Cited by 678Cardiac Ischemia and ReperfusionMitochondrial Function and PathologyCell death mechanisms and regulation

The DOI matches its Crossref record; 46 of the 46 references it cites were found in a registry or an index.

Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart

Open access

Di Lisa, Fabio, Menabò, Roberta, Canton, Marcella, Barile, Maria, Bernardi, Paolo·2001·Journal of Biological Chemistry

Open this paper in CoChat — free account Open PDF

Abstract

The opening of the mitochondrial permeability transition pore (PTP) has been suggested to play a key role in various forms of cell death, but direct evidence in intact tissues is still lacking. We found that in the rat heart, 92% of NAD(+) glycohydrolase activity is associated with mitochondria. This activity was not modified by the addition of Triton X-100, although it was abolished by mild treatment with the protease Nagarse, a condition that did not affect the energy-linked properties of mitochondria. The addition of Ca(2+) to isolated rat heart mitochondria resulted in a profound decrease in their NAD(+) content, which followed mitochondrial swelling. Cyclosporin A(CsA), a PTP inhibitor, completely prevented NAD(+) depletion but had no effect on the glycohydrolase activity. Thus, in isolated mitochondria PTP opening makes NAD(+) available for its enzymatic hydrolysis. Perfused rat hearts subjected to global ischemia for 30 min displayed a 30% decrease in tissue NAD(+) content, which was not modified by extending the duration of ischemia. Reperfusion resulted in a more severe reduction of both total and mitochondrial contents of NAD(+), which could be measured in the coronary effluent together with lactate dehydrogenase. The addition of 0.2 microm CsA or of its analogue MeVal-4-Cs (which does not inhibit calcineurin) maintained higher NAD(+) contents, especially in mitochondria, and significantly protected the heart from reperfusion damage, as shown by the reduction in lactate dehydrogenase release. Thus, upon reperfusion after prolonged ischemia, PTP opening in the heart can be documented as a CsA-sensitive release of NAD(+), which is then partly degraded by glycohydrolase and partly released when sarcolemmal integrity is compromised. These results demonstrate that PTP opening is a causative event in reperfusion damage of the heart.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1074/jbc.m006825200

Cites

46 of 46 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Methods of Enzymatic Analysis
(1975) · Journal of AOAC INTERNATIONAL · doi:10.1093/jaoac/58.5.1085 · Cited by 20,078
Methods of Enzymatic Analysis
(1974) · Elsevier eBooks · doi:10.1016/b978-0-12-091304-6.x5001-0 · Cited by 6,786
Methods of enzymatic analysis
(1985) · International Journal of Biochemistry · doi:10.1016/0020-711x(85)90098-9 · Cited by 3,494
Mitochondrial Transport of Cations: Channels, Exchangers, and Permeability Transition
Bernardi, P. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.4.1127 · Cited by 1,546
Self-citation
Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion
Griffiths, E. J., & Halestrap, A. P. (1995) · Biochemical Journal · doi:10.1042/bj3070093 · Cited by 838
Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle
Palmer, J. W., Tandler, B., & Hoppel, C. L. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)75283-1 · Cited by 830
Transient and Long-Lasting Openings of the Mitochondrial Permeability Transition Pore Can Be Monitored Directly in Intact Cells by Changes in Mitochondrial Calcein Fluorescence
Petronilli, V., Miotto, G., Canton, M., Brini, M., Colonna, R., Bernardi, P., & Lisa, F. D. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)77239-5 · Cited by 677
Self-citation
Myocardial calcium and magnesium in acute ischemic injury.
Shen, A. C., & Jennings, R. B. (1972) · PubMed · Cited by 629
Protection by Cyclosporin A of Ischemia/Reperfusion-Induced Damage in Isolated Rat Hearts
Griffiths, E. J., & Halestrap, A. P. (1993) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1993.1162 · Cited by 587
Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane
Bernardi, P., Broekemeier, K. M., & Pfeiffer, D. R. (1994) · Journal of Bioenergetics and Biomembranes · doi:10.1007/bf00762735 · Cited by 561
Self-citation

