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Research Article

Ischemic Preconditioning Prevents Postischemic Arteriolar, Capillary, and Postcapillary Venular Dysfunction: Signaling Pathways Mediating the Adaptive Metamorphosis to a Protected Phenotype in Preconditioned Endothelium

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Pages 73-89 | Published online: 10 Jul 2009

References

  • Akimitsu T, Gute DC, Korthuis RJ. (1996). Ischemic preconditioning attenuates postischemic leukocyte adhesion and emigration. Am J Physiol 271:H2052–H2059.
  • Akimitsu T, Gute DC, Korthuis RJ. (2002). Ischemic preconditioning reduces postischemic leukocyte adhesion: role of ATP-sensitive potassium channels. Microcirculation (in preparation).
  • Arai M, Thurman RG, Lemasters JJ. (2000). Contri- bution of adenosine A(2) receptors and cyclic aden-osine monophosphate to protective ischemic preconditioning of sinusoidal endothelial cells against stor-age/reperfusion injury in rat livers. Hepatology 32: 297–302.
  • Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, Fini ME, Lo EH. (2001). Effects of matrix metalloproteinase-9 gene knockout on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21: 7724–7732.
  • Attkiss KJ, Suski M, Hunt TK, Buncke HJ. (1999). Ischemic preconditioning of skeletal muscle improves tissue oxygenation during reperfusion. J Reconstruc Surg 15:223–228.
  • Barron DJ, Etherington PJ, Winlove CP, Jarvis JC, Salmons S, Pepper JR. (2001). Combination of preconditioning and delayed flap elevation: evidence for improved perfusion and oxygenation of the latissimus dorsi muscle for cardiomyoplasty. Ann Thorac Surg 71:852–861.
  • Beauchamp P, Richard V, Tamion F, Lallemand F, Lebreton J-P, Vaudry H, Daveau M, Thuillez C. (1999). Protective effects of preconditioning in cultured rat endothelial cells. Effects on neutrophil adhesion and expression of ICAM-1 after anoxia and reoxygenation. Circulation 100:541–546.
  • Beresewicz A, Czarnowska E, Maczewski M. (1998). Ischemic preconditioning and superoxide dismutase protect against endothelial cell dysfunction and en-dothelium glycocalyx disruption in the postischemic guinea pig hearts. Mol Cell Biochem 186:87–97.
  • Bolli R. (2000). The late phase of preconditioning. Circ Res 87:972–983.
  • Bouchard JF, Lamontagne D. (1996). Mechanisms of protection afforded by preconditioning to endothelial function against ischemic injury. Am J Physiol 271:H1801–H1806.
  • Bouchard JF, Choouinard J, Lamontagne D. (1998). Role of kinins in the endothelial protective effect of ischaemic preconditioning. Br J Pharmacol 123:413–420.
  • Bouchard JF, Chouinard J, Lamontagne D. (1998). Role of B1 receptors in the endothelial protective effect of ischaemic preconditioning. Arch Mal Coeur Vaiss 91:941–945.
  • Bouchard JF, Chouinard J, Lamontagne D. (2000). Participation of prostaglandin E2 in the endothelial protective effect of ischaemic preconditioning in isolated rat heart. Cardiovasc Res 45:418–427.
  • Chlopicki S, Lomnicka M, Gryglewski RJ. (1999). Reversal of the postischaemic suppression of coronary function in perfused guinea pig heart by ischaemic preconditioning. J Physiol Pharmacol 50:605–615.
  • Cohen MV, Baines CP, Downey JM. (2000). Ischemic preconditioning: from adenosine receptor to KATP channel. Annu Rev Physiol 62:79–109.
  • Davenpeck KL, Gauthier TW, Lefer AM. (1994). In- hibition of endothelial-derived nitric oxide promotes P-selectin expression and actions in the rat microcirculation. Gastroenterology 107:1050–1058.
  • Davis JM, Gute DC, Jones S, Krsmanovic A, and Korthuis (RJ). (1999). Ischemic preconditioning prevents postischemic P-selectin expression in the small intestine. Am J Physiol 277:H2476–H2481.
  • DeFily DV, Chilian WM. (1993). Preconditioning protects coronary arteriolar endothelium from isch-emia-reperfusion injury. Am J Physiol 265:H700–H706.
  • Dunn GR, Granger DN, Korthuis RJ. (1995). Leuko-cyte/endothelial cell adhesion and ischemia/ reperfusion injury. In: Barker JH, Anderson GL, Menger MD, editors. Clinically Applied Microcirculation Research. Boca Raton, FL: CRC Press, pp. 75–96.
