Alterations in bioenergetic function induced by Parkinson's disease mimetic compounds: Lack of correlation with superoxide generation

Journal of Neurochemistry

Volumn 122, Issue 5, 2012, Pages 941-951

  Dranka, Brian P ^a   Zielonka, Jacek ^a   Kanthasamy, Anumantha G ^b   Kalyanaraman, Balaraman ^a  

^a FREE RADICAL RESEARCH CENTER   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

glycolysis; hydroethidine; mitochondria; reactive oxygen species

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; HYDROETHIDINE; OXIDOPAMINE; OXYGEN; PARAQUAT; ROTENONE; SUPEROXIDE;

ACIDIFICATION; ANIMAL CELL; ARTICLE; BIOENERGY; BIOSYNTHESIS; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOPAMINERGIC NERVE CELL; EXTRACELLULAR MATRIX; GLYCOLYSIS; METABOLIC RATE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXYGEN CONSUMPTION; PARKINSON DISEASE; PRIORITY JOURNAL; RAT;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ADENOSINE TRIPHOSPHATE; ADRENERGIC AGENTS; ANIMALS; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL LINE, TRANSFORMED; DOPAMINE AGENTS; DOPAMINERGIC NEURONS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; HERBICIDES; INSECTICIDES; NEUROTOXINS; OLIGOMYCINS; OXIDOPAMINE; OXYGEN CONSUMPTION; PARAQUAT; PROTON IONOPHORES; RATS; ROTENONE; SUPEROXIDES; TIME FACTORS;

EID: 84865321842     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07836.x     Document Type: Article

References (54)

