Rotenone impairs autophagic flux and lysosomal functions in Parkinson's disease

Neuroscience

Volumn 284, Issue , 2015, Pages 900-911

  Wu, F ^a,b   Xu, H D ^a   Guan, J J ^a   Hou, Y S ^a   Gu, J H ^b   Zhen, X C ^a   Qin, Z H ^a  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

Author keywords

Autophagic flux; Lysosomal membrane permeability; Parkinson's disease; Rotenone; synuclein

Indexed keywords

ALPHA SYNUCLEIN; BECLIN 1; CATHEPSIN D; MICROTUBULE ASSOCIATED PROTEIN 1; N ACETYL BETA GLUCOSAMINIDASE; PROTEIN P62; ROTENONE; TIRON; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB; TREHALOSE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; ANTIPARKINSON AGENT; SNCA PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; LYSOSOME MEMBRANE; MALE; MOTOR ACTIVITY; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PC12 CELL LINE; PHARMACOLOGICAL BLOCKING; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; RAT; SUBSTANTIA NIGRA PARS COMPACTA; ANIMAL; DRUG EFFECTS; LEWIS RAT; LYSOSOME; METABOLISM; PARKINSONIAN DISORDERS; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION;

ALPHA-SYNUCLEIN; ANIMALS; ANTIPARKINSON AGENTS; AUTOPHAGY; LYSOSOMES; MALE; PARKINSONIAN DISORDERS; PARS COMPACTA; PC12 CELLS; RANDOM ALLOCATION; RATS; RATS, INBRED LEW; ROTENONE; TREHALOSE; TYROSINE 3-MONOOXYGENASE;

EID: 84913570274     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.11.004     Document Type: Article

References (53)

1. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 2000, 3:1301-1306.
2. Cannon J.R., Greenamyre J.T. Neurotoxic in vivo models of Parkinson's disease recent advances. Prog Brain Res 2010, 184:17-33.
3. Chen J., Xavier S., Moskowitz-Kassai E., Chen R., Lu C.Y., Sanduski K., Spes A., Turk B., Goligorsky M.S. Cathepsin cleavage of sirtuin 1 in endothelial progenitor cells mediates stress-induced premature senescence. Am J Pathol 2012, 180:973-983.
4. Chen Y., McMillan-Ward E., Kong J., Israels S.J., Gibson S.B. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J Cell Sci 2007, 120:4155-4166.
5. Cicchetti F., Drouin-Ouellet J., Gross R.E. Environmental toxins and Parkinson's disease: what have we learned from pesticide-induced animal models?. Trends Pharmacol Sci 2009, 30:475-483.
6. Cuervo A.M., Stefanis L., Fredenburg R., Lansbury P.T., Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 2004, 305:1292-1295.
7. Cullen V., Lindfors M., Ng J., Paetau A., Swinton E., Kolodziej P., Boston H., Saftig P., Woulfe J., Feany M.B., Myllykangas L., Schlossmacher M.G., Tyynela J. Cathepsin D expression level affects alpha-synuclein processing, aggregation, and toxicity in vivo. Mol Brain 2009, 2:5.
8. Dagda R.K., Das Banerjee T., Janda E. How Parkinsonian toxins dysregulate the autophagy machinery. Int J Mol Sci 2013, 14:22163-22189.
9. Dawson T.M., Ko H.S., Dawson V.L. Genetic animal models of Parkinson's disease. Neuron 2010, 66:646-661.
10. Decressac M., Mattsson B., Weikop P., Lundblad M., Jakobsson J., Bjorklund A TFEB-mediated autophagy rescues midbrain dopamine neurons from alpha-synuclein toxicity. Proc Natl Acad Sci USA 2013, 110:E1817-E1826.
11. Dehay B., Bove J., Rodriguez-Muela N., Perier C., Recasens A., Boya P., Vila M. Pathogenic lysosomal depletion in Parkinson's disease. J Neurosci 2010, 30:12535-12544.
12. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991, 114(Pt 5):2283-2301.
13. Freeman D., Cedillos R., Choyke S., Lukic Z., McGuire K., Marvin S., Burrage A.M., Sudholt S., Rana A., O'Connor C., Wiethoff C.M., Campbell E.M. Alpha-synuclein induces lysosomal rupture and cathepsin dependent reactive oxygen species following endocytosis. PLoS One 2013, 8:e62143.
14. Han Y.H., Park W.H. Tiron, a ROS scavenger, protects human lung cancer Calu-6 cells against antimycin A-induced cell death. Oncol Rep 2009, 21:253-261.
15. Hatcher J.M., Pennell K.D., Miller G.W. Parkinson's disease and pesticides: a toxicological perspective. Trends Pharmacol Sci 2008, 29:322-329.
16. Heid M.E., Keyel P.A., Kamga C., Shiva S., Watkins S.C., Salter R.D. Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J Immunol 2013, 191:5230-5238.
17. Huai J., Vogtle F.N., Jockel L., Li Y., Kiefer T., Ricci J.E., Borner C. TNFalpha-induced lysosomal membrane permeability is downstream of MOMP and triggered by caspase-mediated NDUFS1 cleavage and ROS formation. J Cell Sci 2013, 126:4015-4025.
18. Janda E., Isidoro C., Carresi C., Mollace V. Defective autophagy in Parkinson's disease: role of oxidative stress. Mol Neurobiol 2012, 46:639-661.
19. Kazantsev A.G., Kolchinsky A.M. Central role of alpha-synuclein oligomers in neurodegeneration in Parkinson disease. Arch Neurol 2008, 65:1577-1581.
20. Kingwell K. Genetics: mutations in autophagy gene cause a rare and severe neurodegenerative disease. Nat Rev Neurol 2013, 9:182.
21. Klionsky D.J., Emr S.D. Autophagy as a regulated pathway of cellular degradation. Science 2000, 290:1717-1721.
22. Kreuzaler P.A., Staniszewska A.D., Li W., Omidvar N., Kedjouar B., Turkson J., Poli V., Flavell R.A., Clarkson R.W., Watson C.J. Stat3 controls lysosomal-mediated cell death in vivo. Nat Cell Biol 2011, 13:303-309.
23. Kuma A., Hatano M., Matsui M., Yamamoto A., Nakaya H., Yoshimori T., Ohsumi Y., Tokuhisa T., Mizushima N. The role of autophagy during the early neonatal starvation period. Nature 2004, 432:1032-1036.
24. Lieberman A.P., Puertollano R., Raben N., Slaugenhaupt S., Walkley S.U., Ballabio A. Autophagy in lysosomal storage disorders. Autophagy 2012, 8:719-730.
25. Luk K.C., Kehm V., Carroll J., Zhang B., O'Brien P., Trojanowski J.Q., Lee V.M. Pathological alpha-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 2012, 338:949-953.
26. Mader B.J., Pivtoraiko V.N., Flippo H.M., Klocke B.J., Roth K.A., Mangieri L.R., Shacka J.J. Rotenone inhibits autophagic flux prior to inducing cell death. ACS Chem Neurosci 2012, 3:1063-1072.
27. Malagelada C., Jin Z.H., Jackson-Lewis V., Przedborski S., Greene L.A. Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease. J Neurosci 2010, 30:1166-1175.
