The role of oxidative stress, impaired glycolysis and mitochondrial respiratory redox failure in the cytotoxic effects of 6-hydroxydopamine in vitro - PubMed (original) (raw)
Comparative Study
The role of oxidative stress, impaired glycolysis and mitochondrial respiratory redox failure in the cytotoxic effects of 6-hydroxydopamine in vitro
Elizabeth A Mazzio et al. Brain Res. 2004.
Abstract
The neurotoxin, 6-hydroxydopamine (6-OHDA) has been implicated in the neurodegenerative process of Parkinson's disease. The current study was designed to elucidate the toxicological effects of 6-OHDA on energy metabolism in neuroblastoma (N-2A) cells. The toxicity of 6-OHDA corresponds to the total collapse of anaerobic/aerobic cell function, unlike other mitochondrial toxins such as MPP+ that target specific loss of aerobic metabolism. The toxicity of 6-OHDA paralleled the loss of mitochondrial oxygen (O2) consumption (MOC), glycolytic activity, ATP, H+ ion gradients, membrane potential and accumulation of the autoxidative product, hydrogen peroxide (H2O2). Removing H2O2 with nonenzymatic stoichiometric scavengers, such as carboxylic acids, glutathione and catalase yielded partial protection. The rapid removal of H2O2 with pyruvate or catalase restored only anaerobic glycolysis, but did not reverse the loss of MOC, indicating mitochondrial impairment is independent of H2O2. The H2O2 generated by 6-OHDA contributed toward the loss of anaerobic glycolysis through lipid peroxidation and lactic acid dehydrogenase inhibition. The ability of 6-OHDA to maintain oxidized cytochrome c (CYT-C-OX) in its reduced form (CYT-C-RED), appears to play a role in mitohondrial impairment. The reduction of CYT-C by 6-OHDA, was extensive, occurred within minutes, preceded formation of H2O2 and was unaffected by catalase or superoxide dismutase. At similar concentrations, 6-OHDA readily altered the valence state of iron [Fe(III)] to Fe(II), which would also theoretically sustain CYT-C in its reduced form. In isolated mitochondria, 6-OHDA had negligible effects on complex I, inhibited complex II and interfered with complex III by maintaining the substrate, CYT-C in a reduced state. 6-OHDA caused a transient and potent surge in isolated cytochrome oxidase (complex IV) activity, with rapid recovery as a result of 6-OHDA recycling CYT-C-OX to CYT-C-RED. Typical mitochondrial toxins such as MPP+, azide and antimycin appeared to inhibit the catalytic activity of ETC enzymes. In contrast, 6-OHDA alters the redox of the cytochromes, resulting in loss of substrate availability and obstruction of oxidation-reduction events. Complete cytoprotection against 6-OHDA toxicity and restored MOC was achieved by combining catalase with CYT-C (horse heart). In summary, CYT-C reducing properties are unique to catecholamine neurotransmitters, and may play a significant role in selective vulnerability of dopaminergic neurons to mitochondrial insults.
Similar articles
- Dopamine transporter-mediated cytotoxicity of 6-hydroxydopamine in vitro depends on expression of mutant alpha-synucleins related to Parkinson's disease.
Lehmensiek V, Tan EM, Liebau S, Lenk T, Zettlmeisl H, Schwarz J, Storch A. Lehmensiek V, et al. Neurochem Int. 2006 Apr;48(5):329-40. doi: 10.1016/j.neuint.2005.11.008. Epub 2006 Jan 6. Neurochem Int. 2006. PMID: 16406146 - Loss of cardiolipin in palmitate-treated GL15 glioblastoma cells favors cytochrome c release from mitochondria leading to apoptosis.
Buratta M, Castigli E, Sciaccaluga M, Pellegrino RM, Spinozzi F, Roberti R, Corazzi L. Buratta M, et al. J Neurochem. 2008 May;105(3):1019-31. doi: 10.1111/j.1471-4159.2007.05209.x. Epub 2007 Dec 24. J Neurochem. 2008. PMID: 18182042 - Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging.
Wei YH, Wu SB, Ma YS, Lee HC. Wei YH, et al. Chang Gung Med J. 2009 Mar-Apr;32(2):113-32. Chang Gung Med J. 2009. PMID: 19403001 Review. - The "pro-apoptotic genies" get out of mitochondria: oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes.
Kagan VE, Tyurina YY, Bayir H, Chu CT, Kapralov AA, Vlasova II, Belikova NA, Tyurin VA, Amoscato A, Epperly M, Greenberger J, Dekosky S, Shvedova AA, Jiang J. Kagan VE, et al. Chem Biol Interact. 2006 Oct 27;163(1-2):15-28. doi: 10.1016/j.cbi.2006.04.019. Epub 2006 May 12. Chem Biol Interact. 2006. PMID: 16797512 Review.
Cited by
- Targeting microglia-mediated neurotoxicity: the potential of NOX2 inhibitors.
Surace MJ, Block ML. Surace MJ, et al. Cell Mol Life Sci. 2012 Jul;69(14):2409-27. doi: 10.1007/s00018-012-1015-4. Epub 2012 May 13. Cell Mol Life Sci. 2012. PMID: 22581365 Free PMC article. Review. - Alterations in bioenergetic function induced by Parkinson's disease mimetic compounds: lack of correlation with superoxide generation.
Dranka BP, Zielonka J, Kanthasamy AG, Kalyanaraman B. Dranka BP, et al. J Neurochem. 2012 Sep;122(5):941-51. doi: 10.1111/j.1471-4159.2012.07836.x. Epub 2012 Jul 11. J Neurochem. 2012. PMID: 22708893 Free PMC article. - Air pollutants disrupt iron homeostasis to impact oxidant generation, biological effects, and tissue injury.
Ghio AJ, Soukup JM, Dailey LA, Madden MC. Ghio AJ, et al. Free Radic Biol Med. 2020 May 1;151:38-55. doi: 10.1016/j.freeradbiomed.2020.02.007. Epub 2020 Feb 21. Free Radic Biol Med. 2020. PMID: 32092410 Free PMC article. Review. - Investigating the neuroprotective potential of rAAV2-PCBP1-EGFP gene therapy against a 6-OHDA-induced model of Parkinson's disease.
Ma LY, Wang L, Liang J, Huo L. Ma LY, et al. Brain Behav. 2024 Jan;14(1):e3376. doi: 10.1002/brb3.3376. Brain Behav. 2024. PMID: 38376022 Free PMC article. - Glycolytic enzymes in non-glycolytic web: functional analysis of the key players.
Malla A, Gupta S, Sur R. Malla A, et al. Cell Biochem Biophys. 2024 Jun;82(2):351-378. doi: 10.1007/s12013-023-01213-5. Epub 2024 Jan 9. Cell Biochem Biophys. 2024. PMID: 38196050 Review.