Cell-permeable Peptide Antioxidants Targeted to Inner Mitochondrial Membrane inhibit Mitochondrial Swelling, Oxidative Cell Death, and Reperfusion Injury
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Reactive oxygen species (ROS) play a key role in promoting mitochondrial cytochrome c release and induction of apoptosis. ROS induce dissociation of cytochrome c from cardiolipin on the inner mitochondrial membrane (IMM), and cytochrome c may then be released via mitochondrial permeability transition (MPT)-dependent or MPT-independent mechanisms. We have developed peptide antioxidants that target the IMM, and we used them to investigate the role of ROS and MPT in cell death caused by t-butylhydroperoxide (tBHP) and 3-nitropropionic acid (3NP). The structural motif of these peptides centers on alternating aromatic and basic amino acid residues, with dimethyltyrosine providing scavenging properties. These peptide antioxidants are cell-permeable and concentrate 1000-fold in the IMM. They potently reduced intracellular ROS and cell death caused by tBHP in neuronal N(2)A cells (EC(50) in nm range). They also decreased mitochondrial ROS production, inhibited MPT and swelling, and prevented cytochrome c release induced by Ca(2+) in isolated mitochondria. In addition, they inhibited 3NP-induced MPT in isolated mitochondria and prevented mitochondrial depolarization in cells treated with 3NP. ROS and MPT have been implicated in myocardial stunning associated with reperfusion in ischemic hearts, and these peptide antioxidants potently improved contractile force in an ex vivo heart model. It is noteworthy that peptide analogs without dimethyltyrosine did not inhibit mitochondrial ROS generation or swelling and failed to prevent myocardial stunning. These results clearly demonstrate that overproduction of ROS underlies the cellular toxicity of tBHP and 3NP, and ROS mediate cytochrome c release via MPT. These IMM-targeted antioxidants may be very beneficial in the treatment of aging and diseases associated with oxidative stress.
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SS-31 prevents Ca2+ induced cytochrome c release and inhibits 3-NP-induced activation of the MPT pore and mitochondrial depolarization in isolated mitochondria.
“SS-31 also prevents Ca2+ induced cytochrome c release and inhibits 3-NP-induced activation of the MPT pore and mitochondrial depolarization in isolated mitochondria178.”
From Mitochondrial Approaches for Neuroprotection (2008) · cites this paper as [178]
Peptides containing tyrosine residues have been found effectively to scavenge oxygen radicals and peroxynitrite and to inhibit lipid peroxidation.
“Peptides containing tyrosine residues have been found effectively to scavenge oxygen radicals and peroxynitrite and to inhibit lipid peroxidation (304, 349).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [349]
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Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., & Wang, X. (1997) · Cell · doi:10.1016/s0092-8674(00)80434-1 · Cited by 7,289 · see citing works
Induction of Apoptotic Program in Cell-Free Extracts: Requirement for dATP and Cytochrome c
Liu, X., Kim, C. N., Yang, J., Jemmerson, R., & Wang, X. (1996) · Cell · doi:10.1016/s0092-8674(00)80085-9 · Cited by 5,167 · see citing works
Bax directly induces release of cytochrome c from isolated mitochondria
Jürgensmeier, J. M., Xie, Z., Deveraux, Q. L., Ellerby, L., Bredesen, D. E., & Reed, J. C. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.4997 · Cited by 1,523 · see citing works
Selective Targeting of a Redox-active Ubiquinone to Mitochondria within Cells
Kelso, G. F., Porteous, C. M., Coulter, C. V., Hughes, G., Porteous, W. K., Ledgerwood, E. C., Smith, R. A. J., & Murphy, M. P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009093200 · Cited by 1,091 · see citing works
