Transcriptional regulation of the miR-212/miR-132 cluster in insulin-secreting β-cells by cAMP-regulated transcriptional co-activator 1 and salt-inducible kinases

Molecular and Cellular Endocrinology

Volumn 424, Issue , 2016, Pages 23-33

  Malm, Helena Anna ^a   Mollet, Inês G ^a   Berggreen, Christine ^b   Orho Melander, Marju ^a   Esguerra, Jonathan Lou S ^a   Göransson, Olga ^b   Eliasson, Lena ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Beta cell; CAMP; Diabetes; Insulin secretion; MicroRNA; Transcription

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; CYCLIC AMP REGULATED TRANSCRIPTIONAL CO ACTIVATOR 1; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MICRORNA; MICRORNA 132; MICRORNA 212; PHOSPHOTRANSFERASE; REGULATOR PROTEIN; SALT INDUCIBLE KINASE; UNCLASSIFIED DRUG; CRTC1 PROTEIN, RAT; GLUCOSE; MIRN132 MICRORNA, RAT; MIRN212 MICRORNA, RAT; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; INSULIN RELEASE; MALE; MIDDLE AGED; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PANCREAS ISLET BETA CELL; PHOSPHORYLATION; WISTAR RAT;

ANIMALS; CELL LINE; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; INSULIN-SECRETING CELLS; MALE; MICRORNAS; MIDDLE AGED; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, WISTAR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84959238487     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2016.01.010     Document Type: Article

References (57)

