The plecomacrolide vacuolar-ATPase inhibitor bafilomycin, alters insulin signaling in MIN6 β-cells

Cell Biology and Toxicology

Volumn 22, Issue 3, 2006, Pages 169-181

  Hettiarachchi, K D ^a   Zimmet, P Z ^a,b   Myers, M A ^a  

^a MONASH UNIVERSITY   (Australia)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

Bafilomycin; Insulin signaling; Islet cell; MIN6; Pancreas development; Type 1 diabetes; Vacuolar ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE INHIBITOR; BAFILOMYCIN; BAFILOMYCIN B1; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 2; MACROLIDE; MESSENGER RNA; PLECOMACROLIDE; PREPROINSULIN; PROTEIN BAD; PROTEIN BCL 2; PROTEIN KINASE B; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

ACIDIFICATION; ADIPOSE TISSUE CELL; ANIMAL CELL; ARTICLE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETOGENESIS; ENDOSOME; ENZYME INHIBITION; INSULIN METABOLISM; INSULINOMA; LIVER CELL; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACIDS; ANIMALS; BCL-ASSOCIATED DEATH PROTEIN; CELL LINE; INSULIN; MACROLIDES; MICE; PHOSPHORYLATION; PROINSULIN; PROTEIN PRECURSORS; RNA, MESSENGER; SIGNAL TRANSDUCTION; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES;

ANIMALIA;

EID: 33646497230     PISSN: 07422091     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10565-006-0054-8     Document Type: Article

References (42)

