MicroRNA-7a regulates pancreatic β cell function

Journal of Clinical Investigation

Volumn 124, Issue 6, 2014, Pages 2722-2735

  Latreille, Mathieu ^a,b   Hausser, Jean ^c   Stützer, Ina ^a,b   Zhang, Quan ^d   Hastoy, Benoit ^d   Gargani, Sofia ^e   Kerr Conte, Julie ^e   Pattou, Francois ^e   Zavolan, Mihaela ^c   Esguerra, Jonathan L S ^f   Eliasson, Lena ^f   Rülicke, Thomas ^g   Rorsman, Patrik ^d   Stoffel, Markus ^a,b,h  

^a ETH ZURICH   (Switzerland)

^b Competence Center of Systems Physiology and Metabolic Disease ETH Zurich ^*  (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e France   (France)

^f LUND UNIVERSITY   (Sweden)

^g Institute of Laboratory Animal Science   (Austria)

^h UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BASP1 PROTEIN; CPLX1 PROTEIN; CSPA PROTEIN; GLUCOSE; INSULIN; MICRORNA; MICRORNA 7A; PFN2 PROTEIN; PKCB PROTEIN; SNARE PROTEIN; SNCA PROTEIN; SYNAPTOBREVIN 2; UNCLASSIFIED DRUG; WIPF2 PROTEIN; ZDHHC9 PROTEIN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEDIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELLULAR SECRETION; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; EXOCYTOSIS; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; HUMAN; HUMAN CELL; INSULIN RELEASE; INSULIN TOLERANCE TEST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PRIORITY JOURNAL;

ANIMALS; CELL DEDIFFERENTIATION; DIABETES MELLITUS; EXOCYTOSIS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; MICE, TRANSGENIC; MICRORNAS; OBESITY; SNARE PROTEINS;

EID: 84900797916     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI73066     Document Type: Article

References (63)

1. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature. 2006;444(7121):840-846.
2. Bonnefond A, Froguel P, Vaxillaire M. The emerging genetics of type 2 diabetes. Trends Mol Med. 2010;16(9):407-416.
3. Donath MY, et al. Mechanisms of β-cell death in type 2 diabetes. Diabetes. 2005;54(Suppl 2):S108-S113.
4. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC. Pancreatic β-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab. 2008;10(Suppl 4):32-42.
5. Porte D Jr, Kahn SE. β-Cell dysfunction and failure in type 2 diabetes: potential mechanisms. Diabetes. 2001;50(Suppl 1):S160-S163.
6. Rosengren AH, et al. Reduced insulin exocytosis in human pancreatic β-cells with gene variants linked to type 2 diabetes. Diabetes. 2012;61(7):1726-1733.
7. Landgraf P, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129(7):1401-1414.
8. Poy MN, et al. A pancreatic islet-specific micro-RNA regulates insulin secretion. Nature. 2004;432(7014):226-230.
9. Pullen TJ, da Silva Xavier G, Kelsey G, Rutter GA. miR-29a and miR-29b contribute to pancreatic β-cellspecific silencing of monocarboxylate transporter 1 (Mct1). Mol Cell Biol. 2011;31(15):3182-3194.
10. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell. 2012;148(6):1172-1187.
11. Dumortier O, Hinault C, Van Obberghen E. MicroRNAs and metabolism crosstalk in energy homeostasis. Cell Metab. 2013;18(3):312-324.
12. Lynn FC, et al. MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes. 2007;56(12):2938-2945.
13. Melkman-Zehavi T, et al. miRNAs control insulin content in pancreatic β-cells via downregulation of transcriptional repressors. EMBO J. 2011;30(5):835-845.
14. Mandelbaum AD, et al. Dysregulation of Dicer1 in β cells impairs islet architecture and glucose metabolism. Exp Diabetes Res. 2012;2012:470302.
15. Poy MN, et al. miR-375 maintains normal pancreatic α- and β-cell mass. Proc Natl Acad Sci U S A. 2009;106(14):5813-5818.
16. Joglekar MV, Joglekar VM, Hardikar AA. Expression of islet-specific microRNAs during human pancreatic development. Gene Expr Patterns. 2009;9(2):109-113.
17. Bravo-Egana V, et al. Quantitative differential expression analysis reveals miR-7 as major islet microRNA. Biochem Biophys Res Commun. 2008;366(4):922-926.
18. Kredo-Russo S, Ness A, Mandelbaum AD, Walker MD, Hornstein E. Regulation of pancreatic microRNA-7 expression. Exp Diabetes Res. 2012;2012:695214.
19. Tessmar-Raible K, et al. Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell. 2007;129(7):1389-1400.
20. Choudhury NR, et al. Tissue-specific control of brain-enriched miR-7 biogenesis. Genes Dev. 2013;27(1):24-38.
21. Wang Y, Vogel G, Yu Z, Richard S. The QKI-5 and QKI-6 RNA binding proteins regulate the expression of microRNA 7 in glial cells. Mol Cell Biol. 2013;33(6):1233-1243.
22. Memczak S, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495(7441):333-338.
23. Hansen TB, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495(7441):384-388.
24. Herrera PL. Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development. 2000;127(11):2317-2322.
25. Kanno T, Rorsman P, Göpel SO. Glucose-dependent regulation of rhythmic action potential firing in pancreatic β-cells by kATP-channel modulation. J Physiol. 2002;545(Pt 2):501-507.
26. Gopel S, Kanno T, Barg S, Galvanovskis J, Rorsman P. Voltage-gated and resting membrane currents recorded from B-cells in intact mouse pancreatic islets. J Physiol. 1999;521(pt 3):717-728.
27. Olofsson CS, et al. Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B-cells. Pflugers Arch. 2002;444(1-2):43-51.
28. Burre J, et al. α-Synuclein promotes SNARE-complex assembly in vivo and in vitro. Science. 2010;329(5999):1663-1667.
29. Wang YW, et al. Spontaneous type 2 diabetic rodent models. J Diabetes Res. 2013;2013:401723.
30. Guo S, et al. Inactivation of specific β cell transcription factors in type 2 diabetes. J Clin Invest. 2013;123(8):3305-3316.
31. Kredo-Russo S, et al. Pancreas-enriched miRNA refines endocrine cell differentiation. Development. 2012;139(16):3021-3031.
32. Gargani S, et al. Adaptive changes of human islets to an obesogenic environment in the mouse. Diabetologia. 2013;56(2):350-358.
33. Shibasaki T, et al. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A. 2007;104(49):19333-19338.
34. Barg S, et al. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron. 2002;33(2):287-299.
35. Wang Y, Liu J, Liu C, Naji A, Stoffers DA. Micro-RNA-7 regulates the mTOR pathway and proliferation in adult pancreatic β-cells. Diabetes. 2013;62(3):887-895.
36. Spillantini MG, Goedert M. The alpha-synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. Ann N Y Acad Sci. 2000;920:16-27.
37. Chandra S, Gallardo G, Fernandez-Chacon R, Schluter OM, Sudhof TC. α-Synuclein cooperates with CSPα in preventing neurodegeneration. Cell. 2005;123(3):383-396.
