Role of Heme Oxygenase in the Protection Afforded Skeletal Muscle During Ischemic Tolerance

REFERENCES

• Appleton S D, Chretien M L, Mc Laughlin B E, Vreman H J, Stevenson D K, Brien J F, Nakatsu K, Maurice D H, Marks G S. Selective inhibition of heme oxygenase, without inhibition of nitric oxide synthase or soluble guanylyl cyclase, by metalloporphyrins at low concentrations. Drug Metab Dispos 1999; 27: 1214–1219, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Badhwar A, Bihari A, Dungey A A, Scott J R, Albion C D, Forbes T L, Harris K A, Potter R F. Protective mechanisms during ischemic tolerance in skeletal muscle. Free Radic Biol Med 2004; 36: 371–379, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Badhwar A, Dungey A A, Harris K A, Scott J A, Mc Carter S D, Scott J R, Forbes T L, Potter R F. Limitations of ischemic tolerance in oxidative skeletal muscle: perfusion vs tissue protection. J Surg Res 2003; 109: 62–67, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Barnett C C, Moore E E, Moore F A, Biffl W L, Smith M F, Jr, Carl V S. Intercellular adhesion molecule-1 promotes neutrophil-mediated cytotoxicity. Surgery 1995; 118: 171–175, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Barroso-Aranda J, Schmid-Schönbein G W, Zweifach B W, Engler R L. Granulocytes and no-reflow phenomenon in irreversible hemorrhagic shock. Circ Res 1988; 63: 437–447, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Baxter G F, Goma F M, Yellon D M. Characterisation of the infarct-limiting effect of delayed preconditioning: timecourse and dose-dependency studies in rabbit myocardium. Basic Res Cardiol 1997; 92: 159–167, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMed Web of Science ®Google Scholar
• Bell R M, Smith C C, Yellon D M. Nitric oxide as a mediator of delayed pharmacological (A(1) receptor triggered) preconditioning: is eNOS masquerading as iNOS?. Cardiovasc Res 2002; 53: 405–413, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Bertuglia S, Colantuoni A, Intaglietta M. Effect of leukocyte adhesion and microvascular permeability on capillary perfusion during ischemia-reperfusion injury in hamster cheek pouch. Int J Microcirc Clin Exp 1993; 13: 13–26, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Bolli R, Manchikalapudi S, Tang X L, Takano H, Qiu Y, Guo Y, Zhang Q, Jadoon A K. The protective effect of late preconditioning against myocardial stunning in conscious rabbits is mediated by nitric oxide synthase: evidence that nitric oxide acts both as a trigger and as a mediator of the late phase of ischemic preconditioning. Circ Res 1997; 81: 1094–1107, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Bradford M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248–254, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMed Web of Science ®Google Scholar
• Braide M, Amundson B, Chien S, Bagge U. Quantitative studies on the influence of leukocytes on the vascular resistance in a skeletal muscle preparation. Microvasc Res 1984; 27: 331–352, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMed Web of Science ®Google Scholar
• Butler J, Rocker G M, Westaby S. Inflammatory response to cardiopulmonary bypass. Ann Thorac Surg 1993; 55: 552–559, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Camilleri J P, Fabiani J N. No-reflow phenomenon and acute myocardial ischemia. the need for further investigation. Biomedicine 1977; 26: 353–356, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Carter Y M, Thomas R, Bargatze R, Poppa V, Jutila M, Murry C E, Allen M D. Intracoronary E-/ L-selectin blockade reduces neutrophil infiltration in heart transplantation. Ann Thorac Surg 2002; 74: 2064–2070, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Chen J, Simon R. Ischemic tolerance in the brain. Neurology 1997; 48: 306–311, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Davis J M, Gute D C, Jones S, Krsmanovic A, Korthuis R J. Ischemic preconditioning prevents postischemic P-selectin expression in the rat small intestine. Am J Physiol 1999; 277: H2476–H2481, [PUBMED], [INFOTRIEVE], [CSA]
   PubMedGoogle Scholar
• Duan C, Yan F, Song X, Lu G W. Changes of superoxide dismutase, glutathione perioxidase and lipid peroxides in the brain of mice preconditioned by hypoxia. Biol Signals Recept 1999; 8: 256–260, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Engler R L, Dahlgren M D, Morris D D, Peterson M A, Schmid-Schönbein G W. Role of leukocytes in response to acute myocardial ischemia and reflow in dogs. Am J Physiol 1986; 251: H314–H323, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Fishbein M C, Rit J, Lando U, Kanmatsuse K, Mercier J C, Ganz W. The relationship of vascular injury and myocardial hemorrhage to necrosis after reperfusion. Circulation 1980; 62: 1274–1279, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Galinanes M, Lawson C S, Ferrari R, Limb G A, Derias N W, Hearse D J. Early and late effects of leukopenic reperfusion on the recovery of cardiac contractile function: Studies in the transplanted and isolated blood-perfused rat heart. Circulation 1993; 88: 673–683, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Gute D C, Ishida T, Yarimizu K, Korthuis R J. Inflammatory responses to ischemia and reperfusion in skeletal muscle. Mol Cell Biochem 1998; 179: 169–187, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMed Web of Science ®Google Scholar
