Species- and tissue-specific relationships between mitochondrial permeability transition and generation of ROS in brain and liver mitochondria of rats and mice
Abstract
In animal models of neurodegenerative diseases pathological changes vary with the type of organ and species of the animals. We studied differences in the mitochondrial permeability transition (mPT) and reactive oxygen species (ROS) generation in the liver (LM) and brain (BM) of Sprague-Dawley rats and C57Bl mice. In the presence of ADP mouse LM and rat LM required three times less Ca 2+ to initiate mPT than the corresponding BM. Mouse LM and BM sequestered 70% and 50% more Ca 2+ phosphate than the rat LM and BM. MBM generated 50% more ROS with glutamate than the RBM, but not with succinate. With the NAD substrates, generation of ROS do not depend on the energy state of the BM. Organization of the respiratory complexes into the respirasome is a possible mechanism to prevent ROS generation in the BM. With BM oxidizing succinate, 80% of ROS generation was energy dependent. Induction of mPT does not affect ROS generation with NAD substrates and inhibit with succinate as a substrate. The relative insensitivity of the liver to systemic insults is associated with its high regenerative capacity. Neuronal cells with low regenerative capacity and a long life span protect themselves by minimizing ROS generation and by the ability to withstand very large Ca 2+ insults. We suggest that additional factors, such as oxidative stress, are required to initiate neurodegeneration. Thus the observed differences in the Ca 2+-induced mPT and ROS generation may underlie both the organ-specific and species-specific variability in the animal models of neurodegenerative diseases.
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 can damage TCA-cycle enzymes, especially aconitase and α-ketoglutarate dehydrogenase.
“ROS can damage TCA-cycle enzymes, especially aconitase and α-ketoglutarate dehydrogenase (62, 168, 249, 250, 277).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [249]
Cites
Handbook of chemistry and physics
(1930) · Journal of the Franklin Institute · doi:10.1016/s0016-0032(30)91499-8 · Cited by 11,756 · see citing works
Green, D. R., & Reed, J. C. (1998) · Science · doi:10.1126/science.281.5381.1309 · Cited by 8,998 · 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
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
Chronic systemic pesticide exposure reproduces features of Parkinson's disease
Betarbet, R., Sherer, T., Mackenzie, G., Garcia-Osuna, M., Panov, A., & Greenamyre, J. (2000) · Nature Neuroscience · doi:10.1038/81834 · Cited by 3,797 · see citing works
Self-citationThe mitochondrial permeability transition pore and its role in cell death
CROMPTON, M. (1999) · Biochemical Journal · doi:10.1042/bj3410233 · Cited by 2,432 · see citing works
Shimizu, S., Narita, M., Tsujimoto, Y., & Tsujimoto, Y. (1999) · Nature · doi:10.1038/20959 · Cited by 2,178 · see citing works
THE MITOCHONDRIAL ELECTRON TRANSPORT AND OXIDATIVE PHOSPHORYLATION SYSTEM
Hatefi, Y. (1985) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.54.070185.005055 · Cited by 1,650 · see citing works
Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., & Tsujimoto, Y. (2005) · Nature · doi:10.1038/nature03317 · Cited by 1,635 · see citing works
Mitochondrial Transport of Cations: Channels, Exchangers, and Permeability Transition
Bernardi, P. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.4.1127 · Cited by 1,534 · see citing works
Lemasters, J. J., Nieminen, A.-L., Qian, T., Trost, L. C., Elmore, S. P., Nishimura, Y., Crowe, R. A., Cascio, W. E., Bradham, C. A., Brenner, D. A., et al. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00112-1 · Cited by 1,387 · see citing works
Supercomplexes in the respiratory chains of yeast and mammalian mitochondria
Schägger, H., & Pfeiffer, K. (2000) · The EMBO Journal · doi:10.1093/emboj/19.8.1777 · Cited by 1,356 · 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
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
Dave, K. A., & White, S. W. (2002) · World Highways/Routes du Monde · Cited by 767 · see citing works
Mitochondrial permeability transition: a common pathway to necrosis and apoptosis
