in PPARG with decreased activity in adipocyte differentiation are associated with increased risk of type 2 diabetes. Proc Natl Acad Sci USA 2014; 111: 13127-13132.
28. Flannick J, Thorleifsson G, Beer NL, Jacobs SB, Grarup N, Burtt NP, et al. Loss-of-function mutations in SLC30A8 protect against type 2 diabetes. Nat Genet 2014; 46: 357-363.
29. Steinthorsdottir V, Thorleifsson G, Sulem P, Helgason H, Grarup N, Sigurdsson A, et al. Identification of low-frequency and rare sequence variants associated with elevated or reduced risk of type 2 diabetes. Nat Genet 2014; 46: 294-298.
30. SIGMA Type 2 Diabetes Consortium, Estrada K, Aukrust IA, Bjorkhaug L, Burtt NP, Mercader JM, et al. Association of a low-frequency variant in HNF1A with type 2 diabetes in a Latino population. JAMA 2014; 311: 2305-2314.
31. Bouatia-Naji N, Rocheleau G, Van Lommel L, Lemaire K, Schuit F, Cavalcanti-Proenca C, et al. A polymorphism within the G6PC2 gene is associated with fasting plasma glucose levels. Science 2008; 320: 1085-1088.
32. Prokopenko I, Langenberg C, Florez JC, Saxena R, Soranzo N, Thorleifsson G, et al. Variants in MTNR1B influence fasting glucose levels. Nat Genet 2009; 41: 77-81.
33. Lyssenko V, Nagorny CL, Erdos MR, Wierup N, Jonsson A, Spegel P, et al. Common variant in MTNR1B associated with increased risk of type 2 diabetes and impaired early insulin secretion. Nat Genet 2009; 41: 82-88.
34. Bouatia-Naji N, Bonnefond A, Cavalcanti-Proenca C, Sparso T, Holmkvist J, Marchand M, et al. A variant near MTNR1B is associated with increased fasting plasma glucose levels and type 2 diabetes risk. Nat Genet 2009; 41: 89-94.
35. Saxena R, Hivert MF, Langenberg C, Tanaka T, Pankow JS, Vollenweider P, et al. Genetic variation in GIPR influences the glucose and insulin responses to an oral glucose challenge. Nat Genet 2010; 42: 142-148.
36. Dupuis J, Langenberg C, Prokopenko I, Saxena R, Soranzo N, Jackson AU, et al. New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat Genet 2010; 42: 105-116.
37. Scott RA, Lagou V, Welch RP, Wheeler E, Montasser ME, Luan J, et al. Large-scale association analyses identify new loci influencing glycemic traits and provide insight into the underlying biological pathways. Nat Genet 2012; 44: 991-1005.
38. Hwang JY, Sim X, Wu Y, Liang J, Tabara Y, Hu C, et al. Genome-wide association meta-Analysis identifies novel variants associated with fasting plasma glucose in East Asians. Diabetes 2015; 64: 291-298.
39. Mahajan A, Sim X, Ng HJ, Manning A, Rivas MA, Highland HM, et al. Identification and functional characterization of G6PC2 coding variants influencing glycemic traits define an effector transcript at the G6PC2-ABCB11 locus. PLoS Genet 2015; 11: e1004876.
40. Wessel J, Chu AY, Willems SM, Wang S, Yaghootkar H, Brody JA, et al. Lowfrequency and rare exome chip variants associate with fasting glucose and type 2 diabetes susceptibility. Nat Commun 2015; 6: 5897.
41. Wu C, Morris JR. Genes, genetics, and epigenetics: a correspondence. Science 2001; 293: 1103-1105.
42. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 1992; 35: 595-601.
43. Ravelli AC, van der Meulen JH, Michels RP, Osmond C, Barker DJ, Hales CN, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet 1998; 351: 173-177.
44. Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest 2008; 118: 2316-2324.
45. Lee YY, Park KS, Pak YK, Lee HK. The role of mitochondrial DNA in the development of type 2 diabetes caused by fetal malnutrition. J Nutr Biochem 2005; 16: 195-204.
46. Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, Gabir MM, et al. Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 2000; 49: 2208-2211.
47. Hall E, Volkov P, Dayeh T, Bacos K, Ronn T, Nitert MD, et al. Effects of palmitate on genome-wide mRNA expression and DNA methylation patterns in human pancreatic islets. BMC Med 2014; 12: 103.
48. Bibikova M, Le J, Barnes B, Saedinia-Melnyk S, Zhou L, Shen R, et al. Genome-wide DNA methylation profiling using Infinium(R) assay. Epigenomics 2009; 1: 177-200.
49. ENCODE Project Consortium, An integrated encyclopedia of DNA elements in the human genome Nature 2012 489 57-74.
50. Roadmap Epigenomics Consortium, Kundaje A, Meuleman W, Ernst J, Bilenky M, Yen A, et al. Integrative analysis of 111 reference human epigenomes. Nature 2015; 518: 317-330.
51. Toperoff G, Aran D, Kark JD, Rosenberg M, Dubnikov T, Nissan B, et al. Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood. Hum Mol Genet 2012; 21: 371-383.
52. Chambers JC, Loh M, Lehne B, Drong A, Kriebel J, Motta V, et al. Epigenome-wide association of DNA methylation markers in peripheral blood from Indian Asians and Europeans with incident type 2 diabetes: a nested case-control study. Lancet Diabetes Endocrinol 2015; 3: 526-534.
53. Florath I, Butterbach K, Heiss J, Bewerunge-Hudler M, Zhang Y, Schottker B, et al. Type 2 diabetes and leucocyte DNA methylation: an epigenomewide association study in over 1500 older adults. Diabetologia 2015; 59: 130-138.
54. Kulkarni H, Kos MZ, Neary J, Dyer TD, Kent JW Jr., Goring HH, et al. Novel epigenetic determinants of type 2 diabetes in Mexican-American families. Hum Mol Genet 2015; 24: 5330-5344.
55. Parikh H, Carlsson E, Chutkow WA, Johansson LE, Storgaard H, Poulsen P, et al. TXNIP regulates peripheral glucose metabolism in humans. PLoS Med 2007; 4: e158.
56. Minn AH, Hafele C, Shalev A. Thioredoxin-interacting protein is stimulated by glucose through a carbohydrate response element and induces beta-cell apoptosis. Endocrinology 2005; 146: 2397-2405.
57. Stitzel ML, Sethupathy P, Pearson DS, Chines PS, Song L, Erdos MR, et al. Global epigenomic analysis of primary human pancreatic islets provides insights into type 2 diabetes susceptibility loci. Cell Metab 2010; 12: 443-455.
58. Pasquali L, Gaulton KJ, Rodriguez-Segui SA, Mularoni L, Miguel-Escalada I, Akerman I, et al. Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-Associated variants. Nat Genet 2014; 46: 136-143.
59. Dayeh T, Volkov P, Salo S, Hall E, Nilsson E, Olsson AH, et al. Genome-wide DNA methylation analysis of human pancreatic islets from type 2 diabetic and non-diabetic donors identifies candidate genes that influence insulin secretion. PLoS Genet 2014; 10: e1004160.
60. Barres R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 2009; 10: 189-198.
61. Barres R, Yan J, Egan B, Treebak JT, Rasmussen M, Fritz T, et al. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab 2012; 15: 405-411.
62. Ronn T, Volkov P, Davegardh C, Dayeh T, Hall E, Olsson AH, et al. A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue. PLoS Genet 2013; 9: e1003572.
63. Kim AY, Park YJ, Pan X, Shin KC, Kwak SH, Bassas AF, et al. Obesityinduced DNA hypermethylation of the adiponectin gene mediates insulin resistance. Nat Commun 2015; 6: 7585.
64. Nakatochi M, Ichihara S, Yamamoto K, Ohnaka K, Kato Y, Yokota S, et al. Epigenome-wide association study suggests that SNPs in the promoter region of RETN influence plasma resistin level via effects on DNA methylation at neighbouring sites. Diabetologia 2015; 58: 2781-2790.