Mitochondrial Generation of Oxygen Radicals During Reoxygenation of Ischemic Tissues
Abstract
Ischemia and reperfusion causes severe mitochondrial damage, including swelling and deposits of hydroxyapatite crystals in the mitochondrial matrix. These crystals are indicative of a massive influx of Ca2+ into the mitochondrial matrix occurring during reoxygenation. We have observed that mitochondria isolated from rat hearts after 90 minutes of anoxia followed by reoxygenation, show a specific inhibition in the electron transport chain between NADH dehydrogenase and ubiquinone in addition to becoming uncoupled (unable to generate ATP). This inhibition is associated with an increased H2O2 formation at the NADH dehydrogenase level in the presence of NADH dependent substrates. Control rat mitochondria exposed for 15 minutes to high Ca2+ (200 nmol/mg protein) also become uncoupled and electron transport inhibited between NADH dehydrogenase and ubiquinone, a lesion similar to that observed in post-ischemic mitochondria. This Ca(2+)-dependent effect is time dependent and may be partially prevented by albumin, suggesting that it may be due to phospholipase A2 activation, releasing fatty acids, leading to both inhibition of electron transport and uncoupling. Addition of arachidonic or linoleic acids to control rat heart mitochondria, inhibits electron transport between Complex I and III. These results are consistent with the following hypothesis: during ischemia, the intracellular energy content drops severely, affecting the cytoplasic concentration of ions such as Na+ and Ca2+. Upon reoxygenation, the mitochondrion is the only organelle capable of eliminating the excess cytoplasmic Ca2+ through an electrogenic process requiring oxygen (the low ATP concentration makes other ATP-dependent Ca2+ transport systems non-operational).(ABSTRACT TRUNCATED AT 250 WORDS)
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
ROS trigger or mediate ischemic and pharmacologic preconditioning of hearts.
“It is now well known that ROS trigger or mediate ischemic and pharmacologic preconditioning of hearts (15, 27, 102, 181, 183, 248, 254, 303).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [303]
Mixed-function oxidases can facilitate metal-catalyzed oxidation by O2•− of proteins with 4Fe-4S tetranuclear cores to mark them for ubiquitination and so alter their stability.
“Mixed-function oxidases can facilitate metal-catalyzed oxidation by O2•− of proteins with 4Fe-4S tetranuclear cores to mark them for ubiquitination and so alter their stability (303).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [303]
Cites
Hydroperoxide metabolism in mammalian organs.
Chance, B., Sies, H., & Boveris, A. (1979) · Physiological Reviews · doi:10.1152/physrev.1979.59.3.527 · Cited by 5,827 · see citing works
The American Journal of Physiology
(1899) · The American Naturalist · doi:10.1086/277182 · Cited by 5,680 · see citing works
Oxygen-Derived Free Radicals in Postischemic Tissue Injury
Epstein, F. H., & McCord, J. M. (1985) · New England Journal of Medicine · doi:10.1056/nejm198501173120305 · Cited by 5,399 · see citing works
Self-citationNormal oxidative damage to mitochondrial and nuclear DNA is extensive.
