Molecular and Cellular Biochemistry

, Volume 179, Issue 1–2, pp 169–187

Inflammatory responses to ischemia, and reperfusion in skeletal muscle

  • Dean C Gute
  • Tetsuya Ishida
  • Koji Yarimizu
  • Ronald J. Korthius
Article

Abstract

Skeletal muscle ischemia and reperfusion is now recognized as one form of acute inflammation in which activated leukocytes play a key role. Although restoration of flow is essential in alleviating ischemic injury, reperfusion initiates a complex series of reactions which lead to neutrophil accumulation, microvascular barrier disruption, and edema formation. A large body of evidence exists which suggests that leukocyte adhesion to and emigration across postcapillary venules plays a crucial role in the genesis of reperfusion injury in skeletal muscle. Reactive oxygen species generated by xanthine oxidase and other enzymes promote the formation of proinflammatory stimuli, modify the expression of adhesion molecules on the surface of leukocytes and endothelial cells, and reduce the bioavailability of the potent antiadhesive agent nitric oxide. As a consequence of these events, leukocytes begin to form loose adhesive interactions with postcapillary venular endothelium (leukocyte rolling). If the proinflammatory stimulus is sufficient, leukocytes may become firmly adherent (stationary adhesion) to the venular endothelium. Those leukocytes which become firmly adherent may then diapedese into the perivascular space. The emigrated leukocytes induce parenchymal cell injury via a directed release of oxidants and hydrolytic enzymes. In addition, the emigrating leukocytes also exacerbate ischemic injury by disrupting the microvascular barrier during their egress across the vasculature. As a consequence of this increase in microvascular permeability, transcapillary fluid filtration is enhanced and edema results. The resultant increase in interstitial tissue pressure physically compresses the capillaries, thereby preventing microvascular perfusion and thus promoting the development of the no-reflow phenomenon. The purpose of this review is to summarize the available information regarding these mechanisms of skeletal muscle ischemia/reperfusion injury.

skeletal muscle kukocytes ischemia oxygen derived free radicals adhesion molecules endothelium inflammation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Carden DL, Korthuis RJ: Mechanisms of postischemic vascular dysfunction in skeletal muscle: Implications for therapeutic intervention. Microcirc Endoth Lymphatics 5: 277–298, 1989Google Scholar
  2. 2.
    Gute DC, Korthuis RJ: Role of leukocyte adherence in reperfusioninduced microvascular dysfunction and tissue injury. In: DN Granger, GW Schmid-Schonbein (eds). Physiology and Pathophysiology of Leukocyte Adhesion. Oxford University Press, Oxford, 1994Google Scholar
  3. 3.
    Korthuis RJ, Granger DN: Cellular dysfunction induced by ischemia/ reperfusion: role of reactive oxygen metabolises and granulocytes. In: L Spatz, AD Bloom (eds). Biological Consequences of Oxidative Stress: Implications for Cardiovascular Disease and Carcinogenesis. Oxford University Press, New York, 1992, pp 50–77Google Scholar
  4. 4.
    Lindsay T, Romaschin A, Walker PM: Free radical mediated damage in skeletal muscle. Microcirc Endothelial Lymph 5: 157–170, 1989Google Scholar
  5. 5.
    Korthuis RJ, Anderson DC, Granger DN: Role of neutrophilendothelial cell adhesion in inflammatory disorders. J Crit Care 9: 47–71, 1994Google Scholar
  6. 6.
    Dahlback LO, Rais O: Morphological changes in striated muscle following ischemia: Immediate postischemic phase. Acta Chir Scand 131: 430–440, 1966Google Scholar
  7. 7.
    Korthuis RJ, Carden DL, Kvietys PR, Fuseler J: Phalloidin attenuates postischemic neutrophil infiltration and increased microvascular permeability. J Appl Physiol 71: 1261–1269, 1991Google Scholar
  8. 8.
    Koller A, Kaley G: Prostaglandins mediate arteriolar dilation to increased blood flow velocity in skeletal muscle microcirculation. Circ Res 67: 529–534, 1990Google Scholar
  9. 9.
    Korthuis RJ, Granger DN, Townsley Ml, Taylor AK: The role of oxygen-derived free radicals in ischemia-induced increases in canine skeletal muscle vascular permeability. Circ Res 57: 599–609, 1985Google Scholar
  10. 10.
    Korthuis RJ, Smith JK, Carden DL: Hypoxic reperfusion attenuates postischemic microvascular injury. Am J Physiol 256: H315–H319, 1989Google Scholar
  11. 11.
    Hearse DJ, Humphrey RM, Chain EB: Abrupt reoxygenation of the anoxic potassium arrested rat heart: A study of myocardial enzyme release. J Mol Cell Cardiol 5: 395–407, 1973Google Scholar
  12. 12.
    Wright JG, Fox D, Kerr JC, Valeri CR, Hobson RW: Rate of reperfusion blood flow modulates reperfusion injury in skeletal muscle. J Surg Res 44: 754–761, 1988Google Scholar
  13. 13.
    Parks DA, Granger DN: Xanthine oxidase: Biochemistry, distribution, and physiology. Acta Physiol Scand (Suppl) 548: 87–99, 1986Google Scholar
  14. 14.
    Smith JK, Carden DL, Korthuis RJ: Role of xanthine oxidase in postischemic microvascular injury in skeletal muscle. Am J Physiol 257: H1782–H1789, 1989Google Scholar
  15. 15.
    Granger DN, Rutili G, McCord JM: Superoxide radicals in feline intestinal ischemia. Gastroenterology 81: 22–29, 1981Google Scholar
  16. 16.
    Granger DN, McCord JM, Parks DA, Hollwarth ME: Xanthine oxidase inhibitors attenuate ischemia-induced vascular permeability changes in the cat intestine. Gastroenterology 90: 80–84, 1986Google Scholar
  17. 17.
