Ischemic preconditioning alters real-time measure of O2 radicals in intact hearts with ischemia and reperfusion
Abstract
Reactive oxygen species (ROS) are believed to be involved in triggering cardiac ischemic preconditioning (IPC). Decreased formation of ROS on reperfusion after prolonged ischemia may in part underlie protection by IPC. In heart models, these contentions have been based either on the effect of ROS scavengers to abrogate IPC-induced preservation or on a measurement of oxidation products on reperfusion. Using spectrophotofluorometry at the left ventricular wall and the fluorescent probe dihydroethidium (DHE), we measured intracellular ROS superoxide (O[Formula: see text]·) continuously in isolated guinea pig heart and tested the effect of IPC and the O[Formula: see text]· scavenger manganese(III) tetrakis (4-benzoic acid) porphyrin chloride (MnTBAP) on O[Formula: see text]· formation throughout the phases of preconditioning (PC), 30-min ischemia and 60-min reperfusion (I/R). IPC was evidenced by improved contractile function and reduced infarction; MnTBAP abrogated these effects. Brief PC pulses increased O[Formula: see text]· during the ischemic but not the reperfusion phase. O[Formula: see text]· increased by 35% within 1 min of ischemia, increased further to 95% after 20 min of ischemia, and decreased slowly on reperfusion. In the IPC group, O[Formula: see text]· was not elevated over 35% during index ischemia and was not increased at all on reperfusion; these effects were abrogated by MnTBAP. Our results directly demonstrate how intracellular ROS increase in intact hearts during IPC and I/R and clarify the role of ROS in triggering and mediating IPC.
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?
UCPs 1-4 are believed to induce an inward proton leak in charged mitochondria.
“A small class of “uncoupling” proteins, called UCPs 1–4, are believed to induce an inward proton “leak” in charged mitochondria (49, 55, 176, 300).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [176]
Cites
Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium.
Murry, C. E., Jennings, R. B., & Reimer, K. A. (1986) · Circulation · doi:10.1161/01.cir.74.5.1124 · Cited by 7,813 · see citing works
LeBel, C. P., Ischiropoulos, H., & Bondy, S. C. (1992) · Chemical Research in Toxicology · doi:10.1021/tx00026a012 · Cited by 2,694 · see citing works
Vanden Hoek, T. L., Becker, L. B., Shao, Z., Li, C., & Schumacker, P. T. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.29.18092 · Cited by 721 · see citing works
Bolli, R., Patel, B. S., Jeroudi, M. O., Lai, E. K., & McCay, P. B. (1988) · Journal of Clinical Investigation · doi:10.1172/jci113621 · Cited by 685 · see citing works
Pain, T., Yang, X.-M., Critz, S. D., Yue, Y., Nakano, A., Liu, G. S., Heusch, G., Cohen, M. V., & Downey, J. M. (2000) · Circulation Research · doi:10.1161/01.res.87.6.460 · Cited by 662 · see citing works
Critical evaluation of the use of hydroethidine as a measure of superoxide anion radical
Benov, L., Sztejnberg, L., & Fridovich, I. (1998) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00163-4 · Cited by 495 · see citing works
Baines, C. P., Goto, M., & Downey, J. M. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1996.0265 · Cited by 484 · cited 6× · see citing works
“Exogenous administration of H2O2 can induce a preconditioned state in cardiomyocytes (44) and intact hearts (43), and a similar effect can be achieved by endogenous ROS formation by the xanthine/xanthine oxidase reaction (4, 52) or by using the ETC inhibitor menadione (49).”