Richter, C., Park, J. W., & Ames, B. N. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.17.6465 · Cited by 1,730 · see citing works
Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria
Turrens, J. F., & Boveris, A. (1980) · Biochemical Journal · doi:10.1042/bj1910421 · Cited by 1,601 · see citing works
Self-citationThe cellular production of hydrogen peroxide
Boveris, A., Oshino, N., & Chance, B. (1972) · Biochemical Journal · doi:10.1042/bj1280617 · Cited by 1,549 · see citing works
Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria
Turrens, J. F., Alexandre, A., & Lehninger, A. L. (1985) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(85)90293-0 · Cited by 1,214 · see citing works
Self-citationInduction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism
Wong, G. H. W., & Goeddel, D. V. (1988) · Science · doi:10.1126/science.3263703 · Cited by 914 · see citing works
Role of ubiquinone in the mitochondrial generation of hydrogen peroxide
Boveris, A., Cadenas, E., & Stoppani, A. O. M. (1976) · Biochemical Journal · doi:10.1042/bj1560435 · Cited by 655 · see citing works
Progress in Clinical and Biological Research
Crombie, A. L. (1989) · British Journal of Ophthalmology · doi:10.1136/bjo.73.1.79 · Cited by 553 · see citing works
The effect of hyperoxia on superoxide production by lung submitochondrial particles
Turrens, J. F., Freeman, B. Α., Levitt, J. G., & Crapo, J. D. (1982) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(82)90518-5 · Cited by 448 · see citing works
Self-citationBoveris, A., & Cadenas, E. (1975) · FEBS Letters · doi:10.1016/0014-5793(75)80928-8 · Cited by 401 · see citing works
Hyperoxia increases H2O2 release by lung mitochondria and microsomes
Turrens, J. F., Freeman, B. Α., & Crapo, J. D. (1982) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(82)90519-7 · Cited by 337 · see citing works
Self-citationCadenas, E., & Boveris, A. (1980) · Biochemical Journal · doi:10.1042/bj1880031 · Cited by 275 · see citing works
Studies on Cytochrome c Peroxidase
Yonetani, T., & Ray, G. S. (1965) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)97090-0 · Cited by 261 · see citing works
Malis, C. D., & Bonventre, J. V. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)67004-8 · Cited by 257 · see citing works
Induction of mitochondrial manganese superoxide dismutase by interleukin 1
Masuda, A., Longo, D. L., Kobayashi, Y., Appella, E., Oppenheim, J. J., & Matsushima, K. (1988) · The FASEB Journal · doi:10.1096/fasebj.2.15.3263930 · Cited by 227 · see citing works
Free radical-producing enzyme, xanthine oxidase, is undetectable in human hearts
Eddy, L. J., Stewart, J. R., Jones, H. P., Engerson, T. D., McCord, J. M., & Downey, J. M. (1987) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1987.253.3.h709 · Cited by 198 · see citing works
Self-citationMitochondrial H2O2 formation: Relationship with energy conservation
Loschen, G., Azzi, A., & Flohé, L. (1973) · FEBS Letters · doi:10.1016/0014-5793(73)80165-6 · Cited by 180 · see citing works
Increase in manganese superoxide dismutase activity in the mouse heart after X-irradiation
Oberley, L. W., Clair, D. K. S., Autor, A. P., & Oberley, T. D. (1987) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(87)90082-8 · Cited by 168 · see citing works
Induction of superoxide dismutase by oxygen in neonatal rat lung.
Stevens, J. B., & Autor, A. P. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)40420-0 · Cited by 138 · see citing works
Radioprotection of mice by superoxide dismtuase
Petkau, A., Chelack, W. S., Pleskach, S. D., Meeker, B. E., & Brady, C. M. (1975) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(75)80468-2 · Cited by 115 · see citing works
Maintenance of Energy-Linked Functions in Rat-Liver Mitochondria Aged in the Presence of Nupercaine