Flagged first, then by citations

Show all 46 references

Research works printed but not linked: 6

Ganote, 1976, Am. J. Pathol., 84, 327
Jennings, 1990, Circulation, 82, 2
Di Lisa, 1994, Am. J. Physiol., 267, H455
Di Lisa, 1993, Am. J. Physiol., 264, H2188
Barile, 1996, Biochem. Mol. Biol. Int., 38, 297
Shen, 1972, Am. J. Pathol., 67, 417

Sorted by citations

Items 101–200 of 678

Redox active calcium ion channels and cell death
Waring, P. (2004) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2004.08.001 · Cited by 187
Isoflurane Postconditioning Prevents Opening of the Mitochondrial Permeability Transition Pore through Inhibition of Glycogen Synthase Kinase 3β
Feng, J., Lucchinetti, E., Ahuja, P., Pasch, T., Perriard, J., & Zaugg, M. (2005) · Anesthesiology · doi:10.1097/00000542-200511000-00013 · Cited by 188
Mitochondrial dysfunction in the pathogenesis of Ullrich congenital muscular dystrophy and prospective therapy with cyclosporins
Angelin, A., Tiepolo, T., Sabatelli, P., Grumati, P., Bergamin, N., Golfieri, C., Mattioli, E., Gualandi, F., Ferlini, A., Merlini, L., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610270104 · Cited by 189
Self-citation
Mechanistic Insights Into Diabetes Mellitus and Oxidative Stress
Maiese, K., Chong, Z. Z., & Shang, Y. C. (2007) · Current Medicinal Chemistry · doi:10.2174/092986707781058968 · Cited by 186
Mitochondrial Pathways, Permeability Transition Pore, and Redox Signaling in Cardioprotection: Therapeutic Implications
Penna, C. R. R., Perrelli, M.-G., & Pagliaro, P. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4459 · Cited by 182
Augmented O-GlcNAc signaling attenuates oxidative stress and calcium overload in cardiomyocytes
Ngoh, G. A., Watson, L. J., Facundo, H. T., & Jones, S. P. (2010) · Amino Acids · doi:10.1007/s00726-010-0728-7 · Cited by 180
Physiological Roles of the Permeability Transition Pore
Brenner, C., & Moulin, M. (2012) · Circulation Research · doi:10.1161/circresaha.112.265942 · Cited by 186
Metabolic stages, mitochondria and calcium in hypoxic/ischemic brain damage
Kristián, T. (2004) · Cell Calcium · doi:10.1016/j.ceca.2004.02.016 · Cited by 177
ROS-dependent signalling pathways in plants and algae exposed to high light: Comparisons with other eukaryotes
Mullineaux, P. M., Exposito-Rodriguez, M., Laissue, P. P., & Smirnoff, N. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.01.033 · Cited by 172
Mitochondria and cardioprotection
Lisa, F. D., Canton, M., Menabò, R., Kaludercic, N., & Bernardi, P. (2007) · Heart Failure Reviews · doi:10.1007/s10741-007-9028-z · Cited by 177
Self-citation
The Wnt signaling pathway: Aging gracefully as a protectionist?
Maiese, K., Li, F., Chong, Z. Z., & Shang, Y. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.01.004 · Cited by 171
Melatonin protects against heart ischemia-reperfusion injury by inhibiting mitochondrial permeability transition pore opening
Petrosillo, G., Colantuono, G., Moro, N., Ruggiero, F. M., Tiravanti, E., Venosa, N. D., Fiore, T., & Paradies, G. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00163.2009 · Cited by 168
Cyclic GMP and protein kinase‐G in myocardial ischaemia‐reperfusion: opportunities and obstacles for survival signaling
Burley, D. S., Ferdinandy, P., & Baxter, G. F. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707409 · Cited by 165
The molecular composition of the mitochondrial permeability transition pore
Baines, C. P. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2009.02.007 · Cited by 169
Pathophysiological relevance of mitochondria in NAD+ metabolism
Lisa, F. D., & Ziegler, M. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02198-6 · Cited by 161
Mitochondrial permeability transition pore as a target for cardioprotection in the human heart
Shanmuganathan, S., Hausenloy, D. J., Duchen, M. R., & Yellon, D. M. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01192.2004 · Cited by 161
Interaction of Cardiovascular Nonmodifiable Risk Factors, Comorbidities and Comedications With Ischemia/Reperfusion Injury and Cardioprotection by Pharmacological Treatments and Ischemic Conditioning
