Methamphetamine oxidatively damages parkin and decreases the activity of 26S proteasome in vivo

Journal of Neurochemistry

Volumn 116, Issue 6, 2011, Pages 1005-1017

  Moszczynska, Anna ^a   Yamamoto, Bryan K ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

4 hydroxy 2 nonenal; dopamine; methamphetamine; parkin; proteasome; toxicity

Indexed keywords

METHAMPHETAMINE; PARKIN; PROTEASOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; LIPID PEROXIDATION; MALE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MODIFICATION; RAT; SYNAPTOSOME; UBIQUITINATION;

ALDEHYDES; ANIMALS; ANTIOXIDANTS; CORPUS STRIATUM; CYSTEINE; CYSTEINE PROTEINASE INHIBITORS; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMUNOPRECIPITATION; MALE; METHAMPHETAMINE; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, SPRAGUE-DAWLEY; S-NITROSOTHIOLS; STATISTICS, NONPARAMETRIC; SYNAPTOSOMES; TIME FACTORS; TUBULIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VITAMIN E;

ANIMALIA; RATTUS;

EID: 79952453410     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07147.x     Document Type: Article

References (71)

1. Ali S. F., Newport G. D., Holson R. R., Slikker Jr. W., and, Bowyer J. F., (1994) Low environmental temperatures or pharmacologic agents that produce hypothermia decrease methamphetamine neurotoxicity in mice. Brain Res. 658, 33-38. (Pubitemid 24291700)
2. Anderson K. L., and, Itzhak Y., (2006) Methamphetamine-induced selective dopaminergic neurotoxicity is accompanied by an increase in striatal nitrate in the mouse. Ann. N Y Acad. Sci. 1074, 225-233. (Pubitemid 44532826)
3. Andersson M., Sjostrand J., and, Karlsson J. O., (1999) Differential inhibition of three peptidase activities of the proteasome in human lens epithelium by heat and oxidation. Exp. Eye Res. 69, 129-138. (Pubitemid 29335459)
4. Ardley H. C., Scott G. B., Rose S. A., Tan N. G., Markham A. F., and, Robinson P. A., (2003) Inhibition of proteasomal activity causes inclusion formation in neuronal and non-neuronal cells overexpressing Parkin. Mol. Biol. Cell 14, 4541-4556. (Pubitemid 37444654)
5. Bardag-Gorce F., Li J., French B. A., and, French S. W., (2005) The effect of ethanol-induced CYP2E1 on proteasome activity: the role of 4-hydroxynonenal. Exp. Mol. Pathol. 78, 109-115. (Pubitemid 40248791)
6. Bowyer J. F., Davies D. L., Schmued L., Broening H. W., Newport G. D., Slikker Jr. W., and, Holson R. R., (1994) Further studies of the role of hyperthermia in methamphetamine neurotoxicity. J. Pharmacol. Exp. Ther. 268, 1571-1580. (Pubitemid 24100380)
7. 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.
8. Bulteau A. L., Lundberg K. C., Humphries K. M., Sadek H. A., Szweda P. A., Friguet B., and, Szweda L. I., (2001) Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J. Biol. Chem. 276, 30057-30063.
9. Buneeva O. A., and, Medvedev A. E., (2006) Ubiquitin-protein ligase parkin and its role in the development of Parkinson's disease. Biochemistry (Mosc) 71, 851-860. (Pubitemid 44273661)
10. Catala A., (2009) Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem. Phys. Lipids 157, 1-11.
11. Chan P., Di Monte D. A., Luo J. J., DeLanney L. E., Irwin I., and, Langston J. W., (1994) Rapid ATP loss caused by methamphetamine in the mouse striatum: relationship between energy impairment and dopaminergic neurotoxicity. J. Neurochem. 62, 2484-2487. (Pubitemid 24179535)
12. Chang L., Alicata D., Ernst T., and, Volkow N., (2007) Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction 102 (Suppl 1), 16-32. (Pubitemid 46328220)
13. Choi P., Ostrerova-Golts N., Sparkman D., Cochran E., Lee J. M., and, Wolozin B., (2000) Parkin is metabolized by the ubiquitin/proteosome system. Neuroreport 11, 2635-2638.
14. Chondrogianni N., and, Gonos E. S., (2007) Overexpression of hUMP1/POMP proteasome accessory protein enhances proteasome-mediated antioxidant defence. Exp. Gerontol. 42, 899-903. (Pubitemid 47268730)