    McKelvey TG, Hollwarth ME, Granger DN: Mechanisms of conversion from xanthine dehydrogenase to xanthine oxidase in ischemic rat liver and kidney. Am J Physiol 254: G753–G760, 1988Google Scholar
  18. 18.
    Parks DA, Williams TK, Beckman JS: Conversion of xanthine dehydrogenase to oxidase in ischemic rat intestine: A reevaluation. Am J Physiol 254: G768–G774, 1988Google Scholar
  19. 19.
    Batelli MG: Enzymatic conversion of rat liver xanthine oxidase from dehydrogenase (D form) to oxidase (O form ). FEBS Lett 113: 47–51, 1980Google Scholar
  20. 20.
    McCord JM: Free radicals and myocardial ischemia: Overview and outlook. Free Radical Biol Med 4: 9–14, 1988Google Scholar
  21. 21.
    Saugstad OD: Hypoxanthine as an indicator of hypoxia: Its role in health and disease through free radical production. Pediatric Res 23: 143–150, 1988Google Scholar
  22. 22.
    Gidlof A, Hammersen F, Larsson J, Lewis DH, Liljedahl SO: Is capillary endothelium in human skeletal muscle an ischemic shock tissue. In: DH Lewis (ed). Induced Skeletal Muscle Ischemia in Man. Karger, Basel, 1982, pp 63–79Google Scholar
  23. 23.
    Larsson J, Gidlof A, Lewis DH: Effect of induced ischemia on plasma hypoxanthine levels in man. In: DH Lewis (ed). Induced Skeletal Muscle Ischemia in Man. Karger, Basel, 1982, pp 49–54Google Scholar
  24. 24.
    McCord JM: Oxygen derived free radicals in postischemic tissue injury. N Engl J Med 312: 159–163, 1985Google Scholar
  25. 25.
    Lindsay T, Liauw TS, Romaschin AD: The effect of ischemia/reperfusion on adenine nucleotide metabolism and xanthine oxidase production is skeletal muscle. J Vasc Surg 12: 8–15, 1990Google Scholar
  26. 26.
    Della Corte E, Stirpe F: The regulation of rat liver xanthine oxidase. Involvement of thiol groups in the conversion of the enzyme activity from the dehydrogenase (type D) into oxidase (type O) and purification of the enzyme. Biochem J 126: 739–745, 1972Google Scholar
  27. 27.
    Waud WR, Rajogopalan KV: Purification and properties of the NADdependent (type D) and O2-dependent forms of rat liver xanthine dehydrogenase. Arch Biochem Biophys 172: 354–364, 1988Google Scholar
  28. 28.
    Parks DA, Granger DN, Bulkley GB: Soybean trypsin inhibitor attenuates ischemic injury to the feline small intestine. Gastroenterology 89: 6–12, 1985Google Scholar
  29. 29.
    Smith JK, Carden DL, Grisham MB, Granger DN, Korthuis, RJ: Role of iron in postischemic microvascular injury. Am J Physiol 256: H1472–H1477, 1989Google Scholar
  30. 30.
    Ibrahim B, Stoward PJ: The histochemical localization of xanthine oxidase. J Histochem 10: 615–617, 1978Google Scholar
  31. 31.
    Jarasch ED, Grund C, Bruder G: Localization of xanthine oxidase in mammary gland epithelium and capillary endothelium. Cell 25: 67–82, 1981Google Scholar
  32. 32.
    Jarasch ED, Bruder G, Heid HW: Significance of xanthine oxidase in capillary endothelial cells. Acta Physiol Scand (Suppl) 548: 39–46, 1986Google Scholar
  33. 33.
    Zweier JL, Kuppusamy P, Lutty GA: Measurement of endothelial cell free radical generation: Evidence for a central mechanism of free radical injury in postischemic tissues. Proc Natl Acad Sci USA 85: 4046–4050, 1988Google Scholar
  34. 34.
    Grisham MB, Hernandez LA, Granger DN: Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am J Physiol 251: G567–G574, 1988Google Scholar
  35. 35.
    Bishop CT, Mirza Z, Freeman BA: Free radical damage to cultured porcine aortic endothelial cells and lung fibroblasts: Modulation by culture conditions. In vitro Cell Dev Biol 21: 229–233, 1988Google Scholar
  36. 36.
    McCutchan HJ, Schwappach JR, Enquist EG, Walden DL, Terada LS, Reiss OK, Leff JA, Repine JE: Xanthine oxidase-derived H2O2 contributes to reperfusion injury of ischemic skeletal muscle. Am J Physiol 258: H1415–H1419, 1990Google Scholar
  37. 37.
    Brown JM, Terada LS, Grosso MA, Whitmann GJ, Velasco SE, Patt A, Harden AH, Repine JE: Xanthine oxidase produces hydrogen peroxide which contributes to reperfusion injury of ischemic, isolated, perfused rat hearts. J Clin Invest: 1297–1301, 1988Google Scholar
  38. 38.
    Terada LS, Dormish JJ, Shanley PF, Leff JA, Anderson BO, Repine JE: Circulating xanthine oxidase mediates lung neutrophil sequestration after intestinal ischemia-reperfusion. Am J Physiol 263: L394–L401, 1992Google Scholar
  39. 39.
    Grisham MB, Granger DN: Metabolic sources of reactive oxygen metabolites during oxidant stress and ischemia and reperfusion. Clin Chest Med 10: 71–81, 1989Google Scholar
  40. 40.
    Weiss SJ: Tissue destruction by neutrophils. N Engl J Med 320: 365–376, 1989Google Scholar
  41. 41.
    Winterbourne CC: Myeloperoxidase as an effective inhibitor of hydroxyl radical production. Implications of the oxidative reaction of neutrophils. J Clin Invest 78: 545–550, 1986Google Scholar
  42. 42.