Ferdinandy, P., Andreadou, I., Baxter, G. F., Bøtker, H. E., Davidson, S. M., Dobrev, D., Gersh, B. J., Heusch, G., Lecour, S., Ruiz‐Meana, M., et al. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000348 · Cited by 170
Mitochondrial permeability transition pore: Sensitivity to opening and mechanistic dependence on substrate availability
Briston, T., Roberts, M., Lewis, S., Powney, B., M. Staddon, J., Szabadkai, G., & Duchen, M. R. (2017) · Scientific Reports · doi:10.1038/s41598-017-10673-8 · Cited by 152
The Cardiac Mitochondrion: Nexus of Stress
Baines, C. P. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135929 · Cited by 154
The mitochondrial permeability transition pore: an evolving concept critical for cell life and death
Morciano, G., Naumova, N., Koprowski, P., Valente, S. A., Sardão, V. A., Potes, Y., Rimessi, A., Wieckowski, M. R., & Oliveira, P. J. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12764 · Cited by 161
The cardioprotective effects elicited by p66Shc ablation demonstrate the crucial role of mitochondrial ROS formation in ischemia/reperfusion injury
Carpi, A., Menabò, R., Kaludercic, N., Pelicci, P. G., Lisa, F. D., & Giorgio, M. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.04.001 · Cited by 152
Self-citation
PARP-1--a Perpetrator of Apoptotic Cell Death?
Chiarugi, A., & Moskowitz, M. A. (2002) · Science · doi:10.1126/science.1074592 · Cited by 153
Mitochondria as ATP consumers in cellular pathology
Chinopoulos, C., & Ádám‐Vizi, V. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2009.08.008 · Cited by 147
Mitoenergetic failure in Alzheimer disease
Parihar, M. S., & Brewer, G. J. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00232.2006 · Cited by 153
Epsilon protein kinase C as a potential therapeutic target for the ischemic heart
Inagaki, K., Churchill, E. N., & Mochly‐Rosen, D. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.02.015 · Cited by 150
Mitochondrial Approaches to Protect Against Cardiac Ischemia and Reperfusion Injury
Camara, A. K. S., Bienengraeber, M., & Stowe, D. F. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00013 · Cited by 155
Stress in the brain: novel cellular mechanisms of injury linked to Alzheimer's disease
Chong, Z. Z., Li, F., & Maiese, K. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.11.005 · Cited by 152
Nuclear Poly(ADP-ribose) Polymerase-1 Rapidly Triggers Mitochondrial Dysfunction
Cipriani, G., Rapizzi, E., Vannacci, A., Rizzuto, R., Moroni, F., & Chiarugi, A. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m414526200 · Cited by 148
Remote ischaemic pre‐ and delayed postconditioning – similar degree of cardioprotection but distinct mechanisms
Васильевна, Б. М., Barsukevich, V. C., Mastitskaya, S., Mrochek, A., Pernow, J., Sjöquist, P.-O. B., Ackland, G. L., Gourine, A. V., & Gourine, A. V. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2012.064923 · Cited by 147
SOD1 and MitoTEMPO partially prevent mitochondrial permeability transition pore opening, necrosis, and mitochondrial apoptosis after ATP depletion recovery
Liang, H., Sedlić, F., Bosnjak, Z. J., & Nilakantan, V. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.08.018 · Cited by 146
Iron Overload via Heme Degradation in the Endoplasmic Reticulum Triggers Ferroptosis in Myocardial Ischemia-Reperfusion Injury
Miyamoto, H. D., Ikeda, M., Ide, T., Tadokoro, T., Furusawa, S., Abe, K., Ishimaru, K., Enzan, N., Sada, M., Yamamoto, T., et al. (2022) · JACC Basic to Translational Science · doi:10.1016/j.jacbts.2022.03.012 · Cited by 143
Cyclosporin A and cardioprotection: from investigative tool to therapeutic agent
Hausenloy, D. J., Boston‐Griffiths, E., & Yellon, D. M. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01700.x · Cited by 143
Mitochondrial function and myocardial aging. A critical analysis of the role of permeability transition
DILISA, F., & BERNARDI, P. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2005.02.009 · Cited by 139
Self-citation
Mitochondria in apoptosis of ischemic heart
Borutaitė, V., & Brown, G. C. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00278-3 · Cited by 142
