Melatonin reduces PERK-eIF2α-ATF4-mediated endoplasmic reticulum stress during myocardial ischemia–reperfusion injury: role of RISK and SAFE pathways interaction

Apoptosis

Volumn 21, Issue 7, 2016, Pages 809-824

  Yu, Liming ^a   Li, Buying ^a   Zhang, Meng ^b   Jin, Zhenxiao ^a   Duan, Weixun ^a   Zhao, Guolong ^c   Yang, Yang ^b   Liu, Zhenhua ^a   Chen, Wensheng ^a   Wang, Siwang ^b   Yang, Jian ^a   Yi, Dinghua ^a   Liu, Jincheng ^a   Yu, Shiqiang ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c NINGXIA MEDICAL UNIVERSITY   (China)

Author keywords

Endoplasmic reticulum stress; Melatonin; Myocardial ischemia reperfusion injury; Reperfusion injury salvage kinase pathway; Survivor activating factor enhancement pathway

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; ACTIVATING TRANSCRIPTION FACTOR 4; CASPASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; INITIATION FACTOR 2ALPHA; MELATONIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PROTEIN; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN KINASE RNA LIKE ER KINASE; STAT3 PROTEIN; SUPEROXIDE; UNCLASSIFIED DRUG; GLYCOGEN SYNTHASE KINASE 3; INITIATION FACTOR 2; PERK KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE R;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; HEART FUNCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE ISCHEMIA; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TREATMENT DURATION; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; PHOSPHORYLATION;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; MELATONIN; MICE, INBRED C57BL; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84966694390     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-016-1246-1     Document Type: Article

References (56)