Js, K., He, L., & Lemasters, J. J. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00618-1 · Cited by 756 · see citing works
Trounce, I. A., Kim, Y. L., Jun, A. S., & Wallace, D. C. (1996) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(96)64044-0 · Cited by 749 · see citing works
Mitochondrial α-Ketoglutarate Dehydrogenase Complex Generates Reactive Oxygen Species
Starkov, A. A., Fiskum, G. M., Chinopoulos, C., Lorenzo, B. J., Browne, S. E., Patel, M. S., & Beal, M. F. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1899-04.2004 · Cited by 692 · see citing works
Kushnareva, Y., Murphy, A. N., & Andreyev, A. Y. (2002) · Biochemical Journal · doi:10.1042/bj20021121 · Cited by 677 · see citing works
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
Replicating Huntington's disease phenotype in experimental animals
Brouillet, E. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00005-2 · Cited by 413 · see citing works
Chalmers, S., & Nicholls, D. G. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212661200 · Cited by 390 · see citing works
Sims, N. (1990) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1990.tb04189.x · Cited by 388 · see citing works
Beutner, G., Rück, A., Riede, B., & Brdiczka, D. G. (1998) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(97)00175-2 · Cited by 342 · see citing works
Antioxidant and prooxidant properties of mitochondrial Coenzyme Q
James, A. M., Smith, R. A. J., & Murphy, M. P. (2004) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2003.12.025 · Cited by 292 · see citing works
Rotenone Model of Parkinson Disease
Panov, A., Dikalov, S., Shalbuyeva, N., Taylor, G., Sherer, T., & Greenamyre, J. T. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508628200 · Cited by 288 · see citing works
Self-citationThe Mitochondrial Respiratory Chain Is Partially Organized in a Supercomplex Assembly
Bianchi, C., Genova, M. L., Castelli, G. P., & Lenaz, G. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405135200 · Cited by 277 · see citing works
Neuroenergetics: Calling Upon Astrocytes to Satisfy Hungry Neurons
Pellerin, L., & Magistretti, P. J. (2004) · The Neuroscientist · doi:10.1177/1073858403260159 · Cited by 268 · see citing works
Brustovetsky, N., Brustovetsky, T., Jemmerson, R., & Dubinsky, J. M. (2002) · Journal of Neurochemistry · doi:10.1046/j.0022-3042.2001.00671.x · Cited by 247 · 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
Fujii, M., Hara, H., Meng, W., Vonsattel, J. P., Huang, Z., & Moskowitz, M. A. (1997) · Stroke · doi:10.1161/01.str.28.9.1805 · Cited by 243 · see citing works
Halestrap, A. P. (2005) · Nature · doi:10.1038/434578a · Cited by 240 · see citing works
Genetically engineered mouse models of neurodegenerative diseases
Wong, P. C., Cai, H., Borchelt, D., & Price, D. L. (2002) · Nature Neuroscience · doi:10.1038/nn0702-633 · Cited by 232 · see citing works
Kristal, B. S., & Dubinsky, J. M. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.69020524.x · Cited by 229 · see citing works
[39] Preparation and properties of succinic—cytochrome c reductase (complex II–III)
Tisdale, H. D. (1967) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(67)10042-6 · Cited by 214 · see citing works
Respiratory Chain Supercomplexes
Schägger, H. (2001) · IUBMB Life · doi:10.1080/15216540152845911 · Cited by 201 · see citing works
Andreyev, A. Y., & Fiskum, G. M. (1999) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400565 · Cited by 188 · see citing works
On the Voltage Dependence of the Mitochondrial Permeability Transition Pore
Scorrano, L., Petronilli, V., & Bernardi, P. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.19.12295 · Cited by 178 · 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
Oxidative stress in Ca2+‐induced membrane permeability transition in brain mitochondria
Maciel, E. N., Vercesi, A. E., & Castilho, R. F. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00670.x · Cited by 162 · 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
Valle, V. G. R., Fagian, M. M., Parentoni, L. S., Meinicke, A. R., & Vercesi, A. E. (1993) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1993.1551 · Cited by 133 · see citing works
A Possible Site of Superoxide Generation in the Complex I Segment of Rat Heart Mitochondria
