Could microRNAs contribute to the maintenance of β cell identity?

Trends in Endocrinology and Metabolism

Volumn 25, Issue 6, 2014, Pages 285-292

  Kaspi, Haggai ^a   Pasvolsky, Ronit ^a   Hornstein, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Cellular identity; Dedifferentiation; Diabetes; Endocrine pancreas; MiRNAs; cells

Indexed keywords

INSULIN; MICRORNA;

CELL FATE; CELL FUNCTION; DIABETES MELLITUS; GENE CONTROL; GENE SILENCING; GENETIC TRANSCRIPTION; INSULIN SYNTHESIS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REVIEW; CELL DIFFERENTIATION; GENETICS; HUMAN; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; PHYSIOLOGY;

CELL DIFFERENTIATION; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN-SECRETING CELLS; MICRORNAS;

EID: 84901835072     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2014.01.003     Document Type: Review

References (94)

1. Waddington C.H. Canalization of development and the inheritance of acquired characters. Nature 1942, 150:563-565.
2. Blau H.M., Baltimore D. Differentiation requires continuous regulation. J. Cell Biol. 1991, 112:781-783.
3. Alberti K.G., Zimmet P.Z. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet. Med. 1998, 15:539-553.
4. Dhawan S., et al. Pancreatic beta cell identity is maintained by DNA methylation-mediated repression of Arx. Dev. Cell 2011, 20:419-429.
5. Talchai C., et al. Pancreatic beta cell dedifferentiation as a mechanism of diabetic beta cell failure. Cell 2012, 150:1223-1234.
6. Guo S., et al. Inactivation of specific beta cell transcription factors in type 2 diabetes. J. Clin. Invest. 2013, 123:3305-3316.
7. Prentki M., Nolan C.J. Islet beta cell failure in type 2 diabetes. J. Clin. Invest. 2006, 116:1802-1812.
8. Tattikota S.G., Poy M.N. Re-dicing the pancreatic beta-cell: do microRNAs define cellular identity?. EMBO J. 2011, 30:797-799.
9. Akerman I., et al. Removing the brakes on cell identity. Dev. Cell 2011, 20:411-412.
10. van Arensbergen J., et al. Ring1b bookmarks genes in pancreatic embryonic progenitors for repression in adult beta cells. Genes Dev. 2013, 27:52-63.
11. Schaffer A.E., et al. Nkx6.1 controls a gene regulatory network required for establishing and maintaining pancreatic Beta cell identity. PLoS Genet. 2013, 9:e1003274.
12. Stanger B.Z., Hebrok M. Control of cell identity in pancreas development and regeneration. Gastroenterology 2013, 144:1170-1179.
13. Taylor B.L., et al. Nkx6.1 is essential for maintaining the functional state of pancreatic beta cells. Cell Rep. 2013, 4:1262-1275.
14. Kjorholt C., et al. Chronic hyperglycemia, independent of plasma lipid levels, is sufficient for the loss of beta-cell differentiation and secretory function in the db/db mouse model of diabetes. Diabetes 2005, 54:2755-2763.
15. van Arensbergen J., et al. Derepression of Polycomb targets during pancreatic organogenesis allows insulin-producing beta-cells to adopt a neural gene activity program. Genome Res. 2010, 20:722-732.
16. Szabat M., et al. Maintenance of beta-cell maturity and plasticity in the adult pancreas: developmental biology concepts in adult physiology. Diabetes 2012, 61:1365-1371.
17. Avrahami D., Kaestner K.H. Epigenetic regulation of pancreas development and function. Semin. Cell Dev. Biol. 2012, 23:693-700.
18. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
19. Hornstein E., Shomron N. Canalization of development by microRNAs. Nat. Genet. 2006, 38(Suppl.):S20-S24.
20. Hammond S.M. Dicing and slicing: the core machinery of the RNA interference pathway. FEBS Lett. 2005, 579:5822-5829.
21. Doyle M., et al. The double-stranded RNA binding domain of human Dicer functions as a nuclear localization signal. RNA 2013, 19:1238-1252.
22. Melkman-Zehavi T., et al. miRNAs control insulin content in pancreatic beta-cells via downregulation of transcriptional repressors. EMBO J. 2011, 30:835-845.
23. Lynn F.C., et al. MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 2007, 56:2938-2945.
24. Kanji M.S., et al. Dicer1 is required to repress neuronal fate during endocrine cell maturation. Diabetes 2013, 62:1602-1611.
25. Kalis M., et al. Beta-cell specific deletion of Dicer1 leads to defective insulin secretion and diabetes mellitus. PLoS ONE 2011, 6:e29166.
26. Jonsson J., et al. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 1994, 371:606-609.