1. Adams F. S., La Rosa F. G., Kumar S., Edwards-Prasad J., Kentroti S., Vernadakis A., Freed C. R., and, Prasad K. N., (1996) Characterization and transplantation of two neuronal cell lines with dopaminergic properties. Neurochem. Res. 21, 619-627. (Pubitemid 26151008)
2. Adams Jr J. D., Chang M. L., and, Klaidman L., (2001) Parkinson's disease - redox mechanisms. Curr. Med. Chem. 8, 809-814. (Pubitemid 32427909)
3. Anantharam V., Kaul S., Song C., Kanthasamy A., and, Kanthasamy A. G., (2007) Pharmacological inhibition of neuronal NADPH oxidase protects against 1-methyl-4-phenylpyridinium (MPP+)-induced oxidative stress and apoptosis in mesencephalic dopaminergic neuronal cells. Neurotoxicology 28, 988-997. (Pubitemid 47519806)
4. Beal M. F., (2003) Bioenergetic approaches for neuroprotection in Parkinson's disease. Ann. Neurol. 53, S39-S47; discussion S47-38.
5. Brown G. C., (2007) Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem. Soc. Trans. 035, 1119-1121. (Pubitemid 350206442)
6. Cannon J. R., Tapias V., Na H. M., Honick A. S., Drolet R. E., and, Greenamyre J. T., (2009) A highly reproducible rotenone model of Parkinson's disease. Neurobiol. Dis. 34, 279-290.
7. Castello P. R., Drechsel D. A., and, Patel M., (2007) Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J. Biol. Chem. 282, 14186-14193. (Pubitemid 47100444)
8. Clarke D. D., and, Sokoloff L., (1999) Circulation and energy metabolism of the brain, in Basic Neurochemistry-Molecular, Cellular, and Medical Aspects (, Siegel G. J., Agranoff B. W., Albers R. W., Fisher S. K., and, Uhler M. D., eds.), pp. 638-669. Lippincott-Raven, Philadelphia.
9. Collier T. J., Steece-Collier K., McGuire S., and, Sortwell C. E., (2003) Cellular models to study dopaminergic injury responses. Ann. N. Y. Acad. Sci. 991, 140-151. (Pubitemid 36793810)
10. Czerniczyniec A., Karadayian A. G., Bustamante J., Cutrera R. A., and, Lores-Arnaiz S., (2011) Paraquat induces behavioral changes and cortical and striatal mitochondrial dysfunction. Free Radic. Biol. Med. 51, 1428-1436.
11. Davey G. P., Peuchen S., and, Clark J. B., (1998) Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. J. Biol. Chem. 273, 12753-12757. (Pubitemid 28246828)
12. Dorsey E. R., Constantinescu R., Thompson J. P., et al. (2007) Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 68, 384-386. (Pubitemid 46184217)
13. Dranka B. P., Hill B. G., and, Darley-Usmar V. M., (2010) Mitochondrial reserve capacity in endothelial cells: the impact of nitric oxide and reactive oxygen species. Free Radic. Biol. Med. 48, 905-914.
14. Dranka B. P., Benavides G. A., Diers A. R., et al. (2011) Assessing bioenergetic function in response to oxidative stress by metabolic profiling. Free Radic. Biol. Med. 51, 1621-1635.
15. Drechsel D. A., and, Patel M., (2009) Differential contribution of the mitochondrial respiratory chain complexes to reactive oxygen species production by redox cycling agents implicated in parkinsonism. Toxicol. Sci. 112, 427-434.
16. Dunnett S. B., and, Lelos M., (2010) Behavioral analysis of motor and non-motor symptoms in rodent models of Parkinson's disease. Prog. Brain Res. 184, 35-51.
17. Duty S., and, Jenner P., (2011) Animal models of Parkinson's disease: a source of novel treatments and clues to the cause of the disease. Br. J. Pharmacol. 164, 1357-1391.
18. Frank D. M., Arora P. K., Blumer J. L., and, Sayre L. M., (1987) Model study on the bioreduction of paraquat, MPP+, and analogs. Evidence against a "redox cycling" mechanism in MPTP neurotoxicity. Biochem. Biophys. Res. Commun. 147, 1095-1104. (Pubitemid 17150587)
19. Fukui H., and, Moraes C. T., (2008) The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci. 31, 251-256.
20. Fukushima T., Yamada K., Isobe A., Shiwaku K., and, Yamane Y., (1993) Mechanism of cytotoxicity of paraquat. I. NADH oxidation and paraquat radical formation via complex I. Exp. Toxicol. Pathol. 45, 345-349. (Pubitemid 23349797)
21. Gee P., and, Davison A. J., (1989) Intermediates in the aerobic autoxidation of 6-hydroxydopamine: relative importance under different reaction conditions. Free Radic. Biol. Med. 6, 271-284. (Pubitemid 19076493)
22. Gerencser A. A., Neilson A., Choi S. W., Edman U., Yadava N., Oh R. J., Ferrick D. A., Nicholls D. G., and, Brand M. D., (2009) Quantitative microplate-based respirometry with correction for oxygen diffusion. Anal. Chem. 81, 6868-6878.
23. Ghosh A., Chandran K., Kalivendi S. V., Joseph J., Antholine W. E., Hillard C. J., Kanthasamy A., and, Kalyanaraman B., (2010) Neuroprotection by a mitochondria-targeted drug in a Parkinson's disease model. Free Radic. Biol. Med. 49, 1674-1684.
24. Hill B. G., Dranka B. P., Zou L., Chatham J. C., and, Darley-Usmar V. M., (2009) Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal. Biochem. J. 424, 99-107.
25. Huh S. H., Chung Y. C., Piao Y., et al. (2011) Ethyl pyruvate rescues nigrostriatal dopaminergic neurons by regulating glial activation in a mouse model of Parkinson's disease. J. Immunol. 187, 960-969.
26. Jekabsons M. B., and, Nicholls D. G., (2004) In situ respiration and bioenergetic status of mitochondria in primary cerebellar granule neuronal cultures exposed continuously to glutamate. J. Biol. Chem. 279, 32989-33000. (Pubitemid 39014759)
27. Jenner P., (2008) Preventing and controlling dyskinesia in Parkinson's disease - a view of current knowledge and future opportunities. Mov. Disord. 23, S585-S598.