Mitochondrial permeability transition pore and postconditioning
Gateau-Roesch, O., Argaud, L., & Ovize, M. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.02.024 · Cited by 139
A CaPful of mechanisms regulating the mitochondrial permeability transition
Lisa, F. D., & Bernardi, P. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2009.03.006 · Cited by 143
Self-citation
The effects of idebenone on mitochondrial bioenergetics
Giorgio, V., Petronilli, V., Ghelli, A. M., Carelli, V., Rugolo, M., Lenaz, G., & Bernardi, P. (2011) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2011.10.012 · Cited by 136
Self-citation
Structural characterization of a human cytosolic NMN/NaMN adenylyltransferase and implication in human NAD biosynthesis
Zhang, X., Kurnasov, O. V., Karthikeyan, S., Grishin, N. V., Osterman, A. L., & Zhang, H. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300073200 · Cited by 136
Regulation of and challenges in targeting NAD+ metabolism
Migaud, M. E., Ziegler, M., & Baur, J. A. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00752-w · Cited by 142
Cyclosporin A-insensitive Permeability Transition in Brain Mitochondria
Chinopoulos, C., Starkov, A. A., & Fiskum, G. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303808200 · Cited by 131
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
Noble Gases Without Anesthetic Properties Protect Myocardium Against Infarction by Activating Prosurvival Signaling Kinases and Inhibiting Mitochondrial Permeability Transition In Vivo
Pagel, P. S., Krolikowski, J. G., Shim, Y. H., Venkatapuram, S., Kersten, J. R., Weihrauch, D., Warltier, D. C., & Pratt, P. F. (2007) · Anesthesia & Analgesia · doi:10.1213/01.ane.0000278083.31991.36 · Cited by 129
The mitochondrial permeability transition pore and cyclophilin D in cardioprotection
Lisa, F. D., Carpi, A., Giorgio, V., & Bernardi, P. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.01.031 · Cited by 132
Self-citation
Programmed necrosis in heart disease: Molecular mechanisms and clinical implications
Zhu, H., & Sun, A. (2018) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2018.01.018 · Cited by 127
Cell Life Versus Cell Longevity: The Mysteries Surrounding the NAD+ Precursor Nicotinamide
Li, F., Chong, Z. Z., & Maiese, K. (2006) · Current Medicinal Chemistry · doi:10.2174/092986706776361058 · Cited by 128
Inhibition of myocardial reperfusion injury by ischemic postconditioning requires sirtuin 3-mediated deacetylation of cyclophilin D
Bochaton, T., Silva, C. C. D., Pillot, B., Villedieu, C., Ferreras, L., Alam, M. R., Thibault, H., Strina, M., Gharib, A., Ovize, M., et al. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.03.017 · Cited by 137
Paradox of Ca2+ signaling, cell death and stroke
MacDonald, J. F., Xiong, Z., & Jackson, M. F. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2005.12.001 · Cited by 125
Differences among cell types in NAD+ compartmentalization: A comparison of neurons, astrocytes, and cardiac myocytes
Alano, C. C., Tran, A., Tao, R., Ying, W., Karliner, J. S., & Swanson, R. A. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21479 · Cited by 123
Cardiac Myocyte–Specific Expression of Inducible Nitric Oxide Synthase Protects Against Ischemia/Reperfusion Injury by Preventing Mitochondrial Permeability Transition
West, M. B., Rokosh, G., Obal, D., Velayutham, M., Xuan, Y.-T., Hill, B. G., Keith, R. J., Schrader, J., Guo, Y., Conklin, D. J., et al. (2008) · Circulation · doi:10.1161/circulationaha.108.791533 · Cited by 121
NAD+ and NADH in brain functions, brain diseases and brain aging
Ying, W. (2006) · Frontiers in bioscience · doi:10.2741/2194 · Cited by 124
Erythropoietin and Oxidative Stress
Maiese, K., Chong, Z. Z., Hou, J., & Shang, Y. (2008) · Current Neurovascular Research · doi:10.2174/156720208784310231 · Cited by 120
Cardiac Na + Current Regulation by Pyridine Nucleotides
Liu, M., Sanyal, S., Gao, G., Gurung, I. S., Zhu, X., Gaconnet, G., Kerchner, L. J., Shang, L. L., Huang, C. L.-H., Grace, A. A., et al. (2009) · Circulation Research · doi:10.1161/circresaha.109.197277 · Cited by 119
