Mechanisms of ischemic preconditioning

Shock

Volumn 8, Issue 2, 1997, Pages 86-94

  Ishida, Tetsuya ^a   Yarimizu, Koji ^a   Gute, Dean C ^a   Korthuis, Ronald J ^a,b  

^a Louisiana State University School of Medicine Shreveport   (United States)

^b LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; HUMAN; ISCHEMIC PRECONDITIONING; REVIEW;

ANIMALS; HUMANS; ISCHEMIC PRECONDITIONING;

EID: 0031202315     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/00024382-199708000-00003     Document Type: Article

References (117)

1. Murry, CE, Jenning RB, Reimer KA: Preconditioning with ischemia: A delay in lethal cell injury in ischemic myocardium. Circulation 74:1124-1136, 1986.
2. Granger DN, Korthuis RJ: Physiologic mechanisms of post ischemic injury. Annu Rev Physiol 57:311-332, 1995.
3. Lawson CS, Downey JM: Preconditioning: State of the art myocardial protection. Cardiovasc Res 27:542-550, 1993.
4. Jenning RB, Murry CE, Reimer KA: Preconditioning myocardium with ischemia. Cardiovasc Drug Ther 5:933-938, 1991.
5. Walker DM, Yellon DM: Ischemic preconditioning: From mechanisms to exploitation. Cardiovasc Res 26:734-739, 1992.
6. Gross GJ, Auchampach JA: Role of ATP dependent potassium channels in myocardial ischemia. Cardiol Res 26:1011-1016, 1992.
7. Gross GJ, Yao Z, Pieper GM, Auchampach JA: The ATP-regulated potassium channel in ischemia-reperfusion injury. Ann NY Acad Sci 723:71-81, 1994.
8. Downey JM, Cohen MV, Ytrehus K, Liu Y: Cellular mechanisms in ischemic preconditioning: The role of adenosine and protein kinase C. Ann NY Acad Sci 723:82-98, 1994.
9. Mounsey RA, Pang CY, Boyd JB, Forrest C: Augmentation of skeletal muscle survival in the latissimus dorsi porcine model using acute ischemic preconditioning. Otolaryngology 21:315-320, 1992.
10. Parratt JR: Possibilities for the pharmacological exploitation of ischemic preconditioning. J Mol Cell Cardiol 27:991-1000, 1995.
11. Mounsey RA, Pang CY, Forrest C: Preconditioning: A new technique for improved muscle flap survival. Otolaryngol Head Neck Surg 107:549-552, 1992.
12. Jerome SN, Akimitsu T, Gute DC, Korthuis RJ: Ischemic preconditioning attenuates capillary no-reflow induced by ischemia and reperfusion. Am J Physiol 268:H2063-H2067, 1995.
13. Akimitsu T, Gute DC, Korthuis RJ: Ischemic preconditioning attenuates postischemic leukocyte adhesion and emigration. Am J Physiol 1996. In press.
14. Akimitsu T, Gute DC, Korthuis RJ: Ischemic preconditioning attenuates postischemic leukocyte adhesion and emigration: Role of adenosine and ATP-sensitive potassium channels. Circulation 90(Suppl 1):476, 1994.
15. 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).
16. Li Y, Kloner RA: Cardioprotective effects of ischemic preconditioning are not mediated by prostanoids. Cardiol Res 26:226-231, 1992.
17. + channel in mediating the effects of acetylcholine to mimic preconditioning in dogs. Circ Res 73:1193-1201, 1993.
18. Thornton J, Striplin S, Liu GS, et al: Inhibition of protein synthesis does not block myocardial protection afforded by preconditioning. Am J Physiol 259:H1822-H1825, 1990.
19. Liu GS, Thornton J, Van Winke D, Stanly AWH, Olsson RA, Downey JM: Protection against infarction afforded by preconditioning is mediated by A1 receptors in rabbit heart. Circulation 84:350-356, 1991.
