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Role of Inflammation Following Myocardial Ischemia and Reperfusion

  • Nikolaos G. Frangogiannis
  • Mark L. Entman
Part of the Developments in Cardiovascular Medicine book series (DICM, volume 193)

Abstract

The purpose of this chapter is to discuss the potential mechanisms by which neutrophil-mediated inflammatory injury may complicate myocardial infarction. It should be emphasized that no one seriously proposes that the primary injury associated with myocardial infarction is inflammatory in nature. Rather, our goal is to describe mechanisms of reaction to injury and to present evidence suggesting that this secondary reaction might extend and complicate cardiac injury associated with ischemia.

Keywords

Myocardial Ischemia Cardiac Myocytes Myocardial Injury Cardiac Lymph Neutrophil Localization 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Hillis LD, Braunwald E. Myocardial ischemia. N Engl J Med 296:1093, 1977.PubMedCrossRefGoogle Scholar
  2. 2.
    Mallory GK, White PD, Salcedo-Salgar J. The speed of healing of myocardial infarction. A study of the pathologic anatomy in seventy-two cases. Am Heart J 18:647, 1939.CrossRefGoogle Scholar
  3. 3.
    Hearse DJ, Bolli R. Reperfusion-induced injury: Manifestations, mechanisms and clinical relevance. Trends Cardiovasc Med 1:233, 1993.CrossRefGoogle Scholar
  4. 4.
    Dreyer WJ, Michael LH, West MS, Smith CW, Rothlein R, Rossen RD, Anderson DC, Entman ML. Neutrophil accumulation in ischemic canine myocardium: Insights into the time course, distribution, and mechanism of localization during early reperfusion. Circulation 84:400, 1991.PubMedGoogle Scholar
  5. 5.
    Maroko PR, Carpenter CD, Chiariello M, Fishbein MC, Radvany P, Knostman JD, Hale SL. Reduction by cobra venom factor of myocardial necrosis after coronary artery occlusion. J Clin Invest 61:661, 1978.PubMedGoogle Scholar
  6. 6.
    Shappell SB, Taylor AA, Hughes H, Mitchell JR, Anderson DC, Smith CW. Comparison of antioxidant and nonantioxidant lipoxygenase inhibitors on neutrophil function. Implications for pathogenesis of myocardial reperfusion injury. J Pharmacol Exp Ther 252:531, 1990.PubMedGoogle Scholar
  7. 7.
    Simpson RJ, Mickelson J, Fantone JC, Gallagher KP, Lucchesi BR. Iloprost inhibits neutrophil function in vitro and in vivo and limits experimental infarct size in canine heart. Circ Res 60:666, 1987.PubMedGoogle Scholar
  8. 8.
    Olafsson B, Forman MB, Puett DW, Pou A, Cates CU, Friessinger GC, Virmani R. Reduction of reperfusion injury in the canine preparation by intracoronary adenosine: Importance of the endothelium and the no-reflow phenomenon. Circulation 76:1135, 1987.PubMedGoogle Scholar
  9. 9.
    Romson JL, Hook BG, Kunkel SL, Abrams GD, Schork MA, Lucchesi BR. Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 67:1016, 1983.PubMedGoogle Scholar
  10. 10.
    Mullane KM, Read N, Salmon JA, Moneada S. Role of leukocytes in acute myocardial infarction in anesthesthized dogs. Relationship to myocardial salvage by anti-inflammatory drugs. J Pharmacol Exp Ther 228:510, 1984.PubMedGoogle Scholar
  11. 11.
    Engler RL, Dahlgren MD, Morris DD, Peterson MA, Schmid-Schonbein GW, Role of leukocytes in response to acute myocardial ischemia and reflow in dogs. Am J Physiol 251:H314, 1986.PubMedGoogle Scholar
  12. 12.
    Jolly SR, Kane WJ, Bailie MB, Abrams GD, Lucchesi BR. Canine myocardial reperfusion injury: Its reduction by the combined administration of superoxide dismutase and catalase. Circ Res 54:277, 1984.PubMedGoogle Scholar
  13. 13.
