Implication of epigenetics in pancreas development and disease

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 29, Issue 6, 2015, Pages 883-898

  Quilichini, Evans ^a,b   Haumaitre, Cécile ^a,b,c,d  

^a CNRS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSERM   (France)

^d Sorbonne Universités   (France)

Author keywords

diabetes; DNA methylation; epigenetics; histone modifications; non coding RNAs; pancreas development; pancreatic cancer; stem cell differentiation; cells

Indexed keywords

MICRORNA; UNTRANSLATED RNA;

ACINAR CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL REGENERATION; DEACETYLATION; DNA METHYLATION; EMBRYONIC STEM CELL; ENDOCRINE CELL; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; EXOCRINE CELL; EXOCRINE SECRETION; GENE EXPRESSION; GENETIC ASSOCIATION; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; INSULIN RELEASE; INTRADUCTAL PAPILLARY MUCINOUS TUMOR; MESODERM; MULTIPOTENT STEM CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEAR REPROGRAMMING; ORGANOGENESIS; PANCREAS ADENOCARCINOMA; PANCREAS ADENOMA; PANCREAS CELL; PANCREAS DEVELOPMENT; PANCREAS DISEASE; PANCREAS ISLET BETA CELL; REVIEW; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC CELL; ANIMAL; CYTOLOGY; DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PANCREAS; PANCREAS TUMOR;

ANIMALS; CELL DIFFERENTIATION; DIABETES MELLITUS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; PANCREAS; PANCREATIC NEOPLASMS;

EID: 84970938058     PISSN: 1521690X     EISSN: 15321908     Source Type: Journal    
DOI: 10.1016/j.beem.2015.10.010     Document Type: Review

References (99)

