Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria

Turrens, Julio F.; Alexandre, Adolfo; Lehninger, Albert L.

doi:10.1016/0003-9861(85)90293-0

Cited by 1,214Mitochondrial Function and PathologyCoenzyme Q10 studies and effectsRedox biology and oxidative stress

Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria

Turrens, Julio F., Alexandre, Adolfo, Lehninger, Albert L.·1985·Archives of Biochemistry and Biophysics

DOI 10.1016/0003-9861(85)90293-0

Open this paper in CoChat — free account

Abstract

Much evidence indicates that superoxide is generated from O2 in a cyanide-sensitive reaction involving a reduced component of complex III of the mitochondrial respiratory chain, particularly when antimycin A is present. Although it is generally believed that ubisemiquinone is the electron donor to O2, little experimental evidence supporting this view has been reported. Experiments with succinate as electron donor in the presence of antimycin A in intact rat heart mitochondria, which contain much superoxide dismutase but little catalase, showed that myxothiazol, which inhibits reduction of the Rieske iron-sulfur center, prevented formation of hydrogen peroxide, determined spectrophotometrically as the H2O2-peroxidase complex. Similarly, depletion of the mitochondria of their cytochrome c also inhibited formation of H2O2, which was restored by addition of cytochrome c. These observations indicate that factors preventing the formation of ubisemiquinone also prevent H2O2 formation. They also exclude ubiquinol, which remains reduced under these conditions, as the reductant of O2. Since cytochrome b also remains fully reduced when myxothiazol is added to succinate- and antimycin A-supplemented mitochondria, reduced cytochrome b may also be excluded as the reductant of O2. These observations, which are consistent with the Q-cycle reactions, by exclusion of other possibilities leave ubisemiquinone as the only reduced electron carrier in complex III capable of reducing O2 to O2-.

Integrity signals

Registry

Crossref · 10.1016/0003-9861(85)90293-0

Cites

23 of 23 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

The unpaired electron of ubisemiquinone is normally transferred to the cytochrome b center of complex III, but can also react with molecular oxygen to form superoxide.
“Normally, the unpaired electron of ubisemiquinone is transferred to the cytochrome b center of complex III; however, this electron can also react with molecular oxygen to form superoxide 2, 26.”
From Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes (2010) · cites this paper as [26]