    Lucchesi BR, Mullane KM. Leukocytes and ischemia induced myocardial injury. Ann Rev Pharm Tox 26:201, 1986.CrossRefGoogle Scholar
  14. 14.
    Roberts R, DeMello V, Sobel BE. Deleterious effects of methylprednisolone in patients with myocardial infarction. Circulation 53(Suppl. I):204, 1976.Google Scholar
  15. 15.
    Hammerman H, Kloner RA, Hale S, Schoen FJ, Braunwald E. Dose-dependent effects of short-term methylprednisolone on mycardial infarct extent, scar formation, and ventricular function. Circulation 68:446, 1983.PubMedGoogle Scholar
  16. 16.
    Hill JH, Ward PA. The phlogistic role of C3 leukotactic fragment in myocardial infarcts of rats. J Exp Med 133:885, 1971.PubMedCrossRefGoogle Scholar
  17. 17.
    Pinckard RN, Olson MS, Kelley RE, Detter DH, Palmer JD, O’Rourke RA, Goldfein S. Antibodyindependent activation of human C1 after interaction with heart subcellular membranes. J Immunol 110:1376, 1973.PubMedGoogle Scholar
  18. 18.
    Pinckard RN, Olson MS, Giclas PC, Terry R, Boyer JT, O’Rourke RA. Consumption of classical complement components by heart subcellular membranes in vitro and in patients after acute myocardial infarction. J Clin Invest 56:740, 1975.PubMedGoogle Scholar
  19. 19.
    Rossen RD, Swain JL, Michael LH, Weakley S, Giannini E, Entman ML. Selective accumulation of the first component of complement and leukocytes in ischemic canine heart muscle: A possible initiator of an extra myocardial mechanism of ischemic injury. Circ Res 57:119, 1985.PubMedGoogle Scholar
  20. 20.
    Rossen RD, Michael LH, Kagiyama A, Savage HE, Hanson G, Reisbery JN, Moake JN, Kim SH, Weakly S, Giannini E, Entman ML. Mechanism of complement activation following coronary artery occlusion: Evidence that myocardial ischemia causes release of constituents of myocardial subcellular origin which complex with the first component of complement. Circ Res 62:572, 1988.PubMedGoogle Scholar
  21. 21.
    Rossen RD, Michael LH, Hawkins HK, Youker K, Dreyer WJ, Baughn RE, Entman ML. Cardiolipinprotein complexes and initiation of complement activation after coronary artery occlusion. Circ Res 75:546, 1994.PubMedGoogle Scholar
  22. 22.
    Dreyer WJ, Smith CW, Michael LH, Rossen RD, Hughes BJ, Entman ML, Anderson DC. Canine neutrophil activation by cardiac lymph obtained during reperfusion of ischemic myocardium. Circ Res 65:1751, 1989.PubMedGoogle Scholar
  23. 23.
    Dreyer WJ, Michael LH, Rossen RD, Nguyen T, Anderson DC, Smith CW, Entman ML. Evidence for C5a in post-ischemic canine cardiac lymph (abstr). Clin Res 39:271, 1991.Google Scholar
  24. 24.
    Weisman HF, Barton T, Leppo MK, Marsh HC Jr, Carson GR, Concino MF, Boyle MP, Roux KH, Weisfeldt ML, Fearon DT. Soluble human complement receptor type 1: In vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science 249:146, 1990.PubMedCrossRefGoogle Scholar
  25. 25.
    Buerke M, Murohara T, Lefer AM. Cardioprotective effects of a C1 esterase inhibitor in myocardial ischemia and reperfusion. Circulation 91:393, 1995.PubMedGoogle Scholar
  26. 26.
    Miller MD, Krangel MS. Biology and biochemistry of the chemokines: A family of chemotactic and inflammatory cytokines. Crit Rev Immunol 12:17, 1992.PubMedGoogle Scholar
  27. 27.
    Baggiolini M, Moser B, Clark-Lewis I. Interleukin-8 and related chemotactic cytokines. The Giles Filley Lecture. Chest 105:95S, 1994.Google Scholar
  28. 28.
