Insulin-Like Growth Factor-1 Inhibits 6-Hydroxydopamine-Mediated Endoplasmic Reticulum Stress-Induced Apoptosis via Regulation of Heme Oxygenase-1 and Nrf2 Expression in PC12 Cells

REFERENCES

• Feldman EL, Sullivan KA, Kim B, Russell JW. Insulin-like growth factors regulate neuronal differentiation and survival. Neurobiol Dis. 1997;4:201–14.
   PubMed Web of Science ®Google Scholar
• LeRoith D, Werner H, Beitner-Johnson D, Roberts CT Jr. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev. 1995;16:143–63.
   PubMed Web of Science ®Google Scholar
• Quesada A, Romeo HE, Micevych P. Distribution and localization patterns of estrogen receptor-beta and insulin-like growth factor-1 receptors in neurons and glial cells of the female rat substantia nigra: localization of ERbeta and IGF-1R in substantia nigra. J Comp Neurol. 2007 July 1;503:198–208.
   PubMed Web of Science ®Google Scholar
• Offen D, Shtaif B, Hadad D, Weizman A, Melamed E, Gil-Ad I. Protective effect of insulin-like-growth-factor-1 against dopamine-induced neurotoxicity in human and rodent neuronal cultures: possible implications for Parkinson's disease. Neurosci Lett. 2001 Dec 28;316:129–32.
   PubMed Web of Science ®Google Scholar
• Parrizas M, Saltiel AR, LeRoith D. Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3’-kinase and mitogen-activated protein kinase pathways. J Biol Chem. 1997 Jan 3;272:154–61.
   PubMed Web of Science ®Google Scholar
• Russell JW, Windebank AJ, Schenone A, Feldman EL. Insulin-like growth factor-I prevents apoptosis in neurons after nerve growth factor withdrawal. J Neurobiol. 1998 Sep 15;36:455–67.
   PubMedGoogle Scholar
• Takadera T, Matsuda I, Ohyashiki T. Apoptotic cell death and caspase-3 activation induced by N-methyl-D-aspartate receptor antagonists and their prevention by insulin-like growth factor I. J Neurochem. 1999;73:548–56.
   PubMed Web of Science ®Google Scholar
• Zou CG, Cao XZ, Zhao YS, Gao SY, Li SD, Liu XY, Zhang Y, Zhang KQ. The molecular mechanism of endoplasmic reticulum stress-induced apoptosis in PC-12 neuronal cells: the protective effect of insulin-like growth factor I. Endocrinology. 2009;150:277–85.
   PubMed Web of Science ®Google Scholar
• Sun X, Huang L, Zhang M, Sun S, Wu Y. Insulin like growth factor-1 prevents 1-mentyl-4-phenylphyridinium-induced apoptosis in PC12 cells through activation of glycogen synthase kinase-3beta. Toxicology. 2010 April 30;271:5–12.
   PubMed Web of Science ®Google Scholar
• Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 5-15-1999;13:1211–33.
   PubMed Web of Science ®Google Scholar
• Oyadomari S, Araki E, Mori M. Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis. 2002;7:335–45.
   PubMed Web of Science ®Google Scholar
• Ryu EJ, Harding HP, Angelastro JM, Vitolo OV, Ron D, Greene LA. Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J Neurosci. 2002 Dec 15;22:10690–98.
   Web of Science ®Google Scholar
• Carman LS, Gage FH, Shults CW. Partial lesion of the substantia nigra: relation between extent of lesion and rotational behavior. Brain Res. 7-12-1991;553:275–83.
   PubMed Web of Science ®Google Scholar
• Chen G, Bower KA, Ma C, Fang S, Thiele CJ, Luo J. Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J. 2004;18:1162–64.
   Web of Science ®Google Scholar
• Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976;73:2424–28.
   Web of Science ®Google Scholar
• Zhu TG, Wang XX, Luo WF, Zhang QL, Huang TT, Xu XS, Liu CF. Protective effects of urate against 6-OHDA-induced cell injury in PC12 cells through antioxidant action. Neurosci Lett. 2012 Jan 11;506:175–79.
   Web of Science ®Google Scholar
• Tao L, Li X, Zhang L, Tian J, Li X, Sun X, Li X, Jiang L, Zhang X, Chen J. Protective effect of tetrahydroxystilbene glucoside on 6-OHDA-induced apoptosis in PC12 cells through the ROS-NO pathway. PLoS One. 2011;6:e26055.
