Ischemic preconditioning prevents in vivo hyperoxygenation in postischemic myocardium with preservation of mitochondrial oxygen consumption

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 293, Issue 3, 2007, Pages

  Zhu, Xuehai ^a,b   Liu, Bin ^a   Zhou, Shaotang ^a   Chen, Yeong Renn ^a   Deng, Yuanmu ^a   Zweier, Jay L ^a   He, Guanglong ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c NONE   (United States)

Author keywords

Free radicals; Ischemia reperfusion; Mitochondria; Nitric oxide; Peroxynitrite; Reactive oxygen species; Redox

Indexed keywords

3 NITROTYROSINE; CYTOCHROME C OXIDASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITRO DEXTRO ARGININE METHYL ESTER; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD FLOW; CONTROLLED STUDY; CORONARY REPERFUSION; ELECTRON SPIN RESONANCE; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HYPEROXIA; IN VIVO STUDY; ISCHEMIC PRECONDITIONING; KNOCKOUT MOUSE; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; OXYGEN TENSION; PRIORITY JOURNAL; REPERFUSION INJURY;

ANIMALS; CORONARY VESSELS; CYTOCHROMES C; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCARDIAL INFARCTION; MYOCARDIUM; NADH DEHYDROGENASE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; REGIONAL BLOOD FLOW; TYROSINE;

EID: 34548420201     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00256.2007     Document Type: Article

References (60)

