The Bipyridyl Herbicide Paraquat Induces Proteasome Dysfunction in Human Neuroblastoma SH-SY5Y Cells

REFERENCES

• Abou-Sleiman , P. M. , Muqit , M. K. and Wood , N. W. 2006 . Expanding insights of mitochondrial dysfunction in Parkinson's disease . Nat. Rev. Neurosci. , 7 : 207 – 219 .
   PubMed Web of Science ®Google Scholar
• Andersen , J. K. 2003 . Paraquat and iron exposure as possible synergistic environmental risk factors in Parkinson's disease . Neurotoxicol. Res. , 5 : 307 – 314 .
   PubMed Web of Science ®Google Scholar
• Barnham , K. J. , Masters , C. L. and Bush , A. I. 2004 . Neurodegenerative diseases and oxidative stress . Nat. Rev. Drug Discov. , 3 : 205 – 214 .
   PubMed Web of Science ®Google Scholar
• Barrientos , A. , Kenyon , L. and Moraes , C. T. 1998 . Human xenomitochondrial cybrids. Cellular models of mitochondrial complex I deficiency . J. Biol. Chem. , 273 : 14210 – 14217 .
   PubMedGoogle Scholar
• Ben-Shachar , D. , Zuk , R. , Gazawi , H. and Ljubuncic , P. 2004 . Dopamine toxicity involves mitochondrial complex I inhibition: Implications to dopamine-related neuropsychiatric disorders . Biochem. Pharmacol. , 67 : 1965 – 1974 .
   PubMedGoogle Scholar
• Biasini , E. , Fioriti , L. , Ceglia , I. , Invernizzi , R. , Bertoli , A. , Chiesa , R. and Forloni , G. 2004 . Proteasome inhibition and aggregation in Parkinson's disease: A comparative study in untransfected and transfected cells . J. Neurochem. , 88 : 545 – 553 .
   PubMed Web of Science ®Google Scholar
• Bismuth , C. , Garnier , R. , Baud , F. J. , Muszynski , J. and Keyes , C. 1990 . Paraquat poisoning. An overview of the current status . Drug Safety , 5 : 243 – 251 .
   PubMed Web of Science ®Google Scholar
• Bradford , M. M. 1976 . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding . Anal. Biochem. , 72 : 248 – 254 .
   PubMed Web of Science ®Google Scholar
• Brooks , A. I. , Chadwick , H. A. , Gelbard , D. A. , Cory-Slechta , D. A. and Federoff , H. J. 1999 . Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss . Brain Res. , 823 : 1 – 10 .
   PubMed Web of Science ®Google Scholar
• Carrard , G. , Bulteau , A. L. , Petropoulos , I. and Friguet , B. 2002 . Impairment of proteasome structure and function in aging . Int. J. Biochem. Cell Biol. , 34 : 1461 – 1474 .
   PubMed Web of Science ®Google Scholar
• Chung , K. K. , Dawson , V. L. and Dawson , T. M. 2001 . The role of the ubiquitin-proteasomal pathway in Parkinson's disease and other neurodegenerative disorders . Trends Neurosci. Suppl. , 24 : S7 – S14 .
   PubMedGoogle Scholar
• Ciechanover , A. and Brundin , P. 2003 . The ubiquitin proteasome system in neurodegenerative diseases: Sometimes the chicken, sometimes the egg . Neuron , 40 : 427 – 446 .
   PubMed Web of Science ®Google Scholar
• Cremlyn , J. R. 1991 . Agrochemicals: Preparation and mode of action , Chichester, England : Wiley .
   Google Scholar
• DeMartino , G. N. and Slaughter , C. A. 1999 . The proteasome, a novel protease regulated by multiple mechanisms . J. Biol. Chem. , 274 : 22123 – 22126 .
   PubMed Web of Science ®Google Scholar
• Denizot , F. and Lang , R. 1986 . Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability . J. Immunol. Methods , 89 : 271 – 277 .
   PubMed Web of Science ®Google Scholar
• Dev , K. K. , Hofele , K. , Barbieri , S. , Buchman , V. L. and van der Putten , H. 2003 . Part II: Alpha-synuclein and its molecular pathophysiological role in neurodegenerative disease . Neuropharmacology , 45 : 14 – 44 .
   PubMedGoogle Scholar
• Ding , Q. and Keller , J. N. 2001 . Proteasome inhibition in oxidative stress neurotoxicity: Implications for heat shock proteins . J. Neurochem. , 77 : 1010 – 1017 .