20. Downey JM, Liu GS, Thornton JD: Adenosine and the anti-infarct effects of preconditioning. Cardiol Res 27:3-8, 1993.
21. Kitakaze M, Hori M, Morioka T, et al: Infarct size-limiting effect of ischemic preconditioning is blunted by inhibition of 5′-nucleotidase activity and attenuation of adenosine release. Circulation 89:1237-1246, 1994.
22. Mosca SM, Gelpi RJ, Cingolani HE: Adenosine and diprydamole mimic the effects of preconditioning. J Mol Cell Cardiol 26:1403-1409, 1994.
23. Piacentini L, Wainwright CL, Parratt JR: The antiarrhythmic effect of preconditioning, in rat isolated hearts, does not involve A1 adenosine receptors. Br J Pharmacol 107:137P, 1992 (abstract).
24. Li Y, Kloner RA: The Cardioprotective effects of ischemic "preconditioning" are not mediated by adenosine receptors in rat hearts. Circulation 87:1642-1648, 1993.
25. Murphy E, Fralix TA, London RE, Steenbergen C: Effects of adenosine antagonists on hexose uptake and preconditioning in perfused rat heart. Am J Physiol 265:C1146-C1155, 1993.
26. Hu K, Nattel S: Mechanisms of ischemic preconditioning in rat hearts: Involvement of 1B-adrenoreceptors, pertussis toxin-sensitive G proteins, and protein kinase C. Circulation 92:2259-2265, 1995.
27. Liu GS, Richards SC, Olsson RA, Mullane K, Walsh RS, Downey JM: Evidence that adenosine-A3 receptor may mediate the protection afforded by preconditioning in the isolated rabbit heart. Cardiovasc Res 28:1057-1061, 1994.
28. Gute DC, Ishida T, Korthuis RJ: The beneficial effects of ischemic preconditioning are abolished by blockade of adenosine A1, but not A2, receptors. Microcirculation 1996. In press.
29. Wyatt DA, Edmunds MC, Rubio R, Berne RM, Lasley RD: Adenosine stimulates glycolytic flux in isolated perfused rat hearts by A1 adenosine receptors. Am J Physiol 254:H1952-H1957, 1989.
30. Richardt G, Wass W, Kranzhofer R, Mayer E, Schomig A: Adenosine inhibits exocytotic release of endogenous noradenaline in rat heart: A protective mechanism in early myocardial ischemia. Circ Res 61:117-123, 1987.
31. Cronstein BN, Levin RI, Belanoff J, Weissmann G, Hirschhorn R: Adenosine: An endogenous inhibitor of neutrophil-mediated injury to endothelial cells. J Clin Invest 78:760-770, 1986.
32. Grisham MB, Hernandez LA, Granger DN: Adenosine inhibits ischemia-reperfusion-induced leukocyte adherence and extravasation. Am J Physiol 257:H1334-H1339, 1989.
33. Helper JR, Gilman AG: G proteins. Trend Biol Sci 17:383-387, 1992.
34. Neer EJ: Heterotrimetic G proteins: Organizers of transmembrane signals. Cell 80:249-257, 1995.
35. Baer HP, Vriend P: Adenosine receptors in smooth muscles: Structure-activity studies and the question of adenylate cyclase involvement in control of relaxation. Can J Physiol Pharmacol 63:972-977, 1985.
36. Londos C, Cooper DMF, Wolff J: Subclass of external adenosine receptors. Proc Natl Acad Sci USA 77:2551-2554, 1980.
37. Van Calker D, Muller M, Hamprecht B: Adenosine regulates via two different types of receptors, the accumulation of cyclic AMP in cultured brain cells. J Neurochem 33:999-1005, 1985.
38. Thornton JD, Liu GS, Downey JM: Pretreatment with pertussis toxin blocks the protective effects of preconditioning: Evidence for a G-protein mechanism. Mol Cell Cardiol 25:311-320, 1993.
39. Hu K, Nattel S: Signal transduction systems underlying ischemic preconditioning in rat hearts. Circulation 90(Suppl 1):108, 1994 (abstract).