Scarpa, A., & LINDSAY, J. G. (1972) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1972.tb01851.x · Cited by 95 · see citing works
Effects of ischemia on the isolation and function of canine cardiac sarcoplasmic reticulum
Rapundalo, S., Briggs, F. N., & Feher, J. (1986) · Journal of Molecular and Cellular Cardiology · doi:10.1016/s0022-2828(86)80958-0 · Cited by 67 · see citing works
Mitochondrial Regulation of Intracellular Calcium
Fiskum, G. M., & Lehninger, A. L. (1982) · Elsevier eBooks · doi:10.1016/b978-0-12-171402-4.50008-3 · Cited by 53 · see citing works
Enhancement of ATPase Activity by a Lipid Peroxide of Arachidonic Acid in Rat Brain Microvessels
Koide, T., Asano, T., Matsushita, H., & Takakura, K. (1986) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1986.tb12952.x · Cited by 47 · see citing works
Malis, C. D., & Bonventre, J. V. (1988) · PubMed · Cited by 43 · see citing works
Mitochondrial inner membrane enzyme defects in porcine myocardial ischemia
ROUSLIN, W., & Millard, R. W. (1981) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1981.240.2.h308 · Cited by 23 · see citing works
Rapid procedure for the isolation of cytochrome c peroxidase
English, A. M., Laberge, M., & Walsh, M. (1986) · Inorganica Chimica Acta · doi:10.1016/s0020-1693(00)84310-8 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ischemic Cell Death in Brain Neurons
Lipton, P. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.4.1431 · Cited by 3,043 · see citing works
The mitochondrial permeability transition
Zoratti, M., & Szabó, I. (1995) · Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes · doi:10.1016/0304-4157(95)00003-a · Cited by 2,395 · see citing works
Superoxide production by the mitochondrial respiratory chain
Turrens, J. F. (1997) · Bioscience Reports · doi:10.1023/a:1027374931887 · Cited by 903 · see citing works
Self-citationMitochondrial Dysfunction in Cardiac Disease: Ischemia–Reperfusion, Aging, and Heart Failure
Lesnefsky, E. J., Moghaddas, S., Tandler, B., Kerner, J., & Hoppel, C. L. (2001) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2001.1378 · Cited by 709 · see citing works
Reactive Oxygen Species in the Regulation of Synaptic Plasticity and Memory
Massaad, C. A., & Klann, E. (2011) · Antioxidants & Redox Signaling · doi:10.1089/ars.2010.3208 · Cited by 635 · see citing works
Ambrosio, G., Zweier, J. L., Duilio, C., Kuppusamy, P., Santoro, G., Elia, P. P., Tritto, I., Cirillo, P. L., Condorelli, M., & Chiariello, M. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)46660-9 · Cited by 515 · see citing works
Stowe, D. F., & Camara, A. K. S. (2009) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2331 · Cited by 471 · see citing works
Generation of superoxide in cardiomyocytes during ischemia before reperfusion
Becker, L. B., Hoek, T. L. V., Shao, Z., Li, C., & Schumacker, P. T. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.277.6.h2240 · Cited by 413 · see citing works
Bcl-2 potentiates the maximal calcium uptake capacity of neural cell mitochondria.
Murphy, A. N., Bredesen, D. E., Cortopassi, G. A., Wang, E., & Fiskum, G. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.18.9893 · Cited by 403 · see citing works
Human disease, free radicals, and the oxidant/antioxidant balance
McCord, J. M. (1993) · Clinical Biochemistry · doi:10.1016/0009-9120(93)90111-i · Cited by 376 · see citing works
Self-citationThe syndrome of rhabdomyolysis: Pathophysiology and diagnosis
Giannoglou, G. D., Chatzizisis, Y. S., & Misirli, G. (2007) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2006.09.020 · Cited by 357 · see citing works
Jaarsma, D., Haasdijk, E. D., Grashorn, J., Hawkins, R. K., van Duijn, W., Verspaget, H. W., London, J., & Holstege, J. C. (2000) · Neurobiology of Disease · doi:10.1006/nbdi.2000.0299 · Cited by 351 · see citing works