   PubMed Web of Science ®Google Scholar
• Di Monte , D. A. 2003 . The environment and Parkinson's disease: Is the nigrostriatal system preferentially targeted by neurotoxins? . Lancet Neurol. , 2 : 531 – 538 .
   PubMed Web of Science ®Google Scholar
• Elkon , H. , Melamed , E. and Offen , D. 2001 . 6-Hydroxydopamine increases ubiquitin-conjugates and protein degradation: Implications for the pathogenesis of Parkinson's disease . Cell Mol. Neurobiol. , 21 : 771 – 781 .
   PubMed Web of Science ®Google Scholar
• Elkon , H. , Melamed , E. and Offen , D. 2004 . Oxidative stress, induced by 6‐hydroxydopamine, reduces proteasome activities in PC12 cells: Implications for the pathogenesis of Parkinson's disease . J. Mol. Neurosci. , 24 : 387 – 400 .
   PubMedGoogle Scholar
• Glickman , M. H. and Ciechanover , A. 2002 . The ubiquitin–proteasome proteolytic pathway: Destruction for the sake of construction . Physiol. Rev. , 82 : 373 – 428 .
   PubMed Web of Science ®Google Scholar
• Goldberg , A. L. 2003 . Protein degradation and protection against misfolded or damaged proteins . Nature , 426 : 895 – 899 .
   PubMed Web of Science ®Google Scholar
• Gómez-Santos , C. , Ambrosio , S. , Ventura , F. , Ferrer , I. and Reiriz , J. 2002 . TGF-beta1 increases tyrosine hydroxylase expression by a mechanism blocked by BMP-2 in human neuroblastoma SH-SY5Y cells . Brain Res. , 958 : 152 – 160 .
   PubMed Web of Science ®Google Scholar
• Gómez-Santos , C. , Ferrer , I. , Santidrian , A. F. , Barrachina , M. , Gil , J. and Ambrosio , S. 2003 . Dopamine induces autophagic cell death and alpha-synuclein increase in human neuroblastoma SH-SY5Y cells . J. Neurosci. Res. , 73 : 341 – 350 .
   PubMed Web of Science ®Google Scholar
• Grant , H. , Lantos , P. L. and Parkinson , C. 1980 . Cerebral damage in paraquat poisoning . Histopathology , 4 : 185 – 195 .
   PubMed Web of Science ®Google Scholar
• Hashimoto , M. , Rockenstein , E. , Crews , L. and Masliah , E. 2003 . Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases . Neuromol. Med. , 4 : 21 – 36 .
   PubMed Web of Science ®Google Scholar
• Hertzman , C. , Wiens , M. , Bowering , D. , Snow , B. and Calne , D. 1990 . Parkinson`s disease: A case-control study of occupational and environmental risk factors . Am. J. Ind. Med. , 17 : 349 – 355 .
   PubMed Web of Science ®Google Scholar
• Hoglinger , G. U. , Carrard , G. , Michel , P. P. , Medja , F. , Lombes , A. , Ruberg , M. , Friguet , B. and Hirsch , E. C. 2003 . Dysfunction of mitochondrial complex I and the proteasome: interactions between two biochemical deficits in a cellular model of Parkinson's disease . J. Neurochem. , 86 : 1297 – 1307 .
   PubMed Web of Science ®Google Scholar
• Hughes , J. T. 1988 . Brain damage due to paraquat poisoning: A fatal case with neuropathological examination of the brain . Neurotoxicology , 9 : 243 – 248 .
   PubMed Web of Science ®Google Scholar
• Hyun , D. H. , Gray , D. A. , Halliwell , B. and Jenner , P. 2004 . Interference with ubiquitination causes oxidative damage and increased protein nitration: Implications for neurodegenerative diseases . J. Neurochem. , 90 : 422 – 430 .
   PubMedGoogle Scholar
• Keller , J. N. , Huang , F. F. , Dimayuga , E. R. and Maragos , W. F. 2000 . Dopamine induces proteasome inhibition in neural PC12 cell line . Free Radical Biol. Med. , 29 : 1037 – 1042 .
   PubMed Web of Science ®Google Scholar
• Klegeris , A. and McGeer , P. L. 2000 . R-(–)-Deprenyl inhibits monocytic THP-1 cell neurotoxicity independently of monoamine oxidase inhibition . Exp. Neurol. , 166 : 458 – 464 .