    Baggiolini M, Dewald B, Moser B. Interleukin-8 and related chemotactic cytokines—CXC and CC chemokines. Adv Immunol 55:97, 1994.PubMedGoogle Scholar
  29. 29.
    Baggiolini M, Dewald B, Walz A. Interleukin-8 and related chemotactic cytokines. In Gallin JI, Goldstein IM, Snyderman R (eds). Inflammation: Basic Principles and Clinical Correlates. New York: Raven Press, 1992:247.Google Scholar
  30. 30.
    Baggiolini M, Walz A, Kunkel SL. Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. J Clin Invest 84:1045, 1989.PubMedGoogle Scholar
  31. 31.
    Sekido N, Mukaida N, Harada A, Nakanishi I, Watanabe Y, Matsushima K. Prevention of lung reperfusion injury in rabbits by a monoclonal antibody against interleukin-8. Nature 365:654, 1993.PubMedCrossRefGoogle Scholar
  32. 32.
    Kukielka GL, Smith CW, LaRosa GJ, Manning AM, Mendoza LH, Hughes BJ, Youker KA, Hawkins HK, Michael LH, Rot A, Entman ML. Interleukin-8 gene induction in the myocardium following ischemia and reperfusion in vivo. J Clin Invest 95:89, 1995.PubMedCrossRefGoogle Scholar
  33. 33.
    Ivey CL, Williams FM, Collins PD, Jose PJ, Williams TJ. Neutrophil chemoattractants generated in two phases during reperfusion of ischemic myocardium in the rabbit. J Clin Invest 95:2720, 1995.PubMedCrossRefGoogle Scholar
  34. 34.
    Mehta J, Dinerman J, Mehta P, Saldeen TG, Lawson D, Donnelly WH, Wallin R. Neutrophil function in ischemic heart disease. Circulation 79:549, 1989.PubMedGoogle Scholar
  35. 35.
    Carry M, Korley V, Willerson JT, Weigelt L, Ford-Hutchinson AW, Tagari P. Increased urinary leukotriene excretion in patients with cardiac ischemia. In vivo evidence for 5-lipoxygenase activation. Circulation 85:230, 1992.PubMedGoogle Scholar
  36. 36.
    Mullane KM, Salmon JA, Kraemer R. Leukocyte-derived metabolites of arachidonic acid in ischemiainduced myocardial injury. Fed Proc 46:2422, 1987.PubMedGoogle Scholar
  37. 37.
    Hahn RA, MacDonald BR, Simpson PJ, Potts BD, Parli CJ. Antagonism of leukotriene B4 receptors does not limit canine myocardial infarct size. J Pharmacol Exp Ther 253:58, 1990.PubMedGoogle Scholar
  38. 38.
    Taylor AA, Gasic AC, Kitt TM, Shappell SB, Rui J, Lenz ML, Smith CW, Mitchell JR. A specific leukotriene B4 antagonist protects against myocardial ischemia-reflow injury (abstr). Clin Res 37:528, 1989.Google Scholar
  39. 39.
    Zimmerman GA, McIntyre TM, Mehra M, Prescott SM. Endothelial cell-associated platelet-activating factor: A novel mechanism for signaling intercellular adhesion. J Cell Biol 110:529, 1990.PubMedCrossRefGoogle Scholar
  40. 40.
    Stahl GL, Terashita Z, Lefer AM. Role of platelet activating factor in propagation of cardiac damage during myocardial ischemia. J Pharmacol Exp Ther 244:898, 1988.PubMedGoogle Scholar
  41. 41.
    Petrone WF, English DK, Wong K, McCord JM. Free radicals and inflammation: Superoxidedependent activation of a neutrophil chemotactic factor in plasma. Proc Natl Acad Sci USA 77:1159, 1980.PubMedCrossRefGoogle Scholar
  42. 42.
    Granger DN. Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 255:H1269, 1988.PubMedGoogle Scholar
  43. 43.
