Distinct regulation of insulin receptor substrate-1 and -2 by 90-kDa heat-shock protein in adrenal chromaffin cells

Neurochemistry International

Volumn 56, Issue 1, 2010, Pages 42-50

  Yoshikawa, Norie ^a   Nemoto, Takayuki ^a   Satoh, Shinya ^a   Maruta, Toyoaki ^a   Yanagita, Toshihiko ^a   Chosa, Etsuo ^a   Wada, Akihiko ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

90 kDa heat shock protein; Adrenal chromaffin cells; Geldanamycin; Gene transcription; Insulin receptor substrate 1 and 2; Proteasome

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CALPASTATIN; CYCLOHEXIMIDE; DACTINOMYCIN; GELDANAMYCIN; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; HERBIMYCIN A; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; LACTACYSTIN; LACTACYSTIN BETA LACTONE; LEUPEPTIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEASOME; PROTEIN KINASE B; RADICICOL; RAF PROTEIN; TANESPIMYCIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CHROMAFFIN CELL; COMPLEX FORMATION; CONTROLLED STUDY; COW; DOSE TIME EFFECT RELATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; IC 50; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM;

ADRENAL MEDULLA; ANIMALS; BENZOQUINONES; CATTLE; CELLS, CULTURED; CHROMAFFIN CELLS; DOWN-REGULATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HSP90 HEAT-SHOCK PROTEINS; INSULIN RECEPTOR SUBSTRATE PROTEINS; LACTAMS, MACROCYCLIC; PHOSPHOTRANSFERASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

BOVINAE;

EID: 73449147964     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2009.08.013     Document Type: Article

References (60)

