Alpha-synuclein overexpression and aggregation exacerbates impairment of mitochondrial functions by augmenting oxidative stress in human neuroblastoma cells

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 10, 2009, Pages 2015-2024

  Parihar, Mordhwaj S ^a   Parihar, Arti ^a   Fujita, Masayo ^b   Hashimoto, Makoto ^b   Ghafourifar, Pedram ^c  

^a VIKRAM UNIVERSITY   (India)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c Tri State Institute of Pharmaceutical Sciences   (United States)

Author keywords

Alpha synuclein; Human neuroblastoma cells; Mitochondria; Oxidative stress; Respiration

Indexed keywords

ALPHA SYNUCLEIN; REACTIVE OXYGEN METABOLITE; TYROSINE;

ANIMAL CELL; ARTICLE; BRAIN MITOCHONDRION; CELL RESPIRATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOGOLD ELECTRON MICROSCOPY; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUROBLASTOMA CELL; NITRATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; WILD TYPE;

ALPHA-SYNUCLEIN; ANIMALS; CELL LINE, TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; HUMANS; IMMUNOBLOTTING; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEUROBLASTOMA; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES;

EID: 68949151944     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.05.008     Document Type: Article

References (48)

1. Abou-Sleiman P.M., Muqit M.M., and Wood N.W. Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat Rev Neurosci 7 (2006) 207-219
2. Bossy-Wetzel E., Schwarzenbacher R., and Lipton S.A. Molecular pathways to neurodegeneration. Nat Med 10 (2004) S2-S9
3. Chan P., Jiang X., Forno L.S., Di Monte D.A., Tanner C.M., and Langston J.W. Absence of mutations in the coding region of the alpha-synuclein gene in pathologically proven Parkinson's disease. Neurology 50 (1998) 1136-1137
4. Clementi E., Brown G.C., Feelisch M., and Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci USA 95 (1998) 7631-7636
5. Chartier-Harlin M.C., Kachergus J., Roumier C., Mouroux V., Douay X., Lincoln S., Levecque C., Larvor L., Andrieux J., Hulihan M., Waucquier N., Defebvre L., Amouyel P., Farrer M., and Destee A. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 364 (2004) 1167-1169
6. Choo Y.S., Johnson G.V., MacDonald M., Detloff P.J., and Lesort M. Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum Mol Genet 13 (2004) 1407-1420
7. Cole N.B., Dieuliis D., Leo P., Mitchell D.C., and Nussbaum R.L. Mitochondrial translocation of alpha-synuclein is promoted by intracellular acidification. Exp Cell Res 314 (2008) 2076-2089
8. Conway K.A., Harper J.D., and Lansbury P.T. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat Med 4 (1998) 1318-1320
9. Devi L., Raghavendran V., Prabhu B.M., Avadhani N.G., and Anandatheerthavarada H.K. Mitochondrial import and accumulation of alpha-synuclein impairs complex I in human dopaminergic neuronal cultures and Parkinson's disease brain. J Biol Chem 283 (2008) 9089-9100
10. Ding T.T., Lee S.J., Rochet J.C., and Lansbury Jr. P.T. Annular alpha-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes. Biochemistry 41 (2002) 10209-10217
11. Fink C., Morgan F., and Loew L.M. Intracellular fluorescent probe concentrations by confocal microscopy. Biophys J 75 (1998) 1648-1658
12. Furukawa K., Matsuzaki-Kobayashi M., Hasegawa T., Kikuchi A., Sugeno N., Itoyama Y., Wang Y., Yao P.J., Bushlin I., and Takeda A. Plasma membrane ion permeability induced by mutant alpha-synuclein contributes to the degeneration of neural cells. J Neurochem 97 (2006) 1071-1077
13. Galvin J.E., Lee V.M., and Trojanowski J.Q. Synucleinopathies: clinical and pathological implications. Arch Neurol 58 (2001) 186-190
14. Ghafourifar P., Klein S.D., Schucht O., Schenk U., Pruschy M., Rocha S., and Richter C. Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state. J Biol Chem 274 (1999) 6080-6084
15. Ghafourifar P., Schenk U., Klein S.D., and Richter C. Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria. Evidence for intramitochondrial peroxynitrite formation. J Biol Chem 274 (1999) 31185-31188
16. Ghafourifar P., Asbury M.L., Joshi S.S., and Kincaid E.D. Determination of mitochondrial nitric oxide synthase activity. Methods Enzymol 396 (2005) 424-444
17. Good P.F., Hsu A., Werner P., Perl D.P., and Olanow C.W. Protein nitration in Parkinson's disease. J Neuropathol Exp Neurol 57 (1998) 338-342
18. Hasegawa T., Matsuzaki-Kobayashi M., Takeda A., Sugeno N., Kikuchi A., Furukawa K., Perry G., Smith M.A., and Itoyama Y. Alpha-synuclein facilitates the toxicity of oxidized catechol metabolites: implications for selective neurodegeneration in Parkinson's disease. FEBS Lett 580 (2006) 2147-2152
19. Hashimoto M., Yoshimoto M., Sisk A., Hsu L.J., Sundsmo M., Kittel A., Saitoh T., Miller A., and Masliah E. NACP, a synaptic protein involved in Alzheimer's disease, is differentially regulated during megakaryocyte differentiation. Biochem Biophys Res Commun 237 (1997) 611-616