Superoxide Dismutase
McCord, J. M., & Fridovich, I. (1969) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)63504-5 · Cited by 12,952 · see citing works
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 mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen
Boveris, A., & Chance, B. (1973) · Biochemical Journal · doi:10.1042/bj1340707 · Cited by 2,626 · 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-citation
The 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
Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria
Cadenas, E., Boveris, A., Ragan, C. I., & Stoppani, A. O. M. (1977) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(77)90035-2 · Cited by 855 · 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
Purification of horse-radish peroxidase and comparison of its properties with those of catalase and methaemoglobin
Keilin, D., & Hartree, E. F. (1951) · Biochemical Journal · doi:10.1042/bj0490088 · Cited by 581 · 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-citation
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-citation
The Reversible Removal of Cytochrome c from Mitochondria
Jacobs, E. E., & Sanadi, D. R. (1960) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)69561-4 · Cited by 322 · see citing works
Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids
Takahashi, M., & Asada, K. (1983) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(83)90325-9 · Cited by 309 · see citing works
Oxidoreduction of cytochrome b in the presence of antimycin
Wikström, M. K. F., & BERDEN, J. A. (1972) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(72)90258-7 · Cited by 280 · see citing works
Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria
Cadenas, E., & Boveris, A. (1980) · Biochemical Journal · doi:10.1042/bj1880031 · Cited by 275 · see citing works
Oudemansin, strobilurin A, strobilurin B and myxothiazol: new inhibitors of the bc1 segment of the respiratory chain with an E‐β‐methoxyacrylate system as common structural element
Becker, W. F., von JAGOW, G., Anke, T., & Steglich, W. (1981) · FEBS Letters · doi:10.1016/0014-5793(81)81190-8 · Cited by 262 · see citing works
Myxothiazol, a new inhibitor of the cytochrome b-c1 segment of the respiratory chain
Thierbach, G., & Reichenbach, H. (1981) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(81)90238-3 · Cited by 236 · see citing works
Stoichiometry of H+ ejection and Ca2+ uptake coupled to electron transport in rat heart mitochondria.
Vercesi, A. E., Reynafarje, B., & Lehninger, A. L. (1978) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)46944-5 · Cited by 229 · see citing works
Self-citation
Mitochondrial 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
An inhibitor of mitochondrial respiration which binds to cytochrome b and displaces quinone from the iron-sulfur protein of the cytochrome bc1 complex.
von JAGOW, G., Ljungdahl, P. O., Gräf, P., Ohnishi, T., & Trumpower, B. L. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)82143-7 · Cited by 152 · see citing works
Complete inhibition of electron transfer from ubiquinol to cytochrome b by the combined action of antimycin and myxothiazol
von JAGOW, G., & Engel, W. D. (1981) · FEBS Letters · doi:10.1016/0014-5793(81)81206-9 · Cited by 152 · see citing works
A new species of bound ubisemiquinone anion in QH2: cytochrome c oxidoreductase.
de Vries, S., Albracht, S. P. J., BERDEN, J. A., & Slater, E. C. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)43222-x · Cited by 132 · see citing works
The effect of pH, ubiquinone depletion and myxothiazol on the reduction kinetics of the prosthetic groups of ubiquinol: Cytochrome c oxidoreductase
de Vries, S., Albracht, S. P. J., BERDEN, J. A., Marres, C. A. M., & Slater, E. C. (1983) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(83)90013-0 · Cited by 93 · see citing works
Rapid reduction of cytochrome c1 in the presence of antimycin and its implication for the mechanism of electron transfer in the cytochrome b-c1 segment of the mitochondrial respiratory chain.
Bowyer, J. R., & Trumpower, B. L. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)69768-1 · Cited by 75 · see citing works