Protein kinase C and cardiac dysfunction: a review
Singh, R. M., Cummings, E., Pantos, C. I., & Singh, J. (2017) · Heart Failure Reviews · doi:10.1007/s10741-017-9634-3 · Cited by 117
Oxidative stress: Biomarkers and novel therapeutic pathways
Maiese, K., Chong, Z. Z., Hou, J., & Shang, Y. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.01.004 · Cited by 117
Ischemia/reperfusion injury at the intersection with cell death
Logue, S. E., Gustafsson, Å. B., Samali, A., & Gottlieb, R. A. (2004) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.11.009 · Cited by 116
Paracrine Roles of NAD+ and Cyclic ADP-ribose in Increasing Intracellular Calcium and Enhancing Cell Proliferation of 3T3 Fibroblasts
Franco, L., Zocchi, E., Usai, C., Guida, L., Bruzzone, S., Costa, A., & FLORA, A. D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010536200 · Cited by 115
Erythropoietin: Elucidating new cellular targets that broaden therapeutic strategies
Maiese, K., Chong, Z. Z., Li, F., & Shang, Y. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.02.002 · Cited by 113
Cyclosporine A attenuates mitochondrial permeability transition and improves mitochondrial respiratory function in cardiomyocytes isolated from dogs with heart failure
Sharov, V. G., Todor, A. V., Khanal, S., Imai, M., & Sabbah, H. N. (2006) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2006.09.013 · Cited by 112
Mechanisms of impaired mitochondrial energy metabolism in acute and chronic neurodegenerative disorders
Soane, L., Kahraman, S., Kristián, T., & Fiskum, G. M. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21498 · Cited by 112
Bradykinin prevents reperfusion injury by targeting mitochondrial permeability transition pore through glycogen synthase kinase 3β
Park, S.-S., Zhao, H., Mueller, R. A., & Xu, Z. (2006) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2006.01.024 · Cited by 111
A Self-restricted CD38-connexin 43 Cross-talk Affects NAD+ and Cyclic ADP-ribose Metabolism and Regulates Intracellular Calcium in 3T3 Fibroblasts
Bruzzone, S., Franco, L., Guida, L., Zocchi, E., Contini, P., Bisso, A., Usai, C., & FLORA, A. D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107308200 · Cited by 110
Signalling pathways and mechanisms of protection in pre‐ and postconditioning: historical perspective and lessons for the future
Cohen, M. V., & Downey, J. M. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12903 · Cited by 111
Inhibition of Mitochondrial Permeability Transition Enhances Isoflurane-Induced Cardioprotection During Early Reperfusion: The Role of Mitochondrial KATP Channels
Krolikowski, J. G., Bienengraeber, M., Weihrauch, D., Warltier, D. C., Kersten, J. R., & Pagel, P. S. (2005) · Anesthesia & Analgesia · doi:10.1213/01.ane.0000181288.13549.28 · Cited by 108
Inhibited mitochondrial respiration by amobarbital during cardiac ischaemia improves redox state and reduces matrix Ca2+ overload and ROS release
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 111
Regulation of Glucose Metabolism by NAD+ and ADP-Ribosylation
Hopp, A.-K., Grüter, P., & Hottiger, M. O. (2019) · Cells · doi:10.3390/cells8080890 · Cited by 108
NAD+ precursor modulates post-ischemic mitochondrial fragmentation and reactive oxygen species generation via SIRT3 dependent mechanisms
Klimova, N., Fearnow, A. D., Long, A. N., & Kristián, T. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113144 · Cited by 106
The Voltage-dependent Anion Channel Is the Target for a New Class of Inhibitors of the Mitochondrial Permeability Transition Pore
Cesura, A. M., Pinard, E., Schubenel, R., Goetschy, V., Friedlein, A., Langen, H., Polčic, P., Forte, M. A., Bernardi, P., & Kemp, J. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304748200 · Cited by 110
Self-citation
Role of sarcoplasmic reticulum in mitochondrial permeability transition and cardiomyocyte death during reperfusion
Ruiz‐Meana, M., Abellán, A., Miró‐Casas, E., Agulló, E., & García‐Dorado, D. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00435.2009 · Cited by 111
ROS‐Mediated PARP Activity Undermines Mitochondrial Function After Permeability Transition Pore Opening During Myocardial Ischemia–Reperfusion