   PubMed Web of Science ®Google Scholar
• Li Z, Hu Y, Zhu Q, Zhu J. Neurotrophin-3 reduces apoptosis induced by 6-OHDA in PC12 cells through Akt signaling pathway. Int J Dev Neurosci. 2008;26:635–40.
   PubMed Web of Science ®Google Scholar
• Kang KW, Lee SJ, Kim SG. Molecular mechanism of nrf2 activation by oxidative stress. Antioxid Redox Signal. 2005;7:1664–73.
   PubMed Web of Science ®Google Scholar
• Motterlini R, Green CJ, Foresti R. Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid Redox Signal. 2002;4:615–24.
   PubMed Web of Science ®Google Scholar
• Kirkby KA, Adin CA. Products of heme oxygenase and their potential therapeutic applications. Am J Physiol Renal Physiol. 2006;290:F563–71.
   PubMed Web of Science ®Google Scholar
• Chen YR, Wang X, Templeton D, Davis RJ, Tan TH. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation. Duration of JNK activation may determine cell death and proliferation. J Biol Chem. 1996 Dec 13;271:31929–36.
   PubMed Web of Science ®Google Scholar
• Jiang X, Mu D, Manabat C, Koshy AA, Christen S, Tauber MG, Vexler ZS, Ferriero DM. Differential vulnerability of immature murine neurons to oxygen-glucose deprivation. Exp Neurol. 2004;190:224–32.
   PubMed Web of Science ®Google Scholar
• Walkinshaw G, Waters CM. Neurotoxin-induced cell death in neuronal PC12 cells is mediated by induction of apoptosis. Neuroscience. 1994;63:975–87.
   PubMed Web of Science ®Google Scholar
• Salinas M, Diaz R, Abraham NG, Ruiz de Galarreta CM, Cuadrado A. Nerve growth factor protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a phosphatidylinositol 3-kinase-dependent manner. J Biol Chem. 2003 April 18;278:13898–904.
   PubMed Web of Science ®Google Scholar
• Higashi Y, Sukhanov S, Anwar A, Shai SY, Delafontaine P. IGF-1, oxidative stress and atheroprotection. Trends Endocrinol Metab. 2010;21:245–54.
   PubMed Web of Science ®Google Scholar
• Lee C, Park GH, Jang JH. Cellular antioxidant adaptive survival response to 6-hydroxydopamine-induced nitrosative cell death in C6 glioma cells. Toxicology. 2011 May 10;283:118–28.
   PubMed Web of Science ®Google Scholar
• Russo VC, Gluckman PD, Feldman EL, Werther GA. The insulin-like growth factor system and its pleiotropic functions in brain. Endocr Rev. 2005;26:916–43.
   PubMed Web of Science ®Google Scholar
• Chung H, Seo S, Moon M, Park S. IGF-I inhibition of apoptosis is associated with decreased expression of prostate apoptosis response-4. J Endocrinol. 2007;194:77–85.
   PubMed Web of Science ®Google Scholar
• Kurmasheva RT, Houghton PJ. IGF-I mediated survival pathways in normal and malignant cells. Biochim Biophys Acta. 2006;1766:1–22.
   PubMed Web of Science ®Google Scholar
• Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, Rakic P, Flavell RA. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell. 1998 Aug 7;94:325–37.
   PubMed Web of Science ®Google Scholar
• Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997 Nov 14;91:479–89.
   PubMed Web of Science ®Google Scholar
• Yoshida H, Kong YY, Yoshida R, Elia AJ, Hakem A, Hakem R, Penninger JM, Mak TW. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell. 1998 Sep 18;94:739–50.
   PubMed Web of Science ®Google Scholar
• Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 1997 Aug 8;90:405–13.
   PubMed Web of Science ®Google Scholar
• Dodel RC, Du Y, Bales KR, Ling Z, Carvey PM, Paul SM. Caspase-3-like proteases and 6-hydroxydopamine induced neuronal cell death. Brain Res Mol Brain Res. 1999 Jan 22;64:141–48.
   Google Scholar
• Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson NE, Poirier GG. Specific proteolytic cleavage of poly (ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 1993 Sep 1;53:3976–85.