González‐Flecha, B., Cutrìn, J. C., & Boveris, A. D. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116223 · Cited by 292 · see citing works
Metabolism of oxygen radicals in peroxisomes and cellular implications
del Río, L. A., Sandalio, L. M., Palma, J. M., Bueno, P., & Corpas, F. J. (1992) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(92)90150-f · Cited by 286 · see citing works
Kevin, L. G., Camara, A. K. S., Riess, M. L., Novalija, E., & Stowe, D. F. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00711.2002 · Cited by 272 · see citing works
Chen, Q., Camara, A. K. S., Stowe, D. F., Hoppel, C. L., & Lesnefsky, E. J. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00270.2006 · Cited by 271 · see citing works
Mitochondria as a Drug Target in Ischemic Heart Disease and Cardiomyopathy
Walters, A. M., Porter, G. A., Jr., & Brookes, P. S. (2012) · Circulation Research · doi:10.1161/circresaha.112.265660 · Cited by 268 · see citing works
Direct effect of Taxol on free radical formation and mitochondrial permeability transition
Várbiró, G., Veres, B., Gallyas, F., & Sümegi, B. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00616-5 · Cited by 252 · see citing works
Intracellular generation of reactive oxygen species by mitochondria
Nohl, H., Gille, L., & Staniek, K. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2004.12.002 · Cited by 251 · see citing works
Castilho, R. F., Kowaltowski, A. J., Meinicke, A., Bechara, E. J. H., & Vercesi, A. E. (1995) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(94)00166-h · Cited by 244 · see citing works
Reactive oxygen and DNA damage in mitochondria
Richter, C. (1992) · Mutation Research/DNAging · doi:10.1016/0921-8734(92)90029-o · Cited by 240 · see citing works
Enzyme function of copper, zinc superoxide dismutase as a free radical generator.
Yim, M. B., Chock, P. B., & Stadtman, E. R. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53585-7 · Cited by 228 · see citing works
Cocco, T., Di, M., Papa, P., & Lorusso, M. P. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00034-9 · Cited by 228 · see citing works
Oxygen Free Radicals and the Systemic Inflammatory Response
Closa, D., & Folch‐Puy, E. (2004) · IUBMB Life · doi:10.1080/15216540410001701642 · Cited by 206 · see citing works
Dare, A. J., Bolton, E. A., Pettigrew, G. J., Bradley, J. A., Saeb-Parsy, K., & Murphy, M. P. (2015) · Redox Biology · doi:10.1016/j.redox.2015.04.008 · Cited by 202 · see citing works
Redox signaling during hypoxia in mammalian cells
Smith, K. A., Waypa, G. B., & Schumacker, P. T. (2017) · Redox Biology · doi:10.1016/j.redox.2017.05.020 · Cited by 199 · see citing works
The cardiovascular effects and implications of peroxynitrite
Ronson, R. S. (1999) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00184-4 · Cited by 191 · see citing works
O 2 sensing, mitochondria and ROS signaling: The fog is lifting
Waypa, G. B., Smith, K. A., & Schumacker, P. T. (2016) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2016.01.002 · Cited by 190 · see citing works
Stachowiak, O., Dolder, M., Wallimann, T., & Richter, C. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.27.16694 · Cited by 189 · see citing works
Reperfusion injury on cardiac myocytes after simulated ischemia
Hoek, T. L. V., Shao, Z., Li, C., Zak, R., Schumacker, P. T., & Becker, L. B. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.270.4.h1334 · Cited by 188 · see citing works
Sakellariou, G. K., Jackson, M. J., & Vasilaki, A. (2014) · Free Radical Research · doi:10.3109/10715762.2013.830718 · Cited by 184 · see citing works
Reactive oxygen species in developmental toxicity: Review and hypothesis
Fantel, A. G. (1996) · Teratology · doi:10.1002/(sici)1096-9926(199603)53:3 · Cited by 171 · see citing works
Are mitochondria a permanent source of reactive oxygen species?