BackgroundMethodInfluentialMitochondrial PKCε and MAPK Form Signaling Modules in the Murine Heart
Baines, C. P., Zhang, J., Wang, G.-W., Zheng, Y.-T., Xiu, J. X., Cardwell, E. M., Bolli, R., & Ping, P. (2002) · Circulation Research · doi:10.1161/01.res.0000012702.90501.8d · Cited by 429 · see citing works
Generation of superoxide in cardiomyocytes during ischemia before reperfusion
Becker, L. B., Hoek, T. L. V., Shao, Z., Li, C., & Schumacker, P. T. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.277.6.h2240 · Cited by 413 · see citing works
The Optimal Efficiency and the Economic Degrees of Coupling of Oxidative Phosphorylation
Stucki, J. W. (1980) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1980.tb04792.x · Cited by 401 · see citing works
Hoek, T. L. V., Li, C., Shao, Z., Schumacker, P. T., & Becker, L. B. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1997.0497 · Cited by 398 · see citing works
ATP-Sensitive Potassium Channels: A Review of their Cardioprotective Pharmacology
Grover, G. J., & Garlid, K. (2000) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1111 · Cited by 397 · see citing works
Diazoxide-Induced Cardioprotection Requires Signaling Through a Redox-Sensitive Mechanism
Forbes, R. A., Steenbergen, C., & Murphy, E. (2001) · Circulation Research · doi:10.1161/hh0801.089342 · Cited by 395 · see citing works
Preconditioning in Cardiomyocytes Protects by Attenuating Oxidant Stress at Reperfusion
Hoek, T. L. V., Becker, L. B., Shao, Z., Li, C., & Schumacker, P. T. (2000) · Circulation Research · doi:10.1161/01.res.86.5.541 · Cited by 312 · see citing works
Oxygen-derived free radicals and myocardial reperfusion injury: An overview
Bolli, R. (1991) · Cardiovascular Drugs and Therapy · doi:10.1007/bf00054747 · Cited by 295 · see citing works
Role of DNA Repair Inhibition in Lead- and Cadmium-Induced Genotoxicity: A Review
Hartwig, A. (1994) · Environmental Health Perspectives · doi:10.1289/ehp.94102s345 · Cited by 287 · see citing works
Day, B. J., Fridovich, I., & Crapo, J. D. (1997) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1997.0341 · Cited by 285 · see citing works
Flaherty, J. T., Pitt, B., Gruber, J. W., Heuser, R. R., ROTHBAUM, D. A., Burwell, L. R., George, B. S., Kereiakes, D. J., Deitchman, D., & Gustafson, N. (1994) · Circulation · doi:10.1161/01.cir.89.5.1982 · Cited by 255 · see citing works
Granulocytes cause reperfusion ventricular dysfunction after 15-minute ischemia in the dog.
Engler, R. L., & Covell, J. W. (1987) · Circulation Research · doi:10.1161/01.res.61.1.20 · Cited by 227 · see citing works
Zhou, X., Zhai, X., & Ashraf, M. (1996) · Circulation · doi:10.1161/01.cir.93.6.1177 · Cited by 184 · see citing works
Mitochondrial Generation of Oxygen Radicals During Reoxygenation of Ischemic Tissues
Turrens, J. F., Beconi, M., Barilla, J., Chavez, U. B., & McCord, J. M. (1991) · Free Radical Research Communications · doi:10.3109/10715769109145847 · Cited by 177 · see citing works
Nakano, A., Cohen, M. V., & Downey, J. M. (2000) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(00)00058-9 · Cited by 164 · see citing works
Reactive oxygen species function as second messenger during ischemic preconditioning of heart
Das, D. K., Maulik, N., Sato, M., & Ray, P. S. (1999) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006966128795 · Cited by 164 · see citing works
Vanden Hoek, T. L., Shao, Z., Li, C., Schumacker, P. T., & Becker, L. B. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1997.0481 · Cited by 161 · cited 1× · see citing works
“In one study, the mKATP channel opener nicorandil enhanced postischemic supply of high-energy phosphates and decreased oxidant injury (35); both factors are consistent with improved ETC function and with evidence that the mitochondrion is the most likely source of ROS during ischemia (44, 47).”