40. Piacentini L, Wainwright CL, Parret JR: The antiarrhythmic effect of preconditioning in rat hearts involves a pertussis-toxin sensitive mechanism. Cardiovasc Res 27:674-680, 1993.
41. Weis A, Zeifang F, Rauch B, Firoomand: A functional modification of Gi proteins in the underlying mechanism of ischemic preconditioning. Circulation 88(Suppl 1):633, 1993 (abstract).
42. Fleming JW, Wisler PL, Watanebe AM: Signal transduction by G proteins in cardiac tissues. Circulation 85:420-433, 1992.
43. Exton JH: Phosphoinositide phospholipases, G proteins in hormone action. Annu Rev Physiol 56:349-369, 1994.
44. Tohse N, Kameyama M, Sekiguchi K, Shearman MS, Kanno M: Protein kinase C activation enhances the delayed rectifier potassium current in guinea-pig heart cells. J Mol Cell Cardiol 22:725-734, 1990.
45. Venema RC, Raynor RL, Noland TA Jr, Kuo JF: Role of protein kinase C in the phosphorylation of cardiac myosin light chain 2. Biochem J 294:401-406, 1993.
46. 2+ pump in cardiac sarcolemma. Can J Physiol Pharmacol 70:1230-1235, 1992.
47. Kohl C, Linck B, Schmitz W, Scholz H, Scholz J, Toth M: Effects of carbachol and ( - )-N6-phenylisopropyladenosine on myocardial inositol phosphate content and force of contraction. Br J Pharmacol 101:829-834, 1990.
48. Singer HA: Phorbol ester-induced stress and myosin light chain phosphorylation in swine carotid medial smooth muscle. J Pharmacol Exp Ther 252:1068-1074, 1990.
49. Zhou XB, Zhai XL, Ashraf M: Preconditioning of bovine coronary endothelial cells is mediated by a protein kinase C signaling pathway. Circulation 90(Suppl 1):371, 1994 (abstract).
50. Ytrehas K, Liu Y, Downey JM: Preconditioning protects ischemic rabbit heart by protein kinase C activation. Am J Physiol 266:H1145-H1152, 1994.
51. Liu Y, Ytrehus K, Downey JM: Evidence that translocation of protein kinase C is a key event during ischemic preconditioning of rabbit myocardium. J Mol Cell Cardiol 26:661-668, 1994.
52. Mitchell MB, Meng X, Ao L, Brown JM, Harken AH, Banerjee A: Preconditioning of isolated rat heart is mediated by protein kinase C. Circ Res 76:73-81, 1995.
53. Speechly-Dick ME, Mocanu MM, Yellon DM: Protein kinase C: Its role in ischemic preconditioning in the rat. Circ Res 75:586-590, 1994.
54. Lynch JJ, Ferro TJ, Blumenstoch FA, Brockenauer AM, Malik AB: Increased endothelial albumin permeability mediated by protein kinase C activation. J Clin Invest 85:1991-1998, 1990.
55. Przyklenk K, Sussman MA, Kloner RA: Fluorescence microscopy reveals no evidence of protein kinase C activation in preconditioned canine myocardium. Circulation 90(Suppl 1):647, 1994 (abstract).
56. Vogt A, Barancik M, Weihrauch D, Arras M, Podzuweit T, Schaper W: Protein kinase C inhibitors reduce infarct size in pig hearts in vivo. Circulation 90(Suppl 1):647, 1994 (abstract).
57. Nishizuka Y: Protein kinase C and lipid signaling for sustained responses. FASEB J 9:484-496, 1995.
58. Ramkumar V, Stiles GL, Beaven MA, Ali H: The A3 receptor is the unique adenosine receptor which facilitates release of allergic mediators in mast cells. J Biol Chem 268:16887-16890, 1993.
59. Deisher TA, Sato TT, Pohlman TH, Harlan JM: A protein kinase C agonist, selective for the I isozyme, induces E-selectin and VCAM-1 expression on HUVEC but does not translocate PKC. Biochem Biophys Res Commun 193:1283-1290, 1993.