1. Altarejos J.Y., Montminy M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat. Rev. Mol. Cell Biol. 2011, 12:141-151.
2. Altarejos J.Y., Goebel N., Conkright M.D., Inoue H., Xie J., Arias C.M., Sawchenko P.E., Montminy M. The Creb1 coactivator Crtc1 is required for energy balance and fertility. Nat. Med. 2008, 14:1112-1117.
3. Ammala C., Ashcroft F.M., Rorsman P. Calcium-independent potentiation of insulin release by cyclic AMP in single beta-cells. Nature 1993, 363:356-358.
4. Andersson S.A., Olsson A.H., Esguerra J.L., Heimann E., Ladenvall C., Edlund A., Salehi A., Taneera J., Degerman E., Groop L., Ling C., Eliasson L. Reduced insulin secretion correlates with decreased expression of exocytotic genes in pancreatic islets from patients with type 2 diabetes. Mol. Cell. Endocrinol. 2012, 364:36-45.
5. Berggreen C., Gormand A., Omar B., Degerman E., Goransson O. Protein kinase B activity is required for the effects of insulin on lipid metabolism in adipocytes. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E635-E646.
6. Berggreen C., Henriksson E., Jones H.A., Morrice N., Goransson O. cAMP-elevation mediated by beta-adrenergic stimulation inhibits salt-inducible kinase (SIK) 3 activity in adipocytes. Cell. Signal. 2012, 24:1863-1871.
7. Blanchet E., Van de Velde S., Matsumura S., Hao E., LeLay J., Kaestner K., Montminy M. Feedback inhibition of CREB signaling promotes beta cell dysfunction in insulin resistance. Cell Rep. 2015, 10:1149-1157.
8. Ch'ng T.H., Uzgil B., Lin P., Avliyakulov N.K., O'Dell T.J., Martin K.C. Activity-dependent transport of the transcriptional coactivator CRTC1 from synapse to nucleus. Cell 2012, 150:207-221.
9. Clark K., MacKenzie K.F., Petkevicius K., Kristariyanto Y., Zhang J., Choi H.G., Peggie M., Plater L., Pedrioli P.G., McIver E., Gray N.S., Arthur J.S., Cohen P. Phosphorylation of CRTC3 by the salt-inducible kinases controls the interconversion of classically activated and regulatory macrophages. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:16986-16991.
10. Conkright M.D., Canettieri G., Screaton R., Guzman E., Miraglia L., Hogenesch J.B., Montminy M. TORCs: transducers of regulated CREB activity. Mol. Cell 2003, 12:413-423.
11. Deacon C.F., Carr R.D., Holst J.J. DPP-4 inhibitor therapy: new directions in the treatment of type 2 diabetes. Front. Biosci. 2008, 13:1780-1794.
12. Eberhard C.E., Fu A., Reeks C., Screaton R.A. CRTC2 is required for beta-cell function and proliferation. Endocrinology 2013, 154:2308-2317.
13. Edlund A., Esguerra J.L., Wendt A., Flodström-Tullberg M., Eliasson L. CFTR and anoctamin 1 (ANO1) contribute to cAMP amplified exocytosis and insulin secretion in human and murine pancreatic beta-cells. BMC Med. 2014, 12.
14. El Ouaamari A., Baroukh N., Martens G.A., Lebrun P., Pipeleers D., van Obberghen E. miR-375 targets 3'-phosphoinositide-dependent protein kinase-1 and regulates glucose-induced biological responses in pancreatic beta-cells. Diabetes 2008, 57:2708-2717.
15. Eliasson L., Esguerra J.L. Role of non-coding RNAs in pancreatic beta-cell development and physiology. Acta Physiol. (Oxf.) 2014, 211:273-284.
16. Eliasson L., Ma X.S., Renstrom E., Barg S., Berggren P.O., Galvanovskis J., Gromada J., Jing X.J., Lundquist I., Salehi A., Sewing S., Rorsman P. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J. General Physiol. 2003, 121:181-197.
17. Esguerra J.L., Bolmeson C., Cilio C.M., Eliasson L. Differential glucose-regulation of microRNAs in pancreatic islets of non-obese type 2 diabetes model Goto-Kakizaki rat. PLoS One 2011, 6:e18613.
18. Esguerra J.L., Mollet I.G., Salunkhe V.A., Wendt A., Eliasson L. Regulation of pancreatic beta cell stimulus-secretion coupling by microRNAs. Genes (Basel) 2014, 5:1018-1031.
19. Fadista J., Vikman P., Laakso E.O., Mollet I.G., Esguerra J.L., Taneera J., Storm P., Osmark P., Ladenvall C., Prasad R.B., Hansson K.B., Finotello F., Uvebrant K., Ofori J.K., Di Camillo B., Krus U., et al. Global genomic and transcriptomic analysis of human pancreatic islets reveals novel genes influencing glucose metabolism. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:13924-13929.
