Epigenetic modifiers of islet function and mass

Trends in Endocrinology and Metabolism

Volumn 25, Issue 12, 2014, Pages 628-636

  De Jesus, Dario F ^a,b   Kulkarni, Rohit N ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE;

ADAPTATION; AGING; BIOENERGY; CELL LOSS; DIABETES MELLITUS; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE LOCUS; GENETIC SUSCEPTIBILITY; GENOME; HUMAN; INSULIN RESISTANCE; METABOLITE; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUTRITIONAL STATUS; PANCREAS ISLET; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TARGET ORGAN;

EID: 84922605931     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2014.08.006     Document Type: Review

References (112)

1. Shaw J.E., et al. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res. Clin. Pract. 2010, 87:4-14.
2. Dirice E., Kulkarni R.N. Pathways underlying β-cell regeneration in type 1, type 2 and gestational diabetes. Islet Cell Growth Factors 2011, 142. Landies Bioscience, Texas. R.N. Kulkarni (Ed.).
3. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013, 14:R115.
4. López-Otín C., et al. The hallmarks of aging. Cell 2013, 153:1194-1217.
5. Vijg J., Suh Y. Genome instability and aging. Annu. Rev. Physiol. 2013, 75:645-668.
6. Bird A. Perceptions of epigenetics. Nature 2007, 447:396-398.
7. Dang M.N., et al. Epigenetics in autoimmune diseases with focus on type 1 diabetes. Diabetes Metab. Res. Rev. 2013, 29:8-18.
8. Rakyan V.K., et al. Identification of type 1 diabetes - associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet. 2011, 7:e1002300.
9. Gilbert E.R., Liu D. Epigenetics: the missing link to understanding beta-cell dysfunction in the pathogenesis of type 2 diabetes. Epigenetics 2012, 7:841-852.
10. Pal A., McCarthy M.I. The genetics of type 2 diabetes and its clinical relevance. Clin. Genet. 2013, 83:297-306.
11. Kluth O., et al. Differential transcriptome analysis of diabetes resistant and sensitive mouse islets reveals significant overlap with human diabetes susceptibility genes. Diabetes 2014, 10.2337/db14-0425.
12. Calvanese V., et al. The role of epigenetics in aging and age-related diseases. Ageing Res. Rev. 2009, 8:268-276.
13. Gunasekaran U., Gannon M. Type 2 diabetes and the aging pancreatic beta cell. Aging (Albany N.Y.) 2011, 3:565-575.
14. Szoke E., et al. Effect of aging on glucose homeostasis: accelerated deterioration of β-cell function in individuals with impaired glucose tolerance. Diabetes Care 2008, 31:539-543.
15. Iozzo P., et al. Independent influence of age on basal insulin secretion in nondiabetic humans. J. Clin. Endocrinol. Metab. 1999, 84:863-868.
16. Ihm S-H., et al. Effect of donor age on function of isolated human islets. Diabetes 2006, 55:1361-1368.
17. Ling C., et al. Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 2008, 51:615-622.
18. Andrali S.S., et al. Glucose regulation of insulin gene expression in pancreatic β-cells. Biochem. J. 2008, 415:1-10.
19. Kuroda A., et al. Insulin gene expression is regulated by DNA methylation. PLoS ONE 2009, 4:e6953.
20. Yang B.T., et al. Insulin promoter DNA methylation correlates negatively with insulin gene expression and positively with HbA1c levels in human pancreatic islets. Diabetologia 2011, 54:360-367.
21. Fradin D., et al. Association of the CpG methylation pattern of the proximal insulin gene promoter with type 1 diabetes. PLoS ONE 2012, 7:e36278.
22. Volkmar M., et al. DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients. EMBO J. 2012, 31:1405-1426.
23. Rieck S., Kaestner K.H. Expansion of β-cell mass in response to pregnancy. Trends Endocrinol. Metab. 2010, 21:151-158.
24. Sandovici I., et al. Developmental and environmental epigenetic programming of the endocrine pancreas: consequences for type 2 diabetes. Cell. Mol. Life Sci. 2013, 70:1575-1595.
