Nuclear factor-κB plays an essential role in the late phase of ischemic preconditioning in conscious rabbits

Circulation Research

Volumn 84, Issue 9, 1999, Pages 1095-1109

  Xuan, Yu Ting ^a   Tang, Xian Liang ^a   Banerjee, Supratim ^a   Takano, Hitoshi ^a   Li, Richard C X ^a   Han, Hui ^a   Qiu, Yumin ^a   Li, Jian Jun ^a   Bolli, Roberto ^a  

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

Author keywords

Inducible nitric oxide synthase; Myocardial adaptation; Myocardial ischemia reperfusion; Peroxynitrite; Postischemic myocardial dysfunction

Indexed keywords

CHELERYTHRINE; DIETHYLENETRIAMINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LAVENDUSTIN A; NITRATE; NITRIC OXIDE SYNTHASE; PEROXYNITRITE; PROTEIN TYROSINE KINASE INHIBITOR; SCAVENGER; TRANSCRIPTION FACTOR; ALKALOID; BENZOPHENANTHRIDINE DERIVATIVE; DIETHYLDITHIOCARBAMIC ACID; DIETHYLTOLUAMIDE; DNA; DRUG DERIVATIVE; GLYCINE; N (2 MERCAPTOPROPRIONYL) GLYCINE; N(G) NITROARGININE; N-(2-MERCAPTOPROPRIONYL)-GLYCINE; PHENANTHRIDINE DERIVATIVE; PHENOL DERIVATIVE; THIOL DERIVATIVE; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONSCIOUSNESS; DNA BINDING; ENZYME ACTIVITY; GEL ELECTROPHORESIS; GENE ACTIVATION; GENETIC ANALYSIS; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; RABBIT; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; HEART; HEART INFARCTION PREVENTION; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TISSUE DISTRIBUTION;

ALKALOIDS; ANIMALS; BENZOPHENANTHRIDINES; DEET; DITIOCARB; DNA; GLYCINE; HEART; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; NF-KAPPA B; NITROARGININE; PHENANTHRIDINES; PHENOLS; RABBITS; SULFHYDRYL COMPOUNDS; TISSUE DISTRIBUTION; TRANSCRIPTION FACTOR RELA;

EID: 0033553223     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.84.9.1095     Document Type: Article

References (65)