1. Forouzanfar MH, Moran AE, Flaxman AD, Roth G, Mensah GA, Ezzati M, Naghavi M, Murray CJ (2012) Assessing the global burden of ischemic heart disease, part 2: analytic methods and estimates of the global epidemiology of ischemic heart disease in 2010. Glob Heart 7(4):331–342. doi:10.1016/j.gheart.2012.10.003
2. Moran AE, Oliver JT, Mirzaie M, Forouzanfar MH, Chilov M, Anderson L, Morrison JL, Khan A, Zhang N, Haynes N, Tran J, Murphy A, Degennaro V, Roth G, Zhao D, Peer N, Pichon-Riviere A, Rubinstein A, Pogosova N, Prabhakaran D, Naghavi M, Ezzati M, Mensah GA (2012) Assessing the global burden of ischemic heart disease: part 1: methods for a systematic review of the global epidemiology of ischemic heart disease in 1990 and 2010. Glob Heart 7(4):315–329. doi:10.1016/j.gheart.2012.10.004
3. Piper HM, Garcia-Dorado D, Ovize M (1998) A fresh look at reperfusion injury. Cardiovasc Res 38(2):291–300
4. Yellon DM, Hausenloy DJ (2007) Myocardial reperfusion injury. N Engl J Med 357(11):1121–1135. doi:10.1056/NEJMra071667
5. Cominacini L, Mozzini C, Garbin U, Pasini A, Stranieri C, Solani E, Vallerio P, Tinelli IA, Fratta Pasini A (2015) Endoplasmic reticulum stress and Nrf2 signaling in cardiovascular diseases. Free Radic Biol Med 88(Pt B):233–242. doi:10.1016/j.freeradbiomed.2015.05.027
6. Glembotski CC (2014) Roles for ATF6 and the sarco/endoplasmic reticulum protein quality control system in the heart. J Mol Cell Cardiol 71:11–15. doi:10.1016/j.yjmcc.2013.09.018
7. Lai E, Teodoro T, Volchuk A (2007) Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda) 22:193–201. doi:10.1152/physiol.00050.2006
8. Wang Y, Zong L, Wang X (2016) TGF-beta improves myocardial function and prevents apoptosis induced by anoxia-reoxygenation, through the reduction of endoplasmic reticulum stress. Can J Physiol Pharmacol 94(1):9–17. doi:10.1139/cjpp-2014-0466
9. Wei K, Liu L, Xie F, Hao X, Luo J, Min S (2015) Nerve growth factor protects the ischemic heart via attenuation of the endoplasmic reticulum stress induced apoptosis by activation of phosphatidylinositol 3-kinase. Int J Med Sci 12(1):83–91. doi:10.7150/ijms.10101
10. Wu H, Ye M, Yang J, Ding J, Dong W, Wang X (2015) Nicorandil protects the heart from ischemia/reperfusion injury by attenuating endoplasmic reticulum response-induced apoptosis through PI3K/Akt signaling pathway. Cell Physiol Biochem 35(6):2320–2332. doi:10.1159/000374035
11. Xu J, Hu H, Chen B, Yue R, Zhou Z, Liu Y, Zhang S, Xu L, Wang H, Yu Z (2015) Lycopene protects against hypoxia/reoxygenation injury by alleviating ER stress induced apoptosis in neonatal mouse cardiomyocytes. PLoS ONE 10(8):e0136443. doi:10.1371/journal.pone.0136443
12. Yu L, Liang H, Dong X, Zhao G, Jin Z, Zhai M, Yang Y, Chen W, Liu J, Yi W, Yang J, Yi D, Duan W, Yu S (2015) Reduced silent information regulator 1 signaling exacerbates myocardial ischemia–reperfusion injury in type 2 diabetic rats and the protective effect of melatonin. J Pineal Res 59(3):376–390. doi:10.1111/jpi.12269
13. Yang Y, Duan W, Jin Z, Yi W, Yan J, Zhang S, Wang N, Liang Z, Li Y, Chen W, Yi D, Yu S (2013) JAK2/STAT3 activation by melatonin attenuates the mitochondrial oxidative damage induced by myocardial ischemia/reperfusion injury. J Pineal Res 55(3):275–286. doi:10.1111/jpi.12070
14. Yu L, Liang H, Lu Z, Zhao G, Zhai M, Yang Y, Yang J, Yi D, Chen W, Wang X, Duan W, Jin Z, Yu S (2015) Membrane receptor-dependent Notch1/Hes1 activation by melatonin protects against myocardial ischemia–reperfusion injury: in vivo and in vitro studies. J Pineal Res 59(4):420–433. doi:10.1111/jpi.12272
15. Yu L, Sun Y, Cheng L, Jin Z, Yang Y, Zhai M, Pei H, Wang X, Zhang H, Meng Q, Zhang Y, Yu S, Duan W (2014) Melatonin receptor-mediated protection against myocardial ischemia/reperfusion injury: role of SIRT1. J Pineal Res 57(2):228–238. doi:10.1111/jpi.12161
16. Reiter RJ, Tan DX (2003) Melatonin: a novel protective agent against oxidative injury of the ischemic/reperfused heart. Cardiovasc Res 58(1):10–19
17. Tengattini S, Reiter RJ, Tan DX, Terron MP, Rodella LF, Rezzani R (2008) Cardiovascular diseases: protective effects of melatonin. J Pineal Res 44(1):16–25. doi:10.1111/j.1600-079X.2007.00518.x
18. Moreira AJ, Ordonez R, Cerski CT, Picada JN, Garcia-Palomo A, Marroni NP, Mauriz JL, Gonzalez-Gallego J (2015) Melatonin activates endoplasmic reticulum stress and apoptosis in rats with diethylnitrosamine-induced hepatocarcinogenesis. PLoS ONE 10(12):e0144517. doi:10.1371/journal.pone.0144517