Schriewer, J. M., Peek, C. B., Bass, J. T., & Schumacker, P. T. (2013) · Journal of the American Heart Association · doi:10.1161/jaha.113.000159 · Cited by 101
Mitochondria and reperfusion injury
Lisa, F. D., Canton, M., Menabò, R., Dodoni, G., & Bernardi, P. (2003) · Basic Research in Cardiology · doi:10.1007/s00395-003-0415-x · Cited by 105
Self-citation
Mitochondrial calcium uniporter regulator 1 (MCUR1) regulates the calcium threshold for the mitochondrial permeability transition
Chaudhuri, D., Artiga, D. J., Abiria, S. A., & Clapham, D. E. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602264113 · Cited by 102
Mitochondrial reprogramming through cardiac oxygen sensors in ischaemic heart disease
Cadenas, S., Aragonés, J., & Landázuri, M. O. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq256 · Cited by 101
Neuroprotective Effects of Propofol in Models of Cerebral Ischemia
Adembri, C., Venturi, L., Tani, A., Chiarugi, A., Gramigni, E., Cozzi, A., Pancani, T., Gaudio, R. A. D., & Pellegrini-Giampietro, D. E. (2005) · Anesthesiology · doi:10.1097/00000542-200601000-00014 · Cited by 100
Inhibition of the mitochondrial calcium uniporter by the oxo‐bridged dinuclear ruthenium amine complex (Ru360) prevents from irreversible injury in postischemic rat heart
García‐Rivas, G., Guerrero-Hernández, A., Guerrero‐Serna, G., Rodríguez‐Zavala, J. S., & Zazueta, C. (2005) · FEBS Journal · doi:10.1111/j.1742-4658.2005.04771.x · Cited by 98
Opening of mitochondrial permeability transition pore induces hypercontracture in Ca2+ overloaded cardiac myocytes
Ruiz‐Meana, M., Abellán, A., Miró‐Casas, E., & David Garcia-dorado, A. (2007) · Basic Research in Cardiology · doi:10.1007/s00395-007-0675-y · Cited by 98
Respiratory Complex I Dysfunction Due to Mitochondrial DNA Mutations Shifts the Voltage Threshold for Opening of the Permeability Transition Pore toward Resting Levels
Porcelli, A. M., Angelin, A., Ghelli, A. M., Mariani, E., Martinuzzi, A., Carelli, V., Petronilli, V., Bernardi, P., & Rugolo, M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807321200 · Cited by 97
Self-citation
Stromal derived factor 1α: A chemokine that delivers a two-pronged defence of the myocardium
Bromage, D. I., Davidson, S. M., & Yellon, D. M. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.03.009 · Cited by 99
Cyclophilin D and myocardial ischemia–reperfusion injury: A fresh perspective
Alam, M. R., Baetz, D., & Ovize, M. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.09.026 · Cited by 101
Ischemic Postconditioning: From Receptor to End-Effector
Cohen, M. V., & Downey, J. M. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3318 · Cited by 94
The mitochondrial permeability transition: Nexus of aging, disease and longevity
Rottenberg, H., & Hoek, J. B. (2021) · Cells · doi:10.3390/cells10010079 · Cited by 94
“It is now recognized that one of the major causes of aging and degenerative disease is the depletion of NAD+ in aging cells [87–92].”
BackgroundInfluential
The SR-mitochondria interaction: a new player in cardiac pathophysiology
Ruiz‐Meana, M., Fernández‐Sanz, C., & García‐Dorado, D. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq225 · Cited by 96
Altered NADH and improved function by anesthetic and ischemic preconditioning in guinea pig intact hearts
Riess, M. L., Camara, A. K. S., Chen, Q., Novalija, E., Rhodes, S. S., & Stowe, D. F. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01057.2001 · Cited by 93
Regulation of the Mitochondrial Permeability Transition Pore by Ubiquinone Analogs. A Progress Report
Walter, L., Miyoshi, H., Leverve, X. M., Bernardi, P., & Fontaine, E. M. (2002) · Free Radical Research · doi:10.1080/10715760290021252 · Cited by 94
Self-citation
Hydrogen sulfide prevents OGD/R-induced apoptosis via improving mitochondrial dysfunction and suppressing an ROS-mediated caspase-3 pathway in cortical neurons
Luo, Y., Yang, X., Zhao, S., Wei, C., Yin, Y., Liu, T., Jiang, S., Xie, J., Wan, X., Mao, M.-H., et al. (2013) · Neurochemistry International · doi:10.1016/j.neuint.2013.06.004 · Cited by 92
