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

Circulation Research

Volumn 81, Issue 6, 1997, Pages 1094-1107

  Bolli, Roberto ^a   Manchikalapudi, Srinivas ^a   Tang, Xian Liang ^a   Takano, Hitoshi ^a   Qiu, Yumin ^a   Guo, Yiru ^a   Zhang, Qin ^a   Jadoon, Asad K ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Aminoguanidine; L arginine; Myocardial reperfusion; N( ) nitro L arginine; S methylisothiourea sulfate

Indexed keywords

N(G) NITROARGININE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; HEART FUNCTION; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MEDIATOR RELEASE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; REPERFUSION; SECOND MESSENGER;

EID: 0030777615     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.81.6.1094     Document Type: Article

References (60)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124-1136.
2. Downey JM. Ischemic preconditioning: nature's own cardioprotectivc intervention. Trends Cardiovasc Med. 1992;2:170-176.
3. Cohen MV, Downey JM. Preconditioning during ischemia. Cardiol Rev. 1995;3:137-149.
4. Cohen MV, Yang XM, Downey JM. Conscious rabbits become tolerant to multiple episodes of ischemic preconditioning. Circ Res. 1944;74:998-1004.
5. Burckhartt B, Yang XM, Tsuchida A, Mullane KM, Downey JM, Cohce MV. Acadesine extends the window of protection afforded by ischemic preconditioning in conscious rabbits. Cardiovasc Res. 1995;29:653-657.
6. Oiu Y, Tang X-L, Park S-W, Sun J-Z, Kalya A, Bolli R, The early and late phases of ischemic preconditioning: a comparative analysis of their effects on infarct size, myocardial stunning, and arrhythmias in conscious pigs undergoing a 40-min coronary occlusion. Cire Res. 1997;80:730-742.
7. Kuzuya T, Hoshida S, Yamashita N, Fuji H, Oe H, Hori M, Kamada T, Tada M. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Cire Res. 1993;72:1293-1299.
8. Marber MS, Latchman DS, Walker JM, Yellon DM, Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation. 1993;88:1264-1272.
9. Baxter GF, Marber MS, Patel VC, Yellon DM, Adenosine receptor involvement in a delayed phase of myocardial protection 24 hours after ischemic preconditioning. Circulation. 1994;90:2993-3000.
10. Yang, XM, Baxter GF, Heads RJ, Yellon JM, Downey JM, Cohen MV. Infarct limitation of the second window of protection in a conscious rabbit model. Cardiovasc Res. 1996;31:777-783.
11. Sun J-Z, Tang X-L, Knowlton AA, Park SW, Oiu Y, Bolli R. Late preconditioning against myocardial stunning: an endogenous protective mechanism that confers resistance to postischemic dysfunction 24 h after brief ischemia in conscious pigs. J Clin Invest. 1995;95:388-403.
12. Sun J-Z, Tang X-L, Park SW, Qiu Y. Turrens JF, Bolli R. Evidence for an essential role of reactive oxygen species in the genesis of late preconditioning against myocardial stunning in conscious pigs. J Clin Invest. 1993;97:562-576.
13. Tang X-L, Qiu Y, Park S-W, Sun J-Z, Kalya A, Bolli R. Time course of late preconditioning asainst myocardial stunning in conscious pigs. Circ Res. 1996;79:424-434.
14. Bolli R, Bhatti ZA, Tang X-L, Qiu Y, Zhang Q, Guo Y, Jadoon AK. Evidence that late preconditioning against myocardial stunning in conscious rabbits is triggered by the Reneration of nitric oxide. Circ Res. 1997;81:42-52.
15. Maldonado C, Qiu Y, Tang X-L, Cohen MV, Auchampach J, Bolli R. Role of adenosine receptors in late preconditioning against myocardial stunning in conscious rabbits. Am J Physiol. 1997;273:H1324-H1332.
16. Ping P, Zhang J, Qiu Y, Tang X-L, Manchikalapudi S, Cao X, Bolli R. Ischemic preconditioning induces selective trunslocation of protein kinase C isofornis ∈ and η in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ Res. 1997;81:404-414.
17. 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. 1996;91:57-63.