Staniek, K., & Nohl, H. (2000) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(00)00152-3 · Cited by 162 · see citing works
The reaction of nitric oxide with ubiquinol: kinetic properties and biological significance
Poderoso, J. J., Carreras, M. C., Schopfer, F. J., Lisdero, C. L., Galdo, N. A. R., Giulivi, C., Boveris, A. D., Boveris, A., & Cadenas, E. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00277-9 · Cited by 156 · see citing works
Chinopoulos, C., Tretter, L., & Ádám‐Vizi, V. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0730220.x · Cited by 154 · see citing works
Acquired skeletal muscle metabolic myopathy in atherosclerotic peripheral arterial disease
Brass, E. P., & Hiatt, W. R. (2000) · Vascular Medicine · doi:10.1177/1358836x0000500109 · Cited by 150 · see citing works
Halmosi, R., Berente, Z., Ősz, E., Tóth, K., Literati-Nagy, P., & Sümegi, B. (2001) · Molecular Pharmacology · doi:10.1124/mol.59.6.1497 · Cited by 140 · see citing works
Lactate and P o 2 Modulate Superoxide Anion Production in Bovine Cardiac Myocytes
Mohazzab-H., K. M., Kaminski, P. M., & Wolin, M. S. (1997) · Circulation · doi:10.1161/01.cir.96.2.614 · Cited by 140 · see citing works
Packer, M. A., & Murphy, M. P. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.231_c.x · Cited by 139 · see citing works
Lesnefsky, E. J., Chen, Q., Slabe, T. J., Stoll, M. S. K., Minkler, P. E., Hassan, M. O., Tandler, B., & Hoppel, C. L. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00348.2003 · Cited by 135 · see citing works
Nanotechnology inspired tools for mitochondrial dysfunction related diseases
Wen, R. M., Banik, B., Pathak, R., Kumar, A., Kolishetti, N., & Dhar, S. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.12.024 · Cited by 130 · see citing works
Staniek, K., & Nohl, H. (1999) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(99)00083-3 · Cited by 124 · see citing works
Dare, A. J., Logan, A., Prime, T. A., Rogatti, S., Goddard, M., Bolton, E. M., Bradley, J. A., Pettigrew, G. J., Murphy, M. P., & Saeb-Parsy, K. (2015) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2015.05.007 · Cited by 119 · see citing works
State of the Art in Therapeutic Hypothermia
Lampe, J. W., & Becker, L. B. (2010) · Annual Review of Medicine · doi:10.1146/annurev-med-052009-150512 · Cited by 118 · see citing works
Skeletal Muscle Mitochondrial DNA Injury in Patients With Unilateral Peripheral Arterial Disease
Bhat, H. K., Hiatt, W. R., Hoppel, C. L., & Brass, E. P. (1999) · Circulation · doi:10.1161/01.cir.99.6.807 · Cited by 116 · see citing works
Free radical production in hypoxic pulmonary artery smooth muscle cells
Killilea, D. W., Hester, R. B., Balczon, R., Babál, P., & Gillespie, M. N. (2000) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2000.279.2.l408 · Cited by 114 · see citing works
Leprince, O., Atherton, N. M., DELTOUR, R., & Hendry, G. A. F. (1994) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.4.1333 · Cited by 113 · see citing works
Antioxidant ebselen reduces oxidative damage in focal cerebral ischemia
Imai, H., Graham, D. I., Masayasu, H., & Macrae, I. M. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)01180-2 · Cited by 112 · see citing works
Production of reactive oxygen by mitochondria from normoxic and hypoxic rat heart tissue
Paraidathathu, T., de GROOT, H., & Kehrer, J. P. (1992) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(92)90176-h · Cited by 109 · see citing works
Aldakkak, M., Stowe, D. F., Chen, Q., Lesnefsky, E. J., & Camara, A. K. S. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2007.08.008 · Cited by 108 · see citing works