Beal, M. F., Brouillet, E., Jenkins, B. G., Ferrante, R. J., Kowall, N. W., Miller, J., Storey, E., Srivastava, R., Rosen, B. R., & Hyman, B. T. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-10-04181.1993 · Cited by 1,026 · see citing works
Cytochrome c release from mitochondria proceeds by a two-step process
Ott, M., Robertson, J. D., Gogvadze, V. G., Zhivotovsky, B., & Orrenius, S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.241655498 · Cited by 955 · see citing works
Breaking the mitochondrial barrier
Martinou, J., & Green, D. R. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35048069 · Cited by 951 · see citing works
Mitochondrial 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
Mitochondrial permeability transition and oxidative stress
Kowaltowski, A. J., Castilho, R. F., & Vercesi, A. E. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02316-x · Cited by 832 · see citing works
Halestrap, A. P., & Davidson, A. M. (1990) · Biochemical Journal · doi:10.1042/bj2680153 · Cited by 753 · see citing works
Matthews, 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
Madesh, M., & Hajnóczky, G. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200105057 · Cited by 538 · see citing works
Selective targeting of an antioxidant to mitochondria
Smith, R. A. J., Porteous, C. M., Coulter, C. V., & Murphy, M. P. (1999) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1999.00543.x · Cited by 466 · see citing works
Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria
Petrosillo, G., Ruggiero, F. M., & Paradies, G. (2003) · The FASEB Journal · doi:10.1096/fj.03-0012com · Cited by 384 · see citing works
Jauslin, M. L., Meier, T., Smith, R. A. J., & Murphy, P. M. (2003) · The FASEB Journal · doi:10.1096/fj.03-0240fje · Cited by 358 · see citing works
Nieminen, A. L., Byrne, A. M., Herman, B. A., & Lemasters, J. J. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.272.4.c1286 · Cited by 336 · 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
Testosterone reduces neuronal secretion of Alzheimer's β-amyloid peptides
Gouras, G. K., Xu, H., Gross, R. S., Greenfield, J. P., Hai, B., Wang, R., & Greengard, P. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.1202 · Cited by 300 · see citing works
[30] The isolation of outer and inner mitochondrial membranes
Greenawalt, J. W. (1974) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(74)31033-6 · Cited by 297 · see citing works
Costantini, P., Belzacq, A.-S., Vieira, H. L., Larochette, N., de Pablo, M. A., Zamzami, N., Susin, S. A., Brenner, C., & Kroemer, G. (2000) · Oncogene · doi:10.1038/sj.onc.1203299 · Cited by 284 · see citing works
Batandier, C., Leverve, X., & Fontaine, E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310329200 · Cited by 264 · see citing works
Flaherty, J. T., Pitt, B., Gruber, J. W., Heuser, R. R., ROTHBAUM, D. A., Burwell, L. R., George, B. S., Kereiakes, D. J., Deitchman, D., & Gustafson, N. (1994) · Circulation · doi:10.1161/01.cir.89.5.1982 · Cited by 255 · see citing works
Loss of Molecular Interaction between Cytochrome c and Cardiolipin Due to Lipid Peroxidation
Shidoji, Y., Hayashi, K., KOMURA, S., Ohishi, N., & Yagi, K. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1410 · Cited by 250 · see citing works
The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal
Vieira, H. L., Belzacq, A.-S., Haouzi, D., Bernassola, F., Cohen, I., Jacotot, E., Ferri, K. F., El Hamel, C., Bartle, L. M., Melino, G., et al. (2001) · Oncogene · doi:10.1038/sj.onc.1204575 · Cited by 244 · see citing works
Cytochrome c binding to enzymes and membranes
Nicholls, P. J. (1974) · Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics · doi:10.1016/0304-4173(74)90003-2 · Cited by 242 · see citing works
Paradies, G., Petrosillo, G., Pistolese, M., Venosa, N. D., Serena, D., & Ruggiero, F. M. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00032-5 · Cited by 240 · see citing works
