© 2000 American Heart Association, Inc.
Review |
The Late Phase of Preconditioning
From the Division of Cardiology, University of Louisville and Jewish Hospital Heart and Lung Institute, Louisville, Ky.
Correspondence to Roberto Bolli, MD, Division of Cardiology, University of Louisville, Louisville, KY 40292. E-mail rbolli{at}louisville.edu
Abstract—Unlike
the early phase of preconditioning (PC), which lasts 2 to 3 hours and
protects against infarction but not against stunning, the late phase of
PC lasts 3 to 4 days and protects against both infarction and stunning,
suggesting that it may have greater clinical relevance. It is now clear
that late PC is a polygenic phenomenon that requires the simultaneous
activation of multiple stress-responsive genes. Chemical signals
released by a sublethal ischemic stress (such as NO, reactive oxygen
species, and adenosine) trigger a complex cascade of signaling events
that includes the activation of protein kinase C, Src protein tyrosine
kinases, and nuclear factor 
B and culminates in increased synthesis
of inducible NO synthase, cyclooxygenase-2, aldose reductase, Mn
superoxide dismutase, and probably other cardioprotective proteins. An
analogous sequence of events can be triggered by a variety of stimuli,
such as heat stress, exercise, and cytokines. Thus, late PC appears to
be a universal response of the heart to stress in general. Importantly,
the cardioprotective effects of late PC can be reproduced
pharmacologically with clinically relevant agents (eg, NO donors,
adenosine receptor agonists, endotoxin derivatives, or opioid receptor
agonists), suggesting that this phenomenon might be exploited for
therapeutic purposes. The purpose of this review is to summarize
current information regarding the pathophysiology and mechanism of late
PC.
Key Words: myocardial ischemia • myocardial reperfusion • nitric oxide • cyclooxygenase • aldose reductase
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G. Heusch, R. Schulz, and S. H. Rahimtoola Myocardial hibernation: a delicate balance Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H984 - H999. [Abstract] [Full Text] [PDF]
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T. Date, S. Mochizuki, A. J. Belanger, M. Yamakawa, Z. Luo, K. A. Vincent, S. H. Cheng, R. J. Gregory, and C. Jiang Expression of constitutively stable hybrid hypoxia-inducible factor-1{alpha} protects cultured rat cardiomyocytes against simulated ischemia-reperfusion injury Am J Physiol Cell Physiol, February 1, 2005; 288(2): C314 - C320. [Abstract] [Full Text] [PDF]
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A. S. Leon, B. A. Franklin, F. Costa, G. J. Balady, K. A. Berra, K. J. Stewart, P. D. Thompson, M. A. Williams, and M. S. Lauer Cardiac Rehabilitation and Secondary Prevention of Coronary Heart Disease: An American Heart Association Scientific Statement From the Council on Clinical Cardiology (Subcommittee on Exercise, Cardiac Rehabilitation, and Prevention) and the Council on Nutrition, Physical Activity, and Metabolism (Subcommittee on Physical Activity), in Collaboration With the American Association of Cardiovascular and Pulmonary Rehabilitation Circulation, January 25, 2005; 111(3): 369 - 376. [Abstract] [Full Text] [PDF]
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H. Yamasowa, S. Shimizu, T. Inoue, M. Takaoka, and Y. Matsumura Endothelial Nitric Oxide Contributes to the Renal Protective Effects of Ischemic Preconditioning J. Pharmacol. Exp. Ther., January 1, 2005; 312(1): 153 - 159. [Abstract] [Full Text] [PDF]
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Y. Shi, W. C. Hutchins, J. Su, D. Siker, N. Hogg, K. A. Pritchard Jr., A. Keszler, J. S. Tweddell, and J. E. Baker Delayed cardioprotection with isoflurane: role of reactive oxygen and nitrogen Am J Physiol Heart Circ Physiol, January 1, 2005; 288(1): H175 - H184. [Abstract] [Full Text] [PDF]
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L. Xi, M. Taher, C. Yin, F. Salloum, and R. C. Kukreja Cobalt chloride induces delayed cardiac preconditioning in mice through selective activation of HIF-1{alpha} and AP-1 and iNOS signaling Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2369 - H2375. [Abstract] [Full Text] [PDF]
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G. Kristo, Y. Yoshimura, B. J. Keith, R. M. Stevens, S. A. Jahania, R. M. Mentzer Jr., and R. D. Lasley Adenosine A1/A2a receptor agonist AMP-579 induces acute and delayed preconditioning against in vivo myocardial stunning Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2746 - H2753. [Abstract] [Full Text] [PDF]
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X. Wang, C. Yin, L. Xi, and R. C. Kukreja Opening of Ca2+-activated K+ channels triggers early and delayed preconditioning against I/R injury independent of NOS in mice Am J Physiol Heart Circ Physiol, November 1, 2004; 287(5): H2070 - H2077. [Abstract] [Full Text] [PDF]
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 A. B. Stein, X.-L. Tang, Y. Guo, Y.-T. Xuan, B. Dawn, and R. Bolli Delayed Adaptation of the Heart to Stress: Late Preconditioning Stroke, November 1, 2004; 35(11_suppl_1): 2676 - 2679. [Abstract] [Full Text] [PDF]
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D. B. Buxton Cytokines and Late Preconditioning Cardiovasc Res, October 1, 2004; 64(1): 6 - 8. [Full Text] [PDF]
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B. Dawn, Y.-T. Xuan, Y. Guo, A. Rezazadeh, A. B. Stein, G. Hunt, W.-J. Wu, W. Tan, and R. Bolli IL-6 plays an obligatory role in late preconditioning via JAK-STAT signaling and upregulation of iNOS and COX-2 Cardiovasc Res, October 1, 2004; 64(1): 61 - 71. [Abstract] [Full Text] [PDF]
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A. Bhatnagar Beating Ischemia: A New Feat of EETs? Circ. Res., September 3, 2004; 95(5): 443 - 445. [Full Text] [PDF]
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E. O. McFalls, M. Hou, R. J. Bache, A. Best, D. Marx, J. Sikora, and H. B. Ward Activation of p38 MAPK and increased glucose transport in chronic hibernating swine myocardium Am J Physiol Heart Circ Physiol, September 1, 2004; 287(3): H1328 - H1334. [Abstract] [Full Text] [PDF]
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M. A. G. Hartlage, E. Berendes, H. Van Aken, M. Fobker, M. Theisen, and T. P. Weber Xenon Improves Recovery from Myocardial Stunning in Chronically Instrumented Dogs Anesth. Analg., September 1, 2004; 99(3): 655 - 664. [Abstract] [Full Text] [PDF]
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C. Depre, S.-J. Kim, A. S. John, Y. Huang, O. E. Rimoldi, J. R. Pepper, G. D. Dreyfus, V. Gaussin, D. J. Pennell, D. E. Vatner, et al. Program of Cell Survival Underlying Human and Experimental Hibernating Myocardium Circ. Res., August 20, 2004; 95(4): 433 - 440. [Abstract] [Full Text] [PDF]
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C. J. McLeod, A. P. Jeyabalan, J. O. Minners, R. Clevenger, R. F. Hoyt Jr, and M. N. Sack Delayed Ischemic Preconditioning Activates Nuclear-Encoded Electron-Transfer-Chain Gene Expression in Parallel With Enhanced Postanoxic Mitochondrial Respiratory Recovery Circulation, August 3, 2004; 110(5): 534 - 539. [Abstract] [Full Text] [PDF]
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M. Mayr, B. Metzler, Y.-L. Chung, E. McGregor, U. Mayr, H. Troy, Y. Hu, M. Leitges, O. Pachinger, J. R. Griffiths, et al. Ischemic preconditioning exaggerates cardiac damage in PKC-{delta} null mice Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H946 - H956. [Abstract] [Full Text] [PDF]
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R. V. Plachinta, M. J. M. de Klaver, J. K. Hayes, and G. F. Rich The Protective Effect of Protein Kinase C and Adenosine Triphosphate-Sensitive Potassium Channel Agonists Against Inflammation in Rat Endothelium and Vascular Smooth Muscle In Vitro and In Vivo Anesth. Analg., August 1, 2004; 99(2): 556 - 561. [Abstract] [Full Text] [PDF]
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R. Bolli, L. Becker, G. Gross, R. Mentzer Jr, D. Balshaw, and D. A. Lathrop Myocardial Protection at a Crossroads: The Need for Translation Into Clinical Therapy Circ. Res., July 23, 2004; 95(2): 125 - 134. [Abstract] [Full Text] [PDF]
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Y. Wang, E. Kodani, J. Wang, S. X. Zhang, H. Takano, X.-L. Tang, and R. Bolli Cardioprotection During the Final Stage of the Late Phase of Ischemic Preconditioning Is Mediated by Neuronal NO Synthase in Concert With Cyclooxygenase-2 Circ. Res., July 9, 2004; 95(1): 84 - 91. [Abstract] [Full Text] [PDF]
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M. Zaugg, M. C. Schaub, and P. Foex Myocardial injury and its prevention in the perioperative setting Br. J. Anaesth., July 1, 2004; 93(1): 21 - 33. [Abstract] [Full Text] [PDF]
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A. Crisafulli, F. Melis, F. Tocco, U. M. Santoboni, C. Lai, G. Angioy, L. Lorrai, G. Pittau, A. Concu, and P. Pagliaro Exercise-induced and nitroglycerin-induced myocardial preconditioning improves hemodynamics in patients with angina Am J Physiol Heart Circ Physiol, July 1, 2004; 287(1): H235 - H242. [Abstract] [Full Text] [PDF]
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G. G. Neri Serneri, M. Boddi, P. A. Modesti, M. Coppo, I. Cecioni, T. Toscano, M. L. Papa, M. Bandinelli, G. F. Lisi, and M. Chiavarelli Cardiac Angiotensin II Participates in Coronary Microvessel Inflammation of Unstable Angina and Strengthens the Immunomediated Component Circ. Res., June 25, 2004; 94(12): 1630 - 1637. [Abstract] [Full Text] [PDF]
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 M. Galagudza, D. Kurapeev, S. Minasian, G. Valen, and J. Vaage Ischemic postconditioning: brief ischemia during reperfusion converts persistent ventricular fibrillation into regular rhythm Eur. J. Cardiothorac. Surg., June 1, 2004; 25(6): 1006 - 1010. [Abstract] [Full Text] [PDF]
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C.-M. Cao, Q. Xia, J. Tu, M. Chen, S. Wu, and T.-M. Wong Cardioprotection of Interleukin-2 Is Mediated via {kappa}-Opioid Receptors J. Pharmacol. Exp. Ther., May 1, 2004; 309(2): 560 - 567. [Abstract] [Full Text] [PDF]
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R. Schulz and G. Heusch Connexin 43 and ischemic preconditioning Cardiovasc Res, May 1, 2004; 62(2): 335 - 344. [Abstract] [Full Text] [PDF]
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X.-L. Tang, Y.-T. Xuan, Y. Zhu, G. Shirk, and R. Bolli Nicorandil induces late preconditioning against myocardial infarction in conscious rabbits Am J Physiol Heart Circ Physiol, April 1, 2004; 286(4): H1273 - H1280. [Abstract] [Full Text] [PDF]
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