18. Watanabe AM, Besch HR Jr. Interaction between cyclic adenosine monophosphate and cyclic guanosine monophosphate in guinea pig ventricular myocardium. Circ Res. 1975;37:309-317.
19. Balligand JL, Kelly RA, Marsden PA, Smith TW, Michel T, Control of cardiac muscle cell function by an endogenous nitric oxide signaling system, Proc Natl Acad Sci U S A. 1993;90:347-351.
20. Levi RC, Alloatti G, Fischmeister R. Cyclic GMP regulates the Ca-channel current in guinea pig ventricular myocytes, Eur J Physiol. 1989;413:685-687.
21. 2+ current: involvement of cGMp-inhibited and cGMP-stimulated phosphodiesterases through guanylyl cyclasc activation. J Biol Chem. 1993;268:26286-26295.
22. 2+-independent nitric oxide synthase in the myocardium, Br J Pharmacol. 1992;105:575-580.
23. Finkel MS, Oddis CV, Jacob TD, Watkins SC, Hattler BG, Simmons RL. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science, 1992;257:387-389.
24. Ungureanu-Longrois D, Balligand JL, Kelly RA, Smith TW. Myocardial contractile dysfunction in the systematic inflammatory response syndrome; role of a cytokine-inducible nitric oxide synthase in cardiac myocytes. J Mol Cell Cardiol, 1995;27:155-167.
25. Kelly RA, Balligand J-L, Smith TW. Nitric oxide and cardiac function. Circ Res, 1996;79:363-380.
26. Weiss HR, Rodriguez E, Tse J, Scholz PM. Effect of increased myocardial cyclic GMP induced by GMP-phosphodiesterase inhibition on oxygen consumption and supply of rabbit hearts. Clin Exp Pharmacol Physiol. 1994;21:607-614.
27. 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. 1994;75:1086-1095.
28. Shen W, Hintze TW, Wolin MS. Nitric oxide: an important signaling mechanism between vascular endothelium and parenchymal cells in the regulation of oxygen consumption. Circulation, 1995;92:3505-3512.
29. Xie Y-W, Shen W, Zhao G, Xu X, Wolin MS, Role of endothelium-derived nitric oxide in modulation of canine myocardial mitochondrial respiration in vitro: implications for the development of heart failure. Circ Res. 1996;79:381-387.
30. Bolli R. Mechanism of myocardial 'stunning.' Circulation, 1990;82:723-733.
31. Hasebe N, Shen YT, Vainer SF, Inhibition of endothelium-derived relaxing factor enhances myocardial stunning in conscious dogs, Circulation. 1993;88:2862-2871.
32. Southan GJ, Szabó C. Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. Biochem Pharmacol. 1996;51:383-394.
33. Misko TP, Moore WM, Kasten TP, Nickols GA, Corbett JA, Tilton RG, McDaniel ML, Williamson JR, Currie MG. Selective inhibition of the inducible nitric oxide synthase by aminoguanidine. Eur J Pharmacol. 1993;233:119-125.
34. SzabÓ C, Southan GJ, Thiemermann C. Beneficial effects and improved survival in rodent models of septic shock with S-methylisothiourea sulfate, a potent and selective inhibitor of inducible nitric oxide synthase, Proc Natl Acad Sci U S A. 1994;91:12472-12476.
35. Iadecola C, Zhang F, Xu X, Casey R, Ross ME, Inducible nitric oxide synthase gene expression in brain following focal cerebral ischemia. J Cereb Blood Flow Metab. 1995;15:378-384.
36. Triana JF, Li X-Y, Jamaluddin U, Thomby JI, Bolli R. Posttsehemic myocardial 'stunning': identification of major differences between the open-chest and the conscious dog and evaluation of the oxygen radical hypothesis in the conscious dog. Circ Res. 1991;69:731-747.
37. Li X-Y, McCay PB, Zughaib M, Jeroudi MO, Triana JF, Bolli R. Demonstration of free radical generation in the 'stunned' myocardium in the conscious dog and identification of major differences between conscious and open-chest dogs. J Clin Invest, 1993;92:1025-1041.
38. Bolli R. Common methodological problems and artifacts associated with studies of myocardial stunning in vivo, Basic Res Candiol. 1995;90:257-262.
