Conditional ablation of Gsk-3β in islet beta cells results in expanded mass and resistance to fat feeding-induced diabetes in mice

Diabetologia

Volumn 53, Issue 12, 2010, Pages 2600-2610

  Liu, Y ^a   Tanabe, K ^a,b   Baronnier, D ^a   Patel, S ^c   Woodgett, J ^c   Cras Meneur C ^d   Permutt, M A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Glycogen synthase kinase 3 ; IRS1; IRS2; Islet beta cells; Islet mass; PDX1; Proliferation

Indexed keywords

CRE RECOMBINASE; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; GLUCOSE TOLERANCE; IN VITRO STUDY; INSULIN RELEASE; LIPID DIET; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIET, ATHEROGENIC; DIETARY FATS; DRUG RESISTANCE; EATING; GENE KNOCKDOWN TECHNIQUES; GLYCOGEN SYNTHASE KINASE 3; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, KNOCKOUT; ORGAN SIZE; ORGAN SPECIFICITY; RATS; UP-REGULATION;

EID: 78649335126     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-1882-x     Document Type: Article

References (38)

1. N Neubauer RN Kulkarni 2006 Molecular approaches to study control of glucose homeostasis ILAR J 47 199 211 1:CAS:528:DC%2BD28Xls1SjsLw%3D 16804195
2. RN Kulkarni 2005 New insights into the roles of insulin/IGF-I in the development and maintenance of beta-cell mass Rev Endocr Metab Dis 6 199 210 1:CAS:528:DC%2BD28XhsVegtLw%3D 10.1007/s11154-005-3051-y (Pubitemid 41288281)
3. JJ Heit SK Karnik SK Kim 2006 Intrinsic regulators of pancreatic beta-cell proliferation Annu Rev Cell Dev Biol 22 311 338 1:CAS:528: DC%2BD28Xht1yjs7jM 10.1146/annurev.cellbio.22.010305.104425 16824015
4. E Bernal-Mizrachi W Wen S Stahlhut CM Welling MA Permutt 2001 Islet beta cell expression of constitutively active Akt1/PKB alpha induces striking hypertrophy, hyperplasia, and hyperinsulinemia J Clin Invest 108 1631 1638 1:CAS:528:DC%2BD3MXovVCgs7c%3D 11733558
5. RL Tuttle NS Gill W Pugh, et al. 2001 Regulation of pancreatic beta-cell growth and survival by the serine/threonine protein kinase Akt1/PKBalpha Nat Med 7 1133 1137 1:CAS:528:DC%2BD3MXns12kur4%3D 10.1038/nm1001-1133 11590437 (Pubitemid 33010022)
6. L Kockeritz B Doble S Patel JR Woodgett 2006 Glycogen synthase kinase-3-an overview of an over-achieving protein kinase Curr Drug Targets 7 1377 1388 1:CAS:528:DC%2BD28XhtFensL%2FK 17100578
7. H Eldar-Finkelman EG Krebs 1997 Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action Proc Natl Acad Sci USA 94 9660 9664 1:CAS:528:DyaK2sXlvVWjsLY%3D 10.1073/pnas.94.18.9660 9275179 (Pubitemid 27408118)
8. H Eldar-Finkelman SA Schreyer MM Shinohara RC LeBoeuf EG Krebs 1999 Increased glycogen synthase kinase-3 activity in diabetes- and obesity-prone C57BL/6J mice Diabetes 48 1662 1666 1:CAS:528:DyaK1MXkvVKms78%3D 10.2337/diabetes.48.8.1662 10426388 (Pubitemid 29356878)
9. SE Nikoulina TP Ciaraldi S Mudaliar P Mohideen L Carter RR Henry 2000 Potential role of glycogen synthase kinase-3 in skeletal muscle insulin resistance of type 2 diabetes Diabetes 49 263 271 1:CAS:528: DC%2BD3cXpsl2kug%3D%3D 10.2337/diabetes.49.2.263 10868943 (Pubitemid 30071005)
10. R Rao CM Hao R Redha DH Wasserman OP McGuinness MD Breyer 2007 Glycogen synthase kinase 3 inhibition improves insulin-stimulated glucose metabolism but not hypertension in high-fat-fed C57BL/6J mice Diabetologia 50 452 460 1:CAS:528:DC%2BD2sXitlSksg%3D%3D 10.1007/s00125-006-0552-5 17151860