20. Fred R.G., Bang-Berthelsen C.H., Mandrup-Poulsen T., Grunnet L.G., Welsh N. High glucose suppresses human islet insulin biosynthesis by inducing miR-133a leading to decreased polypyrimidine tract binding protein-expression. PLoS One 2010, 5:e10843.
21. Guay C., Regazzi R. Role of islet microRNAs in diabetes: which model for which question?. Diabetologia 2015, 58:456-463.
22. Henriksson E., Jones H.A., Patel K., Peggie M., Morrice N., Sakamoto K., Goransson O. The AMPK-related kinase SIK2 is regulated by cAMP via phosphorylation at Ser358 in adipocytes. Biochem. J. 2012, 444:503-514.
23. Henriksson E., Sall J., Gormand A., Wasserstrom S., Morrice N.A., Fritzen A.M., Foretz M., Campbell D.G., Sakamoto K., Ekelund M., Degerman E., Stenkula K.G., Goransson O. Salt-inducible kinase 2 regulates CRTCs, HDAC4 and glucose uptake in adipocytes. J. Cell Sci. 2015, 128:472-486.
24. Hohmeier H.E., Mulder H., Chen G., Henkel-Rieger R., Prentki M., Newgard C.B. Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 2000, 49:424-430.
25. Hollander J.A., Im H.I., Amelio A.L., Kocerha J., Bali P., Lu Q., Willoughby D., Wahlestedt C., Conkright M.D., Kenny P.J. Striatal microRNA controls cocaine intake through CREB signalling. Nature 2010, 466:197-202.
26. Iourgenko V., Zhang W., Mickanin C., Daly I., Jiang C., Hexham J.M., Orth A.P., Miraglia L., Meltzer J., Garza D., Chirn G.W., McWhinnie E., Cohen D., Skelton J., Terry R., Yu Y., et al. Identification of a family of cAMP response element-binding protein coactivators by genome-scale functional analysis in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12147-12152.
27. Jacovetti C., Abderrahmani A., Parnaud G., Jonas J.C., Peyot M.L., Cornu M., Laybutt R., Meugnier E., Rome S., Thorens B., Prentki M., Bosco D., Regazzi R. MicroRNAs contribute to compensatory beta cell expansion during pregnancy and obesity. J. Clin. Investig. 2012, 122:3541-3551.
28. Jagannath A., Butler R., Godinho S.I., Couch Y., Brown L.A., Vasudevan S.R., Flanagan K.C., Anthony D., Churchill G.C., Wood M.J., Steiner G., Ebeling M., Hossbach M., Wettstein J.G., Duffield G.E., Gatti S., et al. The CRTC1-SIK1 pathway regulates entrainment of the circadian clock. Cell 2013, 154:1100-1111.
29. Jhala U.S., Canettieri G., Screaton R.A., Kulkarni R.N., Krajewski S., Reed J., Walker J., Lin X., White M., Montminy M. cAMP promotes pancreatic beta-cell survival via CREB-mediated induction of IRS2. Genes Dev. 2003, 17:1575-1580.
30. Kalis M., Bolmeson C., Esguerra J.L.S., Gupta S., Edlund A., Tormo-Badia N., Speidel D., Holmberg D., Mayans S., Khoo N.K.S., Wendt A., Eliasson L., Cilio C.M. Beta-cell specific deletion of dicer1 leads to defective insulin secretion and diabetes mellitus. Plos One 2011, 6.
31. Keller D.M., Clark E.A., Goodman R.H. Regulation of microRNA-375 by cAMP in pancreatic beta-cells. Mol. Endocrinol. 2012, 26:989-999.
32. Kim M.J., Park S.K., Lee J.H., Jung C.Y., Sung D.J., Park J.H., Yoon Y.S., Park J., Park K.G., Song D.K., Cho H., Kim S.T., Koo S.H. Salt inducible kinase 1 terminates cAMP signaling by an evolutionarily conserved negative feedback loop in beta cells. Diabetes 2015, 64:3189-3202. pii: db141240.[Epub ahead of print].
33. Leech C.A., Dzhura I., Chepurny O.G., Kang G., Schwede F., Genieser H.G., Holz G.G. Molecular physiology of glucagon-like peptide-1 insulin secretagogue action in pancreatic beta cells. Prog. Biophys. Mol. Biol. 2011, 107:236-247.
34. Lizcano J.M., Goransson O., Toth R., Deak M., Morrice N.A., Boudeau J., Hawley S.A., Udd L., Makela T.P., Hardie D.G., Alessi D.R. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. Embo J. 2004, 23:833-843.
35. Lovshin J.A., Drucker D.J. Incretin-based therapies for type 2 diabetes mellitus. Nat. Rev. Endocrinol. 2009, 5:262-269.
36. Mayr B., Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2001, 2:599-609.
37. Mihaylova M.M., Shaw R.J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 2011, 13:1016-1023.
38. Nesca V., Guay C., Jacovetti C., Menoud V., Peyot M.L., Laybutt D.R., Prentki M., Regazzi R. Identification of particular groups of microRNAs that positively or negatively impact on beta cell function in obese models of type 2 diabetes. Diabetologia 2013, 56:2203-2212.