28. Martinez-Vicente M., Talloczy Z., Wong E., Tang G.M., Koga H., Kaushik S., de Vries R., Arias E., Harris S., Sulzer D., Cuervo A.M. Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat Neurosci 2010, 13:U567-U574.
29. Micsenyi M.C., Sikora J., Stephney G., Dobrenis K., Walkley S.U. Lysosomal membrane permeability stimulates protein aggregate formation in neurons of a lysosomal disease. J Neurosci 2013, 33:10815-10827.
30. Nixon R.A. The role of autophagy in neurodegenerative disease. Nat Med 2013, 19:983-997.
31. Pattingre S., Tassa A., Qu X.P., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
32. Pickford F., Masliah E., Britschgi M., Lucin K., Narasimhan R., Jaeger P.A., Small S., Spencer B., Rockenstein E., Levine B., Wyss-Coray T. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 2008, 118:2190-2199.
33. Polajnar M., Zerovnik E. Impaired autophagy: a link between neurodegenerative and neuropsychiatric diseases. J Cell Mol Med 2014, 18:1705-1711.
34. Porter K., Nallathambi J., Lin Y., Liton P.B. Lysosomal basification and decreased autophagic flux in oxidatively stressed trabecular meshwork cells: implications for glaucoma pathogenesis. Autophagy 2013, 9:581-594.
35. Poulopoulos M., Levy O.A., Alcalay R.N. The neuropathology of genetic Parkinson's disease. Mov Disord 2012, 27:831-842.
36. Roczniak-Ferguson A., Petit C.S., Froehlich F., Qian S., Ky J., Angarola B., Walther T.C., Ferguson S.M. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 2012, 5:ra42.
37. Rothermel B.A., Hill J.A. Myocyte autophagy in heart disease: friend or foe?. Autophagy 2007, 3:632-634.
38. Sarkar S., Chigurupati S., Raymick J., Mann D., Bowyer J.F., Schmitt T., Beger R.D., Hanig J.P., Schmued L.C., Paule M.G. Neuroprotective effect of the chemical chaperone, trehalose in a chronic MPTP-induced Parkinson's disease mouse model. Neurotoxicology 2014, 44C:250-262.
39. Sarkar S., Davies J.E., Huang Z., Tunnacliffe A., Rubinsztein D.C. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 2007, 282:5641-5652.
40. Sarkar S., Ravikumar B., Floto R.A., Rubinsztein D.C. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine-expanded huntingtin and related proteinopathies. Cell Death Differ 2009, 16:46-56.
41. Settembre C., Di Malta C., Polito V.A., Garcia Arencibia M., Vetrini F., Erdin S., Erdin S.U., Huynh T., Medina D., Colella P., Sardiello M., Rubinsztein D.C., Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science 2011, 332:1429-1433.
42. Sevlever D., Jiang P., Yen S.H. Cathepsin D is the main lysosomal enzyme involved in the degradation of alpha-synuclein and generation of its carboxy-terminally truncated species. Biochemistry 2008, 47:9678-9687.
43. Song W., Wang F., Savini M., Ake A., di Ronza A., Sardiello M., Segatori L. TFEB regulates lysosomal proteostasis. Hum Mol Genet 2013, 22(10):1994-2009.
44. Tan C.C., Yu J.T., Tan M.S., Jiang T., Zhu X.C., Tan L. Autophagy in aging and neurodegenerative diseases: implications for pathogenesis and therapy. Neurobiol Aging 2014, 35:941-957.
45. Vekrellis K., Xilouri M., Emmanouilidou E., Rideout H.J., Stefanis L. Pathological roles of alpha-synuclein in neurological disorders. Lancet Neurol 2011, 10:1015-1025.
46. Vila M., Bove J., Dehay B., Rodriguez-Muela N., Boya P. Lysosomal membrane permeabilization in Parkinson disease. Autophagy 2011, 7:98-100.
47. Vogiatzi T., Xilouri M., Vekrellis K., Stefanis L. Wild type alpha-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem 2008, 283:23542-23556.
48. Wong E., Cuervo A.M. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 2010, 13:805-811.
49. Wyttenbach A., Hands S., King M.A., Lipkow K., Tolkovsky A.M. Amelioration of protein misfolding disease by rapamycin: translation or autophagy?. Autophagy 2008, 4:542-545.
50. Xilouri M., Brekk O.R., Landeck N., Pitychoutis P.M., Papasilekas T., Papadopoulou-Daifoti Z., Kirik D., Stefanis L. Boosting chaperone-mediated autophagy in vivo mitigates alpha-synuclein-induced neurodegeneration. Brain 2013, 136:2130-2146.
51. Yu W.B., Jiang T., Lan D.M., Lu J.H., Yue Z.Y., Zhou P., Wang J. Trehalose inhibits fibrillation of A53T mutant alpha-synuclein and disaggregates existing fibrils. Arch Biochem Biophys 2012, 523(2):144-150.
52. Yu W.H., Dorado B., Figueroa H.Y., Wang L., Planel E., Cookson M.R., Clark L.N., Clark L.N., Duff K.E. Metabolic activity determines efficacy of macroautophagic clearance of pathological oligomeric alpha-synuclein. Am J Pathol 2009, 175:736-747.
53. Zhang X.J., Li L.A., Chen S., Yang D.H., Wang Y., Zhang X., Wang Z., Le W.D. Rapamycin treatment augments motor neuron degeneration in SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Autophagy 2011, 7:412-425.