Tammaro, A., Kers, J., Scantlebery, A. M. L., & Florquin, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01346 · Cited by 102 · see citing works
DNA Damage as the Cause of Ionizing Radiation-Induced Gene Activation
Ward, J. F. (1994) · Radiation Research · doi:10.2307/3578769 · Cited by 92 · see citing works
Formation of reactive oxygen species by the contracting diaphragm is PLA2dependent
Nethery, D. E., Stofan, D. A., Callahan, L. A., DiMarco, A. F., & Supinski, G. S. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.2.792 · Cited by 92 · see citing works
Mitochondrial calcium release induced by prooxidants
Richter, C., & Schlegel, J. (1993) · Toxicology Letters · doi:10.1016/0378-4274(93)90050-8 · Cited by 86 · see citing works
Szabados, E., Literati-Nagy, P., Farkas, B., & Sümegi, B. (2000) · Biochemical Pharmacology · doi:10.1016/s0006-2952(99)00418-9 · Cited by 84 · see citing works
The beneficial effects of dietary restriction: reduced oxidative damage and enhanced apoptosis
Wachsman, J. T. (1996) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(95)00087-9 · Cited by 84 · see citing works
Nohl, H., Koltover, V. K., Stolze, K., & Esterbauer, H. (1993) · Free Radical Research Communications · doi:10.3109/10715769309147486 · Cited by 82 · see citing works
Castiglione, N., Rinaldo, S., Giardina, G., Stelitano, V., & Cutruzzolà, F. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4196 · Cited by 79 · see citing works
Kondo, T., Sharp, F. R., Honkaniemi, J., Mikawa, S., Epstein, C. J., & Chan, P. H. (1997) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199703000-00001 · Cited by 79 · see citing works
Heise, K., Puntarulo, S., Nikinmaa, M., Lucassen, M., Pörtner, H., & Abele, D. (2006) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2006.01.014 · Cited by 78 · see citing works
Mitochondrial sites of hydrogen peroxide production in reperfused rat kidney cortex
González‐Flecha, B., & Boveris, A. (1995) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(94)00160-y · Cited by 77 · see citing works
MacFarlane, N. G., & Miller, D. J. (1992) · Circulation Research · doi:10.1161/01.res.70.6.1217 · Cited by 77 · see citing works
Exercise training and peripheral vascular disease
Tan, K. H., de Cossart, L., & Edwards, P. R. (2000) · British journal of surgery · doi:10.1046/j.1365-2168.2000.01445.x · Cited by 77 · see citing works
Role of oxidative stress in alterations of mitochondrial function in ischemic-reperfused hearts
Makazan, Z., Saini, H. K., & Dhalla, N. S. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01214.2006 · Cited by 76 · see citing works
da Silva, M. M., Sartori, A., Belisle, E., & Kowaltowski, A. J. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00955.2002 · Cited by 73 · see citing works
Role of nitric oxide in liver ischemia and reperfusion injury
Hines, I. N., Kawachi, S., Harada, S., Pavlick, K. P., Hoffman, J. M., Bharwani, S., Wolf, R. E., & Grisham, M. B. (2002) · Springer eBooks · doi:10.1007/978-1-4615-1087-1_27 · Cited by 73 · see citing works
Chinopoulos, C., Tretter, L., Rozsa, A., & Ádám‐Vizi, V. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02094.2000 · Cited by 73 · see citing works
In the eye of the storm: mitochondrial damage during heart and brain ischaemia
Borutaitė, V., Toleikis, A., & Brown, G. C. (2013) · FEBS Journal · doi:10.1111/febs.12353 · Cited by 72 · see citing works
Role of nitric oxide in liver ischemia and reperfusion injury
Hines, I. N., Kawachi, S., Harada, H., Pavlick, K. P., Hoffman, J. M., Bharwani, S., Wolf, R. E., & Grisham, M. B. (2002) · Molecular and Cellular Biochemistry · doi:10.1023/a:1015952926016 · Cited by 67 · see citing works
