Cell‐permeable peptide antioxidants as a novel therapeutic approach in a mouse model of amyotrophic lateral sclerosis
Abstract
Reactive oxygen species (ROS) play a major role in the pathogenesis of neurodegenerative diseases. They are important contributors to necrotic and apoptotic cell death. A major proportion of cellular ROS is generated at the inner mitochondrial membrane by the respiratory chain. In the present study, we investigated a novel peptide antioxidant (SS‐31) targeted to the inner mitochondrial membrane for its therapeutic effects both in vitro and in vivo in the G93A mouse model of amyotrophic lateral sclerosis (ALS). SS‐31 protected against cell death induced by hydrogen peroxide in vitro in neuronal cells stably transfected with either wild‐type or mutant Cu/Zn superoxide dismutase (SOD1). Daily intraperitoneal injections of SS‐31 (5 mg/kg), starting at 30 days of age, led to a significant improvement in survival and motor performance. In comparison with vehicle‐treated G93A mice, SS‐31‐treated mice showed a decreased cell loss and a decrease in immunostaining for markers of oxidative stress in the lumbar spinal cord. This further enhances the concept that pharmacological modification of oxidative stress is a therapeutic option for the treatment of ALS.
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SS-31 mediated significant neuroprotection against cell death induced by hydrogen peroxide in SOD1 neuronal cells.
“We found SS-31 mediated significant neuroprotection against cell death induced by hydrogen peroxide in SOD1 neuronal cells.”
From Mitochondrial Approaches for Neuroprotection (2008) · cites this paper as [180]
Daily intraperitoneal injections of SS-31 (5 mg/kg), starting at 30 days of age, led to a significant improvement in survival and motor performance in the G93A transgenic mouse model of ALS.
“Further, daily intraperitoneal injections of SS-31 (5 mg/kg), starting at 30 days of age, led to a significant improvement in survival and motor performance in the G93A transgenic mouse model of ALS.”
From Mitochondrial Approaches for Neuroprotection (2008) · cites this paper as [180]
Such peptides reduce intracellular ROS and cell death in neuronal and pancreatic islet cells and reduce skeletal myocyte H2O2 production and preserve insulin sensitivity in rats fed a high-fat diet.
“Such peptides reduce intracellular ROS and cell death in neuronal (256) and pancreatic islet cells (309) and recently were reported to reduce skeletal myocyte H2O2 production and to preserve insulin sensitivity in rats fed a high-fat diet (14).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [256]
Cites
Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J. P., Deng, H.-X., et al. (1993) · Nature · doi:10.1038/362059a0 · Cited by 7,062 · see citing works
Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes
Esterbauer, H., Schaur, R. J., & Zollner, H. (1991) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(91)90192-6 · Cited by 6,672 · see citing works
Motor Neuron Degeneration in Mice that Express a Human Cu,Zn Superoxide Dismutase Mutation
Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H.-X., et al. (1994) · Science · doi:10.1126/science.8209258 · Cited by 4,143 · see citing works
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · see citing works
Wong, P. C., Pardo, C. A., Borchelt, D., Lee, M. K., Copeland, N. G., Jenkins, N. A., Sisodia, S. S., Cleveland, D. W., & Price, D. L. (1995) · Neuron · doi:10.1016/0896-6273(95)90259-7 · Cited by 1,439 · see citing works
Mitochondria take center stage in aging and neurodegeneration
Beal, M. F. (2005) · Annals of Neurology · doi:10.1002/ana.20624 · Cited by 957 · see citing works
Self-citationMitochondrial damage induced by conditions of oxidative stress
Kowaltowski, A. J., & Vercesi, A. E. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00216-0 · Cited by 866 · see citing works
Evidence of Increased Oxidative Damage in Both Sporadic and Familial Amyotrophic Lateral Sclerosis
Ferrante, R. J., Browne, S. E., Shinobu, L. A., Bowling, A. C., Baik, M. J., MacGarvey, U. M., Kowall, N. W., Brown, R. H., & Beal, M. F. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.69052064.x · Cited by 808 · see citing works
