A novel mTOR activating protein protects dopamine neurons against oxidative stress by repressing autophagy related cell death

Journal of Neurochemistry

Volumn 112, Issue 2, 2010, Pages 366-376

  Choi, Kyou Chan ^a   Kim, Shin Hee ^a   Ha, Ji Young ^a   Kim, Sang Tae ^a   Son, Jin H ^a  

^a Ewha Womans University   (South Korea)

Author keywords

Autophagy; Cell death; Dopamine neuron; MTOR; Protection

Indexed keywords

3 METHYLADENINE; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; OXI ALPHA PROTEIN; PROTEIN; RAPAMYCIN; S6 KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DEATH; CELL PROTECTION; CELL VACUOLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHYLOGENY; PRIORITY JOURNAL;

ANIMALS; AUTOPHAGY; CARRIER PROTEINS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; DOPAMINE; DOWN-REGULATION; GREEN FLUORESCENT PROTEINS; HYDROGEN PEROXIDE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICROSCOPY, CONFOCAL; NEUROBLASTOMA; NEURONS; OXIDATIVE STRESS; PHOSPHOPROTEINS; PHYLOGENY; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; TRANSFECTION;

MAMMALIA;

EID: 72849127046     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06463.x     Document Type: Article

References (59)

1. Andersen J. K. (2004) Oxidative stress in neurodegeneration: cause or consequence? Nat. Med. 10 (Suppl S18 S25.
2. Anglade P., Vyas S., Javoy-Agid F., Herrero M. T., Michel P. P., Marquez J., Mouatt-Prigent A., Ruberg M., Hirsch E. C. Agid Y. (1997) Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol. 12, 25 31.
3. Asanuma M., Miyazaki I. Ogawa N. (2003) Dopamine- or L-DOPA-induced neurotoxicity: the role of dopamine quinone formation and tyrosinase in a model of Parkinson's disease. Neurotox. Res. 5, 165 176.
4. Basma A. N., Morris E. J., Nicklas W. J. Geller H. M. (1995) L-dopa cytotoxicity to PC12 cells in culture is via its autoxidation. J. Neurochem. 64, 825 832.
5. Biewenga E., Cabell L. Audesirk T. (2005) Estradiol and raloxifene protect cultured SN4741 neurons against oxidative stress. Neurosci. Lett. 373, 179 183.
6. Blommaart E. F., Luiken J. J., Blommaart P. J., van Woerkom G. M. Meijer A. J. (1995) Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes. J. Biol. Chem. 270, 2320 2326.
7. Blum D., Torch S., Lambeng N., Nissou M., Benabid A. L., Sadoul R. Verna J. M. (2001) Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog. Neurobiol. 65, 135 172.
8. Chu C. T. (2006) Autophagic stress in neuronal injury and disease. J. Neuropathol. Exp. Neurol. 65, 423 432.
9. Chun H. S., Gibson G. E., DeGiorgio L. A., Zhang H., Kidd V. J. Son J. H. (2001a) Dopaminergic cell death induced by MPP(+), oxidant and specific neurotoxicants shares the common molecular mechanism. J. Neurochem. 76, 1010 1021.
10. Chun H. S., Lee H. Son J. H. (2001b) Manganese induces endoplasmic reticulum (ER) stress and activates multiple caspases in nigral dopaminergic neuronal cells, SN4741. Neurosci. Lett. 316, 5 8.
11. Codogno P. Meijer A. J. (2005) Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 12 (Suppl 2 1509 1518.
12. Dagda R. K., Cherra S. J. III., Kulich S. M., Tandon A., Park D. Chu C. T. (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 284, 13843 13855.
13. Dann S. G. Thomas G. (2006) The amino acid sensitive TOR pathway from yeast to mammals. FEBS Lett. 580, 2821 2829.
14. Dexter D. T., Carter C. J., Wells F. R., Javoy-Agid F., Agid Y., Lees A., Jenner P. Marsden C. D. (1989) Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem. 52, 381 389.
15. Dexter D. T., Holley A. E., Flitter W. D., Slater T. F., Wells F. R., Daniel S. E., Lees A. J., Jenner P. Marsden C. D. (1994) Increased levels of lipid hydroperoxides in the parkinsonian substantia nigra: an HPLC and ESR study. Mov. Disord. 9, 92 97.
16. Engelhardt J. F. (1999) Redox-mediated gene therapies for environmental injury: approaches and concepts. Antioxid. Redox Signal. 1, 5 27.
17. Fang Y., Vilella-Bach M., Bachmann R., Flanigan A. Chen J. (2001) Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294, 1942 1945.
