PKCζ is essential for pancreatic β-cell replication during insulin resistance by regulating mTOR and cyclin-D2

Diabetes

Volumn 65, Issue 5, 2016, Pages 1283-1296

  Lakshmipathi, Jayalakshmi ^a   Alvarez Perez, Juan Carlos ^a   Rosselot, Carolina ^a   Casinelli, Gabriella P ^b   Stamateris, Rachel E ^c   Rausell Palamos, Francisco ^a   O'Donnell, Christopher P ^d   Vasavada, Rupangi C ^a   Scott, Donald K ^a   Alonso, Laura C ^c   Garcia Ocaña, Adolfo ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D2; GLUCOKINASE; GLUCOSE; INSULIN; KINASE DEAD PROTEIN KINASE C ZETA; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; PROTEIN KINASE C ZETA; UNCLASSIFIED DRUG; CCND2 PROTEIN, MOUSE; MTOR PROTEIN, MOUSE; PROTEIN KINASE C; RECOMBINANT PROTEIN; TARGET OF RAPAMYCIN KINASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; HYPERINSULINEMIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; INSULIN RESISTANCE; LIPID DIET; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; DIABETES MELLITUS, TYPE 2; GENETICS; KNOCKOUT MOUSE; METABOLISM; OBESITY; PANCREAS ISLET; PATHOLOGY; PATHOPHYSIOLOGY; RNA INTERFERENCE; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TISSUE BANK; TRANSGENIC MOUSE;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN D2; DIABETES MELLITUS, TYPE 2; ENZYME ACTIVATION; GLUCOSE; HUMANS; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVERWEIGHT; PROTEIN KINASE C; RECOMBINANT PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE BANKS; TOR SERINE-THREONINE KINASES;

EID: 84964692752     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-1398     Document Type: Article

References (45)