Self-citationZhao, K., Zhao, G.-M., Wu, D., Soong, Y., Birk, A. V., Schiller, P. W., & Szeto, H. H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402999200 · Cited by 782 · see citing works
Self-citationKong, J., & Xu, Z. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03241.1998 · Cited by 723 · see citing works
Evidence that 4-Hydroxynonenal Mediates Oxidative Stress-Induced Neuronal Apoptosis
Kruman, I. I., Bruce‐Keller, A. J., Bredesen, D. E., Waeg, G., & Mattson, M. P. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05089.1997 · Cited by 719 · see citing works
Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis
Klivenyi, P., Ferrante, R. J., Matthews, R. T., Bogdanov, M. B., Klein, A. M., Andreassen, O. A., Mueller, G., Wermer, M., Kaddurah-Daouk, R., & Beal, M. F. (1999) · Nature Medicine · doi:10.1038/6568 · Cited by 682 · see citing works
Self-citationMattiazzi, M., D’Aurelio, M., Gajewski, C. D., Martushova, K., Kiaei, M., Beal, M. F., & Manfredi, G. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203065200 · Cited by 616 · see citing works
Self-citationIncreased 3‐nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis
Beal, M. F., Ferrante, R. J., Browne, S. E., Matthews, R. T., Kowall, N. W., & Brown, R. H. (1997) · Annals of Neurology · doi:10.1002/ana.410420416 · Cited by 599 · see citing works
Self-citationMatthews, R. T., Yang, L., Browne, S., Baik, M., & Beal, M. F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.15.8892 · Cited by 557 · see citing works
Self-citationMark, R. J., Pang, Z., Geddes, J. W., Uchida, K., & Mattson, M. P. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-03-01046.1997 · Cited by 551 · see citing works
Toxicity of Familial ALS-Linked SOD1 Mutants from Selective Recruitment to Spinal Mitochondria
Liu, J., Lillo, C., Jonsson, P. A., Velde, C. V., Ward, C. M., Miller, T. M., Subramaniam, J. R., Rothstein, J. D., Marklund, S. L., Andersen, P. M., et al. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.016 · Cited by 506 · see citing works
Pasinelli, P., Belford, M. E., Lennon, N. J., Bacskai, B. J., Hyman, B. T., Trotti, D., & Brown, R. H. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.021 · Cited by 506 · see citing works
Pasinelli, P., Houseweart, M. K., Brown, R. H., & Cleveland, D. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240305897 · Cited by 344 · see citing works
Increased lipid peroxidation in sera of ALS patients
Simpson, E. P., Henry, Y. K., Henkel-Tigges, J., Smith, R. G., & Appel, S. H. (2004) · Neurology · doi:10.1212/wnl.62.10.1758 · Cited by 328 · see citing works
Mitochondrial Implication in Accidental and Programmed Cell Death: Apoptosis and Necrosis
Zamzami, N., Hirsch, T., Dallaporta, B., PETIT, P. X., & Kroemer, G. (1997) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1022694131572 · Cited by 326 · see citing works
Bruijn, L. I., Beal, M. F., Bêcher, M. W., Schulz, J. B., Wong, P. C., Price, D. L., & Cleveland, D. W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.14.7606 · Cited by 290 · see citing works
Self-citationMitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis
Menzies, F. M. (2002) · Brain · doi:10.1093/brain/awf167 · Cited by 279 · see citing works
Higgins, C. M. J., Jung, C., & Xu, Z. (2003) · BMC Neuroscience · doi:10.1186/1471-2202-4-16 · Cited by 262 · see citing works
Zhao, K., Luo, G., Giannelli, S., & Szeto, H. H. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.08.022 · Cited by 251 · see citing works
Self-citationVijayvergiya, C., Beal, M. F., Buck, J., & Manfredi, G. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4385-04.2005 · Cited by 251 · see citing works
Self-citationFerrante, R. J., Shinobu, L. A., Schulz, J. B., Matthews, R. T., Thomas, C. E., Kowall, N. W., Gurney, M. E., & Beal, M. F. (1997) · Annals of Neurology · doi:10.1002/ana.410420309 · Cited by 251 · see citing works
Self-citationDamiano, M. G., Starkov, A. A., Petri, S., Kipiani, K., Kiaei, M., Mattiazzi, M., Beal, M. F., & Manfredi, G. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03619.x · Cited by 247 · see citing works