    Inauen W, Granger DN, Meininger CJ, Schelling ME, Granger HJ, Kvietys PR. Anoixa/reoxygenationinduced, neutrophil-mediated endothelial cell injury: Role of elastase. Am J Physiol 259:H925, 1990.PubMedGoogle Scholar
  44. 44.
    Suzuki M, Onauen W, Kiretys PR, Grisham MB, Meininger C, Schelling ME, Granger HJ, Granger DN. Superoxide mediates reperfusion-induced leukocyte-endothelial cell interactions. Am J Physiol H1740, 1989.Google Scholar
  45. 45.
    Shingu M, Nobunaga M. Chemotactic activity generated in human serum from the fifth component on hydrogen peroxide. Am J Pathol 117:210, 1984.Google Scholar
  46. 46.
    Patel KD, Zimmerman GA, Prescott SM, McEver RP, McIntyre TM. Oxygen radicals induce human endothelial cells to express GMP-140 and bind neutrophils. J Cell Biol 112:749, 1991.PubMedCrossRefGoogle Scholar
  47. 47.
    Smiley PL, Stremler KE, Prescott SM, Zimmerman GA, McIntyre TM. Oxidatively fragmented phosphatidylcholines activate human neutrophils through the receptor for platelet-activating factor. J Biol Chem 266:11104, 1991.PubMedGoogle Scholar
  48. 48.
    Sellak H, Franzini E, Hakim J, Pasquier C. Reactive oxygen species repidly increase endothelial ICAM-l ability to bind neutrophils without detectable upregulation. Blood 83:2669, 1994.PubMedGoogle Scholar
  49. 49.
    Michael LH, Zhang Z, Hartley CJ, Bolli R, Taylor AA, Entman ML. Thromboxane B2 in cardiac lymph: Effect of superoxide dismutase and catalase during myocardial ischemia and reperfusion. Circ Res 66:1040, 1990.PubMedGoogle Scholar
  50. 50.
    Mullane KM, Westlin W, Kraemer R. Activated neutrophils release mediators that may contribute to myocardial dysfunction associated with ischemia and reperfusion. In Biology of the Leukotrienes. New York: New York Academy of Sciences, 1988:103.Google Scholar
  51. 51.
    Engler RL, Dahlgren MD, Peterson MA, Dobbs A, Schmid-Schonbein GW. Accumulation of polymorphonuclear leukocytes during 3h experimental myocardial ischemia. Am J Physiol 251:H93, 1986.PubMedGoogle Scholar
  52. 52.
    Hernandez LA, Grisham MB, Twohig B, Arfors KE, Harlan JM, Granger DN. Role of neutrophils in ischemia-reperfusion-induced microvascular injury. Am J Physiol 238:H699, 1987.Google Scholar
  53. 53.
    Ambrosio G, Weisman HF, Baker LC. The no-reflow phenomenon: A misnomer. Circulation 74:II260, 1986.Google Scholar
  54. 54.
    Ambrosio G, Weisman HF, Mannisi JA, Becker LC. Progressive impairment of regional myocardial perfusion after initial restoration of post ischemic blood flow. Circulation 80:1846, 1989.PubMedGoogle Scholar
  55. 55.
    Adams DH, Shaw S. Leukocyte-endothelial interactions and regulation of leukocyte migration. Lancet 343:831, 1994.PubMedCrossRefGoogle Scholar
  56. 56.
    Bevilacqua MP, Butcher E, Furie B, Gallatin M, Gimbrone MA, Harlan JM, Kishimoto TK, Lasky LA, McEver RP, Paulson JC, Rosen SD, Seed B, Siegelman M, Springer TA, Stoolman LM, Tedder TF, Varki A, Wagner DD, Weissman IL, Zimmerman GA. Selectins: A family of adhesion receptors. Cell 67:233, 1991.PubMedCrossRefGoogle Scholar
  57. 57.
    Lasky LA. Selectins: Interpretors of cell-specific carbohydrate information during inflammation. Science 258:964, 1992.PubMedCrossRefGoogle Scholar
  58. 58.