BackgroundTanaka, M., Fujiwara, H., Yamasaki, K., & Sasayama, S. (1994) · Cardiovascular Research · doi:10.1093/cvr/28.7.980 · Cited by 143 · see citing works
WeinaChen, ScottGabel, CharlesSteenbergen, & ElizabethMurphy (1995) · Circulation Research · Cited by 142 · see citing works
Nakagawa, Y., Ito, H., Kitakaze, M., Kusuoka, H., Hori, M., Kuzuya, T., Higashino, Y., Fujii, K., & Minamino, T. (1995) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(94)00542-x · Cited by 139 · see citing works
Chen, W., Gabel, S. A., Steenbergen, C., & Murphy, E. (1995) · Circulation Research · doi:10.1161/01.res.77.2.424 · Cited by 135 · see citing works
Sun, J. Z., Kaur, H., Halliwell, B. B., Li, X. Y., & Bolli, R. (1993) · Circulation Research · doi:10.1161/01.res.73.3.534 · Cited by 126 · see citing works
IWAMOTO, T., Miura, T., Adachi, T., Noto, T., Ogawa, T., Tsuchida, A., & Iimura, O. (1991) · Circulation · doi:10.1161/01.cir.83.3.1015 · Cited by 111 · see citing works
Novalija, E., Varadarajan, S. G., Camara, A. K. S., An, J., Chen, Q., Riess, M. L., Hogg, N., & Stowe, D. F. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01056.2001 · Cited by 105 · see citing works
Self-citationAn, J., Varadarajan, S. G., Camara, A. K. S., Chen, Q., Novalija, E., Gross, G. J., & Stowe, D. F. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.6.h2398 · Cited by 94 · see citing works
Self-citationRiess, 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 · see citing works
Self-citationTósaki, Á., Cordis, G. A., Szerdahelyi, P., Engelman, R. M., & Das, D. K. (1994) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199403000-00002 · Cited by 89 · see citing works
Varadarajan, S. G., An, J., Novalija, E., Smart, S. C., & Stowe, D. F. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.1.h280 · Cited by 88 · see citing works
Self-citationOpenings of cardiac KATP channel by oxygen free radicals produced by xanthine oxidase reaction
Tokube, K., Kiyosue, T., & Arita, M. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.2.h478 · Cited by 81 · see citing works
An, J., Varadarajan, S. G., Novalija, E., & Stowe, D. F. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.4.h1508 · Cited by 77 · see citing works
Self-citationRiess, M. L., Camara, A. K. S., Novalija, E., Chen, Q., Rhodes, S. S., & Stowe, D. F. (2002) · Anesthesia & Analgesia · doi:10.1097/00000539-200212000-00013 · Cited by 76 · see citing works
Self-citationPreconditioning cultured human pediatric myocytes requires adenosine and protein kinase C
Ikonomidis, J. S., Shirai, T., Weisel, R. D., Derylo, B., Rao, V., Whiteside, C. I., Mickle, D. A. G., & Li, R. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.272.3.h1220 · Cited by 74 · see citing works
Tósaki, Á., Cordis, G. A., Szerdahelyi, P., et al. (1994) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199423030-00002 · Cited by 73 · see citing works
Evidence for the involvement of peroxynitrite in ischaemic preconditioning in rat isolated hearts
Altuǧ, S., Demiryürek, A. T., Kane, K. A., & Kanzık, İ. (2000) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0703280 · Cited by 72 · see citing works
Zhang, H., McPherson, B. C., Liu, H., Baman, T. S., Rock, P., & Yao, Z. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00683.2001 · Cited by 66 · see citing works
Bogoyevitch, M. A., Ng, D. C. H., Court, N. W., Draper, K. A., Dhillon, A. S., & Abas, L. (2000) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1187 · Cited by 62 · see citing works
Park, J.-W., Chun, Y.-S., Kim, Y., Kim, C., & Kim, M. (1997) · Life Sciences · doi:10.1016/s0024-3205(97)00236-1 · Cited by 55 · see citing works
Inhibition of DNA-ethidium bromide intercalation due to free radical attack upon DNA
Pr�tz, W. A. (1984) · Radiation and Environmental Biophysics · doi:10.1007/bf01326731 · Cited by 54 · see citing works
Inhibition of DNA-ethidium bromide intercalation due to free radical attack upon DNA
Pr�tz, W. A. (1984) · Radiation and Environmental Biophysics · doi:10.1007/bf01326732 · Cited by 49 · see citing works
Stowe, D. F., Varadarajan, S. G., An, J., & Smart, S. C. (2000) · Circulation · doi:10.1161/01.cir.102.10.1172 · Cited by 45 · see citing works
Self-citationIschaemic preconditioning is not mediated by oxygen derived free radicals in rats
Richard, V. J., Tron, C., & Thuillez, C. (1993) · Cardiovascular Research · doi:10.1093/cvr/27.11.2016 · Cited by 44 · see citing works
Hydroxyl radical production during myocardial ischemia and reperfusion in cats
O’Neill, C., Fu, L., Halliwell, B. B., & Longhurst, J. C. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.2.h660 · Cited by 42 · see citing works