1. F.C. Pan, and C. Wright Pancreas organogenesis: from bud to plexus to gland Dev Dyn 240 2011 530 565
2. Z.D. Smith, and A. Meissner DNA methylation: roles in mammalian development Nat Rev Genet 14 2013 204 220
3. B. Schuettengruber, D. Chourrout, M. Vervoort, and et al. Genome regulation by polycomb and trithorax proteins Cell 128 2007 735 745
4. G.P. Delcuve, D.H. Khan, and J.R. Davie Roles of histone deacetylases in epigenetic regulation: emerging paradigms from studies with inhibitors Clin Epigenetics 4 2012 5
5. D. Holoch, and D. Moazed RNA-mediated epigenetic regulation of gene expression Nat Rev Genet 16 2015 71 84
6. M. Oda, Y. Kumaki, M. Shigeta, and et al. DNA methylation restricts lineage-specific functions of transcription factor Gata4 during embryonic stem cell differentiation PLoS Genet 9 2013 e1003574
7. T.S. Mikkelsen, M. Ku, D.B. Jaffe, and et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells Nature 448 2007 553 560
8. A.E.R. Kartikasari, J.X. Zhou, M.S. Kanji, and et al. The histone demethylase Jmjd3 sequentially associates with the transcription factors Tbx3 and Eomes to drive endoderm differentiation EMBO J 32 2013 1393 1408
9. W. Jiang, J. Wang, and Y. Zhang Histone H3K27me3 demethylases KDM6A and KDM6B modulate definitive endoderm differentiation from human ESCs by regulating WNT signaling pathway Cell Res 23 2013 122 130
10. C.-R. Xu, P.A. Cole, D.J. Meyers, and et al. Chromatin "prepattern" and histone modifiers in a fate choice for liver and pancreas Science 332 2011 963 966
11. E.S. Noël, A. Casal-Sueiro, E. Busch-Nentwich, and et al. Organ-specific requirements for Hdac1 in liver and pancreas formation Dev Biol 322 2008 237 250
12. S. Georgia, M. Kanji, and A. Bhushan DNMT1 represses p53 to maintain progenitor cell survival during pancreatic organogenesis Genes Dev 27 2013 372 377
13. G. Von Figura, A. Fukuda, N. Roy, and et al. The chromatin regulator Brg1 suppresses formation of intraductal papillary mucinous neoplasm and pancreatic ductal adenocarcinoma Nat Cell Biol 16 2014 255 267
14. B. McKenna, M. Guo, A. Reynolds, and et al. Dynamic recruitment of functionally distinct Swi/Snf chromatin remodeling complexes modulates Pdx1 activity in islet β cells Cell Rep 10 2015 2032 2042
15. F.C. Lynn, P. Skewes-Cox, Y. Kosaka, and et al. MicroRNA expression is required for pancreatic islet cell genesis in the mouse Diabetes 56 2007 2938 2945
16. K. Rai, L.D. Nadauld, S. Chidester, and et al. Zebra fish Dnmt1 and Suv39h1 regulate organ-specific terminal differentiation during development Mol Cell Biol 26 2006 7077 7085
17. R.M. Anderson, J.A. Bosch, M.G. Goll, and et al. Loss of Dnmt1 catalytic activity reveals multiple roles for DNA methylation during pancreas development and regeneration Dev Biol 334 2009 213 223
18. C. Haumaitre, O. Lenoir, and R. Scharfmann Histone deacetylase inhibitors modify pancreatic cell fate determination and amplify endocrine progenitors Mol Cell Biol 28 2008 6373 6383
19. W. Zhou, I.-C. Liang, and N.S. Yee Histone deacetylase 1 is required for exocrine pancreatic epithelial proliferation in development and cancer Cancer Biol Ther 11 2011 659 670
20. P.-P. Prévot, C. Augereau, A. Simion, and et al. Let-7b and miR-495 stimulate differentiation and prevent metaplasia of pancreatic acinar cells by repressing HNF6 Gastroenterology 145 2013 668-78.e3
21. Y. Yang, L. Ding, Y. An, and et al. MiR-18a regulates expression of the pancreatic transcription factor Ptf1a in pancreatic progenitor and acinar cells FEBS Lett 586 2012 422 427
22. C.-R. Xu, L.-C. Li, G. Donahue, and et al. Dynamics of genomic H3K27me3 domains and role of EZH2 during pancreatic endocrine specification EMBO J 33 2014 2157 2170
23. J. Van Arensbergen, J. García-Hurtado, M.A. Maestro, and et al. Ring1b bookmarks genes in pancreatic embryonic progenitors for repression in adult β cells Genes Dev 27 2013 52 63
24. C. Haumaitre, O. Lenoir, and R. Scharfmann Directing cell differentiation with small-molecule histone deacetylase inhibitors: the example of promoting pancreatic endocrine cells Cell Cycle 8 2009 536 544