Petrosillo, G., Ruggiero, F. M., Pistolese, M., & Paradies, G. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)03206-9 · Cited by 223 · see citing works
Lim, K. H. H., Javadov, S. A., Das, M., Clarke, S. J., Suleiman, M. S., & Halestrap, A. P. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.031484 · Cited by 219 · see citing works
Petronilli, V., Nicolli, A., Costantini, P., Colonna, R., & Bernardi, P. (1994) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(94)90122-8 · Cited by 210 · see citing works
Oxidative stress-elicited myocardial apoptosis during reperfusion
Zhao, Z. (2004) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2003.10.010 · Cited by 188 · see citing works
Limitations of Cyclosporin A Inhibition of the Permeability Transition in CNS Mitochondria
Brustovetsky, N., & Dubinsky, J. M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-22-08229.2000 · Cited by 169 · see citing works
Beal, M. F., Ferrante, R. J., Henshaw, R., Matthews, R. T., Chan, P. H., Kowall, N. W., Epstein, C. J., & Schulz, J. B. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.65020919.x · Cited by 162 · 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
Self-citationTranscellular 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-citationLi, Y. R., Zhu, H., & Trush, M. A. (1999) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(99)00040-9 · Cited by 146 · see citing works
Doran, E., & Halestrap, A. P. (2000) · Biochemical Journal · doi:10.1042/bj3480343 · Cited by 139 · see citing works
BH3 Death Domain Peptide Induces Cell Type-selective Mitochondrial Outer Membrane Permeability
Polster, B. M., Kinnally, K. W., & Fiskum, G. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104552200 · Cited by 130 · see citing works
Oxidative Stress Underlies the Mechanism for Ca2+-induced Permeability Transition of Mitochondria
Kanno, T., Sato, E. F., Muranaka, S., Fujita, H., Fujiwara, T., Utsumi, T., Inoue, M., & Utsumi, K. (2003) · Free Radical Research · doi:10.1080/10715760310001626266 · Cited by 127 · see citing works
Hines, E. P., Ekshyyan, O. Y., Rhoads, C. A., Fuseler, J. W., Harrison, L., & Aw, T. Y. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208670200 · Cited by 125 · see citing works
Fontana, M., Mosca, L., & Rosei, M. A. (2001) · Biochemical Pharmacology · doi:10.1016/s0006-2952(01)00565-2 · Cited by 123 · see citing works
Byrne, A. M., Lemasters, J. J., & Nieminen, A. (1999) · Hepatology · doi:10.1002/hep.510290521 · Cited by 120 · see citing works
Rosenstock, T. R., Carvalho, A. C. P., Jurkiewicz, A., Frussa‐Filho, R., & Smaili, S. S. (2004) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02250.x · Cited by 117 · see citing works
Secretory Peptide Hormones Are Biochemical Antioxidants: Structure-Activity Relationship
Moosmann, B., & Behl, C. (2002) · Molecular Pharmacology · doi:10.1124/mol.61.2.260 · Cited by 104 · see citing works
Pong, K., Doctrow, S. R., Huffman, K. D., Adinolfi, C. A., & Baudry, M. (2001) · Experimental Neurology · doi:10.1006/exnr.2001.7747 · Cited by 91 · see citing works
On the involvement of a mitochondrial pore in reperfusion injury
Crompton, M., & Andreeva, L. V. (1993) · Basic Research in Cardiology · doi:10.1007/bf00795416 · Cited by 86 · see citing works
The Fate of the Oxidizing Tyrosyl Radical in the Presence of Glutathione and Ascorbate
Sturgeon, B. E., Sipe, H. J., Barr, D. P., Corbett, J. T., Martinez, J. G., & Mason, R. P. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.46.30116 · Cited by 86 · see citing works
Galindo, 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
Pichorner, H., Metodiewa, D., & Winterbourn, C. C. (1995) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1995.0064 · Cited by 70 · see citing works
Zhao, G., Qian, X., Schiller, P. W., & Szeto, H. H. (2003) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.054775 · Cited by 65 · see citing works
Self-citationProtein kinase activity at the inner membrane of mammalian mitochondria.