Self-citationCarrı̀, M. T., Ferri, A., Battistoni, A., Famhy, L., Gabbianelli, R., Poccia, F., & Rotilio, G. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01051-x · Cited by 221 · see citing works
Pasinelli, P., Borchelt, D., Houseweart, M. K., Cleveland, D. W., & Brown, R. H. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15763 · Cited by 221 · see citing works
Klivènyi, P., Kiaei, M., Gardian, G., Calingasan, N. Y., & Beal, M. F. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02160.x · Cited by 201 · see citing works
Self-citationNeely, M. D., Sidell, K. R., Graham, D. G., & Montine, T. J. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0722323.x · Cited by 186 · see citing works
Protein Nitration in a Mouse Model of Familial Amyotrophic Lateral Sclerosis
Casoni, F., Basso, M., Massignan, T., Gianazza, E., Cheroni, C., Salmona, M., Bendotti, C., & Bonetto, V. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413111200 · Cited by 180 · see citing works
Synthesis and in vitro opioid activity profiles of DALDA analogues
Schiller, P. W., Nguyen, T. M. ‐., Berezowska, I., Dupuis, S., Weltrowska, G., Chung, N. N., & Lemieux, C. (2000) · European Journal of Medicinal Chemistry · doi:10.1016/s0223-5234(00)01171-5 · Cited by 162 · see citing works
Petri, S., Kiaei, M., Kipiani, K., Chen, J., Calingasan, N. Y., Crow, J. P., & Beal, M. F. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.09.013 · Cited by 161 · see citing works
Self-citationMarzia Perluigi, A., Poon, H. F., Hensley, K., Pierce, W. M. J., Klein, J. B., Calabrese, V., Marco, C. M. D., & Butterfield, D. A. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.12.021 · Cited by 151 · see citing works
Transcellular Transport of a Highly Polar 3+ Net Charge Opioid Tetrapeptide
Zhao, K., Luo, G., Zhao, G., Schiller, P. W., & Szeto, H. H. (2003) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.040147 · Cited by 150 · see citing works
Self-citationManganese porphyrin given at symptom onset markedly extends survival of ALS mice
Crow, J. P., Calingasan, N. Y., Chen, J., Hill, J. L., & Beal, M. F. (2005) · Annals of Neurology · doi:10.1002/ana.20552 · Cited by 136 · see citing works
Self-citationMitochondrial dysfunction and amyotrophic lateral sclerosis
Hervías, I., Beal, M. F., & Manfredi, G. (2005) · Muscle & Nerve · doi:10.1002/mus.20489 · Cited by 122 · see citing works
Self-citationIncreased oxidative damage to DNA in an animal model of amyotrophic lateral sclerosis
Aguirre, N., Beal, M. F., Matson, W. R., & Bogdanov, M. B. (2005) · Free Radical Research · doi:10.1080/10715760400027979 · Cited by 90 · see citing works
Self-citationWu, A. S., Kiaei, M., Aguirre, N., Crow, J. P., Calingasan, N. Y., Browne, S. E., & Beal, M. F. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01639.x · Cited by 88 · see citing works
Self-citationGalindo, M. F., Jordán, J., Gonzalez-Garcia, C., & Ceña, V. (2003) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705309 · Cited by 73 · see citing works
Mechanisms of 4-hydroxynonenal-induced neuronal microtubule dysfunction
Neely, M. D., Boutté, A. M., Milatović, D., & Montine, T. J. (2005) · Brain Research · doi:10.1016/j.brainres.2004.12.027 · Cited by 65 · see citing works
Maxwell, M. M., Pasinelli, P., Kazantsev, A. G., & Brown, R. H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308726100 · Cited by 59 · see citing works
Induction of motor neuron apoptosis by free 3‐nitro‐ l ‐tyrosine
Peluffo, H., Shacka, J. J., Ricart, K. C., Bisig, C. G., Palma, L. M., Pritsch, O., Kamaid, A., Eiserich, J. P., Crow, J. P., Barbeito, L., et al. (2004) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2004.02363.x · Cited by 56 · see citing works
Song, W., Shin, J., Lee, J., Kim, H. J., Oh, D.-J., Edelberg, J. M., Wong, S. C., Szeto, H. H., & Hong, M. K. (2005) · Coronary Artery Disease · doi:10.1097/00019501-200509000-00011 · Cited by 31 · see citing works
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Anderson, E. J., Lustig, M. E., Boyle, K. E., Woodlief, T. L., Kane, D. A., Lin, C.-T., Price, J. W., Kang, L., Rabinovitch, P. S., Szeto, H. H., et al. (2009) · Journal of Clinical Investigation · doi:10.1172/jci37048 · Cited by 1,253 · see citing works
Self-citationMitochondrial Dysfunction in Neurodegenerative Diseases