15. Chung K. K., Thomas B., Li X., Pletnikova O., Troncoso J. C., Marsh L., Dawson V. L., and, Dawson T. M., (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304, 1328-1331. (Pubitemid 38697430)
16. Dahlmann B., (2005) Proteasomes. Essays Biochem. 41, 31-48. (Pubitemid 41500969)
17. Dasuri K., Nguyen A., Zhang L., Fernandez-Kim O. S., Bruce-Keller A. J., Blalock B. A., Cabo R. D., and, Keller J. N., (2009) Comparison of rat liver and brain proteasomes for oxidative stress-induced inactivation: Influence of ageing and dietary restriction. Free Radic. Res. 43, 28-36.
18. Davies K. J., (2001) Degradation of oxidized proteins by the 20S proteasome. Biochimie 83, 301-310. (Pubitemid 32293650)
19. Dietrich J. B., Mangeol A., Revel M. O., Burgun C., Aunis D., and, Zwiller J., (2005) Acute or repeated cocaine administration generates reactive oxygen species and induces antioxidant enzyme activity in dopaminergic rat brain structures. Neuropharmacology 48, 965-974. (Pubitemid 40602604)
20. Ding Q., Reinacker K., and, Dimayuga E., et al. (2003) Role of the proteasome in protein oxidation and neural viability following low-level oxidative stress. FEBS Lett. 546, 228-232. (Pubitemid 36782416)
21. 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. (Pubitemid 41389376)
22. Ethen C. M., Hussong S. A., Reilly C., Feng X., Olsen T. W., and, Ferrington D. A., (2007) Transformation of the proteasome with age-related macular degeneration. FEBS Lett. 581, 885-890. (Pubitemid 46282718)
23. Eyerman D. J., and, Yamamoto B. K., (2007) A rapid oxidation and persistent decrease in the vesicular monoamine transporter 2 after methamphetamine. J. Neurochem. 103, 1219-1227. (Pubitemid 47568738)
24. Farout L., Lamare M. C., Cardozo C., Harrisson M., Briand Y., and, Briand M., (2000) Distribution of proteasomes and of the five proteolytic activities in rat tissues. Arch. Biochem. Biophys. 374, 207-212. (Pubitemid 30120254)
25. Fornai F., Lenzi P., and, Gesi M., et al. (2003) Fine structure and biochemical mechanisms underlying nigrostriatal inclusions and cell death after proteasome inhibition. J. Neurosci. 23, 8955-8966. (Pubitemid 37210909)
26. Fornai F., Lazzeri G., Bandettini Di Poggio A., Soldani P., De Blasi A., Nicoletti F., Ruggieri S., and, Paparelli A., (2006) Convergent roles of alpha-synuclein, DA metabolism, and the ubiquitin-proteasome system in nigrostriatal toxicity. Ann. N Y Acad. Sci. 1074, 84-89. (Pubitemid 44532812)
27. Gluck M. R., Moy L. Y., Jayatilleke E., Hogan K. A., Manzino L., and, Sonsalla P. K., (2001) Parallel increases in lipid and protein oxidative markers in several mouse brain regions after methamphetamine treatment. J. Neurochem. 79, 152-160. (Pubitemid 32946652)
28. Grune T., Reinheckel T., and, Davies K. J., (1997) Degradation of oxidized proteins in mammalian cells. FASEB J. 11, 526-534. (Pubitemid 27274426)
29. Hershko A., and, Ciechanover A., (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479. (Pubitemid 28411135)
30. Hotchkiss A. J., and, Gibb J. W., (1980) Long-term effects of multiple doses of methamphetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J. Pharmacol. Exp. Ther. 214, 257-262. (Pubitemid 10049032)
31. Hyun D. H., Lee M., Hattori N., Kubo S., Mizuno Y., Halliwell B., and, Jenner P., (2002) Effect of wild-type or mutant Parkin on oxidative damage, nitric oxide, antioxidant defenses, and the proteasome. J. Biol. Chem. 277, 28572-28577. (Pubitemid 41079284)
32. Jariel-Encontre I., Bossis G., and, Piechaczyk M., (2008) Ubiquitin-independent degradation of proteins by the proteasome. Biochim. Biophys. Acta 1786, 153-177.
33. Jefferson R. A., Burgess S. M., and, Hirsh D., (1986) beta-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc. Natl Acad. Sci. USA 83, 8447-8451. (Pubitemid 17194890)
34. Junn E., Lee S. S., Suhr U. T., and, Mouradian M. M., (2002) Parkin accumulation in aggresomes due to proteasome impairment. J. Biol. Chem. 277, 47870-47877. (Pubitemid 36159314)