39. Oetjen E., Diedrich T., Eggers A., Eckert B., Knepel W. Distinct properties of the cAMP-responsive element of the rat insulin I gene. J. Biol. Chem. 1994, 269:27036-27044.
40. Pedersen M.G., Salunkhe V.A., Svedin E., Edlund A., Eliasson L. Calcium current inactivation rather than pool depletion explains reduced exocytotic rate with prolonged stimulation in insulin-secreting INS-1 832/13 cells. Plos One 2014, 9:e103874.
41. Rehfuss R.P., Walton K.M., Loriaux M.M., Goodman R.H. The cAMP-regulated enhancer-binding protein ATF-1 activates transcription in response to cAMP-dependent protein kinase A. J. Biol. Chem. 1991, 266:18431-18434.
42. Remenyi J., Hunter C.J., Cole C., Ando H., Impey S., Monk C.E., Martin K.J., Barton G.J., Hutvagner G., Arthur J.S. Regulation of the miR-212/132 locus by MSK1 and CREB in response to neurotrophins. Biochem. J. 2010, 428:281-291.
43. Sakamaki J., Fu A., Reeks C., Baird S., Depatie C., Al Azzabi M., Bardeesy N., Gingras A.C., Yee S.P., Screaton R.A. Role of the SIK2-p35-PJA2 complex in pancreatic beta-cell functional compensation. Nat. Cell Biol. 2014, 16:234-244.
44. Salunkhe V.A., Esguerra J.L., Ofori J.K., Mollet I.G., Braun M., Stoffel M., Wendt A., Eliasson L. Modulation of microRNA-375 expression alters voltage-gated Na(+) channel properties and exocytosis in insulin-secreting cells. Acta Physiol. (Oxf.) 2015, 213:882-892.
45. Sanosaka M., Fujimoto M., Ohkawara T., Nagatake T., Itoh Y., Kagawa M., Kumagai A., Fuchino H., Kunisawa J., Naka T., Takemori H. Salt-inducible kinase 3 deficiency exacerbates lipopolysaccharide-induced endotoxin shock accompanied by increased levels of pro-inflammatory molecules in mice. Immunology 2015, 145:268-278.
46. Screaton R.A., Conkright M.D., Katoh Y., Best J.L., Canettieri G., Jeffries S., Guzman E., Niessen S., Yates J.R., Takemori H., Okamoto M., Montminy M. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 2004, 119:61-74.
47. Seino S. Cell signalling in insulin secretion: the molecular targets of ATP, cAMP and sulfonylurea. Diabetologia 2012, 55:2096-2108.
48. Shang J., Li J., Keller M.P., Hohmeier H.E., Wang Y., Feng Y., Zhou H.H., Shen X., Rabaglia M., Soni M., Attie A.D., Newgard C.B., Thornberry N.A., Howard A.D., Zhou Y.P. Induction of miR-132 and miR-212 expression by glucagon-like peptide 1 (GLP-1) in rodent and human pancreatic beta-cells. Mol. Endocrinol. 2015, 29:1243-1253.
49. Shao W., Wang Z., Ip W., Chiang Y.T., Xiong X., Chai T., Xu C., Wang Q., Jin T. GLP-1(28-36) improves beta-cell mass and glucose disposal in streptozotocin-induced diabetic mice and activates cAMP/PKA/beta-catenin signaling in beta-cells in vitro. Am. J. Physiol. Endocrinol. Metab. 2013, 304:E1263-E1272.
50. Shin S., Le Lay J., Everett L.J., Gupta R., Rafiq K., Kaestner K.H. CREB mediates the insulinotropic and anti-apoptotic effects of GLP-1 signaling in adult mouse beta-cells. Mol. Metab. 2014, 3:803-812.
51. Takemori H., Okamoto M. Regulation of CREB-mediated gene expression by salt inducible kinase. J. Steroid Biochem. Mol. Biol. 2008, 108:287-291.
52. Uebi T., Tamura M., Horike N., Hashimoto Y.K., Takemori H. Phosphorylation of the CREB-specific coactivator TORC2 at Ser(307) regulates its intracellular localization in COS-7 cells and in the mouse liver. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E413-E425.
53. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. RESEARCH0034.
54. Vatamaniuk M.Z., Gupta R.K., Lantz K.A., Doliba N.M., Matschinsky F.M., Kaestner K.H. Foxa1-deficient mice exhibit impaired insulin secretion due to uncoupled oxidative phosphorylation. Diabetes 2006, 55:2730-2736.
55. Vo N., Klein M.E., Varlamova O., Keller D.M., Yamamoto T., Goodman R.H., Impey S. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16426-16431.
56. Wang Z., Takemori H., Halder S.K., Nonaka Y., Okamoto M. Cloning of a novel kinase (SIK) of the SNF1/AMPK family from high salt diet-treated rat adrenal. FEBS Lett. 1999, 453:135-139.
57. Zhao E., Keller M.P., Rabaglia M.E., Oler A.T., Stapleton D.S., Schueler K.L., Neto E.C., Moon J.Y., Wang P., Wang I.M., Lum P.Y., Ivanovska I., Cleary M., Greenawalt D., Tsang J., Choi Y.J., et al. Obesity and genetics regulate microRNAs in islets, liver, and adipose of diabetic mice. Mamm. Genome 2009, 20:476-485.