    Tedder TF, Steeber DA, Chen A, Engel P. The selectins: Vascular adhesion molecules. FASEB J 9:866, 1995.PubMedGoogle Scholar
  59. 59.
    Lasky LA, Presta LG, Erbe DV. Structure-function aspects of selectin-carbohydrate interactions. Molecular definition to therapeutic potential. In Metcalf BW, Dalton BJ, Poste G (eds). Cellular Adhesion. New York: Plenum Press, 1994:37.Google Scholar
  60. 60.
    Kishimoto TK, Jutila MA, Berg EL, Butcher EC. Neutrophil Mac-1 and MEL-14 adhesion proteins inversely regulated by chemotactic factors. Science 245:1238, 1989.PubMedCrossRefGoogle Scholar
  61. 61.
    Smith CW, Kishimoto TK, Abbassi O, Hughes BJ, Rothlein R, McIntire LV, Butcher E, Anderson DC. Chemotactic factors regulare lectin adhesion molecule 1 (LECAM-1)-dependent neutrophil adhesion to cytokine-stimulated endothelial cells in vitro. J Clin Invest 87:609, 1991.PubMedGoogle Scholar
  62. 62.
    Bevilacqua MP, Stengelin S, Gimbrone Jr, Seed B. Endothelial leukocyte adhesion molecule 1: An inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 243:1160, 1989.PubMedCrossRefGoogle Scholar
  63. 63.
    Altieri DC, Edgington TS. The saturable high affinity association of Factor X to ADP-stimulated monocytes defines a novel function of the Mac-1 receptor. J Biol Chem 263:7007, 1988.PubMedGoogle Scholar
  64. 64.
    Geng JG, Bevilacqua MP, Moore KL, McIntyre TM, Prescott SM, Kim JM, Bliss GA, Zimmerman GA, McEver RP. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature 343:757, 1990.PubMedCrossRefGoogle Scholar
  65. 65.
    Frangogiannis NG, Youker KA, Kukielka GL, Breasler RB, Michael LH, Spengler RN, Smith CW, Entman ML. Resident cardiac mast cells degranulate and release preformed TNF-α during ischemia/ reperfusion injury. J Invest Med 43:313, 1995.Google Scholar
  66. 66.
    Picker LJ, Warnock RA, Burns AR, Doerschuk CM, Berg EL, Butcher EC. The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell 66:921, 1991.PubMedCrossRefGoogle Scholar
  67. 67.
    Ma X-L, Weyrich AS, Lefer DJ, Buerke M, Albertine KH, Kishimoto TK, Lefer AM. Monoclonal antibody to L-selectin attenuates neutrophil accumulation and protects ischemic reperfused cat myocardium. Circulation 88:649, 1993.PubMedGoogle Scholar
  68. 68.
    Weyrich AS, Ma X-L, Lefer DJ, Albertine KH, Lefer AM. In vivo neutralization of P-selectin protects feline heart and endothelium in myocardial ischemia and reperfusion injury. J Clin Invest 91:2620, 1993.PubMedGoogle Scholar
  69. 69.
    Albelda SM, Smith CW, Ward PA. Adhesion molecules and inflammatory injury. FASEB J 8:504, 1994.PubMedGoogle Scholar
  70. 70.
    Luscinskas FW, Lawler J. Integrins as dynamic regulators of vasular function. FASEB J 8:929, 1994.PubMedGoogle Scholar
  71. 71.
    Anderson DC. The role of beta-2 integrins and intercellular adhesion molecule type I in inflammation. In Granger DN, Schmid-Schonbein GW (eds). Physiology and Pathophysiology of Leukocyte Adhesion. New York: Oxford University Press, 1995:3.Google Scholar
  72. 72.
    Smith CW, Marlin SD, Rothlein R, Toman C, Anderson DC. Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro. J Clin Invest 83:2008, 1989.PubMedGoogle Scholar
  73. 73.
    Fehr J, Moser R, Leppert D, Groscurth P. Antiadhesive properties of biological surfaces are protective against stimlated granulocytes. J Clin Invest 76:535, 1985.PubMedGoogle Scholar
  74. 74.