Flagged first, then by citations

Sorted by citations

Free Radicals in the Physiological Control of Cell Function
Dröge, W. (2002) · Physiological Reviews · doi:10.1152/physrev.00018.2001 · Cited by 9,855 · see citing works
How mitochondria produce reactive oxygen species
Murphy, M. P. (2009) · Biochemical Journal · doi:10.1042/bj20081386 · Cited by 8,207 · see citing works
Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple
Schafer, F. Q., & Buettner, G. R. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00480-4 · Cited by 4,587 · see citing works
Mitochondria, Oxidants, and Aging
Balaban, R. S., Nemoto, S., & Finkel, T. (2005) · Cell · doi:10.1016/j.cell.2005.02.001 · Cited by 4,388 · see citing works
Mitochondrial formation of reactive oxygen species
Turrens, J. F. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049478 · Cited by 5,084 · see citing works
Self-citation
Cellular energy utilization and molecular origin of standard metabolic rate in mammals
Rolfe, D. F., & Brown, G. C. (1997) · Physiological Reviews · doi:10.1152/physrev.1997.77.3.731 · Cited by 2,021 · see citing works
Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia
Chandel, N. S., McClintock, D. S., Feliciano, C. E., Wood, T. M., Melendez, J. A., Rodriguez, A. M., & Schumacker, P. T. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001914200 · Cited by 2,000 · see citing works
Regulation of Mammalian O 2 Homeostasis by Hypoxia-Inducible Factor 1
Semenza, G. L. (1999) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.15.1.551 · Cited by 1,914 · see citing works
Mitochondrial reactive oxygen species trigger hypoxia-induced transcription
Chandel, N. S., Maltepe, E., Goldwasser, E., Mathieu, C. E., Simon, M. C., & Schumacker, P. T. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11715 · Cited by 1,926 · see citing works
Production of Reactive Oxygen Species by Mitochondria
Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L., & Lesnefsky, E. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304854200 · Cited by 1,616 · see citing works
Topology of superoxide production from different sites in the mitochondrial electron transport chain
St-Pierre, J., Buckingham, J. A., Roebuck, S. J., & Brand, M. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207217200 · Cited by 1,545 · see citing works
Selective degradation of mitochondria by mitophagy
Kim, I., Rodriguez-Enriquez, S., & Lemasters, J. J. (2007) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2007.03.034 · Cited by 1,558 · see citing works
Mitochondrial metabolism of reactive oxygen species
Andreyev, A. Y., Kushnareva, Y. E., & Starkov, A. A. (2005) · Biochemistry (Moscow) · doi:10.1007/s10541-005-0102-7 · Cited by 1,336 · see citing works
Generation of reactive oxygen species by the mitochondrial electron transport chain
Liu, Y., Fiskum, G., & Schubert, D. (2002) · Journal of Neurochemistry · doi:10.1046/j.0022-3042.2002.00744.x · Cited by 1,260 · see citing works
The sites and topology of mitochondrial superoxide production
Brand, M. D. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.01.003 · Cited by 1,217 · see citing works
Mitochondria and reactive oxygen species
Kowaltowski, A. J., de Souza-Pinto, N. C., Castilho, R. F., & Vercesi, A. E. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.05.004 · Cited by 1,162 · see citing works
Mitochondrial generation of superoxide and hydrogen peroxide as the source of mitochondrial redox signaling
Brand, M. D. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.04.001 · Cited by 1,063 · see citing works
Complex iii releases superoxide to both sides of the inner mitochondrial membrane
Muller, F. L., Liu, Y., & Van Remmen, H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407715200 · Cited by 1,036 · see citing works
Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins
Brand, M. D., Affourtit, C., Esteves, T. C., Green, K., Lambert, A. J., Miwa, S., Pakay, J. L., & Parker, N. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.05.034 · Cited by 1,032 · see citing works
Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes
Hamanaka, R. B., & Chandel, N. S. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.04.002 · Cited by 1,011 · see citing works
Radicals and oxidative stress in diabetes
West, I. C. (2000) · Diabetic Medicine · doi:10.1046/j.1464-5491.2000.00259.x · Cited by 913 · 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-citation
Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia
Guzy, R. D., & Schumacker, P. T. (2006) · Experimental Physiology · doi:10.1113/expphysiol.2006.033506 · Cited by 881 · 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
Persistent inhibition of cell respiration by nitric oxide: Crucial role of S -nitrosylation of mitochondrial complex I and protective action of glutathione
Clementi, E., Brown, G. C., Feelisch, M., & Moncada, S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.13.7631 · Cited by 863 · see citing works
A Unifying Mechanism for Mitochondrial Superoxide Production during Ischemia-Reperfusion Injury
Chouchani, E. T., Pell, V. R., James, A. M., Work, L. M., Saeb-Parsy, K., Frezza, C., Krieg, T., & Murphy, M. P. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.12.009 · Cited by 752 · see citing works
Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes
Vanden Hoek, T. L., Becker, L. B., Shao, Z., Li, C., & Schumacker, P. T. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.29.18092 · Cited by 721 · see citing works
Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol
Han, D., Antunes, F., Canali, R., Rettori, D., & Cadenas, E. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210269200 · Cited by 711 · see citing works
Redistribution of Intracellular Oxygen in Hypoxia by Nitric Oxide: Effect on HIF1α
Hagen, T., Taylor, C. T., Lam, F., & Moncada, S. (2003) · Science · doi:10.1126/science.1088805 · Cited by 704 · see citing works
A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes.
Ishii, N., Fujii, M., Hartman, P. S., Tsuda, M., Yasuda, K., Senoo-Matsuda, N., Yanase, S., Ayusawa, D., & Suzuki, K. (1998) · Nature · doi:10.1038/29331 · Cited by 687 · see citing works
Role of mitochondria in oxidative stress and ageing
Lenaz, G. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00120-0 · Cited by 650 · see citing works
ΔΨ m ‐Dependent and ‐independent production of reactive oxygen species by rat brain mitochondria
Votyakova, T. V., & Reynolds, I. J. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00548.x · Cited by 601 · see citing works
Mitochondrial disease in superoxide dismutase 2 mutant mice
Melov, S., Coskun, P., Patel, M., Tuinstra, R., Cottrell, B., Jun, A. S., Zastawny, T. H., Dizdaroglu, M., Goodman, S. I., Huang, T.-T., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.3.846 · Cited by 581 · see citing works
Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies
Förstermann, U. (2008) · Nature Clinical Practice Cardiovascular Medicine · doi:10.1038/ncpcardio1211 · Cited by 576 · see citing works
The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production
Bell, E. L., Klimova, T. A., Eisenbart, J., Moraes, C. T., Murphy, M. P., Budinger, G. R. S., & Chandel, N. S. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200609074 · Cited by 568 · see citing works
Mitochondrial mutations may increase oxidative stress: Implications for carcinogenesis and aging?
Bandy, B., & Davison, A. J. (1990) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(90)90152-9 · Cited by 550 · see citing works
Synchronized Whole Cell Oscillations in Mitochondrial Metabolism Triggered by a Local Release of Reactive Oxygen Species in Cardiac Myocytes
Aon, M. A., Cortassa, S., Marbán, E., & O'Rourke, B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302673200 · Cited by 521 · see citing works
Mitochondrial Oxygen Radical Generation and Leak: Sites of Production in States 4 and 3, Organ Specificity, and Relation to Aging and Longevity
Barja, G. (1999) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1005427919188 · Cited by 494 · see citing works
Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial nadh:Ubiquinone oxidoreductase (complex i)
Lambert, A. J., & Brand, M. D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406576200 · Cited by 480 · see citing works
Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation
Tahara, E. B., Navarete, F. D. T., & Kowaltowski, A. J. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.02.008 · Cited by 479 · see citing works
Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane
LAMBERT, A. J., & BRAND, M. D. (2004) · Biochemical Journal · doi:10.1042/bj20040485 · Cited by 470 · see citing works
Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function
Stowe, D. F., & Camara, A. K. S. (2009) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2331 · Cited by 471 · see citing works
Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age
Hansford, R. G., Hogue, B. A., & Mildaziene, V. (1997) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1022420007908 · Cited by 447 · see citing works
Production of Reactive Oxygen Species in Brain Mitochondria: Contribution by Electron Transport Chain and Non–Electron Transport Chain Sources
Adam-Vizi, V. (2005) · Antioxidants & Redox Signaling · doi:10.1089/ars.2005.7.1140 · Cited by 439 · see citing works
Loss of the SdhB, but Not the SdhA, Subunit of Complex II Triggers Reactive Oxygen Species-Dependent Hypoxia-Inducible Factor Activation and Tumorigenesis
Guzy, R. D., Sharma, B., Bell, E., Chandel, N. S., & Schumacker, P. T. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01338-07 · Cited by 427 · see citing works
Aerobic glycolysis by proliferating cells: a protective strategy against reactive oxygen species 1
Brand, K. A., & Hermfisse, U. (1997) · The FASEB Journal · doi:10.1096/fasebj.11.5.9141507 · Cited by 401 · see citing works
Mitochondrial ROS Generation and Its Regulation: Mechanisms Involved in H 2 O 2 Signaling
Rigoulet, M., Yoboue, E. D., & Devin, A. (2011) · Antioxidants & Redox Signaling · doi:10.1089/ars.2010.3363 · Cited by 394 · see citing works
Superoxide generation by complex III: From mechanistic rationales to functional consequences
Bleier, L., & Dröse, S. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.12.002 · Cited by 369 · see citing works
Model for Hypoxic Pulmonary Vasoconstriction Involving Mitochondrial Oxygen Sensing
Waypa, G. B., Chandel, N. S., & Schumacker, P. T. (2001) · Circulation Research · doi:10.1161/hh1201.091960 · Cited by 367 · see citing works
Mitochondrial reactive oxygen species and Ca 2+ signaling
Camello-Almaraz, C., Gomez-Pinilla, P. J., Pozo, M. J., & Camello, P. J. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00217.2006 · Cited by 336 · see citing works
Mitochondrial reactive oxygen species regulate hypoxic signaling