38. Steneberg P, et al. The type 2 diabetes-associated gene ide is required for insulin secretion and suppression of α-synuclein levels in β-cells. Diabetes. 2013;62(6):2004-2014.
39. Pinton P, et al. Dynamics of glucose-induced membrane recruitment of protein kinase C β II in living pancreatic islet β-cells. J Biol Chem. 2002;277(40):37702-37710.
40. Shu Y, Liu X, Yang Y, Takahashi M, Gillis KD. Phosphorylation of SNAP-25 at Ser187 mediates enhancement of exocytosis by a phorbol ester in INS-1 cells. J Neurosci. 2008;28(1):21-30.
41. Nili U, et al. Munc18-1 phosphorylation by protein kinase C potentiates vesicle pool replenishment in bovine chromaffin cells. Neuroscience. 2006;2(143):487-500.
42. Barclay JW, et al. Phosphorylation of Munc18 by protein kinase C regulates the kinetics of exocytosis. J Biol Chem. 2003;278(12):10538-10545.
43. Esguerra JL, Bolmeson C, Cilio CM, Eliasson L. Differential glucose-regulation of microRNAs in pancreatic islets of non-obese type 2 diabetes model Goto-Kakizaki rat. PLoS One. 2011;6(4):e18613.
44. Andrali SS, Sampley ML, Vanderford NL, Ozcan S. Glucose regulation of insulin gene expression in pancreatic β-cells. Biochem J. 2008;415(1):1-10.
45. Harmon JS, Stein R, Robertson RP. Oxidative stressmediated, post-translational loss of MafA protein as a contributing mechanism to loss of insulin gene expression in glucotoxic beta cells. J Biol Chem. 2005;280(12):11107-11113.
46. Harmon JS, et al. β-Cell-specific overexpression of glutathione peroxidase preserves intranuclear MafA and reverses diabetes in db/db mice. Endocrinology. 2009;150(11):4855-4862.
47. Sander M, et al. Genetic analysis reveals that PAX6 is required for normal transcription of pancreatic hormone genes and islet development. Genes Dev. 1997;11(13):1662-1673.
48. St-Onge L, Sosa-Pineda B, Chowdhury K, Mansouri A, Gruss P. Pax6 is required for differentiation of glucagon-producing α-cells in mouse pancreas. Nature. 1997;387(6631):406-409.
49. Xuan S, et al. Pancreas-specific deletion of mouse Gata4 and Gata6 causes pancreatic agenesis. J Clin Invest. 2012;122(10):3516-3528.
50. Carrasco M, Delgado I, Soria B, Martin F, Rojas A. GATA4 and GATA6 control mouse pancreas organogenesis. J Clin Invest. 2012;122(10):3504-3515.
51. Hart AW, Mella S, Mendrychowski J, van Heyningen V, Kleinjan DA. The developmental regulator Pax6 is essential for maintenance of islet cell function in the adult mouse pancreas. PLoS One. 2013;8(1):e54173.
52. Ketola I, et al. Transcription factor GATA-6 is expressed in the endocrine and GATA-4 in the exocrine pancreas. Mol Cell Endocrinol. 2004;226(1-2):51-57.
53. De Franco E, et al. GATA6 mutations cause a broad phenotypic spectrum of diabetes from pancreatic agenesis to adult-onset diabetes without exocrine insufficiency. Diabetes. 2013;62(3):993-997.
54. + ductal cells are multipotent progenitors throughout development but do not produce new endocrine cells in the normal or injured adult pancreas. Development. 2011;138(4):653-665.
55. Talchai C, Xuan S, Lin HV, Sussel L, Accili D. Pancreatic beta cell dedifferentiation as a mechanism of diabetic β cell failure. Cell. 2012;150(6):1223-1234.
56. Nagamatsu S, et al. Decreased expression of t-SNARE, syntaxin 1, and SNAP-25 in pancreatic β-cells is involved in impaired insulin secretion from diabetic GK rat islets: restoration of decreased t-SNARE proteins improves impaired insulin secretion. Diabetes. 1999;48(12):2367-2373.
57. Gaisano HY, Ostenson CG, Sheu L, Wheeler MB, Efendic S. Abnormal expression of pancreatic islet exocytotic soluble N-ethylmaleimide-sensitive factor attachment protein receptors in Goto-Kakizaki rats is partially restored by phlorizin treatment and accentuated by high glucose treatment. Endocrinology. 2002;143(11):4218-4226.
58. Ostenson CG, Gaisano H, Sheu L, Tibell A, Bartfai T. Impaired gene and protein expression of exocytotic soluble N-ethylmaleimide attachment protein receptor complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes. 2006;55(2):435-440.
59. Andersson SA, et al. Reduced insulin secretion correlates with decreased expression of exocytotic genes in pancreatic islets from patients with type 2 diabetes. Mol Cell Endocrinol. 2012;364(1-2):36-45.
60. Sudhof TC, Rizo J. Synaptic vesicle exocytosis. Cold Spring Harb Perspect Biol. 2011;3(12):a005637.
61. de Chevigny A, et al. miR-7a regulation of Pax6 controls spatial origin of forebrain dopaminergic neurons. Nat Neurosci. 2012;15(8):1120-1126.
62. Braun M, et al. Voltage-gated ion channels in human pancreatic β-cells: electrophysiological characterization and role in insulin secretion. Diabetes. 2008;57(6):1618-1628.
63. Barg S, et al. Fast exocytosis with few Ca (2+) channels in insulin-secreting mouse pancreatic B cells. Biophys J. 2001;81(6):3308-3323.