© 1999 American Heart Association, Inc.
Rapid Communication |
Nuclear Factor-
B Plays an Essential Role in the Late Phase of Ischemic Preconditioning in Conscious Rabbits
From the Experimental Research Laboratory, Division of Cardiology, University of Louisville and Jewish Hospital Heart and Lung Institute, Louisville, Ky.
Correspondence to Roberto Bolli, MD, Division of Cardiology, 3rd Floor ACB, 550 S Jackson St, University of Louisville, Louisville, KY 40292. E-mail rbolli{at}louisville.edu
Abstract—Although it is
recognized that late preconditioning (PC) results from upregulation of
cardioprotective genes, the specific transcription factor(s) that
govern this genetic adaptation remains unknown. The aim of this study
was to test the hypothesis that the development of late PC is mediated
by nuclear factor-
B (NF-B) and to elucidate the mechanisms that
control the activation of NF-B after an ischemic stimulus in
vivo. A total of 152 chronically instrumented, conscious rabbits were
used. A sequence of six 4-minute coronary occlusion/4-minute
reperfusion cycles, which elicits late PC, induced rapid activation of
NF-B, as evidenced by a marked increase in p65 content (+164%;
Western immunoblotting) and NF-B DNA binding
activity (+306%; electrophoretic mobility shift assay) in nuclear
extracts isolated 30 minutes after the last reperfusion. These changes
were attenuated 2 hours after ischemic PC and resolved by 4
hours. Competition and supershift assays confirmed the specificity of
the NF-B DNA complex signals. The mobility of the NF-B DNA
complex was shifted by anti-p65 and anti-p50 antibodies but not by
anti–c-Rel antibodies, indicating that the subunits of NF-B
involved in gene activation after ischemic PC consist of
p65-p50 heterodimers. Pretreatment with the NF-B
inhibitor diethyldithiocarbamate (DDTC; 150 mg/kg IP 15
minutes before ischemic PC) completely blocked the nuclear
translocation and increased DNA binding activity of NF-B. The same
dose of DDTC completely blocked the cardioprotective effects of late PC
against both myocardial stunning and myocardial infarction, indicating
that NF-B activation is essential for the development of this
phenomenon in vivo. The ischemic PC-induced activation of
NF-B was also blocked by pretreatment with
N
-nitro-L-arginine (L-NA), a
nitric oxide synthase (NOS) inhibitor,
N-2-mercaptopropionyl glycine (MPG), a reactive oxygen
species (ROS) scavenger, chelerythrine, a protein kinase C (PKC)
inhibitor, and lavendustin A, a tyrosine kinase
inhibitor (all given at doses previously shown to block
late PC), indicating that ischemic PC activates NF-B
via formation of NO and ROS and activation of PKC- and tyrosine
kinase–dependent signaling pathways. A subcellular redistribution and
increased DNA binding activity of NF-B quantitatively similar to
those induced by ischemic PC could be reproduced
pharmacologically by giving the NO donor diethylenetriamine/NO
(DETA/NO) (at a dose previously shown to elicit late PC), demonstrating
that NO in itself can activate NF-B in the heart. Taken
together, these results provide direct evidence that activation of
NF-B is a critical step in the signal transduction pathway that
underlies the development of the late phase of ischemic PC in
conscious rabbits. The finding that four different pharmacological
manipulations (L-NA, MPG, chelerythrine, and lavendustin A) produced
similar inhibition of NF-B suggests that this transcription factor
is a common downstream pathway through which multiple signals elicited
by ischemic stress (NO, ROS, PKC, tyrosine kinases) act to
induce gene expression. To our knowledge, this is the first
demonstration that NO can promote NF-B activation in the heart, a
finding that identifies a new biological function of NO and may have
important implications for various
pathophysiological conditions in which NO is
involved and for nitrate therapy.
Key Words: inducible nitric oxide synthase • myocardial ischemia/reperfusion • postischemic myocardial dysfunction • peroxynitrite • myocardial adaptation
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A. Lochner, E. Marais, S. Genade, and J. A. Moolman Nitric oxide: a trigger for classic preconditioning? Am J Physiol Heart Circ Physiol, December 1, 2000; 279(6): H2752 - H2765. [Abstract] [Full Text] [PDF]
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R. Bolli The Late Phase of Preconditioning Circ. Res., November 24, 2000; 87(11): 972 - 983. [Abstract] [Full Text] [PDF]
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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]
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Y.-T. Xuan, X.-L. Tang, Y. Qiu, S. Banerjee, H. Takano, H. Han, and R. Bolli Biphasic response of cardiac NO synthase isoforms to ischemic preconditioning in conscious rabbits Am J Physiol Heart Circ Physiol, November 1, 2000; 279(5): H2360 - H2371. [Abstract] [Full Text] [PDF]
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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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R. C. X. Li, P. Ping, J. Zhang, W. B. Wead, X. Cao, J. Gao, Y. Zheng, S. Huang, J. Han, and R. Bolli PKCepsilon modulates NF-kappa B and AP-1 via mitogen-activated protein kinases in adult rabbit cardiomyocytes Am J Physiol Heart Circ Physiol, October 1, 2000; 279(4): H1679 - H1689. [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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J. W. Mockridge, A. Punn, D. S. Latchman, M. S. Marber, and R. J. Heads PKC-dependent delayed metabolic preconditioning is independent of transient MAPK activation Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H492 - H501. [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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J. Sadoshima Cytokine Actions of Angiotensin II Circ. Res., June 23, 2000; 86(12): 1187 - 1189. [Full Text] [PDF]
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A. Dana, A. K. Jonassen, N. Yamashita, and D. M. Yellon Adenosine A1 Receptor Activation Induces Delayed Preconditioning in Rats Mediated by Manganese Superoxide Dismutase Circulation, June 20, 2000; 101(24): 2841 - 2848. [Abstract] [Full Text] [PDF]
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J. Liu, I. Ginis, M. Spatz, and J. M. Hallenbeck Hypoxic preconditioning protects cultured neurons against hypoxic stress via TNF-alpha and ceramide Am J Physiol Cell Physiol, January 1, 2000; 278(1): C144 - C153. [Abstract] [Full Text] [PDF]
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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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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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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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T. C. Zhao, M. M. Taher, K. C. Valerie, and R. C. Kukreja p38 Triggers Late Preconditioning Elicited by Anisomycin in Heart: Involvement of NF-{kappa}B and iNOS Circ. Res., November 9, 2001; 89(10): 915 - 922. [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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