1. Akune T., Ogata N., Hoshi K., Kubota N., Terauchi Y., Tobe K., Takagi H., Azuma Y., Kadowaki T., Nakamura K., and Kawaguchi H. Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts. J. Cell. Biol. 159 (2002) 147-156
2. Basso A.D., Solit D.B., Chiosis G., Giri B., Tsichlis P., and Rosen N. Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J. Biol. Chem. 277 (2002) 39858-39866
3. Batulan Z., Taylor D.M., Aarons R.J., Minotti S., Doroudchi M.M., Nalbantoglu J., and Durham H.D. Induction of multiple heat shock proteins and neuroprotection in a primary culture model of familial amyotrophic lateral sclerosis. Neurobiol. Dis. 24 (2006) 213-225
4. Burks D.J., Font de Mora J., Schubert M., Withers D.J., Myers M.G., Towery H.H., Altamuro S.L., Flint C.L., and White M.F. IRS-2 pathways integrate female reproduction and energy homeostasis. Nature 407 (2000) 377-382
5. Chen J., Wu A., Sun H., Drakas R., Garofalo C., Cascio S., Surmacz E., and Baserga R. Functional significance of type 1 insulin-like growth factor-mediated nuclear translocation of the insulin receptor substrate-1 and β-catenin. J. Biol. Chem. 280 (2005) 29912-29920
6. 2-terminal kinase 1 regulates the stability of transcription factor Sp1 during mitosis. Mol. Biol. Cell 19 (2008) 1139-1151
7. Collins G.A., and Tansey W.P. The proteasome: a utility tool for transcription?. Curr. Opin. Genet. Dev. 16 (2006) 197-202
8. Elbi C., Walker D.A., Romero G., Sullivan W.P., Toft D.O., Hager G.L., and DeFranco D.B. Molecular chaperones function as steroid receptor nuclear mobility factors. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2876-2881
9. Freeman B.C., and Yamamoto K.R. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 296 (2002) 2232-2235
10. Friedman J.E., Ishizuka T., Shao J., Huston L., Highman T., and Catalano P. Impaired glucose transport and insulin receptor tyrosine phosphorylation in skeletal muscle from obese women with gestational diabetes. Diabetes 48 (1999) 1807-1814
11. Fujita N., Sato S., Ishida A., and Tsuruo T. Involvement of Hsp90 in signaling and stability of 3-phosphoinositide-dependent kinase-1. J. Biol. Chem. 277 (2002) 10346-10353
12. Gelling R.W., Morton G.J., Morrison C.D., Niswender K.D., Myers Jr. M.D., Rhodes C.J., and Schwartz M.W. Insulin action in the brain contributes to glucose lowering during insulin treatment of diabetes. Cell. Metab. 3 (2006) 67-73
13. Gibson S.L., Ma Z., and Shaw L.M. Divergent roles of IRS-1 and IRS-2 in breast cancer metastasis. Cell Cycle 6 (2007) 631-637
14. 1 integrins. J. Cell. Biol. 166 (2004) 407-418
15. Hegde A.N. Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity. Prog. Neurobiol. 73 (2004) 311-357
16. Huang C., Thirone A.C.P., Huang X., and Klip A. Differential contribution of insulin receptor substrates 1 versus 2 to insulin signaling and glucose uptake in L6 myotubes. J. Biol. Chem. 280 (2005) 19426-19435
17. Hung J.-J., Wu C.-Y., Liao P.-C., and Chang W.-C. Hsp90α recruited by Sp1 is important for transcription of 12(S)-lipoxygenase in A431 cells. J. Biol. Chem. 280 (2005) 36283-36292
18. Isaacs J.S., Jung Y.-J., Mimnaugh E.G., Martinez A., Cuttitta F., and Neckers L.M. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J. Biol. Chem. 277 (2002) 29936-29944
19. Kamal A., Thao L., Sensintaffar J., Zhang L., Boehm M.F., Fritz L.C., and Burrows F.J. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425 (2003) 407-410
20. Kamal A., Boehm M.F., and Burrows F.J. Therapeutic and diagnostic implications of Hsp90 activation. Trends Mol. Med. 10 (2004) 283-290
21. 2+ influx decreases tau phosphorylation via glycogen synthase kinase-3β in adrenal chromaffin cells. Neurochem. Int. 545 (2009) 497-505
22. Kubota T., Kubota N., Moroi M., Terauchi Y., Kobayashi T., Kamata K., Suzuki R., Tobe K., Namiki A., Aizawa S., Nagai R., Kadowaki T., and Yamaguchi T. Lack of insulin receptor substrate-2 causes progressive neointima formation in response to vessel injury. Circulation 107 (2003) 3073-3080
23. Kubota N., Terauchi Y., Tobe K., Yano W., Suzuki R., Ueki K., Takamoto I., Satoh H., Maki T., Kubota T., Moroi M., Okada-Iwabu M., Ezaki O., Nagai R., Ueta Y., Kadowaki T., and Noda T. Insulin receptor substrate 2 plays a crucial role in β cells and the hypothalamus. J. Clin. Invest. 114 (2004) 917-927 (Commentaries: Brady, M.J., 2004. J. Clin. Invest. 114, 886-888).