    Granger DN, Hollwarth ME, Parks DA: Ischemia-reperfusion injury: Role of oxygen-derived free radicals. Acta Physiol Scand 548: 47–63, 1986Google Scholar
  43. 43.
    Fantini GA, Minei JP, Perry MO: Reperfusion with superoxide dismutase improves cellular membrane function in postischemic skeletal muscle. Surgical Forum 38: 317–319, 1987Google Scholar
  44. 44.
    Lee KR, Cronenwett JL, Shlafer M: Effect of superoxide dismutase plus catalase on Ca2+ transport in ischemic and reperfused skeletal muscle. J Surg Res 42: 24–32, 1987Google Scholar
  45. 45.
    Granger DN, Parks DA: Role of oxygen radicals in the pathogenesis of intestinal ischemia. Physiologist 26: 159–164, 1983Google Scholar
  46. 46.
    Bolli R: Oxygen-derived free radicals and postischemic myocardial dysfunction (‘stunned myocardium’). J Am Coll Cardiol 12: 239–249, 1988Google Scholar
  47. 47.
    Menger MD, Steiner D, Messmer K: Microvascualr ischemiareperfusion injury in striated muscle: Significance of ‘no-reflow’. Am J Physiol 263: H1892–H1900, 1992Google Scholar
  48. 48.
    Menger MD, Pelikan S, Steiner D, Messmer K: Microvascular ischemia-reperfusion injury in striated muscle: Significance of ‘reflow paradox’. Am J Physiol 263: H1901–H1906, 1992Google Scholar
  49. 49.
    Walker PM, Lindsay TF, Labbe R, Mickle DA, Romaschin AD: Salvage of skeletal muscle with free radical scavengers. J Vasc Surg 5: 68–75, 1987Google Scholar
  50. 50.
    Perler BA, Tohmen AG, Bulkley GB: Inhibition of the compartment syndrome by ablation of the radical-mediated reperfusion injury. Surgery 108: 40–47, 1990Google Scholar
  51. 51.
    Smith JK, Carden DL, Korthuis RJ: Role of hydroxyl radicals in ischemia/reperfusion-induced injury to skeletal muscle microvasculature. FASEB J 3: A1234, 1989Google Scholar
  52. 52.
    Bolli R, Shu W, Hartley CJ, Michael LH, Repine JE, Hess ML, Kukreja RC, Roberts R: Attenuation of dysfunction in the postischemic ‘stunned’ myocardium bydimethylthiourea. Circulation 76: 458–468, 1987Google Scholar
  53. 53.
    Fantini GA, Yoshioka T: Deferoxamine prevents lipid peroxidation and attenuates reoxygenation injury in postischemic skeletal muscle. Am J Physiol 264: H1953–H1959, 1993Google Scholar
  54. 54.
    Bolli R, Patel BS, Shu WX, O'Neill PG, Hartley CS, Charlat ML, Roberts R: The iron chelator desferrioxamine attenuates postischemic ventricular dysfunction. Am J Physiol 253: H 137–H 1380, 1987Google Scholar
  55. 55.
    Hernandez LA, Grisham MB, Granger DN: A role for iron in oxidantmediated ischemic injury to intestinal microvaculature. Am J Physiol 253: G49–G53, 1987Google Scholar
  56. 56.
    Reddy BR, Kloner RA, Przklenk K: Early treatment with deferoxamine limits myocardial ischemic/reperfusiohn injury. Free Radical Biol Med 7: 45–52, 1989Google Scholar
  57. 57.
    Bolli R, Patel BS, Jeroudi MO, Li XY, Triana JF, Lai EK, McCay PB: Iron-mediated radical reactions upon reperfusion contribute to myocardial ‘stunning’. Am J Physiol 259: H1901–H1911, 1990Google Scholar
  58. 58.
    Maruyama M, Pieper GM, Kalyanaraman B: Effects of hydroxyethyl starch conjugated deferoxamine on myocardial functional recovery following coronary occlusion and reperfusion in dogs. J Cardiovasc Pharmacol 17: 166–175, 1991Google Scholar
  59. 59.
    Sinaceur J, Ribiere C, Nordmann J, Nordmann R: Desferrioxamine: A scavenger of superoxide radicals. Biochem Pharmacol 33: 1693–1694, 1984Google Scholar
  60. 60.
    Halliwell B: Use of desferrioxamine as a ‘probe’ for iron-dependent formation of hydroxyl radicals. Evidence for a direct reaction between desferal and the superoxide radical. Biochem Pharmacol 34: 229–233, 1985Google Scholar
  61. 61.
    Darley-Usmar VM, Hersey A, Garland LG: A method for comparative assessment of antioxidants as peroxyl radical scavengers. Biochem Pharmacol 38: 1465–1469, 1989Google Scholar
  62. 62.
    Hartley A, Davies M, Rice-Evans C: Desferrioxamine as a chainbreaking antioxidant in sickle cell membranes. FEBS Lett 264: 145–148, 1990Google Scholar
  63. 63.
    Klebanoff SJ, Waltersdorph AM: Inhibition of peroxidase-catalyzed reactions by deferoxamine. Arch Biochem Biophys 264: 600–606, 1988Google Scholar
  64. 64.
    Grisham MB, McCord JM: Chemistry and cytotoxicity of reactive oxygen metabolites. In: AK Taylor, S Matalon, PA Ward. (eds). Physiology of Oxygen Radicals. American Physiological Society, Bethesda, 1986, pp 1–18Google Scholar
  65. 65.
    Rodell TC, Cheronis JC, Ohnemus CL, Piermattei DS, Repine JE: Xanthine oxidase mediates elastase-induced injury to isolated lungs and endothelium. J Appl Physiol 63: 2159–2163, 1987Google Scholar
  66. 66.
