Nicorandil protects the heart from ischemia/reperfusion injury by attenuating endoplasmic reticulum response-induced apoptosis through PI3K/Akt signaling pathway

Cellular Physiology and Biochemistry

Volumn 35, Issue 6, 2015, Pages 2320-2332

  Wu, Hui ^a   Ye, Ming ^a   Yang, Jun ^a   Ding, Jiawang ^b   Yang, Jian ^b   Dong, Wusong ^b   Wang, Xinan ^b  

^a CHINA THREE GORGES UNIVERSITY   (China)

^b Department of General Surgery Yichang Central People s Hospital   (China)

Author keywords

Apoptosis; Endoplasmic Reticulum; Heart; Ischemia Reperfusion; Nicorandil; PI3K Akt

Indexed keywords

LACTATE DEHYDROGENASE; NICORANDIL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TUNICAMYCIN; WORTMANNIN; PROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; DOSE RESPONSE; DRUG EFFECT; ENDOPLASMIC RETICULUM STRESS; ENZYME RELEASE; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FUNCTION; HEART PROTECTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; ANIMAL; DRUG EFFECTS; ENDOPLASMIC RETICULUM; HEART; ISCHEMIC POSTCONDITIONING; METABOLISM; MYOCARDIAL INFARCTION; MYOCARDIAL ISCHEMIA; PROCEDURES; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HEART; ISCHEMIC POSTCONDITIONING; MALE; MYOCARDIAL INFARCTION; MYOCARDIAL ISCHEMIA; NICORANDIL; PHOSPHATIDYLINOSITOL 3-KINASES; PROTECTIVE AGENTS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

EID: 84928155276     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000374035     Document Type: Article

References (45)

