ROS scavenging before 27°C ischemia protects hearts and reduces mitochondrial ROS, Ca2+ overload, and changes in redox state

Camara, Amadou K. S.; Aldakkak, Mohammed; Heisner, James S.; Rhodes, Samhita S.; Riess, Matthias L.; An, JiangZhong; Heinen, André; Stowe, David F.

doi:10.1152/ajpcell.00231.2006

Cited by 42Cardiac Ischemia and ReperfusionNitric Oxide and Endothelin EffectsTransplantation: Methods and Outcomes

ROS scavenging before 27°C ischemia protects hearts and reduces mitochondrial ROS, Ca2+ overload, and changes in redox state

Camara, Amadou K. S., Aldakkak, Mohammed, Heisner, James S., Rhodes, Samhita S., Riess, Matthias L., An, JiangZhong, Heinen, André, Stowe, David F.·2007·American Journal of Physiology-Cell Physiology

DOI 10.1152/ajpcell.00231.2006

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Abstract

We have shown that cold perfusion of hearts generates reactive oxygen and nitrogen species (ROS/RNS). In this study, we determined 1) whether ROS scavenging only during cold perfusion before global ischemia improves mitochondrial and myocardial function, and 2) which ROS leads to compromised cardiac function during ischemia and reperfusion (I/R) injury. Using fluorescence spectrophotometry, we monitored redox balance (NADH and FAD), O 2•− levels and mitochondrial Ca 2+ (m[Ca 2+]) at the left ventricular wall in 120 guinea pig isolated hearts divided into control (Con), MnTBAP (a superoxide dismutase 2 mimetic), MnTBAP (M) + catalase (C) + glutathione (G) (MCG), C+G (CG), and N G-nitro-l-arginine methyl ester (l-NAME; a nitric oxide synthase inhibitor) groups. After an initial period of warm perfusion, hearts were treated with drugs before and after at 27°C. Drugs were washed out before 2 h at 27°C ischemia and 2 h at 37°C reperfusion. We found that on reperfusion the MnTBAP group had the worst functional recovery and largest infarction with the highest m[Ca 2+], most oxidized redox state and increased ROS levels. The MCG group had the best recovery, the smallest infarction, the lowest ROS level, the lowest m[Ca 2+], and the most reduced redox state. CG and l-NAME groups gave results intermediate to those of the MnTBAP and MCG groups. Our results indicate that the scavenging of cold-induced O 2•− species to less toxic downstream products additionally protects during and after cold I/R by preserving mitochondrial function. Because MnTBAP treatment showed the worst functional return along with poor preservation of mitochondrial bioenergetics, accumulation of H 2 O 2 and/or hydroxyl radicals during cold perfusion may be involved in compromised function during subsequent cold I/R injury.

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Other damaging effects of ROS are on the respiratory complexes, most at complex I and least at complex IV.
“Other damaging effects of ROS are on the respiratory complexes, most at complex I and least at complex IV (66).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [66]

Mitochondrial free radical generation, oxidative stress, and aging
Cadenas, E., & Davies, K. J. A. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00317-8 · Cited by 3,010 · see citing works
Production of Reactive Oxygen Species by Mitochondria
Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L., & Lesnefsky, E. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304854200 · Cited by 1,616 · see citing works
PRINCIPLES OF SOLID-ORGAN PRESERVATION BY COLD STORAGE
Belzer, F. O., & Southard, J. H. (1988) · Transplantation · doi:10.1097/00007890-198804000-00001 · Cited by 1,388 · see citing works
Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: Potential implications in intracellular fluorescence detection of superoxide
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
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
Di Lisa, F., Menabò, R., Canton, M., Barile, M., & Bernardi, P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m006825200 · Cited by 678 · 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
Significant Levels of Oxidants are Generated by Isolated Cardiomyocytes During Ischemia Prior to Reperfusion
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
Myocardial alterations due to free-radical generation
Burton, K. P., McCord, J. M., & Ghai, G. R. (1984) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1984.246.6.h776 · Cited by 305 · see citing works
Ischemic preconditioning alters real-time measure of O<sub>2</sub> radicals in intact hearts with ischemia and reperfusion
Kevin, L. G., Camara, A. K. S., Riess, M. L., Novalija, E., & Stowe, D. F. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00711.2002 · Cited by 272 · see citing works
Self-citation
Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential
Ku, H., & Sohal, R. S. (1993) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(93)90132-b · Cited by 240 · see citing works
Reactive oxygen species from smooth muscle mitochondria initiate cold-induced constriction of cutaneous arteries
Bailey, S. R., Mitra, S., Flavahan, S., & Flavahan, N. A. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01305.2004 · Cited by 212 · see citing works
Selective Loading of Rhod 2 into Mitochondria Shows Mitochondrial Ca2+Transients during the Contractile Cycle in Adult Rabbit Cardiac Myocytes
Trollinger, D. R., Cascio, W. E., & Lemasters, J. J. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7042 · Cited by 199 · see citing works
Chronic cold exposure affects the antioxidant defense system in various rat tissues
Kaushik, S., & Kaur, J. (2003) · Clinica Chimica Acta · doi:10.1016/s0009-8981(03)00171-2 · Cited by 194 · see citing works
Reactive oxygen species in tissue injury.
de Groot, H. (1994) · PubMed · Cited by 184 · see citing works
The Integration of Mitochondrial Calcium Transport and Storage
Nicholls, D. G., & Chalmers, S. (2004) · Journal of Bioenergetics and Biomembranes · doi:10.1023/b:jobb.0000041753.52832.f3 · Cited by 162 · see citing works
Cold‐induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle
Toyomizu, M., Ueda, M., Sato, S., Seki, Y., Sato, K., & Akiba, Y. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03395-1 · Cited by 143 · see citing works
Reduced reactive O2 species formation and preserved mitochondrial NADH and [Ca2+] levels during short-term 17 °C ischemia in intact hearts
Riess, M. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.09.016 · Cited by 118 · see citing works
Self-citation
Mild intraischemic hypothermia suppresses consumption of endogenous antioxidants after temporary focal ischemia in rats
Karibe, H., Chen, S. F., Zarow, G. J., Gafni, J., Graham, S. H., Chan, P. H., & Weinstein, P. R. (1994) · Brain Research · doi:10.1016/0006-8993(94)91043-x · Cited by 101 · see citing works
Increased work in cardiac trabeculae causes decreased mitochondrial NADH fluorescence followed by slow recovery
Brandes, R. P., & Bers, D. M. (1996) · Biophysical Journal · doi:10.1016/s0006-3495(96)79303-7 · Cited by 98 · see citing works
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 · see citing works
Self-citation
Nitric oxide kinetics during hypoxia in proximal tubules: Effects of acidosis and glycine
Yaqoob, M. M., Edelstein, C. L., Wieder, E., Alkhunaizi, A. M., Gengaro, P. E., Nemenoff, R. A., & Schrier, R. W. (1996) · Kidney International · doi:10.1038/ki.1996.187 · Cited by 92 · see citing works
Changes in [Na+]i, compartmental [Ca2+], and NADH with dysfunction after global ischemia in intact hearts
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-citation
The effect of hypothermia on H2O2 production during ischemia and reperfusion: a microdialysis study in the gerbil hippocampus
Lei, B., Adachi, N., & Arai, T. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)13349-3 · Cited by 87 · see citing works
Cold-Induced Release of Reactive Oxygen Species as a Decisive Mediator of Hypothermia Injury to Cultured Liver Cells
Rauen, U., & de GROOT, H. (1998) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(97)00456-5 · Cited by 84 · 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-citation
Mammalian Cell Injury Induced by Hypothermia the Emerging Role for Reactive Oxygen Species
Rauen, U., & de GROOT, H. (2002) · Biological Chemistry · doi:10.1515/bc.2002.050 · Cited by 79 · see citing works
Anesthetic Preconditioning Attenuates Mitochondrial Ca2+ Overload During Ischemia in Guinea Pig Intact Hearts: Reversal by 5-Hydroxydecanoic Acid
Riess, 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-citation
Myocardial temperature reduction attenuates necrosis after prolonged ischemia in rabbits
Hale, S. (1998) · Cardiovascular Research · doi:10.1016/s0008-6363(98)00191-6 · Cited by 74 · see citing works
Quantitation of cytosolic [Ca2+] in whole perfused rat hearts using Indo-1 fluorometry
Brandes, R. P., Figueredo, V. M., Camacho, S. A., Baker, A. J., & Weiner, M. W. (1993) · Biophysical Journal · doi:10.1016/s0006-3495(93)81274-8 · Cited by 68 · see citing works
Cold-induced apoptosis in isolated rat hepatocytes: protective role of glutathione
Vairetti, M., Griffini, P., Pietrocola, G., Richelmi, P., & Freitas, I. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00670-0 · Cited by 63 · see citing works
Modulation of myocardial function and [Ca2+] sensitivity by moderate hypothermia in guinea pig isolated hearts
Stowe, D. F., Fujita, S., An, J., Paulsen, R. A., Varadarajan, S. G., & Smart, S. C. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.277.6.h2321 · Cited by 58 · see citing works
Self-citation
Effect of low temperature on the cytosolic free Ca2+ in rat ventricular myocytes
Liu, B., Wang, L. C. H., & Belke, D. D. (1991) · Cell Calcium · doi:10.1016/0143-4160(91)90080-x · Cited by 57 · see citing works
Oxygen-free radical-mediated injury to cultured rat hepatocytes during cold incubation in preservation solutions
Rauen, U., Reuters, I., Fuchs, A., & de GROOT, H. (1997) · Hepatology · doi:10.1002/hep.510260215 · Cited by 56 · see citing works
Protective effect of the SOD/catalase mimetic MnTMPyP on inflammation-mediated dopaminergic neurodegeneration in mesencephalic neuronal-glial cultures
Wang, T., Liu, B., Qin, L., Wilson, B. C., & Hong, J. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2003.10.040 · Cited by 51 · see citing works
Reduced Cytosolic Ca 2+ Loading and Improved Cardiac Function After Cardioplegic Cold Storage of Guinea Pig Isolated Hearts
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-citation
COLD PRESERVATION OF ISOLATED RABBIT PROXIMAL TUBULES INDUCES RADICAL-MEDIATED CELL INJURY1
Peters, S. M. A., Rauen, U., Tijsen, M. J. H., Bindels, R. J. M., van Os, C. H., de GROOT, H., & Wetzels, J. F. M. (1998) · Transplantation · doi:10.1097/00007890-199803150-00005 · Cited by 44 · see citing works
Warm ischemic preconditioning improves mitochondrial redox balance during and after mild hypothermic ischemia in guinea pig isolated hearts
An, J., Camara, A. K. S., Rhodes, S. S., Riess, M. L., & Stowe, D. F. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01124.2004 · Cited by 33 · see citing works
Self-citation
Effects of warm and cold ischemia on mitochondrial functions in brain, liver and kidney
Baumann, M., Bender, E., S�mmer, G., Gross, G., & Brand, K. (1989) · Molecular and Cellular Biochemistry · doi:10.1007/bf00219256 · Cited by 24 · see citing works
Na+/H+ Exchange Inhibition with Cardioplegia Reduces Cytosolic [Ca2+] and Myocardial Damage after Cold Ischemia
Camara, A. K. S., An, J., Chen, Q., Novalija, E., Varadarajan, S. G., Schelling, P., & Stowe, D. F. (2003) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-200305000-00004 · Cited by 23 · see citing works
Self-citation
Factors influencing survival of mammalian cells exposed to hypothermia
Zieger, M. A. J., Glofcheski, D. J., Lepock, J. R., & Kruuv, J. (1990) · Cryobiology · doi:10.1016/0011-2240(90)90022-v · Cited by 22 · see citing works
Factors influencing survival of mammalian cells exposed to hypothermia
Zieger, M. A. J., Glofcheski, D. J., Lepock, J. R., & Kruuv, J. (1991) · Cryobiology · doi:10.1016/0011-2240(91)90003-7 · Cited by 22 · see citing works
Cardiac preconditioning with 4-h, 17°C ischemia reduces [Ca2+]iload and damage in part via KATPchannel opening
Chen, Q., Camara, A. K. S., An, J., Riess, M. L., Novalija, E., & Stowe, D. F. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01032.2001 · Cited by 21 · see citing works
Self-citation
Deep hypothermia during ischemia improves functional recovery and reduces free-radical generation in isolated reperfused rat heart
Gambert, S., Bès-Houtmann, S., Vandroux, D., Tissier, C., Vergely, C., Rochette, L., & Athias, P. (2004) · The Journal of Heart and Lung Transplantation · doi:10.1016/s1053-2498(03)00211-0 · Cited by 19 · see citing works
Oxygen Free Radicals in Cardiac Transplantation
Keith, F. M. (1993) · Journal of Cardiac Surgery · doi:10.1111/j.1540-8191.1993.tb01317.x · Cited by 19 · see citing works
Improved Mitochondrial Bioenergetics by Anesthetic Preconditioning During and After 2 Hours of 27°C Ischemia in Isolated Hearts
An, J., Camara, A. K. S., Riess, M. L., Rhodes, S. S., Varadarajan, S. G., & Stowe, D. F. (2005) · Journal of Cardiovascular Pharmacology · doi:10.1097/01.fjc.0000175238.18702.40 · Cited by 16 · see citing works
Self-citation
THE ROLE OF A HYDROXYL RADICAL SCAVENGER (NICARAVEN) IN RECOVERY OF CARDIAC FUNCTION FOLLOWING PRESERVATION AND REPERFUSION1
Ku, K., Kin, S., Hashimoto, M., Saitoh, Y., Nosaka, S., Iwasaki, S., Alam, M. S., & Nakayama, K. (1996) · Transplantation · doi:10.1097/00007890-199610270-00012 · Cited by 16 · see citing works
How Inotropic Drugs Alter Dynamic and Static Indices of Cyclic Myoplasmic [Ca2+] to Contractility Relationships in Intact Hearts
Rhodes, S. S., ROPELLA, K. M., Camara, A. K. S., Chen, Q., Riess, M. L., & Stowe, D. F. (2003) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-200310000-00013 · Cited by 15 · see citing works
Self-citation
Effects of l -Arginine andNω-Nitro- l -Arginine Methyl Ester on Cardiac Perfusion and Function After 1-Day Cold Preservation of Isolated Hearts
Stowe, D. F., Boban, M., Roerig, D. L., Chang, D., Palmisano, B. W., & Bosnjak, Z. J. (1997) · Circulation · doi:10.1161/01.cir.95.6.1623 · Cited by 10 · see citing works
Self-citation
Effects of oxidant exposure on substrate utilization and high-energy phosphates in isolated rat hearts.
Burton, K. P., Jones, J. G., Le, T. H., Sherry, A. D., & Malloy, C. R. (1994) · Circulation Research · doi:10.1161/01.res.75.1.97 · Cited by 9 · see citing works
Optimal storage temperature and benefit of hypothermic cardioplegic arrest for long-term preservation of donor hearts: a study in the dog
Minten, J., Flameng, W. J., & Dyszkiewicz, W. (1988) · Transplant International · doi:10.1007/bf00337844 · Cited by 7 · see citing works
Exposure to free radicals alters ionic calcium transients in isolated adult rat cardiac myocytes.
Kp, B., Hk, H., & Nazeran, H. (1992) · PubMed · Cited by 6 · see citing works
Optimal storage temperature and benefit of hypothermic cardioplegic arrest for long-term preservation of donor hearts: a study in the dog
Minten, J., Flameng, W. J., & Dyszkiewicz, W. (1988) · Transplant International · doi:10.1111/j.1432-2277.1988.tb01774.x · Cited by 6 · see citing works
Effect of sodium nitroprusside and L-arginine methyl ester on rat hearts stored at 4 °C for 24 h
FAGBEMI, O. S., & Northover, B. J. (1998) · Clinical Science · doi:10.1042/cs0950557 · Cited by 3 · see citing works

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Authors: Camara, A. K. S., Aldakkak, M., Heisner, J. S., Rhodes, S. S., Riess, M. L., An, J., Heinen, A., & Stowe, D. F.
Affiliations: Medical College of Wisconsin (US)
ORCID: Camara, Amadou K. S.
Aldakkak, Mohammed
Riess, Matthias L.
Heinen, André
Stowe, David F.
Venue: American Journal of Physiology-Cell Physiology
Publisher: American Physiological Society
Published: 2007-06
Volume: 292
Issue: 6
Pages: C2021-C2031
ISSN: 0363-6143 (ISSN-L)
1522-1563
DOI: 10.1152/ajpcell.00231.2006
OpenAlex: W2113073611
Cited by: 42
References: 52
Citations by year: 2025: 2 · 2024: 1 · 2023: 1 · 2022: 2 · 2020: 3 · 2018: 3 · 2017: 2 · 2016: 1 · 2015: 2 · 2014: 4 · 2013: 4 · 2012: 3
FWCI: 1.89
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Cell Physiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Heart, Lung, and Blood Institute (K01HL073246, HL073246-01)
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 › Transplantation: Methods and Outcomes
Keywords: reactive oxygen species, cold ischemia, ischemia-reperfusion injury, superoxide radical scavenging, MnTBAP, catalase, glutathione, nitric oxide synthase inhibition, mitochondrial calcium overload, mitochondrial redox state, myocardial infarction, hydrogen peroxide, hydroxyl radicals, cardioprotection, isolated heart
MeSH terms: Animals, Calcium, Catalase, Female, Glutathione, Guinea Pigs, Ischemia, Male, Manganese, Mitochondria, Heart, Oxidation-Reduction, Temperature, Time Factors, Free Radical Scavengers, Reactive Oxygen Species, NG-Nitroarginine Methyl Ester

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ROS scavenging before 27°C ischemia protects hearts and reduces mitochondrial ROS, Ca2+ overload, and changes in redox state

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