© 1999 by European Society of Cardiology
Copyright © 1999, European Society of Cardiology
The role of neutrophils in myocardial ischemia–reperfusion injury
The Cardiothoracic Research Laboratory, Carlyle Fraser Heart Center of Crawford Long Hospital, 550 Peachtree Street N.E., Atlanta, GA 30365, USA
* Corresponding author. Tel.: +1-404-686-2511; fax: +1-404-686-4888 jvinten{at}emory.edu
Reperfusion of ischemic myocardium is necessary to salvage tissue from eventual death. However, reperfusion after even brief periods of ischemia is associated with pathologic changes that represent either an acceleration of processes initiated during ischemia per se, or new pathophysiological changes that were initiated after reperfusion. This ‘reperfusion injury’ shares many characteristics with inflammatory responses in the myocardium. Neutrophils feature prominently in this inflammatory component of postischemic injury. Ischemia–reperfusion prompts a release of oxygen free radicals, cytokines and other proinflammatory mediators that activate both the neutrophils and the coronary vascular endothelium. Activation of these cell types promotes the expression of adhesion molecules on both the neutrophils and endothelium, which recruits neutrophils to the surface of the endothelium and initiates a specific cascade of cell–cell interactions, leading first to adherence of neutrophils to the vascular endothelium, followed later by transendothelial migration and direct interaction with myocytes. This specific series of events is a prerequisite to the phenotypic expression of reperfusion injury, including endothelial dysfunction, microvascular collapse and blood flow defects, myocardial infarction and apoptosis. Pharmacologic therapy can target the various components in this critical series of events. Effective targets for these pharmacologic agents include: (a) inhibiting the release or accumulation of proinflammatory mediators, (b) altering neutrophil or endothelial cell activation and (c) attenuating adhesion molecule expression on endothelium, neutrophils and myocytes. Monoclonal antibodies to adhesion molecules (P-selectin, L-selectin, CD11, CD18), complement fragments and receptors attenuate neutrophil-mediated injury (vascular injury, infarction), but clinical application may encounter limitations due to antigen–antibody reactions with the peptides. Humanized antibodies and non-peptide agents, such as oligosaccharide analogs to sialyl Lewisx, may prove effective in this regard. Both nitric oxide and adenosine exhibit broad spectrum effects against neutrophil-mediated events and, therefore, can intervene at several critical points in the ischemic–reperfusion response, and may offer greater benefit than agents that interdict at a single point in the cascade. The understanding of the molecular processes regulating actions of neutrophils in ischemic–reperfusion injury may be applicable to other clinical situations, such as trauma, shock and organ or tissue (i.e. vascular conduits) transplantation.
KEYWORDS Neutrophils; Endothelium; Nitric oxide; Adenosine; Infarction; Reperfusion injury; Inflammation; Monoclonal antibodies
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S. Zahler, A. Hoffmann, T. Gloe, and U. Pohl Gap-junctional coupling between neutrophils and endothelial cells: a novel modulator of transendothelial migration J. Leukoc. Biol., January 1, 2003; 73(1): 118 - 126. [Abstract] [Full Text] [PDF]
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S. Muraki, C. D. Morris, J. M. Budde, Z.-Q. Zhao, R. A. Guyton, and J. Vinten-Johansen Blood cardioplegia supplementation with the sodium-hydrogen ion exchange inhibitor cariporide to attenuate infarct size and coronary artery endothelial dysfunction after severe regional ischemia in a canine model J. Thorac. Cardiovasc. Surg., January 1, 2003; 125(1): 155 - 164. [Abstract] [Full Text] [PDF]