Yu, H., Guan, Q., Guo, L., Zhang, H., Pang, X., Cheng, Y., Zhang, X., & Sun, Y. (2016) · Cell Stress and Chaperones · doi:10.1007/s12192-016-0669-5 · Cited by 66 · see citing works
Radí, R., Sims, S., Cassina, A., & Turrens, J. F. (1993) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(93)90169-u · Cited by 66 · see citing works
Self-citationChen, Q., & Lesnefsky, E. J. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.02.029 · Cited by 64 · see citing works
Dev, R. R., Ganji, R., Singh, S. P., Mahalingam, S., Banerjee, S., & Khosla, S. (2017) · Biochemical Journal · doi:10.1042/bcj20170258 · Cited by 64 · see citing works
Okuda, M., LEE, H. ‐., Kumar, C., & Chance, B. (1992) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1992.tb09351.x · Cited by 64 · see citing works
Sodium tanshinone IIA sulfonate mediates electron transfer reaction in rat heart mitochondria
Zhou, G., Jiang, W., Zhao, Y., Ma, G.-E., Xin, W., Yin, J., & Zhao, B. (2002) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)01447-8 · Cited by 61 · see citing works
Thomas, G. P., Sims, S. M., Cook, M. A., & Karmazyn, M. (1998) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37713-4 · Cited by 60 · see citing works
The protective effect of nebivolol on ischemia/reperfusion injury in rabbit spinal cord
İlhan, A., Yılmaz, H. R., Armutçu, F., Gürel, A., & Akyol, Ö. (2004) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2004.06.023 · Cited by 60 · see citing works
Mitochondrial dysfunction in ischaemia‐reperfusion
Saris, N., & ERIKSSON, K. O. (1995) · Acta Anaesthesiologica Scandinavica · doi:10.1111/j.1399-6576.1995.tb04353.x · Cited by 60 · see citing works
Ischemia/reperfusion: A new hypothesis for the developmental toxicity of cocaine
Fantel, A. G., Barber, C. V., & Mackler, B. F. (1992) · Teratology · doi:10.1002/tera.1420460313 · Cited by 60 · see citing works
Sepsis increases contraction-related generation of reactive oxygen species in the diaphragm
Nethery, D. E., DiMarco, A. F., Stofan, D. A., & Supinski, G. S. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.4.1279 · Cited by 59 · see citing works
Castilho, R. F., Kowaltowski, A. J., & Vercesi, A. E. (1998) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1998.0657 · Cited by 59 · see citing works
Therapeutic Hypothermia in Stroke and Traumatic Brain Injury
Faridar, A., Bershad, E. M., Emiru, T., Iaizzo, P. A., Suárez, J. I., & Divani, A. A. (2011) · Frontiers in Neurology · doi:10.3389/fneur.2011.00080 · Cited by 58 · see citing works
The Role of Mitochondrial Dysfunction in Preeclampsia: Causative Factor or Collateral Damage?
Smith, A. N., Wang, X., Thomas, D. G., Tatum, R. E., Booz, G. W., & Cunningham, M. (2021) · American Journal of Hypertension · doi:10.1093/ajh/hpab003 · Cited by 54 · see citing works
Herrero, A., Portero‐Otín, M., Bellmunt, M. J., Pamplona, R., & Barja, G. (2001) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00214-7 · Cited by 53 · see citing works
Lambert, W. S., Clark, A. F., & Wordinger, R. J. (2004) · BMC Neuroscience · doi:10.1186/1471-2202-5-51 · Cited by 48 · see citing works
McCord, J. M., & Omar, B. A. (1993) · Toxicology and Industrial Health · doi:10.1177/0748233793009001-204 · Cited by 48 · see citing works
Self-citationHeart mitochondria and calpain 1: Location, function, and targets
Chen, Q., & Lesnefsky, E. J. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.08.004 · Cited by 47 · see citing works
Fragmentation of human ceruloplasmin induced by hydrogen peroxide
Choi, S.-W. (2000) · Biochimie · doi:10.1016/s0300-9084(00)00380-1 · Cited by 47 · see citing works