• Harkin D W, Barros D'Sa A A, Mc Callion K, Hoper M, Campbell F C. Ischemic preconditioning before lower limb ischemia–reperfusion protects against acute lung injury. J Vasc Surg 2002; 35: 1264–1273, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Harkin D W, Barros D'Sa A A, Mc Callion K, Hoper M, Halliday M I, Campbell F C. Circulating neutrophil priming and systemic inflammation in limb ischaemia-reperfusion injury. Int Angiol 2001; 20: 78–89, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Harris A G, Skalak T C. Effects of leukocyte capillary plugging in skeletal muscle ischemia-reperfusion injury. Am J Physiol 1996; 271: H2653–H2660, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Hartsfield C L, Alam J, Cook J L, Choi A M. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol 1997; 273: L980–L988, [PUBMED], [INFOTRIEVE], [CSA]
   PubMedGoogle Scholar
• Hayashi S, Takamiya R, Yamaguchi T, Matsumoto K, Tojo S J, Tamatani T, Kitajima M, Makino N, Ishimura Y, Suematsu M. Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme. Circ Res 1999; 85: 663–671, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Ishikawa K, Navab M, Leitinger N, Fogelman A M, Lusis A J. Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL. J Clin Invest 1997; 100: 1209–1216, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Kaeffer N, Richard V, Francois A, Lallemand F, Henry J P, Thuillez C. Preconditioning prevents chronic reperfusion-induced coronary endothelial dysfunction in rats. Am J Physiol 1996; 271: H842–H849, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Kitagawa K, Matsumoto M, Kuwabara K, Tagaya M, Ohtsuki T, Hata R, Ueda H, Handa N, Kimura K, Kamada T. ‘Ischemic tolerance’ phenomenon detected in various brain regions. Brain Res 1991; 561: 203–211, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMed Web of Science ®Google Scholar
• Kukreja R C. Essential role of oxygen radicals in delayed pharmacological preconditioning. J Mol Cell Cardiol 2001; 33: 1395–1398, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMedGoogle Scholar
• Kume M, Yamamoto Y, Saad S, Gomi T, Kimoto S, Shimabukuro T, Yagi T, Nakagami M, Takada Y, Morimoto T, Yamaoka Y. Ischemic preconditioning of the liver in rats: implications of heat shock protein induction to increase tolerance of ischemia-reperfusion injury. J Lab Clin Med 1996; 128: 251–258, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMed Web of Science ®Google Scholar
• Kurose I, Anderson D C, Miyasaka M, Tamatani T, Paulson J C, Todd R F, Rusche J R, Granger D N. Molecular determinants of reperfusion-induced leukocyte adhesion and vascular protein leakage. Circ Res 1994; 74: 336–343, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Lee B Y, Wilson G J, Domenech R J, Mac Gregor D C. Relative roles of edema versus contracture in the myocardial postischemic “no-reflow” phenomenon. J Surg Res 1980; 29: 50–61, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Lu R, Peng J, Xiao L, Deng H W, Li Y J. Heme oxygenase-1 pathway is involved in delayed protection induced by heat stress against cardiac ischemia–reperfusion injury. Int J Cardiol 2002; 82: 133–140, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMedGoogle Scholar
• Mattei A, Sutter P M, Marx A, Stierli P, Heberer M, Gurke L. Preconditioning with short cycles improves ischemic tolerance in rat fast- and slowtwitch skeletal muscle. Eur Surg Res 2000; 32: 297–304, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• McCarter S D, Akyea T G, Lu X, Bihari A, Scott J R, Badhwar A, Dungey A A, Harris K A, Feng Q, Potter R F. Endogenous heme oxygenase induction is a critical mechanism attenuating apoptosis and restoring microvascular perfusion following limb ischemia/reperfusion. Surgery 2004; 136: 67–75, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Mc Cord J M. Free radicals and myocardial ischemia: overview and outlook. Free Radic Biol Med 1988; 4: 9–14, [CSA], [CROSSREF]
   Google Scholar
• McCord J M, Roy R S. The pathophysiology of superoxide: roles in inflammation and ischemia. Can J Physiol Pharmacol 1982; 60: 1346–1352, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• McCord J M, Roy R S, Schaffer S W. Free radicals and myocardial ischemia: The role of xanthine oxidase. Adv Myocardiol 1985; 5: 183–189, [PUBMED], [INFOTRIEVE], [CSA]
   PubMedGoogle Scholar