11. H Liu MS Remedi KL Pappan, et al. 2009 Glycogen synthase kinase-3 and mammalian target of rapamycin pathways contribute to DNA synthesis, cell cycle progression, and proliferation in human islets Diabetes 58 663 672 1:CAS:528:DC%2BD1MXjt1Wktro%3D 10.2337/db07-1208 19073772
12. S Patel BW Doble K MacAulay EM Sinclair DJ Drucker JR Woodgett 2008 Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action Mol Cell Biol 28 6314 6328 1:CAS:528:DC%2BD1cXht1Cit7bF 10.1128/MCB.00763-08 18694957
13. PL Herrera 2000 Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages Development 127 2317 2322 1:CAS:528:DC%2BD3cXksVKmsrg%3D 10804174
14. JY Lee M Ristow X Lin MF White MA Magnuson L Hennighausen 2006 RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function J Biol Chem 281 2649 2653 1:CAS:528:DC%2BD28XovVeitA%3D%3D 10.1074/jbc.M512373200 16326700 (Pubitemid 43845726)
15. K Tanabe Z Liu S Patel, et al. 2008 Genetic deficiency of glycogen synthase kinase-3-beta corrects diabetes in mouse models of insulin resistance PLoS Biol 6 e37 10.1371/journal.pbio.0060037 18288891 (Pubitemid 351329051)
16. V Girish A Vijayalakshmi 2004 Affordable image analysis using NIH Image/ImageJ Indian J Cancer 41 47 1:STN:280:DC%2BD2c3gslCktA%3D%3D 15105580
17. SC Martinez C Cras-Meneur E Bernal-Mizrachi MA Permutt 2006 Glucose regulates Foxo1 through insulin receptor signaling in the pancreatic islet β-cell Diabetes 55 1581 1591 1:CAS:528:DC%2BD28XlsF2rtLc%3D 10.2337/db05-0678 16731820 (Pubitemid 44324110)
18. E Bernal-Mizrachi S Fatrai JD Johnson, et al. 2004 Defective insulin secretion and increased susceptibility to experimental diabetes are induced by reduced Akt activity in pancreatic islet beta cells J Clin Invest 114 928 936 1:CAS:528:DC%2BD2cXot12gtrY%3D 15467831
19. M Ohsugi C Cras-Meneur Y Zhou, et al. 2005 Reduced expression of the insulin receptor in mouse insulinoma (MIN6) cells reveals multiple roles of insulin signaling in gene expression, proliferation, insulin content, and secretion J Biol Chem 280 4992 5003 1:CAS:528:DC%2BD2MXhtVymtbY%3D 10.1074/jbc.M411727200 15546857 (Pubitemid 40288675)
20. JJ Heit AA Apelqvist X Gu, et al. 2006 Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function Nature 443 345 349 1:CAS:528:DC%2BD28Xpslaksrs%3D 10.1038/nature05097 16988714 (Pubitemid 44435154)
21. MF White 2006 Regulating insulin signaling and beta-cell function through IRS proteins Can J Physiol Pharmacol 84 725 737 1:CAS:528:DC%2BD28XhtFGqtLnM 10.1139/Y06-008 16998536 (Pubitemid 44897893)
22. SE Nikoulina TP Ciaraldi S Mudaliar L Carter K Johnson RR Henry 2002 Inhibition of glycogen synthase kinase 3 improves insulin action and glucose metabolism in human skeletal muscle Diabetes 51 2190 2198 1:CAS:528: DC%2BD38Xlt1Wlu78%3D 10.2337/diabetes.51.7.2190 12086949
23. JA Kushner J Ye M Schubert, et al. 2002 Pdx1 restores beta cell function in Irs2 knockout mice J Clin Invest 109 1193 1201 1:CAS:528:DC%2BD38XjsFalsLY%3D 11994408
24. MP Coghlan AA Culbert DA Cross, et al. 2000 Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription Chem Biol 7 793 803 1:CAS:528:DC%2BD3cXotVWitrs%3D 10.1016/S1074-5521(00)00025-9 11033082
