Mitochondria-targeted peptide antioxidants: Novel neuroprotective agents

Beal MF. Mitochondria take center stage in aging and neurodegeneration.Ann Neurol. 2005;58:495–505. Schapira AH. Mitochondrial involvement in Parkinson’s disease, Huntington’s disease, hereditary spastic paraplegia and Friedreich’s ataxia.Biochim Biophys Acta. 1999;1410:159–170. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants.Proc Natl Acad Sci USA. 2003;100: 4078–4083. Palacino JJ, Sagi D, Goldberg MS, et al. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice.J Biol Chem. 2004;279:18614–18622. Coskun PE, Beal MF, Wallace DC. Alzheimer’s brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication.Proc Natl Acad Sci USA. 2004;101:10726–10731. Lustbader JW, Cirilli M, Lin C, et al. ABAD directly links Abeta to mitochondrial toxicity in Alzheimer’s disease.Science. 2004;304:448–452. Crouch PJ, Blake R, Duce JA, et al. Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-betal-42.J Neurosci. 2005;25:672–679. Beckman JS, Estevez AG, Crow JP, Barbeito L. Superoxide dismutase and the death of motoneurons in ALS.Trends Neurosci. 2001;24:S15-S20. Mattiazzi M, D’Aurelio M, Gajewski CD, et al. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice.J Biol Chem. 2002;277:29626–29633. Ferreirinha F, Quattrini A, Pirozzi M, et al. Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport.J Clin Invest. 2004;113:231–242. Browne SE, Beal MF. The energetics of Huntington’s disease.Neurochem Res. 2004;29:531–546. Beal MF. Oxidatively modified proteins in aging and disease.Free Radic Biol Med. 2002;32:797–803. Reddy PH, Beal MF. Are mitochondria critical in the pathogenesis of Alzheimer’s disease?Brain Res Brain Res Rev. 2005;49:618–632. Andersen JK. Oxidative stress in neurodegeneration: cause or consequence?Nat Med. 2004;10:S18-S25. Giasson BI, Ischiropoulos H, Lee VM, Trojanowski JQ. The relationship between oxidative/nitrative stress and pathological inclusions in Alzheimer’s and Parkinson’s diseases.Free Radic Biol Med. 2002;32:1264–1275. McLellan ME, Kajdasz ST, Hyman BT, Bacskai BJ. In vivo imaging of reactive oxygen species specifically associated with thioflavine S-positive amyloid plaques by multiphoton microscopy.J Neurosci. 2003;23:2212–2217. Casoni F, Basso M, Massignan T, et al. Protein nitration in a mouse model of familial amyotrophic lateral sclerosis: possible multifunctional role in the pathogenesis.J Biol Chem. 2005;280: 16295–16304. Turrens JF. Superoxide production by the mitochondrial respiratory chain.Biosci Rep. 1997;17:3–8. Muller FL, Liu Y, Van RH. Complex III releases superoxide to both sides of the inner mitochondrial membrane.J Biol Chem. 2004;279: 49064–49073. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging.Free Radic Biol Med. 2000;29: 222–230. Imam SZ, Karahalil B, Hogue BA, Souza-Pinto NC, Bohr VA. Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner.Neurobiol Aging. In press. Navarro A. Mitochondrial enzyme activities as biochemical markers of aging.Mol Aspects Med. 2004;25:37–48. MacMillan-Crow LA, Crow JP, Thompson JA. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues.Biochemistry. 1998;37:1613–1622. Chen JJ, Yu BP. Alterations in mitochondrial membrane fluidity by lipid peroxidation products.Free Radic Biol Med. 1994;17: 411–418. Laganiere S, Yu BP. Modulation of membrane phospholipid fatty acid composition by age and food restriction.Gerontology. 1993;39:7–18. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species.Biochemistry (Mosc). 2005;70:200–214. Petrosillo G, Ruggiero FM, Paradies G. Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria.FASEB J. 2003;17:2202–2208. Shidoji Y, Hayashi K, Komura S, Ohishi N, Yagi K. Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation.Biochem Biophys Res Commun. 1999;264:343–347. Crompton M. The mitochondrial permeability transition pore and its role in cell death.Biochem J. 1999;341:233–249. Kroemer G, Dallaporta B, Resche-Rigon M. the mitochondrial death/life regulator in apoptosis and necrosis.Annu Rev Physiol. 1998;60:619–642. Vieira HL, Belzacq AS, Haouzi D, et al. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal.Oncogene. 