Pearce, L. L., Pitt, B. R., & Peterson, J. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.50.35763 · Cited by 47 · see citing works
Hendgen-Cotta, U. B., Kelm, M., & Rassaf, T. (2010) · Nitric Oxide · doi:10.1016/j.niox.2009.10.003 · Cited by 46 · see citing works
Daval, J., Ghersi‐Egea, J., Oillet, J., & Koziel, V. (1995) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1995.8 · Cited by 46 · see citing works
Fantel, A. G., Barber, C. V., Carda, M. B., Tumbic, R. W., & Mackler, B. F. (1992) · Teratology · doi:10.1002/tera.1420460314 · Cited by 46 · see citing works
Mehrotra, A., Kanwal, A., Banerjee, S., & Sandhir, R. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.02.004 · Cited by 45 · see citing works
Calcium-dependent free radical generation in cultured retinal neurons injured by kainate
Dutrait, N., Culcasi, M., Cazevieille, C., Pietri, S., Tordo, P., Bonne, C., & Müller, A. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11948-v · Cited by 45 · see citing works
Oxidative stress modifies the activity of cardiac sarcolemmal phospholipase C
Meij, J. T. A., Suzuki, S., Panagia, V., & Dhalla, N. S. (1994) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(94)90089-2 · Cited by 40 · see citing works
Complexity of free radical Metabolism in human Erythrocytes
Nikolić‐Kokić, A., Blagojević, D. P., & Spasić, M. B. (2010) · Journal of Medical Biochemistry · doi:10.2478/v10011-010-0018-7 · Cited by 38 · see citing works
The Slo(w) path to identifying the mitochondrial channels responsible for ischemic protection
Smith, C. O., Nehrke, K. W., & Brookes, P. S. (2017) · Biochemical Journal · doi:10.1042/bcj20160623 · Cited by 37 · see citing works
Liu, X., Murphy, M. P., Xing, W., Wu, H., Zhang, R., & Sun, H. (2017) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26772 · Cited by 37 · see citing works
Hamed, M. O., Logan, A., Gruszczyk, A. V., Beach, T. E., James, A. M., Dare, A. J., Barlow, A. D., Martin, J. L., Georgakopoulos, N., Gane, A., et al. (2021) · British journal of surgery · doi:10.1093/bjs/znab108 · Cited by 37 · see citing works
Studies of mitochondria in oxidative embryotoxicity
Fantel, A. G., Person, R., Tumbic, R. W., Nguyen, T., & Mackler, B. F. (1995) · Teratology · doi:10.1002/tera.1420520404 · Cited by 36 · see citing works
- Authors
- Turrens, J. F., Beconi, M., Barilla, J., Chavez, U. B., & McCord, J. M.
- Affiliations
- University of South Alabama (US)
- ORCID
- McCord, Joe M.
- Venue
- Free Radical Research Communications
- Publisher
- Informa UK Limited
- Published
- 1991-01
- Volume
- 13
- Issue
- 1
- Pages
- 681-689
- ISSN
- 8755-0199 (ISSN-L)
- OpenAlex
- W2113144597
- Cited by
- 177
- References
- 29
- Citations by year
- 2026: 2 · 2024: 1 · 2023: 1 · 2021: 6 · 2020: 1 · 2019: 1 · 2018: 3 · 2017: 7 · 2016: 3 · 2015: 6 · 2014: 3 · 2013: 4 · 2012: 6
- FWCI
- 10.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Free Radical Research Communications (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association
- Universidad de Buenos Aires
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- ischemia-reperfusion injury, reoxygenation, hydroxyapatite crystals, mitochondrial calcium overload, electron transport inhibition, NADH dehydrogenase, coenzyme Q10, mitochondrial uncoupling, hydrogen peroxide, phospholipase A2, arachidonic acid, linoleic acid, albumin, heart mitochondria
- MeSH terms
- Animals, Fatty Acids, Free Radicals, Hydrogen Peroxide, Mitochondria, Heart, Oxygen, Oxygen Consumption, Rabbits, Myocardial Reperfusion Injury, Rats, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