Johri, A., & Beal, M. F. (2012) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.192138 · Cited by 806 · see citing works
Self-citationSivitz, W. I., & Yorek, M. A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2531 · Cited by 742 · see citing works
Szeto, H. H. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12461 · Cited by 550 · see citing works
Self-citationMitochondrial Dysfunction and Biogenesis in Neurodegenerative diseases: Pathogenesis and Treatment
Golpich, M., Amini, E., Mohamed, Z., Raymond, A. A., Ibrahim, N. M., & Ahmadiani, A. (2016) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12655 · Cited by 540 · see citing works
Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS
Turner, B. J., & Talbot, K. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.01.001 · Cited by 495 · see citing works
Mitochondrial oxidative stress in aging and healthspan
Dai, D., Chiao, Y. A., Marcinek, D. J., Szeto, H. H., & Rabinovitch, P. S. (2014) · Longevity & Healthspan · doi:10.1186/2046-2395-3-6 · Cited by 481 · see citing works
Self-citationMitochondria and Reactive Oxygen Species in Aging and Age-Related Diseases
Giorgi, C., Marchi, S., Simões, I. C. M., Ren, Z., Morciano, G., Perrone, M., Patalas‐Krawczyk, P., Borchard, S., Jędrak, P., Pierzynowska, K., et al. (2018) · International review of cytology · doi:10.1016/bs.ircmb.2018.05.006 · Cited by 467 · see citing works
Mitochondria and Cardiovascular Aging
Dai, D., Rabinovitch, P. S., & Ungvari, Z. I. (2012) · Circulation Research · doi:10.1161/circresaha.111.246140 · Cited by 435 · see citing works
Mitochondrial Diseases of the Brain
Chaturvedi, R. K., & Beal, M. F. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.03.018 · Cited by 416 · see citing works
Self-citationAmyotrophic Lateral Sclerosis: A Focus on Disease Progression
Calvo, A. C., Manzano, R., de Mendonça, D. M. F., Muñoz, M. J., Zaragoza, P., & Osta, R. (2014) · BioMed Research International · doi:10.1155/2014/925101 · Cited by 404 · see citing works
Neuroprotective strategies involving ROS in Alzheimer disease
Dumont, M., & Beal, M. F. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.11.026 · Cited by 402 · see citing works
Self-citationReddy, P. H., Tripathi, R., Troung, Q., Tirumala, K., Reddy, T. P., Anekonda, V., Shirendeb, U. P., Calkins, M. J., Reddy, A. P., Mao, P., et al. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.10.011 · Cited by 394 · see citing works
Mitochondria-targeted peptide antioxidants: Novel neuroprotective agents
Szeto, H. H. (2006) · The AAPS Journal · doi:10.1208/aapsj080362 · Cited by 332 · see citing works
Self-citationCardiac Aging: From Molecular Mechanisms to Significance in Human Health and Disease
Dai, D.-F., Chen, T., Johnson, S. C., Szeto, H., & Rabinovitch, P. S. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4179 · Cited by 334 · see citing works
Self-citationMitochondria as a Therapeutic Target in Heart Failure
Bayeva, M., Gheorghiade, M., & Ardehali, H. (2012) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2012.08.1021 · Cited by 336 · see citing works
Oxidative stress in spinal cord injury and antioxidant-based intervention
Jia, Z., Zhu, H., Li, J., Wang, X., Misra, H., & Li, Y. (2011) · Spinal Cord · doi:10.1038/sc.2011.111 · Cited by 330 · see citing works
Molecular Strategies for Targeting Antioxidants to Mitochondria: Therapeutic Implications
Apostolova, N., & Víctor, V. M. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5952 · Cited by 303 · see citing works
Mitochondrial Approaches for Neuroprotection
Chaturvedi, R. K., & Beal, M. F. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1427.027 · Cited by 294 · see citing works
Self-citationMitochondria: A therapeutic target in neurodegeneration
Moreira, P. I., Zhu, X., Wang, X., Lee, H., Nunomura, A., Petersen, R. B., Perry, G. L., & Smith, M. A. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2009.10.007 · Cited by 286 · see citing works
Reactive Oxygen Species: Stuck in the Middle of Neurodegeneration
Patten, D. A., Germain, M., Kelly, M., & Slack, R. S. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-100498 · Cited by 280 · see citing works
Metformin: Is it a drug for all reasons and diseases?