1. 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. Circ Res. 1993;72:1293-1299.
2. 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.
3. 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.
4. Yang XM, Baxter GF, Heads RJ, Yellon DM, Downey JM, Cohen MV. Infarct limitation of the second window of protection in a conscious rabbit model. Cardiovasc Res. 1996;31:777-783.
5. Bolli R, Bhatti ZA, Tang XL, Qiu Y, Zhang Q, Guo Y, Jadoon AK. Evidence that late preconditioning against myocardial stunning in conscious rabbits is triggered by the generation of nitric oxide. Circ Res. 1997;81:42-52.
6. Qiu Y, Rizvi A, Tang XL, Machikalapudi S, Takano H, Jadoon AK, Wu WJ, Bolli R. Nitric oxide triggers late preconditioning against myocardial infarction in conscious rabbits. Am J Physiol. 1997;273:H2931-H2936.
7. Maldonado C, Qiu Y, Tang XL, 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.
8. Bolli R, Manchikalapudi S, Tang XL, Takano H, Qiu Y, Guo Y, Zhang Q, Jadoon AK. 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.
9. Baxter GF, Goma FM, Yellon DM. Characterization of the infarct-limiting effect of delayed preconditioning: timecourse and dose-dependency studies in rabbit myocardium. Basic Res Cardiol. 1997;92: 159-167.
10. Tang XL, Qiu Y, Park SW, Sun JZ, Kalya A, Bolli R. Time course of late preconditioning against myocardial stunning in conscious pigs. Circ Res. 1996;79:424-434.
11. Takano H, Manchikalapudi S, Tang XL, Qiu Y, Rizvi A, Jadoon AK, Zhang Q, Bolli R. Nitric oxide synthase is the mediator of late preconditioning against myocardial infarction in conscious rabbits. Circulation. 1998;98:441-449.
12. Marber MS, Yellon DM. Myocardial adaptation, stress proteins, and the second window of protection. Ann N Y Acad Sci. 1996;793:123-141.
13. Qiu Y, Ping P, Tang XL, Manchikalapudi S, Rizi A, Zhang J, Takano H, Wu WJ, Teschner S, Bolli R. Direct evidence that protein kinase C plays an essential role in the development of late preconditioning against myocardial stunning in conscious rabbits and that ∈ is the isoform involved. J Clin Invest. 1998;101:2182-2198.
14. Sun JZ, Tang XL, 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. 1996;97:562-576.
15. Tang XL, Rizvi A, Qiu Y, Takano H, Zhang Q, Guo Y, Bolli R. Evidence that the hydroxyl radical triggers late preconditioning against myocardial stunning in conscious rabbits. Circulation. 1997;96(suppl I):I-255. Abstract.
16. Baxter GF, Goma FM, Yellon DM. Involvement of protein kinase C in the delayed cytoprotection following sublethal ischaemia in rabbit myocardium. Br J Pharmacol. 1995;115:222-224.
17. Ping P, Zhang J, Qiu Y, Tang XL, Manchikalapudi S, Cao X, Bolli R. Ischemic preconditioning induces selective translocation of protein kinase C isoforms ∈ and η in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ Res. 1997;81: 404-414.
18. Ping P, Takano H, Zhang J, Tang XL, Qiu Y, Li RCX, Banerjee S, Dawn B, Balafonova Z, Bolli R. Isoform-selective activation of protein kinase C by nitric oxide in the heart of conscious rabbits: a signaling mechanism for both nitric oxide-induced and ischemia-induced preconditioning. Circ Res. 1999;84:587-604.
19. 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. 1997;29:1885-1893.
20. Dawn B, Qiu Y, Tang XL, Takano H, Banerjee S, Bolli R. Involvement of tyrosine kinases in the development of late preconditioning against myocardial stunning in conscious rabbits. J Mol Cell Cardiol. 1998; 30:A264. Abstract.
21. Ping P, Zhang J, Li RCX, Tang XL., Qiu Y, Banerjee S, Zheng YT, Bolli R. Ischemic preconditioning (PC) induces selective activation of Src and Lck tyrosine kinases in conscious rabbits via a PKC-dependent pathway. Circulation. 1998;98(suppl I):I-71. Abstract.
22. Rizvi A, Tang XL, Qiu Y, Xuan YT, Takano H, Jadoon AK, Bolli R. Increased protein synthesis is necessary for the development of late preconditioning against myocardial stunning in conscious rabbits. Am J Physiol. In press.
23. Thanos D, Maniatis T. NF-κB. A lesson in family values. Cell. 1995;80: 529-532.
24. Baeuerle PA, Henkel T. Function and activation of NF-κB in the immune system. Annu Rev Immunol. 1994;12:141-179.
25. Xie Q, Whisnant R, Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon γ and bacterial lipopolysaccharide. J Exp Med. 1993;177: 1779-1784.
26. Balligand JL, Ungureanu-Longrois D, Simmons WW, Pimental D, Malinski TA, Kapturczak M, Taha Z, Lowenstein CJ, Davidoff AJ, Kelly RA, Smith TW, Michel T. Cytokine-inducible nitric oxide synthase (iNOS) expression in cardiac myocytes. J Biol Chem. 1994;269: 27580-27588.
27. Gross SS, Wolin MS. Nitric oxide: pathophysiological mechanisms. Annu Rev Physiol. 1995;57:737-769.
28. Kelly RA, Balligand JL, Smith TW. Nitric oxide and cardiac function. Circ Res. 1996;79:363-380.
29. Takano H, Tang XL, Qiu Y, Guo Y, French BA, Bolli R. Nitric oxide donors induce late preconditioning against myocardial stunning and infarction in conscious rabbits via an antioxidant-sensitive mechanism. Circ Res. 1998;83:73-84.
30. Jugdutt BI. Different relations between infarct size and occluded bed size in barbiturate-anesthetized versus conscious dogs. J Am Coll Cardiol. 1985;6:1035-1046.
31. Triana JF, Li XY, Jamaluddin U, Thornby JI, Bolli R. Postischemic 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.