Ohnishi, S. T., Ohnishi, T., Muranaka, S., Fujita, H., Kimura, H., Uemura, K., Yoshida, K.-I., & Utsumi, K. (2005) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-005-4117-y · 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
Berman, S. B., Watkins, S. C., & Hastings, T. G. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7438 · Cited by 115 · see citing works
Brand, M. D. (1990) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80131-6 · Cited by 115 · see citing works
Oxidative stress in amyotrophic lateral sclerosis
Robberecht, W. (2000) · Journal of Neurology · doi:10.1007/s004150050551 · Cited by 112 · see citing works
Modeling mitochondrial function in aging neurons
Melov, S. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.08.004 · Cited by 111 · see citing works
Gostimskaya, I. S., Grivennikova, V. G., Zharova, T. V., Bakeeva, L. E., & Vinogradov, A. D. (2003) · Analytical Biochemistry · doi:10.1016/s0003-2697(02)00534-1 · Cited by 98 · see citing works
Panov, A. V., Lund, S. A., & Greenamyre, J. T. (2005) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-005-3454-9 · Cited by 92 · see citing works
Self-citationKobayashi, T., Kuroda, S., Tada, M., Houkin, K., Iwasaki, Y., & Abe, H. (2003) · Brain Research · doi:10.1016/s0006-8993(02)03767-8 · Cited by 83 · see citing works
Mg2+ Control of Respiration in Isolated Rat Liver Mitochondria
Panov, A. V., & Scarpa, A. (1996) · Biochemistry · doi:10.1021/bi960139f · Cited by 81 · see citing works
Self-citationStrategies for metabolic exchange between glial cells and neurons
Deitmer, J. W. (2001) · Respiration Physiology · doi:10.1016/s0034-5687(01)00283-3 · Cited by 68 · see citing works
Therapeutics against Mitochondrial Oxidative Stress in Animal Models of Aging
Melov, S. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02104.x · Cited by 68 · see citing works
Panov, A. V., Filippova, S., & Lyakhovich, V. V. (1980) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(80)90298-2 · Cited by 64 · see citing works
Self-citationWigdal, S. S., Kirkland, R. A., Franklin, J. L., & Haak‐Frendscho, M. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01049.x · Cited by 61 · see citing works
Panov, A. V., Andreeva, L. V., & Greenamyre, J. T. (2004) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2004.01.013 · Cited by 60 · see citing works
Self-citationPuranam, K. L., Wu, G., Strittmatter, W. J., & Burke, J. R. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.01.007 · Cited by 43 · see citing works
Protection Provided by Cyclosporin A against Excitotoxic Neuronal Death Is Genotype Dependent
Santos, J. B., & Schauwecker, P. E. (2003) · Epilepsia · doi:10.1046/j.1528-1157.2003.66302.x · Cited by 42 · see citing works
Lack of mitochondrial nitric oxide production in the mouse brain
Lacza, Z., Horn, T. F. W., Snipes, J. A., Zhang, J., Roychowdhury, S., Horvath, E. M., Figueroa, J. P., Kollai, M., Szabó, C., & Busija, D. W. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02553.x · Cited by 42 · see citing works
Oxygen radicals and hydrogen peroxide in rat brain mitochondria
Sorgato, M. C., & Sartorelli, L. (1974) · FEBS Letters · doi:10.1016/0014-5793(74)80818-5 · Cited by 39 · see citing works
An ADP‐sensitive cyclosporin‐A‐binding protein in rat liver mitochondria
Andreeva, L. V., & Crompton, M. (1994) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1994.tb18737.x · Cited by 37 · see citing works
Influence of Calcium on NADH and Succinate Oxidation by Rat Heart Submitochondrial Particles
Panov, A. V., & Scaduto, R. C. (1995) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1995.1109 · Cited by 34 · see citing works
Self-citationTurlejski, K., & Djavadian, R. L. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)36006-0 · Cited by 31 · see citing works
A protective function of superoxide dismutase during respiratory chain activity
Tyler, D. D. (1975) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(75)90140-1 · Cited by 30 · see citing works
Flagged first, then by citations
1 of the 66 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Oxidative stress caused by mitochondrial calcium overload
Peng, T., & Jou, M. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05634.x · Cited by 569 · 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
