Mitochondrial dysfunction precedes other sub-cellular abnormalities in an in vitro model linked with cell death in Parkinson's disease

Neurotoxicity Research

Volumn 21, Issue 2, 2012, Pages 185-194

  Yong Kee, C J ^a   Sidorova, E ^b   Hanif, A ^a   Perera, G ^a   Nash, J E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Cell stress; Lysosome; Mitochondria; Parkinson's disease; Ubiquitin proteasome system (UPS)

Indexed keywords

NAPHTHAZARIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; UBIQUITIN;

ARTICLE; BIOLOGICAL MODEL; CANCER CELL CULTURE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; HUMAN CELL; IN VITRO STUDY; LYSOSOME MEMBRANE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE DEGENERATION; NEUROBLASTOMA; NEUROPATHOLOGY; PARKINSON DISEASE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; UPREGULATION; WESTERN BLOTTING;

CELL DEATH; CELL LINE, TUMOR; HUMANS; LYSOSOMES; MITOCHONDRIA; NAPHTHOQUINONES; NEURONS; PARKINSON DISEASE, SECONDARY; PROTEASOME ENDOPEPTIDASE COMPLEX; ROTENONE; TIME FACTORS; UBIQUITIN;

EID: 84856451662     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-011-9259-6     Document Type: Article

References (53)