39. Haessler R, Kuzume K, Chien GL, Wolff RA, Davis RF, Van Winkle DM. Anaesthetics alter the magnitude of infarct limitation by ischaemic preconditioning, Cardiovasc Res. 1994;28:1574-1580.
40. Schwanz LM, Jennings RB, Reimer KA, Premedication with the opioid analgesic butorphanol raises the threshold for ischemic preconditioning in dogs, Basic Res Cardiol. 1997;92:106-114.
41. G-nitro-L-arginine and aminoguanidine on constitutive and inducible nitric oxide synthase in rat aorta, Biochem Res Commun, 1994;199:147-154.
42. Wu C-C, Chen S-J, Szabó C, Thiemermann C, Vane JR. Aminoguanidine attenuates the delayed circulatory failure and improves survival in rodent models of endotoxic shock, Br J Pharmacol. 1995;114:1666-1672.
43. Griffiths MJ, Messent M, MacAllister RJ, Evans TW. Aminoguanidine selectively inhibits inducible nitric oxide synthase, Br J Pharmacol, 1993;110:963-968.
44. Bolli R, Zhu WX, Myers ML, Hartley CJ, Roberts R. Betaadrenergic stimulation reverses postischemic myocardial dysfunction without producing subsequent functional deterioration. Am J Cardiol. 1985;56:964-968.
45. SAS institute. SAS/STAT User's Guide, Release of 6.03 ed, Cary, NC: SAS Institute; 1988:675-712.
46. Hoshida S, Kuzuya T, Fuji H, Yamashita N, Oe H, Hori M, Suzuki K, Taniguchi N, Tada M. Sublethal ischemia alters myocardial antioxidani activity in canine heart, Am J Physiol. 1993;264:H33-H39.
47. Thanos T, Maniatts T. NF-κB: a lesson in family values. Cell. 1995;80:529-532.
48. Traystman RJ, Moore LE. Helfaer MA, Davis S, Banasiak K, Williams M, Hurn PD, Nitro-L-arginine analogues: dose- and timerelated nitric oxide synthase inhibition in brain. Stroke, 1995;26:864-869.
49. Liu J-L, Murakami H, Zucker IH. Effects of NO on baroreflex control of heart rate and renal nerve activity in conscious rabbits. Am J Physiol. 1996;39:R1361-R1370.
50. Reinhart GA, Lohmeier TE, Mizelle HL. Temporal influence of the renal nerves on renal excretory function during chronic inhibition of nitric oxide synthesis. Hypertension, 1997;29:199-204.
51. Hasan K, Heesen B-J, Corbett JA, McDaniel ML, Chang K, Allison W, Wolffenbuttel BHR, Williarason JR, Tilton RG. Inhibition of nitric oxide formation by guanidines. Eur J Pharmacol. 1993;249:101-106.
52. Corbett JA, Tilton RG, Chang K, Hasan KS, Ido Y, Wang JL, Sweetland MA, Lancaster JR Jr, Williamson JR, McDaniel ML. Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction, Diabetes. 1992;41:552-556.
53. Southan GJ, Szabo C, Thiemermann C. Isothioureas: potent inhibitors of nitric oxide syntheses with variable isoform selectivity. Br J Pharmacol. 1995;114:510-516.
54. Kim S-J, Ghaleh B, Kudej RK, Huang C-H, Hintze TH, Vatner SF. Delayed enhanced nitric oxide-mediated coronary vasodilation following brief ischemia and prolonged reperfusion in conscious dogs, Cire Res. 1997;81:53-59.
55. Zhao L, Weber PA, Smith JR, Comerford ML, Elliott GT. Role of inducible nitric oxide synthase in pharmacological 'preconditioning' with monophosphoryl lipid A, J Mol Cell Cardiol, 1997;29:1567-1576.
56. 3, in plasma after experimental myocardial infarction. J Mol Cell Cardiol. 1997;29:1-9.
57. Vegh A, Papp JG, Parratt JR. Prevention by dexamethasone of the marked antiarrhythmic effects of preconditioning induced 20 h after rapid cardiac pacing, Br J Pharmacol. 1994;113:1081-1082.
58. Lander HM, Schajpal P, Levine DM, Novogrodsky A. Activation of human peripheral blood mononuclear cells by nitric oxidegenerating compounds. J Immunol. 1993;150:1509-1516.
59. Sase K, Michel T. Expression and regulation of endothelial nitric oxide synthase. Trends Cardiovasc Med. 1997;7:28-37.
60. Sessa WC, Kirkwood P, Seyedi N, Wang J, Hintze TH. Chronic exercise in dogs increase coronary vascular nitric oxide production and endotheiial cell nitric oxide synthase gene expression. Circ Res. 1994;74:349-353.