32. Li XY, 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.
33. Chien GL, Wolff RA, Davis RF, van Winkle DM. "Normothermic range" temperature affects myocardial infarct size. Cardiovasc Res. 1994;28: 1014-1017.
34. Bolli R. Common methodological problems and artifacts associated with studies of myocardial stunning in vivo. Basic Res Cardiol. 1995;90: 257-262.
35. Duncker DJ, Klassen CL, Ishibashi Y, Herrlinger SH, Pavek TJ, Bache RJ. Effect of temperature on myocardial infarction in swine. Am J Physiol. 1996;270:H1189-H1199.
36. Schwartz LM, Verbinski SG, Vander Heide RS, Reimer KA. Epicardial temperature is a major predictor of myocardial infarct size in dogs. J Mol Cell Cardiol. 1997;29:1577-1583.
37. Cohen MV, Yang XM, Downey JM. Conscious rabbits become tolerant to multiple episodes of ischemic preconditioning. Circ Res. 1994;74: 998-1004.
38. 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.
39. Burckhartt B, Yang XM, Tsuchida A, Mullane KM, Downey JM, Cohen MV. Acadesine extends the window of protection afforded by ischaemic preconditioning in conscious rabbits. Cardiovasc Res. 1995;29:653-657.
40. Schwartz 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. Bolli R, Zhu WX, Myers ML, Hartley CJ, Roberts R. β-Adrenergic stimulation reverses postischemic myocardial dysfunction without producing subsequent functional deterioration. Am J Cardiol. 1985;56: 964-968.
42. Garcia-Cardena G, Fan R, Stern DF, Liu J, Sessa WC. Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem. 1996;271:27237-27240.
43. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983;11:1475-1489.
44. Essani NA, McGuire GM, Manning AM, Jaeschke H. Endotoxin-induced activation of the nuclear transcription factor κB and expression of E-selectin messenger RNA in hepatocytes, Kupffer cells, and endothelial cells in vivo. J Immunol. 1996;156:2956-2963.
45. Wallenstein S, Zucker CL, Fleiss JL. Some statistical methods useful in circulation research. Circ Res. 1980;47:1-9.
46. Das DK, Maulik N, Moraru II. Gene expression in acute myocardial stress. Induction by hypoxia, ischemia, reperfusion, hyperthermia and oxidative stress. J Mol Cell Cardiol. 1995;27:181-193.
47. Schreck R, Meier B, Mannel DN, Droge W, Baeuerle PA. Dithiocarbamates as potent inhibitors of nuclear factor KB activation in intact cells. J Exp Med. 1992;175:1181-1194.
48. Ziegler-Heitbrock HWL, Sternsdorf T, Liese J, Belohradsky B, Weber C, Wedel A, Schreck R, Baeuerle PA, Strobel M. Pyrrolidine dithiocarbamate inhibits NF-κB mobilization and TNF production in human monocytes. J Immunol. 1993;151:6986-6993.
49. Sherman MP, Aeberhard EE, Wong VZ, Griscavage JM, Ignarro LJ. Pyrrolidine dithiocarbamate inhibits induction of nitric oxide synthase activity in rat alveolar macrophages. Biochem Biophys Res Commun. 1993;191:1301-1308.
50. Oddis CV, Finkel MS. NF-κB and GTP cyclohydrolase regulate cytokine-induced nitric oxide production by cardiac myocytes. Am J Physiol. 1996;270:H1864-H1868.
51. Hattori Y, Nakanishi N, Kasai K. Role of nuclear factor κB in cytokine-induced nitric oxide and tetrahydrobiopterin synthesis in rat neonatal cardiac myocytes. J Mol Cell Cardiol. 1997;29:1585-1592.
52. Zeiher AM, Fisslthaler B, Schray-Utz B, Busse R. Nitric oxide modulates the expression of monocyte chemoattractant protein 1 in cultured human endothelial cells. Circ Res. 1995;76:980-986.
53. Peng HB, Libby P, Liao JK. Induction and stabilization of IκBα by nitric oxide mediates inhibition of NF-κB. J Biol Chem. 1995;270: 14214-14219.
54. Matthews JR, Botting CH, Panico M, Morris HR, Hay RT. Inhibition of NF-κB DNA binding by nitric oxide. Nucleic Acids Res. 1996;24: 2236-2242.
55. ras. J Biol Chem. 1995;270:7017-7020.
56. Umansky V, Hehner SP, Dumont A, Hofmann TG, Schirrmacher V, Droge W, Schmitz ML. Co-stimulalory effect of nitric oxide on endothelial NF-κB implies a physiological self-amplifying mechanism. Eur J Immunol. 1998;28:2276-2282.
57. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A. 1990;87:1620-1624.
58. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem. 1991;266:4244-4250.
59. Herbert JM, Augereau JM, Gleye J, Maffrand JP. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun. 1990;172:993-999.
60. Onoda T, Iinuma H, Sasaki Y, Hamada M, Isshiki K, Naganawa H, Takeuchi T, Tatsuta K, Umezawa K. Isolation of a novel tyrosine kinase inhibitor, lavendustin A, from Streptomyces griseolavendus. J Nat Prod. 1989;52:1252-1257.
61. O'Dell TJ, Kandel ER, Grant SG. Long-term potentiation in the hippocampus is blocked by tyrosine kinase inhibitors. Nature. 1991;353: 558-560.
62. 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. 1998;30:383-392.
63. Chandrasekar B, Freeman GL. Induction of nuclear factor κB and activation protein 1 in postischemic myocardium. FEBS Letters. 1997;401: 30-34.
64. Chandrasekar B, Streitman JE, Colston JT, Freeman GL. Inhibition of nuclear factor κB attenuates proinflammatory cytokine and inducible nitric-oxide synthase expression in postischemic myocardium. Biochim Biophys Acta. 1998;1406:91-106.
65. Maulik N, Sato M, Price BD, Das DK. An essential role of NFκB in tyrosine kinase signaling of p38 MAP kinase regulation of myocardial adaptation to ischemia. FEBS Lett. 1998;429:365-369.