1. Ardley HC, Scott GB, Rose SA, Tan NG, Robinson PA (2004) UCH-L1 aggresome formation in response to proteasome impairment indicates a role in inclusion formation in Parkinson's disease. J Neurochem 90:379-391 (Pubitemid 38938224)
2. Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 20:415-455
3. Braak H, Braak E, Yilmazer D, de Vos RA, Jansen EN, Bohl J (1996) Pattern of brain destruction in Parkinson's and Alzheimer's diseases. J Neural Transm 103:455-490 (Pubitemid 26131746)
4. Busija DW, Gaspar T, Domoki F, Katakam PV, Bari F (2008) Mitochondrial-mediated suppression of ROS production upon exposure of neurons to lethal stress: mitochondrial targeted preconditioning. Adv Drug Deliv Rev 60:1471-1477
5. Cho HS, Kim S, Lee SY, Park JA, Kim SJ, Chun HS (2008) Protective effect of the green tea component, l-theanine on environmental toxins-induced neuronal cell death. Neurotoxicology 29:656-662
6. Chu Y, Dodiya H, Aebischer P, Olanow CW, Kordower JH (2009) Alterations in lysosomal and proteasomal markers in Parkinson's disease: relationship to alpha-synuclein inclusions. Neurobiol Dis 35:385-398
7. Chung WG, Miranda CL, Maier CS (2007) Epigallocatechin gallate (EGCG) potentiates the cytotoxicity of rotenone in neuroblastoma SH-SY5Y cells. Brain Res 1176:133-142 (Pubitemid 47553116)
8. Cookson MR (2003) Parkin's substrates and the pathways leading to neuronal damage. Neuromol Med 3:1-13 (Pubitemid 37070578)
9. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D (2004) Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305:1292-1295 (Pubitemid 39129234)
10. Dadakhujaev S, Noh HS, Jung EJ, Cha JY, Baek SM, Ha JH, Kim DR (2010) Autophagy protects the rotenone-induced cell death in alpha-synuclein overexpressing SH-SY5Y cells. Neurosci Lett 472:47-52
11. Di Fonzo A et al (2007) ATP13A2 missense mutations in juvenile parkinsonism and young onset Parkinson disease. Neurology 68:1557-1562 (Pubitemid 46717978)
12. Gidday JM (2006) Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci 7:437-448 (Pubitemid 44012284)
13. Hardy J (2010) Genetic analysis of pathways to Parkinson disease. Neuron 68:201-206
14. Hatano T, Kubo S, Sato S, Hattori N (2009) Pathogenesis of familial Parkinson's disease: new insights based on monogenic forms of Parkinson's disease. J Neurochem 111:1075-1093
15. Hochstrasser M (1992) Ubiquitin and intracellular protein degradation. Curr Opin Cell Biol 4:1024-1031
16. Hornykiewicz O (1972) Dopamine and extrapyramidal motor function and dysfunction. Res Publ Assoc Res Nerv Ment Dis 50:390-415
17. Irrcher I et al (2010) Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum Mol Genet 19:3734-3746
18. Jenner P (1993) Altered mitochondrial function, iron metabolism and glutathione levels in Parkinson's disease. Acta Neurol Scand Suppl 146:6-13 (Pubitemid 23251601)
19. Jiang H, Ren Y, Zhao J, Feng J (2004) Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Hum Mol Genet 13:1745-1754 (Pubitemid 39173443)
20. Kanda S, Bishop JF, Eglitis MA, Yang Y, Mouradian MM (2000) Enhanced vulnerability to oxidative stress by alpha-synuclein mutations and C-terminal truncation. Neuroscience 97:279-284 (Pubitemid 30224765)
21. Kettern N, Dreiseidler M, Tawo R, Hohfeld J (2010) Chaperone-assisted degradation: multiple paths to destruction. Biol Chem 391:481-489
22. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392:605-608 (Pubitemid 28207717)
23. Koch A, Lehmann-Horn K, Dachsel JC, Gasser T, Kahle PJ, Lucking CB (2009) Proteasomal inhibition reduces parkin mRNA in PC12 and SH-SY5Y cells. Parkinsonism Relat Disord 15:220-225
24. Kubota H (2009) Quality control against misfolded proteins in the cytosol: a network for cell survival. J Biochem 146:609-616
25. Lannuzel A, Michel PP, Hoglinger GU, Champy P, Jousset A, Medja F, Lombes A, Darios F, Gleye C, Laurens A, Hocquemiller R, Hirsch EC, Ruberg M (2003) The mitochondrial complex I inhibitor annonacin is toxic to mesencephalic dopaminergic neurons by impairment of energy metabolism. Neuroscience 121:287-296 (Pubitemid 37176917)
26. Lees AJ, Singleton AB (2007) Clinical heterogeneity of ATP13A2 linked disease (Kufor-Rakeb) justifies a PARK designation. Neurology 68:1553-1554 (Pubitemid 46717976)
27. Leigh PN, Probst A, Dale GE, Power DP, Brion JP, Dodson A, Anderton BH (1989) New aspects of the pathology of neurodegenerative disorders as revealed by ubiquitin antibodies. Acta Neuropathol 79:61-72 (Pubitemid 19259291)
28. Magen I, Chesselet MF (2010) Genetic mouse models of Parkinson's disease the state of the art. Prog Brain Res 184:53-87
29. Martinat C, Shendelman S, Jonason A, Leete T, Beal MF, Yang L, Floss T, Abeliovich A (2004) Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ES-derived cell model of primary Parkinsonism. PLoS Biol 2:e327 (Pubitemid 40280475)