Hamanaka, R. B., & Chandel, N. S. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.08.005 · Cited by 332 · see citing works
Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria
López-Torres, M., Gredilla, R., Sanz, A., & Barja, G. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00773-6 · Cited by 277 · see citing works
HO 2 •: The Forgotten Radical
de Grey, A. D. N. J. (2002) · DNA and Cell Biology · doi:10.1089/104454902753759672 · Cited by 279 · see citing works
Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin
Petrosillo, G., Francesca, M. R., Di Venosa, N., & Paradies, A. G. (2003) · The FASEB Journal · doi:10.1096/fj.02-0729fje · Cited by 261 · see citing works
Understanding Ubiquinone
Wang, Y., & Hekimi, S. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.12.007 · Cited by 256 · see citing works
A Mitochondrial Oscillator Dependent on Reactive Oxygen Species
Cortassa, S., Aon, M. A., Winslow, R. L., & O’Rourke, B. (2004) · Biophysical Journal · doi:10.1529/biophysj.104.041749 · Cited by 235 · see citing works
Superoxides from mitochondrial complex III: the role of manganese superoxide dismutase
Raha, S., McEachern, G. E., Myint, A. T., & Robinson, B. H. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00338-5 · Cited by 223 · see citing works
Novel DNA mismatch-repair activity involving YB-1 in human mitochondria
de Souza-Pinto, N. C., Mason, P. A., Hashiguchi, K., Weissman, L., Tian, J., Guay, D., Lebel, M., Stevnsner, T. V., Rasmussen, L. J., & Bohr, V. A. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.01.021 · Cited by 214 · see citing works
Essential role of complex II of the respiratory chain in hypoxia-induced ROS generation in the pulmonary vasculature
Paddenberg, R., Ishaq, B., Goldenberg, A., Faulhammer, P., Rose, F., Weissmann, N., Braun-Dullaeus, R. C., & Kummer, W. (2003) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00149.2002 · Cited by 184 · see citing works
Redefining the major contributors to superoxide production in contracting skeletal muscle. The role of NAD(P)H oxidases
Sakellariou, G. K., Jackson, M. J., & Vasilaki, A. (2014) · Free Radical Research · doi:10.3109/10715762.2013.830718 · Cited by 184 · see citing works
Suppressors of Superoxide Dismutase (SOD1) Deficiency in Saccharomyces cerevisiae
Strain, J., Lorenz, C. R., Bode, J., Garland, S., Smolen, G. A., Ta, D. T., Vickery, L. E., & Culotta, V. C. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.47.31138 · Cited by 181 · see citing works
Mitochondrial Generation of Oxygen Radicals During Reoxygenation of Ischemic Tissues
Turrens, J. F., Beconi, M., Barilla, J., Chavez, U. B., & McCord, J. M. (1991) · Free Radical Research Communications · doi:10.3109/10715769109145847 · Cited by 177 · see citing works
Self-citation
Ischemic Injury to Mitochondrial Electron Transport in the Aging Heart: Damage to the Iron–Sulfur Protein Subunit of Electron Transport Complex III
Lesnefsky, E. J., Gudz, T. I., Migita, C. T., Ikeda-Saito, M., Hassan, M. O., Turkaly, P. J., & Hoppel, C. L. (2001) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2000.2066 · Cited by 160 · see citing works
Frataxin interacts functionally with mitochondrial electron transport chain proteins
González-Cabo, P., Vázquez-Manrique, R. P., García-Gimeno, M. A., Sanz, P., & Palau, F. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi214 · Cited by 140 · see citing works
Inhibitor-complexed Structures of the Cytochrome bc1 from the Photosynthetic Bacterium Rhodobacter sphaeroides
Esser, L., Elberry, M., Zhou, F., Yu, C.-A., Yu, L., & Xia, D. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m708608200 · Cited by 137 · see citing works
Myxothiazol Induces H2O2 Production from Mitochondrial Respiratory Chain
Starkov, A. A., & Fiskum, G. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4409 · Cited by 133 · see citing works
Respiration-dependent Removal of Exogenous H2O2 in Brain Mitochondria
Zoccarato, F., Cavallini, L., & Alexandre, A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m308143200 · Cited by 130 · see citing works
Self-citation
Effect of Coenzyme Q10 Intake on Endogenous Coenzyme Q Content, Mitochondrial Electron Transport Chain, Antioxidative Defenses, and Life Span of Mice
Sohal, R. S., Kamzalov, S., Sumien, N., Ferguson, M., Rebrin, I., Heinrich, K. R., & Forster, M. J. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.08.037 · Cited by 131 · see citing works
Hypoxia Promotes Immune Evasion by Triggering β-Glucan Masking on the Candida albicans Cell Surface via Mitochondrial and cAMP-Protein Kinase A Signaling
Pradhan, A., Avelar, G. M., Bain, J. M., Childers, D. S., Larcombe, D. E., Netea, M. G., Shekhova, E., Munro, C. A., Brown, G. D., Erwig, L. P., et al. (2018) · mBio · doi:10.1128/mbio.01318-18 · Cited by 133 · see citing works
Effect of Cytochrome c on the Generation and Elimination of O<mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML" altimg="si1.gif"><mml:msubsup><mml:mrow/><mml:mrow><mml:mn>2</mml:mn></mml:mrow><mml:mrow><mml:mo>⨪</mml:mo></mml:mrow></mml:msubsup></mml:math> and H2O2 in Mitochondria
Zhao, Y., Wang, Z.-B., & Xu, J.-X. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209681200 · Cited by 129 · see citing works
Reactive oxygen species production by the mitochondrial respiratory chain in isolated rat hepatocytes and liver mitochondria: studies using myxothiazol
Young, T. A., Cunningham, C. C., & Bailey, S. M. (2002) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(02)00338-7 · Cited by 128 · see citing works