Fatty acids as modulators of the cellular production of reactive oxygen species
Schönfeld, P., & Wojtczak, L. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.04.029 · Cited by 441 · see citing works
Maranzana, E., Barbero, G., Falasca, A. I., Lenaz, G., & Genova, M. L. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4845 · Cited by 425 · see citing works
Mitochondrial association of alpha-synuclein causes oxidative stress
Parihar, M. S., Parihar, A., Fujita, M., Hashimoto, M., & Ghafourifar, P. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-7589-1 · Cited by 331 · see citing works
ROS and Brain Diseases: The Good, the Bad, and the Ugly
Popa-Wagner, A., Mitran, S., Sivanesan, S., Chang, E., & Buga, A.-M. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/963520 · Cited by 427 · see citing works
Functional role of mitochondrial respiratory supercomplexes
Genova, M. L., & Lenaz, G. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.11.002 · Cited by 306 · see citing works
Diabetes-Induced Reactive Oxygen Species: Mechanism of Their Generation and Role in Renal Injury
Fakhruddin, S., Alanazi, W. A., & Jackson, K. E. (2017) · Journal of Diabetes Research · doi:10.1155/2017/8379327 · Cited by 295 · see citing works
Lenaz, G., & Genova, M. L. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2704 · Cited by 261 · see citing works
Mitochondrial dysfunction in the limelight of Parkinson's disease pathogenesis
Banerjee, R., Starkov, A. A., Beal, M. F., & Thomas, B. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.11.007 · Cited by 256 · see citing works
Calcium and Mitochondrial Reactive Oxygen Species Generation: How to Read the Facts
Ádám‐Vizi, V., & Starkov, A. A. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-100465 · Cited by 250 · see citing works
Fatty Acids in Energy Metabolism of the Central Nervous System
Panov, A., Orynbayeva, Z., Vavilin, V., & Lyakhovich, V. (2014) · BioMed Research International · doi:10.1155/2014/472459 · Cited by 227 · see citing works
Self-citationPhenotypic characterization of recessive gene knockout rat models of Parkinson's disease
Dave, K. D., Silva, S., Sheth, N. P., Ramboz, S., Beck, M. J., Quang, C., Switzer, R. C., Ahmad, S. O., Sunkin, S. M., Walker, D., et al. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.06.009 · Cited by 222 · see citing works
Mitochondrial calcium function and dysfunction in the central nervous system
Nicholls, D. G. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.03.010 · Cited by 213 · see citing works
Mitochondria and Reactive Oxygen Species. Which Role in Physiology and Pathology?
Lenaz, G. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-2869-1_5 · Cited by 214 · see citing works
The Role of Thyroid Hormones as Inductors of Oxidative Stress and Neurodegeneration
Villanueva, I., Alva-Sánchez, C., & Pacheco-Rosado, J. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/218145 · Cited by 204 · see citing works
Role of mitochondrial oxidative stress in hypertension
Dikalov, S., & Ungvari, Z. I. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00089.2013 · Cited by 202 · see citing works
Self-citationMeyer, J. N., Hartman, J. H., & Mello, D. F. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy008 · Cited by 172 · see citing works
Rahman, M. H., Bajgai, J., Fadriquela, A., Sharma, S., Trinh, T. T., Akter, R., Jeong, Y. J., Goh, S. H., Kim, C.-S., & Lee, K.-J. (2021) · Molecules · doi:10.3390/molecules26175327 · Cited by 182 · see citing works
Mouse models of atherosclerosis: a historical perspective and recent advances
Lee, Y. T., Lin, H. Y., Chan, Y. W. F., Li, K. H. C., To, O. T. L., Yan, B. P., Liu, T., Li, G., Wong, W. T., Keung, W., et al. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-016-0402-5 · Cited by 168 · see citing works
Functional asymmetry and electron flow in the bovine respirasome
Sousa, J. S., Mills, D. J., Vonck, J., & Kühlbrandt, W. (2016) · eLife · doi:10.7554/elife.21290 · Cited by 162 · see citing works
Tse, G., Yan, B. P., Chan, Y. W. F., Tian, X. Y., & Huang, Y. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00313 · Cited by 160 · see citing works