  • Engler RL, Schmid-Schonbein GW, Pavelec RS. (1983). Leukocyte capillary plugging in myocardial ischemia and reperfusion in the dog. Am J Pathol 111: 98–111.
  • Fleming I, Hecker M, Busse R. (1994). Intracellular alkalinization induced by bradykinin sustains activation of the constitutive nitric oxide synthase in endothelial cells. Circ Res 74:1220–1226.
  • Frassetto SS, Schetinger MR, Schierholt R, Webber A, Bonan CD, Wyse AT, Dias RD, Netto CA, Sarkis JJ. (2000). Brain ischemia alters platelet ATP diphos-phohydrolase and 5'-nucleotidase activities in naive and preconditioned rats. Braz J Med Biol Res 33: 1369–1377.
  • Gianella E, Mochmann H-C, Levi R. (1997). Ischemic preconditioning prevents the impairment of hypoxic coronary vasodilatation caused by ischemia/ reperfusion. Roles of adenosine A1/A3 and bradykinin B2 receptor activation. Circ Res 81:415–422.
  • Grisham MB, Granger DN, Lefer DJ. (1998). Modulation of leukocyte-endothelial interactions by reactive metabolites of oxygen and nitrogen: relevance to ischemic heart disease. Free Radic Biol Med 25:404–433.
  • Gross GJ, Fryer RM. (1999). Sarcolemmal versus mi-tochondrial ATP-sensitive K channels and myocardial preconditioning. Circ Res 87:1431–1433.
  • Gumina RJ, Moore J, Schelling P, Beier N, Gross GJ. (2001). Na+/H+ exchange inhibition prevents endothelial dysfunction after I/R injury. Am J Physiol 281: H1260–H1266.
  • Gute D, Korthuis RJ. (1995). Role of leukocyte adherence in reperfusion-induced microvascular dysfunction and tissue injury. In: Granger DN, Schmid-Schonbein, editors. Physiology and Pathophysiology of Leukocyte Adhesion New York: Oxford University Press, pp. 359–380.
  • Gute DC, Shigematsu S, Ishida T, Yarimizu K, Korthuis RJ. (2001). Ischemic preconditioning prevents microvascular dysfunction: Role of protein kinase C. Microcirculation (in preparation).
  • Gute DC, Ishida T, Akimitsu T, Korthuis RJ. (2002). Ischemic preconditioning prevents leukocyte adhesion in postischemic mesenteric venules. Microcirculation (in preparation).
  • Hamel L, Kenney M, Clark K, Merkel L, Rojas C. (2000). Preconditioning of human smooth muscle cells via cyclopentenone prostaglandins protects against toxic effects of oxidized low-density lipoprotein. Biochem Biophys Res Commun 269:327–330.
  • Howell JG, Zibari GB, Brown MF, Burney DL, Sawaya DE, Olinde JG, Granger DN, McDonald JC. (2000). Both ischemic and pharmacological preconditioning decrease hepatic leukocyte/endothelial cell interactions. Transplantation 69:300–303.
  • Ishida S, Shigematsu S, Gute DC, Korthuis RJ. (2001). Nitric oxide mediates the anti-inflammatory effects of ischemic preconditioning. Am J Physiol (in preparation).
  • Iwakura K, Ito H, Kawano S, Shintani Y, Yamamoto K, Kato A, Ikushima M, Tanaka K, Kitakaze M, Hori M, Higashino Y, Fujii K. (2001). Predictive factors for development of the no-reflow phenomenon in patients with reperfused anterior wall acute myocardial infarction. J Am Coll Cardiol 38:472–477.
  • Jerome SN, Akimitsu T, Korthuis RJ. (1994). Leukocyte adhesion, edema, and the development of postischemic capillary no-reflow. Am J Physiol 267: H1329–H1336.
  • Jerome SN, Akimitsu T, Gute DC, Korthuis RJ. (1995). Ischemic preconditioning attenuates capillary no-reflow induced by prolonged ischemia and reperfusion. Am J Physiol 268:H2063–H2067.
  • Kaeffer N, Richard V, Thuillez C. (1997). Delayed coronary endothelial protection 24 hours afer preconditioning: role of free radicals. Circulation 96:2311–2316.
  • Kaeffer N, Richard V, Francois A, Lallemand F, Henry J-P, Thuillez C. (1996). Preconditioning prevents reperfusion-induced coronary endothelial dysfunction in rats. Am J Physiol 271:H842–H849.