    Phan SH, Gannon DE, Varani J, Ryan US, Ward PA: Xanthine oxidase activity in rat pulmonary artery endothelial cells and its alteration by activated neutrophils. Am J Pathol 134: 1201–1211, 1989Google Scholar
  67. 67.
    Moorhouse PC, Grootveld M, Hal l iwell B, Quinlan JG, Gutteridge JM: Al lopurinol and oxypurinol are hydroxyl radical scavengers. FEBS Lett 213: 23–28, 1987Google Scholar
  68. 68.
    Zimmerman BJ, Parks DA, Grisham MB, Granger DN: Allopurinol does not enhance antioxidant properties of extracellular fluid. Am J Physiol 255: H202–H206, 1988Google Scholar
  69. 69.
    Carden DL, Smith JK, Korthuis RJ: Oxidant-mediated, CD18-dependent microvascular dysfunction induced by complementactivated neutrophils in skeletal muscle. Am J Physiol 260: H1144–H1152, 1991Google Scholar
  70. 70.
    Korthuis RJ, Smith JK, Carden DL: Role of xanthine oxidase in postischemic granulocyte infiltration and microvascular injury in canine gracilis muscle. Physiologist (Suppl) 32: 158, 1989Google Scholar
  71. 71.
    Zimmerman BJ, Guillory DJ, Gaginella T, Granger DN: Role of leukoctriene B4 in granulocyte infiltration into the postischemic feline intestine. Gastroenterology 99: 1358–1363, 1990Google Scholar
  72. 72.
    Smith JK, Carden DL, Korthuis RJ: Activated neutrophils increase microvascular permeability in skeletal muscle: role of xanthine oxidase. J Appl Physiol 70: 2003–2009, 1991Google Scholar
  73. 73.
    Pemberton M, Anderson G, Vetvicka V, Justus DE, Ross GD: Microvascular effects of complement blockade with soluble recombinant CR1 on ischemia/reperfusion injury in skeletal muscle. J Immunol 150: 5104–5113, 1993Google Scholar
  74. 74.
    Lehr HA, Guhimann A, Nolte D, Keppler D, Messmer K: Preservation of postischemic caplilary perfusion by selective inhibition of leukotriene biosynthesis. Transplantation Proceedings 23: 833–834, 1991Google Scholar
  75. 75.
    Granger DN: Role of xanthine oxidase and granulocytes in ischemiareperfusion injury. Am J Physiol 255: H1275, 1988Google Scholar
  76. 76.
    Granger DN, Villareal D: Mechanisms of reperfusion-induced microvascular dysfunction. J Vasc Surg 18: 104–106, 1993Google Scholar
  77. 77.
    Korthuis RJ, Jerome SN: Role of neutrophils in the pathogenesis of microvascular dysfunction in postischemic skeletal muscle. J Vasc Surg 18: 114–117, 1993Google Scholar
  78. 78.
    Korthuis RJ, Grisham MB, Granger DN: Leukocyte depletion attenuates vascular injury in postischemic skeletal muscle. Am J Physiol 254: H823–H827, 1988Google Scholar
  79. 79.
    Yokota J, Minei JP, Fantini GA, Shires GT: Role of leukocytes in reperfusion injury of skeletal muscle after partial ischemia. Am J Physiol 257: H1068–H1075, 1989Google Scholar
  80. 80.
    Rubin BB, Chang G, Liauw S, Young A, Romaschin A, Walker PM: Phospholipid peroxidation dacylation and remodeling in postischemic skeletal muscle. Am J Physiol 263: H1695–H1702, 1992Google Scholar
  81. 81.
    Walden DL, McCutchan HJ, Enquist EG, Schwappach JR, Shanley PF, Reiss OK, Terada LS, Leff JA, Repione JE: Neutrophils accumulate and contribute to skeletal muscle dysfunction after ischemiareperfusion. Am J Physiol 259: H1809–H1812, 1990Google Scholar
  82. 82.
    Gallin Jl, Goldstein IM, Snyderman R: Inflammation: Basic Principles and Clinical Correlates (2nd edn). Raven Press, New York, 1992Google Scholar
  83. 83.
    Harlan JM: Leukocyte-endothelial cell interactions. Blood 65: 513–525, 1985Google Scholar
  84. 84.
    Springer T, Anderson DC, Rosenthal A: Leukocyte Adhesion Molecules. Springer-Verlag, New York, 1989Google Scholar
  85. 85.
    Tranum-Jensen J, Janse MJ, Fiolet JWT, Krieger WJG, D'Alnoncourt CN, Durrer D: Tissue osmoiality, cell swelling, and reperfusion in acute regional myocaridal ischemia in the isolated porcine heart. Circ Res 49: 364–381, 1981Google Scholar
  86. 86.
    Kurtel H, Tso P, Granger DN: Granulocyte accumulation in postischemic intestine: role of leukocyte adhesion glycoprotein CD11/CD18. Am J Physiol 262: G878–G882, 1992Google Scholar
  87. 87.
    Paterson IS, Klausner JM, Goldman G, Welbourne R, Alexander JS, Shepro D, Hechtman HB: The endothelial cell cytoskeleton modulates extravascular polymorphonuclear leukocyte accumulations in vivo.Microvasc Res 38: 49–56, 1989Google Scholar
  88. 88.
    Tanaka M, Brooks SE, Richard VJ, FitzHarris GP, Stoler RC, Jennings RB, Arfors KE, Reimer KA: Effect of anti-CD18 antibody on myocardial neutrophil accumulation and infarct size after ischemia and reperfusion in dogs. Circulation 87: 526–535, 1993Google Scholar
  89. 89.
    Entman ML, Youker K, Shappell SB, Seigel 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: 1497–1506, 1990Google Scholar
  90. 90.