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J. Vinten-Johansen, Z.-Q. Zhao, and R. A. Guyton Cardiac Surgical Physiology Card. Surg. Adult, January 1, 2003; 2(2003): 53 - 84. [Full Text]
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K. A. Detillieux, F. Sheikh, E. Kardami, and P. A. Cattini Biological activities of fibroblast growth factor-2 in the adult myocardium Cardiovasc Res, January 1, 2003; 57(1): 8 - 19. [Abstract] [Full Text] [PDF]
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N. Daddi, T. Suda, F. D'Ovidio, S. A. Kanaan, T. Tagawa, K. Grapperhaus, B. D. Kozower, J. H. Ritter, N. S Yew, T. Mohanakumar, et al. Recipient intramuscular cotransfection of naked plasmid transforming growth factor {beta}1 and interleukin 10 ameliorates lung graft ischemia-reperfusion injury J. Thorac. Cardiovasc. Surg., August 1, 2002; 124(2): 259 - 269. [Abstract] [Full Text] [PDF]
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L. M. Riou, M. Ruiz, G. W. Sullivan, J. Linden, H. Leong-Poi, J. R. Lindner, T. D. Harris, G. A. Beller, and D. K. Glover Assessment of Myocardial Inflammation Produced by Experimental Coronary Occlusion and Reperfusion With 99mTc-RP517, a New Leukotriene B4 Receptor Antagonist That Preferentially Labels Neutrophils In Vivo Circulation, July 30, 2002; 106(5): 592 - 598. [Abstract] [Full Text] [PDF]
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Q.-D. Wang, J. Pernow, P.-O. Sjoquist, and L. Ryden Pharmacological possibilities for protection against myocardial reperfusion injury Cardiovasc Res, July 1, 2002; 55(1): 25 - 37. [Abstract] [Full Text] [PDF]
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J. T. Colston, B. Chandrasekar, and G. L. Freeman A Novel Peroxide-induced Calcium Transient Regulates Interleukin-6 Expression in Cardiac-derived Fibroblasts J. Biol. Chem., June 21, 2002; 277(26): 23477 - 23483. [Abstract] [Full Text] [PDF]
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S. Verma, P. W.M. Fedak, R. D. Weisel, J. Butany, V. Rao, A. Maitland, R.-K. Li, B. Dhillon, and T. M. Yau Fundamentals of Reperfusion Injury for the Clinical Cardiologist Circulation, May 21, 2002; 105(20): 2332 - 2336. [Full Text] [PDF]
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S. C. Stoica, M. Goddard, and S. R. Large The endothelium in clinical cardiac transplantation Ann. Thorac. Surg., March 1, 2002; 73(3): 1002 - 1008. [Abstract] [Full Text] [PDF]
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D. Paparella, T.M. Yau, and E. Young Cardiopulmonary bypass induced inflammation: pathophysiology and treatment. An update Eur. J. Cardiothorac. Surg., February 1, 2002; 21(2): 232 - 244. [Abstract] [Full Text] [PDF]
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A. K. Thukkani, F.-F. Hsu, J. R. Crowley, R. B. Wysolmerski, C. J. Albert, and D. A. Ford Reactive Chlorinating Species Produced during Neutrophil Activation Target Tissue Plasmalogens. PRODUCTION OF THE CHEMOATTRACTANT, 2-CHLOROHEXADECANAL J. Biol. Chem., February 1, 2002; 277(6): 3842 - 3849. [Abstract] [Full Text] [PDF]
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B. I. Jugdutt Monocytosis and adverse left ventricular remodeling after reperfused myocardial infarction J. Am. Coll. Cardiol., January 16, 2002; 39(2): 247 - 250. [Full Text] [PDF]
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M. Chello, P. Mastroroberto, A. Quirino, G. Cuda, F. Perticone, F. Cirillo, and E. Covino Inhibition of neutrophil apoptosis after coronary bypass operation with cardiopulmonary bypass Ann. Thorac. Surg., January 1, 2002; 73(1): 123 - 129. [Abstract] [Full Text] [PDF]