Khalifa, A. R. M., Abdel‐Rahman, E. A., Mahmoud, A. M., Ali, M. H., Noureldin, M., Saber, S. H., Mohsen, M., & Ali, S. S. (2017) · Physiological Reports · doi:10.14814/phy2.13125 · Cited by 154 · see citing works
Hansson, M. J., Månsson, R., Morota, S., Uchino, H., Kallur, T., Sumi, T., Ishii, N., Shimazu, M., Keep, M. F., Jegorov, A., et al. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.04.021 · Cited by 130 · see citing works
Gaignard, P., Lière, P., Thérond, P., Schumacher, M., Slama, A., & Guennoun, R. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00406 · Cited by 127 · see citing works
Mitochondrial Dysfunction—A Pharmacological Target in Alzheimer's Disease
Eckert, G. P., Renner, K., Eckert, S. H., Eckmann, J., Hagl, S., Abdel-Kader, R. M., Kurz, C., Leuner, K., & Muller, W. E. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8271-z · Cited by 126 · see citing works
The Interplay Between Respiratory Supercomplexes and ROS in Aging
Genova, M. L., & Lenaz, G. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6214 · Cited by 126 · see citing works
Martin, L. J., Semenkow, S., Hanaford, A. R., & Wong, M. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.11.008 · Cited by 123 · see citing works
Bojar, M. (2009) · Cited by 120 · see citing works
Mitochondrial respiratory chain super-complex I–III in physiology and pathology
Lenaz, G., Baracca, A., Barbero, G., Bergamini, C., Dalmonte, M. E., Sole, M. D., Faccioli, M., Falasca, A. I., Fato, R., Genova, M. L., et al. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.01.025 · Cited by 120 · see citing works
Lenaz, G., & Genova, M. L. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3573-0_5 · Cited by 114 · see citing works
Complex I function in mitochondrial supercomplexes
Lenaz, G., Tioli, G., Falasca, A. I., & Genova, M. L. (2016) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2016.01.013 · Cited by 109 · see citing works
Mitophagy and reactive oxygen species interplay in Parkinson’s disease
Xiao, B., Kuruvilla, J., & Tan, E. (2022) · npj Parkinson s Disease · doi:10.1038/s41531-022-00402-y · Cited by 112 · see citing works
Mariappan, N., Elks, C. M., Fink, B., & Francis, J. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.10.049 · Cited by 103 · see citing works
Miwa, S., Treumann, A., Bell, A., Vistoli, G., Nelson, G., Hay, S., & von Zglinicki, T. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.11.011 · Cited by 104 · see citing works
Cardiolipin, Perhydroxyl Radicals, and Lipid Peroxidation in Mitochondrial Dysfunctions and Aging
Panov, A. V., & Dikalov, S. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/1323028 · Cited by 100 · see citing works
Self-citationSchönfeld, P., Wieckowski, M. R., Lebiedzińska, M., & Wojtczak, L. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.01.010 · Cited by 100 · see citing works
Nox2 as a potential target of mitochondrial superoxide and its role in endothelial oxidative stress
Nazarewicz, R. R., Dikalova, A., Bikineyeva, A. T., & Dikalov, S. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00063.2013 · Cited by 98 · see citing works
Self-citationCalcium Signaling in Brain Mitochondria
Contreras, L., & Satrústegui, J. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808066200 · Cited by 98 · see citing works
Gómez, L. A., & Hagen, T. M. (2012) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2012.04.002 · Cited by 91 · see citing works
Oxidative stress: A target to treat Alzheimer's disease and stroke
Briyal, S., Ranjan, A. K., & Gulati, A. (2023) · Neurochemistry International · doi:10.1016/j.neuint.2023.105509 · Cited by 86 · see citing works
Nesci, S., Trombetti, F., Pagliarani, A., Ventrella, V., Algieri, C., Tioli, G., & Lenaz, G. (2021) · Life · doi:10.3390/life11030242 · Cited by 80 · see citing works
Mouzaoui, S., Rahim, I., & Djerdjouri, B. (2011) · International Immunopharmacology · doi:10.1016/j.intimp.2011.10.010 · Cited by 81 · see citing works
Kim, J., Wang, J., & Lemasters, J. J. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00082.2011 · Cited by 80 · see citing works
Coenzyme Q and the Respiratory Chain: Coenzyme Q Pool and Mitochondrial Supercomplexes
Enrı́quez, J. A., & Lenaz, G. (2014) · Molecular Syndromology · doi:10.1159/000363364 · Cited by 80 · see citing works