Oxygen-regulated isoforms of cytochrome c oxidase have differential effects on its nitric oxide production and on hypoxic signaling
Castello, P. R., Woo, D. K., Ball, K., Wojcik, J., Liu, L., & Poyton, R. O. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709461105 · Cited by 121 · see citing works
Reduced reactive O2 species formation and preserved mitochondrial NADH and [Ca2+] levels during short-term 17 °C ischemia in intact hearts
Riess, M. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.09.016 · Cited by 118 · see citing works
Does oxidative stress contribute to the pathology of Friedreich's ataxia? A radical question
Armstrong, J. S., Khdour, O., & Hecht, S. M. (2010) · The FASEB Journal · doi:10.1096/fj.09-143222 · Cited by 107 · see citing works
Induction of Mitochondrial Reactive Oxygen Species Production by Itraconazole, Terbinafine, and Amphotericin B as a Mode of Action against Aspergillus fumigatus
Shekhova, E., Kniemeyer, O., & Brakhage, A. A. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00978-17 · Cited by 105 · see citing works
The Hog1 MAP kinase controls respiratory metabolism in the fungal pathogen Candida albicans
Alonso-Monge, R., Carvaihlo, S., Nombela, C., Rial, E., & Pla, J. (2009) · Microbiology · doi:10.1099/mic.0.023309-0 · Cited by 105 · see citing works
Oxidative stress-a key emerging impact factor in health, ageing, lifestyle and aesthetics
Kandola, K., Bowman, A., & Birch‐Machin, M. A. (2015) · International Journal of Cosmetic Science · doi:10.1111/ics.12287 · Cited by 103 · see citing works
Reverse electron flow-induced ROS production is attenuated by activation of mitochondrial Ca2+-sensitive K+ channels
Heinen, A., Aldakkak, M., Stowe, D. F., Rhodes, S. S., Riess, M. L., Varadarajan, S. G., & Camara, A. K. S. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00198.2007 · Cited by 103 · see citing works
Reactive oxygen species are generated by the respiratory complex <scp>II</scp> – evidence for lack of contribution of the reverse electron flow in complex <scp>I</scp>
Moreno‐Sánchez, R., Hernández‐Esquivel, L., Rivero‐Segura, N. A., Marín‐Hernández, A., Neuzil, J., Ralph, S. J., & Rodríguez‐Enríquez, S. (2013) · The FEBS Journal · doi:10.1111/febs.12086 · Cited by 100 · see citing works
Coenzyme Q10 Depletion in Medical and Neuropsychiatric Disorders: Potential Repercussions and Therapeutic Implications
Morris, G., Anderson, G., Berk, M., & Maes, M. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8477-8 · Cited by 96 · see citing works
Controlled oxygen delivery to power tissue regeneration
Zoneff, E., Wang, Y., Jackson, C., Smith, O., Duchi, S., Onofrillo, C., Farrugia, B., Moulton, S. E., Williams, R., Parish, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-48719-x · Cited by 89 · see citing works
First evidence and characterization of an uncoupling protein in fungi kingdom: CpUCP of Candida parapsilosis
Jarmuszkiewicz, W., Milani, G., Fortes, F., Schreiber, A. Z., Sluse, F. E., & Vercesi, A. E. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01138-8 · Cited by 67 · see citing works
Succinate modulation of H2O2 release at NADH:ubiquinone oxidoreductase (complex I) in brain mitochondria
Zoccarato, F., Cavallini, L., Bortolami, S., & Alexandre, A. (2007) · Biochemical Journal · doi:10.1042/bj20070215 · Cited by 66 · see citing works
Self-citation
Reactive oxygen species in the pathogenesis of sarcopenia
Xu, H., Brown, J. L., Bhaskaran, S., & Van Remmen, H. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.11.046 · Cited by 61 · see citing works
Coenzyme Q10 Supplementation Reverses Age-Related Impairments in Spatial Learning and Lowers Protein Oxidation
Shetty, R. A., Forster, M. J., & Sumien, N. (2013) · AGE · doi:10.1007/s11357-012-9484-9 · Cited by 47 · see citing works
Prolonged Intake of Coenzyme Q10 Impairs Cognitive Functions in Mice
Sumien, N., Heinrich, K. R., Shetty, R. A., Sohal, R. S., & Forster, M. J. (2009) · The Journal of Nutrition · doi:10.3945/jn.109.110437 · Cited by 46 · see citing works
Calcium, mitochondria and oxygen sensing in the pulmonary circulation
Ward, J. P. T., Snetkov, V. A., & Aaronson, P. I. (2004) · Cell Calcium · doi:10.1016/j.ceca.2004.02.017 · Cited by 45 · see citing works
Astaxanthin Prevents Atrophy in Slow Muscle Fibers by Inhibiting Mitochondrial Reactive Oxygen Species via a Mitochondria-Mediated Apoptosis Pathway
Sun, L., Miyaji, N., Yang, M., Mills, E. M., Taniyama, S., Uchida, T., Nikawa, T., Li, J., Shi, J., Tachibana, K., et al. (2021) · Nutrients · doi:10.3390/nu13020379 · Cited by 45 · see citing works
An Adaptation to Low Copper in Candida albicans Involving SOD Enzymes and the Alternative Oxidase
Broxton, C. N., & Culotta, V. C. (2016) · PLOS ONE · doi:10.1371/journal.pone.0168400 · Cited by 41 · see citing works
Effect of oxygen on activation state of complex I and lack of oxaloacetate inhibition of complex II in Langendorff perfused rat heart
Maklashina, E., Kotlyar, A. B., Karliner, J. S., & Cecchini, G. (2004) · FEBS Letters · doi:10.1016/s0014-5793(03)01369-3 · Cited by 37 · see citing works
Long chain fatty acyl-CoA modulation of H2O2 release at mitochondrial complex I
Bortolami, S., Comelato, E., Zoccarato, F., Alexandre, A., & Cavallini, L. (2008) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-008-9126-1 · Cited by 13 · see citing works
Self-citation