1. Kalogeris T, Baines CP, Krenz M, Korthuis RJ: Cell biology of ischemia/reperfusion injury. Int Rev Cell Mol Biol 2012;298:229-317.
2. Eltzschig HK, Eckle T: Ischemia and reperfusion-from mechanism to translation. Nat Med 2011;17:1391-1401.
3. Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, Zheng ZJ, Flegal K, O'Donnell C, Kittner S, Lloyd-Jones D, Goff DC Jr, Hong Y, Adams R, Friday G, Furie K, Gorelick P, Kissela B, Marler J, Meigs J, Roger V, Sidney S, Sorlie P, Steinberger J, Wasserthiel-Smoller S, Wilson M, Wolf P, American Heart Association Statistics C, Stroke Statistics S: Heart disease and stroke statistics-2006 update: A report from the american heart association statistics committee and stroke statistics subcommittee. Circulation 2006;113:e85-151.
4. Schroder M, Kaufman RJ: Er stress and the unfolded protein response. Mutat Res 2005;569:29-63.
5. Xu C, Bailly-Maitre B, Reed JC: Endoplasmic reticulum stress: Cell life and death decisions. J Clin Invest 2005;115:2656-2664.
6. Hammadi M, Oulidi A, Gackiere F, Katsogiannou M, Slomianny C, Roudbaraki M, Dewailly E, Delcourt P, Lepage G, Lotteau S, Ducreux S, Prevarskaya N, Van Coppenolle F: Modulation of er stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: Involvement of grp78. FASEB J 2013;27:1600-1609.
7. Li N, Zoubeidi A, Beraldi E, Gleave ME: Grp78 regulates clusterin stability, retrotranslocation and mitochondrial localization under er stress in prostate cancer. Oncogene 2013;32:1933-1942.
8. Liu G, Shang Y, Yu Y: Induced endoplasmic reticulum (er) stress and binding of over-expressed er specific chaperone grp78/bip with dimerized epidermal growth factor receptor in mammalian cells exposed to low concentration of n-methyl-n'-nitro-n-nitrosoguanidine. Mutat Res 2006;596:12-21.
9. Lee AS: The er chaperone and signaling regulator grp78/bip as a monitor of endoplasmic reticulum stress. Methods 2005;35:373-381.
10. Rao RV, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T, Goldsmith PC, Ellerby LM, Ellerby HM, Bredesen DE: Coupling endoplasmic reticulum stress to the cell death program: Role of the er chaperone grp78. FEBS Lett 2002;514:122-128.
11. Martindale JJ, Fernandez R, Thuerauf D, Whittaker R, Gude N, Sussman MA, Glembotski CC: Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of atf6. Circ Res 2006;98:1186-1193.
12. Liu XH, Zhang ZY, Sun S, Wu XD: Ischemic postconditioning protects myocardium from ischemia/ reperfusion injury through attenuating endoplasmic reticulum stress. Shock 2008;30:422-427.
13. Vitadello M, Penzo D, Petronilli V, Michieli G, Gomirato S, Menabo R, Di Lisa F, Gorza L: Overexpression of the stress protein grp94 reduces cardiomyocyte necrosis due to calcium overload and simulated ischemia. FASEB J 2003;17:923-925.
14. Okada K, Minamino T, Tsukamoto Y, Liao Y, Tsukamoto O, Takashima S, Hirata A, Fujita M, Nagamachi Y, Nakatani T, Yutani C, Ozawa K, Ogawa S, Tomoike H, Hori M, Kitakaze M: Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: Possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 2004;110:705-712.
15. Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC: Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003;22:8608-8618.
16. Glembotski CC: Endoplasmic reticulum stress in the heart. Circ Res 2007;101:975-984.
17. Rao J, Yue S, Fu Y, Zhu J, Wang X, Busuttil RW, Kupiec-Weglinski JW, Lu L, Zhai Y: Atf6 mediates a proinflammatory synergy between er stress and tlr activation in the pathogenesis of liver ischemia-reperfusion injury. Am J Transplant 2014;14:1552-1561.
18. Vekich JA, Belmont PJ, Thuerauf DJ, Glembotski CC: Protein disulfide isomerase-associated 6 is an atf6-inducible er stress response protein that protects cardiac myocytes from ischemia/reperfusion-mediated cell death. J Mol Cell Cardiol 2012;53:259-267.
19. Szegezdi E, Duffy A, O'Mahoney ME, Logue SE, Mylotte LA, O'Brien T, Samali A: Er stress contributes to ischemia-induced cardiomyocyte apoptosis. Biochem Biophys Res Commun 2006;349:1406-1411.
20. Ron D, Walter P: Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529.
21. Miyazaki Y, Kaikita K, Endo M, Horio E, Miura M, Tsujita K, Hokimoto S, Yamamuro M, Iwawaki T, Gotoh T, Ogawa H, Oike Y: C/ebp homologous protein deficiency attenuates myocardial reperfusion injury by inhibiting myocardial apoptosis and inflammation. Arterioscler Thromb Vasc Biol 2011;31:1124-1132.
22. Groenendyk J, Sreenivasaiah PK, Kim do H, Agellon LB, Michalak M: Biology of endoplasmic reticulum stress in the heart. Circ Res 2010;107:1185-1197.