Dikalov, S., Li, W., Doughan, A. K., Blanco, R. R., & Zafari, A. M. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00842.2010 · Cited by 73 · see citing works
Self-citationHill, R. L., Kulbe, J. R., Singh, I. N., Wang, J. A., & Hall, E. D. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.06.028 · Cited by 73 · see citing works
Dubinin, M. V., Talanov, E. Y., Tenkov, K. S., Starinets, V. S., Mikheeva, I. B., Sharapov, M. G., & Belosludtsev, K. N. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165674 · Cited by 71 · see citing works
Koju, N., Taleb, A., Zhou, J., Ge, L., Yang, J., Cao, X., Lei, H., & Ding, Q. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.11.128 · Cited by 71 · see citing works
Kesäniemi, J., Lavrinienko, A., Tukalenko, E., Boratyński, Z., Kivisaari, K., Mappes, T., Milinevsky, G. P., Møller, A. P., Mousseau, T. A., & Watts, P. C. (2019) · Scientific Reports · doi:10.1038/s41598-018-37164-8 · Cited by 63 · see citing works
Mitochondrial Permeability Transition: A Pore Intertwines Brain Aging and Alzheimer’s Disease
Jia, K., & Du, H. (2021) · Cells · doi:10.3390/cells10030649 · Cited by 61 · see citing works
Panov, A. V., Schönfeld, P., Dikalov, S., Hemendinger, R. A., Bonkovsky, H. L., & Brooks, B. R. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m900985200 · Cited by 62 · see citing works
Self-citationRole of Fatty Acids β-Oxidation in the Metabolic Interactions Between Organs
Panov, A. V., Mayorov, V., & Dikalov, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252312740 · Cited by 63 · see citing works
Self-citationCardioprotection leads to novel changes in the mitochondrial proteome
Wong, R., Aponte, A. M., Steenbergen, C., & Murphy, E. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00515.2009 · Cited by 60 · see citing works
Panov, A. V., & Orynbayeva, Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072078 · Cited by 58 · see citing works
Self-citationAzarashvili, T., Stricker, R., & Reiser, G. (2010) · Biological Chemistry · doi:10.1515/bc.2010.070 · Cited by 57 · see citing works
Rodriguez, K. A., Wywiał, E., Pérez, V., Lambert, A. J., Edrey, Y. H., Lewis, K. N., Grimes, K. M., Lindsey, M. L., Brand, M. D., & Buffenstein, R. (2011) · Current Pharmaceutical Design · doi:10.2174/138161211797052457 · Cited by 57 · see citing works
Büttiker, P., Weissenberger, S., Esch, T., Anders, M., Raboch, J., Ptáček, R., Kream, R. M., & Stefano, G. B. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1095923 · Cited by 64 · see citing works
mt-Nd2 Suppresses Reactive Oxygen Species Production by Mitochondrial Complexes I and III
Gusdon, A. M., Votyakova, T. V., & Mathews, C. E. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m708801200 · Cited by 56 · see citing works
Gangolf, M., Wins, P., Thiry, M., Moualij, B. E., & Bettendorff, L. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.054379 · Cited by 54 · see citing works
Neonatal cardiac mitochondria and ischemia/reperfusion injury
Milerová, M., Charvátová, Z., Skarka, L., Ostadalova, I., Drahota, Z., Fialová, M., & Ostadal, B. (2009) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-009-0251-x · Cited by 50 · see citing works
Attenuating effects of coenzyme Q10 and amlodipine in ulcerative colitis model in rats
Morsy, E. M. E., Kamel, R., & Ahmed, M. A. E. (2015) · Immunopharmacology and Immunotoxicology · doi:10.3109/08923973.2015.1021357 · Cited by 49 · see citing works
Panov, A. V., Kubalik, N., Zinchenko, N., Ridings, D. M., Radoff, D. A., Hemendinger, R. A., Brooks, B. R., & Bonkovsky, H. L. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00528.2010 · Cited by 47 · see citing works
Self-citationPanov, A. V., Mayorov, V., & Dikalov, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23074047 · Cited by 44 · see citing works
Self-citationKadenbach, B., Ramzan, R., & Vogt, S. K. (2012) · Mitochondrion · doi:10.1016/j.mito.2012.11.005 · Cited by 41 · see citing works
Dani, D. N., Shimokawa, I., Komatsu, T., Higami, Y., Warnken, U. H., Schokraie, E., Schnölzer, M., Krause, F., Sugawa, M. D., & Dencher, N. A. (2009) · Biogerontology · doi:10.1007/s10522-009-9254-y · Cited by 39 · see citing works
Impaired mitochondrial homeostasis and neurodegeneration: towards new therapeutic targets?