  • Kawata H, Yoshida K-I, Kawamoto A, Kurioka H, Takase E, Sasaki Y, Hatanaka K, Kobayashi M, Ueyama T, Hashimoto T, Dohi K. (2001). Ischemic preconditioning upregulates vascular endothelial growth factor mRNA expression and neovasculariza-tion via nuclear translocation of protein kinase C e in the rat ischemic myocardium. Circ Res 88:696–704.
  • Kharbanda RK, Peters M, Walton B, Kattenhorn M, Mullen M, Klein N, Vallance P, Deanfield J, MacAl-lister R. (2001). Ischemic preconditioning prevents endothelial injury and systemic neutrophil activation during ischemia-reperfusion in humans in vivo. Circulation 103:1624–1630.
  • Komamura K, Kitakaze M, Nishida K, Naka M, Ta-mai J, Uematsu M, Koretsune Y, Nanto S, Hori M, Inoue M, Kamada T, Kodama K. (1994). Progressive decreases in coronary vein flow during reperfusion in acute myocardial infarction: clinical documentation of the no reflow phenomenon after successful throm-bolysis. J Am Coll Cardiol 24:370–377.
  • Korthuis RJ, Gute DC, Cepinskas G, Kvietys PR. (1998). Cellular mechanisms of acute vs delayed preconditioning. Pathophysiology 5:35–48.
  • Korthuis RJ, Dayton C, Yamaguchi T. (2002). Early and late preconditioning prevent ischemia/reperfusion injury: signaling pathways mediating the adaptive metamorphosis to a protected phenotype in preconditioned tissues. In: Schmid-Schonbein GW, Granger DN, editors Molecular Mechanisms of Microvascular Disorders. In press.
  • Kubes P, Payne D, Ostrovsky L. (1998). Preconditioning and adenosine in I/R-induced leukocyte-endothelial cell interactions. Am J Physiol 274: H1230–H1238.
  • Kurose I, Wolf R, Grisham MB, Granger DN. (1994). Modulation of ischemia/reperfusion-induced micro-vascular dysfunction by nitric oxide. Circ Res 74: 376–382.
  • Kurzelewski M, Czarnowska E, Maczewski M, Bere-sewicz A. (1999). Effect of ischemic preconditioning on endothelial dysfunction and granulocyte adhesion in isolated guinea pig hearts subjected to ischemia/ reperfusion. J Physiol Pharmacol 50:617–628.
  • Laude K, Thuillez C, Richard V. (2001). Coronary endothelial dysfunction after ischemia and reperfusion: a new therapeutic target? Braz J Med Biol Res 34:1–7.
  • Laude K, Richard V, Henry J-P, Lallemand F, Thu-illez C. (2000). Evidence against a role of inducible nitric oxide synthase in the endothelial protective effects of delayed preconditioning. Br J Pharmacol 130: 1547–1552.
  • Lefer AM, Hayward R. (2000). The role of nitric oxide in ischemia-reperfusion. In: Loscalzo J, Vita JA, editors. Contemporary Cardiology, vol 4: Nitric Oxide and the Cardiovascular System. Totowa, NJ: Humana Press Inc., pp. 357–380.
  • Liu X, Wu X, Wang S, Pang Y, Su J, Tang C. (1997). Protein kinase C in the protective effect of anoxic preconditioning on vascular smooth muscle cells. Zhongguo Ying Yong Sheng Li Xue Za Zhi 13:213–215.
  • Loke KE, Woodman OL. (1998). Preconditioning improves myocardial function and reflow, but not vasodilator reactivity, after ischaemia and reperfusion in anaesthetized dogs. Clin Exp Pharmacol Physiol 25:552–558.
  • Maczewski B, Beresewicz A. (1998). The role of aden-osine and ATP-sensitive potassium channels in the protection afforded by ischemic preconditioning against the post-ischemic endothelial dysfunction in guinea pig hearts. J Mol Cell Cardiol 30:1735–1747.
  • Maines MD. (1997). The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517–554.
  • Maines MD. (2000). The heme oxygenase system and its functions in the brain. Cell Mol Biol 46:573–585.
  • Marber MS. (2000). Ischemic preconditioning of isolated cells. Circ Res 86:926–931.
  • Masada T, Hua Y, Xi G, Ennis S, Keep RF. (2001). Attenuation of ischemic brain edema and cerebrovas-cular injury after ischemic preconditioning in the rat. J Cereb Blood Flow Metab 21:22–33.
