IGF-1 Alleviates NMDA-Induced Excitotoxicity in Cultured Hippocampal Neurons Against Autophagy via the NR2B/PI3K-AKT-mTOR Pathway

Journal of Cellular Physiology

Volumn 229, Issue 11, 2014, Pages 1618-1629

  Wang, Yansong ^a,b   Wang, Wei ^c   Li, Dongguo ^a,c   Li, Mi ^b   Wang, Peipei ^a   Wen, Jian ^b   Liang, Min ^b   Su, Bo ^b   Yin, Yanling ^a  

^a BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

^b HARBIN MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; CASPASE 3; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASSAY; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CELL LYSATE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CELL ULTRASTRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; IMMUNOBLOTTING; LACTATE DEHYDROGENASE ASSAY; LIGHT CHAIN; LYSOSOME; MACROAUTOPHAGY; MTT ASSAY; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CASPASE 3; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR I; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; N-METHYLASPARTATE; NEURONS; NEUROTOXINS; PHAGOSOMES; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PHOSPHOSERINE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SYNAPSES; TOR SERINE-THREONINE KINASES;

EID: 84904858375     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24607     Document Type: Article

References (51)

1. Baehrecke EH. 2005. Autophagy: Dual roles in life and death? Nat Rev Mol Cell Biol 6:505-510.
2. Bitto A, Lerner C, Torres C, Roell M, Malaguti M, Perez V, Lorenzini A, Hrelia S, Ikeno Y, Matzko ME, McCarter R, Sell C. 2010. Long-term IGF-I exposure decreases autophagy and cell viability. PLoS ONE 5:e12592.
3. Chang HC, Yang YR, Wang PS, Kuo CH, Wang RY. 2013. The neuroprotective effects of intramuscular insulin-like growth factor-I treatment in brain ischemic rats. PLoS ONE 8:e64015.
4. Chen BS, Roche KW. 2009. Growth factor-dependent trafficking of cerebellar NMDA receptors via protein kinase B/Akt phosphorylation of NR2C. Neuron 62:471-478.
5. Daido S, Kanzawa T, Yamamoto A, Takeuchi H, Kondo Y, Kondo S. 2004. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res 64:4286-4293.
6. Ferraro E, Cecconi F. 2007. Autophagic and apoptotic response to stress signals in mammalian cells. Arch Biochem Biophys 462:210-219.
7. Gao L, Jiang T, Guo J, Liu Y, Cui G, Gu L, Su L, Zhang Y. 2012. Inhibition of autophagy contributes to ischemic postconditioning-induced neuroprotection against focal cerebral ischemia in rats. PLoS ONE 7:e46092.
8. Garcia-Arencibia M, Hochfeld WE, Toh PP, Rubinsztein DC. 2010. Autophagy, a guardian against neurodegeneration. Semin Cell Dev Biol 21:691-698.
9. Gasparini F, DI PT, Gomez-Mancilla B. 2013. Metabotropic glutamate receptors for Parkinson's disease therapy. Parkinsons Dis 2013:196028.
10. Gerkin RC, Lau PM, Nauen DW, Wang YT, Bi GQ. 2007. Modular competition driven by NMDA receptor subtypes in spike-timing-dependent plasticity. J Neurophysiol 97:2851-2862.
11. Greenamyre JT, Porter RH. 1994. Anatomy and physiology of glutamate in the CNS. Neurology 44:S7-S13.
12. Guan J. 2008. Insulin-like growth factor-1 and its derivatives: potential pharmaceutical application for ischemic brain injury. Recent Pat CNS Drug Discov 3:112-127.
13. Guan J, Bennet L, Gluckman PD, Gunn AJ. 2003. Insulin-like growth factor-1 and post-ischemic brain injury. Prog Neurobiol 70:443-462.
14. Hori Y, Endo K. 1992. Miniature postsynaptic currents recorded from identified rat spinal dorsal horn projection neurons in thin-slice preparations. Neurosci Lett 142:191-195.
15. Jennings JS, Gerber AM, Vallano ML. 2008. Pharmacological strategies for neuroprotection in traumatic brain injury. Mini Rev Med Chem 8:689-701.
16. Jia G, Cheng G, Gangahar DM, Agrawal DK. 2006. Insulin-like growth factor-1 and TNF-alpha regulate autophagy through c-jun N-terminal kinase and Akt pathways in human atherosclerotic vascular smooth cells. Immunol Cell Biol 84:448-454.
17. Kalb RG. 1994. Regulation of motor neuron dendrite growth by NMDA receptor activation. Development 120:3063-3071.
18. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. 2004. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ 11:448-457.
19. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K. 2006. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880-884.
20. Kroemer G, Marino G, Levine B. 2010. Autophagy and the integrated stress response. Mol Cell 40:280-293.
21. Kuma A, Matsui M, Mizushima N. 2007. LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: Caution in the interpretation of LC3 localization. Autophagy 3:323-328.
22. Lai TW, Shyu WC, Wang YT. 2011. Stroke intervention pathways: NMDA receptors and beyond. Trends Mol Med 17:266-275.
23. Lee SJ, Koh JY. 2010. Roles of zinc and metallothionein-3 in oxidative stress-induced lysosomal dysfunction, cell death, and autophagy in neurons and astrocytes. Mol Brain 3:30.
24. Liu SB, Zhao MG. 2013. Neuroprotective effect of estrogen: Role of nonsynaptic NR2B-containing NMDA receptors. Brain Res Bull 93:27-31.
25. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, Thompson CB. 2005. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237-248.
26. Luo L, Lu AM, Wang Y, Hong A, Chen Y, Hu J, Li X, Qin ZH. 2013. Chronic resistance training activates autophagy and reduces apoptosis of muscle cells by modulating IGF-1 and its receptors, Akt/mTOR and Akt/FOXO3a signaling in aged rats. Exp Gerontol 48:427-436.
27. Martin ED, Sanchez-Perez A, Trejo JL, Martin-Aldana JA, Cano JM, Pons S, Acosta UC, Menes L, White MF, Burks DJ. 2012. IRS-2 deficiency impairs NMDA receptor-dependent long-term potentiation. Cereb Cortex 22:1717-1727.
28. Miltiadous P, Stamatakis A, Stylianopoulou F. 2010. Neuroprotective effects of IGF-I following kainic acid-induced hippocampal degeneration in the rat. Cell Mol Neurobiol 30:347-360.
29. Mizushima N, Komatsu M. 2011. Autophagy: Renovation of cells and tissues. Cell 147:728-741.
30. Mizushima N, Yoshimori T. 2007. How to interpret LC3 immunoblotting. Autophagy 3:542-545.
31. Nencioni A, Cea M, Montecucco F, Longo VD, Patrone F, Carella AM, Holyoake TL, Helgason GV. 2013. Autophagy in blood cancers: Biological role and therapeutic implications. Haematologica 98:1335-1343.
32. Oldham S, Hafen E. 2003. Insulin/IGF and target of rapamycin signaling: A TOR de force in growth control. Trends Cell Biol 13:79-85.
33. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, Domingo D, Yahalom J. 2001. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 61:439-444.
34. Pan W, Kastin AJ. 2000. Interactions of IGF-1 with the blood-brain barrier in vivo and in situ. Neuroendocrinology 72:171-178.
35. Sadasivan S, Zhang Z, Larner SF, Liu MC, Zheng W, Kobeissy FH, Hayes RL, Wang KK. 2010. Acute NMDA toxicity in cultured rat cerebellar granule neurons is accompanied by autophagy induction and late onset autophagic cell death phenotype. BMC Neurosci 11:21.
36. Shehata M, Matsumura H, Okubo-Suzuki R, Ohkawa N, Inokuchi K. 2012. Neuronal stimulation induces autophagy in hippocampal neurons that is involved in AMPA receptor degradation after chemical long-term depression. J Neurosci 32:10413-10422.
37. Shi R, Weng J, Zhao L, Li XM, Gao TM, Kong J. 2012. Excessive autophagy contributes to neuron death in cerebral ischemia. CNS Neurosci Ther 18:250-260.
38. Snyder MA, Cooke BM, Woolley CS. 2011. Estradiol potentiation of NR2B-dependent EPSCs is not due to changes in NR2B protein expression or phosphorylation. Hippocampus 21:398-408.
39. Sun C, Wang D, Zheng W. 2012. Hydrogen peroxide attenuates the prosurvival signaling of insulin-like growth factor-1 through two pathways. Neuroreport 23:768-773.
40. Sun XJ, Rothenberg P, Kahn CR, Backer JM, Araki E, Wilden PA, Cahill DA, Goldstein BJ, White MF. 1991. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352:73-77.
41. Talloczy Z, Jiang W, Virgin HW, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B. 2002. Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci USA 99:190-195.
42. Troncoso R, Vicencio JM, Parra V, Nemchenko A, Kawashima Y, Del CA, Toro B, Battiprolu PK, Aranguiz P, Chiong M, Yakar S, Gillette TG, Hill JA, Abel ED, Leroith D, Lavandero S. 2012. Energy-preserving effects of IGF-1 antagonize starvation-induced cardiac autophagy. Cardiovasc Res 93:320-329.
43. Troncoso R, az-Elizondo J, Espinoza SP, Navarro-Marquez MF, Oyarzun AP, Riquelme JA, Garcia-Carvajal I, az-Araya G, Garcia L, Hill JA, Lavandero S. 2013. Regulation of cardiac autophagy by insulin-like growth factor 1. IUBMB Life 65:593-601.
44. Wardas J, Pietraszek M, Wolfarth S, Ossowska K. 2003. The role of metabotropic glutamate receptors in regulation of striatal proenkephalin expression: Implications for the therapy of Parkinson's disease. Neuroscience 122:747-756.
45. Xing C, Yin Y, Chang R, He X, Xie Z. 2005. A role of insulin-like growth factor 1 in beta amyloid-induced disinhibition of hippocampal neurons. Neurosci Lett 384:93-97.
46. Yin Y, Wang Y, Chen L, Han S, Zhao L, Luo Y, Li J. 2013. Tat-collapsin response mediator protein 2 (CRMP2) increases the survival of neurons after NMDA excitotoxity by reducing the cleavage of CRMP2. Neurochem Res 38:2095-2104.
47. Yu L, Alva A, Su H, Dutt P, Freundt E, Welsh S, Baehrecke EH, Lenardo MJ. 2004. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304:1500-1502.
48. Yue Z, Friedman L, Komatsu M, Tanaka K. Biochim Biophys Acta 1793:1496-1507.
49. Zelinka CP, Scott MA, Volkov L, Fischer AJ. 2012. The reactivity, distribution and abundance of non-astrocytic inner retinal glial (NIRG) cells are regulated by microglia, acute damage, and IGF1. PLoS ONE 7:e44477.
50. Zhang B, Shozu M, Okada M, Ishikawa H, Kasai T, Murakami K, Nomura K, Harada N, Inoue M. 2010. Insulin-like growth factor I enhances the expression of aromatase P450 by inhibiting autophagy. Endocrinology 151:4949-4958.
51. Zhang X, Yan H, Yuan Y, Gao J, Shen Z, Cheng Y, Shen Y, Wang RR, Wang X, Hu WW, Wang G, Chen Z. 2013. Cerebral ischemia-reperfusion-induced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy 9.