    Nathan CF: Neutrophil activation on biological surfaces: Massive secretion of hydrogen peroxide in response to products of macrophages and Iymphocytes. J Clin Invest 80: 1550–1560, 1987Google Scholar
  91. 91.
    Nathan CF: Respiratory burst in adherent human neutrophils: triggering by colony stimulating factors CSF-GM and CSF-G. Blood 73: 301–306, 1989Google Scholar
  92. 92.
    Shappell SB, Toman C, Anderson DC: Mac-1 (CDllb/CD18) mediates adherence-dependent hydrogen peroxide production by human and canine neutrophils. J Immunol 90: 1335–1345, 1990Google Scholar
  93. 93.
    Suzuki M, Inauen W, Kvietys PR, Grisham MB, Meininger C, Schelling ME, Granger HJ, Granger DN: Superoxide mediates reperfusion-induced leukocyte endothelial cell interactions. Am J Physiol 257: H1740–H1745, 1989Google Scholar
  94. 94.
    Kishimoto TK: A dynamic model for neutrophil localization to inflammatory sites. J NIH Res 3: 75–77, 1991Google Scholar
  95. 95.
    McEver RP: Selectins: Novel adhesion receptors that mediate leukocyte adhesion during inflammation. Thromb Haem 65: 223–228, 1991Google Scholar
  96. 96.
    Smith CW, Kishimoto TK, Abbassi O, Hughes BJ, Rothlein R, Mcintire LV: Chemotactic factors regulate lectn adhesion molecule-1 (LECAM-1)-dependent neutrophil adhesion to cytokine-stimulated endothelial cells in vitro. J Clin Invest 87: 609, 1991Google Scholar
  97. 97.
    Dore M, Hawkins HK, Entman ML, Smith CW: P-selectin mediates spontaneous leukocyte rolling in vivo. Blood 82: 1308–1316, 1993Google Scholar
  98. 98.
    Bevilacqua MP, Strengelin S, Gimbrone MA, Seed B: Endothelialleukocyte adhesion molecule-1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 243: 1160–1165, 1989Google Scholar
  99. 99.
    Bevilacqua MP, Corless C, Lo SK: Endothelial-leukocyte adhesion molecule-1 (ELAM-1): A vascular selectin that regulates inflammation. In: CG Cochrane, MG Gimbrone (eds). Cellular and Molecular Mechanisms of Inflammation (vol 2). Academic Press, San Diego, 1991, pp 1–14Google Scholar
  100. 100.
    Nolte D, Hecht R, Botzlar A, Menger MD, Sinowatz F, Messmer K, Vestweber D: Role of adhesion proteins during postischemic reperfusion of mouse striated muscle. Eur Surg Res 25: 414–415, 1993Google Scholar
  101. 101.
    Walcheck B, Moore KL, McEver RP, Kishimoto TK: Neutrophilneutrophil interactions under hydrodynamic shear stress involve Lselectin and PSGL-1. A mechanism that amplifies initial leukocyte accum ulation of P-selectin in vitro. J Clin Invest 98(5): 1081–1087, 1996Google Scholar
  102. 102.
    Guyer DA, Moore KL, Lynam EB, Schammel CM, Rogelj S, McEver RP, Sklar LA: P-selectin glycoprotein ligand-1 (PSGL-1) is a ligand for L-selectin in neutrophil aggregation. Blood 88(7): 2415–2421, 1996Google Scholar
  103. 103.
    Atherton A, Born GVR: Relationship between the velocity of rolling granulocytes and that of blood flow in venules. J Physiol 233: 157–165, 1973Google Scholar
  104. 104.
    Schmid-Schonbein GW, Shih W, Chien S: Vascular endotheliumleukocyte interaction, sticking shear force in capillaries. Circ Res 36: 173–184, 1975Google Scholar
  105. 105.
    Mayrovitz HN, Wiedeman MP, Tuma RF: Experimental and clinicalthrombosis: factors influencing leukocyte adherence in microvessels. Thromb Haem 38: 823–830, 1977Google Scholar
  106. 106.
    Carden DL, Smith JK, Korthuis RJ: Neubrophil-mediated microvascular dysfunction in postischemic canine skeletal muscle. Circ Res 66: 1436–1444, 1990Google Scholar
  107. 107.
    Dreyer WJ, Michael LH, West MS, Smith CW, Rothlein R, Rossen RD, Anderson DC, Entman ML: Neutrophil accumulation in ischemic myocardium. Insights into time course, distribution, and mechanism of localization during early reperfusion. Circulation 84: 400–411, 1991Google Scholar
  108. 108.
    Horgan MJ, Wright SD, Malik AB: Antibody against leukocyte integrin (CD18) prevents reperfusion-induced lung vascular injury. Am J Physiol 259: L315–L319, 1990Google Scholar
  109. 109.
    Schoenberg MH, Poch B, Younes M, Schwartz A, Baczako K, Lundberg C, Haglund U, Berger HG: Involvement of neutrophils in postischaemic damage to the small intestine. Gut 32: 905–912, 1991Google Scholar
  110. 110.
    Oliver MG, Specian RD, Perry MA, Granger DN: Morphologic assessment of leukocyte-endothelial cell interactions in mesenteric venules subjected to ischemia and reperfusion. Inflammation 15(5): 331–346, 1991Google Scholar
  111. 111.
    Suzuki M, Asako H, Kubes P, Granger DN: Neutrophil-derived oxidants promote leukocyte adherence in postcapillary venules. Microvasc Res 42: 125–138, 1991Google Scholar
  112. 112.
    Wesselcouch EO, Grove Rl, Demusz CD, Baird AJ: Effect of in vivo inhibition of neutrophil adherence on skeletal muscle function during ischemia in the ferret. Am J Physiol 261: H1178–H1183, 1991Google Scholar
  113. 113.
    Jerome SN, Akimitsu T, Korthuis RJ: Leukocyte adhesion, edema, and the development of postischemic capillary no-reflow. Am J Physiol 267: H1329–H1336, 1994Google Scholar
  114. 114.