    Simpson PJ, Todd III, Fantone JC, Mickelson JK, Griffin JD, Lucchesi BR. Reduction of experimental canine myocardial reperfusion injury by a monoclonal antibody (anti-Mol. anti-CD11b) that inhibits leukocyte adhesion. J Clin Invest 81:624, 1988.PubMedGoogle Scholar
  75. 75.
    Simpson PJ, Todd III, Mickelson JK, Fantone JC, Gallagher KP, Lee KA, Tamura Y, Cronin M, Lucchesi BR. Sustained limitation of myocardial reperfusion injury by a monoclonal antibody that alters leukocyte function. Circulation 81:226, 1990.PubMedGoogle Scholar
  76. 76.
    Seewaldt-Becker E, Rothlein R, Dammgen JW. CDw 18 dependent adhesion of leukocytes to endothelium and its relevance for cardiac reperfusion. In Springer TA, Anderson DC, Rosenthal AS, Rothlein R (eds). Leukocyte Adhesion Molecules: Structure, Function, and Regulation. New York: Springer-Verlag, 1989:138.Google Scholar
  77. 77.
    Williams FM, Collins PD, Nourshargh S, Williams TJ. Suppression of 111 In-neutrophil accumlation in rabbit mycoardium by MoA isechmic injury. J Mol Cell Cardiol 20:S33, 1989.Google Scholar
  78. 78.
    Lefer DJ, Suresh ML, Shandelya ML, Serrano CV, Becker LC, Kuppusamy P, Zweier JL. Cardio-protective actions of a monoclonal antibody against CD-18 in myocardial ischemia-reperfusion injury. Circulation 88:1779, 1993.PubMedGoogle Scholar
  79. 79.
    Aversano T, Zhou W, Nedelman M, Nakada M, Weisman H. A chimeric IgG4 monoclonal antibody directed against CD18 reduces infarct size in a primate model of myocardial ischemia and reperfusion. J Am Coll Cardiol 25:781, 1995.PubMedCrossRefGoogle Scholar
  80. 80.
    Ballantyne CM, Smith CW, Beaudet A, Yagita H, Dai XY. Endothelial-leukocyte cell adhesion molecules in cardiac allograft rejection (abstr). Circulation 88:I419, 1993.Google Scholar
  81. 81.
    Ma XL, Tsao PS, Lefer AM. Antibody to CD18 exerts endothelial and cardiac protective effects in myocardial ischemia and reperfusion. J Clin Invest 88:1237, 1991.PubMedGoogle Scholar
  82. 82.
    Carden DL, Smith JK, Korthuis RJ. Neutrophilmediated microvascular dysfunction in postischemic canine skeletal muscle. Role of granulocyte adherence. Circ Res 66:1436, 1990.PubMedGoogle Scholar
  83. 83.
    Hughes BJ, Hollers JC, Crockett-Torabi E, Smith CW. Recruitment of CD11b/CD18 to the neutrophil surface and adherence-dependent cell locomotion. J Clin Invest 90:1687, 1992.PubMedGoogle Scholar
  84. 84.
    Muller WA. The role of PECAM-1 (CD31) in leukocyte emigration: Studies in vitro and in vivo. J Leukoc Biol 57:523, 1995.PubMedGoogle Scholar
  85. 85.
    Muller WA, Weigl SA, Deng X, Phillips DM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med 178:449, 1993.PubMedCrossRefGoogle Scholar
  86. 86.
    Cooper D, Lindberg FP, Gamble JR, Brown EJ, Vadas MA. Transendothelial migration of neutrophils involves integrin-associated protein (CD47). Proc Natl Acad Sci USA 92:3978, 1995.PubMedCrossRefGoogle Scholar
  87. 87.
    Shappell SB, Toman C, Anderson DC, Taylor AA, Entman ML, Smith CW. Mac-1 (CD11b/CD18) mediates adherence-dependent hydrogen peroxide production by human and canine neutrophils. J Immunol 144:2702, 1990.PubMedGoogle Scholar
  88. 88.