25. O. Lenoir, K. Flosseau, F.X. Ma, and et al. Specific control of pancreatic endocrine β- and δ-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9 Diabetes 60 2011 2861 2871
26. J.B. Papizan, R.A. Singer, S.-I. Tschen, and et al. Nkx2.2 repressor complex regulates islet β-cell specification and prevents β-to-α-cell reprogramming Genes Dev 25 2011 2291 2305
27. M.S. Kanji, M.G. Martin, and A. Bhushan Dicer1 is required to repress neuronal fate during endocrine cell maturation Diabetes 62 2013 1602 1611
28. W.P. Kloosterman, A.K. Lagendijk, R.F. Ketting, and et al. Targeted inhibition of miRNA maturation with Morpholinos reveals a role for miR-375 in pancreatic islet development PLoS Biol 5 2007
29. S. Kredo-Russo, A.D. Mandelbaum, A. Ness, and et al. Pancreas-enriched miRNA refines endocrine cell differentiation Development 139 2012 3021 3031
30. X. Fu, L. Jin, X. Wang, and et al. MicroRNA-26a targets ten eleven translocation enzymes and is regulated during pancreatic cell differentiation Proc Natl Acad Sci U S A 110 2013 17892 17897
31. I. Morán, ̄. Akerman, M. van de Bunt, and et al. Human β cell transcriptome analysis uncovers lncRNAs that are tissue-specific, dynamically regulated, and abnormally expressed in type 2 diabetes Cell Metab 16 2012 435 448
32. G.M. Ku, H. Kim, I.W. Vaughn, and et al. Research resource: RNA-Seq reveals unique features of the pancreatic β-cell transcriptome Mol Endocrinol 26 2012 1783 1792
33. C. Martínez-Romero, I. Rooman, A. Skoudy, and et al. The epigenetic regulators Bmi1 and Ring1B are differentially regulated in pancreatitis and pancreatic ductal adenocarcinoma J Pathol 219 2009 205 213
34. J.M.-S. Clair, R. Soydaner-Azeloglu, K.E. Lee, and et al. EZH2 couples pancreatic regeneration to neoplastic progression Genes Dev 26 2012 439 444
35. N.C. Bramswig, L.J. Everett, J. Schug, and et al. Epigenomic plasticity enables human pancreatic α to β cell reprogramming J Clin Invest 123 2013 1275 1284
36. S. Dhawan, S. Georgia, S. Tschen, and et al. Pancreatic beta cell identity is maintained by DNA methylation-mediated repression of Arx Dev Cell 20 2011 419 429
37. A.L. Mosley, and S. Ozcan Glucose regulates insulin gene transcription by hyperacetylation of histone h4 J Biol Chem 278 2003 19660 19666
38. H.-W. Wang, M.B. Breslin, and M.S. Lan Pdx-1 modulates histone H4 acetylation and insulin gene expression in terminally differentiated alpha-TC-1 cells Pancreas 34 2007 248 253
39. A.L. Mosley, and S. Ozcan The pancreatic duodenal homeobox-1 protein (Pdx-1) interacts with histone deacetylases Hdac-1 and Hdac-2 on low levels of glucose J Biol Chem 279 2004 54241 54247
40. T.G. Deering, T. Ogihara, A.P. Trace, and et al. Methyltransferase Set7/9 maintains transcription and euchromatin structure at islet-enriched genes Diabetes 58 2009 185 193
41. C. Evans-Molina, R.D. Robbins, T. Kono, and et al. Peroxisome proliferator-activated receptor gamma activation restores islet function in diabetic mice through reduction of endoplasmic reticulum stress and maintenance of euchromatin structure Mol Cell Biol 29 2009 2053 2067
42. R.A. Singer, L. Arnes, and L. Sussel Noncoding RNAs in β cell biology Curr Opin Endocrinol Diabetes Obes 22 2015 77 85
43. M. Kalis, C. Bolmeson, J.L.S. Esguerra, and et al. Beta-cell specific deletion of Dicer1 leads to defective insulin secretion and diabetes mellitus PLoS One 6 2011 e29166
44. D. Klein, R. Misawa, V. Bravo-Egana, and et al. MicroRNA expression in alpha and beta cells of human pancreatic islets PLoS One 8 2013 e55064
45. M.N. Poy, J. Hausser, M. Trajkovski, and et al. miR-375 maintains normal pancreatic alpha- and beta-cell mass Proc Natl Acad Sci U S A 106 2009 5813 5818
46. T. Melkman-Zehavi, R. Oren, S. Kredo-Russo, and et al. miRNAs control insulin content in pancreatic β-cells via downregulation of transcriptional repressors EMBO J 30 2011 835 845
47. T.J. Pullen, and G.A. Rutter Roles of lncRNAs in pancreatic beta cell identity and diabetes susceptibility Front Genet 5 2014 193
48. S.K. Karnik, H. Chen, G.W. McLean, and et al. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus Science 318 2007 806 809
49. H. Chen, X. Gu, I-Hsi Su, and et al. Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus Genes Dev 23 2009 975 985