    Jerome SN, Smith CW, Korthuis RJ: CD18-dependent adherence reactions play an important role in the development of the no-reflow phenomenon. Am J Physiol 264: H479–H483, 1993Google Scholar
  115. 115.
    Horgan MJ, Ge M, Gu J, Rothlein R, Malik AB: Role of ICAM-1 in neutrophil-mediated lung vascular injury after occlusion and reperfusion. Am J Physiol 259: L315–L319, 1991Google Scholar
  116. 116.
    Ma XL, Lefer DJ, Lefer AM, Rothlein R: Coronary endothelial and cardiac protective effects of a monoclonal antibody to intercellular adhesion molecule-1 in myocardial ischemia and reperfusion. Circulation 86: 937–946, 1992Google Scholar
  117. 117.
    Clark WM, Madden KP, Rothlein R, Zivin JA: Reduction of central nervous system ischemic injury in rabbits using leukocyte adhesion antibody treatment. Stroke 22: 877–883, 1991Google Scholar
  118. 118.
    Smith CW, Entman ML, Lane CL, Beaudet AL, Ty TI, Youker K, Hawkins HK, Anderson DC: Adherence of neutrophils to canine cardiac myocytes in vitro is dependent on intercellular adhesion molecule-1. J Clin Invest 88: 1216–1223, 1991Google Scholar
  119. 119.
    Lewis RE, Granger HJ: Diapedesis and the permeability of venous microvessels to protein macromolecules: the impact of leukotriene B4 (LTB4). Microvasc Res 35: 27–47, 1988Google Scholar
  120. 120.
    Doukas J, Shepro D, Hechtman HB: Vasoactive amines directly modify endothelial cells to affect polymorphonuclear leukocyte diapedesis in vitro. Blood 69: 1563–1569, 1987Google Scholar
  121. 121.
    Alexander JS, Hechtman HB, Shepro D: Phalloidin enhances endothelial barrier function and reduces inflam matory perm eability in vitro. Microvasc Res 35: 308–315, 1988Google Scholar
  122. 122.
    Asako H, Wolf RE, Granger DN, Korthuis RJ: Phalloidin reduces leukocyte emigration and vascular permeability in postcapil lary venules. Am J Physiol 26: H1637–H1642, 1992Google Scholar
  123. 123.
    Lewis MS, Whatley RE, Cain P, Mcintyre TM, Prescott SM, Zimmerman GA: Hydrogen peroxide stimulates the synthesis of platelet-activating factor by endothelium and induces endothelial cell-dependent neutrophil adhesion. J Clin Invest 82: 2045–2055, 1988Google Scholar
  124. 124.
    Gasic AC, McGuire G, Krater S, Farhood Al, Goldstein MA, Smith CW, Entman ML, Taylor M: Hydrogen peroxide pretreatment of perfused canine vessels induces ICAM-1 and CD18-dependent neutrophil adherence. Circulation 84: 2154–2166, 1991Google Scholar
  125. 125.
    Grisham MB: Anonymous Reactive Metabolites of Oxygen and Nitrogen in Biology and Medicine. R.G. Landes, Austin, TX. 1993Google Scholar
  126. 126.
    Zimmerman BJ, Grisham MB, Granger DN: Role of hydrogen peroxide, iron, and hydroxyl radicals in ischemia/reperfusion-induced neutrophil infiltration. Physiologist (Suppl) 31: A229, 1988Google Scholar
  127. 127.
    Zimmerman BJ, Grisham MB, Granger DN: Role of oxidants in ischemia/reperfusion-induced granulocyte infiltration. Am J Physiol 258: G185–G190, 1990Google Scholar
  128. 128.
    Suzuki M, Grisham MB, Granger DN: Leukocyte-endothelial cell interactions: Role of xanthine oxidase-derived oxidants. J Leukocyte Biol 50: 488–494, 1991Google Scholar
  129. 129.
    Carden DL, Korthuis RJ: Neutrophil chemotactic activity generated in canine plasma by superoxide. FASEB J 6: A2071, 1992Google Scholar
  130. 130.
    Shingu M, Nobunaga M: Chemotactic activity generated in human serum from the fifth component of complement by hydrogen peroxide. Am J Pathol 117: 201–206, 1984Google Scholar
  131. 131.
    Vogt W, von Zabern I, Hesse D, Nolte R, Haller Y: Generation of activated form of human C5 (C6b-like C5) by oxygen radicals. Immunol Lett 14: 209–215, 1987Google Scholar
  132. 132.
    Kubes P, Suzuki M, Granger DN: An endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88: 4651–4655, 1991Google Scholar
  133. 133.
    Kubes P, Granger DN: Nitric oxide modulates microvascular permeability. Am J Physiol 262: H611–H615, 1992Google Scholar
  134. 134.
    Kurose I, Kubes P, Wolf R, Anderson DC, Paulson S, Miyasaka M, Granger DN: Inhibition of nitric oxide production: mechanisms of vascular albumin leakage. Circ Res 73: 164–171, 1993Google Scholar
  135. 135.
    Akimitsu T, Gute DC, Korthuis RJ: Leukocyte adhesion induced by inhibition of nitric oxide production in skeletal muscle. J Appl Physiol 78: 1725–1732, 1995Google Scholar
  136. 136.
    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: 749–759, 1991Google Scholar
  137. 137.
    Weiss SJ: Oxygen, ischemia, and inflammation. Acta Physiol Scand (Suppl) 548: 9–38, 1986Google Scholar
  138. 138.
    Soussi B, Idstrom JP, Schersten T, Bylund-Fellenius AC: Cytochrome c oxidase and cardiolipin alterations in response to skeletal muscle ischemia and reperfusion. Acta Physiol Scand 138: 107–114, 1991Google Scholar
  139. 139.