Corona, J. C., & Duchen, M. R. (2014) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-014-9576-6 · Cited by 38 · see citing works
Respiratory supercomplexes and the functional segmentation of the CoQ pool
Moreno‐Loshuertos, R., & Enrı́quez, J. A. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.04.018 · Cited by 38 · see citing works
Panov, A. V., Kubalik, N., Zinchenko, N., Hemendinger, R. A., Dikalov, S., & Bonkovsky, H. L. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.06.003 · Cited by 36 · see citing works
Self-citationJat, D., Parihar, P., Kothari, S., & Parihar, M. S. (2013) · PubMed · Cited by 37 · see citing works
Yarana, C., Sanit, J., Chattipakorn, N., & Chattipakorn, S. C. (2012) · Life Sciences · doi:10.1016/j.lfs.2012.04.004 · Cited by 37 · see citing works
Dikalova, A., Mayorov, V., Xiao, L., Panov, A. V., Amarnath, V., Zagol-Ikapitte, I. A., Vergeade, A., Ao, M., Yermalitsky, V. N., Nazarewicz, R. R., et al. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.15236 · Cited by 36 · see citing works
Self-citationKomary, Z., Tretter, L., & Ádám‐Vizi, V. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.03.010 · Cited by 35 · see citing works
Dóczi, J., Turiák, L., Vajda, S., Mándi, M., Törőcsik, B., Gerencser, A. A., Kiss, G., Konràd, C., Ádám‐Vizi, V., & Chinopoulos, C. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.196600 · Cited by 33 · see citing works
Long-Chain and Medium-Chain Fatty Acids in Energy Metabolism of Murine Kidney Mitochondria
Panov, A. V., Mayorov, V., Dikalova, A., & Dikalov, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms24010379 · Cited by 35 · see citing works
Self-citationDubinin, M. V., Talanov, E. Y., Tenkov, K. S., Starinets, V. S., Belosludtseva, N. V., & Belosludtsev, K. N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228763 · Cited by 31 · see citing works
Mitochondria-Mediated Anticancer Effects of Non-Thermal Atmospheric Plasma
Zhunussova, A., Vitol, E. A., Polyak, B., Tuleukhanov, S. T., Brooks, A. D., Sensenig, R., Friedman, G., & Orynbayeva, Z. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156818 · Cited by 30 · see citing works
Effect of Bovine Serum Albumin on Mitochondrial Respiration in the Brain and Liver of Mice and Rats
Panov, A. V., Андреевич, В. В., Lyakhovich, V. V., Brooks, B., & Bonkovsky, H. L. (2010) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-010-0904-5 · Cited by 28 · see citing works
Self-citationPanov, A. V., & Orynbayeva, Z. (2017) · Analytical Biochemistry · doi:10.1016/j.ab.2017.10.010 · Cited by 27 · see citing works
Self-citationFörster, D., & Reiser, G. (2015) · Purinergic Signalling · doi:10.1007/s11302-015-9471-6 · Cited by 27 · see citing works
Gusdon, A. M., Fernandez‐Bueno, G. A., Wohlgemuth, S. E., Fernandez, J., Chen, J., & Mathews, C. E. (2015) · BMC Biochemistry · doi:10.1186/s12858-015-0051-8 · Cited by 27 · see citing works
Panov, A. V., Kubalik, N., Brooks, B., & Shaw, C. A. (2010) · The Journal of Membrane Biology · doi:10.1007/s00232-010-9307-9 · Cited by 27 · see citing works
Self-citationTargeting of reactive isolevuglandins in mitochondrial dysfunction and inflammation
Mayorov, V., Uchakin, P., Amarnath, V., Panov, A. V., Bridges, C. C., Uzhachenko, R. V., Zackert, B., Moore, C. S., Davies, S. S., Dikalova, A., et al. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101300 · Cited by 25 · see citing works
Self-citationCalcium overload decreases net free radical emission in cardiac mitochondria
Duong, Q. V., Hoffman, A., Zhong, K., Dessinger, M. J., Zhang, Y., & Bazil, J. N. (2020) · Mitochondrion · doi:10.1016/j.mito.2020.01.005 · Cited by 25 · see citing works
What to do with low O2: Redox adaptations in vertebrates native to hypoxic environments
Eaton, L., & Pamenter, M. E. (2022) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2022.111259 · Cited by 23 · see citing works
Bioenergetics of the aging heart and skeletal muscles: Modern concepts and controversies
Tepp, K., Timohhina, N., Puurand, M., Klepinin, A., Chekulayev, V., Shevchuk, I., & Kaambre, T. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.04.001 · Cited by 21 · see citing works