24. Lin X., Taguchi A., Park S., Kushner J.A., Li F., Li Y., and White M.F. Dysregulation of insulin receptor substrate 2 in β cells and brain causes obesity and diabetes. J. Clin. Invest. 114 (2004) 908-916 (commentaries: Brady, M.J., 2004. J. Clin. Invest. 114, 886-888).
25. Loo M.A., Jensen T.J., Cui L., Hou Y., Chang X.B., and Riordan J.R. Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J. 17 (1998) 6879-6887
26. Mortensen E.R., Marks P.A., Shiotani A., and Merchant J.L. Epidermal growth factor and okadaic acid stimulate Sp1 proteolysis. J. Biol. Chem. 272 (1997) 16540-16547
27. Nagoshi T., Matsui T., Aoyama T., Leri A., Anversa P., Li L., Ogawa W., del Monte F., Gwathmey J.K., Grazette L., Hemmings B., Kass D.A., Champion H.C., and Rosenzweig A. PI3K rescues the detrimental effects of chronic Akt activation in the heart during ischemia/reperfusion injury. J. Clin. Invest. 115 (2005) 2128-2138
28. Nemoto T., Yokoo H., Satoh S., Yanagita T., Sugano T., Yoshikawa N., Maruta T., Kobayashi H., and Wada A. Constitutive activity of glycogen synthase kinase-3β: positive regulation of steady-state levels of insulin receptor substrates-1 and -2 in adrenal chromaffin cells. Brain Res. 1110 (2006) 1-12
29. Nemoto T., Kanai T., Yanagita T., Satoh S., Maruta T., Yoshikawa N., Kobayashi H., and Wada A. Regulation of Akt mRNA and protein levels by glycogen synthase kinase-3β in adrenal chromaffin cells: effects of LiCl and SB216763. Eur. J. Pharmacol. 586 (2008) 82-89
30. Oh J.E., Han J.A., and Hwang E.S. Downregulation of transcription factor, Sp1, during cellular senescence. Biochem. Biophys. Res. Commun. 353 (2007) 86-91
31. Panno M.L., Mauro L., Marsico S., Bellizzi D., Rizza P., Morelli C., Salerno M., Giordano F., and Andò S. Evidence that the mouse insulin receptor substrate-1 belongs to the gene family on which the promoter is activated by estrogen receptor α through its interaction with Sp1. J. Mol. Endocrinol. 36 (2006) 91-105
32. Pratt W.B., Morishima Y., Murphy M., and Harrell M. Chaperoning of glucocorticoid receptors. Handb. Exp. Pharmacol. 172 (2006) 111-138
33. Russo S.J., Bolanos C.A., Theobald D.E., DeCarolis N.A., Renthal W., Kumar A., Winstanley C.A., Renthal N.E., Wiley M.D., Self D.W., Russell D.S., Neve R.L., Eisch A.J., and Nestler E.J. IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat. Neurosci. 10 (2007) 93-99
34. Sadagurski M., Weingarten G., Rhodes C.J., White M.F., and Wertheimer E. Insulin receptor substrate 2 plays diverse cell-specific roles in the regulation of glucose transport. J. Biol. Chem. 280 (2005) 14536-14544
35. Saitoh T., Yanagita T., Shiraishi S., Yokoo H., Kobayashi H., Minami S., Onitsuka T., and Wada A. Down-regulation of cell surface insulin receptor and insulin receptor substrate-1 phosphorylation by inhibitor of 90-kDa heat-shock protein family: endoplasmic reticulum retention of monomeric insulin receptor precursor with calnexin in adrenal chromaffin cells. Mol. Pharmacol. 62 (2002) 847-855
36. Satoh S., Yanagita T., Maruta T., Nemoto T., Yoshikawa N., Kobayashi H., Tono T., and Wada A. Proteasomal degradation of IRS-2, but not IRS-1 by calcineurin inhibition: attenuation of insulin-like growth factor-I-induced GSK-3β and ERK pathways in adrenal chromaffin cells. Neuropharmacology 55 (2008) 71-79
37. Schneider C., Sepp-Lorenzino L., Nimmesgern E., Ouerfelli O., Danishefsky S., Rosen N., and Hartl F.U. Pharmacological shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 14536-14541
38. Schubert M., Brazil D.P., Burks D.J., Kushner J.A., Ye J., Flint C.L., Farhang-Fallah J., Dikkes P., Warot X.M., Rio C., Corfas G., and White M.F. Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 23 (2003) 7084-7092
39. Sesti G., Federici M., Hribal M.L., Lauro D., Sbraccia P., and Lauro R. Defects of the insulin receptor substrate (IRS) system in human metabolic disorders. FASEB J. 15 (2001) 2099-2111