    Girotti AW: Mechanisms of lipid peroxidation. Free Radical Biol Med 1: 87–95, 1985Google Scholar
  140. 140.
    Perry MO, Fantini G: Ischemia: Profile of an enemy. Reperfusion injury of skeletal muscle. J Vasc Surg 6: 231–234, 1987Google Scholar
  141. 141.
    Yoshioka T, Shires GT, Fantini GA: Hypothermia relieves oxidative stress in reperfused skeletal muscle following partial ischemia. J Surg Res 53: 408–416, 1992Google Scholar
  142. 142.
    Tsai AG, Friesenecker B, Intaglietta M: Capillary flow impairment and functional capillary density. Int J Microcirc 15: 238, 1995Google Scholar
  143. 143.
    Varani J, Ginsburg I, Schuger L, Gibbs DF, Bromberg J, Johnson KS, Ryan US, Ward PA: Endothelial cell killing by neutrophils. Am J Pathol 135: 435–438, 1989Google Scholar
  144. 144.
    Vissers CM, Winterbourn CC: Oxidative damage to fibronectin. The effects of the neutrophil myeloperoxidase system and HOCI. Arch Biochem Biophys 285: 53–59, 1991Google Scholar
  145. 145.
    Weiss SJ, Peppin G, Ortiz X: Oxidative auto-activation of latent collagenase by human neutrophils. Science 222: 747–749, 1985Google Scholar
  146. 146.
    Weiss SJ, Regiani S: Neutrophils degrade subendothelial matrices in the presence of alpha-1-proteinase inhibitor. Cooperative use of lysosomal proteinase and oxygen metabolises. J Clin Invest 73: 1297–1303, 1984Google Scholar
  147. 147.
    Carden DL, Korthuis RJ: Role of neutrophilic elastase in postischemic granulocyte extravasation and microvascular dysfunction in skeletal muscle. FASEB J 4: A1248, 1990Google Scholar
  148. 148.
    Ames A, Wright RL, Kowada M, Thurston JM, Majno GM: Cerebral ischemia: The no-reflow phenomenon. Am J Pathol 52: 437–453, 1968Google Scholar
  149. 149.
    Barroso-Aranda J, Schmid-Schonbein GW, Zweifach BW, Engler RL: Granulocytes and no-reflow in irreversible hemorrhagic shock. Circ Res 63: 437–447, 1988Google Scholar
  150. 150.
    Del Zoppo GJ, Schmid-Schonbein GW, Mori E, Copeland BR, Chang CM: Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion in baboons. Stroke 22: 1276–1283, 1991Google Scholar
  151. 151.
    Engler RL, Dahigren 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–H322, 1986Google Scholar
  152. 152.
    Engler RL, Dahigren MD, Morris DD, Peterson MA, Schmid-Schonbein GW: Accumulation of polymorphonuclear leukocytes during 3-h experimental myocardial ischemia. Am J Physiol 251: H93–H100, 1986Google Scholar
  153. 153.
    Engler RL, Schmid-Schonbein GW, Pavelec RS: Leukocyte capillary plugging in myocardial ischemia and reperfusion in the dog. Am J Pathol 111: 98–111, 1983Google Scholar
  154. 154.
    Fischer EG, Ames A, Hedley-White ET, O'Gorman S: Reassessment of cerebral capillary changes in acute global ischemia and their relationship to the ‘no-reflow phenomenon.’Stroke 8: 36–39, 1977Google Scholar
  155. 155.
    Harmon JW: The significance of local vascular phenomena in production of ischemic necrosis in skeletal muscle. Am J Pathol 24: 625–641, 1948Google Scholar
  156. 156.
    Kloner RA, Ganote CE, Jennings RB: The ‘no-reflow’ phenomenon after temporary coronary occlusion in the dog. J Clin Invest 54: 1496–1508, 1974Google Scholar
  157. 157.
    Korthuis RJ, Granger DN: Ischemia-reperfusion injury: Role of oxygen-derived free radicals. In: AK Taylor, S Matalon, PA Ward PA. (eds). Physiology of Oxygen Radicals. American Physiological Society, Bethesda, MD, 1986, pp 217–250Google Scholar
  158. 158.
    Mori E, Del Zoppo GJ, Chambers D, Copeland BR, Arfors KE: Inhibition of polymorphonuclear leukocyte adherence suppresses no-reflow after focal cerebral ischemia in baboons. Stroke 23: 712–718, 1992Google Scholar
  159. 159.
    Schmid-Schonbein GW: Capillary plugging by granulocytes and the no-reflow phenomenon in the microcirculation. Fed Proc 46: 2397–2401, 1987Google Scholar
  160. 160.
    Strock PE, Majno G: Microvascular changes in acutely ischemic rat muscle. Surg Gynecol Obstet 129(6): 1213–1224, 1969Google Scholar
  161. 161.
    Quinones-Baldrich WJ, Chervu A, Hernandez JJ, Colburn M, Moore WS: Skeletal muscle function after ischemia: ‘No-reflow’ versus reperfusion injury. J Surg Res 51: 5–12, 1991Google Scholar
  162. 162.
    Messina LM: In vivo assessment of acute microvascular injury after reperfusion of ischemic tibialis anterior muscle of the hamster. J Surg Res 48: 615–621, 1990Google Scholar
  163. 163.
    Bagge U, Amundson B, Lauritzen C: White blood cell deformability and plugging of skeletal muscle capillaries in hemorrhagic shock. Acta Physiol Scand 108: 159–163, 1980Google Scholar
  164. 164.
    Jerome SN, Dore M, Paulson JC, Smith CW, Korthuis RJ: P-selectin and ICAM-1 dependent adherence reactions: Role in the genesis of postischemic no-reflow. Am J Physiol 266: H1316–H1321, 1994Google Scholar
  165. 165.