35. Kisselev A. F., and, Goldberg A. L., (2005) Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol. 398, 364-378. (Pubitemid 41578898)
36. Kretz-Remy C., and, Arrigo A. P., (2003) Modulation of the chymotrypsin-like activity of the 20S proteasome by intracellular redox status: effects of glutathione peroxidase-1 overexpression and antioxidant drugs. Biol. Chem. 384, 589-595. (Pubitemid 36609174)
37. Kurepa J., Toh E. A., and, Smalle J. A., (2008) 26S proteasome regulatory particle mutants have increased oxidative stress tolerance. Plant J. 53, 102-114. (Pubitemid 350265244)
38. LaVoie M. J., Ostaszewski B. L., Weihofen A., Schlossmacher M. G., and, Selkoe D. J., (2005) Dopamine covalently modifies and functionally inactivates parkin. Nat. Med. 11, 1214-1221. (Pubitemid 43093669)
39. LaVoie M. J., Cortese G. P., Ostaszewski B. L., and, Schlossmacher M. G., (2007) The effects of oxidative stress on parkin and other E3 ligases. J. Neurochem. 103, 2354-2368. (Pubitemid 350173558)
40. Lazzeri G., Lenzi P., Busceti C. L., Ferrucci M., Falleni A., Bruno V., Paparelli A., and, Fornai F., (2007) Mechanisms involved in the formation of dopamine-induced intracellular bodies within striatal neurons. J. Neurochem. 101, 1414-1427. (Pubitemid 46718813)
41. Lee C. S., Tee L. Y., Warmke T., Vinjamoori A., Cai A., Fagan A. M., and, Snider B. J., (2004) A proteasomal stress response: pre-treatment with proteasome inhibitors increases proteasome activity and reduces neuronal vulnerability to oxidative injury. J. Neurochem. 91, 996-1006. (Pubitemid 39507376)
42. Lim K. L., (2007) Ubiquitin-proteasome system dysfunction in Parkinson's disease: current evidence and controversies. Expert Rev. Proteomics 4, 769-781.
43. Liu C. W., Strickland E., Demartino G. N., and, Thomas P. J., (2005) Recognition and processing of misfolded proteins by PA700, the 19S regulatory complex of the 26S proteasome. Methods Mol. Biol. 301, 71-81.
44. Lo Bianco C., Schneider B. L., Bauer M., Sajadi A., Brice A., Iwatsubo T., and, Aebischer P., (2004) Lentiviral vector delivery of parkin prevents dopaminergic degeneration in an alpha-synuclein rat model of Parkinson's disease. Proc. Natl Acad. Sci. USA 101, 17510-17515. (Pubitemid 39657434)
45. Mirecki A., Fitzmaurice P., and, Ang L., et al. (2004) Brain antioxidant systems in human methamphetamine users. J. Neurochem. 89, 1396-1408. (Pubitemid 38802661)
46. Moore D. J., (2006) Parkin: a multifaceted ubiquitin ligase. Biochem. Soc. Trans. 34, 749-753. (Pubitemid 44796412)
47. Nakahara T., Kuroki T., and, Ohta E., et al. (2003) Effect of the neurotoxic dose of methamphetamine on gene expression of parkin and Pael-receptors in rat striatum. Parkinsonism Relat. Disord. 9, 213-219. (Pubitemid 36287154)
48. Nash J. F., and, Yamamoto B. K., (1992) Methamphetamine neurotoxicity and striatal glutamate release: comparison to 3, 4-methylenedioxymethamphetamine. Brain Res. 581, 237-243.
49. Osna N. A., White R. L., Krutik V. M., Wang T., Weinman S. A., and, Donohue Jr. T. M., (2008) Proteasome activation by hepatitis C core protein is reversed by ethanol-induced oxidative stress. Gastroenterology 134, 2144-2152. (Pubitemid 351783253)
50. Park M. J., Lee S. K., Lim M. A., Chung H. S., Cho S. I., Jang C. G., and, Lee S. M., (2006) Effect of alpha-tocopherol and deferoxamine on methamphetamine-induced neurotoxicity. Brain Res. 1109, 176-182.
51. Petersen A., Honarvar A., and, Zetterberg M., (2010) Changes in Activity and Kinetic Properties of the Proteasome in Different Rat Organs during Development and Maturation. Curr. Gerontol. Geriatr. Res. 2010, 230697.
52. Quan L., Ishikawa T., Michiue T., Li D. R., Zhao D., Oritani S., Zhu B. L., and, Maeda H., (2005) Ubiquitin-immunoreactive structures in the midbrain of methamphetamine abusers. Leg Med. (Tokyo) 7, 144-150. (Pubitemid 40545076)