27. Morita S., et al. Dicer is required for maintaining adult pancreas. PLoS ONE 2009, 4:e4212.
28. Krek A., et al. Combinatorial microRNA target predictions. Nat. Genet. 2005, 37:495-500.
29. Poy M.N., et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004, 432:226-230.
30. Poy M.N., et al. miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5813-5818.
31. Ventura A., et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008, 132:875-886.
32. Wystub K., et al. miR-1/133a clusters cooperatively specify the cardiomyogenic lineage by adjustment of myocardin levels during embryonic heart development. PLoS Genet. 2013, 9:e1003793.
33. Medeiros L.A., et al. Mir-290-295 deficiency in mice results in partially penetrant embryonic lethality and germ cell defects. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14163-14168.
34. Shibata M., et al. MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J. Neurosci. 2011, 31:3407-3422.
35. Kuhnert F., et al. Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development 2008, 135:3989-3993.
36. Wang S., et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev. Cell 2008, 15:261-271.
37. Pullen T.J., Rutter G.A. When less is more: the forbidden fruits of gene repression in the adult beta-cell. Diabetes Obes. Metab. 2013, 15:503-512.
38. Quintens R., et al. Why expression of some genes is disallowed in beta-cells. Biochem. Soc. Trans. 2008, 36:300-305.
39. Pullen T.J., et al. miR-29a and miR-29b contribute to pancreatic beta-cell-specific silencing of monocarboxylate transporter 1 (Mct1). Mol. Cell. Biol. 2011, 31:3182-3194.
40. Pullen T.J., et al. Identification of genes selectively disallowed in the pancreatic islet. Islets 2010, 2:89-95.
41. Thorrez L., et al. Tissue-specific disallowance of housekeeping genes: the other face of cell differentiation. Genome Res. 2011, 21:95-105.
42. Ishihara H., et al. Overexpression of monocarboxylate transporter and lactate dehydrogenase alters insulin secretory responses to pyruvate and lactate in beta cells. J. Clin. Invest. 1999, 104:1621-1629.
43. Sekine N., et al. Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic beta-cells. Potential role in nutrient sensing. J. Biol. Chem. 1994, 269:4895-4902.
44. Pullen T.J., et al. Overexpression of monocarboxylate transporter-1 (SLC16A1) in mouse pancreatic beta-cells leads to relative hyperinsulinism during exercise. Diabetes 2012, 61:1719-1725.
45. Hornstein E. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 2005, 438:671-674.
46. Farh K.K., et al. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 2005, 310:1817-1821.
47. Lim L.P., et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
48. Stark A., et al. Animal microRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 2005, 123:1133-1146.
49. Oetjen E., et al. Inhibition of MafA transcriptional activity and human insulin gene transcription by interleukin-1beta and mitogen-activated protein kinase kinase kinase in pancreatic islet beta cells. Diabetologia 2007, 50:1678-1687.
50. Zhao X., et al. MicroRNA-30d induces insulin transcription factor MafA and insulin production by targeting mitogen-activated protein 4 kinase 4 (MAP4K4) in pancreatic beta-cells. J. Biol. Chem. 2012, 287:31155-31164.
51. 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.
52. Nieto M., et al. Antisense miR-7 impairs insulin expression in developing pancreas and in cultured pancreatic buds. Cell Transplant. 2012, 21:1761-1774.
53. Roggli E., et al. Involvement of microRNAs in the cytotoxic effects exerted by proinflammatory cytokines on pancreatic beta-cells. Diabetes 2010, 59:978-986.
54. Ruan Q., et al. The microRNA-21-PDCD4 axis prevents type 1 diabetes by blocking pancreatic beta cell death. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12030-12035.
55. Kameswaran V., et al. Epigenetic regulation of the DLK1-MEG3 microRNA cluster in human type 2 diabetic islets. Cell Metab. 2014, 19:135-145.
56. Arntfield M.E., van der Kooy D. Beta-cell evolution: how the pancreas borrowed from the brain: The shared toolbox of genes expressed by neural and pancreatic endocrine cells may reflect their evolutionary relationship. Bioessays 2011, 33:582-587.
57. Collombat P., et al. Embryonic endocrine pancreas and mature beta cells acquire alpha and PP cell phenotypes upon Arx misexpression. J. Clin. Invest. 2007, 117:961-970.