60. Gute DC, Ishida T, Korthuis RJ: Ischemic preconditioning (IPC) prevents postischemic leukocyte adhesion: Role of protein kinase C (PKC). Int J Microcirc 16(Suppl 1):P256, 1996 (abstract).
61. Yarimizu K, Ishida T, Gute DC, Korthuis RJ: Role of protein kinase C in ischemia/reperfusion induced leukocyte adhesion, emigration, and venular protein leakage, Int J Microcirc 16(Suppl 1):P251, 1996.
62. Sluiter W, Pietersma A, Lamers JMJ, Koster JF: Leukocyte adhesion molecules on the vascular endothelium: Their role in the pathogenesis of cardiovascular disease and the mechanisms underlying their expression. J Cardiovasc Pharmacol 22:S37-S44, 1993.
63. Spruce AE, Standen NB, Stanfield PR: Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane. Nature 316:736-738, 1985.
64. +: Channels that are blocked by hypoglycemia-inducing sulfonylureas in insulin-secreting cells are activated by galanin, a hyperglycemia-inducing hormone. Proc Natl Acad Sci USA 85:1312-1316, 1989.
65. Treheme JM, Ashford MLJ: The regional distribution of sulphonylurea binding sites in rat brain. Neuroscience 40:523-531, 1991.
66. + channels to A1 receptors by G proteins in rat ventricular myocytes. Am J Physiol 259:H820-H826, 1990.
67. Grover GJ, Sleph PG, Dzwonczyk S: Role of myocardial ATP-sensitive potassium channels in mediating preconditioning in dog heart and their possible interaction with adenosine A1-receptors. Circulation 86:1310-1316, 1992.
68. ATP channel. Am J Physiol 266:H829-H839, 1994.
69. Toombs CF, McGee DS, Johnston WE, Vinten-Johansen J: Protection from ischaemic-reperfusion injury with adenosine treatment is reversed by inhibition of ATP-sensitive potassium channels. Cardiovasc Res 27:623-629, 1993.
70. ATP: Channels and ischemic preconditioning in dogs. Am J Physiol 264:H1327-H1336, 1993.
71. + channel in mediating the effects of acetylcholine to mimic preconditioning in dogs. Circ Res 73:1193-1201.
72. Gross GJ, Auchampach JA: Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ Res 70:223-233, 1992.
73. Pieper GM, Gross GJ: HMD 52692 (bimakalim), a new potassium channel opener, attenuates luminol-enhanced chemiluminescence and Superoxide anion radical formation by zymosan-activated polymorpho-nuclear leukocytes Immunopharmacology 23:191-197, 1992.
74. Gross GJ, Auchampach JA, Maruyama M, Warltier DC, Pieper GM: Cardioprotective effects of nicorandil. J Cardiovasc Pharmacol 20(Suppl 3):S22-S28, 1992.
75. + channels in insulinoma cells: Activation of somatostatin and protein kinase C and the role of cAMP. Proc Natl Acad Sci USA 86:2971-2975, 1989.
76. 2+ release and PKC. Biophys J 66:A429, 1994 (abstract).
77. Thornton JD, Thornton CS, Sterling DL, Downey JM: Blockade of ATP-sensitive potassium channels increases infarct size but does not prevent preconditioning in rabbit hearts. Circ Res 72:44-49, 1993.
78. Ishtda T, Gute DC, Korthuis RJ: Ischemic preconditioning prevents postischemic leukocyte adhesion in rat mesenteric venules: Role of ATP-sensitive potassium channels. Microcirculation 1996. In press.
79. Granger DN: Role of xanthine oxidase and granulocytes in ischemic-reperfusion injury. Am J Phiysiol 255:H1269-H1275, 1988.
80. Granger DN, Kvietys PR, Perry MA: Leukocyte-endothelial cell adhesion induced by ischemia and reperfusion. Can J Physiol Pharmacol 71:67-75, 1993.