Heme-copper terminal oxidase using both cytochrome c and ubiquinol as electron donors
Gao, Y., Meyer, B., Sokolová, L., Zwicker, K., Karas, M., Brutschy, B., Peng, G., & Michel, H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121040109 · Cited by 33 · see citing works
The Crystal Structure of Mitochondrial Cytochrome bc 1 Complex
Yu, C., Zhang, L., Kachurin, A. M., Shenoy, S. K., Deng, K.-P., Yu, L. P. C., Xia, D., Kim, H., & Deisenhofer, J. (1999) · Springer eBooks · doi:10.1007/978-1-4615-4843-0_12
Inhibition of the Yeast Cytochrome bc1 Complex by Ilicicolin H, a Novel Inhibitor That Acts at the Qn Site of the bc1 Complex
Gutiérrez-Cirlos, E. B., Merbitz-Zahradnik, T., & Trumpower, B. L. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311805200 · Cited by 63 · see citing works
Ascochlorin is a novel, specific inhibitor of the mitochondrial cytochrome bc1 complex
Berry, E. A., Huang, L.-S., Lee, D., Daldal, F., Nagai, K., & Minagawa, N. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.12.003 · Cited by 89 · see citing works
On the oxidation pathways of the mitochondrial bc1 complex from beef heart
Esposti, M. D., Tsai, A.-L., Palmer, G., et al. (1986) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1986.tb10073.x · Cited by 23 · see citing works