Triggle, C. R., Mohammed, I., Bshesh, K., Marei, I., Ye, K., Ding, H., MacDonald, R. S., Hollenberg, M. D., & Hill, M. A. (2022) · Metabolism · doi:10.1016/j.metabol.2022.155223 · Cited by 282 · see citing works
Mitochondria-Targeted Cytoprotective Peptides for Ischemia–Reperfusion Injury
Szeto, H. H. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1892 · Cited by 269 · see citing works
Self-citationEffects of natural antioxidants in neurodegenerative disease
Albarracín, S. L., Stab, B., Casas, Z., Sutachan, J. J., Samudio, I. J., González, J., Gonzalo, L., Capani, F., Morales, L., & Barreto, G. E. (2012) · Nutritional Neuroscience · doi:10.1179/1476830511y.0000000028 · Cited by 273 · see citing works
Mitochondrial dysfunction in ALS
Cozzolino, M., & Carrı̀, M. T. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.06.003 · Cited by 239 · see citing works
Mitochondrial Medicine for Aging and Neurodegenerative Diseases
Reddy, P. H. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8044-z · Cited by 230 · see citing works
Cunha‐Oliveira, T., Montezinho, L., Mendes, C., Firuzi, O., Saso, L., Oliveira, P. J., & Silva, F. S. G. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/5021694 · Cited by 214 · see citing works
Zhao, W., Xu, Z., Cao, J., Fu, Q., Wu, Y., Zhang, X., Yue, L., Zhang, X., Yang, Y., Li, Y., et al. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1627-9 · Cited by 207 · see citing works
Serendipity and the Discovery of Novel Compounds That Restore Mitochondrial Plasticity
Szeto, H. H., & Birk, A. (2014) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2014.174 · Cited by 191 · see citing works
Self-citationMitochondrial Dysfunction in Aging and Alzheimer's Disease: Strategies to Protect Neurons
Reddy, P. H. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1754 · Cited by 187 · see citing works
Mitochondria as a target in treatment
Frantz, M., & Wipf, P. (2010) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20554 · Cited by 177 · see citing works
Cho, S., Szeto, H. H., Kim, E., Kim, H., Tolhurst, A. T., & Pinto, J. T. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m609388200 · Cited by 170 · see citing works
Self-citationNovel Therapies Targeting Inner Mitochondrial Membrane—From Discovery to Clinical Development
Szeto, H. H., & Schiller, P. W. (2011) · Pharmaceutical Research · doi:10.1007/s11095-011-0476-8 · Cited by 170 · see citing works
Self-citationYang, L., Zhao, K., Calingasan, N. Y., Luo, G., Szeto, H. H., & Beal, M. F. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2445 · Cited by 169 · see citing works
Self-citationMorton, H., Kshirsagar, S., Orlov, E., Bunquin, L. E., Sawant, N. A., Boleng, L., George, M., Basu, T., Ramasubramanian, B., Pradeepkiran, J. A., et al. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.07.013 · Cited by 171 · see citing works
Glutathione Binding to the Bcl-2 Homology-3 Domain Groove
Zimmermann, A. K., Loucks, F. A., Schroeder, E. K., Bouchard, R. J., Tyler, K. L., & Linseman, D. A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702853200 · Cited by 163 · see citing works
Amyotrophic Lateral Sclerosis: From Current Developments in the Laboratory to Clinical Implications
Cozzolino, M., Ferri, A., & Teresa Carrì, M. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2007.1760 · Cited by 156 · see citing works
Alzheimer's Disease: A Lesson from Mitochondrial Dysfunction
Moreira, P. I., Santos, M. S., & Oliveira, C. R. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1703 · Cited by 150 · see citing works
Reddy, P. H. (2011) · Pharmaceuticals · doi:10.3390/ph4030429 · Cited by 143 · see citing works
Yin, X., Mańczak, M., & Reddy, P. H. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw045 · Cited by 142 · see citing works
Reddy, P. H., Mańczak, M., & Kandimalla, R. J. L. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx052 · Cited by 134 · see citing works
Gruber, J., Fong, S., Chen, C.-B., Yoong, S. L., Pastorin, G., Schaffer, S., Cheah, I. K.-M., & Halliwell, B. B. (2012) · Biotechnology Advances · doi:10.1016/j.biotechadv.2012.09.005 · Cited by 138 · see citing works