40. Solomon S.S., Majumdar G., Martinez-Hernandez A., and Raghow R. A critical role of Sp1 transcription factor in regulating gene expression in response to insulin and other hormones. Life Sci. 83 (2008) 305-312
41. Sõti C., Nagy E., Giricz Z., Vígh L., Csermely P., and Ferdinandy P. Review. Heat shock proteins as emerging therapeutic targets. Br. J. Pharmacol. 146 (2005) 769-780
42. Su K., Yang X., Roos M.D., Paterson A.J., and Kudlow J.E. Human Sug1/p45 is involved in the proteasome-dependent degradation of Sp1. Biochem. J. 348 (2000) 281-289
43. Sugano T., Yanagita T., Yokoo H., Satoh S., Kobayashi H., and Wada A. Enhancement of insulin-induced PI3K/Akt/GSK-3β and ERK signaling by neuronal nicotinic receptor/PKC-α/ERK pathway: up-regulation of IRS-1/-2 mRNA and protein in adrenal chromaffin cells. J. Neurochem. 98 (2006) 20-33
44. Sun H., Tu X., Prisco M., Wu A., Casiburi I., and Baserga R. Insulin-like growth factor I receptor signaling and nuclear translocation of insulin receptor substrates 1 and 2. Mol. Endocrinol. 17 (2003) 472-486
45. Tago K., Tsukahara F., Naruse M., Yoshioka T., and Takano K. Regulation of nuclear retention of glucocorticoid receptor by nuclear Hsp90. Mol. Cell. Endocrinol. 213 (2004) 131-138
46. Taniguchi C.M., Ueki K., and Kahn C.R. Complementary roles of IRS-1 and IRS-2 in the hepatic regulation of metabolism. J. Clin. Invest. 115 (2005) 718-727 (corrigendum: J. Clin. Invest. 2005. 115, 1388)
47. Terasawa K., Minami M., and Minami Y. Constantly updated knowledge of Hsp90. J. Biochem. 137 (2005) 443-447
48. Tseng Y.-H., Ueki K., Kriauciunas K.M., and Kahn C.R. Differential roles of insulin receptor substrates in the anti-apoptotic function of insulin-like growth factor-1 and insulin. J. Biol. Chem. 277 (2002) 31601-31611
49. Tu X., Batta P., Innocent N., Prisco M., Casaburi I., Belletti B., and Baserga R. Nuclear translocation of insulin receptor substrate-1 by oncogenes and Igf-I. J. Biol. Chem. 277 (2002) 44357-44365
50. Vassen L., Wegrzyn W., and Klein-Hitpass L. Human insulin receptor substrate-2. Gene organization and promoter characterization. Diabetes 48 (1999) 1877-1880
51. Wada A., Yokoo H., Yanagita T., and Kobayashi H. New twist on neuronal insulin receptor signaling in health, disease, and therapeutics. J. Pharmacol. Sci. 99 (2005) 128-143
52. Wada A., Yokoo H., Yanagita T., and Kobayashi H. Lithium: potential therapeutics against acute brain injuries and chronic neurodegenerative diseases. J. Pharmacol. Sci. 99 (2005) 307-321
53. Wada A. Lithium and neuropsychiatric therapeutics: neuroplasticity via glycogen synthase kinase-3β, β-catenin, and neurotrophin cascades. J. Pharmacol. Sci. 110 (2009) 14-28
54. Wang X., Khaleque M.A., Zhao M.J., Zhong R., Gaestel M., and Calderwood S.K. Phosphorylation of HSF1 by MAPK-activated protein kinase 2 on serine 121, inhibits transcriptional activity and promotes HSP90 binding. J. Biol. Chem. 281 (2006) 782-791
55. Wang S.-A., Chuang J.-Y., Yeh S.-H., Wang Y.-T., Liu Y.-W., Chang W.-C., and Hung J.-J. Heat shock protein 90 is important for Sp1 stability during mitosis. J. Mol. Biol. 387 (2009) 1106-1119
56. Wildhage I., Trusheim H., Göke B., and Lankat-Buttgereit B. Gene expression of the human glucagons-like peptide-1 receptor is regulated by Sp1 and Sp3. Endocrinology 140 (1999) 624-631
57. Wu A., Chen J., and Baserga R. Nuclear insulin receptor substrate-1 activates promoters of cell cycle progression genes. Oncogene 27 (2008) 397-403
58. Yamamoto R., Yanagita T., Kobayashi H., Yuhi T., Yokoo H., and Wada A. Up-regulation of functional voltage-dependent sodium channels by insulin in cultured bovine adrenal chromaffin cells. J. Neurochem. 67 (1996) 1401-1408
59. Yamamoto R., Kobayashi H., Yanagita T., Yokoo H., Kurose T., Shiraishi S., Minami S., Matsukura S., and Wada A. Up-regulation of cell surface insulin receptor by protein kinase C-α in adrenal chromaffin cells: involvement of transcriptional and translational events. J. Neurochem. 75 (2000) 672-682
60. Yi X., Schubert M., Peachey N.S., Suzuma K., Burks D.J., Kushner J.A., Suzuma I., Cahill C., Flint C.L., Dow M.A., Leshan R.L., King G.L., and White M.F. Insulin receptor substrate 2 is essential for maturation and survival of photoreceptor cells. J. Neurosci. 25 (2005) 1240-1248