Ca2+-dependent permeability transition regulation in rat brain mitochondria by 2′,3′-cyclic nucleotides and 2′,3′-cyclic nucleotide 3′-phosphodiesterase
Azarashvili, T., Krestinina, O. V., Galvita, A., Grachev, D., Baburina, Y. L., Stricker, R., Evtodienko, Y. V., & Reiser, G. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00006.2009 · Cited by 92
Mitochondrial Injury and Protection in Ischemic Pre- and Postconditioning
Lisa, F. D., Canton, M., Carpi, A., Kaludercic, N., Menabò, R., Menazza, S., & Semenzato, M. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3375 · Cited by 95
Self-citation
Bcl-2 Is a Key Factor for Cardiac Fibroblast Resistance to Programmed Cell Death
Mayorga, M. E., Bahí, N., Ballester, M., Comella, J. X., & Sanchı́s, D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404616200 · Cited by 91
Reperfusion injury as a therapeutic challenge in patients with acute myocardial infarction
Rodríguez‐Sinovas, A., Abdallah, Y., Piper, H. M., & David Garcia-dorado, A. (2007) · Heart Failure Reviews · doi:10.1007/s10741-007-9039-9 · Cited by 90
Mitochondrial dysfunction causing cardiac sodium channel downregulation in cardiomyopathy
Liu, M., Gu, L., Sulkin, M. S., Liu, H., Jeong, E.-M., Greener, I. D., Xie, A., Efimov, I. R., & Dudley, S. C. (2012) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2012.10.011 · Cited by 90
Exercise training decreases rat heart mitochondria free radical generation but does not prevent Ca2+-induced dysfunction
Starnes, J. W., Barnes, B. D., & Olsen, M. E. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00849.2006 · Cited by 88
Temperature preconditioning of isolated rat hearts – a potent cardioprotective mechanism involving a reduction in oxidative stress and inhibition of the mitochondrial permeability transition pore
Халиулин, И. Г., Clarke, S. J., Lin, H., Parker, J. E., Suleiman, M. S., & Halestrap, A. P. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.130369 · Cited by 88
The Mitochondrial Permeability Transition in Mitochondrial Disorders
Šileikytė, J., & Forte, M. A. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/3403075 · Cited by 86
Mitochondrial Ca2+ uptake during simulated ischemia does not affect permeability transition pore opening upon simulated reperfusion☆
Ruiz‐Meana, M., GARCIADORADO, D., Miró‐Casas, E., ABELLAN, A., & Soler‐Soler, J. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.06.019 · Cited by 87
Novel Role of Silent Information Regulator 1 in Myocardial Ischemia
Yang, Y., Duan, W., Li, Y., Jin, Z., Yan, J., Yu, S., & Yi, D. (2013) · Circulation · doi:10.1161/circulationaha.113.002480 · Cited by 87
Isoflurane Postconditioning Protects against Reperfusion Injury by Preventing Mitochondrial Permeability Transition by an Endothelial Nitric Oxide Synthase–dependent Mechanism
Ge, Z., Pravdić, D., Bienengraeber, M., Pratt, P. F., Auchampach, J. A., Gross, G. J., Kersten, J. R., & Warltier, D. C. (2009) · Anesthesiology · doi:10.1097/aln.0b013e3181c4a607 · Cited by 86
Effects of CCCP-induced mitochondrial uncoupling and cyclosporin A on cell volume, cell injury and preconditioning protection of isolated rabbit cardiomyocytes
Ganote, C. E. (2003) · Journal of Molecular and Cellular Cardiology · doi:10.1016/s0022-2828(03)00114-7 · Cited by 85
Mitochondrial translocator protein (TSPO): From physiology to cardioprotection
Morin, D., Musman, J., Pons, S., Berdeaux, A., & Ghaleh, B. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.12.003 · Cited by 89
Mitochondrial energy dissipation by fatty acids
Bernardi, P., Penzo, D., & Wojtczak, L. (2002) · Vitamins and hormones · doi:10.1016/s0083-6729(02)65061-7 · Cited by 85
Self-citation
Bcl-xL mediates RIPK3-dependent necrosis in M. tuberculosis-infected macrophages
Zhao, X., Khan, N., Gan, H. T., Tzelepis, F., Nishimura, T., Park, S.-Y., Divangahi, M., & Remold, H. G. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.12 · Cited by 80
Redox-dependent Changes in Molecular Properties of Mitochondrial Apoptosis-inducing Factor
Churbanova, I. Y., & Sevrioukova, I. F. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709147200 · Cited by 83