   PubMed Web of Science ®Google Scholar
• Krieger , C. and Duchen , M. R. 2002 . Mitochondria, Ca2+ and neurodegenerative disease . Eur. J. Pharmacol. , 447 : 177 – 188 .
   PubMedGoogle Scholar
• Lai , C. T. and Yu , P. H. 1997 . Dopamine- and L-β-3,4-dihydrophenylalanine hydrochloride (L-dopa)-induced cytotoxicity towards catecholaminergic neuroblastoma SH-SY5Ycells . Biochem. Pharmacol. , 53 : 363 – 372 .
   PubMed Web of Science ®Google Scholar
• Langston , J. W. , Ballard , P. A. , Terud , J. W. and Irwin , I. 1983 . Chronic parkinsonism in humans due to a product of merperidine analog synthesis . Science , 219 : 979 – 980 .
   PubMed Web of Science ®Google Scholar
• Langston , J. W. , Forno , L. S. , Tetrud , J. , Reeves , A. G. , Kaplan , J. A. and Karluk , D. 1999 . Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropryidine exposure . Ann. Neurol. , 46 : 598 – 605 .
   PubMed Web of Science ®Google Scholar
• Lee , H. S. , Park , C. W. and Kim , Y. S. 2000 . MPP+ increases the vulnerability to oxidative stress rather than directly mediating oxidative damage in human neuroblastoma cells . Exp. Neurol. , 165 : 164 – 171 .
   PubMed Web of Science ®Google Scholar
• Legros , H. , Dingeval , M. G. , Janin , F. , Costentin , J. and Bonnet , J. J. 2004 . Toxicity of treatment asociating dopamine and disulfiram for catecholaminergic neuroblastoma SH-SY5Y cells: Relationships with 3,4-dihydroxyphenylacetaldehyde formation . Neurotoxicology , 25 : 365 – 375 .
   PubMed Web of Science ®Google Scholar
• Liou , H. H. , Chen , R. C. , Tsai , Y. F. , Chen , W. P. , Chang , Y. C. and Tsai , M. C. 1996 . Effects of paraquat on the substantia nigra of the Wistar rats: Neurochemical, histological, and behavioral studies . Toxicol. Appl. Pharmacol. , 137 : 34 – 41 .
   PubMed Web of Science ®Google Scholar
• Liou , H. H. , Tsai , M. C. , Chen , C. J. , Jeng , J. S. , Chang , Y. C. , Chen , S. Y. and Chen , R. C. 1997 . Environmental risk factors and Parkinson's disease: A case-control study in Taiwan . Neurology , 48 : 1583 – 1588 .
   PubMed Web of Science ®Google Scholar
• Lopes , U. G. , Erhardt , P. , Yao , R. and Cooper , G. M. 1997 . p53-Dependent induction of apoptosis by proteasome inhibitors . J. Biol. Chem. , 272 : 12893 – 12896 .
   PubMed Web of Science ®Google Scholar
• Maňáková , S. , Puttonen , K. , Raasmaja , A. A. and Mannisto , P. T. 2004 . The roles of dopamine transporter and Bcl-2 protein in the protection of CV1-P cells from 6-OHDA-induced toxicity . Toxicol. Lett. , 154 : 117 – 123 .
   PubMed Web of Science ®Google Scholar
• Manning-Bog , A. B. , McCormack , A. L. , Li , J. , Uversky , V. N. , Fink , A. L. and Di Monte , D. A. 2002 . The herbicide paraquat causes up-regulation and aggregation of α-synuclein in mice . J. Biol. Chem. , 277 : 1641 – 1644 .
   PubMed Web of Science ®Google Scholar
• Masliah , E. , Rockenstein , E. , Veinbergs , I. , Mallory , M. , Hashimoto , M. , Takeda , A. , Sagara , Y. , Sisk , A. and Mucke , L. 2000 . Dopaminergic loss and inclusion body formation in alpha-synuclein mice: Implications for neurodegenerative disorders . Science , 287 : 1265 – 1269 .
   PubMed Web of Science ®Google Scholar
• Masayo , S. N. , Wakako , M. , Yoji , K. , Isobe , K. , Masashi , T. , Makoto , N. and Toshihiko , O. 2003 . An inhibitor of mitochondrial complex I, rotenone inactivates proteasome by oxidative modification and induces aggregation of oxidized proteins in SH-SY5Ycells . J. Neurosci. Res. , 74 : 589 – 597 .