53. Rechsteiner M., and, Hill C. P., (2005) Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol. 15, 27-33. (Pubitemid 40094678)
54. Ricaurte G. A., Guillery R. W., Seiden L. S., Schuster C. R., and, Moore R. Y., (1982) Dopamine nerve terminal degeneration produced by high doses of methylamphetamine in the rat brain. Brain Res. 235, 93-103. (Pubitemid 12188130)
55. Riddle E. L., Topham M. K., Haycock J. W., Hanson G. R., and, Fleckenstein A. E., (2002) Differential trafficking of the vesicular monoamine transporter-2 by methamphetamine and cocaine. Eur. J. Pharmacol. 449, 71-74.
56. Schlehe J. S., Lutz A. K., Pilsl A., Lammermann K., Grgur K., Henn I. H., Tatzelt J., and, Winklhofer K. F., (2008) Aberrant folding of pathogenic Parkin mutants: aggregation versus degradation. J. Biol. Chem. 283, 13771-13779.
57. Shang F., and, Taylor A., (1995) Oxidative stress and recovery from oxidative stress are associated with altered ubiquitin conjugating and proteolytic activities in bovine lens epithelial cells. Biochem. J. 307 (Pt 1), 297-303.
58. Singh S., and, Khar A., (2006) Activation of NFkappaB and Ub-proteasome pathway during apoptosis induced by a serum factor is mediated through the upregulation of the 26S proteasome subunits. Apoptosis 11, 845-859. (Pubitemid 43876852)
59. Sulzer D., and, Rayport S., (1990) Amphetamine and other psychostimulants reduce pH gradients in midbrain dopaminergic neurons and chromaffin granules: a mechanism of action. Neuron 5, 797-808.
60. Tai H. C., and, Schuman E. M., (2008) Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat. Rev. Neurosci. 9, 826-838.
61. Thomas D. M., Walker P. D., Benjamins J. A., Geddes T. J., and, Kuhn D. M., (2004) Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J. Pharmacol. Exp. Ther. 311, 1-7. (Pubitemid 39287777)
62. Tydlacka S., Wang C. E., Wang X., Li S., and, Li X. J., (2008) Differential activities of the ubiquitin-proteasome system in neurons versus glia may account for the preferential accumulation of misfolded proteins in neurons. J. Neurosci. 28, 13285-13295.
63. Wagner G. C., Ricaurte G. A., Seiden L. S., Schuster C. R., Miller R. J., and, Westley J., (1980) Long-lasting depletions of striatal dopamine and loss of dopamine uptake sites following repeated administration of methamphetamine. Brain Res. 181, 151-160. (Pubitemid 10159505)
64. Wang C., Ko H. S., and, Thomas B., et al. (2005) Stress-induced alterations in parkin solubility promote parkin aggregation and compromise parkin's protective function. Hum. Mol. Genet. 14, 3885-3897. (Pubitemid 43020090)
65. Wang J., Wang C. E., Orr A., Tydlacka S., Li S. H., and, Li X. J., (2008a) Impaired ubiquitin-proteasome system activity in the synapses of Huntington's disease mice. J. Cell Biol. 180, 1177-1189. (Pubitemid 351468473)
66. Wang J., Xu W., Ali S. F., and, Angulo J. A., (2008b) Connection between the striatal neurokinin-1 receptor and nitric oxide formation during methamphetamine exposure. Ann. N Y Acad. Sci. 1139, 164-171.
67. Wilson J. M., Kalasinsky K. S., and, Levey A. I., et al. (1996) Striatal dopamine nerve terminal markers in human, chronic methamphetamine users. Nat. Med. 2, 699-703. (Pubitemid 26191961)
68. Winklhofer K. F., Henn I. H., Kay-Jackson P. C., Heller U., and, Tatzelt J., (2003) Inactivation of parkin by oxidative stress and C-terminal truncations: a protective role of molecular chaperones. J. Biol. Chem. 278, 47199-47208. (Pubitemid 37452306)
69. Wrona M. Z., Yang Z., Zhang F., and, Dryhurst G., (1997) Potential new insights into the molecular mechanisms of methamphetamine-induced neurodegeneration. NIDA Res. Monogr. 173, 146-174.
70. Yamamoto B. K., and, Zhu W., (1998) The effects of methamphetamine on the production of free radicals and oxidative stress. J. Pharmacol. Exp. Ther. 287, 107-114. (Pubitemid 29140192)
71. Yamamoto B. K., Moszczynska A., and, Gudelsky G. A., (2010) Amphetamine toxicities: classical and emerging mechanisms. Ann. N Y Acad. Sci. 1187, 101-121.