18. Feng Z., Zhang H., Levine A. J. Jin S. (2005) The coordinate regulation of the p53 and mTOR pathways in cells. Proc. Natl Acad. Sci. USA 102, 8204 8209.
19. Gomez-Santos C., Ferrer I., Santidrian A. F., Barrachina M., Gil J. Ambrosio S. (2003) Dopamine induces autophagic cell death and alpha-synuclein increase in human neuroblastoma SH-SY5Y cells. J. Neurosci. Res. 73, 341 350.
20. Gonzalez-Polo R. A., Niso-Santano M., Ortiz-Ortiz M. A., Gomez-Martin A., Moran J. M., Garcia-Rubio L., Francisco-Morcillo J., Zaragoza C., Soler G. Fuentes J. M. (2007) Inhibition of paraquat-induced autophagy accelerates the apoptotic cell death in neuroblastoma SH-SY5Y cells. Toxicol. Sci. 97, 448 458.
21. Hara K., Maruki Y., Long X., Yoshino K., Oshiro N., Hidayat S., Tokunaga C., Avruch J. Yonezawa K. (2002) Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110, 177 189.
22. Hartmann A., Hunot S., Michel P. P. et al. (2000) Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc. Natl Acad. Sci. USA 97, 2875 2880.
23. Horrevoets A. J., Fontijn R. D., van Zonneveld A. J., de Vries C. J., ten Cate J. W. Pannekoek H. (1999) Vascular endothelial genes that are responsive to tumor necrosis factor-alpha in vitro are expressed in atherosclerotic lesions, including inhibitor of apoptosis protein-1, stannin, and two novel genes. Blood 93, 3418 3431.
24. Hoyer-Hansen M., Bastholm L., Szyniarowski P. et al. (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25, 193 205.
25. Inoki K., Corradetti M. N. Guan K. L. (2005) Dysregulation of the TSC-mTOR pathway in human disease. Nat. Genet. 37, 19 24.
26. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y. Yoshimori T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720 5728.
27. Kim D. H., Sarbassov D. D., Ali S. M., King J. E., Latek R. R., Erdjument-Bromage H., Tempst P. Sabatini D. M. (2002) mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110, 163 175.
28. Kim D. H., Sarbassov D. D., Ali S. M., Latek R. R., Guntur K. V., Erdjument-Bromage H., Tempst P. Sabatini D. M. (2003) GbetaL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11, 895 904.
29. Kroemer G., El-Deiry W. S., Golstein P. et al. (2005) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ. 12 (Suppl 2 1463 1467.
30. Kuan C. Y. Burke R. E. (2005) Targeting the JNK signaling pathway for stroke and Parkinson's diseases therapy. Curr. Drug Targets CNS Neurol. Disord. 4, 63 67.
31. Kumar R., Agarwal A. K. Seth P. K. (1995) Free radical-generated neurotoxicity of 6-hydroxydopamine. J. Neurochem. 64, 1703 1707.
32. Larsen K. E., Fon E. A., Hastings T. G., Edwards R. H. Sulzer D. (2002) Methamphetamine-induced degeneration of dopaminergic neurons involves autophagy and upregulation of dopamine synthesis. J. Neurosci. 22, 8951 8960.
33. Lee S. J., Kim D. C., Choi B. H., Ha H. Kim K. T. (2006) Regulation of p53 by activated protein kinase C-delta during nitric oxide-induced dopaminergic cell death. J. Biol. Chem. 281, 2215 2224.
34. Lee C. H., Inoki K. Guan K. L. (2007) mTOR pathway as a target in tissue hypertrophy. Annu. Rev. Pharmacol. Toxicol. 47, 443 467.
35. Lein E. S., Hawrylycz M. J., Ao N. et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168 176.
36. Malagelada C., Ryu E. J., Biswas S. C., Jackson-Lewis V. Greene L. A. (2006) RTP801 is elevated in Parkinson brain substantia nigral neurons and mediates death in cellular models of Parkinson's disease by a mechanism involving mammalian target of rapamycin inactivation. J. Neurosci. 26, 9996 10005.
37. Miller R. M. Federoff H. J. (2005) Altered gene expression profiles reveal similarities and differences between Parkinson disease and model systems. Neuroscientist 11, 539 549.
38. Mizushima N., Yamamoto A., Matsui M., Yoshimori T. Ohsumi Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101 1111.
39. Muller T., Hefter H., Hueber R., Jost W. H., Leenders K. L., Odin P. Schwarz J. (2004) Is levodopa toxic? J. Neurol. 251 (Suppl 6 VI44 VI46.