    Granger DN, Benoit JN, Suzuki M, Grisham MB: Leukocyte adherence to venular endotheiium during ischemia-reperfusion. Am J Physiol 257: G683–G688, 1989Google Scholar
  166. 166.
    Hansell P, Borgstrom P, Arfors KE: Pressure-related capillary leukostasis following ischemia-reperfusion and hemorrhagic shock. Am J Physiol 265: H381–H388, 1993Google Scholar
  167. 167.
    Mazzoni MC, Borgstrom P, Intaglietta M, Arfors KE: Lumenal narrowing and endothelial cell swelling in skeletal muscle capillaries during hemorrhagic shock. Circulatory Shock 29: 27–39, 1989Google Scholar
  168. 168.
    Gidlof A, Lewis DH, Hammersen F: The effect of prolonged total ischemia on the ultrastructure of human skeletal muscle capillaries. A morphometric analysis. Int J Microcirc Clin Exp 7: 67–86, 1987Google Scholar
  169. 169.
    Mazzoni MC, Borgstrom P, Intaglietta M, Arfors KE: Capillary narrowing in hemorrhagic shock is rectified by hyperosmotic salinedextran reinfusion. Circulatory Shock 31: 407–418, 1990Google Scholar
  170. 170.
    Mazzoni MC, Intaglietta M, Cragoe EJ, Arfors KE: Amiloride-sensitive Na pathways in capillary endothelial cell swelling during hemorrhagic shock. J Appl Physiol 73: 1467–1473, 1992Google Scholar
  171. 171.
    House S, Lipowsky H: Leukocyte-endothelium adhesion: microhemodynamics in mesentery of the cat. Microvasc Res 34: 363–379, 1987Google Scholar
  172. 172.
    Hammersen F, Barker JH, Gidlof A, Menger MD, Hammerson E, Messmer K: The ultrastructure of the microvessels and their contents following ischemia and reperfusion. Prog Appl Microcirc 13: 1–26, 1989Google Scholar
  173. 173.
    Menger MD, Sack FU, Barker JH, Feifel G, Messmer K: Quantitative analysis of microcirculatory disorders after prolonged ischemia in skeletal muscle. Res Exp Med 188: 151–165, 1988Google Scholar
  174. 174.
    Welbourne R, Goldman G, Paterson IS, Valeri CR, Shepro D, Hechtman HB: Pathophysiology of ischaemia reperfusion injury, central role of the neutrophil. Br J Surg 78: 651–655, 1991Google Scholar
  175. 175.
    Hill J, Lindsay T, Rusche J: A Mac-1 antibody reduces liver and lung injury but not neutrophil sequestration after intestinal ischem iareperfusion. Surgery 112: 166–172, 1992Google Scholar
  176. 176.
    Klausner JM, Anner H, Paterson IS, Kobzik L, Valeri CR, Shepro D, Hechtman HB: Lower torso ischemia-induced lung injury is leukocyte dependent. Ann Surg 209: 231–236, 1988Google Scholar
  177. 177.
    Welbourne R, Goldman G, Hill J, Kobzik L, Paterson IS, Valeri CR, Shepro D, Hechtman HB: Role of neutrophil adherence receptors (CD18) in lung permeability following lower torso ischemia. Circ Res 71: 82–86, 1992Google Scholar
  178. 178.
    Carden DL, Young JA, Granger DN: Pulmonary microvascular injury following intestinal ischemia/reperfusion: Role of P-selectin. J Appl Physiol 75: 2529–2534, 1993Google Scholar
  179. 179.
    Goldman G, Welbourne R, Klausner JM, Alexander S, Kobzik L, Valeri CR, Shepro D, Hechtman HB: Attenuation of acid aspiration edema with phalloidin. Am J Physiol 259: L378–L383, 1990Google Scholar
  180. 180.
    Liauw K, Rubin BB, Romaschin AD, Walker PM: Sequential canine skeletal muscle ischemia: Prior ischemia/reperfusion results in contralateral muscle salvage. Am J Physiol 1996, in pressGoogle Scholar
  181. 181.
    Mounsey RA, Pang CY, Forrest C: Preconditioning: A new technique for improved muscle flap survival. Otolaryngology-Head and Neck Surgery 107: 549–552, 1992Google Scholar
  182. 182.
    Jerome SN, Akimitsu T, Gute DC, Korthuis RJ: Ischemic preconditioning attenuates capillary no-reflow induced by prolonged ischemia and reperfusion. Am J Physiol 268: H2063–H2067, 1995Google Scholar
  183. 183.
    Akimitsu T, Gute DC, Korthuis RJ: Ischemic preconditioning (IPC) attenuates postischemic leukocyte adherence and emigration via activation of adenosine receptors during IPC and reperfusion. Microcirculation 2: 106, 1995 (Abstract)Google Scholar
  184. 184.
    Akimitsu T, Gute DC, Korthuis RJ: Ischemic preconditioning attenuates postischemic leukocyte adhesion and emigration: Role of adenosine and ATP-sensitive potassium channels. Circulation 90: 1476, 1994Google Scholar
  185. 185.
    Akimitsu T, Gute DC, Korthuis RJ: Ischemic preconditioning attenuates postischemic leukocyte adhesion and emigration. Am J Physiol 1996, in pressGoogle Scholar
  186. 186.
    Gute DC, Akimitsu T, Korthuis RJ: Adenosine preconditioning is partially blocked by the KATP channel antagonist glibenclamide. Microcirculation 2: 1081, 1995Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Dean C Gute
    • 1
  • Tetsuya Ishida
    • 1
  • Koji Yarimizu
    • 1
  • Ronald J. Korthius
    • 1
  1. 1.Departmernt of Molecular and Cellular PysiologyLouisiana State University Medical Center, School of Medicine in ShreveportShreveportUSA

Personalised recommendations