Verdanis, A. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)75168-0 · Cited by 51 · see citing works
Lee, W., Yin, H., & Shen, Y.-C. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00097-0 · Cited by 48 · see citing works
Machida, K., Hayashi, Y., & Osada, H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204564200 · Cited by 44 · see citing works
Inhibition of Lipid Peroxidation by N-Acetylserotonin and Its Role in Retinal Physiology
Longoni, B., Pryor, W. A., & Marchiafava, P. L. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6563 · Cited by 44 · see citing works
Nakamura, M., Yamazaki, I., Ohtaki, S., et al. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)66960-1 · Cited by 40 · see citing works
Regulation of apoptosis by respiration: cytochrome c release by respiratory substrates
Nishimura, G., Proske, R. J., Doyama, H., et al. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02859-9 · Cited by 40 · see citing works
Highly potent fluorescent analogues of the opioid peptide [Dmt1]DALDA
Berezowska, I., Chung, N. N., Lemieux, C., et al. (2003) · Peptides · doi:10.1016/j.peptides.2003.07.004 · Cited by 28 · see citing works
Oxidative ring-coupling of tyrosine and its derivatives by purified rat intestinal peroxidase
Valoti, M., Tipton, K. F., & Sgaragli, G. P. (1992) · Biochemical Pharmacology · doi:10.1016/0006-2952(92)90597-c · Cited by 14 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- Matthews, R. T., Yang, L., Browne, S., Baik, M., and Beal, M. F. (1998) Proc. Natl. Acad. Sci. U. S. A. 95, 8892-8897
- Ott, M., Robertson, J. D., Gogvadze, V., Zhivotovsky, B., and Orrenius, S. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 1259 -1263
- Jurgensmeier, J. M., Xie, Z., Deveraux, Q., Ellerby, L., Bredesen, D., and Reed, J. C. (1998) Proc. Natl. Acad. Sci. U. S. A. 95, 4997-5002
- Gouras, G. K., Xu, H., Gross, R. S., Greenfield, J. P., Hai, B., Wang, R., and Greengard, P. (2000) Proc. Natl. Acad. Sci. U. S. A. 97, 1202-1205
Cited by
Sorted by citations
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-citationSivitz, W. I., & Yorek, M. A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2531 · Cited by 742 · see citing works
Exercise-induced oxidative stress in humans: cause and consequences
Powers, S. K., Nelson, W. B., & Hudson, M. B. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.12.009 · Cited by 441 · see citing works
Mitochondria-Targeted Small Molecule Therapeutics and Probes
Smith, R. A. J., Hartley, R. C., & Murphy, M. P. (2011) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.3969 · Cited by 399 · see citing works
Münzel, T., Gori, T., Keaney, J. F., Maack, C., & Daiber, A. (2015) · European Heart Journal · doi:10.1093/eurheartj/ehv305 · 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-citationCell-permeable, mitochondrial-targeted, peptide antioxidants
Szeto, H. H. (2006) · The AAPS Journal · doi:10.1007/bf02854898 · Cited by 316 · see citing works
Self-citationLinking mitochondrial bioenergetics to insulin resistance via redox biology
Fisher-Wellman, K. H., & Neufer, P. D. (2012) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2011.12.008 · Cited by 316 · see citing works
Targeting Oxidative Stress in Central Nervous System Disorders
Patel, M. (2016) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2016.06.007 · Cited by 312 · 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
Min, K., Smuder, A. J., Kwon, O.-S., Kavazis, A. N., Szeto, H. H., & Powers, S. K. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00591.2011 · Cited by 265 · see citing works
Self-citationPowers, S. K., Hudson, M. B., Nelson, W. B., Talbert, E. E., Min, K., Szeto, H. H., Kavazis, A. N., & Smuder, A. J. (2011) · Critical Care Medicine · doi:10.1097/ccm.0b013e3182190b62 · Cited by 255 · 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-citationMitochondrial 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
Petri, S., Kiaei, M., Damiano, M., Hiller, A., Wille, E., Manfredi, G., Calingasan, N. Y., Szeto, H. H., & Beal, M. F. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04018.x · Cited by 166 · see citing works
Self-citationGibson, C. M., Giugliano, R. P., Kloner, R. A., Bode, C., Tendera, M., Jánosi, A., Merkely, B., Godlewski, J., Halaby, R., Korjian, S., et al. (2016) · European Heart Journal · doi:10.1093/eurheartj/ehv597 · Cited by 162 · see citing works
Potent mitochondria-targeted peptides reduce myocardial infarction in rats
Cho, J., Won, K., Wu, D., Soong, Y., Liu, S., Szeto, H. H., & Hong, M. K. (2007) · Coronary Artery Disease · doi:10.1097/01.mca.0000236285.71683.b6 · Cited by 144 · see citing works