1. Al-Obaidi MK, Etherington PJ, Barron DJ, Winlove CP, Pepper JR. Myocardial tissue oxygen supply and utilization during coronary artery bypass surgery: evidence of microvascular no-reflow. Clin Sci (Lond) 98: 321-328, 2000.
2. An J, Camara AK, Rhodes SS, Riess ML, Stowe DF. Warm ischemic preconditioning improves mitochondrial redox balance during and after mild hypothermic ischemia in guinea pig isolated hearts. Am J Physiol Heart Circ Physiol 288: H2620-H2627, 2005.
3. Baines CP, Wang L, Cohen MV, Downey JM. Protein tyrosine kinase is downstream of protein kinase C for ischemic preconditioning's anti-infarct effect in the rabbit heart. J Mol Cell Cardiol 30: 383-392, 1998.
4. Baxter GF, Ferdinandy P. Delayed preconditioning of myocardium: current perspectives. Basic Res Cardiol 96: 329-344, 2001.
5. Bolli R. The early and late phases of preconditioning against myocardial stunning and the essential role of oxyradicals in the late phase: an overview. Basic Res Cardiol 91: 57-63, 1996.
6. Bolli R, Dawn B, Tang XL, Qiu Y, Ping P, Xuan YT, Jones WK, Takano H, Guo Y, Zhang J. The nitric oxide hypothesis of late preconditioning. Basic Res Cardiol 93: 325-338, 1998.
7. Borbely A, Toth A, Edes I, Virag L, Papp JG, Varro A, Paulus WJ, van der Velden J, Stienen GJ, Papp Z. Peroxynitrite-induced alpha-actinin nitration and contractile alterations in isolated human myocardial cells. Cardiovasc Res 67: 225-233, 2005.
8. Braunwald E, Kloner RA. Myocardial reperfusion: a double-edged sword? J Clin Invest 76: 1713-1719, 1985.
9. Brown GC. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 1504: 46-57, 2001.
10. Chen YR, Chen CL, Chen W, Zweier JL, Augusto O, Radi R, Mason RP. Formation of protein tyrosine ortho-semiquinone radical and nitrotyrosine from cytochrome c-derived tyrosyl radical. J Biol Chem 279: 18054-18062, 2004.
11. Cohen MV, Baines CP, Downey JM. Ischemic preconditioning: from adenosine receptor to KATP channel. Annu Rev Physiol 62: 79-109, 2000.
12. Csonka C, Csont T, Onody A, Ferdinandy P. Preconditioning decreases ischemia/reperfusion-induced peroxynitrite formation. Biochem Biophys Res Commun 285: 1217-1219, 2001.
13. Dawn B, Bolli R. Role of nitric oxide in myocardial preconditioning. Ann NY Acad Sci 962: 18-41, 2002.
14. Ferdinandy P, Das DK, Tosaki A. Pacing-induced ventricular fibrillation leading to oxygen free radical formation in aerobically perfused rat hearts. J Mol Cell Cardiol 25: 683-692, 1993.
15. Ferdinandy P, Schulz R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 138: 532-543, 2003.
16. Guo Y, Wu WJ, Qiu Y, Tang XL, Yang Z, Bolli R. Demonstration of an early and a late phase of ischemic preconditioning in mice. Am J Physiol Heart Circ Physiol 275: H1375-H1387, 1998.
17. Hide EJ, Thiemermann C. Limitation of myocardial infarct size in the rabbit by ischaemic preconditioning is abolished by sodium 5-hydroxydecanoate. Cardiovasc Res 31: 941-946, 1996.
18. Hoffmeyer MR, Jones SP, Ross CR, Sharp B, Grisham MB, Laroux FS, Stalker TJ, Scalia R, Lefer DJ. Myocardial ischemia/reperfusion injury in NADPH oxidase-deficient mice. Circ Res 87: 812-817, 2000.
19. Ilangovan G, Zweier JL, Kuppusamy P. Mechanism of oxygen-induced EPR line broadening in lithium phthalocyanine microcrystals. J Magn Reson 170: 42-48, 2004.
20. Imagawa J, Baxter GF, Yellon DM. Genistein, a tyrosine kinase inhibitor, blocks the "second window of protection" 48 h after ischemic preconditioning in the rabbit. J Mol Cell Cardiol 29: 1885-1893, 1997.
21. Jones SP, Trocha SD, Strange MB, Granger DN, Kevil CG, Bullard DC, Lefer DJ. Leukocyte and endothelial cell adhesion molecules in a chronic murine model of myocardial reperfusion injury. Am J Physiol Heart Circ Physiol 279: H2196-H2201, 2000.
22. Juhasz B, Der P, Turoczi T, Bacskay I, Varga E, Tosaki A. Preconditioning in intact and previously diseased myocardium: laboratory or clinical dilemma? Antioxid Redox Signal 6: 325-333, 2004.
23. Liaudet L, Yang Z, Al-Affar EB, Szabo C. Myocardial ischemic preconditioning in rodents is dependent on poly (ADP-ribose) synthetase. Mol Med 7: 406-417, 2001.
24. Liu GS, Thornton J, Van Winkle DM, Stanley AW, Olsson RA, Downey JM. Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation 84: 350-356, 1991.
25. Liu KJ, Gast P, Moussavi M, Norby SW, Vahidi N, Walczak T, Wu M, Swartz HM. Lithium phthalocyanine: a probe for electron paramagnetic resonance oximetry in viable biological systems. Proc Natl Acad Sci USA 90: 5438-5442, 1993.
26. Liu Y, Downey JM. Ischemic preconditioning protects against infarction in rat heart. Am J Physiol Heart Circ Physiol 263: H1107-H1112, 1992.
27. Lizasoain I, Moro MA, Knowles RG, Darley-Usmar V, Moncada S. Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem J 314: 877-880, 1996.
28. Mani AR, Ippolito S, Ollosson R, Moore KP. Nitration of cardiac proteins is associated with abnormal cardiac chronotropic responses in rats with biliary cirrhosis. Hepatology 43: 847-856, 2006.
29. Maulik N, Sato M, Price BD, Das DK. An essential role of NFkappaB in tyrosine kinase signaling of p38 MAP kinase regulation of myocardial adaptation to ischemia. FEBS Lett 429: 365-369, 1998.