Osada, M., Sato, T., Komori, S., & Tamura, K. (1991) · Cardiovascular Research · doi:10.1093/cvr/25.6.441 · Cited by 41 · see citing works
Menadione mimics the infarct-limiting effect of preconditioning in isolated rat hearts
Yue, Y., Krenz, M., Cohen, M. V., Downey, J. M., & Critz, S. D. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.2.h590 · Cited by 41 · see citing works
Preconditioning with hydrogen peroxide (H2O2) or ischemia in H2O2-induced cardiac dysfunction
Valen, G., Starkopf, J., Takeshima, S., Kullisaar, T., Vihalemm, T., Kengsepp, A., Löwbeer, C., Vaage, J., & Zilmer, M. (1998) · Free Radical Research · doi:10.1080/10715769800300271 · Cited by 39 · see citing works
Ischemic Preconditioning Decreases Oxidative Stress during Reperfusion: A Chemiluminescence Study
Crestanello, J. A., Lingle, D. M., Kamelgard, J. I., Millili, J. J., & Whitman, G. J. R. (1996) · Journal of Surgical Research · doi:10.1006/jsre.1996.0342 · Cited by 37 · see citing works
Horobin, R. W., & Rashid‐Doubell, F. (1990) · Histochemistry and Cell Biology · doi:10.1007/bf02440189 · Cited by 36 · see citing works
Nicorandil decreases postischemic actin oxidation
Schwalb, H., Olivson, A., Li, J., Houminer, E., Wahezi, S. E., Opie, L. H., Maulik, D., Borman, J. B., & Powell, S. R. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00620-7 · Cited by 19 · see citing works
In vivo EPR spectroscopy of free radicals in the heart.
Zweier, J. L., & Kuppusamy, P. (1994) · Environmental Health Perspectives · doi:10.1289/ehp.94102s1045 · Cited by 17 · see citing works
Flumazenil preconditions cardiomyocytes via oxygen radicals and KATPchannels
Zhang, Q., & Yao, Z. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.279.4.h1858 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mechanisms Underlying Acute Protection From Cardiac Ischemia-Reperfusion Injury
Murphy, E., & Steenbergen, C. (2008) · Physiological Reviews · doi:10.1152/physrev.00024.2007 · Cited by 1,472 · 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
Zhao, H., Kalivendi, S., Zhang, H., Joseph, J., Nithipatikom, K., Vásquez-Vivar, J., & Kalyanaraman, B. (2003) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(03)00142-4 · Cited by 803 · see citing works
New concepts in reactive oxygen species and cardiovascular reperfusion physiology
Becker, L. C. (2003) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.10.025 · Cited by 703 · see citing works
Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury
Vinten-Johansen, J. (2003) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.10.011 · Cited by 676 · see citing works
Kin, H. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.01.006 · Cited by 561 · see citing works
Ischemic preconditioning protects by activating prosurvival kinases at reperfusion
Hausenloy, D. J., Tsang, A., Mocanu, M. M., & Yellon, D. M. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00374.2004 · Cited by 512 · see citing works
Ovize, M., Baxter, G. F., Lisa, F. D., Ferdinandy, P., David Garcia-dorado, A., Hausenloy, D. J., Heusch, G., Vinten-Johansen, J., Yellon, D. M., & Schulz, R. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq129 · Cited by 502 · 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
Self-citationMitochondrial 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
Figueira, T. R., de Barros, M. H., Camargo, A. A., Castilho, R. F., Ferreira, J. C. B., Kowaltowski, A. J., Sluse, F. E., de Souza-Pinto, N. C., & Vercesi, A. E. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4729 · Cited by 417 · see citing works
Fukuda, K.-I., Asoh, S., Ishikawa, M., Yamamoto, Y., Ohsawa, I., & Ohta, S. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.07.088 · Cited by 413 · see citing works
Hypoxia-induced reactive oxygen species formation in skeletal muscle
Clanton, T. L. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01298.2006 · Cited by 401 · 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
The Role of Oxidative Stress in Cardiac Disease: From Physiological Response to Injury Factor
D’Oria, R., Schipani, R., Leonardini, A., Natalicchio, A., Perrini, S., Cignarelli, A., Laviola, L., & Giorgino, F. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/5732956 · Cited by 387 · 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
Ischemia/Reperfusion Injury in Kidney Transplantation: Mechanisms and Prevention
Kosieradzki, M., & Rowinski, W. A. (2008) · Transplantation Proceedings · doi:10.1016/j.transproceed.2008.10.004 · Cited by 326 · 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
Role of Oxidative Stress in Reperfusion following Myocardial Ischemia and Its Treatments
Xiang, M., Lu, Y., Xin, L., Gao, J., Shang, C., Jiang, Z., Lin, H., Fang, X., Qu, Y., Wang, Y., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/6614009 · Cited by 301 · see citing works
Sun, H.-Y., Wang, N.-P., Kerendi, F., Halkos, M. E., Kin, H., Guyton, R. A., Vinten‐Johansen, J., & Zhao, Z. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01244.2003 · Cited by 283 · 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
Chen, Q., Camara, A. K. S., Stowe, D. F., Hoppel, C. L., & Lesnefsky, E. J. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00270.2006 · Cited by 271 · see citing works
Self-citationThe mitochondrial permeability transition pore as a target for preconditioning and postconditioning
Hausenloy, D. J., Ong, S., & Yellon, D. M. (2009) · Basic Research in Cardiology · doi:10.1007/s00395-009-0010-x · Cited by 268 · see citing works
Autophagy During Cardiac Stress: Joys and Frustrations of Autophagy
Gottlieb, R. A., & Mentzer, R. M. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135757 · Cited by 267 · 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
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
Oxidative Stress and Left Ventricular Function with Chronic Intermittent Hypoxia in Rats
Chen, L., Einbinder, E., Zhang, Q., Hasday, J. D., Balke, C. W., & Scharf, S. M. (2005) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200504-560oc · Cited by 237 · see citing works
Hermes‐Lima, M., Moreira, D. C., Rivera‐Ingraham, G. A., Giraud‐Billoud, M., Genaro‐Mattos, T. C., & Campos, E. G. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.07.156 · Cited by 241 · see citing works
Postconditioning A new link in nature’s armor against myocardial ischemia–reperfusion injury
Vinten-Johansen, J., Zhao, Z., Zatta, A. J., Kin, H., Halkos, M. E., & Kerendi, F. (2005) · Basic Research in Cardiology · doi:10.1007/s00395-005-0523-x · Cited by 224 · see citing works
Cardioprotection: A radical view
Penna, C. R. R., Mancardi, D., Rastaldo, R., & Pagliaro, P. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.02.008 · Cited by 219 · see citing works
HANLEY, P., & DAUT, J. (2005) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2005.04.002 · Cited by 218 · see citing works
Chen, Q., Moghaddas, S., Hoppel, C. L., & Lesnefsky, E. J. (2006) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.110262 · Cited by 215 · see citing works
Dröse, S. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.01.004 · Cited by 201 · see citing works
Mechanism of Cardioprotection by Early Ischemic Preconditioning
Yang, X., Cohen, M. V., & Downey, J. M. (2010) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-010-6236-x · Cited by 201 · see citing works
Kevin, L. G., Novalija, E., & Stowe, D. F. (2005) · Anesthesia & Analgesia · doi:10.1213/01.ane.0000180999.81013.d0 · Cited by 197 · see citing works
Self-citationPotential Therapeutic Benefits of Strategies Directed to Mitochondria
Camara, A. K. S., Lesnefsky, E. J., & Stowe, D. F. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2788 · Cited by 195 · see citing works
Self-citationCardioprotective 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
Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance
Sack, M. N. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.07.010 · Cited by 185 · see citing works
Myocardial protection with postconditioning is not enhanced by ischemic preconditioning
Halkos, M. E., Kerendi, F., Corvera, J. S., Wang, N.-P., Kin, H., Payne, C. S., Sun, H.-Y., Guyton, R. A., Vinten‐Johansen, J., & Zhao, Z. (2004) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2004.03.033 · Cited by 182 · see citing works
Penna, C. R. R., Perrelli, M.-G., & Pagliaro, P. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4459 · Cited by 182 · see citing works
α-Ketoglutarate dehydrogenase: A mitochondrial redox sensor
McLain, A. L., Szweda, P. A., & Szweda, L. I. (2010) · Free Radical Research · doi:10.3109/10715762.2010.534163 · Cited by 170 · see citing works
Clarke, S. J., Халиулин, И. Г., Das, M., Parker, J. E., Heesom, K. J., & Halestrap, A. P. (2008) · Circulation Research · doi:10.1161/circresaha.107.167072 · Cited by 163 · see citing works
Hydrogen sulfide and ischemia–reperfusion injury
Nicholson, C. K., & Calvert, J. W. (2010) · Pharmacological Research · doi:10.1016/j.phrs.2010.06.002 · Cited by 158 · see citing works
The role of succinate and ROS in reperfusion injury – A critical appraisal
Andrienko, T., Pasdois, P., Pereira, G. C., Ovens, M. J., & Halestrap, A. P. (2017) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2017.06.016 · Cited by 158 · see citing works
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 · see citing works
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 150 · see citing works
Self-citationMiller, S., Yan, E. B., Castillo-Meléndez, M., Jenkin, G., & Walker, D. W. (2005) · Developmental Neuroscience · doi:10.1159/000085993 · Cited by 149 · see citing works
Hoerter, J. A., González‐Barroso, M. M., Couplan, E., Matéo, P., Gelly, C., Cassard, A., Diolez, P., & Bouillaud, F. (2004) · Circulation · doi:10.1161/01.cir.0000137824.30476.0e · Cited by 149 · see citing works
Redox Control of Protein Kinase C: Cell- and Disease-Specific Aspects
Giorgi, C., Agnoletto, C., Baldini, C., Bononi, A., Bonora, M., Marchi, S., Missiroli, S., Patergnani, S., Poletti, F., Rimessi, A., et al. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2825 · Cited by 146 · see citing works
Paradies, G., Paradies, V., Ruggiero, F. M., & Petrosillo, G. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00028.2018 · Cited by 143 · see citing works
Chen, Q., Hoppel, C. L., & Lesnefsky, E. J. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.091702 · Cited by 140 · see citing works
Yang, K., Bonini, M. G., & Dudley, S. C. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.03.033 · Cited by 139 · see citing works
Lesnefsky, E. J., Chen, Q., Slabe, T. J., Stoll, M. S. K., Minkler, P. E., Hassan, M. O., Tandler, B., & Hoppel, C. L. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00348.2003 · Cited by 135 · see citing works
Stowe, D. F., Aldakkak, M., Camara, A. K. S., Riess, M. L., Heinen, A., Varadarajan, S. G., & Jiang, M.-T. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00763.2005 · Cited by 136 · see citing works
Self-citationROS Control Mitochondrial Motility through p38 and the Motor Adaptor Miro/Trak
Debattisti, V., Gerencser, A. A., Saotome, M., Das, S., & Hajnóczky, G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.060 · Cited by 132 · see citing works
Pasdois, P., Parker, J. E., Griffiths, E. J., & Halestrap, A. P. (2011) · Biochemical Journal · doi:10.1042/bj20101957 · Cited by 127 · see citing works
Heinen, A., Camara, A. K. S., Aldakkak, M., Rhodes, S. S., Riess, M. L., & Stowe, D. F. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00215.2006 · Cited by 127 · see citing works
Self-citationMitochondrial dysfunction as the cause of the failure to precondition the diabetic human myocardium
HASSOUNA, A., Loubani, M., Matata, B. M., FOWLER, A., Standen, N. B., & Galiñanes, M. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2005.11.004 · Cited by 123 · see citing works
Ischemia–reperfusion injury in the aged heart: role of mitochondria
Lesnefsky, E. J., & Hoppel, C. L. (2003) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2003.09.046 · Cited by 122 · see citing works
Chen, Q., & Lesnefsky, E. J. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.10.043 · Cited by 119 · see citing works
Riess, M. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.09.016 · Cited by 118 · see citing works
Self-citationSzczepanek, K., Chen, Q., Larner, A. C., & Lesnefsky, E. J. (2012) · Mitochondrion · doi:10.1016/j.mito.2011.08.011 · Cited by 117 · see citing works
Aldakkak, M., Camara, A. K. S., Heisner, J. S., Yang, M., & Stowe, D. F. (2011) · Pharmacological Research · doi:10.1016/j.phrs.2011.06.018 · Cited by 116 · see citing works
Self-citationReactive oxygen species formation in the transition to hypoxia in skeletal muscle
Zuo, L., & Clanton, T. L. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00449.2004 · Cited by 113 · see citing works
Leng, Y., Wu, Y., Lei, S., Zhou, B., Qiu, Z., Wang, K., & Xia, Z. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/9494052 · Cited by 108 · see citing works
Yue, D., Yan, L., Luo, H., Xu, X., & Jin, X. (2009) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2009.08.004 · Cited by 108 · see citing works
Aldakkak, M., Stowe, D. F., Chen, Q., Lesnefsky, E. J., & Camara, A. K. S. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2007.08.008 · Cited by 108 · see citing works
Self-citationThe role of mitochondrial membrane potential in ischemic heart failure
Kadenbach, B., Ramzan, R., Moosdorf, R., & Vogt, S. K. (2011) · Mitochondrion · doi:10.1016/j.mito.2011.06.001 · Cited by 103 · see citing works
Probing cytochrome c in living mitochondria with surface-enhanced Raman spectroscopy
Brazhe, N. A., Evlyukhin, A. B., Goodilin, E. A., Semenova, A. A., Novikov, S. M., Bozhevolnyi, S. I., Chichkov, B. N., Sarycheva, A. S., Байжуманов, А. А., Nikelshparg, E. I., et al. (2015) · Scientific Reports · doi:10.1038/srep13793 · Cited by 103 · see citing works
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 · see citing works
The Ryanodine Receptors Ca2 + Release Channels: Cellular Redox Sensors?
Hidalgo, C., Donoso, P., & Carrasco, M. A. (2005) · IUBMB Life · doi:10.1080/15216540500092328 · Cited by 102 · see citing works
Ischemic Preconditioning: From Molecular Mechanisms to Therapeutic Opportunities
Otani, H. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1679 · Cited by 101 · see citing works
Yeung, H. M., Hung, M., Lau, C. G., & Fung, M. (2014) · Journal of Pineal Research · doi:10.1111/jpi.12190 · Cited by 99 · see citing works
Kim, J., Jang, H., & Park, K. M. (2009) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00474.2009 · Cited by 98 · see citing works
Subudhi, U., Das, K., Paital, B., Bhanja, S., & Chainy, G. B. N. (2008) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2008.02.005 · Cited by 96 · see citing works
The Heart As a Target for Xenobiotic Toxicity: The Cardiac Susceptibility to Oxidative Stress
Costa, V. M., Carvalho, F. D., Duarte, J. A., Bastos, M. D. L., & Remião, F. (2013) · Chemical Research in Toxicology · doi:10.1021/tx400130v · Cited by 96 · see citing works
Klein, L. E., Cui, L., Gong, Z., Su, K., & Muzumdar, R. H. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.08.055 · Cited by 95 · see citing works
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 91 · see citing works
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 · see citing works
Mitochondrial Complex I Inhibition by Metformin Limits Reperfusion Injury
Mohsin, A. A., Chen, Q., Quan, N., Rousselle, T. V., Maceyka, M. W., Samidurai, A., Thompson, J., Hu, Y., Li, J., & Lesnefsky, E. J. (2019) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.118.254300 · Cited by 87 · see citing works
Inflammation, Proinflammatory Mediators and Myocardial Ischemia–reperfusion Injury
Vinten‐Johansen, J., Jiang, R., Reeves, J. G., Mykytenko, J., Deneve, J., & Jobe, L. J. (2007) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2006.11.010 · Cited by 86 · see citing works
Oxidative modification of hepatic mitochondria protein thiols: effect of chronic alcohol consumption
Venkatraman, A., Landar, A., Davis, A. J., Ulasova, E., Page, G., Murphy, M. P., Darley-Usmar, V., & Bailey, S. M. (2004) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00399.2003 · Cited by 85 · see citing works
Stowe, D. F., Gadicherla, A. K., Zhou, Y., Aldakkak, M., Cheng, Q., Kwok, W., Jiang, M. T., Heisner, J. S., Yang, M., & Camara, A. K. S. (2012) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2012.08.031 · Cited by 85 · see citing works
Self-citationCardiolipin as an oxidative target in cardiac mitochondria in the aged rat
Lesnefsky, E. J., & Hoppel, C. L. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.05.444 · Cited by 83 · see citing works
Alleman, R. J., Katunga, L. A., Nelson, M. A. M., Brown, D. A., & Anderson, E. J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00358 · Cited by 84 · see citing works
García, S., Henry, T. D., Wang, Y. L., Chavez, I. J., Pedersen, W. R., Lesser, J. R., Shroff, G. R., Moore, L., & Traverse, J. H. (2010) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-010-9252-0 · Cited by 83 · see citing works
Mitochondria “THE” target of myocardial conditioning
Boengler, K., Lochnit, G., & Schulz, R. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00124.2018 · Cited by 82 · see citing works
Hausenloy, D. J. (2013) · Current Pharmaceutical Design · doi:10.2174/1381612811319250004 · Cited by 81 · see citing works
Hypothermia augments reactive oxygen species detected in the guinea pig isolated perfused heart
Camara, A. K. S., Riess, M. L., Kevin, L. G., Novalija, E., & Stowe, D. F. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00811.2003 · Cited by 81 · see citing works
Self-citationCatalytic Coupling of Oxidative Phosphorylation, ATP Demand, and Reactive Oxygen Species Generation
Bazil, J. N., Beard, D. A., & Vinnakota, K. C. (2016) · Biophysical Journal · doi:10.1016/j.bpj.2015.09.036 · Cited by 81 · see citing works
Regulation of Cellular Gas Exchange, Oxygen Sensing, and Metabolic Control
Clanton, T. L., Hogan, M. C., & Gladden, L. B. (2013) · Comprehensive physiology · doi:10.1002/cphy.c120030 · Cited by 88 · see citing works
Mitochondria and GSK-3β in Cardioprotection Against Ischemia/Reperfusion Injury
Miura, T., & Tanno, M. (2010) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-010-6234-z · Cited by 79 · see citing works
Immediate postconditioning during reperfusion attenuates intestinal injury
Liu, K., Li, Y., Huang, W., Chen, S.-Q., Wang, Z., Liu, J., & Xia, Z. (2009) · Intensive Care Medicine · doi:10.1007/s00134-009-1428-1 · Cited by 78 · see citing works
Flavonoids and mitochondrial pharmacology: A new paradigm for cardioprotection
Testai, L. (2015) · Life Sciences · doi:10.1016/j.lfs.2015.04.017 · Cited by 77 · see citing works
Mitochondrial Potassium Channels as Pharmacological Target for Cardioprotective Drugs
Testai, L., Rapposelli, S., Martelli, A., Breschi, M. C., & Calderone, V. (2014) · Medicinal Research Reviews · doi:10.1002/med.21332 · Cited by 74 · see citing works
Use of Nicorandil in Cardiovascular Disease and Its Optimization
Horinaka, S. (2011) · Drugs · doi:10.2165/11592300-000000000-00000 · Cited by 74 · see citing works
Novel therapeutic strategies for cardioprotection
Sluijter, J. P. G., Condorelli, G., Davidson, S. M., Engel, F. B., Ferdinandy, P., Hausenloy, D. J., Lecour, S., Madonna, R., Ovize, M., Ruiz‐Meana, M., et al. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.05.005 · Cited by 73 · see citing works
Daiber, A., Andreadou, I., Oelze, M. W., Davidson, S. M., & Hausenloy, D. J. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.12.026 · Cited by 73 · see citing works
Extracellular superoxide enhances 5-HT-induced murine pulmonary artery vasoconstriction
Liu, J. Q., & Folz, R. J. (2004) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00006.2004 · Cited by 70 · see citing works
Nuclear-encoded mitochondrial proteins and their role in cardioprotection
Boengler, K., Heusch, G., & Schulz, R. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.01.009 · Cited by 68 · see citing works
- Authors
- Kevin, L. G., Camara, A. K. S., Riess, M. L., Novalija, E., & Stowe, D. F.
- Affiliations
- Anesthesiology Research Laboratories, Departments ofAnesthesiology and
- Medical College of Wisconsin (US)
- Venue
- American Journal of Physiology-Heart and Circulatory Physiology
- Publisher
- American Physiological Society
- Published
- 2003-02-01
- Volume
- 284
- Issue
- 2
- Pages
- H566-H574
- ISSN
- 0363-6135 (ISSN-L)
- 1522-1539
- OpenAlex
- W2079438155
- Cited by
- 272
- References
- 56
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 4 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 4 · 2019: 9 · 2018: 9 · 2017: 15 · 2016: 7 · 2015: 15 · 2014: 15 · 2013: 9 · 2012: 12
- FWCI
- 11.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Heart and Circulatory Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL 58691, R01HL058691)
- National Institute of General Medical Sciences (GM-8204-06)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Health Sciences › Medicine › Surgery › Organ Transplantation Techniques and Outcomes
- Keywords
- ischemic preconditioning, reactive oxygen species, superoxide, myocardial ischemia-reperfusion injury, MnTBAP, dihydroethidium, cardioprotection, myocardial infarction, guinea pig heart
- MeSH terms
- Animals, Computer Systems, Ethidium, Guinea Pigs, Myocardial Infarction, Myocardium, Spectrometry, Fluorescence, Myocardial Reperfusion Injury, Myocardial Ischemia, Reactive Oxygen Species, Ischemic Preconditioning, Myocardial, 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