  • Massberg S, Enders G, Leiderer R, Eisenmenger S, Vestweber D, Kromback F, Messmer K. (1998). Platelet-endothelial cell interactions during ischemia/ reperfusion; the role of P-selectin. Blood 92:507–515.
  • Massberg S, Enders G, Matos FC, Tomic LI, Leiderer R, Eisenmenger S, Messmer K, Krombach F. (1999). Fibrinogen deposition at the postischemic vessel wall promotes platelet adhesion during ischemia-reperfusion in vivo. Blood 94:3829–3838.
  • Matsuda N, Morgan KG, Sellke FW. (1999). Preconditioning improves cardioplegia-related coronary mi-crovascular smooth muscle hypercontractility: role of KATP channels. J Thorac Cardiovasc Surg 118:438–445.
  • Mazzoni M, Intaglietta M, Crogue Jr EJ, Arfors KE. (1992). Amiloride-sensitive Na+ pathways in capillary endothelial cell swelling during hemorrhagic shock. J Appl Physiol 73:1467–1473.
  • Meng X, Brown JM, Ao L, Shames BD, Banerjee A, Harken AH. (1999). Reduction in infarct size in the rat heart by LPS preconditioning is associated with expression of angiogenic growth factors and increased capillary density. Shock 12:25–31.
  • Merkus D, Stepp DW, Jones DW, Nishikawa Y, Chilian WM. (2000). Adenosine preconditions against en-dothelin-induced constriction of coronary arterioles. Am J Physiol 279:H2593–H2597.
  • Parratt JR, Vegh A, Zeitlein IJ, Ahmad M, Oldroyd K, Kaszala K, Papp JG. (1997). Bradykinin and endo-thelial-cardiac myocyte interactions in ischemic preconditioning. Am J Cardiol 80:124A–131A.
  • Parratt JR, Vegh A. (1999). Coronary vascular endo-thelium-myocyte interactions in protection of the heart by ischaemic preconditioning. J Physiol Pharmacol 50:509–524.
  • Peralta C, Prats N, Xaus C, Gelpi E, Rosello-Catafau J. (1999). Protective effect of liver ischemic preconditioning on liver and lung injury induced by hepatic ischemia-reperfusion in the rat. Hepatology 30: 1481–1489.
  • Pudupakkam S, Harris KA, Jamieson WG, DeRsoe G, Scott JA, Carson MW, Schlag MG, Kvietys PR, Potter RF. (1998). Ischemic tolerance in skeletal muscle: role of nitric oxide. Am J Physiol 275:H94–H99.
  • Ray PS, Estrada-Hernandez T, Sasaki H, Zhu L, Maulik N. (2000). Effects of hypoxia/reoxygenation on VEGF, Ang-1, Ang-2 and their receptors in the rat myocardium: implications for myocardial angiogene-sis. Mol Cell Biochem 213:145–153.
  • Ren Z, Yang Q, Floten HSA, Furnary AP, Yim AP, He GW. (2001). ATP-sensitive potassium channel openers may mimic the effects of hypoxic preconditioning on the coronary artery. Ann Thorac Surg 71:642–647.
  • Ricciardi R, Meyers WC, Schaffer BK, Kim RD, Shah SA, Wheeler SM, Donohue SE, Sheth KR, Callery MP, Chari RS. (2001). Protein kinase C inhibition abrogates hepatic ischemic preconditioning responses. J Surg Res 97:144–149.
  • Richard V, Kaeffer N, Tron C, Thuillez C. (1994). Ischemic preconditioning protects against coronary endothelial dysfunction induced by ischemia and reperfusion. Circulation 89:1254–1261.
  • Rubino A, Yellon DM. (2000). Ischaemic preconditioning of the vasculature: an overlooked phenomenon for protecting the heart? Trends Pharmacol Sci 21:225–230.
  • Sammut IA, Foresti R, Clark JE, Exon DJ, Vesely MJJ, Sarathchandra P, Green CJ, Motterlini R. (1998). Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1. Br J Pharmacol 125:1437–1444.
  • Sanz E, Dorado D, Oliveras J, Barrabes JA, Gonzales MA, Ruiz-Meana M, Solares J, Carreras MJ, Garcia-Lafuente A, Desco M, Soler-Soler J. (1995). Dissociation between anti-infarct effect and anti-edema effect of ischemic preconditioning. Am J Physiol 268:H233–H241.
  • Sasaki H, Ray PS, Zhu L, Otani H, Asahara T, Mau-lik N. (2001). Hypoxia/reoxygenation promotes myo-cardial angiogenesis via an NfkB-dependent mechanism in a rat model of chronic myocardial infarction. J Mol Cell Cardiol 33:283–294.