50. S. Dhawan, S.-I. Tschen, and A. Bhushan Bmi-1 regulates the Ink4a/Arf locus to control pancreatic β-cell proliferation Genes Dev 23 2009 906 911
51. J.X. Zhou, S. Dhawan, H. Fu, and et al. Combined modulation of polycomb and trithorax genes rejuvenates β cell replication J Clin Invest 123 2013 4849 4858
52. J.V. Schiesser, and J.M. Wells Generation of β cells from human pluripotent stem cells: are we there yet? Ann N Y Acad Sci 1311 2014 124 137
53. F.W. Pagliuca, J.R. Millman, M. Gürtler, and et al. Generation of functional human pancreatic β cells in vitro Cell 159 2014 428 439
54. A. Rezania, J.E. Bruin, P. Arora, and et al. Reversal of diabetes with insulin-producing cells derived in vitro from human pluripotent stem cells Nat Biotech 32 2014 1121 1133
55. R. Xie, L.J. Everett, H.-W. Lim, and et al. Dynamic chromatin remodeling mediated by polycomb proteins orchestrates pancreatic differentiation of human embryonic stem cells Cell Stem Cell 12 2013 224 237
56. G.E. Zentner, P.J. Tesar, and P.C. Scacheri Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions Genome Res 21 2011 1273 1283
57. C.-T. Ong, and V.G. Corces Enhancers: emerging roles in cell fate specification EMBO Rep 13 2012 423 430
58. B. Papp, and K. Plath Epigenetics of reprogramming to induced pluripotency Cell 152 2013 1324 1343
59. A. Wang, F. Yue, Y. Li, and et al. Epigenetic priming of enhancers predicts developmental competence of hESC-derived endodermal lineage intermediates Cell Stem Cell 16 2015 386 399
60. G. Pennarossa, S. Maffei, M. Campagnol, and et al. Brief demethylation step allows the conversion of adult human skin fibroblasts into insulin-secreting cells Proc Natl Acad Sci U S A 110 2013 8948 8953
61. L.S. Katz, E. Geras-Raaka, and M.C. Gershengorn Reprogramming adult human dermal fibroblasts to islet-like cells by epigenetic modification coupled to transcription factor modulation Stem Cells Dev 22 2013 2551 2560
62. B. Johannesson, I. Sagi, A. Gore, and et al. Comparable frequencies of coding mutations and loss of imprinting in human pluripotent cells derived by nuclear transfer and defined factors Cell Stem Cell 15 2014 634 642
63. 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, and et al. Genome-wide trans-ancestry meta-analysis provides insight into the genetic architecture of type 2 diabetes susceptibility Nat Genet 46 2014 234 244
64. J.H. Park, D.A. Stoffers, R.D. Nicholls, and et al. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1 J Clin Invest 118 2008 2316 2324
65. I. Sandovici, N.H. Smith, M.D. Nitert, and 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 108 2011 5449 5454
66. I. Prokopenko, W. Poon, R. Mägi, and et al. A central role for GRB10 in regulation of islet function in man PLoS Genet 10 2014 e1004235
67. B.T. Yang, T.A. Dayeh, P.A. Volkov, and et al. Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes Mol Endocrinol 26 2012 1203 1212
68. C. Ling, S. Del Guerra, R. Lupi, and et al. Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion Diabetologia 51 2008 615 622
69. M. Volkmar, S. Dedeurwaerder, D.A. Cunha, and et al. DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients EMBO J 31 2012 1405 1426
70. T. Dayeh, P. Volkov, S. Salö, and 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 10 2014
71. T.A. Dayeh, A.H. Olsson, P. Volkov, and et al. Identification of CpG-SNPs associated with type 2 diabetes and differential DNA methylation in human pancreatic islets Diabetologia 56 2013 1036 1046
72. L. Pasquali, K.J. Gaulton, S.A. Rodríguez-Seguí, and et al. Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants Nat Genet 46 2014 136 143
73. R. Bhandare, J. Schug, J. Le Lay, and et al. Genome-wide analysis of histone modifications in human pancreatic islets Genome Res 20 2010 428 433
74. M.L. Stitzel, P. Sethupathy, D.S. Pearson, and et al. Global epigenomic analysis of primary human pancreatic islets provides insights into type 2 diabetes susceptibility loci Cell Metab 12 2010 443 455
75. J. Van Arensbergen, J. García-Hurtado, I. Moran, and et al. Derepression of polycomb targets during pancreatic organogenesis allows insulin-producing beta-cells to adopt a neural gene activity program Genome Res 20 2010 722 732
