Cited by 484Cardiac Ischemia and ReperfusionOrgan Transplantation Techniques and OutcomesNitric Oxide and Endothelin Effects

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Oxygen Radicals Released During Ischemic Preconditioning Contribute to Cardioprotection in the Rabbit Myocardium

Baines, Christopher P., Goto, Mahiko, Downey, James M.·1997·Journal of Molecular and Cellular Cardiology

DOI 10.1006/jmcc.1996.0265

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Abstract

Previous studies have proposed that oxygen radicals may play a role in the triggering of ischemic preconditioning. However, studies evaluating the effects of radical scavengers have yielded conflicting results, possibly because of differences in the number of preconditioning episodes used. The present study tested whether N-2-mercaptopropionylglycine (MPG) could block protection of both single and multiple episodes of preconditioning in in situ and in vitro rabbit hearts. All hearts were subjected to 30 min of regional ischemia followed by reperfusion for 2 (in vitro) or 3 (in situ) h. Infarct size was measured by tetrazolium. Infarction in control in situ hearts was 37.5+/-3.5% of the risk zone. A single cycle of preconditioning (PC1), with 5 min ischemia/10 min reperfusion, reduced infarct size to 12.3+/-2.0% (P<0.05). Four cycles of preconditioning (PC4) were equally protective. MPG (1 mg/kg/min i.v.) alone had no effect on infarction but abolished protection afforded by PC1 (35.4+/-3.9%). However, MPG failed to block protection in the PC4 group. In isolated control hearts, infarct size was 31.1+/-1.8% and was reduced to 10.2+/-2.2% (P<0.05) by preconditioning. MPG (300 microM) aborted protection. Infusion of hypoxanthine or xanthine oxidase separately in lieu of preconditioning had no effect on infarct size, but induced protection when combined (14.1+/-2.2%; P<0.05). Polymyxin B, an inhibitor of protein kinase C (PKC), abolished this protection (53.1+/-4.1%). In conclusion, oxygen radicals contribute to ischemic preconditioning in the rabbit and appear to do so via activation of PKC. The fact that MPG could not block protection by PC4 suggests that oxygen radicals act in concert with other triggers of preconditioning such as adenosine and bradykinin.

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Background
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Background
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Self-citation
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Background
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BackgroundInfluential
Adrenomedullin actsvianitric oxide and peroxynitrite to protect against myocardial ischaemia‐induced arrhythmias in anaesthetized rats
Looi, Y. H., Kane, K. A., McPhaden, A. R., & Wainwright, C. L. (2006) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706771 · Cited by 26
“Reactive oxygen species (ROS) have also been shown to be one of the triggers that can mimic the cardioprotective effects of preconditioning (Bilinska et al., 1996; Baines et al., 1997).”
Background
Cardiomyocyte mitochondrial KATP channels participate in the antiarrhythmic and antiinfarct effects of KATP activators during ischemia and reperfusion in an intact anesthetized rabbit model.
Das, B., & Sarkar, C. (2003) · PubMed · Cited by 26
Mitochondrial Therapies in Heart Failure
von Hardenberg, A., & Maack, C. (2016) · Handbook of experimental pharmacology · doi:10.1007/164_2016_123 · Cited by 26
ROLE OF p38‐MITOGEN‐ACTIVATED PROTEIN KINASE IN ISCHAEMIC PRECONDITIONING IN RAT HEART
Bell, J. R., Eaton, P., & Shattock, M. J. (2007) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2007.04794.x · Cited by 25
“Most studies suggest that p38-MAPK is phosphorylated during ischaemia, irrespective of whether the heart has been preconditioned.29,31,32 However, some studies have found p38-MAPK to be dual phosphorylated during sustained ischaemia only in preconditioned hearts.7,9,10 Fryer et al.28 failed to see a change in activity…”
BackgroundInfluential
Ischemic preconditioning preserves mitochondrial membrane potential and limits reactive oxygen species production
Quarrie, R., Lee, D. S., Steinbaugh, G. E., Cramer, B., Erdahl, W. L., Pfeiffer, D. R., Zweier, J. L., & Crestanello, J. A. (2012) · Journal of Surgical Research · doi:10.1016/j.jss.2012.05.090 · Cited by 25
Preconditioning at a distance: Involvement of endothelial vasoactive substances in cardioprotection against ischemia-reperfusion injury
Aggarwal, S., Randhawa, P. K., Singh, N., & Jaggi, A. S. (2016) · Life Sciences · doi:10.1016/j.lfs.2016.03.021 · Cited by 25
Cardioprotection of Interleukin-2 Is Mediated via κ-Opioid Receptors
Cao, C., Xia, Q., Tu, J., Chen, M., Wu, S., & Wong, T. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.061135 · Cited by 25
“Reactive oxygen species (ROS) have been implicated to be involved in cardioprotection of IPC (Baines et al., 1997; Tritto et al., 1997).”
Background
The mechanism of protection from 5 (N-ethyl-N-isopropyl)amiloride differs from that of ischemic preconditioning in rabbit heart
Sato, H., Miki, T., Vallabhapurapu, R., et al. (1997) · Basic Research in Cardiology · doi:10.1007/bf00788946 · Cited by 25
Self-citation
Roles of Mitochondrial Benzodiazepine Receptor in the Heart
Surinkaew, S., Chattipakorn, S. C., & Chattipakorn, N. (2011) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2010.12.023 · Cited by 27
Nox1 NADPH oxidase is necessary for late but not early myocardial ischaemic preconditioning
Jiang, S., Streeter, J., Schickling, B., Zimmerman, K., Weiss, R. M., & Miller, F. J. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu027 · Cited by 24
Mitochondria: A mirror into cellular dysfunction in heart disease
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“PKC pathway activation has been suggested to be dependent upon ROS activation during ischemic PC [130], pharmacological PC [131–133], PostC [134], cardiomyopathy and HF (as reviewed in [135]).”
Background
Role of microtubules in ischemic preconditioning against myocardial infarction
NAKAMURA, Y., Miura, T., NAKANO, A., Ichikawa, Y., Takafumi, Y. A. N. O., Kobayashi, H., IKEDA, Y., MIKI, T., & Shimamoto, K. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.07.013 · Cited by 24
“This explanation is consistent with earlier findings that infusion of free radical scavengers during PC abolished PC-induced cardioprotection and that transient infusion of free radicals induced PClike protection that was sensitive to PKC inhibitors [31,32].”
Result
Role of protein kinase C in intestinal ischemic preconditioning1,2
Um, J. W., Matthews, J. B., Song, J. C., et al. (2004) · Journal of Surgical Research · doi:10.1016/j.jss.2004.10.011 · Cited by 23
Is oxytocin a therapeutic factor for ischemic heart disease?
Alizadeh, A. M., & Mirzabeglo, P. (2013) · Peptides · doi:10.1016/j.peptides.2013.04.016 · Cited by 22
Stimulation of neuronal KATPchannels by cGMP-dependent protein kinase: involvement of ROS and 5-hydroxydecanoate-sensitive factors in signal transduction
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Ischemic Preconditioning: Triggering Role of Nitric Oxide-Derived Oxidants in Isolated Hearts
Novalija, E., Hogg, N., Kevin, L. G., Camara, A. K. S., & Stowe, D. F. (2003) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-200311000-00003 · Cited by 24
Milrinone-Induced Pharmacological Preconditioning in Cardioprotection: Hints for a Role of Mitochondrial Mechanisms
Raupach, A., Reinle, J., Stroethoff, M., Mathes, A., Heinen, A., Hollmann, M. W., Huhn, R., & Bunte, S. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8040507 · Cited by 22
“[32] support our findings with the ROS scavenger MPG in an isolated, perfused rabbit heart model.”
Result
Ischemic preconditioning and remote ischemic preconditioning provide combined protective effect against ischemia/reperfusion injury
Li, D.-Y., Shi, X., Li, W., et al. (2016) · Life Sciences · doi:10.1016/j.lfs.2016.02.077 · Cited by 21
“Endothelial NO, free radicals, adenosine, kinases, opioids, catecholamines and ATP-sensitive potassium (KATP) channels may be involved, but the mechanism is not fully understood [15-17].”
Background
Integrated pharmacological preconditioning in combination with adenosine, a mitochondrial KATP channel opener and a nitric oxide donor
Uchiyama, Y., Otani, H., Okada, T., et al. (2003) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/s0022-5223(03)00236-8 · Cited by 21
A Dual Role of ATM in Ischemic Preconditioning and Ischemic Injury
Xie, G.-H., Dai, H., Liu, F., Zhang, Y., Zhu, L., Nie, J.-J., & Wu, J.-H. (2019) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-019-00773-6 · Cited by 19
Ischemia and reperfusion-induced arrhythmias: role of hyperoxic preconditioning
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Ischaemic postconditioning: from bench to bedside ...
van Vuuren, D., & Lochner, A. (2008) · Europe PMC (PubMed Central) · Cited by 20
Mitochondrialne kanały potasowe: podsumowanie
Szewczyk, A. M., Bednarczyk, P., Jędraszko, J., Kampa, R. P., Koprowski, P., Krajewska, M., Kucman, S. K., Kulawiak, B., Laskowski, M., Rotko, D., et al. (2018) · Postępy Biochemii · doi:10.18388/pb.2018_132 · Cited by 21
The protective effect of ischemic preconditioning on rat testis
Şahinkanat, T., Özkan, K. U., Tolun, F. İ., et al. (2007) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-5-47 · Cited by 20
Ceramide-induced preconditioning involves reactive oxygen species
Lecour, S., Owira, P. M. O., & Opie, L. H. (2005) · Life Sciences · doi:10.1016/j.lfs.2005.08.013 · Cited by 19
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
Differential Effect of Ischemic and Pharmacological Preconditioning on PKC Isoform Translocation in Adult Rat Cardiac Myocytes
Tsouka, V., Markou, T., & Lazou, A. (2002) · Cellular Physiology and Biochemistry · doi:10.1159/000067901 · Cited by 19
Angiotensin II type 1 receptor blocker preserves tolerance to ischemia-reperfusion injury in Dahl salt-sensitive rat heart
Matsuhisa, S., Otani, H., Okazaki, T., et al. (2008) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.91533.2007 · Cited by 18
“The redox-sensitive nature of IPC has been substantiated by the use of antioxidants, such as N-acetylcysteine and 2-mercaptopropionylglycine (MPG), which blocked IPC-induced cardioprotection by eliminating oxidative stress (2, 6).”
Background
Mitochondrial superoxide production and respiratory activity: Biphasic response to ischemic duration
Matsuzaki, S., Szweda, L. I., & Humphries, K. M. (2009) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2009.01.006 · Cited by 18

Authors: Baines, C. P., Goto, M., & Downey, J. M.
Affiliations: University of South Alabama (US)
ORCID: Baines, Christopher P.
Downey, James M.
Venue: Journal of Molecular and Cellular Cardiology
Publisher: Elsevier BV
Published: 1997-01
Volume: 29
Issue: 1
Pages: 207-216
ISSN: 0022-2828 (ISSN-L)
DOI: 10.1006/jmcc.1996.0265
OpenAlex: W2122501550
Cited by: 484
References: 0
Citations by year: 2025: 1 · 2023: 1 · 2022: 5 · 2021: 4 · 2020: 7 · 2019: 8 · 2018: 8 · 2017: 11 · 2016: 12 · 2015: 12 · 2014: 16 · 2013: 21 · 2012: 18
FWCI: 13.61
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of Molecular and Cellular Cardiology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Ischemia and Reperfusion
Health Sciences › Medicine › Surgery › Organ Transplantation Techniques and Outcomes
Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
Keywords: ischemic preconditioning, oxygen free radicals, cardioprotection, protein kinase C, infarct size, myocardial ischemia-reperfusion injury, xanthine oxidase, hypoxanthine, adenosine, bradykinin, radical scavengers
MeSH terms: Analysis of Variance, Animals, Enzyme Activation, Female, Free Radicals, Hemodynamics, Male, Tiopronin, Myocardial Infarction, Protein Kinase C, Rabbits, Free Radical Scavengers, Reactive Oxygen Species, Ischemic Preconditioning, Myocardial, In Vitro Techniques

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Oxygen Radicals Released During Ischemic Preconditioning Contribute to Cardioprotection in the Rabbit Myocardium

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