1. Araki E, Lipes MA, Patti ME, Brunning JC, Haag BL, Johnson RS. Alternative pathways of insulin signalling in mice with targeted disruption of IRS-1 gene. Nature. 1994;372:186-90.
2. Authier F, Metioui M, Fabrega S, Kouach M, Briand G. Endosomal proteolysis of internalized insulin at the C-terminal region of the B chain by Cathepsin D. J Biol Chem. 2002;277:9437-46.
3. Balbis A, Baquiran G, Dumas V, Posner BI. Effect of inhibiting vacuolar acidification on insulin signaling in hepatocytes. J Biol Chem. 2004;279:12777-85.
4. Bernal-Mizrachi E, Wen W, Stahlhut S, Welling CM, Permutt MA. Islet beta-cell expression of constitutively active Akt1/PKB alpha induces striking hypertrophy, hyperplasia, and hyperinsulinemia. J Clin Invest. 2001;108:1631-8.
5. Sevan AP, Krook A, Tikerpae J, Seabright PJ, Siddle K, Smith GD. Chloroquine extends the lifetime of the activated insulin receptor complex in endosomes. J Biol Chem. 1997;272:26833-1-0.
6. Bevan P. Insulin signalling. J Cell Sci. 2001;114:1429-30.
7. Biggs WH, Meisenhelder J, Hunter T, Cavenee WK, Arden KC. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Nat Acad Sci USA. 1999;96:7421-26.
8. Birkenkamp KU, Coffer PJ. FOXO transcription factors as regulators of immune homeostasis: molecules to die for? J Immunol. 2003a;171:1623-9.
9. Birkenkamp KU, Coffer PJ. Regulation of cell survival and proliferation by the FOXO (Forkhead box, class O) subfamily of Forkhead transcription factors. Biochem Soc Trans. 2003b;31:292-7.
10. Chinni SR, Shisheva A. Arrest of endosome acidification by bafilomycin A1 mimics insulin action on GLUT4 translocation in 3T3-L1 adipocytes. Biochem J. 1999;339:599-606.
11. Da Silva XG, Qian Q, Cullen PJ, Rutter GA. Distinct roles for insulin and insulin-like growth factor-1 receptors in pancreatic beta-cell glucose sensing revealed by RNA silencing. Biochem J. 2004;377:149-58.
12. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y. Phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997;91:231-41.
13. del Peso L, Gonzalez VM, Hernandez R, Barr FG, Nunez G. Regulation of the forkhead transcription factor FKHR, but not the PAX3-FKHR fusion protein, by the serine/threonine kinase Akt. Oncogene. 1999;18:7328-33.
14. Di Guglielmo GM, Drake P, Baass P, Authier F, Posner BI, Bergeron JM. Insulin receptor internalization and signalling. Mol Cell Biol. 1998;182:59-63.
15. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer P. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol. 2000;10:1201-4.
16. Doherty JJ, Kay DG, Lai WH, Posner BI, Bergeron JJ. Selective degradation of insulin within rat liver endosomes. J Cell Biol. 1990;110:35-42.
17. Drose S, Boddien C, Gassel M, Ingenhorst G, Zeeck A, Altendorf K. Semisynthetic derivatives of concanamycin A and C, as inhibitors of V- and P-type ATPases: structure-activity investigations and developments of photoaffinity probes. Biochemistry. 2001;40:2816-25.
18. Hettiarachchi KD, Zimmet PZ, Myers MA. Transplacental exposure to bafilomycin disrupts pancreatic islet organogenesis and accelerates diabetes onset in NOD mice. J Autoimmun. 2004;22:287-96.
19. Kulkarni RN, Bruning JC, Winnay JN, Postic C, Magnuson MA, Kahn CR. Tissue-specific knockout of the insulin receptor in pancreatic beta cells creates an insulin secretory defect similar to that in Type 2 diabetes. Cell. 1999a;96:329-39.
20. Kulkarni RN, Winnay JN, Daniels M, et al. Altered function of insulin receptor substrate-1-deficient mouse islets and cultured beta-cell lines. J Clin Invest. 1999b;104:R69-75.
21. Kulkarni RN, Holzenberger M, Shih DQ, et al. Beta-cell-specific deletion of the Igf1 receptor leads to hyperinsulinemia and glucose intolerance but does not alter beta-cell mass. Nat Genet. 2002;31:111-5.
22. Leibiger B, Leibiger IB, Moede T, et al. Selective insulin signaling through A and B insulin receptors regulates transcription of insulin and glucokinase genes in pancreatic beta-cells. Mol Cell. 2001;7:559-70.
23. Leibiger IB, Leibiger B, Berggren PO. Insulin feedback action on pancreatic beta-cell function. FEBS Lett. 2002;532:1-6.
24. Lingohr M, Dickson L, McCuaig J, Hugi S, Twardzik D, Rhodes CJ. Activation of IRS-2 mediated signal transduction by IGF-1, but not TGF-α or EGF, augments pancreatic beta-cell proliferation. Diabetes. 2002;51:966-76.
25. Liu W, Chin-Chance C, Lee EJ, Lowe WL. Activation of phosphatidylinositol 3-kinase contributes to insulin-like growth factor I-mediated inhibition of pancreatic beta-cell death. Endocrinology. 2002;143:3802-12.
26. Myers MA, Hettiarachchi K, Ludeman J, Wilson AJ, Wilson CR, Zimmet PZ. Dietary microbial toxins and Type 1 diabetes. Ann NY Acad Sci. 2003;1005:418-22.
27. Navab R, Chevet E, Authier F, Di Guglielmo GM, Bergeron JM, Brodt P. Inhibition of endosomal insulin-like growth factor-I processing by cysteine proteinase inhibitors blocks receptor-mediated functions. J Biol Chem. 2001;276:13644-9.
28. Navarro-Tableros V, Sanchez-Soto MC, Garcia S, Hiriart M. Autocrine regulation of single pancreatic beta-cell survival. Diabetes. 2004;53:2018-23.
29. Ohsugi M, Cras-Meneur C, Zhou Y, et al. 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. 2005;280:4992-5003.
30. L and Bcl-2 via a MEK-dependent pathway. Correlation with resistance to etoposide-induced apoptosis. J Biol Chem. 2002;277:12040-6.
31. Peruzzi F, Prisco M, Dews M, et al. Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol Cell Biol. 1999;19:7203-15.
32. Peruzzi F, Prisco M, Morrione A, Valentinis B, Baserga R. Antiapoptotic signaling of the insulin-like growth factor-1 receptor through mitochondrial translocation of c-Raf and Nedd4. J Biol Chem. 2001;276:25990-6.
33. Rhodes CJ. IGF-I and GH post-receptor signaling mechanisms for pancreatic beta-cell replication. J Mol Endocrinol. 2000;24:303-11.
34. Rhodes CJ, White MF. Molecular insights into insulin action and secretion. Eur J Clin Invest. 2002;32:3-13.
35. Sherrill KW, Byrd MP, Van Eden ME, Lloyd RE. BCL-2 translation is mediated via internal ribosome entry during cell stress. J Biol Chem. 2004;279:29066-74.
36. Shymko RM, Dumont E, De-Meyts P, Dumont JE. Timing-dependence of insulin-receptor mitogenic versus metabolic signalling: a plausible model based on coincidence of hormone and effector binding. Biochem J. 1999;339:675-83.
37. Srinivasan S, Ohsugi M, Liu Z, Fatrai S, Bernal-Mizrachi E, Permutt MA. Endoplasmic reticulum stress-induced apoptosis is partly mediated by reduced insulin signaling through phosphatidylinositol 3-kinase/Akt and increased glycogen synthase kinase-3[beta] in mouse insulinoma cells. Diabetes. 2005;54:968-75.
38. Tuttle RL, Gill NS, Pugh W, et al. Regulation of pancreatic beta-cell growth and survival by the serine/threonine protein kinase Akt1/PKBalpha. Nat Med. 2001;7:1133-7.
39. van Haeften TW, Twickler TB. Insulin-like growth factors and pancreatic beta cells. Eur J Clin Invest. 2004;34:249-55.
40. Wrede C, Dickson L, Longohr M, Briaud I, Rhodes CJ. Protein kinase B/Akt prevents fatty acid-induced apoptosis in pancreatic beta-cells (INS-1). J Biol Chem. 2002;277:49676-84.
41. Xu GG, Rothenberg PL. Insulin receptor signaling in the beta-cell influences insulin gene expression and insulin content: evidence for autocrine beta-cell regulation. Diabetes. 1998;47:1243-52.
42. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell. 1996;87:619-28.