25. Dhawan S., et al. Pancreatic β cell identity is maintained by DNA methylation-mediated repression of Arx. Dev. Cell 2011, 20:419-429.
26. Papizan J.B., et al. Nkx2.2 repressor complex regulates islet beta-cell specification and prevents beta-to-alpha-cell reprogramming. Genes Dev. 2011, 25:2291-2305.
27. Lenoir O., et al. Specific control of pancreatic endocrine β- and δ-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9. Diabetes 2011, 60:2861-2871.
28. Kulkarni R.N., et al. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J. Clin. Invest. 2004, 114:828-836.
29. Yang B.T., et al. Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes. Mol. Endocrinol. 2012, 26:1203-1212.
30. Deering T.G., et al. Methyltransferase set7/9 maintains transcription and euchromatin structure at islet-enriched genes. Diabetes 2009, 58:185-193.
31. Chen H., et al. Polycomb protein Ezh2 regulates pancreatic β-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev. 2009, 23:975-985.
32. Xu C-R., et al. Chromatin 'prepattern' and histone modifiers in a fate choice for liver and pancreas. Science 2011, 332:963-966.
33. Dhawan S., et al. Bmi-1 regulates the Ink4a/Arf locus to control pancreatic β-cell proliferation. Genes Dev. 2009, 23:906-911.
34. Zhou J.X., et al. Combined modulation of polycomb and trithorax genes rejuvenates β cell replication. J. Clin. Invest. 2013, 123:4849-4858.
35. Garcia-Ocana A., Stewart A.F. 'RAS'ling beta cells to proliferate for diabetes: why do we need MEN?. J. Clin. Invest. 2014, 124:3698-3700.
36. Karnik S.K., et al. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 2007, 318:806-809.
37. Chamberlain C.E., et al. Menin determines K-RAS proliferative outputs in endocrine cells. J. Clin. Invest. 2014, 124:4093-4101.
38. Ameres S.L., Zamore P.D. Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 2013, 14:475-488.
39. Guay C., et al. Diabetes mellitus, a microRNA-related disease?. Transl. Res. 2011, 157:253-264.
40. Zhao E., et al. Obesity and genetics regulate microRNAs in islets, liver, and adipose of diabetic mice. Mamm. Genome 2009, 20:476-485.
41. Morita S., et al. Dicer is required for maintaining adult pancreas. PLoS ONE 2009, 4:e4212.
42. Joglekar M.V., et al. Expression of islet-specific microRNAs during human pancreatic development. Gene Expr. Patterns 2009, 9:109-113.
43. Vetere A., et al. Targeting the pancreatic beta-cell to treat diabetes. Nat. Rev. Drug Discov. 2014, 13:278-289.
44. Wang Y., et al. MicroRNA-7 regulates the mTOR pathway and proliferation in adult pancreatic beta-cells. Diabetes 2013, 62:887-895.
45. Dunmore S.J., Brown J.E.P. The role of adipokines in β-cell failure of type 2 diabetes. J. Endocrinol. 2013, 216:T37-T45.
46. Weaver J.R., et al. Integration of pro-inflammatory cytokines, 12-lipoxygenase and NOX-1 in pancreatic islet beta cell dysfunction. Mol. Cell. Endocrinol. 2012, 358:88-95.
47. Qi Y., Xia P. Cellular inhibitor of apoptosis protein-1 (cIAP1) plays a critical role in β-cell survival under endoplasmic reticulum stress: promoting ubiquitination and degradation of C/EBP homologous protein (CHOP). J. Biol. Chem. 2012, 287:32236-32245.
48. Supale S., et al. Mitochondrial dysfunction in pancreatic β cells. Trends Endocrinol. Metab. 2012, 23:477-487.
49. Tang C., et al. Susceptibility to fatty acid-induced β-cell dysfunction is enhanced in prediabetic diabetes-prone biobreeding rats: a potential link between β-cell lipotoxicity and islet inflammation. Endocrinology 2013, 154:89-101.
50. Eizirik D.L., et al. Signalling danger: endoplasmic reticulum stress and the unfolded protein response in pancreatic islet inflammation. Diabetologia 2013, 56:234-241.
51. Cnop M., et al. Endoplasmic reticulum stress, obesity and diabetes. Trends Mol. Med. 2012, 18:59-68.
52. Franco R., et al. Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett. 2008, 266:6-11.