Mitochondrial ROS regulate oxidative damage and mitophagy but not age-related muscle fiber atrophy
Sakellariou, G. K., Pearson, T., Lightfoot, A. P., Nye, G. A., Wells, N., Giakoumaki, I. I., Vasilaki, A., Griffiths, R. D., Jackson, M. J., & McArdle, A. (2016) · Scientific Reports · doi:10.1038/srep33944 · Cited by 133 · see citing works
Dare, A. J., Phillips, A. R. J., Hickey, A. J., Mittal, A., Loveday, B. P. T., Thompson, N. M., & Windsor, J. A. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.08.019 · Cited by 138 · see citing works
Brand, M. D. (2020) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2020.1828258 · Cited by 123 · see citing works
Mitochondria: a new therapeutic target in chronic kidney disease
Granata, S., Gassa, A. D., Tomei, P., Lupo, A., & Zaza, G. (2015) · Nutrition & Metabolism · doi:10.1186/s12986-015-0044-z · Cited by 122 · see citing works
Mechanisms of Disease: DNA repair defects and neurological disease
Subba Rao, K. (2007) · Nature Clinical Practice Neurology · doi:10.1038/ncpneuro0448 · Cited by 121 · see citing works
Pfohl, S. R., Halicek, M. T., & Mitchell, C. S. (2015) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-140068 · Cited by 114 · see citing works
Martinelli, C., Pucci, C., Battaglini, M., Marino, A., & Ciofani, G. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201901589 · Cited by 111 · see citing works
Hemigramicidin–TEMPO conjugates: Novel mitochondria-targeted anti-oxidants
Fink, M. P., Macias, C. A., Xiao, J., Tyurina, Y. Y., Jiang, J., Belikova, N. A., Delude, R. L., Greenberger, J. S., Kagan, V. E., & Wipf, P. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.05.019 · Cited by 107 · see citing works
The Centrality of Mitochondria in the Pathogenesis and Treatment of Parkinson's Disease
Camilleri, A., & Vassallo, N. (2014) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12264 · Cited by 104 · see citing works
Wu, J., Zhang, M., Hao, S., Jia, M., Ji, M., Qiu, L., Sun, X., Yang, J., & Li, K. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8918-z · Cited by 104 · see citing works
Mitochondrial protein tyrosine nitration
Castro, L., Demicheli, V., Tórtora, V., & Radí, R. (2010) · Free Radical Research · doi:10.3109/10715762.2010.516254 · Cited by 100 · see citing works
Development of Mitochondria‐targeted Aromatic‐cationic Peptides for Neurodegenerative Diseases
Szeto, H. H. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1427.013 · Cited by 100 · see citing works
Self-citationHeart Failure and Mitochondrial Dysfunction
Knowlton, A. A., Chen, L., & Malik, Z. A. (2013) · Journal of Cardiovascular Pharmacology · doi:10.1097/01.fjc.0000432861.55968.a6 · Cited by 97 · see citing works
Reddy, P. H., Mańczak, M., Yin, X., & Reddy, A. P. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-170988 · Cited by 96 · see citing works
Calvo-Rodríguez, M., Kharitonova, E. K., Snyder, A. C., Hou, S. S., Sanchez-Mico, M. V., Das, S., Fan, Z., Shirani, H., Nilsson, K. P. R., Serrano‐Pozo, A., et al. (2024) · Molecular Neurodegeneration · doi:10.1186/s13024-024-00702-2 · Cited by 97 · see citing works
Thomas, D. A., Stauffer, C., Zhao, K., Yang, H., Sharma, V. K., Szeto, H. H., & Suthanthiran, M. (2007) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006080825 · Cited by 84 · see citing works
Self-citationMitochondrial medicine for neurodegenerative diseases
Du, H., & Yan, S. S. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2010.01.004 · Cited by 81 · see citing works
SS‐31 Provides Neuroprotection by Reversing Mitochondrial Dysfunction after Traumatic Brain Injury
Zhu, Y., Wang, H., Fang, J., Dai, W., Zhou, J., Wang, X., & Zhou, M. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/4783602 · Cited by 79 · see citing works
Mitochondrial dysfunction in central nervous system white matter disorders
Morató, L., Bertini, E., Verrigni, D., Ardissone, A., Ruíz, M., Ferrer, I., Uziel, G., & Pujol, A. (2014) · Glia · doi:10.1002/glia.22670 · Cited by 75 · see citing works
Calkins, M. J., Mańczak, M., & Reddy, P. (2012) · Pharmaceuticals · doi:10.3390/ph5101103 · Cited by 71 · see citing works
Mizuguchi, Y., Chen, J., Seshan, S. V., Poppas, D. P., Szeto, H. H., & Felsen, D. (2008) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00395.2007 · Cited by 72 · see citing works