28. Jin H., Kanthasamy A., Ghosh A., Yang Y., Anantharam V., and, Kanthasamy A. G., (2011) alpha-Synuclein negatively regulates protein kinase Cdelta expression to suppress apoptosis in dopaminergic neurons by reducing p300 histone acetyltransferase activity. J. Neurosci. 31, 2035-2051.
29. Johannessen J. N., Adams J. D., Schuller H. M., Bacon J. P., and, Markey S. P., (1986) 1-Methyl-4-phenylpyridine (MPP+) induces oxidative stress in the rodent. Life Sci. 38, 743-749. (Pubitemid 16163953)
30. Kalivendi S. V., Kotamraju S., Cunningham S., Shang T., Hillard C. J., and, Kalyanaraman B., (2003) 1-Methyl-4-phenylpyridinium (MPP+)-induced apoptosis and mitochondrial oxidant generation: role of transferrin-receptor- dependent iron and hydrogen peroxide. Biochem. J. 371, 151-164. (Pubitemid 36458089)
31. Keeney P. M., Dunham L. D., Quigley C. K., Morton S. L., Bergquist K. E., and, Bennett Jr J. P., (2009) Cybrid models of Parkinson's disease show variable mitochondrial biogenesis and genotype-respiration relationships. Exp. Neurol. 220, 374-382.
32. Klaidman L. K., Adams Jr J. D., Leung A. C., Kim S. S., and, Cadenas E., (1993) Redox cycling of MPP+: evidence for a new mechanism involving hydride transfer with xanthine oxidase, aldehyde dehydrogenase, and lipoamide dehydrogenase. Free Radic. Biol. Med. 15, 169-179. (Pubitemid 23218819)
33. Latchoumycandane C., Anantharam V., Jin H., and, Kanthasamy A., (2011) Dopaminergic neurotoxicant 6-OHDA induces oxidative damage through proteolytic activation of PKCdelta in cell culture and animal models of Parkinson's disease. Toxicol. Appl. Pharmacol. 256, 314-323.
34. Mazzio E. A., Reams R. R., and, Soliman K. F., (2004) The role of oxidative stress, impaired glycolysis and mitochondrial respiratory redox failure in the cytotoxic effects of 6-hydroxydopamine in vitro. Brain Res. 1004, 29-44. (Pubitemid 38368060)
35. Rodriguez-Pallares J., Parga J. A., Munoz A., Rey P., Guerra M. J., and, Labandeira-Garcia J. L., (2007) Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine-induced degeneration of dopaminergic neurons. J. Neurochem. 103, 145-156. (Pubitemid 47404195)
36. Sayre L. M., (1989) Biochemical mechanism of action of the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Toxicol. Lett. 48, 121-149. (Pubitemid 19213423)
37. Schapira A. H., (2012) Targeting mitochondria for neuroprotection in Parkinson's disease. Antioxid. Redox Signal. 16, 965-973.
38. Schapira A. H., and, Jenner P., (2011) Etiology and pathogenesis of Parkinson's disease. Mov. Disord. 26, 1049-1055.
39. Schneider L., Giordano S., Zelickson B. R., Johnson M. S., Benevides G. A., Ouyang X., Fineberg N., Darley-Usmar V. M., and, Zhang J., (2011) Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radic. Biol. Med. 51, 2007-2017.
40. Schulz J. B., and, Beal M. F., (1995) Neuroprotective effects of free radical scavengers and energy repletion in animal models of neurodegenerative disease. Ann. N. Y. Acad. Sci. 765, 100-110; discussion 116-108. (Pubitemid 26136233)
41. Scotcher K. P., Irwin I., DeLanney L. E., Langston J. W., and, Di Monte D., (1991) Mechanism of accumulation of the 1-methyl-4-phenylpyridinium species into mouse brain synaptosomes. J. Neurochem. 56, 1602-1607.
42. Snow B. J., Rolfe F. L., Lockhart M. M., Frampton C. M., O'Sullivan J. D., Fung V., Smith R. A., Murphy M. P., and, Taylor K. M., (2010) A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant MitoQ as a disease-modifying therapy in Parkinson's disease. Mov. Disord. 25, 1670-1674.
43. Surmeier D. J., Guzman J. N., Sanchez-Padilla J., and, Goldberg J. A., (2010) What causes the death of dopaminergic neurons in Parkinson's disease? Prog. Brain Res. 183, 59-77.
44. Tanner C. M., Kamel F., and, Ross G. W., et al. (2011) Rotenone, paraquat and Parkinson's Disease. Environ. Health Perspect. 119, 866-872.
45. Trimmer P. A., and, Bennett Jr J. P., (2009) The cybrid model of sporadic Parkinson's disease. Exp. Neurol. 218, 320-325.
46. Vander Heiden M. G., Cantley L. C., and, Thompson C. B., (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033.
47. Votyakova T. V., and, Reynolds I. J., (2001) DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 79, 266-277. (Pubitemid 32988942)
48. Wu M., Neilson A., Swift A. L., et al. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136. (Pubitemid 46115126)
49. Yacoubian T. A., and, Standaert D. G., (2009) Targets for neuroprotection in Parkinson's disease. Biochim. Biophys. Acta 1792, 676-687.
50. Zhang D., Anantharam V., Kanthasamy A., and, Kanthasamy A. G., (2007) Neuroprotective effect of protein kinase C delta inhibitor rottlerin in cell culture and animal models of Parkinson's disease. J. Pharmacol. Exp. Ther. 322, 913-922. (Pubitemid 47295809)
51. Zhao H., Kalivendi S., Zhang H., Joseph J., Nithipatikom K., Vasquez-Vivar J., and, Kalyanaraman B., (2003) Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic. Biol. Med. 34, 1359-1368. (Pubitemid 36570409)
52. Zielonka J., and, Kalyanaraman B., (2010) Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth. Free Radic. Biol. Med. 48, 983-1001.
53. Zielonka J., Hardy M., and, Kalyanaraman B., (2009) HPLC study of oxidation products of hydroethidine in chemical and biological systems: ramifications in superoxide measurements. Free Radic. Biol. Med. 46, 329-338.
54. Zielonka J., Zielonka M., Sikora A., Adamus J., Joseph J., Hardy M., Ouari O., Dranka B. P., and, Kalyanaraman B., (2012) Global profiling of reactive oxygen and nitrogen species in biological systems: high-throughput real-time analyses. J. Biol. Chem. 287, 2984-2995.