© 1997 American Heart Association, Inc.
Articles |
Evidence That Late Preconditioning Against Myocardial Stunning in Conscious Rabbits Is Triggered by the Generation of Nitric Oxide
From the Experimental Research Laboratory, Division of Cardiology, University of Louisville (Ky).
Correspondence to Roberto Bolli, MD, Division of Cardiology, University of Louisville, Louisville, KY 40292. E-mail rObollO1{at}ulkyvm.louisville.edu
Abstract Recent studies in conscious pigs and rabbits
have demonstrated that a series of brief coronary occlusions
renders the heart relatively resistant to myocardial
"stunning" 24 hours later (late preconditioning [PC] against
stunning). The mechanism of this powerful cardioprotective response is
unknown. The goal of the present study was to test the hypothesis
that the development of late PC against stunning is triggered by
increased generation of NO during the first ischemic challenge.
Conscious rabbits underwent a sequence of six 4-minute coronary
occlusion/4-minute reperfusion cycles for 3 consecutive days (days 1,
2, and 3). On day 1, rabbits received either an intravenous
infusion of the NO synthase inhibitor
N
-nitro-L-arginine (L-NA, 13
mg/kg before the first occlusion) (group II, n=10) or vehicle (group I
[control], n=10). In the control group, on day 1 systolic
wall thickening (WTh) in the ischemic/reperfused region
remained significantly depressed for 4 hours after the sixth
reperfusion, indicating myocardial stunning. On days 2 and 3, however,
the recovery of WTh improved markedly, so that the total deficit of WTh
decreased by 60% on day 2 and 55% on day 3 compared with day 1
(P<.01). In the L-NA–treated group, the total deficit of
WTh on day 1 was similar to that observed in the control group. On day
2, however, the total deficit of WTh was not significantly different
from that observed on day 1 and was 132% greater than that observed in
control rabbits on day 2 (P<.01). On day 3, the total
deficit of WTh was 66% less than that noted on day 2
(P<.01). Thus, in L-NA–treated rabbits the sequence of six
coronary occlusions and reperfusions performed on day 1 failed
to precondition against stunning on day 2, but the same sequence
performed on day 2 did precondition against stunning on day 3. Another
group of rabbits (group III, n=6) received L-NA on day 1 in the absence
of ischemia and was subjected to the occlusion/reperfusion
sequence on days 2 and 3. In these animals, the total deficit of WTh on
day 2 did not differ from that observed in control rabbits on day 1,
indicating that administration of L-NA did not exacerbate the severity
of myocardial stunning 24 hours later; therefore, the absence of late
PC against stunning on day 2 in group II cannot be ascribed to a
delayed deleterious action of L-NA on WTh. In conclusion, these results
demonstrate that the NO synthase inhibitor L-NA completely
blocks the development of late PC against myocardial stunning in
conscious rabbits, indicating that NO generated as a result of the PC
ischemia triggers the development of the cardioprotective
response observed 24 hours later. NO is known to exert numerous
biological actions resulting in rapid but transient
physiological responses. The present
observations support a novel pathophysiological
paradigm in which NO also plays a key role in the delayed myocardial
adaptations to ischemic stress, acting as a signaling step in
the transduction pathway that leads to increased resistance to
subsequent ischemic injury.
Key Words: L-arginine • nitric oxide synthase • nitrogen radicals • oxygen radicals • myocardial ischemia/reperfusion
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M. V. Cohen, X.-M. Yang, and J. M. Downey Smaller infarct after preconditioning does not predict extent of early functional improvement of reperfused heart Am J Physiol Heart Circ Physiol, November 1, 1999; 277(5): H1754 - H1761. [Abstract] [Full Text] [PDF]
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P. Ping, J. Zhang, S. Huang, X. Cao, X.-L. Tang, R. C. X. Li, Y.-T. Zheng, Y. Qiu, A. Clerk, P. Sugden, et al. PKC-dependent activation of p46/p54 JNKs during ischemic preconditioning in conscious rabbits Am J Physiol Heart Circ Physiol, November 1, 1999; 277(5): H1771 - H1785. [Abstract] [Full Text] [PDF]
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C. J. Lowenstein NO news is good news PNAS, September 28, 1999; 96(20): 10953 - 10954. [Full Text] [PDF]
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Y. Guo, W. K. Jones, Y.-T. Xuan, X.-L. Tang, W. Bao, W.-J. Wu, H. Han, V. E. Laubach, P. Ping, Z. Yang, et al. The late phase of ischemic preconditioning is abrogated by targeted disruption of the inducible NO synthase gene PNAS, September 28, 1999; 96(20): 11507 - 11512. [Abstract] [Full Text] [PDF]
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P. Ping, J. Zhang, Y.-T. Zheng, R. C. X. Li, B. Dawn, X.-L. Tang, H. Takano, Z. Balafanova, and R. Bolli Demonstration of Selective Protein Kinase C–Dependent Activation of Src and Lck Tyrosine Kinases During Ischemic Preconditioning in Conscious Rabbits Circ. Res., September 17, 1999; 85(6): 542 - 550. [Abstract] [Full Text] [PDF]
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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]
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R. D Rakhit, R. J Edwards, and M. S Marber Nitric oxide, nitrates and ischaemic preconditioning Cardiovasc Res, August 15, 1999; 43(3): 621 - 627. [Full Text] [PDF]
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 N.-P. Wang, B. L. Bufkin, M. Nakamura, Z.-Q. Zhao, J. N. Wilcox, K. O. Hewan-Lowe, R. A. Guyton, and J. Vinten-Johansen Ischemic preconditioning reduces neutrophil accumulation and myocardial apoptosis Ann. Thorac. Surg., June 1, 1999; 67(6): 1689 - 1695. [Abstract] [Full Text] [PDF]
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J. R. Kersten and D. C. Warltier Modulation of the adaptive response to myocardial ischemia by coexisting disease Am J Physiol Heart Circ Physiol, June 1, 1999; 276(6): H2268 - H2270. [Full Text] [PDF]
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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]
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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]
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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]
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M. Kitakaze, K. Node, T. Minamino, H. Asanuma, T. Kuzuya, and M. Hori A Ca channel blocker, benidipine, increases coronary blood flow and attenuates the severity of myocardial ischemia via NO-dependent mechanisms in dogs J. Am. Coll. Cardiol., January 1, 1999; 33(1): 242 - 249. [Abstract] [Full Text] [PDF]
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E. C Lascano, J. A Negroni, H. F del Valle, and A. J Crottogini Left ventricular regional systolic and diastolic function in conscious sheep undergoing ischemic preconditioning Cardiovasc Res, January 1, 1999; 41(1): 77 - 86. [Abstract] [Full Text] [PDF]
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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]
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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]
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H. Takano, X.-L. Tang, Y. Qiu, Y. Guo, B. A. French, and R. Bolli Nitric Oxide Donors Induce Late Preconditioning Against Myocardial Stunning and Infarction in Conscious Rabbits via an Antioxidant-Sensitive Mechanism Circ. Res., July 13, 1998; 83(1): 73 - 84. [Abstract] [Full Text] [PDF]
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R. A. Kloner, R. Bolli, E. Marban, L. Reinlib, and E. Braunwald Medical and Cellular Implications of Stunning, Hibernation, and Preconditioning : An NHLBI Workshop Circulation, May 19, 1998; 97(18): 1848 - 1867. [Full Text] [PDF]
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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]
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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]
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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]
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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]
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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]
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K. M. Kurrelmeyer, L. H. Michael, G. Baumgarten, G. E. Taffet, J. J. Peschon, N. Sivasubramanian, M. L. Entman, and D. L. Mann Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemic-induced apoptosis in a murine model of acute myocardial infarction PNAS, May 9, 2000; 97(10): 5456 - 5461. [Abstract] [Full Text] [PDF]
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H. Ninomiya, H. Otani, K. Lu, T. Uchiyama, M. Kido, and H. Imamura Enhanced IPC by activation of pertussis toxin-sensitive and -insensitive G protein-coupled purinoceptors Am J Physiol Heart Circ Physiol, May 1, 2002; 282(5): H1933 - H1943. [Abstract] [Full Text] [PDF]
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K. Shinmura, Y.-T. Xuan, X.-L. Tang, E. Kodani, H. Han, Y. Zhu, and R. Bolli Inducible Nitric Oxide Synthase Modulates Cyclooxygenase-2 Activity in the Heart of Conscious Rabbits During the Late Phase of Ischemic Preconditioning Circ. Res., March 22, 2002; 90(5): 602 - 608. [Abstract] [Full Text] [PDF]
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