Authors: Di Lisa, F., Menabò, R., Canton, M., Barile, M., & Bernardi, P.
Affiliations: University of Padua (IT)
National Research Council (IT)
ORCID: Menabò, Roberta
Canton, Marcella
Barile, Maria
Bernardi, Paolo
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2001-01
Volume: 276
Issue: 4
Pages: 2571-2575
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m006825200
OpenAlex: W2147640676
Cited by: 678
References: 46
Citations by year: 2026: 5 · 2025: 12 · 2024: 16 · 2023: 16 · 2022: 12 · 2021: 26 · 2020: 20 · 2019: 27 · 2018: 34 · 2017: 24 · 2016: 25 · 2015: 24 · 2014: 33 · 2013: 23 · 2012: 33
FWCI: 15.49
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 7224 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion)
Padua Research Archive (University of Padova) (submittedVersion)
INFM-OAR (INFN Catania) (submittedVersion, cc-by)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Ischemia and Reperfusion
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
Keywords: mitochondrial permeability transition pore, NAD+ depletion, NAD glycohydrolase, cyclosporine, myocyte death, myocardial ischemia, mitochondrial swelling, calcineurin, cardioprotection, lactate dehydrogenase release
MeSH terms: Mitochondrial Permeability Transition Pore, Animals, Cytosol, Ion Channels, Male, Membrane Proteins, Mitochondria, Heart, Myocardium, NAD, NAD+ Nucleosidase, Myocardial Reperfusion Injury, Cyclosporine, Cell Death, Myocardial Ischemia, Rats, Wistar, Mitochondrial Membrane Transport Proteins, 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

Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks