© 1997 American Heart Association, Inc.
Articles |
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
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 Seventy-four conscious rabbits undergoing a sequence
of six 4-minute coronary occlusion/4-minute reperfusion cycles
for 3 consecutive days (days 1, 2, and 3) were assigned to nine groups.
In group I (controls, n=8), the recovery of systolic wall
thickening (WTh) after the sixth reperfusion was markedly improved on
days 2 and 3 compared with day 1, indicating late preconditioning (PC)
against myocardial stunning; the total deficit of WTh after the sixth
reperfusion was reduced by 56% on day 2 and 50% on day 3 compared
with day 1 (P<.01). Administration on day 2 of the
nonselective NO synthase (NOS) inhibitor
N
-nitro-L-arginine (L-NA)
(group II, n=8) or of the selective inducible NOS
inhibitors aminoguanidine (AG) (group IV, n=8) and
S-methylisothiourea sulfate (SMT) (group VI, n=6)
completely abrogated late PC against stunning on day 2. On day 3, the
expected PC effect became manifest in all groups. Administration of
L-NA, AG, or SMT on day 1 (groups III [n=7], V [n=6], and VII
[n=5], respectively) had no discernible effect on the deficit of WTh
on day 1, indicating that these agents do not augment the severity of
myocardial stunning in nonpreconditioned
myocardium. In group VIII (n=7), the abrogation of late PC
by SMT on day 2 was completely reversed by the concomitant
administration of L-arginine (595 mg/kg IV), indicating
that it was not due to nonspecific NOS-unrelated actions.
Administration of L-arginine alone on day 2 (group IX
[n=5]) had no effect on the deficit of WTh. Furthermore,
administration of L-NA on day 1 (group III) prevented the appearance of
the PC effect on day 2, whereas AG (group V) and SMT (group VI) did
not, suggesting that the development of late PC on day 1 is triggered
by the endothelial (type III) isoform of NOS. This
study demonstrates that three structurally different NOS
inhibitors (L-NA, AG, and SMT), given 24 hours after the PC
ischemia, consistently abrogate late PC against
myocardial stunning in conscious rabbits, indicating that this
cardioprotective effect is mediated by the activity of NOS. The results
obtained with AG and SMT specifically implicate the inducible (type II)
isoform as the mediator of the protection on day 2. Previous studies
have shown that NO triggers the development of late PC. The present
results indicate that NO plays a dual role in late PC against stunning,
acting initially as the trigger and subsequently as the mediator of
the protection.
Key Words: myocardial reperfusion • N-nitro-L-arginine • aminoguanidine • S-methylisothiourea sulfate • L-arginine
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H. Takano, X.-L. Tang, E. Kodani, and R. Bolli Late preconditioning enhances recovery of myocardial function after infarction in conscious rabbits Am J Physiol Heart Circ Physiol, November 1, 2000; 279(5): H2372 - H2381. [Abstract] [Full Text] [PDF]
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 T. J. Koh and J. G. Tidball Nitric oxide inhibits calpain-mediated proteolysis of talin in skeletal muscle cells Am J Physiol Cell Physiol, September 1, 2000; 279(3): C806 - C812. [Abstract] [Full Text] [PDF]
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K. Shinmura, X.-L. Tang, Y. Wang, Y.-T. Xuan, S.-Q. Liu, H. Takano, A. Bhatnagar, and R. Bolli Cyclooxygenase-2 mediates the cardioprotective effects of the late phase of ischemic preconditioning in conscious rabbits PNAS, August 29, 2000; 97(18): 10197 - 10202. [Abstract] [Full Text] [PDF]
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 G. L. Semenza HIF-1 and human disease: one highly involved factor Genes & Dev., August 15, 2000; 14(16): 1983 - 1991. [Full Text]
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R. K. Kudej, S.-J. Kim, Y.-T. Shen, J. B. Jackson, A. B. Kudej, G.-P. Yang, S. P. Bishop, and S. F. Vatner Nitric oxide, an important regulator of perfusion-contraction matching in conscious pigs Am J Physiol Heart Circ Physiol, July 1, 2000; 279(1): H451 - H456. [Abstract] [Full Text] [PDF]
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G. Valen, G. K Hansson, A. Dumitrescu, and J. Vaage Unstable angina activates myocardial heat shock protein 72, endothelial nitric oxide synthase, and transcription factors NF{kappa}B and AP-1 Cardiovasc Res, July 1, 2000; 47(1): 49 - 56. [Abstract] [Full Text] [PDF]
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 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]
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T. Oxman, M. Shapira, A. Diver, R. Klein, N. Avazov, and B. Rabinowitz A new method of long-term preventive cardioprotection using Lactobacillus Am J Physiol Heart Circ Physiol, May 1, 2000; 278(5): H1717 - H1724. [Abstract] [Full Text] [PDF]
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R. D. Rakhit, R. J. Edwards, J. W. Mockridge, A. R. Baydoun, A. W. Wyatt, G. E. Mann, and M. S. Marber Nitric oxide-induced cardioprotection in cultured rat ventricular myocytes Am J Physiol Heart Circ Physiol, April 1, 2000; 278(4): H1211 - H1217. [Abstract] [Full Text] [PDF]
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M. Barton Sex and NO -- beyond regulation of vasomotor tone Cardiovasc Res, April 1, 2000; 46(1): 20 - 23. [Full Text] [PDF]
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N. Sasaki, T. Sato, A. Ohler, B. O’Rourke, and E. Marban Activation of Mitochondrial ATP-Dependent Potassium Channels by Nitric Oxide Circulation, February 1, 2000; 101(4): 439 - 445. [Abstract] [Full Text] [PDF]
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A. J. Spanier and K. H. McDonough Dexamethasone Blocks Sepsis-Induced Protection of the Heart from Ischemia Reperfusion Injury Experimental Biology and Medicine, January 1, 2000; 223(1): 82 - 87. [Abstract] [Full Text]
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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]
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R. Ockaili, V. R. Emani, S. Okubo, M. Brown, K. Krottapalli, and R. C. Kukreja Opening of mitochondrial KATP channel induces early and delayed cardioprotective effect: role of nitric oxide Am J Physiol Heart Circ Physiol, December 1, 1999; 277(6): H2425 - H2434. [Abstract] [Full Text] [PDF]
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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]
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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]
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C. Csonka, Z. Szilvassy, F. Fulop, T. Pali, I. E. Blasig, A. Tosaki, R. Schulz, and P. Ferdinandy Classic Preconditioning Decreases the Harmful Accumulation of Nitric Oxide During Ischemia and Reperfusion in Rat Hearts Circulation, November 30, 1999; 100(22): 2260 - 2266. [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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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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C. S.R. Baker, O. Rimoldi, P. G. Camici, E. Barnes, M. R. Chacon, T. Y. Huehns, D. O. Haskard, J. M. Polak, and R. J.C. Hall Repetitive myocardial stunning in pigs is associated with the increased expression of inducible and constitutive nitric oxide synthases Cardiovasc Res, August 15, 1999; 43(3): 685 - 697. [Abstract] [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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Q. Li, R. Bolli, Y. Qiu, X.-L. Tang, S. S. Murphree, and B. A. French Gene Therapy With Extracellular Superoxide Dismutase Attenuates Myocardial Stunning in Conscious Rabbits Circulation, October 6, 1998; 98(14): 1438 - 1448. [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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S. Pudupakkam, K. A. Harris, W. G. Jamieson, G. DeRose, J. A. Scott, M. W. Carson, M. G. Schlag, P. R. Kvietys, and R. F. Potter Ischemic tolerance in skeletal muscle: role of nitric oxide Am J Physiol Heart Circ Physiol, July 1, 1998; 275(1): H94 - H99. [Abstract] [Full Text] [PDF]
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