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 accessAbstract
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
Cites
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?
Low concentrations of ONOO− (0.1 mM) protect neurons against NO•-mediated apoptosis by activating the PI3K/Akt antiapoptotic signaling pathway.
“but low concentrations of ONOO− (0.1 mM) were found to protect neurons against NO•-mediated apoptosis by activating the phosphoinositide-3-kinase (PI3K)/Akt antiapoptotic signaling pathway (106).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [106]
Extended mPTP opening causes loss of NAD+.
“An additional deleterious outcome of extended mPTP opening is the loss of NAD+.”
From The mitochondrial permeability transition: Nexus of aging, disease and longevity (2021) · cites this paper as [3]
Oxidative stress-dependent cell death largely depends on the activation of mPTP.
“Oxidative stress-dependent cell death largely depends on the activation of mPTP.”
From The mitochondrial permeability transition: Nexus of aging, disease and longevity (2021) · cites this paper as [3]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
(1975) · Journal of AOAC INTERNATIONAL · doi:10.1093/jaoac/58.5.1085 · Cited by 20,078 · see citing works
(1974) · Elsevier eBooks · doi:10.1016/b978-0-12-091304-6.x5001-0 · Cited by 6,786 · see citing works
(1985) · International Journal of Biochemistry · doi:10.1016/0020-711x(85)90098-9 · Cited by 3,497 · 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
Self-citationMitochondrial 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 · see citing works
Palmer, J. W., Tandler, B., & Hoppel, C. L. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)75283-1 · Cited by 830 · see citing works
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 · see citing works
Self-citationMyocardial calcium and magnesium in acute ischemic injury.
Shen, A. C., & Jennings, R. B. (1972) · PubMed · Cited by 629 · see citing works
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 · see citing works
Bernardi, P., Broekemeier, K. M., & Pfeiffer, D. R. (1994) · Journal of Bioenergetics and Biomembranes · doi:10.1007/bf00762735 · Cited by 561 · see citing works
Self-citationPoly (ADP-ribose) polymerase, nitric oxide and cell death
Pieper, A. A. (1999) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(99)01292-4 · Cited by 521 · see citing works
Nicolli, A., Basso, E., Petronilli, V., Wenger, R. M., & Bernardi, P. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.4.2185 · Cited by 482 · see citing works
Self-citationZimmerman, A. N. E., & Hülsmann, W. C. (1966) · Nature · doi:10.1038/211646a0 · Cited by 479 · see citing works
Coenzyme A and carnitine distribution in normal and ischemic hearts.
Idell-Wenger, J. A., Grotyohann, L. W., & Neely, J. R. (1978) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)34721-x · Cited by 476 · see citing works
Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP
Lee, H. C. (1997) · Physiological Reviews · doi:10.1152/physrev.1997.77.4.1133 · Cited by 371 · see citing works
The Cell Biology of Acute Myocardial Ischemia
Jennings, R. B., & Reimer, K. A. (1991) · Annual Review of Medicine · doi:10.1146/annurev.me.42.020191.001301 · Cited by 352 · see citing works
Thiemermann, C., Bowes, J., Myint, F., & Vane, J. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.2.679 · Cited by 305 · see citing works
On the involvement of a cyclosporin A sensitive mitochondrial pore in myocardial reperfusion injury
Duchen, M. R., McGuinness, O. M., Brown, L. A., & Crompton, M. (1993) · Cardiovascular Research · doi:10.1093/cvr/27.10.1790 · Cited by 294 · see citing works
Di Lisa, F., Blank, P. S., Colonna, R., Gambassi, G., Silverman, H. S., Stern, M. D., & Hansford, R. G. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020786 · Cited by 286 · see citing works
Inhibition of anoxia-induced injury in heart myocytes by cyclosporin A
Nazareth, W. (1991) · Journal of Molecular and Cellular Cardiology · doi:10.1016/0022-2828(91)90181-k · Cited by 272 · see citing works
Loetscher, H., Winterhalter, K. H., Carafoli, E., & Richter, C. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)70565-1 · Cited by 223 · see citing works
Ionic basis of ischaemic cardiac injury: insights from cellular studies
Silverman, H. S., & Stern, M. D. (1994) · Cardiovascular Research · doi:10.1093/cvr/28.5.581 · Cited by 182 · see citing works
Miyata, H., Lakatta, E. G., Stern, M. D., & Silverman, H. S. (1992) · Circulation Research · doi:10.1161/01.res.71.3.605 · Cited by 177 · see citing works
Scorrano, L., Petronilli, V., Lisa, F. D., & Bernardi, P. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.32.22581 · Cited by 161 · see citing works
Self-citationReperfusion of ischemic myocardium: Ultrastructural and histochemical aspects
Schaper, J., & Schaper, W. K. A. (1983) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(83)80106-5 · Cited by 145 · see citing works
Lindenmayer, G. E., Sordahl, L. A., & Schwartz, A. (1968) · Circulation Research · doi:10.1161/01.res.23.3.439 · Cited by 142 · see citing works
Ischaemia and the myocyte cytoskeleton: review and speculation
Ganote, C. E., & Armstrong, S. (1993) · Cardiovascular Research · doi:10.1093/cvr/27.8.1387 · Cited by 140 · see citing works
Potential role of calcineurin for brain ischemia and traumatic injury
Morioka, M., Hamada, J., Ushio, Y., & Miyamoto, E. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00073-2 · Cited by 127 · see citing works
The role of mitochondria in the salvage and the injury of the ischemic myocardium
Lisa, F. D., Menabò, R., Canton, M., & Petronilli, V. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00121-2 · Cited by 127 · see citing works
Self-citationCalcium and pyridine nucleotide interaction in mitochondrial membranes
Vinogradov, A., Scarpa, A., & Chance, B. (1972) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(72)90261-5 · Cited by 126 · see citing works
A Fluorescent Analog of Nicotinamide Adenine Dinucleotide
Barrio, J. R., Secrist, J. A. I., & Leonard, N. J. (1972) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.69.8.2039 · Cited by 121 · see citing works
Ganote, C. E., Worstell, J., & Kaltenbach, J. P. (1976) · PubMed · Cited by 88 · see citing works
ADP-ribosylation in inner membrane of rat liver mitochondria.
Richter, C., Winterhalter, K. H., Baumhueter, S., Loetscher, H., & Moser, B. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.11.3188 · Cited by 84 · see citing works
Protective Effect of FK506 on Ischemia/Reperfusion-Induced Myocardial Damage in Canine Heart
Nishinaka, Y., Sugiyama, S., Yokota, M., Saito, H., & Ozawa, T. (1993) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199303000-00015 · Cited by 67 · see citing works
Cyclosporine a inhibits mitochondrial pyridine nucleotide hydrolysis and calcium release
Richter, C., Theus, M., & Schlegel, J. (1990) · Biochemical Pharmacology · doi:10.1016/0006-2952(90)90315-c · Cited by 61 · see citing works
Cyclosporin A targets involved in protection against glutamate excitotoxicity
Ruiz, F. H., Alvarez, G., Ramos, M., Hernández, M., Bogónez, E., & Satrústegui, J. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00584-7 · Cited by 60 · see citing works
Minezaki, K., Suleiman, M. S., & Chapman, R. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020147 · Cited by 59 · see citing works
Flavin Adenine Dinucleotide and Flavin Mononucleotide Metabolism in Rat Liver
Barile, M., Brizio, C., Virgilio, C. D., Delfine, S., Quagliariello, E., & Passarella, S. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.00777.x · Cited by 57 · see citing works
Self-citationVeloso, D., & Veech, R. L. (1974) · Analytical Biochemistry · doi:10.1016/0003-2697(74)90177-8 · Cited by 54 · see citing works
Fluxes of Nicotinamide Adenine Dinucleotides through Mitochondrial Membranes in Human Cultured Cells
Rustin, P., Parfait, B., Chrétien, D., Bourgeron, T., Djouadi, F., Bastin, J., Rötig, A., & Münnich, A. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.25.14785 · Cited by 54 · see citing works
Molecular Mechanisms of Immunosuppression by Cyclosporins
Zenke, G., Baumann, G., Wenger, R. M., HIESTAND, P. C., Quesniaux, V. F. J., Andersen, E., & Schreier, M. H. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb35882.x · Cited by 53 · see citing works
Frei, B. B., Winterhalter, K. H., & Richter, C. (1985) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1985.tb08971.x · Cited by 52 · see citing works
Barile, M., Passarella, S., Danese, G., & Quagliariello, E. (1996) · PubMed · Cited by 52 · see citing works
Self-citationGanote, C. E. (1980) · Journal of Molecular and Cellular Cardiology · doi:10.1016/0022-2828(80)90049-8 · Cited by 42 · see citing works
Boyer, C. S., Moore, G., & Moldéus, P. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53572-9 · Cited by 36 · see citing works
NAD glycohydrolase activity in hearts with acute experimental infarction
Nunez, R. M., Calva, E., Marsch, M., Briones, E., & López-Soriano, F. (1976) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1976.231.4.1173 · Cited by 21 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Barrio, J. R., Secrist, J. A., and Leonard, N. J. (1972) Proc. Natl. Acad. Sci.
- Richter, C., Winterhalter, K. H., Baumhuter, S., Lotscher, H. R., and Moser, B. (1983) Proc. Natl. Acad. Sci. U. S. A. 80, 3188 -3192
- Thiemermann, C., Bowes, J., Myint, F. P., and Vane, J. R. (1997) Proc. Natl. Acad. Sci. U. S. A. 94, 679 -683
Cited by
Sorted by citations
Mediation of Poly(ADP-Ribose) Polymerase-1-Dependent Cell Death by Apoptosis-Inducing Factor
Yu, S.-W., Wang, H., Poitras, M. F., Coombs, C., Bowers, W. J., Federoff, H. J., Poirier, G. G., Dawson, T. M., & Dawson, V. L. (2002) · Science · doi:10.1126/science.1072221 · Cited by 1,826 · see citing works
Ying, W. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2007.1672 · Cited by 1,494 · see citing works
Effect of Cyclosporine on Reperfusion Injury in Acute Myocardial Infarction
Piot, C. A., Croisille, P., Staat, P., Thibault, H., Rioufol, G., Mewton, N., Belghiti, R. E., Cung, T. T., Bonnefoy‐Cudraz, E., Angoulvant, D., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa071142 · Cited by 1,339 · see citing works
Halestrap, A. P. (2003) · Cardiovascular Research · doi:10.1016/s0008-6363(03)00533-9 · Cited by 1,223 · see citing works
NAD(H) and NADP(H) Redox Couples and Cellular Energy Metabolism
Xiao, W., Wang, R., Handy, D. E., & Loscalzo, J. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7216 · Cited by 1,074 · see citing works
Camacho-Pereira, J., Tarragó, M. G., Chini, C. C. S., Nin, V., Escande, C., Warner, G. M., Puranik, A. S., Schoon, R. A., Reid, J. M., Galina, A., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.05.006 · Cited by 901 · see citing works
ROS and redox signaling in myocardial ischemia-reperfusion injury and cardioprotection
Cadenas, S. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.01.024 · Cited by 819 · see citing works
Properties of the Permeability Transition Pore in Mitochondria Devoid of Cyclophilin D
Basso, E., Fante, L., Fowlkes, J., Petronilli, V., Forte, M. A., & Bernardi, P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.c500089200 · Cited by 808 · see citing works
Self-citationFerdinandy, P., Schulz, R., & Baxter, G. F. (2007) · Pharmacological Reviews · doi:10.1124/pr.107.06002 · Cited by 738 · see citing works
Necrosis: a specific form of programmed cell death?
Proskuryakov, S., Konoplyannikov, A. G., & Gabai, V. L. (2003) · Experimental Cell Research · doi:10.1016/s0014-4827(02)00027-7 · Cited by 721 · 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
Gandhi, S., Wood-Kaczmar, A., Yao, Z., Plun-Favreau, H., Deas, E., Klupsch, K., Downward, J., Latchman, D. S., Tabrizi, S. J., Wood, N. W., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.02.013 · Cited by 682 · see citing works
Mitochondrial dysfunction in diabetic kidney disease
Forbes, J. M., & Thorburn, D. R. (2018) · Nature Reviews Nephrology · doi:10.1038/nrneph.2018.9 · Cited by 641 · see citing works
NAD+ homeostasis in health and disease
Katsyuba, E., Romani, M., Hofer, D., & Auwerx, J. (2020) · Nature Metabolism · doi:10.1038/s42255-019-0161-5 · Cited by 627 · see citing works
The mitochondrial permeability transition from<i>in vitro</i>artifact to disease target
Bernardi, P., Krauskopf, A., Basso, E., Petronilli, V., Blalchy‐Dyson, E., Di Lisa, F., & Forte, M. A. (2006) · The FEBS Journal · doi:10.1111/j.1742-4658.2006.05213.x · Cited by 627 · see citing works
Self-citationSchwer, B., North, B. J., Frye, R. A., Ott, M., & Verdin, E. M. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200205057 · Cited by 599 · see citing works
Bernardi, P., Rasola, A., Forte, M. A., & Lippe, G. (2015) · Physiological Reviews · doi:10.1152/physrev.00001.2015 · Cited by 586 · see citing works
Self-citationMitochondrial permeability transition in Ca2+-dependent apoptosis and necrosis
Rasola, A., & Bernardi, P. (2011) · Cell Calcium · doi:10.1016/j.ceca.2011.04.007 · Cited by 563 · see citing works
Self-citationPostconditioning Inhibits Mitochondrial Permeability Transition
Argaud, L., Gateau-Roesch, O., Raisky, O., Loufouat, J., Robert, D., & Ovize, M. (2005) · Circulation · doi:10.1161/01.cir.0000151290.04952.3b · Cited by 561 · see citing works
Molecular mechanisms and consequences of mitochondrial permeability transition
Bonora, M., Giorgi, C., & Pinton, P. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00433-y · Cited by 549 · see citing works
Hafner, A. V., Dai, J., Gomes, A. P., Xiao, C., Palmeira, C. M., Rosenzweig, A., & Sinclair, D. A. (2010) · Aging · doi:10.18632/aging.100252 · Cited by 547 · see citing works
The dynamic regulation of NAD metabolism in mitochondria
Stein, L. R., & Imai, S. (2012) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.06.005 · Cited by 529 · see citing works
Chong, Z. Z., Li, F., & Maiese, K. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.02.004 · Cited by 536 · see citing works
Reperfusion injury salvage kinase signalling: taking a RISK for cardioprotection
Hausenloy, D. J., & Yellon, D. M. (2007) · Heart Failure Reviews · doi:10.1007/s10741-007-9026-1 · Cited by 511 · see citing works
Rasola, A., & Bernardi, P. (2007) · APOPTOSIS · doi:10.1007/s10495-007-0723-y · Cited by 507 · see citing works
Self-citationStowe, D. F., & Camara, A. K. S. (2009) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2331 · Cited by 471 · see citing works
Mitochondrial ROS in myocardial ischemia reperfusion and remodeling
Bugger, H., & Pfeil, K. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165768 · Cited by 469 · see citing works
Generation of Reactive Oxygen Species in the Reaction Catalyzed by α-Ketoglutarate Dehydrogenase
Tretter, L., & Ádám‐Vizi, V. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1842-04.2004 · Cited by 455 · see citing works
Baines, C. P., Song, C., Zheng, Y.-T., Wang, G.-W., Zhang, J., Wang, O.-L., Guo, Y., Bolli, R., Cardwell, E. M., & Ping, P. (2003) · Circulation Research · doi:10.1161/01.res.0000069215.36389.8d · Cited by 450 · see citing works
Alano, C. C., Garnier, P., Ying, W., Higashi, Y., Kauppinen, T. M., & Swanson, R. A. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5552-09.2010 · Cited by 439 · see citing works
The ubiquitous role of nitric oxide in cardioprotection
Jones, S. P., & Bolli, R. (2006) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2005.09.011 · Cited by 434 · see citing works
Bøtker, H. E., Hausenloy, D. J., Andreadou, I., Antonucci, S., Boengler, K., Davidson, S. M., Deshwal, S., Devaux, Y., Lisa, F. D., Sante, M. D., et al. (2018) · Basic Research in Cardiology · doi:10.1007/s00395-018-0696-8 · Cited by 426 · see citing works
Hausenloy, D. J. (2003) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.09.025 · Cited by 419 · see citing works
Bid Is Cleaved by Calpain to an Active Fragment in Vitro and during Myocardial Ischemia/Reperfusion*
Chen, M., He, H.-P., Zhan, S., Krajewski, S., Reed, J. C., & Gottlieb, R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103701200 · Cited by 416 · see citing works
Geng, H.-H., Li, R., Su, Y.-M., Xiao, J., Pan, M., Cai, X.-X., & Ji, X.-P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151753 · Cited by 372 · see citing works
The role of mitochondria in protection of the heart by preconditioning
Halestrap, A. P., Clarke, S. J., & Khaliulin, I. (2007) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2007.05.008 · Cited by 390 · see citing works
Raedschelders, K., Ansley, D. M., & Chen, D. D. Y. (2011) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2011.11.004 · Cited by 387 · see citing works
Clarke, S. J., McStay, G. P., & Halestrap, A. P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202191200 · Cited by 376 · see citing works
Alano, C. C., Ying, W., & Swanson, R. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313329200 · Cited by 374 · see citing works
The role of the mitochondrial permeability transition pore in heart disease
Halestrap, A. P., & Pasdois, P. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.12.017 · Cited by 362 · see citing works
Specific inhibition of the mitochondrial permeability transition prevents lethal reperfusion injury
Argaud, L., Gateau-Roesch, O., Muntean, D. M., Chalabreysse, L., Loufouat, J., Robert, D., & Ovize, M. (2005) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.12.001 · Cited by 359 · see citing works
Javadov, S. A., Clarke, S. J., Das, M., Griffiths, E. J., Lim, K. H. H., & Halestrap, A. P. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.034231 · Cited by 350 · see citing works
Mitochondria and ischemia–reperfusion injury of the heart: Fixing a hole
Lisa, F. D., & Bernardi, P. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.01.016 · Cited by 341 · see citing works
Self-citationMitochondrial calcium and oxidative stress as mediators of ischemic brain injury
Starkov, A. A., Chinopoulos, C., & Fiskum, G. M. (2004) · Cell Calcium · doi:10.1016/j.ceca.2004.02.012 · Cited by 339 · see citing works
Protein acetylation in metabolism – metabolites and cofactors
Menzies, K. J., Zhang, H., Katsyuba, E., & Auwerx, J. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.181 · Cited by 331 · see citing works
Garlid, K., Santos, P. D. D., Xie, Z., Costa, A. D. T., & Pauček, P. (2003) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(03)00109-9 · Cited by 332 · see citing works
Mitochondrial morphology transitions and functions: implications for retrograde signaling?
Picard, M. A., Shirihai, O. S., Gentil, B. J., & Burelle, Y. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00584.2012 · Cited by 320 · see citing works
Ong, S., Samangouei, P., Kalkhoran, S. B., & Hausenloy, D. J. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.11.005 · Cited by 323 · see citing works
A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection
Halestrap, A. P. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380841 · Cited by 307 · see citing works
Calcium-mediated cell death during myocardial reperfusion
García‐Dorado, D., Ruiz‐Meana, M., Inserte, J., Rodríguez‐Sinovas, A., & Piper, H. M. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs116 · Cited by 308 · see citing works
NAD+ and Vitamin B3: From Metabolism to Therapies
Sauve, A. A. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.120758 · Cited by 303 · see citing works
Chen, Q., Moghaddas, S., Hoppel, C. L., & Lesnefsky, E. J. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00211.2007 · Cited by 299 · see citing works
Preconditioning and postconditioning: United at reperfusion
Hausenloy, D. J., & Yellon, D. M. (2007) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2007.06.005 · Cited by 285 · see citing works
Hsu, C., Oka, S., Shao, D., Hariharan, N., & Sadoshima, J. (2009) · Circulation Research · doi:10.1161/circresaha.109.203703 · Cited by 284 · see citing works
The mitochondrial permeability transition pore and ischemia-reperfusion injury
Baines, C. P. (2009) · Basic Research in Cardiology · doi:10.1007/s00395-009-0004-8 · Cited by 280 · see citing works
Javadov, S. A., & Karmazyn, M. (2007) · Cellular Physiology and Biochemistry · doi:10.1159/000103747 · Cited by 281 · see citing works
Luth, E. S., Stavrovskaya, I. G., Bartels, T., Kristal, B. S., & Selkoe, D. J. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.545749 · Cited by 281 · see citing works
Rottenberg, H., & Hoek, J. B. (2017) · Aging Cell · doi:10.1111/acel.12650 · Cited by 275 · see citing works
Postconditioning: Reduction of reperfusion-induced injury
ZHAO, Z., & Vinten‐Johansen, J. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.01.024 · Cited by 272 · see citing works
Mitochondria as a Drug Target in Ischemic Heart Disease and Cardiomyopathy
Walters, A. M., Porter, G. A., Jr., & Brookes, P. S. (2012) · Circulation Research · doi:10.1161/circresaha.112.265660 · Cited by 268 · see citing works
NAD + as a metabolic link between DNA damage and cell death
Ying, W., Alano, C. C., Garnier, P. E., & Swanson, R. A. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20289 · Cited by 269 · see citing works
Mitochondria in cell death: novel targets for neuroprotection and cardioprotection
Mattson, M. P., & Kroemer, G. (2003) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(03)00046-7 · Cited by 264 · see citing works
Calabrese, V., Scapagnini, G., Giuffrida Stella, A. M., Bates, T. E., & Clark, J. B. (2001) · Neurochemical Research · doi:10.1023/a:1010955807739 · Cited by 263 · see citing works
Regulation of mitochondrial matrix volume
Kaasik, A., Safiulina, D., Zharkovsky, A., & Veksler, V. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00272.2006 · Cited by 259 · 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
Biochemical dysfunction in heart mitochondria exposed to ischaemia and reperfusion
Solaini, G., & Harris, D. A. (2005) · Biochemical Journal · doi:10.1042/bj20042006 · Cited by 248 · see citing works
Identification of an ATP-sensitive potassium channel in mitochondria
Paggio, A., Checchetto, V., del Campo, A. F., Menabò, R., Marco, G. D., Lisa, F. D., Szabó, I., Rizzuto, R., & Stefani, D. D. (2019) · Nature · doi:10.1038/s41586-019-1498-3 · Cited by 251 · see citing works
Self-citationLiu, D., Gharavi, R. B., PITTA, M. G. R., Gleichmann, M., & Mattson, M. P. (2009) · NeuroMolecular Medicine · doi:10.1007/s12017-009-8058-1 · Cited by 248 · see citing works
NAD+ and NADH in cellular functions and cell death
Ying, W. (2006) · Frontiers in bioscience · doi:10.2741/2038 · Cited by 250 · 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
Javadov, S. A., Karmazyn, M., & Escobales, N. (2009) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.153213 · Cited by 248 · see citing works
Basic Biology of Oxidative Stress and the Cardiovascular System
Sack, M. N., Fyhrquist, F., Saijonmaa, O. J., Fuster, V., & Kovacic, J. C. (2017) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.05.034 · Cited by 243 · see citing works
Calcium, mitochondria and oxidative stress in neuronal pathology
Chinopoulos, C., & Ádám‐Vizi, V. (2006) · FEBS Journal · doi:10.1111/j.1742-4658.2005.05103.x · Cited by 239 · see citing works
Guidelines for evaluating myocardial cell death
Mishra, P. K., Adameová, A., Hill, J. A., Baines, C. P., Kang, P. M., Downey, J. M., Narula, J., Takahashi, M., Abbate, A., Piristine, H. C., et al. (2019) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00259.2019 · Cited by 238 · see citing works
Intramitochondrial signaling: interactions among mitoK<sub>ATP</sub>, PKCε, ROS, and MPT
Costa, A. D. T., & Garlid, K. D. (2008) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01189.2007 · Cited by 238 · see citing works
The Vitamin Nicotinamide: Translating Nutrition into Clinical Care
Maiese, K., Chong, Z. Z., Hou, J., & Shang, Y. C. (2009) · Molecules · doi:10.3390/molecules14093446 · Cited by 240 · see citing works
Huang, J.-Y., Hirschey, M. D., Shimazu, T., Ho, L., & Verdin, E. (2010) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2009.12.021 · Cited by 231 · see citing works
Oxidative stress and myocardial injury in the diabetic heart
Ansley, D. M., & Wang, B. (2012) · The Journal of Pathology · doi:10.1002/path.4113 · Cited by 231 · see citing works
Metabolic stress, reactive oxygen species, and arrhythmia
Jeong, E.-M., Liu, M., Sturdy, M., Gao, G., Varghese, S. T., Sovari, A. A., & Dudley, S. C. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.09.018 · Cited by 234 · see citing works
KATPChannels in the Cardiovascular System
Foster, M. N., & Coetzee, W. A. (2015) · Physiological Reviews · doi:10.1152/physrev.00003.2015 · Cited by 222 · see citing works
Cell death during ischemia: relationship to mitochondrial depolarization and ROS generation
Levraut, J., Iwase, H., Shao, Z. H., Hoek, T. L. V., & Schumacker, P. T. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00708.2002 · Cited by 226 · see citing works
Cardiac mitochondria and arrhythmias
Brown, D. A., & O'Rourke, B. P. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq231 · Cited by 226 · see citing works
The role of Coenzyme Q in mitochondrial electron transport
Lenaz, G., Fato, R., Formiggini, G., & Genova, M. L. (2007) · Mitochondrion · doi:10.1016/j.mito.2007.03.009 · Cited by 224 · see citing works
Nitric oxide and cardiac function
Rastaldo, R., Pagliaro, P., Cappello, S., Penna, C. R. R., Mancardi, D., Westerhof, N., & Losano, G. A. (2007) · Life Sciences · doi:10.1016/j.lfs.2007.07.019 · Cited by 224 · see citing works
Radical roles for RAGE in the pathogenesis of oxidative stress in cardiovascular diseases and beyond
Daffu, G., Del Pozo, C., O'Shea, K., Ananthakrishnan, R., Ramasamy, R., & Schmidt, A. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms141019891 · Cited by 222 · see citing works
Germline Energetics, Aging, and Female Infertility
Tilly, J. L., & Sinclair, D. A. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.05.007 · Cited by 220 · see citing works
Reactive Oxygen Species Originating From Mitochondria Regulate the Cardiac Sodium Channel
Liu, M., Liu, H., & Dudley, S. C. (2010) · Circulation Research · doi:10.1161/circresaha.110.220673 · Cited by 217 · see citing works
Mitochondrial Reactive Oxygen Species at the Heart of the Matter
Kornfeld, O. S., Hwang, S., Disatnik, M., Chen, C., Qvit, N., & Mochly‐Rosen, D. (2015) · Circulation Research · doi:10.1161/circresaha.116.305432 · Cited by 210 · see citing works
Mitochondrial oxidant stress triggers cell death in simulated ischemia–reperfusion
Loor, G., Kondapalli, J., Iwase, H., Chandel, N. S., Waypa, G. B., Guzy, R. D., Hoek, T. L. V., & Schumacker, P. T. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.12.008 · Cited by 214 · see citing works
Costa, A. D. T., Jakob, R., Costa, C. L., Andrukhiv, K., West, I. C., & Garlid, K. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600959200 · Cited by 210 · see citing works
Merlini, L., Angelin, A., Tiepolo, T., Braghetta, P., Sabatelli, P., Zamparelli, A., Ferlini, A., Maraldi, N. M., Bonaldo, P., & Bernardi, P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800962105 · Cited by 207 · see citing works
Self-citationCalcium and Cell Death: The Mitochondrial Connection
Bernardi, P., & Rasola, A. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6191-2_18 · Cited by 202 · see citing works
Self-citationMitochondrial permeability transitions: how many doors to the house?
Zoratti, M., Szabó, I., & Marchi, U. D. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2004.10.006 · Cited by 205 · see citing works
Role of the anion nitrite in ischemia-reperfusion cytoprotection and therapeutics
DEZFULIAN, C., RAAT, N., SHIVA, S., & GLADWIN, M. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2007.05.001 · Cited by 198 · see citing works
Gomez, L., Thibault, H., Gharib, A., Dumont, J., Vuagniaux, G., Scalfaro, P., Dérumeaux, G., & Ovize, M. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01378.2006 · Cited by 199 · see citing works
Effect of Cyclosporine on Left Ventricular Remodeling After Reperfused Myocardial Infarction
Mewton, N., Croisille, P., Gahide, G., Rioufol, G., Bonnefoy‐Cudraz, E., Sanchez, I., Cung, T. T., Sportouch, C., Angoulvant, D., Finet, G., et al. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2009.10.052 · Cited by 198 · see citing works
Das, S., Wong, R. P., Rajapakse, N. C., Murphy, E., & Steenbergen, C. (2008) · Circulation Research · doi:10.1161/circresaha.108.178970 · Cited by 197 · see citing works
Cardioprotective signaling to mitochondria
Garlid, K., Costa, A. D. T., Quinlan, C. L., Pierre, S. V., & Santos, P. D. D. (2008) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2008.11.019 · Cited by 192 · see citing works
Šileikytė, J., Blachly‐Dyson, E., Sewell, R., Carpi, A., Menabò, R., Lisa, F. D., Ricchelli, F., Bernardi, P., & Forte, M. A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.549634 · Cited by 190 · see citing works
Self-citationInhibition of Nicotinamide Phosphoribosyltransferase
Pittelli, M., Formentini, L., Faraco, G., Lapucci, A., Rapizzi, E., Cialdai, F., Romano, G., Moneti, G., Moroni, F., & Chiarugi, A. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.136739 · Cited by 189 · see citing works
- Authors
- Di Lisa, F., Menabò, R., Canton, M., Barile, M., & Bernardi, P.
- Affiliations
- University of Padua (IT)
- National Research Council (IT)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2001-01
- Volume
- 276
- Issue
- 4
- Pages
- 2571-2575
- ISSN
- 0021-9258 (ISSN-L)
- 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
- 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 › Pathology and Forensic 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