  • Shigematsu S, Ishida S, Gute DC, Korthuis RJ. (2001). Postischemic anti-inflammatory effects of bradykinin preconditioning. Am J Physiol 280:H441- H454.
  • Shinmura K, Tang XL, Xuan YT, Liu SQ, Takano H, Bhatnagar A, Bolli R. (2000). Cyclooxygenase-2 mediates the cardioprotective effects of the late phase of ischemic preconditioning in conscious rabbits. Proc Natl Acad Sci USA 97:10197–10202.
  • Tailor A, Granger DN. (2000). Role of adhesion molecules in vascular regulation and damage. Curr Hy-pertens Rep 2:78–83.
  • Thourani VH, Nakamura M, Duarte IG, Bufkin BL, Zhao ZQ, Jordan JE, Shearer ST, Guyton RA, Vinten-Johansen J. (1999). Ischemic preconditioning attenuates postischemic coronary artery endothelial dysfunction in a model of minimally invasive direct coronary artery bypass grafting. J Thorac Cardiovasc Surg 117:383–389.
  • Tofukuji M, Metais C, Li J, Hariawala MD, Franklin A, Vassileva C, Li J, Simons M, Sellke FW. (1998). Effects of ischemic preconditioning on myocardial perfusion, function, and microvascular regulation. Circulation 98(Suppl II):197–204.
  • Tong H, Chen W, Steenbergen C, Murphy E. (2000). Ischemic preconditioning activates phosphatidylino-sitol-3-kinase upstream from protein kinase C. Circ Res 87:309–315.
  • Tucker VL, Huxley VH. (1988). O2 modulation of single-vessel hydraulic conductance. Am J Physiol 254:H317–H323.
  • Vanhoutte P, Shimokawa H. (1989). Endothelium-derived relaxing factor and coronary vasospasm. Circulation 80:1–9.
  • Wang NP, Bufkin BL, Nakamura M, Zhao ZQ, Wil-cox JN, Hewan-Lowe KO, Guyton RA, Vinten-Johansen J. (1999). Ischemic preconditioning reduces neutrophil accumulation and myocardial apoptosis. Ann Thorac Surg 67:1689–1695.
  • Wang WZ, Tsai T-M, Anderson GL. (1999). Late-preconditioning protection is evident in the microcirculation of denervated skeletal muscle. J Orthopaed Res 17:571–577.
  • Wang WZ, Anderson GL, Maldonado C, Barker J. (1996). Attenuation of vasospasm and capillary no-reflow by ischemic preconditioning in skeletal muscle. Microsurgery 17:324–329.
  • Wang WZ, Anderson G, Firrell JC, Tsai T-M. (1998). Ischemic preconditioning versus intermittent reperfusion to improve blood flow to a vascular isolated skeletal muscle flap of rats. J Trauma 45:953–959.
  • Wang WZ, Anderson GL, Guo SZ, Tsai T-M, Miller FN. (2000). Initiation of microvascular protection by nitric oxide in late preconditioning. J Reconstruct Mi-crosurg 16:621–628.
  • Wang WZ, Guo SZ, Anderson GL, Miller FN. (2001). The initiating factors of late preconditioning in skeletal muscle. J Surg Res 99:92–99.
  • Woodman OL. (1999). Approaches to the prevention of coronary vascular dysfunction caused by myocar-dial ischaemia and reperfusion. Curr Pharm Des 5: 1077–1087.
  • Xuan YT, Y Guo, H Han, Y Zhu, R Bolli. (2001). An essential role of the JAK/STAT pathway in ischemic preconditioning. Proc Natl Acad Sci 98:9050–9055.
  • Yarimizu K, Ishida T, Akimitsu T, Korthuis RJ. (2002). Role of protein kinase C in postischemic mi-crovascular dysfunction. Am J Physiol (in preparation).
  • Zhang Y, Wu Y-X, Hao Y-B, Dun Y, Yang S-P. (2001). Role of endogenous opioid peptides in protection of ischemic preconditioning in rat small intestine. Life Sci 68:1013–1019.
  • Zhou X, Zhai X, Ashraf M. (1996). Preconditioning of bovine endothelial cells. The protective effect is mediated by an adenosine A2 receptor through a protein kinase C signaling pathway. Circ Res 78:73–81.
  • Zhou FW, Li YJ, Deng HW. (1998). Mediation of calcitonin gene-related peptide in protection of ische-mic preconditioning in rat hindlimbs. Zhongguo Yao Li Xue Bao 19:477–480.

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