• Murry C E, Jennings R B, Reimer K A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124–1136, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Oberle S, Abate A, Grosser N, Hemmerle A, Vreman H J, Dennery P A, Schneider H T, Stalleicken D, Schroder H. Endothelial protection by pentaerithrityl trinitrate: bilirubin and carbon monoxide as possible mediators. Exp Biol Med (Maywood) 2003; 228: 529–534, [CSA]
   PubMed Web of Science ®Google Scholar
• Osborne D L, Aw T Y, Cepinskas G, Kvietys P R. Development of ischemia/reperfusion tolerance in the rat small intestine: an epithelium-independent event. J Clin Invest 1994; 94: 1910–1918, [PUBMED], [INFOTRIEVE], [CSA]
   PubMedGoogle Scholar
• Potter R F, Dietrich H H, Tyml K, Ellis C G, Cronkwright J, Groom A C. Ischemia–reperfusion induced microvascular dysfunction in skeletal muscle: application of intravital video microscopy. Int J Microcirc Clin Exp 1993; 13: 173–186, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Pudupakkam S, Harris K A, Jamieson W G, De Rose G, Scott J A, Carson M W, Schlag M G, Kvietys P R, Potter R F. Ischemic tolerance in skeletal muscle: role of nitric oxide. Am J Physiol 1998; 275: H94–H99, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Reimer K A, Murry C E, Yamasawa I, Hill M L, Jennings R B. Four brief periods of myocardial ischemia cause no cumulative ATP loss or necrosis. Am J Physiol 1986; 251: H1306–H1315, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Rowland R T, Meng X, Ao L, Terada L S, Harken A H, Brown J M. Mechanisms of immature myocardial tolerance to ischemia: phenotypic differences in antioxidants, stress proteins, and oxidases. Surgery 1995; 118: 446–452, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Sammut I A, Foresti R, Clark J E, Exon D J, Vesely M J, Sarathchandra P, Green C J, Motterlini R. Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1. Br J Pharmacol 1998; 125: 1437–1444, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   PubMed Web of Science ®Google Scholar
• Sawaya D E. J, Brown M, Minardi A, Bilton B, Burney D, Granger D N, McDonald J C, Zibari G B. The role of ischemic preconditioning in the recruitment of rolling and adherent leukocytes in hepatic venules after ischemia/reperfusion. J Surg Res 1999; 85: 163–170, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Schlag M G, Clarke S, Carson M W, Harris K A, Potter R F. The effect of mannitol versus dimethyl thiourea at attenuating ischemia/reperfusion-induced injury to skeletal muscle. J Vasc Surg 1999; 29: 511–521, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Sekizuka E, Benoit J N, Grisham M B, Granger D N. Dimethylsulfoxide prevents chemoattractant-induced leukocyte adherence. Am J Physiol 1989; 256: H594–H597, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Werns S W, Shea M J, Lucchesi B R. Free radicals in ischemic myocardial injury. J Free Radic Biol Med 1985; 1: 103–110, [PUBMED], [INFOTRIEVE], [CSA]
   PubMedGoogle Scholar
• Wunder C, Brock R W, Mc Carter S D, Bihari A, Harris K, Eichelbronner O, Potter R F. Inhibition of haem oxygenase activity increases leukocyte accumulation in the liver following limb ischaemia-reperfusion in mice. J Physiol 2002; 540: 1013–1021, [PUBMED], [INFOTRIEVE], [CSA]
   Google Scholar
• Wunder C, Scott J R, Lush C W, Brock R W, Bihari A, Harris K, Eichelbronner O, Potter R F. Heme oxygenase modulates hepatic leukocyte sequestration via changes in sinusoidal tone in systemic inflammation in mice. Microvasc Res 2004; 68: 20–29, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Xuan Y T, Tang X L, Qiu Y, Banerjee S, Takano H, Han H, Bolli R. Biphasic response of cardiac NO synthase isoforms to ischemic preconditioning in conscious rabbits. Am J Physiol Heart Circ Physiol 2000; 279: H2360–H2371, [PUBMED], [INFOTRIEVE], [CSA]
   PubMedGoogle Scholar
• Yokota J, Minei J P, Fantini G A, Shires G T. Role of leukocytes in reperfusion injury of skeletal muscle after partial ischemia. Am J Physiol 1989; 257: H1068–H1075, [PUBMED], [INFOTRIEVE], [CSA]
   PubMedGoogle Scholar
• Zhang F, Kaide J, Wei Y, Jiang H, Yu C, Balazy M, Abraham N G, Wang W, Nasjletti A. Carbon monoxide produced by isolated arterioles attenuates pressure-induced vasoconstriction. Am J Physiol Heart Circ Physiol 2001; 281: H350–H358, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar
• Zhao L, Weber P A, Smith J R, Comerford M L, Elliott G T. Role of inducible nitric oxide synthase in pharmacological “preconditioning” with monophosphoryl lipid A. J Mol Cell Cardiol 1997; 29: 1567–1576, [PUBMED], [INFOTRIEVE], [CSA], [CROSSREF]
   Google Scholar
• Zhao T, Xi L, Chelliah J, Levasseur J E, Kukreja R C. Inducible nitric oxide synthase mediates delayed myocardial protection induced by activation of adenosine A(1) receptors: evidence from gene-knockout mice. Circulation 2000; 102: 902–907, [PUBMED], [INFOTRIEVE], [CSA]
   PubMed Web of Science ®Google Scholar