Self-citationMitochondrially-targeted treatment strategies
Bozi, L. H. M., Campos, J. C., Zambelli, V. O., Ferreira, N. D., & Ferreira, J. C. B. (2019) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2019.100836 · Cited by 65 · see citing works
Bhatti, G. K., Gupta, A., Pahwa, P., Khullar, N., Singh, S., Navik, U., Kumar, S., Mastana, S. S., Reddy, A. P., Reddy, P. H., et al. (2022) · Biomedical Journal · doi:10.1016/j.bj.2022.05.002 · Cited by 65 · see citing works
Mitochondrial therapies for Parkinson's disease
Thomas, B., & Beal, M. F. (2010) · Movement Disorders · doi:10.1002/mds.22781 · Cited by 61 · see citing works
Self-citationCalkins, M. J., & Reddy, P. H. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.04.006 · Cited by 62 · see citing works
Catalytic Antioxidants and Neurodegeneration
Golden, T. R., & Patel, M. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2256 · Cited by 61 · see citing works
Wu, J., Zhang, M., Li, H., Sun, X., Hao, S., Ji, M., Yang, J., & Li, K. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.02.036 · Cited by 58 · see citing works
Toyama, S., Shimoyama, N., Ishida, Y., Koyasu, T., Szeto, H. H., & Shimoyama, M. (2013) · Anesthesiology · doi:10.1097/01.anes.0000435634.34709.65 · Cited by 57 · see citing works
Self-citationBond, L., Bernhardt, K. D., Madria, P., Sorrentino, K., Scelsi, H. F., & Mitchell, C. S. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00010 · Cited by 57 · see citing works
A Mitochondrion-Targeted Antioxidant Ameliorates Isoflurane-Induced Cognitive Deficits in Aging Mice
Wu, J., Li, H., Sun, X., Zhang, H., Hao, S., Ji, M., Yang, J., & Li, K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138256 · Cited by 54 · see citing works
Oxidative Stress Treatment for Clinical Trials in Neurodegenerative Diseases
Ienco, E. C., LoGerfo, A., Carlesi, C., Orsucci, D., Ricci, G., Mancuso, M., & Siciliano, G. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-110164 · Cited by 54 · see citing works
Mitochondrial oxidative stress and mammalian healthspan
Wanagat, J., Dai, D., & Rabinovitch, P. S. (2010) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2010.06.002 · Cited by 52 · see citing works
Joshi, A. U., Kornfeld, O. S., & Mochly‐Rosen, D. (2016) · Cell Calcium · doi:10.1016/j.ceca.2016.04.010 · Cited by 51 · see citing works
Cai, J., Jiang, Y. Y., Zhang, M., Zhao, H., Li, H., Li, K., Zhang, X., & Tong, Q. Z. (2018) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-018-0617-1 · Cited by 48 · see citing works
Edens, B. M., Miller, N., & Ma, Y. C. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00044 · Cited by 51 · see citing works
Serviddio, G., Romano, A. D., Cassano, T., Bellanti, F., Altomare, E., & Vendemiale, G. (2011) · Current Pharmaceutical Design · doi:10.2174/138161211796904740 · Cited by 45 · see citing works
Whiteman, M., Spencer, J. P. E., Szeto, H. H., & Armstrong, J. S. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1879 · Cited by 44 · see citing works
Self-citationMitochondria as a Therapeutic Target in Alzheimers Disease and Diabetes
Moreira, P. I., Cardoso, S. M., Pereira, C., Santos, M. S., & Oliveira, C. R. (2009) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152709789824651 · Cited by 44 · see citing works
MacDougall, G., Anderton, R. S., Mastaglia, F. L., Knuckey, N. W., & Meloni, B. P. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.09.010 · Cited by 41 · see citing works
Bhatti, J. S., Thamarai, K., Kandimalla, R., Manczak, M., Yin, X., Kumar, S., Vijayan, M., & Reddy, P. H. (2021) · Molecular Neurobiology · doi:10.1007/s12035-020-02142-7 · Cited by 41 · see citing works
Prospects for neuroprotective therapies in prodromal Huntington's disease
Chandra, A., Johri, A., & Beal, M. F. (2014) · Movement Disorders · doi:10.1002/mds.25835 · Cited by 41 · see citing works
Self-citationLee, H.-Y., Kaneki, M., Andreas, J., Tompkins, R. G., & Martyn, J. A. J. (2011) · Shock · doi:10.1097/shk.0b013e3182366872 · Cited by 41 · see citing works
Whether short peptides are good candidates for future neuroprotective therapeutics?