1. Muoio DM, Newgard CB. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 2008;9:193-205
2. Sachdeva MM, Stoffers DA. Minireview: meeting the demand for insulin: molecular mechanisms of adaptive postnatal beta-cell mass expansion. Mol Endocrinol 2009;23:747-758
3. Alonso LC, Yokoe T, Zhang P, et al. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 2007;56:1792-1801
4. Levitt HE, Cyphert TJ, Pascoe JL, et al. Glucose stimulates human beta cell replication in vivo in islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia 2011;54:572-582
5. Stamateris RE, Sharma RB, Hollern DA, Alonso LC. Adaptive β-cell proliferation increases early in high-fat feeding in mice, concurrent with metabolic changes, with induction of islet cyclin D2 expression. Am J Physiol Endocrinol Metab 2013;305:E149-E159
6. Zarrouki B, Benterki I, Fontés G, et al. Epidermal growth factor receptor signaling promotes pancreatic β-cell proliferation in response to nutrient excess in rats through mTOR and FOXM1. Diabetes 2014;63:982-993
7. Georgia S, Hinault C, Kawamori D, et al. Cyclin D2 is essential for the compensatory beta-cell hyperplastic response to insulin resistance in rodents. Diabetes 2010;59:987-996
8. El Ouaamari A, Kawamori D, Dirice E, et al. Liver-derived systemic factors drive β cell hyperplasia in insulin-resistant states. Cell Reports 2013;3:401-410
9. Yi P, Park JS, Melton DA. Betatrophin: a hormone that controls pancreatic β cell proliferation. Cell 2013;153:747-758
10. Imai J, Katagiri H, Yamada T, et al. Regulation of pancreatic beta cell mass by neuronal signals from the liver. Science 2008;322:1250-1254
11. Wellcome Trust Case Control Consortium. Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature 2007;447:661-678
12. Morris AP. Fine mapping of type 2 diabetes susceptibility loci. Curr Diab Rep 2014;14:549
13. Qin L, Zhou L, Wu X, et al. Genetic variants in protein kinase C zeta gene and type 2 diabetes risk: a case-control study of a Chinese Han population. Diabetes Metab Res Rev 2008;24:480-485
14. Li YF, Sun HX, Wu GD, et al. Protein kinase C/zeta (PRKCZ) gene is associated with type 2 diabetes in Han population of North China and analysis of its haplotypes. World J Gastroenterol 2003;9:2078-2082
15. Hirai T, Chida K. Protein kinase Czeta (PKCzeta): activation mechanisms and cellular functions. J Biochem 2003;133:1-7
16. Buteau J, Foisy S, Rhodes CJ, Carpenter L, Biden TJ, Prentki M. Protein kinase Czeta activation mediates glucagon-like peptide-1-induced pancreatic beta-cell proliferation. Diabetes 2001;50:2237-2243
17. Vasavada RC, Wang L, Fujinaka Y, et al. Protein kinase C-ζ activation markedly enhances β-cell proliferation: an essential role in growth factor mediated β-cell mitogenesis. Diabetes 2007;56:2732-2743
18. Velazquez-Garcia S, Valle S, Rosa TC, et al. Activation of protein kinase C-ζ in pancreatic β-cells in vivo improves glucose tolerance and induces β-cell expansion via mTOR activation. Diabetes 2011;60:2546-2559
19. Porat S, Weinberg-Corem N, Tornovsky-Babaey S, et al. Control of pancreatic β cell regeneration by glucose metabolism. Cell Metab 2011;13:440-449
20. Balcazar N, Sathyamurthy A, Elghazi L, et al. mTORC1 activation regulates beta-cell mass and proliferation by modulation of cyclin D2 synthesis and stability. J Biol Chem 2009;284:7832-7842
21. Kushner JA, Ciemerych MA, Sicinska E, et al. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005;25:3752-3762
22. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 2004;114:963-968
23. García-Ocaña A, Takane K, Syed MA, Philbrick WM, Vasavada RC, Stewart AF. Hepatocyte growth factor overexpression in the islet of transgenic mice increases beta cell proliferation, enhances islet mass, and induces hypoglycemia. J Biol Chem 2000;275:1226-1232
24. Chou MM, Hou W, Johnson J, et al. Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Curr Biol 1998;8:1069-1077
25. Romanelli A, Martin KA, Toker A, Blenis J. p70 S6 kinase is regulated by protein kinase Czeta and participates in a phosphoinositide 3-kinase-regulated signalling complex. Mol Cell Biol 1999;19:2921-2928
26. Wicksteed B, Brissova M, Yan W, et al. Conditional gene targeting in mouse pancreatic β-cells: analysis of ectopic Cre transgene expression in the brain. Diabetes 2010;59:3090-3098
27. Zhang H, Fujitani Y, Wright CV, Gannon M. Efficient recombination in pancreatic islets by a tamoxifen-inducible Cre-recombinase. Genesis 2005;42:210-217
28. Alvarez-Perez JC, Ernst S, Demirci C, et al. Hepatocyte growth factor/c-Met signaling is required for β-cell regeneration. Diabetes 2014;63:216-223
29. Wang P, Alvarez-Perez JC, Felsenfeld DP, et al. A high-throughput chemical screen reveals that harmine-mediated inhibition of DYRK1A increases human pancreatic beta cell replication. Nat Med 2015;21:383-388
30. Limatola C, Schaap D, Moolenaar WH, van Blitterswijk WJ. Phosphatidic acid activation of protein kinase C-zeta overexpressed in COS cells: comparison with other protein kinase C isotypes and other acidic lipids. Biochem J 1994;304:1001-1008
31. Müller G, Ayoub M, Storz P, Rennecke J, Fabbro D, Pfizenmaier K. PKC zeta is a molecular switch in signal transduction of TNF-alpha, bifunctionally regulated by ceramide and arachidonic acid. EMBO J 1995;14:1961-1969
32. Charruyer A, Jean C, Colomba A, et al. PKCzeta protects against UV-C-induced apoptosis by inhibiting acid sphingomyelinase-dependent ceramide production. Biochem J 2007;405:77-83
33. Mendez R, Kollmorgen G, White MF, Rhoads RE. Requirement of protein kinase C zeta for stimulation of protein synthesis by insulin. Mol Cell Biol 1997;17:5184-5192
34. Terauchi Y, Takamoto I, Kubota N, et al. Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance. J Clin Invest 2007;117:246-257
35. Terauchi Y, Sakura H, Yasuda K, et al. Pancreatic beta-cell-specific targeted disruption of glucokinase gene. Diabetes mellitus due to defective insulin secretion to glucose. J Biol Chem 1995;270:30253-30256
36. Takamoto I, Terauchi Y, Kubota N, Ohsugi M, Ueki K, Kadowaki T. Crucial role of insulin receptor substrate-2 in compensatory beta-cell hyperplasia in response to high fat diet-induced insulin resistance. Diabetes Obes Metab 2008;10(Suppl. 4):147-156
37. Brouwers B, de Faudeur G, Osipovich AB, et al. Impaired islet function in commonly used transgenic mouse lines due to human growth hormone minigene expression. Cell Metab 2014;20:979-990
38. Oropeza D, Jouvet N, Budry L, et al. Phenotypic characterization of MIP-CreERT1Lphi mice with transgene-driven islet expression of human growth hormone. Diabetes 2015;64:3798-3807
39. Fiaschi-Taesch NM, Salim F, Kleinberger J, et al. Induction of human betacell proliferation and engraftment using a single G1/S regulatory molecule, cdk6. Diabetes 2010;59:1926-1936
40. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004;18:1926-1945
41. Rachdi L, Balcazar N, Osorio-Duque F, et al. Disruption of Tsc2 in pancreatic beta cells induces beta cell mass expansion and improved glucose tolerance in a TORC1-dependent manner. Proc Natl Acad Sci U S A 2008;105:9250-9255
42. Zahr E, Molano RD, Pileggi A, et al. Rapamycin impairs in vivo proliferation of islet beta-cells. Transplantation 2007;84:1576-1583
43. Jetton TL, Lausier J, LaRock K, et al. Mechanisms of compensatory betacell growth in insulin-resistant rats: roles of Akt kinase. Diabetes 2005;54:2294-2304
44. Bernal-Mizrachi E, Fatrai S, Johnson JD, et al. Defective insulin secretion and increased susceptibility to experimental diabetes are induced by reduced Akt activity in pancreatic islet beta cells. J Clin Invest 2004;114:928-936
45. Chiang GG, Abraham RT. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J Biol Chem 2005;280:25485-25490