Tissue Specific Sensitivity of Mitochondrial Permeability Transition Pore to Ca2+ Ions
Endlicher, R., Staňková, P., Lotková, H., Milerová, M., Drahota, Z., & Červinková, Z. (2009) · Acta Medica (Hradec Kralove Czech Republic) · doi:10.14712/18059694.2016.107 · Cited by 21 · see citing works
Marroquin, L. D., Swiss, R. L., & Will, Y. (2014) · Current Protocols in Toxicology · doi:10.1002/0471140856.tx2504s60 · Cited by 19 · see citing works
Mitochondrial proteomics as a selective tool for unraveling Parkinson’s disease pathogenesis
Pienaar, I. S., Dexter, D. T., & Burkhard, P. R. (2010) · Expert Review of Proteomics · doi:10.1586/epr.10.8 · Cited by 19 · see citing works
Marcu, R., Neeley, C. K., Karamanlidis, G., & Hawkins, B. J. (2012) · Journal of Visualized Experiments · doi:10.3791/4131 · Cited by 18 · see citing works
Ramírez-Camacho, I., Correa, F., Hafidi, M. E., Silva‐Palacios, A., Ostolga-Chavarría, M., Esparza-Perusquía, M., Olvera-Sánchez, S., Flores-Herrera, Ó., & Zazueta, C. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.09.047 · Cited by 19 · see citing works
Drahota, Z., Endlicher, R., Staňková, P., Rychtrmoc, D., Milerová, M., & Červinková, Z. (2012) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-012-9443-2 · Cited by 18 · see citing works
The Structure of the Cardiac Mitochondria Respirasome Is Adapted for the β-Oxidation of Fatty Acids
Panov, A. V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042410 · Cited by 17 · see citing works
Self-citationHill, R. L., Singh, I. N., Wang, J. A., & Hall, E. D. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2018.5946 · Cited by 17 · see citing works
Drahota, Z., Milerová, M., Endlicher, R., Rychtrmoc, D., Červinková, Z., & Ošťádal, B. (2012) · Physiological Research · doi:10.33549/physiolres.932377 · Cited by 17 · see citing works
Dikalov, S., Mayorov, V., & Panov, A. V. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00907 · Cited by 17 · see citing works
Self-citationStefano, G. B., & Kream, R. M. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2471 · Cited by 15 · see citing works
Enhanced ROS Production in Mitochondria from Prematurely Aging mtDNA Mutator Mice
Shabalina, I. G., Edgar, D., Gibanova, N. V., Kalinovich, A., Petrovič, N., Vyssokikh, M. Y., Cannon, B., & Nedergaard, J. (2024) · Biochemistry (Moscow) · doi:10.1134/s0006297924020081 · Cited by 12 · see citing works
Gavaldà‐Navarro, A., Mampel, T., & Viñas, O. (2016) · Open Biology · doi:10.1098/rsob.150108 · Cited by 12 · see citing works
Lee, S.-B., Kim, J.-H., Cho, M., Choe, E.-S., Kim, K.-S., & Shim, S. (2017) · Journal of Toxicology and Environmental Health · doi:10.1080/15287394.2017.1355863 · Cited by 12 · see citing works
- Authors
- Panov, A., Dikalov, S., Shalbuyeva, N., Hemendinger, R., Greenamyre, J. T., & Rosenfeld, J.
- Affiliations
- Carolinas Medical Center (US)
- Venue
- American Journal of Physiology-Cell Physiology
- Publisher
- American Physiological Society
- Published
- 2007-02
- Volume
- 292
- Issue
- 2
- Pages
- C708-C718
- ISSN
- 0363-6143 (ISSN-L)
- 1522-1563
- OpenAlex
- W2116830452
- Cited by
- 141
- References
- 66
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 8 · 2023: 6 · 2022: 5 · 2021: 6 · 2020: 6 · 2019: 3 · 2018: 6 · 2017: 10 · 2016: 11 · 2015: 8 · 2014: 6 · 2013: 9 · 2012: 12
- FWCI
- 2.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Cell Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (12068)
- 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 › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- mitochondrial permeability transition, reactive oxygen species, brain mitochondria, liver mitochondria, species differences, neurodegenerative disease models, glutamate, succinic acid, respirasome, oxidative stress, mitochondrial calcium sequestration
- MeSH terms
- Animals, Brain, Calcium, Hydrogen, Male, Mice, Inbred C57BL, Mitochondria, Mitochondria, Liver, Organ Specificity, Permeability, Phosphates, Species Specificity, Rats, Sprague-Dawley, Reactive Oxygen Species, Mitochondrial Membranes, Mice, Rats, Membrane Potential, Mitochondrial
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