   PubMed Web of Science ®Google Scholar
• McCormack , A. L. , Thiruchelvam , M. , Manning-Bog , A. B. , Thiffault , C. , Langston , J. W. , Cory-Slechta , D. and Di Monte , D. A. 2002 . Environmental risk factors and Parkinson`s disease: Selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat . Neurobiol. Dis. , 19 : 119 – 127 .
   Web of Science ®Google Scholar
• McNaught , K. S. and Jenner , P. 2001 . Proteasomal function is impaired in substantia nigra in Parkinson's disease . Neurosci. Lett. , 297 : 191 – 194 .
   PubMed Web of Science ®Google Scholar
• McNaught , K. S. , Olanow , C. W. , Halliwell , B. , Isacson , O. and Jenner , P. 2001 . Failure of the ubiquitin–proteasome system in Parkinson's disease . Nat. Rev. Neurosci. , 2 : 589 – 594 .
   PubMed Web of Science ®Google Scholar
• McNaught , K. S. , Belizaire , R. , Jenner , P. , Olanow , C. W. and Isacson , O. 2002 . Selective loss of 20S proteasome alpha-subunits in the substantia nigra pars compacta in Parkinson's disease . Neurosci. Lett. , 326 : 155 – 158 .
   PubMed Web of Science ®Google Scholar
• McNaught , K. S. , Belizaire , R. , Isacson , O. , Jenner , P. and Olanow , C. W. 2003 . Altered proteasomal function in sporadic Parkinson's disease . Exp. Neurol. , 179 : 38 – 46 .
   PubMed Web of Science ®Google Scholar
• McNaught , K. S. , Perl , D. P. , Brownell , A. L. and Olanow , C. W. 2004 . Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's disease . Ann. Neurol. , 56 : 149 – 162 .
   PubMed Web of Science ®Google Scholar
• McNaught , K. S. , Jackson , T. , JnoBaptiste , R. , Kapustin , A. and Olanow , C. W. 2006 . Proteasomal dysfunction in sporadic Parkinson`s disease . Neurology , 66 : S37 – S49 .
   PubMedGoogle Scholar
• Moldeus , P. , Hogberg , J. and Orrenius , S. 1978 . Isolation and use of liver cells . Methods Enzymol. , 52 : 60 – 71 .
   PubMedGoogle Scholar
• Onyon , L. J. and Volans , G. N. 1987 . The epidemiology and prevention of paraquat poisoning . Hum. Toxicol. , 6 : 19 – 26 .
   PubMedGoogle Scholar
• Pasquini , L. A. , Marta , C. B. , Adamo , A. M. , Pasquini , J. M. and Soto , E. F. 2000 . Relationship between the ubiquitin-dependent pathway and apoptosis in different cells of the central nervous system: Effect of thyroid hormones . Neurochem. Res. , 25 : 627 – 635 .
   PubMed Web of Science ®Google Scholar
• Presgraves , S. P. , Ahmed , T. , Borwege , S. and Joyce , J. N. 2004 . Terminally differentiated SH-SY5Y cells provide a model system for studying neuroprotective effects of dopamine agonists . Neurotox. Res. , 5 : 579 – 598 .
   PubMed Web of Science ®Google Scholar
• Roos-Mattjus , P. and Sistonen , L. 2004 . The ubiquitin-proteasome pathway . Ann. Med. , 36 : 285 – 295 .
   PubMed Web of Science ®Google Scholar
• Ross , C. A. and Pickart , C. M. 2004 . The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases . Trends Cell Biol. , 14 : 703 – 711 .
   PubMed Web of Science ®Google Scholar
• Sanchez-Ramos , J. R. , Hefti , F. and Weiner , W. J. 1987 . Paraquat and Parkinson`s disease . Neurology , 37 : 728
   PubMed Web of Science ®Google Scholar
• Shamoto-Nagai , M. , Maruyama , W. , Kato , Y. , Isobe , K. , Tanaka , M. , Naoi , M. and 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 .
   PubMedGoogle Scholar
• Shamoto-Nagai , M. , Maruyama , W. , Akao , Y. , Osawa , T. , Tribl , F. , Gerlach , M. , Zucca , F. A. , Zecca , L. , Riederer , P. and Naoi , M. 2004 . Neuromelanin inhibits enzymatic activity of 26S proteasome in human dopaminergic SH-SY5Y cells . J. Neural Transm. , 111 : 1253 – 1265 .