23. Frampton J, Buckley MM, Fitton A: Nicorandil. A review of its pharmacology and therapeutic efficacy in angina pectoris. Drugs 1992;44:625-655.
24. Kitakaze M, Asakura M, Kim J, Shintani Y, Asanuma H, Hamasaki T, Seguchi O, Myoishi M, Minamino T, Ohara T, Nagai Y, Nanto S, Watanabe K, Fukuzawa S, Hirayama A, Nakamura N, Kimura K, Fujii K, Ishihara M, Saito Y, Tomoike H, Kitamura S, investigators JW: Human atrial natriuretic peptide and nicorandil as adjuncts to reperfusion treatment for acute myocardial infarction (j-wind): Two randomised trials. Lancet 2007;370:1483-1493.
25. Ishii H, Ichimiya S, Kanashiro M, Amano T, Imai K, Murohara T, Matsubara T: Impact of a single intravenous administration of nicorandil before reperfusion in patients with st-segment-elevation myocardial infarction. Circulation 2005;112:1284-1288.
26. Akao M, Teshima Y, Marban E: Antiapoptotic effect of nicorandil mediated by mitochondrial atp-sensitive potassium channels in cultured cardiac myocytes. J Am Coll Cardiol 2002;40:803-810.
27. Schalla S, Higgins CB, Chujo M, Saeed M: Effect of potassium-channel opener therapy on reperfused infarction in hypertrophied hearts: Demonstration of preconditioning by using functional and contrastenhanced magnetic resonance imaging. J Cardiovasc Pharmacol Ther 2004;9:193-202.
28. Lindy S, Turto H, Uitto J, Helin P, Lorenzen I: Injury and repair in arterial tissue in the rabbit. Analysis of DNA, rna, hydroxyproline, and lactate dehydrogenase in experimental arteriosclerosis. Circ Res 1972;30:123-130.
29. Lee Y, Gustafsson AB: Role of apoptosis in cardiovascular disease. Apoptosis 2009;14:536-548.
30. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ: Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001;21:1249-1259.
31. Kroemer G, Galluzzi L, Brenner C: Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007;87:99-163.
32. Song G, Ouyang G, Bao S: The activation of akt/pkb signaling pathway and cell survival. J Cell Mol Med 2005;9:59-71.
33. Hyoda K, Hosoi T, Horie N, Okuma Y, Ozawa K, Nomura Y: Pi3k-akt inactivation induced chop expression in endoplasmic reticulum-stressed cells. Biochem Biophys Res Commun 2006;340:286-290.
34. Tang XL, Xuan YT, Zhu Y, Shirk G, Bolli R: Nicorandil induces late preconditioning against myocardial infarction in conscious rabbits. Am J Physiol Heart Circ Physiol 2004;286:H1273-1280.
35. Minamino T, Kitakaze M: Er stress in cardiovascular disease. J Mol Cell Cardiol 2010;48:1105-1110.
36. Thuerauf DJ, Marcinko M, Gude N, Rubio M, Sussman MA, Glembotski CC: Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res 2006;99:275-282.
37. Tsuchida A, Miura T, Tanno M, Sakamoto J, Miki T, Kuno A, Matsumoto T, Ohnuma Y, Ichikawa Y, Shimamoto K: Infarct size limitation by nicorandil: Roles of mitochondrial k(atp) channels, sarcolemmal k(atp) channels, and protein kinase c. J Am Coll Cardio 2002;40:1523-1530.
38. Mizumura T, Nithipatikom K, Gross GJ: Infarct size-reducing effect of nicorandil is mediated by the katp channel but not by its nitrate-like properties in dogs. Cardiovasc Res 1996;32:274-285.
39. Zhang H, Song LC, Jia CH, Lu YL: Effects of atp sensitive potassium channel opener on the mrna and protein expressions of caspase-12 after cerebral ischemia-reperfusion in rats. Neurosci Bull 2008;24:7-12.
40. Izumiya Y, Kojima S, Kojima S, Araki S, Usuku H, Matsubara J, Sakamoto K, Tsujita K, Nagayoshi Y, Kaikita K, Sugiyama S, Ogawa H: Long-term use of oral nicorandil stabilizes coronary plaque in patients with stable angina pectoris. Atherosclerosis 2011;214:415-421.
41. Schönthal AH: Endoplasmic reticulum stress: its role in disease and novel prospects for therapy. Scientifica 2012;2012:857516-857542.
42. Wolfrum S, Dendorfer A, Rikitake Y, Stalker TJ, Gong Y, Scalia R, Dominiak P, Liao JK: Inhibition of rho-kinase leads to rapid activation of phosphatidylinositol 3-kinase/protein kinase akt and cardiovascular protection. Arterioscler Thromb Vasc Biol 2004;24:1842-1847.
43. Bao W, Hu E, Tao L, Boyce R, Mirabile R, Thudium DT, Ma XL, Willette RN, Yue TL: Inhibition of rho-kinase protects the heart against ischemia/reperfusion injury. Cardiovasc Res 2004;61:548-558.
44. Hu P, Han Z, Couvillon AD, Exton JH: Critical role of endogenous akt/iaps and mek1/erk pathways in counteracting endoplasmic reticulum stress-induced cell death. J Biol Chem 2004;279:49420-49429.
45. Lecour S: Activation of the protective survivor activating factor enhancement (safe) pathway against reperfusion injury: Does it go beyond the risk pathway? J Mol Cell Cardiol 2009;47:32-40.