    Entman ML, Youker KA, Shoji T, Kukielka GL, Shappell SB, Taylor AA, Smith CW. Neutrophil induced oxidative injury of cardiac myocytes: A compartmented system requiring CD11b/ CD18-ICAM-1 adherence. J Clin Invest 90:1335, 1992.PubMedCrossRefGoogle Scholar
  89. 89.
    Smith CW, Entman ML, Lane CL, Beaudet AL, Ty TI, Youker KA, Hawkins HK, Anderson DC. Adherence of neutrophils to canine cardiac myocytes in vitro is dependent on intercellular adhesion molecule1. J Clin Invest 88:1216, 1991.PubMedGoogle Scholar
  90. 90.
    Youker KA, Smith CW, Anderson DC, Miller D, Michael LH, Rossen RD, Entman ML. Neutrophil adherence to isolated adult cardiac myocytes: Induction by cardiac lymph collected during ischemia and reperfusion. J Clin Invest 89:602, 1992.PubMedGoogle Scholar
  91. 91.
    Entman ML, Youker KA, Shappell SB, Siegel C, Rothlein R, Dreyer WJ, Schmalstieg FC, Smith CW. Neutrophil adherence to isolated adult canine myocytes: Evidence for a CD18-dependent mechanism. J Clin Invest 85:1497, 1990.PubMedCrossRefGoogle Scholar
  92. 92.
    Weitz JI, Huang AJ, Landman SL, et al. Elastasemediated fibrinogenolysis by chemoattraccantstimulated neutrophils occurs in the presence of physiologic concentrations of anti-proteinases. J Exp Med 166:1836, 1987.PubMedCrossRefGoogle Scholar
  93. 93.
    Dreyer WJ, Michael LH, Nguyen T, Smith CW, Anderson DC, Entman ML, Rossen RD. Kinetics of C5a release in cardic lymph of dogs experiencing coronary artery ischemia-reperfusion injury. Circ Res 71:1518, 1992.PubMedGoogle Scholar
  94. 94.
    Kukielka GL, Hawkins HK, Michael LH, Manning AM, Lane CL, Entman ML, Smith CW, Anderson DC. Regulation of intercellular adhesion molecule-1 (ICAM-1) in ischemic and reperfused canine myocardium. J Clin Invest 92:1504, 1993.PubMedGoogle Scholar
  95. 95.
    Youker KA, Hawkins HK, Kukielka GL, Perrard JL, Michael LH, Ballantyne CM, Smith CW, Entman ML. Molecular evidence for induction of intercellular adhesion molecule-1 in the viable border zone associated with ischemia-reperfusion injury of the dog heart. Circulation 89:2736, 1994.PubMedGoogle Scholar
  96. 96.
    Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94:1621, 1994.PubMedGoogle Scholar
  97. 97.
    Kukielka GL, Smith CW, Manning AM, Youker KA, Michael LH, Entman ML. Induction of Interleukin6 synthesis in the myocardium: Potential role in post-reperfusion inflammatory injury. Circulation 92:1866, 1995.PubMedGoogle Scholar
  98. 98.
    Kharazmi A, Mielsen H, Rechnitzer C, Bendtzen K. Interleukin 6 primes human neutrophil and monocyte oxidative burst response. Immunol Lett 21:177, 1989.PubMedCrossRefGoogle Scholar
  99. 99.
    Birdsall HH, Green DM, Trial JA, Youker KA, Entman ML, Michael LH, Rossen RD. Reperfusion of ischemic myocardium releases TGF-beta, MCP-1 and C5a into cardiac extracellular fluids and stimulates transendothelial migration of TNF-alpha and IL-1 secreting monocytes (abstr). Circulation I-711, 1995.Google Scholar
  100. 100.
    Kumar AG, Ballantyne CM, Ty MT, Kukielka GL, Michael LH, Entman ML. Cardiac reperfusion initiates the induction of monocyte chemoattractant molecule-1 and vascular cell adhesion molecule-1. Circulation 90:I427, 1994.Google Scholar

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© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Nikolaos G. Frangogiannis
  • Mark L. Entman

There are no affiliations available

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