53. Quan X., et al. Reactive oxygen species downregulate catalase expression via methylation of a CpG island in the Oct-1 promoter. FEBS Lett. 2011, 585:3436-3441.
54. Bernal A.J., et al. Adaptive radiation-induced epigenetic alterations mitigated by antioxidants. FASEB J. 2013, 27:665-671.
55. Shock L.S., et al. DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3630-3635.
56. Minocherhomji S., et al. Mitochondrial regulation of epigenetics and its role in human diseases. Epigenetics 2012, 7:326-334.
57. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
58. Tahiliani M., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
59. Chia N., et al. Hypothesis: environmental regulation of 5-hydroxymethylcytosine by oxidative stress. Epigenetics 2011, 6:853-856.
60. Weir G.C., et al. Towards better understanding of the contributions of overwork and glucotoxicity to the beta-cell inadequacy of type 2 diabetes. Diabetes Obes. Metab. 2009, 11(Suppl 4):82-90.
61. Poitout V., Robertson R.P. Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr. Rev. 2008, 29:351-366.
62. Tang C., et al. Glucose-induced beta cell dysfunction in vivo in rats: link between oxidative stress and endoplasmic reticulum stress. Diabetologia 2012, 55:1366-1379.
63. Coughlan M.T., et al. Advanced glycation end products are direct modulators of β-cell function. Diabetes 2011, 60:2523-2532.
64. El-Osta A., et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J. Exp. Med. 2008, 205:2409-2417.
65. Brasacchio D., et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 2009, 58:1229-1236.
66. INK4a suppression by glucose restriction contributes to human cellular lifespan extension through SIRT1-mediated epigenetic and genetic mechanisms. PLoS ONE 2011, 6:e17421.
67. Houtkooper R.H., et al. Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 2012, 13:225-238.
68. Zheng Z., et al. Sirtuin 1-mediated cellular metabolic memory of high glucose via the LKB1/AMPK/ROS pathway and therapeutic effects of metformin. Diabetes 2012, 61:217-228.
69. Tang X., et al. Identification of glucose-regulated miRNAs from pancreatic β cells reveals a role for miR-30d in insulin transcription. RNA 2009, 15:287-293.
70. Esguerra J.L.S., et al. Differential glucose-regulation of microRNAs in pancreatic islets of non-obese type 2 diabetes model Goto-Kakizaki rat. PLoS ONE 2011, 6:e18613.
71. Goldfine A.B., Kulkarni R.N. Modulation of β-cell function: a translational journey from the bench to the bedside. Diabetes Obes. Metab. 2012, 14:152-160.
72. Mezza T., Kulkarni R. The regulation of pre- and post-maturational plasticity of mammalian islet cell mass. Diabetologia 2014, 57:1291-1303.
73. Maures T.J., et al. The H3K27 demethylase UTX-1 regulates C. elegans lifespan in a germline-independent, insulin-dependent manner. Aging Cell 2011, 10:980-990.
74. Wang Y., et al. Phosphorylation and recruitment of BAF60c in chromatin remodeling for lipogenesis in response to insulin. Mol. Cell 2013, 49:283-297.
75. Kabra D.G., et al. Insulin induced alteration in post-translational modifications of histone H3 under a hyperglycemic condition in L6 skeletal muscle myoblasts. Biochim. Biophys. Acta 2009, 1792:574-583.
76. Chen H., et al. PDGF signalling controls age-dependent proliferation in pancreatic beta-cells. Nature 2011, 478:349-355.
77. Park J.H., et al. 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.
78. Pinney S.E., et al. Exendin-4 increases histone acetylase activity and reverses epigenetic modifications that silence Pdx1 in the intrauterine growth retarded rat. Diabetologia 2011, 54:2606-2614.
79. El Ouaamari A., et al. Liver-derived systemic factors drive β cell hyperplasia in insulin-resistant states. Cell Rep. 2013, 3:401-410.