2001;20:4305–4316. Ott M, Robertson JD, Gogvadze V, Zhivotovsky B, Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process.Proc Natl Acad Sci USA. 2002;99:1259–1263. Marzo I, Brenner C, Zamzami N, et al. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis.Science. 1998;281:2027–2031. Green DR, Reed JC. Mitochondrial and apoptosis.Science. 1998;281:1309–1312. Li P, Nijhawan D, Budihardjo I, et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade.Cell. 1997;91:479–489. Erdelyi K, Bakondi E, Gergely P, Szabo C, Virag L. Pathophysiologic role of oxidative stress-induced poly(ADP-ribose) polymerase-1 activation: focus on cell death and transcriptional regulation.Cell Mol Life Sci. 2005;62:751–759. Beal MF. Mitochondria, oxidative damage, and inflammation in Parkinson’s disease.Ann NY Acad Sci. 2003;991:120–131. Levites Y, Weinreb O, Maor G, Youdim MB, Mandel S. Green tea polyphenol (−)-epigallocatechin-3-gallate prevents N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced dopaminergic neurodegeneration.J Neurochem. 2001;78:1073–1082. Miller ER, III, Pastor-Barriuso R, Dalal D, Riemersma RA, Appel LJ, Guallar E. Meta-analysis high-dosage vitamin E supplementation may increase all-cause mortality.Ann Intern Med. 2005;142:37–46. Beal MF, Matthews RT. Coenzyme Q10 in the central nervous system and its potential usefulness in the treatment of neurodegenerative diseases.Mol Aspects Med. 1997;18 Suppl:S169-S179. Day BJ. Catalytic antioxidants: a radical approach to new therapeutics.Drug Discov Today. 2004;9:557–566. Kaul S, Kanthasamy A, Kitazawa M, Anantharam V, Kanthasamy AG. Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration.Eur J Neurosci. 2003;18:1387–1401. Pong K, Doctrow SR, Baudry M. Prevention of 1-methyl-4-phenylpyridinium-and 6-hydroxydopamine-induced nitration of tyrosine hydroxylase and neurotoxicity by EUK-134, a superoxide dismutase and catalase mimetic, in cultured dopaminergic neurons.Brain Res. 2000;881:182–189. Jung C, Rong Y, Doctrow S, Baudry M, Malfroy B, Xu Z. Synthetic superoxide dismutase/catalase mimetics reduce oxidative stress and prolong survival in a mouse amyotrophic lateral sclerosis model.Neurosci Lett. 2001;304:157–160. Peng J, Stevenson FF, Doctrow SR, Andersen JK. Superoxide dismutase/catalase mimetics are neuroprotective against selective paraquat-mediated dopaminergic neuron death in the substantial nigra: implications for Parkinson disease.J Biol Chem. 2005;280:29194–29198. Petri S, Kiaei M, Kipiani K, et al. Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis.Neurobiol Dis. 2006;22:40–49. Melov S, Schneider JA, Day BJ, et al. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase.Nat Genet. 1998;18:159–163. Schriner SE, Linford NJ, Martin GM, et al. Extension of murine life span by overexpression of catalase targeted to mitochondria.Science. 2005;308:1909–1911. Shen SS, Nauduri D, Anders MW. Targeting antioxidants to mitochondria: a new therapeutic direction.Biochim Biophys Acta. 2006;1762:256–265. Murphy MP, Smith RA. Drug delivery to mitochondria: the key to mitochondrial medicine.Adv Drug Deliv Rev. 2000;41: 235–250. Jauslin ML, Meier T, Smith RA, Murphy MP. Mitochondria-targeted antioxidants protect Friedreich Ataxia fibroblasts from endogenous oxidative stress more effectively than untargeted antioxidants.FASEB J. 2003;17:1972–1974. Dhanasekaran A, Kotamraju S, Kalivendi SV, et al. Supplementation of endothelial cells with mitochondria-targeted antioxidants inhibit peroxide-induced mitochondrial iron uptake, oxidative damage, and apoptosis.J Biol Chem. 2004;279: 37575–37587. Smith RA, Porteous CM, Gane AM, Murphy MP. Delivery of bioactive molecules to mitochondria in vivo.Proc Natl Acad Sci USA. 2003;100:5407–5412. Adlam VJ, Harrison JC, Porteous CM, et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury.FASEB J. 2005;19:1088–1095. Smith RA, Porteous CM, Coulter CV, Murphy MP. Selective targeting of an antioxidant to mitochondria.Eur J Biochem. 1999;263:709–716. Kelso GF, Porteous CM, Coulter CV, et al. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties.J Biol Chem. 2001;276:4588–4596. James AM, Cocheme HM, Smith RA, Murphy MP. Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species. Implications for the use of exogenous ubiquinones as therapies and experimental tools.J Biol Chem. 2005;280:21295–21312. Zhao K, Zhao GM, Wu D, et al. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial sweeling, oxidative cell death, and reperfusion injury.J Biol Chem. 2004;279:34682–34690. Szeto HH. Cell-permeable, mitochondrial-targeted, peptide antioxidants.AAPS J. 2006;8:E277-E283. Winterbourn CC, Parsons-Mair HN, Gebicki S, Gebicki JM, Davies MJ. Requirements for superoxide-dependent tyrosine hydroperoxide formation in peptides.Biochem J. 2004;381: 241–248. Zhao K, Luo G, Zhao GM, Schiller PW, Szeto HH. Transcellular transport of a highly polar 3+ net charge opioid tetrapeptide.J Pharmacol Exp Ther. 2003;304:425–432. Zhao K, Luo G, Giannelli S, Szeto HH. Mitochondria-targeted peptide prevents mitochondrial depolarization and apoptosis induced by tert-butyl hydroperoxide in neuronal cell lines.Biochem Pharmacol. 2005;70:1796–1806. Drin G, Cottin S, Blanc E, Rees AR, Temsamani J. Studies on the internalization mechanism of cationic cell-penetrating peptides.J Biol Chem. 2003;278:31192–31201. Derossi D, Calvet S, Trembleau A, Brunissen A, Chassaing G, Prochiantz A. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent.J Biol Chem. 1996;271:18188–18193. Szeto HH, Schiller PW, Zhao K, Luo G. Fluorescent dyes alter intracellular targeting and function of cell-penetrating tetrapeptides.FASEB J. 2005;19:118–120. Haidara K, Morel I, Abalea V, Gascon BM, Denizeau F. Mechanism of tert-butylhydroperoxide induced apoptosis in rat hepatocytes: involvement of mitochondria and endoplasmic reticulum.Biochim Biophys Acta. 2002;1542:173–185. Piret JP, Arnould T, Fuks B, Chatelain P, Remacle J, Michiels C. Mitochondria permeability transition-dependent tert-butyl hydroperoxide-induced apoptosis in hepatoma HepG2 cells.Biochem Pharmacol. 2004;67:611–620. Byrne AM, Lemasters JJ, Nieminen AL. Contribution of increased mitochondrial free Ca2+ to the mitochondrial permeability transition induced by tert-butylhydroperoxide in rat hepatocytes.Hepatology. 1999;29:1523–1531. Nieminen AL, Byrne AM, Herman B, Lemasters JJ. Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species.Am J Physiol. 1997;272:C1286-C1294. Pias EK, Ekshyyan OY, Rhoads CA, Fuseler J, Harrison L, Aw TY. Differential effects of superoxide dismutase isoform expression on hydroperoxide-induced apoptosis in PC-12 cells.J Biol Chem. 2003;278:13294–13301. Szeto HH, Lovelace JL, Fridland G, et al. In vivo pharmacokinetics of selective mu-opioid peptide agonists.J Pharmacol Exp Ther. 2001;298:57–61. Zhao GM, Wu D, Soong Y, et al. Profound spinal tolerance after repeated exposure to a highly selective mu-opioid peptide agonist: role of delta-opioid receptors.J Pharmacol Exp Ther. 2002;302:188–196. Przyklenk K. Pharmacologic treatment of the stunned myocardium: the concepts and the challenges.Coron Artery Dis. 2001;12:363–369. Masini E, Cuzzocrea S, Mazzon E, Marzocca C, Mannaioni PF. Salvemini D. Protective effects of M40403, a selective superoxide dismutase mimetic, in myocardial ischaemia and reperfusion injury in vivo.Br J Pharmacol. 2002;136:905–917. Mackensen GB, Patel M, Sheng H, et al. Neuroprotection from delayed postischemic administration of a metalloporphyrin catalytic antioxidant.J Neurosci. 2001;21:4582–4592. Wu D, Soong Y, Zhao GM, Szeto HH. A highly potent peptide analgesic that protects against ischemia-reperfusion-induced myocardial stunning.Am J Physiol Heart Circ Physiol. 2002;283: H783-H791. Song W, Shin J, Lee J, et al. A potent opiate agonist protects against myocardial stunning during myocardial ischemia and reperfusion in rats.Coron Artery Dis. 2005;16:407–410. Cho J, Won K, Wu D, et al. Potent mitochondria-targeted peptides reduce myocardial infarction in rats.Coron Artery Dis. 2006; In press. Cho S, Szeto HH, Kim HJ, Pinto J.A cell permeable antioxidant peptide SS31 attenuates CD36-mediated ischemic injury via normalizing redox state [abstract]. Washington, DC: Society for Neuroscience; 2005. Vijayvergiya C, Beal MF, Buck J, Manfredi G. Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice.J Neurosci. 2005;25:2463–2470. Petri S, Kiaei M, Damiano M, et al. Cell-permeable peptide antioxidants as a novel therapeutic approach in a mouse model of amyotrophic lateral sclerosis.J Neurochem. 2006;98: 1141–1148.