81. Petrone WF, English DK, Wong K, McCord JM: Free radicals and inflammation: Superoxide-dependent activation of a neutrophil chemotactic factor in plasma. Proc Natl Acad Sci USA 77:1150-1163, 1980.
82. Carden DL, Jerome SN, Korthuis RJ: Neutrophil chemotactic activity generated in canine plasma by Superoxide. Proc 5th World Congr Microcirc 13, 1991.
83. Suzuki M, Grisham MB, Granger DN: Leukocyte-endothelial cell interactions: Role of xanthine oxidase-derived oxidants. J Leukocyte Biol 50:488-494, 1991.
84. Zimmerman BJ, Granger DN: Oxygen free radicals and the gastrointestinal tract: Role in ischemia/reperfusion injury. Hepatogastroenterology 41:337-342, 1994.
85. Kurose I, Granger DN: PAF in ischemia and reperfusion: Effects on the microvasculature. J Lipid Mediat Cell Signal 10:89-91, 1994.
86. Marletta MA, Yoon PS, Iyengar R, Leaf CD, Wishnock JS: Macrophage oxidation of L-arginine to nitrite and nitrate: Nitric oxide is intermediate. Biochemistry 27:8706-8711, 1988.
87. Kubes P, Suzuki M, Granger DN: Nitric oxide: An endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88:4651-4655, 1991.
88. Radomski MW, Palmer PM, Moncada S: The role of nitric oxide and cGMP in platelet adhesion to vascular endothelium. Biochem Biophys Res Commun 148:1482-1489, 1987.
89. Kurose I, Wolf R, Grisham MB, Granger DN: Modulation of ischemia/ reperfusion-induced microvascular dysfunction by nitric oxide. Circ Res 74:376-382, 1994.
90. Gaboury J, Anderson DC, Kubes P: Molecular mechanisms involved in superoxide-induced leukocyte-endothelial cell interactions in vivo. Am J Physiol 266:H637-H642, 1994.
91. Lefer AM, Siegfried MR, Ma X-L: Protection of ischemia-reperfusion injury by synonomine NO donors via inhibition of neutrophil-endothelium interaction. J Cardiol Pharm 22:S22-S33, 1993.
92. Cooke JP, Tsao PS: Cytoprotective effects of nitric oxide. Circulation 88:2451-2454, 1993.
93. Lefer DJ, Nakanishi K, Johnston WE, Vinten-Johansen J: Antineutrophil and myocardial protecting actions of a novel nitric oxide donor after acute myocardial ischemia and reperfusion in dogs. Circulation 88:2337-2350, 1993.
94. Kanwar S, Tepperman BL, Payne D, Sutherland LR, Kubes P: Time course of nitric oxide production and epithelial dysfunction during ischemia/reperfusion on the feline small intestine. Circ Shock 42:135-140, 1994.
95. Fukahori M, Ichimori K, Ishida H, Nakagawa H, Okino H: Nitric oxide reversibly suppresses xanthine oxidase activity. Free Radic Res 21:202-212:1994.
96. Kurose I, Wolf R, Grisham MB, Aw TY, Specian RD, Granger DN: Microvascular response to inhibition of nitric oxide production: Role of active oxidants. Circ Res 76:30-39, 1994.
97. Akimitsu T, Gute DC, Korthuis RJ: Leukocyte adhesion induced by inhibition of nitric oxide production in skeletal muscle. J Appl Physiol 78:1725-1732, 1995.
98. Davenpeck KL, Gauthier TW, Lefer AM: Inhibition of endothelial-derived nitric oxide promotes P-selectin expression and actions in the rat microcirculation. Gastroenterology 107:1050-1058, 1994.
99. Russell J, Eppihimer M, Granger DN: Kinetics and modulation of P-selectin expression in mouse intestine exposed to ischemia/reperfusion (I/R). FASEB J 10(Suppl):A612, 1996 (abstract).
100. Heller R, Bussolino F, Ghigo D, et al: Nitorvasodilators inhibit thrombininduced PAF synthesis in human endothelial cells. Biochem Pharmacol 44:223-229, 1992.