80. Yi P., et al. Betatrophin: a hormone that controls pancreatic β cell proliferation. Cell 2013, 153:747-758.
81. Lo J.C., et al. Adipsin is an adipokine that improves β cell function in diabetes. Cell 2014, 158:41-53.
82. Dumortier O., et al. Different mechanisms operating during different critical time-windows reduce rat fetal beta cell mass due to a maternal low-protein or low-energy diet. Diabetologia 2007, 50:2495-2503.
83. Theys N., et al. Early low protein diet aggravates unbalance between antioxidant enzymes leading to islet dysfunction. PLoS ONE 2009, 4:e6110.
84. 2 mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 2005, 122:337-349.
85. Sandovici I., et al. Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:5449-5454.
86. Jimenez-Chillaron J.C., et al. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009, 58:460-468.
87. Radford E.J., et al. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 2014, 345:1255903.
88. Martínez D., et al. In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered Lxra DNA methylation. Cell Metab. 2014, 19:941-951.
89. de Miguel-Santos L., et al. Maternal undernutrition increases pancreatic IGF-2 and partially suppresses the physiological wave of β-cell apoptosis during the neonatal period. J. Mol. Endocrinol. 2010, 44:25-36.
90. Xu Y-P., et al. The levels of Pdx1/insulin, Cacna1c and Cacna1d, and β-cell mass in a rat model of intrauterine undernutrition. J. Mater. Fetal Neonatal Med. 2011, 24:437-443.
91. Simmons R. Role of metabolic programming in the pathogenesis of β-cell failure in postnatal life. Rev. Endocr. Metab. Disord. 2007, 8:95-104.
92. Park I-H., et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008, 451:141-146.
93. Carone B.R., et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010, 143:1084-1096.
94. Ng S-F., et al. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 2010, 467:963-966.
95. Duque-Guimarães D.E., Ozanne S.E. Nutritional programming of insulin resistance: causes and consequences. Trends Endocrinol. Metab. 2013, 24:525-535.
96. Yi S. Birds do it, bees do it, worms and ciliates do it too: DNA methylation from unexpected corners of the tree of life. Genome Biol. 2012, 13:174.
97. Suzuki M.M., Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 2008, 9:465-476.
98. Mazzio E.A., Soliman K.F.A. Basic concepts of epigenetics: impact of environmental signals on gene expression. Epigenetics 2012, 7:119-130.
99. Bhutani N., et al. DNA demethylation dynamics. Cell 2011, 146:866-872.
100. Williams K., et al. DNA methylation: TET proteins - guardians of CpG islands?. EMBO Rep. 2012, 13:28-35.
101. Hackett J.A., et al. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 2013, 339:448-452.
102. Waki H., et al. The epigenome and its role in diabetes. Curr. Diab. Rep. 2012, 12:673-685.
103. Xu Y., et al. Histone H2A.Z. controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol. Cell 2012, 48:723-733.
104. Bramswig N.C., Kaestner K.H. Epigenetics and diabetes treatment: an unrealized promise?. Trends Endocrinol. Metab. 2012, 23:286-291.
105. Rando O.J. Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr. Opin. Genet. Dev. 2012, 22:148-155.
106. Verdone L., et al. Role of histone acetylation in the control of gene expression. Biochem. Cell Biol. 2005, 83:344-353.
107. Suganuma T., Workman J.L. Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 2011, 80:473-499.
108. Guo H., et al. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
109. Fukaya T., Tomari Y. MicroRNAs mediate gene silencing via multiple different pathways in Drosophila. Mol. Cell 2012, 48:825-836.
110. Fraga M.F., et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:10604-10609.
111. Heijmans B.T., et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:17046-17049.
112. Daxinger L., Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 2012, 13:153-162.