   PubMed Web of Science ®Google Scholar
• Shavali , S. , Carlson , E. C. , Swinscoe , J. C. and Ebadi , M. 2004 . 1-Benzyl-1,2,3,4,-tetrahydroisoquinoline, a Parkinsonism-inducing endogenous toxin, increases α-synuclein expression and causes nuclear damage in human dopaminergic cells . J. Neurosci. Res. , 76 : 563 – 572 .
   PubMed Web of Science ®Google Scholar
• Sherer , T. B. , Kim , J. H. , Betarbet , R. and Greenamyre , J. T. 2003 . Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation . Exp. Neurol. , 179 : 9 – 16 .
   PubMed Web of Science ®Google Scholar
• Sherman , N. Y. and Goldberg , A. L. 2001 . Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases . Neuron , 29 : 15 – 32 .
   PubMed Web of Science ®Google Scholar
• Sun , F. , Anantharam , V. , Latchoumycandane , C. , Kanthasamy , A. and Kanthasamy , A. G. 2005 . Dieldrin induces ubiquitin-proteasome dysfunction in -synuclein overexpressing dopaminergic neuronal cells and enhances susceptibility to apoptotic cell death . J. Pharmcol. Exp. Ther. , 315 : 69 – 79 .
   PubMedGoogle Scholar
• Tanaka , K. and Chiba , T. 1998 . The proteasome: A protein-destroying machine . Genes Cells , 3 : 499 – 510 .
   PubMedGoogle Scholar
• Tawara , T. , Fukushima , T. , Hojo , N. , Isobe , A. , Shiwaku , K. , Setogawa , T. and Yamane , Y. 1996 . Effects of paraquat on mitochondrial electron transport system and catecholamine contents in rat brain . Arch. Toxicol. , 70 : 585 – 589 .
   PubMed Web of Science ®Google Scholar
• Theron , M. , Guerrero , F. and Sebert , P. 2000 . Improvement in the efficiency of oxidative phosphorylation in the freshwater eel acclimated to 10.1 MPa hydrostatic pressure . J. Exp. Biol. , 203 : 3019 – 3023 .
   PubMed Web of Science ®Google Scholar
• Vekrellis , K. , Rideout , H. J. and Stefanis , L. 2004 . Neurobiology of alpha-synuclein . Mol. Neurobiol. , 30 : 1 – 21 .
   PubMedGoogle Scholar
• Vigouroux , S. , Briand , M. and Briand , Y. 2004 . Linkage between the proteasome pathway and neurodegenerative diseases and aging . Mol. Neurobiol. , 30 : 201 – 221 .
   PubMed Web of Science ®Google Scholar
• Yang , W. and Tiffany-Castiglioni , E. 2005 . The bipyridyl herbicide paraquat produces oxidative stress-mediated toxicity in human neuroblastoma SH-SY5Y cells: Relevance to the dopaminergic pathogenesis . J. Toxicol. Environ. Health A , 68 : 1939 – 1961 .
   PubMed Web of Science ®Google Scholar
• Yoshimoto , Y. , Nakaso , K. and Nakashima , K. 2005 . L-dopa and dopamine enhance the formation of aggregates under proteasome inhibition in PC12 cells . FEBS Lett. , 579 : 1197 – 1202 .
   PubMedGoogle Scholar
• Zhang , J. , Fitsanakis , V. A. , Gu , G. , Jing , D. , Ao , M. , Amarnath , V. and Montine , T. J. 2003 . Manganese ethylene-bis-dithiocarbamate and selective dopaminergic neurodegeneration in rat: A link through mitochondrial dysfunction . J. Neurochem. , 84 : 336 – 346 .
   PubMed Web of Science ®Google Scholar
• Zheng , J. and Ramirez , V. D. 2000 . Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals . Br. J. Pharmacol. , 130 : 1115 – 1123 .
   PubMed Web of Science ®Google Scholar
• Zhou , Y. , Shie , F. S. , Piccardo , P. , Montine , T. J. and Zhang , J. 2004 . Proteasomal inhibition induced by manganese ethylene-bis-dithiocarbamate: Relevance to Parkinson's disease . Neuroscience , 128 : 281 – 291 .
   PubMed Web of Science ®Google Scholar