101. Eigler A, Moeller J, Enders S: Exogenous and endogenous nitric oxide attenuates tumor necrosis factor synthesis in the murine macrophage cell line RAW 267.4. J Immunol 154:4048-4054, 1995.
102. Gute DC, Ishida T, Korthuis RJ: The effect of ischemic preconditioning on postischemic leukocyte adhesion: Role of nitric oxide. Gasteroenterology 110(Suppl):A327, 1996 (abstract).
103. Patterson CE, David HW, Schaphorst KL, Garcia JGN: Mechanisms of cholera toxin prevention of thrombin- and PMA-induced endothelial barrier function. Microvasc Res 48:212-235, 1994.
104. Siflinger-Birnboim A, Bode DC, Malik AB: Adenosine 3′:5′-cyclic monophosphate attenuates neutrophil-mediated increase in endothelial permeability. Am J Physiol 264:H370-H375, 1993.
105. Adkins WK, Barnard JW, May S, Seibert AF, Haynes J, Taylor AE: Compounds that increase cAMP prevent ischemia-reperfusion capillary injury. J Appl Physiol 72:492-497, 1992.
106. Seibert AF, Thompson WJ, Taylor A, Wilborn WH, Barnard J, Haynes J: Reversal of increased microvascular permeability with ischemia-reperfusion: Role of cAMP. J Appl Physiol 72:389-395, 1992.
107. Ogawa S, Koga S, Kuwabara K, et al: Hypoxia-induced increased permeability of cultured bovine pulmonary and aortic endothelial monolayers occurs through lowering of cellular cAMP levels and is modulated by glucocorticoids. Am J Physiol 262:C546-C554, 1992.
108. Pinsky D, Oz M, Liao H, et al: Restoration of the cAMP second messenger pathway enhances cardiac preservation for transplantation in a heterotopic rat model. J Clin Invest 92:2994-3002, 1993.
109. Zhou X, Zhai X, Ashraf M: Preconditioning of bovine endothelial cells: The protective effect is mediated by an adenosine A2 receptor through a protein kinase C signalling pathway. Circ Res 78:73-81, 1996.
110. Haselton FR, Mueller SN, Howell EM, Levine EM, Fishman AP: Chromatographic demonstration of reversible changes in endothelial permeability. J Appl Physiol 67:2032-2048, 1989.
111. Shasby DM, Shasby SS, Sullivan JM, Peach MJ: Role of endothelial cell cytoskeleton in control of endothelial permeability. Circ Res 51:657-661, 1982.
112. Patterson CE, Davis HW, Schaphorst KL, Garcia JGN: Mechanisms of cholera toxin prevention of thrombin- and PMA-induced endothelial cell barrier dysfunction. Microvasc Res 48:212-235, 1994.
113. Haverstic DM, Gray LL: Lymphocyte adhesion mediated by lymphocyte function-associated antigen-1. J Immunol 149:397-402, 1992.
114. Pober JS, Slowik MR, Delula LG, Ritchie AJ: Elevated cyclic AMP inhibits endothelial cell synthesis and expression of TNF-induced endothelial leukocyte adhesion molecule-1, and vascular cell adhesion molecule-1, but not intercellular adhesion molecule-1. J Immunol 150:5114-5123, 1993.
115. Boxer LA, Allen JM, Baehner RL: Diminished polymorphonuclear adherence: Function dependent on release of cAMP by endothelial cells after stimulation of receptors by epinephrine. J Clin Invest 66:268-274, 1980.
116. Bessler H, Gilgil R, Djaldetti M, Zahavi I: Effect of pentoxifylline on the phagocytic activity, cAMP levels, and super oxide anion production by monocytes and polymorphonuclear cells. J Leukocyte Biol 40:747-754, 1986.
117. Ishida T, Gute DC, Yarimizu K, Korthuis RJ: Ischemic preconditioning attenuates leukocyte adhesion and venular protein leakage: Role of adenylyl cyclase and protein kinase A. Int J Microcirc 16(Suppl 1):P253,1996 (abstract).