Self-citationSong, B.-J., Akbar, M., Abdelmegeed, M. A., Byun, K., Lee, B., Yoon, S. K., & Hardwick, J. P. (2014) · Redox Biology · doi:10.1016/j.redox.2014.10.004 · Cited by 123 · see citing works
Wang, D., Malo, D., & Hekimi, S. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902352 · Cited by 123 · see citing works
Young, M. L., & Franklin, J. L. (2019) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2019.103409 · Cited by 120 · see citing works
Skeletal muscle NOX4 is required for adaptive responses that prevent insulin resistance
Xirouchaki, C. E., Jia, Y., McGrath, M. J., Greatorex, S., Tran, M., Merry, T. L., Hong, D., Eramo, M. J., Broome, S. C., Woodhead, J. S. T., et al. (2021) · Science Advances · doi:10.1126/sciadv.abl4988 · Cited by 107 · see citing works
Berthiaume, J. M., Oliveira, P. J., Fariss, M. W., & Wallace, K. B. (2005) · Cardiovascular Toxicology · doi:10.1385/ct:5:3:257 · Cited by 101 · 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-citationPhysical inactivity, insulin resistance, and the oxidative-inflammatory loop
Gratas-Delamarche, A., Derbré, F., Vincent, S., & Cillard, J. (2014) · Free Radical Research · doi:10.3109/10715762.2013.847528 · Cited by 99 · see citing works
Jin, L.-W., Horiuchi, M., Wulff, H., Liu, X.-B., Cortopassi, G. A., Erickson, J. D., & Maezawa, I. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2778-14.2015 · Cited by 88 · see citing works
“To test whether enhanced mtROS production as a result of SNAT1 overexpression leads to mitochondrial dysfunction in microglia, we used two mitochondria-targeted approaches using the following: (1) SS-31, a cell-permeable, mitochondriatargeted peptide antioxidant (Zhao et al., 2004) able to concentrate 1000- to 5000-fo…”
MethodThomas, 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 dynamics: orchestrating the journey to advanced age
Biala, A. K., Dhingra, R., & Kirshenbaum, L. A. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.04.015 · Cited by 82 · see citing works
Escribano-Lopez, I., Diaz-Morales, N., Iannantuoni, F., Lopez-Domenech, S., de Marañon, A. M., Abad-Jimenez, Z., Bañuls, C., Rovira-Llopis, S., Herance, J. R., Rocha, M., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-34251-8 · Cited by 71 · see citing works
Eating the dead to keep atherosclerosis at bay
Brophy, M. L., Dong, Y., Wu, H., Rahman, H. N. A., Song, K., & Chen, H. (2017) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2017.00002 · Cited by 68 · see citing works
Durand, E., Lecomte, J., Upasani, R., Chabi, B., Bayrasy, C., Baréa, B., Jublanc, E., Clarke, M. J., Moore, D. J., Crowther, J., et al. (2017) · Pharmaceutical Research · doi:10.1007/s11095-017-2124-4 · Cited by 50 · 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
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
Ma, J., Lim, C., Sacher, J. R., Van Houten, B., Qian, W., & Wipf, P. (2015) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2015.06.073 · Cited by 27 · see citing works
- Authors
- Zhao, K., Zhao, G.-M., Wu, D., Soong, Y., Birk, A. V., Schiller, P. W., & Szeto, H. H.
- Affiliations
- Cornell University (US)
- Montreal Clinical Research Institute (CA)
- Corresponding author
- Szeto, Hazel H.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2004-08
- Volume
- 279
- Issue
- 33
- Pages
- 34682-34690
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2055456981
- Cited by
- 782
- References
- 57
- Citations by year
- 2026: 18 · 2025: 25 · 2024: 38 · 2023: 46 · 2022: 45 · 2021: 50 · 2020: 43 · 2019: 39 · 2018: 50 · 2017: 32 · 2016: 47 · 2015: 49 · 2014: 41 · 2013: 43 · 2012: 43
- FWCI
- 7.34
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Memorial Sloan-Kettering Cancer Center
- National Institutes of Health
- National Institute on Drug Abuse (DA08924, K01DA018268, P01DA008924)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Keywords
- inner mitochondrial membrane, mitochondrial permeability transition, reactive oxygen species, mitochondrial swelling, oxidative cell death, cytochrome c release, ischemia-reperfusion injury, myocardial stunning, tert-butyl hydroperoxide, 3-nitropropionic acid, mitochondrial reactive oxygen species, apoptosis, oxidative stress
- MeSH terms
- Animals, Antioxidants, Calcium, Cardiolipins, Cell Survival, Humans, Hydrogen Peroxide, Intracellular Membranes, Liver, Male, Mitochondria, Mitochondria, Liver, Nitro Compounds, Oxygen, Oxygen Consumption, Peptides, Propionates, Time Factors, Tyrosine, Reperfusion, Reperfusion Injury, Cell Death, Reactive Oxygen Species, Oxidative Stress, Caco-2 Cells, tert-Butylhydroperoxide, Amino Acid Motifs, Cytochromes c, Mice
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