76. V. Kameswaran, N.C. Bramswig, L.B. McKenna, and et al. Epigenetic regulation of the DLK1-MEG3 microRNA cluster in human type 2 diabetic islets Cell Metab 19 2014 135 145
77. M. Latreille, J. Hausser, I. Stützer, and et al. MicroRNA-7a regulates pancreatic β cell function J Clin Invest 124 2014 2722 2735
78. X. Zhao, R. Mohan, S. Özcan, and et al. MicroRNA-30d induces insulin transcription factor MafA and insulin production by targeting mitogen-activated protein 4 kinase 4 (MAP4K4) in pancreatic β-cells J Biol Chem 287 2012 31155 31164
79. L. Bao, X. Fu, M. Si, and et al. MicroRNA-185 targets SOCS3 to inhibit beta-cell dysfunction in diabetes PLoS One 10 2015 e0116067
80. S. Erener, M. Mojibian, J.K. Fox, and et al. Circulating miR-375 as a biomarker of β-cell death and diabetes in mice Endocrinology 154 2013 603 608
81. C. Higuchi, A. Nakatsuka, J. Eguchi, and et al. Identification of circulating miR-101, miR-375 and miR-802 as biomarkers for type 2 diabetes Metab Clin Exp 64 2015 489 497
82. V. Kameswaran, and K.H. Kaestner The missing lnc(RNA) between the pancreatic β-cell and diabetes Front Genet 5 2014 200
83. C. Guerra, and M. Barbacid Genetically engineered mouse models of pancreatic adenocarcinoma Mol Oncol 7 2013 232 247
84. M. Guo, Y. Jia, Z. Yu, and et al. Epigenetic changes associated with neoplasms of the exocrine and endocrine pancreas Discov Med 17 2014 67 73
85. K. Nones, N. Waddell, S. Song, and et al. Genome-wide DNA methylation patterns in pancreatic ductal adenocarcinoma reveal epigenetic deregulation of SLIT-ROBO, ITGA2 and MET signaling Int J Cancer 135 2014 1110 1118
86. A. Vincent, S.-M. Hong, C. Hu, and et al. Epigenetic silencing of EYA2 in pancreatic adenocarcinomas promotes tumor growth Oncotarget 5 2014 2575 2587
87. C. Dutruel, F. Bergmann, I. Rooman, and et al. Early epigenetic downregulation of WNK2 kinase during pancreatic ductal adenocarcinoma development Oncogene 33 2014 3401 3410
88. W. Gao, Y. Gu, Z. Li, and et al. miR-615-5p is epigenetically inactivated and functions as a tumor suppressor in pancreatic ductal adenocarcinoma Oncogene 34 2015 1629 1640
89. Y. Jiao, C. Shi, B.H. Edil, and et al. DAXX/ATRX, MEN1 and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors Science 331 2011 1199 1203
90. W. Wang, J. Gao, X.-H. Man, and et al. Significance of DNA methyltransferase-1 and histone deacetylase-1 in pancreatic cancer Oncol Rep 21 2009 1439 1447
91. K.B. Grandinetti, P. Jelinic, T. DiMauro, and et al. Sin3B expression is required for cellular senescence and is up-regulated upon oncogenic stress Cancer Res 69 2009 6430 6437
92. M. Rielland, D.J. Cantor, R. Graveline, and et al. Senescence-associated SIN3B promotes inflammation and pancreatic cancer progression J Clin Invest 124 2014 2125 2135
93. T. DiMauro, D.J. Cantor, A.J. Bainor, and et al. Transcriptional repression of Sin3B by Bmi-1 prevents cellular senescence and is relieved by oncogene activation Oncogene 34 2015 4011 4017
94. J. Xu, W. Zhu, W. Xu, and et al. Up-regulation of MBD1 promotes pancreatic cancer cell epithelial-mesenchymal transition and invasion by epigenetic down-regulation of E-cadherin Curr Mol Med 13 2013 387 400
95. S. Chen, J. Chen, Q. Zhan, and et al. H2AK119Ub1 and H3K27Me3 in molecular staging for survival prediction of patients with pancreatic ductal adenocarcinoma Oncotarget 5 2014 10421 10433
96. J. Jia, H. Parikh, W. Xiao, and et al. An integrated transcriptome and epigenome analysis identifies a novel candidate gene for pancreatic cancer BMC Med Genomics 6 2013 33
97. J.Y. Park, J. Helm, D. Coppola, and et al. MicroRNAs in pancreatic ductal adenocarcinoma World J Gastroenterol 17 2011 817 827
98. S. Caponi, N. Funel, A.E. Frampton, and et al. The good, the bad and the ugly: a tale of miR-101, miR-21 and miR-155 in pancreatic intraductal papillary mucinous neoplasms Ann Oncol 24 2013 734 741
99. O. Nakahara, H. Takamori, M. Iwatsuki, and et al. Carcinogenesis of intraductal papillary mucinous neoplasm of the pancreas: loss of microRNA-101 promotes overexpression of histone methyltransferase EZH2 Ann Surg Oncol 19 Suppl. 3 2012 S565 S571