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J. Bao, K. Sato, M. Li, Y. Gao, R. Abid, W. Aird, M. Simons, and M. J. Post PR-39 and PR-11 peptides inhibit ischemia-reperfusion injury by blocking proteasome-mediated Ikappa Balpha degradation Am J Physiol Heart Circ Physiol, December 1, 2001; 281(6): H2612 - H2618. [Abstract] [Full Text] [PDF]
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T.-l. Yue, J. Chen, W. Bao, P. K. Narayanan, A. Bril, W. Jiang, P. G. Lysko, J.-L. Gu, R. Boyce, D. M. Zimmerman, et al. In Vivo Myocardial Protection From Ischemia/Reperfusion Injury by the Peroxisome Proliferator-Activated Receptor-{gamma} Agonist Rosiglitazone Circulation, November 20, 2001; 104(21): 2588 - 2594. [Abstract] [Full Text] [PDF]
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R. Schulz, M. V Cohen, M. Behrends, J. M Downey, and G. Heusch Signal transduction of ischemic preconditioning Cardiovasc Res, November 1, 2001; 52(2): 181 - 198. [Full Text] [PDF]
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S. C. Stoica, D. K. Satchithananda, J. Dunning, and S. R. Large Two-decade analysis of cardiac storage for transplantation Eur. J. Cardiothorac. Surg., October 1, 2001; 20(4): 792 - 798. [Abstract] [Full Text] [PDF]
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M. LA, M. D'AMICO, S. BANDIERA, C. DI FILIPPO, S. M. OLIANI, F. N. E. GAVINS, R. J. FLOWER, and M. PERRETTI Annexin 1 peptides protect against experimental myocardial ischemia-reperfusion: analysis of their mechanism of action FASEB J, October 1, 2001; 15(12): 2247 - 2256. [Abstract] [Full Text] [PDF]
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R. T. Smolenski, O. Raisky, E. M. Slominska, H. Abunasra, K. K. Kalsi, J. Jayakumar, K. Suzuki, and M. H. Yacoub Protection From Reperfusion Injury After Cardiac Transplantation by Inhibition of Adenosine Metabolism and Nucleotide Precursor Supply Circulation, September 18, 2001; 104 (2009): I-246 - I-252. [Abstract] [Full Text] [PDF]
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T. Rui, G. Cepinskas, Q. Feng, Y.-S. Ho, and P. R. Kvietys Cardiac myocytes exposed to anoxia-reoxygenation promote neutrophil transendothelial migration Am J Physiol Heart Circ Physiol, July 1, 2001; 281(1): H440 - H447. [Abstract] [Full Text] [PDF]
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A. Iwata, S. Sai, Y. Nitta, M. Chen, R. de Fries-Hallstrand, J. Dalesandro, R. Thomas, and M. D. Allen Liposome-Mediated Gene Transfection of Endothelial Nitric Oxide Synthase Reduces Endothelial Activation and Leukocyte Infiltration in Transplanted Hearts Circulation, June 5, 2001; 103(22): 2753 - 2759. [Abstract] [Full Text] [PDF]
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J. Pernow, A.T. Gonon, and A. Gourine The role of the endothelium for reperfusion injury Eur. Heart J. Suppl., June 1, 2001; 3(suppl_C): C22 - C27. [Abstract] [PDF]
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B. Chandrasekar, J. B. Smith, and G. L. Freeman Ischemia-Reperfusion of Rat Myocardium Activates Nuclear Factor-{{kappa}}B and Induces Neutrophil Infiltration Via Lipopolysaccharide-Induced CXC Chemokine Circulation, May 8, 2001; 103(18): 2296 - 2302. [Abstract] [Full Text] [PDF]
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C. Seligmann, A. Bock, T. Leitsch, M. Schimmer, Y. Simsek, and H.-P. Schultheiss Polymorphonuclear granulocytes induce myocardial dysfunction during ischemia and in later reperfusion of hearts exposed to low-flow ischemia J. Leukoc. Biol., May 1, 2001; 69(5): 727 - 731. [Abstract] [Full Text]
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