25. S Ikeda S Kishida H Yamamoto H Murai S Koyama A Kikuchi 1998 Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin EMBO J 17 1371 1384 1:CAS:528:DyaK1cXitFOqsL0%3D 10.1093/emboj/17.5.1371 9482734 (Pubitemid 28105516)
26. S Amit A Hatzubai Y Birman, et al. 2002 Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway Genes Dev 16 1066 1076 1:CAS:528:DC%2BD38XjvV2ku78%3D 10.1101/gad.230302 12000790 (Pubitemid 34507196)
27. M Surjit SK Lal 2007 Glycogen synthase kinase-3 phosphorylates and regulates the stability of p27kip1 protein Cell Cycle 6 580 588 1:CAS:528:DC%2BD2sXnvFygurk%3D 17351340
28. BB Dokken JA Sloniger EJ Henriksen 2005 Acute selective glycogen synthase kinase-3 inhibition enhances insulin signaling in prediabetic insulin-resistant rat skeletal muscle Am J Physiol Endocrinol Metab 288 E1188 E1194 1:CAS:528:DC%2BD2MXlsVylsL0%3D 10.1152/ajpendo.00547.2004 15671078 (Pubitemid 40726806)
29. MJ Boucher L Selander L Carlsson H Edlund 2006 Phosphorylation marks IPF1/PDX1 protein for degradation by glycogen synthase kinase 3-dependent mechanisms J Biol Chem 281 6395 6403 1:CAS:528:DC%2BD28XhvFOhu7Y%3D 10.1074/jbc.M511597200 16407209 (Pubitemid 43847571)
30. S Guo R Burnette L Zhao, et al. 2009 The stability and transactivation potential of the mammalian MafA transcription factor are regulated by serine 65 phosphorylation J Biol Chem 284 759 765 1:CAS:528:DC%2BD1MXhsV2huw%3D%3D 10.1074/jbc.M806314200 19004825
31. H Sharfi H Eldar-Finkelman 2008 Sequential phosphorylation of insulin receptor substrate-2 by glycogen synthase kinase-3 and c-Jun NH2-terminal kinase plays a role in hepatic insulin signaling Am J Physiol Endocrinol Metab 294 E307 E315 1:CAS:528:DC%2BD1cXit1yktLY%3D 10.1152/ajpendo.00534.2007 18029441 (Pubitemid 351231456)
32. SC Martinez K Tanabe C Cras-Meneur NA Abumrad E Bernal-Mizrachi MA Permutt 2008 Inhibition of Foxo1 protects pancreatic islet beta-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis Diabetes 57 846 859 1:CAS:528:DC%2BD1cXksVGktbo%3D 10.2337/db07-0595 18174526
33. ES Horton 2009 Effects of lifestyle changes to reduce risks of diabetes and associated cardiovascular risks: results from large scale efficacy trials Obesity (Silver Spring) 17 Suppl 3 S43 S48 10.1038/oby.2009.388
34. Y Terauchi I Takamoto N Kubota, et al. 2007 Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance J Clin Invest 117 246 257 1:CAS:528: DC%2BD2sXmvFSjtA%3D%3D 10.1172/JCI17645 17200721 (Pubitemid 46048470)
35. DJ Withers JS Gutierrez H Towery, et al. 1998 Disruption of IRS-2 causes type 2 diabetes in mice Nature 391 900 904 1:CAS:528:DyaK1cXhsFyksr0%3D 10.1038/36116 9495343 (Pubitemid 28157668)
36. T Kitamura J Nakae Y Kitamura, et al. 2002 The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth J Clin Invest 110 1839 1847 1:CAS:528:DC%2BD38XpslWmsbw%3D 12488434
37. J Buteau A Shlien S Foisy D Accili 2007 Metabolic diapause in pancreatic beta-cells expressing a gain-of-function mutant of the forkhead protein Foxo1 J Biol Chem 282 287 293 1:CAS:528:DC%2BD2sXks1yr 10.1074/jbc.M606118200 17107961 (Pubitemid 47076601)
38. SH Um F Frigerio M Watanabe, et al. 2004 Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity Nature 431 200 205 1:CAS:528:DC%2BD2cXntlGks7g%3D 10.1038/nature02866 15306821 (Pubitemid 39243474)