   PubMed Web of Science ®Google Scholar
• Cheng B, Maffi SK, Martinez AA, Acosta YP, Morales LD, Roberts JL. Insulin-like growth factor-I mediates neuroprotection in proteasome inhibition-induced cytotoxicity in SH-SY5Y cells. Mol Cell Neurosci. 2011;47:181–90.
   PubMed Web of Science ®Google Scholar
• Leinninger GM, Russell JW, Van Golen CM, Berent A, Feldman EL. Insulin-like growth factor-I regulates glucose-induced mitochondrial depolarization and apoptosis in human neuroblastoma. Cell Death Differ. 2004;11:885–96.
   PubMed Web of Science ®Google Scholar
• Novosyadlyy R, Kurshan N, Lann D, Vijayakumar A, Yakar S, LeRoith D. Insulin-like growth factor-I protects cells from ER stress-induced apoptosis via enhancement of the adaptive capacity of endoplasmic reticulum. Cell Death Differ. 2008;15:1304–17.
   PubMed Web of Science ®Google Scholar
• Cunha DA, Ladriere L, Ortis F, Igoillo-Esteve M, Gurzov EN, Lupi R, Marchetti P, Eizirik DL, Cnop M. Glucagon-like peptide-1 agonists protect pancreatic beta-cells from lipotoxic endoplasmic reticulum stress through upregulation of BiP and JunB. Diabetes. 2009;58:2851–62.
   PubMed Web of Science ®Google Scholar
• Fleury C, Mignotte B, Vayssiere JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie. 2002;84: 131–41.
   PubMed Web of Science ®Google Scholar
• Kajstura J, Fiordaliso F, Andreoli AM, Li B, Chimenti S, Medow MS, Limana F, Nadal-Ginard B, Leri A, Anversa P. IGF-1 overexpression inhibits the development of diabetic cardiomyopathy and angiotensin II-mediated oxidative stress. Diabetes. 2001;50:1414–24.
   PubMed Web of Science ®Google Scholar
• Gustafsson H, Soderdahl T, Jonsson G, Bratteng JO, Forsby A. Insulin-like growth factor type 1 prevents hyperglycemia-induced uncoupling protein 3 down-regulation and oxidative stress. J Neurosci Res. 2004 July 15;77:285–91.
   PubMed Web of Science ®Google Scholar
• Pi Y, Goldenthal MJ, Marin-Garcia J. Mitochondrial involvement in IGF-1 induced protection of cardiomyocytes against hypoxia/reoxygenation injury. Mol Cell Biochem. 2007;301:181–89.
   Web of Science ®Google Scholar
• Pugazhenthi S, Miller E, Sable C, Young P, Heidenreich KA, Boxer LM, Reusch JE. Insulin-like growth factor-I induces bcl-2 promoter through the transcription factor cAMP-response element-binding protein. J Biol Chem. 1999 Sep 24;274:27529–35.
   PubMed Web of Science ®Google Scholar
• Sidoti-de FC, Rincheval V, Risler Y, Mignotte B, Vayssiere JL. TNF-alpha activates at least two apoptotic signaling cascades. Oncogene. 1998 Oct 1;17:1639–51.
   PubMed Web of Science ®Google Scholar
• Baek D, Nam J, Koo YD, Kim DH, Lee J, Jeong JC, Kwak SS, Chung WS, Lim CO, Bahk JD, Hong JC, Lee SY, Kawai-Yamada M, Uchimiya H, Yun DJ. Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and -independent processes. Plant Mol Biol. 2004;56:15–27.
   PubMed Web of Science ®Google Scholar
• Sarfstein R, Werner H. The WT1 Wilms’ tumor suppressor gene is a downstream target for insulin-like growth factor-I (IGF-I) action in PC12 cells. J Neurochem. 2006;99:818–26.
   PubMed Web of Science ®Google Scholar
• Carro E, Nunez A, Busiguina S, Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci. 2000 April 15;20:2926–33.
   PubMed Web of Science ®Google Scholar
• Pan W, Kastin AJ. Interactions of IGF-1 with the blood-brain barrier in vivo and in situ. Neuroendocrinology. 2000;72:171–78.
   Web of Science ®Google Scholar
• Reinhardt RR, Bondy CA. Insulin-like growth factors cross the blood-brain barrier. Endocrinology. 1994;135:1753–61.
   PubMed Web of Science ®Google Scholar