Perlikowska, R. (2021) · Peptides · doi:10.1016/j.peptides.2021.170528 · Cited by 42 · see citing works
Mitochondria-Directed Therapeutics
Armstrong, J. S. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1929 · Cited by 40 · see citing works
Skawratananond, S., Xiong, D. X., Zhang, C., Tonk, S. S., Pinili, A., Delacruz, B., Pham, P., Smith, S. C., Navab, R., & Reddy, P. H. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102732 · Cited by 39 · see citing works
Yang, D., Zuo, Q., Wang, T., Xu, D., Liu, L., Gao, L., Wan, C., Chen, L., Wen, F., & Shen, Y. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/6644238 · Cited by 36 · see citing works
Yo, K., Yu, Y., Zhao, G., Bonab, A. A., Aikawa, N., Tompkins, R. G., & Fischman, A. J. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00098.2012 · Cited by 35 · see citing works
New Therapeutics to Modulate Mitochondrial Function in Neurodegenerative Disorders
Wilkins, H., & Morris, J. K. (2017) · Current Pharmaceutical Design · doi:10.2174/1381612822666161230144517 · Cited by 34 · see citing works
Mangrulkar, S. V., Wankhede, N. L., Kale, M. B., Upaganlawar, A. B., Taksande, B. G., Umekar, M. J., Anwer, M. K., Dailah, H. G., Mohan, S., & Behl, T. (2023) · Neurotoxicity Research · doi:10.1007/s12640-023-00647-2 · Cited by 35 · see citing works
Metal attenuating therapies in neurodegenerative disease
Mot, A. I., Wedd, A. G., Sinclair, L., Brown, D. R., Collins, S. J., & Brazier, M. W. (2011) · Expert Review of Neurotherapeutics · doi:10.1586/ern.11.170 · Cited by 31 · see citing works
Strategic approaches to developing drug treatments for ALS
Vincent, A. M., Sakowski, S. A., Schuyler, A. D., & Feldman, E. L. (2007) · Drug Discovery Today · doi:10.1016/j.drudis.2007.10.011 · Cited by 32 · see citing works
Lin, F., Li, R., Tu, W., Chen, Y., Wang, K., Chen, X., & Zhao, J. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.772036 · Cited by 31 · see citing works
Visioli, F., Ingram, A., Beckman, J. S., Magnusson, K. R., & Hagen, T. M. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.12.008 · Cited by 31 · see citing works
Relationships between Exercise, Mitochondrial Biogenesis and Type 2 Diabetes
Joseph, A.-M., & Hood, D. A. (2014) · Medicine and sport science/Medicine and sport · doi:10.1159/000357335 · Cited by 32 · see citing works
Bhatti, J. S., Tamarai, K., Kandimalla, R., Manczak, M., Yin, X., Ramasubramanian, B., Sawant, N., Pradeepkiran, J. A., Vijayan, M., Kumar, S., et al. (2021) · Mitochondrion · doi:10.1016/j.mito.2021.02.007 · Cited by 30 · see citing works
A synthetic cell permeable antioxidant protects neurons against acute oxidative stress
Drummond, N. J., Davies, N. O., Lovett, J. E., Miller, M. R., Cook, G., Becker, T., Becker, C. G., McPhail, D. B., & Kunath, T. (2017) · Scientific Reports · doi:10.1038/s41598-017-12072-5 · Cited by 30 · see citing works
Shen, R., Zhou, J., Li, G., Chen, W., Zhong, W., & Chen, Z. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134654 · Cited by 29 · see citing works
Mitochondria as Potential Targets in Antidiabetic Therapy
Moreira, P. I., & Oliveira, C. R. (2011) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-17214-4_14 · Cited by 27 · see citing works
- Authors
- Petri, S., Kiaei, M., Damiano, M., Hiller, A., Wille, E., Manfredi, G., Calingasan, N. Y., Szeto, H. H., & Beal, M. F.
- Affiliations
- Cornell University (US)
- Venue
- Journal of Neurochemistry
- Publisher
- Wiley
- Published
- 2006-07-10
- Volume
- 98
- Issue
- 4
- Pages
- 1141-1148
- ISSN
- 0022-3042 (ISSN-L)
- 1471-4159
- OpenAlex
- W2036154524
- Cited by
- 166
- References
- 46
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 12 · 2023: 4 · 2022: 11 · 2021: 12 · 2020: 3 · 2019: 9 · 2018: 10 · 2017: 4 · 2016: 10 · 2015: 10 · 2014: 12 · 2013: 6 · 2012: 10
- FWCI
- 6.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurochemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- ALS Association
- Muscular Dystrophy Association
- Deutsche Forschungsgemeinschaft
- U.S. Public Health Service (NINDS 48295, NIDA08924)
- National Institute of Neurological Disorders and Stroke
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- amyotrophic lateral sclerosis, SS-31, reactive oxygen species, oxidative stress, Cu/Zn superoxide dismutase, inner mitochondrial membrane, hydrogen peroxide-induced cell death, neuroprotection, motor performance, lumbar spinal cord
- MeSH terms
- Superoxide Dismutase-1, Aging, Amyotrophic Lateral Sclerosis, Animals, Antioxidants, Body Weight, Cell Count, Cell Membrane Permeability, Cells, Cultured, Disease Models, Animal, Mice, Transgenic, Peptides, Psychomotor Performance, Spinal Cord, Superoxide Dismutase, Reactive Oxygen Species, Mice
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