20. Hashimoto M., Takeda A., Hsu L.J., Takenouchi T., and Masliah E. Role of cytochrome c as a stimulator of alpha-synuclein aggregation in Lewy body disease. J Biol Chem 274 (1999) 28849-28852
21. Hsu L.J., Sagara Y., Arroyo A., Rockenstein E., Sisk A., Mallory M., Wong J., Takenouchi T., Hashimoto M., and Masliah E. Alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am J Pathol 157 (2000) 401-410
22. Ibanez P., Bonnet A.M., Debarges B., Lohmann E., Tison F., Pollak P., Agid Y., Durr A., and Brice A. Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease. Lancet 364 (2004) 1169-1171
23. Koeck T., Fu X., Hazen S.L., Crabb J.W., Stuehr D.J., and Aulak K.S. Rapid and selective oxygen regulated protein tyrosine "denitration" and nitration in mitochondria. J Biol Chem 279 (2004) 27257-27262
24. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J.T., Schols L., and Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18 (1998) 106-108
25. Lashuel H.A., Hartley D., Petre B.M., Walz T., and Lansbury Jr. P.T. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418 (2002) 91
26. Lin M.T., and Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006) 787-795
27. Manczak M., Anekonda T.S., Henson E., Park B.S., Quinn J., and Reddy P.H. Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum Mol Genet 15 (2006) 1437-1449
28. McNaught K.S., and Olanow C.W. Protein aggregation in the pathogenesis of familial and sporadic Parkinson's disease. Neurobiol Aging 27 (2006) 530-545
29. Narhi L., Wood S.J., Steavenson S., Jiang Y., Wu G.M., Anafi D., Kaufman S.A., Martin F., Sitney K., Denis P., Louis J.C., Wypych J., Biere A.L., and Citron M. Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J Biol Chem 274 (1999) 9843-9846
30. Parihar M.S., Parihar A., Fujita M., Hashimoto M., and Ghafourifar P. Mitochondrial association of alpha-synuclein causes oxidative stress. Cell Mol Life Sci 65 (2008) 1272-1284
31. Parihar M.S., Parihar A., Villamena F.A., Vaccaro P.S., and Ghafourifar P. Inactivation of mitochondrial respiratory chain complex I leads mitochondrial nitric oxide synthase to become pro-oxidative. Biochem Biophys Res Commun 367 (2008) 761-767
32. Parihar M.S., Parihar A., Chen Z., and Nazarewicz R. Ghafourifar P. mAtNOS1 regulates mitochondrial functions and apoptosis of human neuroblastoma cells. Biochim Biophys Acta 1780 (2008) 921-926
33. Parihar M.S., Nazarewicz R.R., Kincaid E., Bringold U., and Ghafourifar P. Association of mitochondrial nitric oxide synthase activity with respiratory chain complex I. Biochem Biophys Res Commun 366 (2008) 23-28
34. Peluffo G., and Radi R. Biochemistry of protein tyrosine nitration in cardiovascular pathology. Cardiovasc Res 75 (2007) 291-302
35. Perier C., Bove J., Wu D.C., Dehay B., Choi D.K., Jackson-Lewis V., et al. Two molecular pathways initiate mitochondria-dependent dopaminergic neurodegeneration in experimental Parkinson's disease. Proc Natl Acad Sci USA 104 (2007) 8161-8166
36. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 (1997) 2045-2047
37. Raichur A., Vali S., and Gorin F. Dynamic modeling of alpha-synuclein aggregation for the sporadic and genetic forms of Parkinson's disease. Neuroscience 142 (2006) 859-870
38. Sayre L.M., Perry G., and Smith M.A. Oxidative stress and neurotoxicity. Chem Res Toxicol 21 (2008) 172-188
39. Shults C.W. Lewy bodies. Proc Natl Acad Sci USA 103 (2006) 1661-1668
40. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., et al. alpha-Synuclein locus triplication causes Parkinson's disease. Science 302 (2003) 41
41. Smith W.W., Jiang H., Pei Z., Tanaka Y., Morita H., Sawa A., et al. Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. Hum Mol Genet 14 (2005) 3801-3811
42. Souza J.M., Giasson B.I., Chen Q., Lee V.M., and Ischiropoulos H. Dityrosine cross-linking promotes formation of stable alpha-synuclein polymers. Implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J Biol Chem 275 (2000) 18344-18349
43. Spillantini M.G., Crowther R.A., Jakes R., Hasegawa M., and Goedert M. alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci USA 95 (1998) 6469-6473
44. Stack E.C., Ferro J.L., Kim J., Del Signore S.J., Goodrich S., Matson S., et al. Therapeutic attenuation of mitochondrial dysfunction and oxidative stress in neurotoxin models of Parkinson's disease. Biochim Biophys Acta 1782 (2008) 151-162
45. Trojanowski J.Q., and Lee V.M. Aggregation of neurofilament and alpha-synuclein proteins in Lewy bodies: implications for the pathogenesis of Parkinson disease and Lewy body dementia. Arch Neurol 55 (1998) 151-152
46. Vander Heiden M.G., Chandel N.S., Li X.X., Schumacker P.T., Colombini M., and Thompson C.B. Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc Natl Acad Sci US A 97 (2000) 4666-4671
47. Volles M.J., and Lansbury Jr. P.T. Relationships between the sequence of alpha-synuclein and its membrane affinity, fibrillization propensity, and yeast toxicity. J Mol Biol 366 (2007) 1510-1522
48. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., et al. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55 (2004) 164-173