40. Mytilineou C., Walker R. H., JnoBaptiste R. Olanow C. W. (2003) Levodopa is toxic to dopamine neurons in an in vitro but not an in vivo model of oxidative stress. J. Pharmacol. Exp. Ther. 304, 792 800.
41. Nair V. D., Olanow C. W. Sealfon S. C. (2003) Activation of phosphoinositide 3-kinase by D2 receptor prevents apoptosis in dopaminergic cell lines. Biochem. J. 373, 25 32.
42. Nair V. D., Yuen T., Olanow C. W. Sealfon S. C. (2004) Early single cell bifurcation of pro- and antiapoptotic states during oxidative stress. J. Biol. Chem. 279, 27494 27501.
43. Pan T., Kondo S., Zhu W., Xie W., Jankovic J. Le W. (2008) Neuroprotection of rapamycin in lactacystin-induced neurodegeneration via autophagy enhancement. Neurobiol. Dis. 32, 16 25.
44. Patel S., Wang F. H., Whiteside T. L. Kasid U. (1997) Identification of seven differentially displayed transcripts in human primary and matched metastatic head and neck squamous cell carcinoma cell lines: implications in metastasis andor radiation response. Oral Oncol. 33, 197 203.
45. Peng J., Mao X. O., Stevenson F. F., Hsu M. Andersen J. K. (2004) The herbicide paraquat induces dopaminergic nigral apoptosis through sustained activation of the JNK pathway. J. Biol. Chem. 279, 32626 32632.
46. Sarbassov D. D. Sabatini D. M. (2005) Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex. J. Biol. Chem. 280, 39505 39509.
47. Sarkar S., Davies J. E., Huang Z., Tunnacliffe A. Rubinsztein D. C. (2007) Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J. Biol. Chem. 282, 5641 5652.
48. Sherer T. B., Betarbet R., Stout A. K., Lund S., Baptista M., Panov A. V., Cookson M. R. Greenamyre J. T. (2002) An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered alpha-synuclein metabolism and oxidative damage. J. Neurosci. 22, 7006 7015.
49. Son J. H., Chun H. S., Joh T. H., Cho S., Conti B. Lee J. W. (1999) Neuroprotection and neuronal differentiation studies using substantia nigra dopaminergic cells derived from transgenic mouse embryos. J. Neurosci. 19, 10 20.
50. Sriram K., Pai K. S., Boyd M. R. Ravindranath V. (1997) Evidence for generation of oxidative stress in brain by MPTP: in vitro and in vivo studies in mice. Brain Res. 749, 44 52.
51. Steece-Collier K., Collier T. J., Sladek C. D. Sladek J. R. Jr. (1990) Chronic levodopa impairs morphological development of grafted embryonic dopamine neurons. Exp. Neurol. 110, 201 208.
52. Stefanis L., Larsen K. E., Rideout H. J., Sulzer D. Greene L. A. (2001) Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci. 21, 9549 9560.
53. Tatton N. A., Maclean-Fraser A., Tatton W. G., Perl D. P. Olanow C. W. (1998) A fluorescent double-labeling method to detect and confirm apoptotic nuclei in Parkinson's disease. Ann. Neurol. 44, S142 S148.
54. The Parkinson's study group (1993) Effects of tocopherol and deprenyl on the progression of disability in early Parkinson's disease. The Parkinson Study Group. N. Engl. J. Med. 328, 176 183.
55. Thiruchelvam M., Richfield E. K., Baggs R. B., Tank A. W. Cory-Slechta D. A. (2000) The nigrostriatal dopaminergic system as a preferential target of repeated exposures to combined paraquat and maneb: implications for Parkinson's disease. J. Neurosci. 20, 9207 9214. (Pubitemid 32042923)
56. Yoo M. S., Kawamata H., Kim D. J., Chun H. S. Son J. H. (2004) Experimental strategy to identify genes susceptible to oxidative stress in nigral dopaminergic neurons. Neurochem. Res. 29, 1223 1234.
57. Yoritaka A., Hattori N., Uchida K., Tanaka M., Stadtman E. R. Mizuno Y. (1996) Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl Acad. Sci. USA 93, 2696 2701.
58. Zhang J., Perry G., Smith M. A., Robertson D., Olson S. J., Graham D. G. Montine T. J. (1999) Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol. 154, 1423 1429.
59. Zhu J. H., Horbinski C., Guo F., Watkins S., Uchiyama Y. Chu C. T. (2007) Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am. J. Pathol. 170, 75 86.