30. Murray AM, Weihmueller FB, Marshall JF, Hurtig HI, Gottleib GL, Joyce JN (1995) Damage to dopamine systems differs between Parkinson's disease and Alzheimer's disease with parkinsonism. Ann Neurol 37:300-312
31. Naoi M, Maruyama W, Shamoto-Nagai M, Yi H, Akao Y, Tanaka M (2005) Oxidative stress in mitochondria: decision to survival and death of neurons in neurodegenerative disorders. Mol Neurobiol 31:81-93 (Pubitemid 41271195)
32. Nonaka T, Hasegawa M (2009) A cellular model to monitor proteasome dysfunction by alpha-synuclein. Biochemistry 48:8014-8022
33. Olzmann JA, Chin LS (2008) Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresome-autophagy pathway. Autophagy 4:85-87
34. Parker WD Jr, Boyson SJ, Parks JK (1989) Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann Neurol 26:719-723 (Pubitemid 20011004)
35. Qian JJ, Cheng YB, Yang YP, Mao CJ, Qin ZH, Li K, Liu CF (2008) Differential effects of overexpression of wild-type and mutant human alpha-synuclein on MPP+-induced neurotoxicity in PC12 cells. Neurosci Lett 435:142-146
36. Radke S, Chander H, Schafer P, Meiss G, Kruger R, Schulz JB, Germain D (2008) Mitochondrial protein quality control by the proteasome involves ubiquitination and the protease Omi. J Biol Chem 283:12681-12685
37. Ramirez A, Heimbach A, Grundemann J, Stiller B, Hampshire D, Cid LP, Goebel I, Mubaidin AF, Wriekat AL, Roeper J, Al-Din A, Hillmer AM, Karsak M, Liss B, Woods CG, Behrens MI, Kubisch C (2006) Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat Genet 38:1184-1191 (Pubitemid 44470365)
38. Sakata E, Yamaguchi Y, Kurimoto E, Kikuchi J, Yokoyama S, Yamada S, Kawahara H, Yokosawa H, Hattori N, Mizuno Y, Tanaka K, Kato K (2003) Parkin binds the Rpn10 subunit of 26S proteasomes through its ubiquitin-like domain. EMBO Rep 4:301-306 (Pubitemid 36511728)
39. Sapkota K, Kim S, Park SE, Kim SJ (2011) Detoxified extract of Rhus verniciflua stokes inhibits rotenone-induced apoptosis in human dopaminergic cells, SH-SY5Y. Cell Mol Neurobiol 31:213-223
40. Shamoto-Nagai M, Maruyama W, Kato Y, Isobe K, Tanaka M, Naoi M, Osawa T (2003) An inhibitor of mitochondrial complex I, rotenone, inactivates proteasome by oxidative modification and induces aggregation of oxidized proteins in SH-SY5Y cells. J Neurosci Res 74:589-597 (Pubitemid 37352081)
41. Shendelman S, Jonason A, Martinat C, Leete T, Abeliovich A (2004) DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol 2:e362 (Pubitemid 40280476)
42. Sherer TB, Richardson JR, Testa CM, Seo BB, Panov AV, Yagi T, Matsuno-Yagi A, Miller GW, Greenamyre JT (2007) Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson's disease. J Neurochem 100:1469-1479 (Pubitemid 46376213)
43. Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA (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 (Pubitemid 34184043)
44. Sullivan PG, Dragicevic NB, Deng JH, Bai Y, Dimayuga E, Ding Q, Chen Q, Bruce-Keller AJ, Keller JN (2004) Proteasome inhibition alters neural mitochondrial homeostasis and mitochondria turnover. J Biol Chem 279:20699-20707 (Pubitemid 38656466)
45. Tanaka Y, Engelender S, Igarashi S, Rao RK, Wanner T, Tanzi RE, Sawa A, LD V, Dawson TM, Ross CA (2001) Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria- dependent apoptosis. Hum Mol Genet 10:919-926 (Pubitemid 32401408)
46. Todde V, Veenhuis M, van der Klei IJ (2009) Autophagy: principles and significance in health and disease. Biochim Biophys Acta 1792:3-13
47. von Bohlen und Halbach O, Schober A, Krieglstein K (2004) Genes, proteins, and neurotoxins involved in Parkinson's disease. Prog Neurobiol 73:151-177 (Pubitemid 38952827)
48. Whitworth AJ, Pallanck LJ (2009) The PINK1/Parkin pathway: a mitochondrial quality control system? J Bioenerg Biomembr 41:499-503
49. Wu F, Poon WS, Lu G, Wang A, Meng H, Feng L, Li Z, Liu S (2009) Alpha-synuclein knockdown attenuates MPP+ induced mitochondrial dysfunction of SH-SY5Y cells. Brain Res 1292:173-179
50. Xie HR, Hu LS, Li GY (2010) SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinson's disease. Chin Med J 123:1086-1092
51. Xie H, Chang M, Hu X, Wang D, Tian M, Li G, Jiang H, Wang Y, Dong Z, Zhang Y, Hu L (2011) Proteomics analysis of MPP(+)-induced apoptosis in SH-SY5Y cells. Neurol Sci 32:221-228
52. Yong-Kee CJ, Salomonczyk D, Nash JE (2011) Development and validation of a screening assay for the evaluation of putative neuroprotective agents in the treatment of Parkinson's disease. Neurotox Res 19:7
53. Yun J, Cao JH, Dodson MW, Clark IE, Kapahi P, Chowdhury RB, Guo M (2008) Loss-of-function analysis suggests that Omi/HtrA2 is not an essential component of the PINK1/PARKIN pathway in vivo. J Neurosci 28:14500-14510