Authors: Turrens, J. F., Alexandre, A., & Lehninger, A. L.
Affiliations: University of Padua (IT)
Corresponding author: Lehninger, Albert L.
Venue: Archives of Biochemistry and Biophysics
Publisher: Elsevier BV
Published: 1985-03
Volume: 237
Issue: 2
Pages: 408-414
ISSN: 0003-9861 (ISSN-L)
DOI: 10.1016/0003-9861(85)90293-0
OpenAlex: W2060363769
Cited by: 1,214
References: 23
Citations by year: 2026: 8 · 2025: 12 · 2024: 15 · 2023: 10 · 2022: 22 · 2021: 33 · 2020: 27 · 2019: 18 · 2018: 26 · 2017: 22 · 2016: 31 · 2015: 40 · 2014: 45 · 2013: 37 · 2012: 50
FWCI: 2.88
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Archives of Biochemistry and Biophysics (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (CA 25360)
National Institute of General Medical Sciences (GM05919)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Coenzyme Q10 studies and effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Keywords: ubisemiquinone, superoxide production, mitochondrial complex III, heart mitochondria, antimycin A, hydrogen peroxide production, myxothiazol, cytochrome c, cytochrome b, ubiquinol, Q-cycle, electron transfer to oxygen, superoxide dismutase
MeSH terms: Animals, Antimycin A, Coenzymes, Cytochrome b Group, Cytochrome c Group, Electron Transport, Hydrogen Peroxide, Methacrylates, Mitochondria, Heart, Multienzyme Complexes, NADH, NADPH Oxidoreductases, Oxygen Consumption, Quinone Reductases, Succinates, Superoxides, Thiazoles, Electron Transport Complex III, Ubiquinone, 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

Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks