Articles |
the Experimental Research Laboratory, Section of Cardiology, Department of Medicine, Baylor College of Medicine (X.-L.T., Y.Q., S.-W.P., J.-Z.S., R.B.), Houston, Tex, and the Experimental Research Laboratory, Division of Cardiology, University of Louisville (X.-L.T., Y.Q., A.K., R.B.), Louisville, Ky.
Correspondence to Roberto Bolli, MD, Division of Cardiology, University of Louisville, Louisville, KY 40292. E-mail r0boll01@ulkyvm.louisville.edu.
We have recently found in conscious pigs that a sequence of brief coronary occlusions induces severe myocardial stunning, but when the same sequence is repeated 24 hours later, the severity of stunning is markedly reduced (
50%) ("late preconditioning against stunning"). As an initial step toward elucidating the mechanism and potential clinical significance of this powerful cardioprotective response, the present study was conducted to define the time course of late preconditioning against myocardial stunning. Conscious pigs underwent a sequence of ten 2-minute coronary occlusion/2-minute reperfusion cycles and then a second identical sequence at 6 hours (group I, n=7), 12 hours (group II, n=6), 24 hours (group III, n=10), 3 days (group IV, n=10), or 6 days (group V, n=11) after the first. Systolic wall thickening (WTh) in the ischemic/reperfused region remained significantly depressed for at least 3 hours after the 10th reperfusion of the first sequence, indicating myocardial stunning. When the second sequence of coronary occlusions was performed 6 hours after the first (group I), the recovery of WTh was similar to the first. In contrast, when the second sequence was repeated 12 hours after the first (group II), the recovery of WTh was improved, though not consistently, and the total deficit of WTh decreased by 41% (P<.05) compared with the first sequence. When the second sequence was repeated 24 hours (group III) and 3 days (group IV) after the first, the recovery of WTh was substantially enhanced, with 52% and 49% reductions in the total deficit of WTh, respectively (P<.01 versus the first sequence). When the second sequence was repeated 6 days later (group V), the recovery of WTh was indistinguishable from the first sequence. Thus, late preconditioning against myocardial stunning requires >6 hours to develop, lasts for at least 60 hours after its appearance (with the most effective protection present at 24 hours and 3 days), and disappears within 6 days after the preconditioning ischemia, a time course that is consistent with the synthesis and degradation of cardioprotective proteins. In view of its sustained duration, this endogenous cardioprotective mechanism is of potential clinical importance.
Key Words: ischemic preconditioning myocardial stunning contractile function thickening fraction pig
This article has been cited by other articles:
![]() |
T. Kamota, T.-S. Li, N. Morikage, M. Murakami, M. Ohshima, M. Kubo, T. Kobayashi, A. Mikamo, Y. Ikeda, M. Matsuzaki, et al. Ischemic pre-conditioning enhances the mobilization and recruitment of bone marrow stem cells to protect against ischemia/reperfusion injury in the late phase. J. Am. Coll. Cardiol., May 12, 2009; 53(19): 1814 - 1822. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. S. Gaskin, K. Kamada, M. Yusof, and R. J. Korthuis 5'-AMP-activated protein kinase activation prevents postischemic leukocyte-endothelial cell adhesive interactions Am J Physiol Heart Circ Physiol, January 1, 2007; 292(1): H326 - H332. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. M. Bell, J. E. Clark, D. J. Hearse, and M. J. Shattock Reperfusion kinase phosphorylation is essential but not sufficient in the mediation of pharmacological preconditioning: Characterisation in the bi-phasic profile of early and late protection Cardiovasc Res, January 1, 2007; 73(1): 153 - 163. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Jneid, M. Chandra, M. Alshaher, C. A. Hornung, X.-L. Tang, M. Leesar, and R. Bolli Delayed Preconditioning-Mimetic Actions of Nitroglycerin in Patients Undergoing Exercise Tolerance Tests Circulation, May 24, 2005; 111(20): 2565 - 2571. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Jiang, E. Shi, Y. Nakajima, S. Sato, K. Ohno, and H. Yue Cyclooxygenase-1 Mediates the Final Stage of Morphine-Induced Delayed Cardioprotection in Concert With Cyclooxygenase-2 J. Am. Coll. Cardiol., May 17, 2005; 45(10): 1707 - 1715. [Abstract] [Full Text] [PDF] |
||||
![]() |
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] |
||||
![]() |
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] |
||||
![]() |
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] |
||||
![]() |
X. Monnet, P. Colin, B. Ghaleh, L. Hittinger, J.-F. Giudicelli, and A. Berdeaux Heart rate reduction during exercise-induced myocardial ischaemia and stunning Eur. Heart J., April 1, 2004; 25(7): 579 - 586. [Abstract] [Full Text] [PDF] |
||||
![]() |
G.F Baxter Role of adenosine in delayed preconditioning of myocardium Cardiovasc Res, August 15, 2002; 55(3): 483 - 494. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. O. McFalls, B. Murad, J.-S. Liow, M. C. Gannon, H. C. Haspel, A. Lange, D. Marx, J. Sikora, and H. B. Ward Glucose uptake and glycogen levels are increased in pig heart after repetitive ischemia Am J Physiol Heart Circ Physiol, January 1, 2002; 282(1): H205 - H211. [Abstract] [Full Text] [PDF] |
||||
![]() |
X.-L. Tang, H. Takano, A. Rizvi, J. F. Turrens, Y. Qiu, W.-J. Wu, Q. Zhang, and R. Bolli Oxidant species trigger late preconditioning against myocardial stunning in conscious rabbits Am J Physiol Heart Circ Physiol, January 1, 2002; 282(1): H281 - H291. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. A. Kloner and R. B. Jennings Consequences of Brief Ischemia: Stunning, Preconditioning, and Their Clinical Implications: Part 1 Circulation, December 11, 2001; 104(24): 2981 - 2989. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Monnet, B. Ghaleh, P. Colin, O. P. de Curzon, J.-F. Giudicelli, and A. Berdeaux Effects of Heart Rate Reduction with Ivabradine on Exercise-Induced Myocardial Ischemia and Stunning J. Pharmacol. Exp. Ther., December 1, 2001; 299(3): 1133 - 1139. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. H. E. H. Snoeckx, R. N. Cornelussen, F. A. Van Nieuwenhoven, R. S. Reneman, and G. J. Van der Vusse Heat Shock Proteins and Cardiovascular Pathophysiology Physiol Rev, October 1, 2001; 81(4): 1461 - 1497. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Hill, H. Takano, X.-L. Tang, E. Kodani, G. Shirk, and R. Bolli Nitroglycerin Induces Late Preconditioning Against Myocardial Infarction in Conscious Rabbits Despite Development of Nitrate Tolerance Circulation, August 7, 2001; 104(6): 694 - 699. [Abstract] [Full Text] [PDF] |
||||
![]() |
O. Parent De Curzon, B. Ghaleh, R. Tissier, J.-F. Giudicelli, L. Hittinger, and A. Berdeaux Myocardial stunning in exercise-induced ischemia in dogs: lack of late preconditioning Am J Physiol Heart Circ Physiol, January 1, 2001; 280(1): H302 - H310. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Bolli The Late Phase of Preconditioning Circ. Res., November 24, 2000; 87(11): 972 - 983. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Takano, X.-L. Tang, and R. Bolli Differential role of KATP channels in late preconditioning against myocardial stunning and infarction in rabbits Am J Physiol Heart Circ Physiol, November 1, 2000; 279(5): H2350 - H2359. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. M. Yellon and A. Dana The Preconditioning Phenomenon : A Tool for the Scientist or a Clinical Reality? Circ. Res., September 29, 2000; 87(7): 543 - 550. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Zacharowski, S. Frank, M. Otto, P. K. Chatterjee, S. Cuzzocrea, G. Hafner, J. Pfeilschifter, and C. Thiemermann Lipoteichoic Acid Induces Delayed Protection in the Rat Heart : A Comparison With Endotoxin Arterioscler Thromb Vasc Biol, June 1, 2000; 20(6): 1521 - 1528. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Dana, M. Skarli, J. Papakrivopoulou, and D. M. Yellon Adenosine A1 Receptor Induced Delayed Preconditioning in Rabbits : Induction of p38 Mitogen-Activated Protein Kinase Activation and Hsp27 Phosphorylation via a Tyrosine Kinase- and Protein Kinase C-Dependent Mechanism Circ. Res., May 12, 2000; 86(9): 989 - 997. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Dawn, Y.-T. Xuan, Y. Qiu, H. Takano, X.-L. Tang, P. Ping, S. Banerjee, M. Hill, and R. Bolli Bifunctional Role of Protein Tyrosine Kinases in Late Preconditioning Against Myocardial Stunning in Conscious Rabbits Circ. Res., December 3, 1999; 85(12): 1154 - 1163. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Noda, S. Minatoguchi, K. Fujii, M. Hori, T. Ito, K. Kanmatsuse, M. Matsuzaki, T. Miura, H. Nonogi, M. Tada, et al. Evidence for the delayed effect in human ischemic preconditioning: Prospective multicenter study for preconditioning in acute myocardial infarction J. Am. Coll. Cardiol., December 1, 1999; 34(7): 1966 - 1974. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Banerjee, X.-L. Tang, Y. Qiu, H. Takano, S. Manchikalapudi, B. Dawn, G. Shirk, and R. Bolli Nitroglycerin induces late preconditioning against myocardial stunning via a PKC-dependent pathway Am J Physiol Heart Circ Physiol, December 1, 1999; 277(6): H2488 - H2494. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Shinmura, X.-L. Tang, H. Takano, M. Hill, and R. Bolli Nitric oxide donors attenuate myocardial stunning in conscious rabbits Am J Physiol Heart Circ Physiol, December 1, 1999; 277(6): H2495 - H2503. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Zacharowski, M. Otto, G. Hafner, P. K. Chatterjee, and C. Thiemermann Endotoxin Induces a Second Window of Protection in the Rat Heart as Determined by Using p-Nitro-Blue Tetrazolium Staining, Cardiac Troponin T Release, and Histology Arterioscler Thromb Vasc Biol, September 1, 1999; 19(9): 2276 - 2280. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Rizvi, X.-L. Tang, Y. Qiu, Y.-T. Xuan, H. Takano, A. K. Jadoon, and R. Bolli Increased protein synthesis is necessary for the development of late preconditioning against myocardial stunning Am J Physiol Heart Circ Physiol, September 1, 1999; 277(3): H874 - H884. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y.-T. Xuan, X.-L. Tang, S. Banerjee, H. Takano, R. C. X. Li, H. Han, Y. Qiu, J.-J. Li, and R. Bolli Nuclear Factor-{kappa}B Plays an Essential Role in the Late Phase of Ischemic Preconditioning in Conscious Rabbits Circ. Res., May 14, 1999; 84(9): 1095 - 1109. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Baghelai, L. J. Graham, A. S. Wechsler, and E. R. Jakoi DELAYED MYOCARDIAL PRECONDITIONING BY {{alpha}}1-ADRENOCEPTORS INVOLVES INHIBITION OF APOPTOSIS J. Thorac. Cardiovasc. Surg., May 1, 1999; 117(5): 980 - 986. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Ping, J. Zhang, X. Cao, R. C. X. Li, D. Kong, X.-L. Tang, Y. Qiu, S. Manchikalapudi, J. A. Auchampach, R. G. Black, et al. PKC-dependent activation of p44/p42 MAPKs during myocardial ischemia-reperfusion in conscious rabbits Am J Physiol Heart Circ Physiol, May 1, 1999; 276(5): H1468 - H1481. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Ping, H. Takano, J. Zhang, X.-L. Tang, Y. Qiu, R. C. X. Li, S. Banerjee, B. Dawn, Z. Balafonova, and R. Bolli Isoform-Selective Activation of Protein Kinase C by Nitric Oxide in the Heart of Conscious Rabbits : A Signaling Mechanism for Both Nitric Oxide–Induced and Ischemia-Induced Preconditioning Circ. Res., March 19, 1999; 84(5): 587 - 604. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Guo, W.-J. Wu, Y. Qiu, X.-L. Tang, Z. Yang, and R. Bolli Demonstration of an early and a late phase of ischemic preconditioning in mice Am J Physiol Heart Circ Physiol, October 1, 1998; 275(4): H1375 - H1387. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Takano, S. Manchikalapudi, X.-L. Tang, Y. Qiu, A. Rizvi, A. K. Jadoon, Q. Zhang, and R. Bolli Nitric Oxide Synthase Is the Mediator of Late Preconditioning Against Myocardial Infarction in Conscious Rabbits Circulation, August 4, 1998; 98(5): 441 - 449. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. J. Benjamin and D. R. McMillan Stress (Heat Shock) Proteins : Molecular Chaperones in Cardiovascular Biology and Disease Circ. Res., July 27, 1998; 83(2): 117 - 132. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. J Duncker, R. Schulz, R. Ferrari, D. Garcia-Dorado, C. Guarnieri, G. Heusch, and P. D Verdouw "Myocardial stunning": remaining questions Cardiovasc Res, June 1, 1998; 38(3): 549 - 558. [Full Text] [PDF] |
||||
![]() |
D. M Yellon, G. F Baxter, D. Garcia-Dorado, G. Heusch, and M. S Sumeray Ischaemic preconditioning: present position and future directions Cardiovasc Res, January 1, 1998; 37(1): 21 - 33. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Bolli, S. Manchikalapudi, X.-L. Tang, H. Takano, Y. Qiu, Y. Guo, Q. Zhang, and A. K. Jadoon The Protective Effect of Late Preconditioning Against Myocardial Stunning in Conscious Rabbits Is Mediated by Nitric Oxide Synthase : Evidence That Nitric Oxide Acts Both as a Trigger and as a Mediator of the Late Phase of Ischemic Preconditioning Circ. Res., December 19, 1997; 81(6): 1094 - 1107. [Abstract] [Full Text] |
||||
![]() |
Y. Qiu, A. Rizvi, X.-L. Tang, S. Manchikalapudi, H. Takano, A. K. Jadoon, W.-J. Wu, and R. Bolli Nitric oxide triggers late preconditioning against myocardial infarction in conscious rabbits Am J Physiol Heart Circ Physiol, December 1, 1997; 273(6): H2931 - H2936. [Abstract] [Full Text] [PDF] |
||||
![]() |
X.-L. Tang, Y. Qiu, J. F. Turrens, J.-Z. Sun, and R. Bolli Late preconditioning against stunning is not mediated by increased antioxidant defenses in conscious pigs Am J Physiol Heart Circ Physiol, October 1, 1997; 273(4): H1651 - H1657. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Ping, J. Zhang, Y. Qiu, X.-L. Tang, S. Manchikalapudi, X. Cao, and R. Bolli Ischemic Preconditioning Induces Selective Translocation of Protein Kinase C Isoforms {epsilon} and {eta} in the Heart of Conscious Rabbits Without Subcellular Redistribution of Total Protein Kinase C Activity Circ. Res., September 19, 1997; 81(3): 404 - 414. [Abstract] [Full Text] |
||||
![]() |
G. von Degenfeld, W. Giehrl, and P. Boekstegers Targeting of dobutamine to ischemic myocardium without systemic effects by selective suction and pressure-regulated retroinfusion Cardiovasc Res, August 1, 1997; 35(2): 233 - 240. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Bolli, Z. A. Bhatti, X.-L. Tang, Y. Qiu, Q. Zhang, Y. Guo, and A. K. Jadoon Evidence That Late Preconditioning Against Myocardial Stunning in Conscious Rabbits Is Triggered by the Generation of Nitric Oxide Circ. Res., July 19, 1997; 81(1): 42 - 52. [Abstract] [Full Text] |
||||
![]() |
Y. Qiu, X.-L. Tang, S.-W. Park, J.-Z. Sun, A. Kalya, and R. Bolli The Early and Late Phases of Ischemic Preconditioning : A Comparative Analysis of Their Effects on Infarct Size, Myocardial Stunning, and Arrhythmias in Conscious Pigs Undergoing a 40-Minute Coronary Occlusion Circ. Res., May 19, 1997; 80(5): 730 - 742. [Abstract] [Full Text] |
||||
![]() |
G. Brooks and D. J. Hearse Role of Protein Kinase C in Ischemic Preconditioning: Player or Spectator? Circ. Res., September 1, 1996; 79(3): 628 - 631. [Full Text] |
||||
|
Circulation Research Home | Subscriptions | Archives | Feedback | Authors | Help | AHA Journals Home | Search Copyright © 1996 American Heart Association, Inc. All rights reserved. Unauthorized use prohibited. |