30. 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.
31. Murphy E. Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection. Circ Res 94: 7-16, 2004.
32. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136, 1986.
33. O'Rourke B. Evidence for mitochondrial K+ channels and their role in cardioprotection. Circ Res 94: 420-432, 2004.
34. Ping P, Zhang J, Qiu Y, Tang XL, Manchikalapudi S, Cao X, Bolli R. Ischemic preconditioning induces selective translocation of protein kinase C isoforms epsilon and eta in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ Res 81: 404-414, 1997.
35. Robinson MJ, Cobb MH. Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 9: 180-186, 1997.
36. Rolfe DF, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77: 731-758, 1997.
37. Roy S, Khanna S, Bickerstaff AA, Subramanian SV, Atalay M, Bierl M, Pendyala S, Levy D, Sharma N, Venojarvi M, Strauch A, Orosz CG, Sen CK. Oxygen sensing by primary cardiac fibroblasts: a key role of p21(Waf1/Cip1/Sdi1). Circ Res 92: 264-271, 2003.
38. Schultz JJ, Hsu AK, Gross GJ. Ischemic preconditioning and morphine-induced cardioprotection involve the delta (delta)-opioid receptor in the intact rat heart. J Mol Cell Cardiol 29: 2187-2195, 1997.
39. Schulz R, Cohen MV, Behrends M, Downey JM, Heusch G. Signal transduction of ischemic preconditioning. Cardiovasc Res 52: 181-198, 2001.
40. Shen W, Xu X, Ochoa M, Zhao G, Wolin MS, Hintze TH. Role of nitric oxide in the regulation of oxygen consumption in conscious dogs. Circ Res 75: 1086-1095, 1994.
41. Swartz HM, Bacic G, Friedman B, Goda F, Grinberg O, Hoopes PJ, Jiang J, Liu KJ, Nakashima T, O'Hara J. Measurements of pO2 in vivo, including human subjects, by electron paramagnetic resonance. Adv Exp Med Biol 361: 119-128, 1994.
42. Szendrei L, Turoczi T, Kovacs P, Vecsernyes M, Das DK, Tosaki A. Mitochondrial gene expression and ventricular fibrillation in ischemic/reperfused nondiabetic and diabetic myocardium. Biochem Pharmacol 63: 543-552, 2002.
43. Tanoue Y, Herijgers P, Meuris B, Verbeken E, Leunens V, Lox M, Flameng W. Ischemic preconditioning reduces unloaded myocardial oxygen consumption in an in-vivo sheep model. Cardiovasc Res 55: 633-641, 2002.
44. Teng RJ, Ye YZ, Parks DA, Beckman JS. Urate produced during hypoxia protects heart proteins from peroxynitrite-mediated protein nitration. Free Radic Biol Med 33: 1243-1249, 2002.
45. Tosaki A, Engelman DT, Engelman RM, Das DK. The evolution of diabetic response to ischemia/reperfusion and preconditioning in isolated working rat hearts. Cardiovasc Res 31: 526-536, 1996.
46. Tosaki A, Pali T, Droy-Lefaix MT. Effects of Ginkgo biloba extract and preconditioning on the diabetic rat myocardium. Diabetologia 39: 1255-1262, 1996.
47. Vahlhaus C, Schulz R, Post H, Onallah R, Heusch G. No prevention of ischemic preconditioning by the protein kinase C inhibitor staurosporine in swine. Circ Res 79: 407-414, 1996.
48. Van Winkle DM, Chien GL, Wolff RA, Soifer BE, Kuzume K, Davis RF. Cardioprotection provided by adenosine receptor activation is abolished by blockade of the KATP channel. Am J Physiol Heart Circ Physiol 266: H829-H839, 1994.
49. Wall TM, Sheehy R, Hartman JC. Role of bradykinin in myocardial preconditioning. J Pharmacol Exp Ther 270: 681-689, 1994.
50. Wang P, Zweier JL. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J Biol Chem 271: 29223-29230, 1996.
51. Wei G, Zweier JL. Endothelial nitric oxide synthase is essential for acute ischemic preconditioning (Abstract). FASEB J 15: A465, 2001.
52. Wolin MS, Xie YW, Hintze TH. Nitric oxide as a regulator of tissue oxygen consumption. Curr Opin Nephrol Hypertens 8: 97-103, 1999.
53. Xi L, Hess ML, Kukreja RC. Ischemic preconditioning in isolated perfused mouse heart: reduction in infarct size without improvement of post-ischemic ventricular function. Mol Cell Biochem 186: 69-77, 1998.
54. Xie YW, Shen W, Zhao G, Xu X, Wolin MS, Hintze TH. Role of endothelium-derived nitric oxide in the modulation of canine myocardial mitochondrial respiration in vitro. Implications for the development of heart failure. Circ Res 79: 381-387, 1996.
55. Zhao X, He G, Chen YR, Pandian RP, Kuppusamy P, Zweier JL. Endothelium-derived nitric oxide regulates postischemic myocardial oxygenation and oxygen consumption by modulation of mitochondrial electron transport. Circulation 111: 2966-2972, 2005.
56. Zhu X, Zuo L, Cardounel AJ, Zweier JL, He G. Characterization of in vivo tissue redox status, oxygenation, and formation of reactive oxygen species in postischemic myocardium. Antioxid Redox Signal 9: 447-455, 2007.
57. Zweier JL, Chzhan M, Ewert U, Schneider G, Kuppusamy P. Development of a highly sensitive probe for measuring oxygen in biological tissues. J Magn Reson B 105: 52-57, 1994.
58. 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, 1988.
59. Zweier JL, Kuppusamy P, Williams R, Rayburn BK, Smith D, Weisfeldt ML, Flaherty JT. Measurement and characterization of postischemic free radical generation in the isolated perfused heart. J Biol Chem 264: 18890-18895, 1989.
60. Zweier JL, Talukder MA. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 70: 181-190, 2006.