58. Thorel F., et al. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 2010, 464:1149-1154.
59. Yang Y.P., et al. Context-specific alpha- to-beta-cell reprogramming by forced Pdx1 expression. Genes Dev. 2011, 25:1680-1685.
60. Collombat P., et al. The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 2009, 138:449-462.
61. Spijker H.S., et al. Conversion of mature human beta-cells into glucagon-producing alpha-cells. Diabetes 2013, 62:2471-2480.
62. 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.
63. Collombat P., et al. Opposing actions of Arx and Pax4 in endocrine pancreas development. Genes Dev. 2003, 17:2591-2603.
64. Klein D., et al. MicroRNA expression in alpha and beta cells of human pancreatic islets. PLoS ONE 2013, 8:e55064.
65. Fred R.G., et al. High glucose suppresses human islet insulin biosynthesis by inducing miR-133a leading to decreased polypyrimidine tract binding protein-expression. PLoS ONE 2010, 5:e10843.
66. Setyowati Karolina D., et al. miR-25 and miR-92a regulate insulin I biosynthesis in rats. RNA Biol. 2013, 10:1365-1378.
67. Kim J.W., et al. miRNA-30a-5p-mediated silencing of Beta2/NeuroD expression is an important initial event of glucotoxicity-induced beta cell dysfunction in rodent models. Diabetologia 2013, 56:847-855.
68. Xu G., et al. Thioredoxin-interacting protein regulates insulin transcription through microRNA-204. Nat. Med. 2013, 19:1141-1146.
69. Zhang Z.W., et al. MicroRNA-19b downregulates insulin 1 through targeting transcription factor NeuroD1. FEBS Lett. 2011, 585:2592-2598.
70. Li X. MiR-375, a microRNA related to diabetes. Gene 2013, 533:1-4.
71. Tattikota S.G., et al. Argonaute2 mediates compensatory expansion of the pancreatic beta cell. Cell Metab. 2014, 19:122-134.
72. Morita S., et al. MiR-184 regulates insulin secretion through repression of Slc25a22. PeerJ 2013, 1:e162.
73. Guay C., et al. Emerging roles of non-coding RNAs in pancreatic beta-cell function and dysfunction. Diabetes Obes. Metab. 2012, 14(Suppl. 3):12-21.
74. Miska E.A., et al. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet. 2007, 3:e215.
75. Alvarez-Saavedra E., Horvitz H.R. Many families of C. elegans microRNAs are not essential for development or viability. Curr. Biol. 2010, 20:367-373.
76. Kent O.A., Mendell J.T. A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene 2006, 25:6188-6196.
77. Kredo-Russo S., et al. Pancreas-enriched miRNA refines endocrine cell differentiation. Development 2012, 139:3021-3031.
78. Mukherji S., et al. MicroRNAs can generate thresholds in target gene expression. Nat. Genet. 2011, 43:854-859.
79. Park C.Y., et al. Analysis of microRNA knockouts in mice. Hum. Mol. Genet. 2010, 19:R169-R175.
80. Mendell J.T., Olson E.N. MicroRNAs in stress signaling and human disease. Cell 2012, 148:1172-1187.
81. Esteller M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011, 12:861-874.
82. Cordes K.R., et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009, 460:705-710.
83. Yoo A.S., et al. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 2011, 476:228-231.
84. Anokye-Danso F., et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011, 8:376-388.
85. Subramanyam D., et al. Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat. Biotechnol. 2011, 29:443-448.
86. Nimmo R., et al. MiR-142-3p controls the specification of definitive hemangioblasts during ontogeny. Dev. Cell 2013, 26:237-249.
87. Cheng L.C., et al. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 2009, 12:399-408.
88. Sanuki R., et al. miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat. Neurosci. 2011, 14:1125-1134.
89. Zhao Y., et al. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 2007, 129:303-317.
90. Boettger T., et al. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J. Clin. Invest. 2009, 119:2634-2647.
91. Elia L., et al. The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ. 2009, 16:1590-1598.
92. Rasmussen K.D., et al. The miR-144/451 locus is required for erythroid homeostasis. J. Exp. Med. 2010, 207:1351-1358.
93. Yu D., et al. miR-451 protects against erythroid oxidant stress by repressing 14-3-3zeta. Genes Dev. 2010, 24:1620-1633.
94. Lu L.F., et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 2010, 142:914-929.