19. Wu SM, Lin WY, Shen CC, Pan HC, Keh-Bin W, Chen YC, Jan YJ, Lai DW, Tang SC, Tien HR, Chiu CS, Tsai TC, Lai YL, Sheu ML (2015) Melatonin set out to ER stress signaling thwarts epithelial mesenchymal transition and peritoneal dissemination via Calpain-mediated C/EBPbeta and NFkappaB cleavage. J Pineal Res. doi:10.1111/jpi.12295
20. Fernandez A, Ordonez R, Reiter RJ, Gonzalez-Gallego J, Mauriz JL (2015) Melatonin and endoplasmic reticulum stress: relation to autophagy and apoptosis. J Pineal Res 59(3):292–307. doi:10.1111/jpi.12264
21. Pagliaro P, Penna C (2011) Cardiac postconditioning. Antioxid Redox Signal 14(5):777–779. doi:10.1089/ars.2010.3531
22. Hausenloy DJ, Lecour S, Yellon DM (2011) Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischemic postconditioning: two sides of the same coin. Antioxid Redox Signal 14(5):893–907. doi:10.1089/ars.2010.3360
23. Suleman N, Somers S, Smith R, Opie LH, Lecour SC (2008) Dual activation of STAT-3 and Akt is required during the trigger phase of ischaemic preconditioning. Cardiovasc Res 79(1):127–133. doi:10.1093/cvr/cvn067
24. Frias MA, Rebsamen MC, Gerber-Wicht C, Lang U (2007) Prostaglandin E2 activates Stat3 in neonatal rat ventricular cardiomyocytes: a role in cardiac hypertrophy. Cardiovasc Res 73(1):57–65. doi:10.1016/j.cardiores.2006.09.016
25. Nduhirabandi F, Huisamen B, Strijdom H, Blackhurst D, Lochner A (2014) Short-term melatonin consumption protects the heart of obese rats independent of body weight change and visceral adiposity. J Pineal Res 57(3):317–332. doi:10.1111/jpi.12171
26. Liu RR, Li J, Gong JY, Kuang F, Liu JY, Zhang YS, Ma QL, Song CJ, Truax AD, Gao F, Yang K, Jin BQ, Chen LH (2015) MicroRNA-141 regulates the expression level of ICAM-1 on endothelium to decrease myocardial ischemia–reperfusion injury. Am J Physiol Heart Circ Physiol 309(8):H1303–1313. doi:10.1152/ajpheart.00290.2015
27. Wolfrum S, Dendorfer A, Rikitake Y, Stalker TJ, Gong Y, Scalia R, Dominiak P, Liao JK (2004) Inhibition of Rho-kinase leads to rapid activation of phosphatidylinositol 3-kinase/protein kinase Akt and cardiovascular protection. Arterioscler Thromb Vasc Biol 24(10):1842–1847. doi:10.1161/01.atv.0000142813.33538.82
28. Montecucco F, Lenglet S, Braunersreuther V, Burger F, Pelli G, Bertolotto M, Mach F, Steffens S (2009) CB(2) cannabinoid receptor activation is cardioprotective in a mouse model of ischemia/reperfusion. J Mol Cell Cardiol 46(5):612–620. doi:10.1016/j.yjmcc.2008.12.014
29. Zhang X, Gao M, Ha T, Kalbfleisch JH, Williams DL, Li C, Kao RL (2012) The toll-like receptor 9 agonist, CpG-oligodeoxynucleotide 1826, ameliorates cardiac dysfunction after trauma-hemorrhage. Shock 38(2):146–152. doi:10.1097/SHK.0b013e31825ce0de
30. Yu L, Li Q, Yu B, Yang Y, Jin Z, Duan W, Zhao G, Zhai M, Liu L, Yi D, Chen M, Yu S (2016) Berberine attenuates myocardial ischemia/reperfusion injury by reducing oxidative stress and inflammation response: role of silent information regulator 1. Oxid Med Cell Longev 2016:1689602. doi:10.1155/2016/1689602
31. Yu L, Li F, Zhao G, Yang Y, Jin Z, Zhai M, Yu W, Zhao L, Chen W, Duan W, Yu S (2015) Protective effect of berberine against myocardial ischemia reperfusion injury: role of Notch1/Hes1-PTEN/Akt signaling. Apoptosis 20(6):796–810. doi:10.1007/s10495-015-1122-4
32. Han CK, Kuo WW, Shen CY, Chen TS, Pai P, Tsai CH, Lo FY, Ju DT, Huang CY (2014) Dilong prevents the high-KCl cardioplegic solution administration-induced apoptosis in H9c2 cardiomyoblast cells mediated by MEK. Am J Chin Med 42(6):1507–1519. doi:10.1142/s0192415x14500943
33. Kim DE, Kim B, Shin HS, Kwon HJ, Park ES (2014) The protective effect of hispidin against hydrogen peroxide-induced apoptosis in H9c2 cardiomyoblast cells through Akt/GSK-3beta and ERK1/2 signaling pathway. Exp Cell Res 327(2):264–275. doi:10.1016/j.yexcr.2014.07.037
34. Liao W, Yu C, Wen J, Jia W, Li G, Ke Y, Zhao S, Campell W (2009) Adiponectin induces interleukin-6 production and activates STAT3 in adult mouse cardiac fibroblasts. Biol Cell 101(5):263–272. doi:10.1042/bc20080117
35. Xue R, Lei S, Xia ZY, Wu Y, Meng Q, Zhan L, Su W, Liu H, Xu J, Liu Z, Zhou B, Xia Z (2015) Selective inhibition of PTEN preserves ischemic postconditioning cardioprotection in STZ-induced Type 1 diabetic rats: role of the PI3K/Akt and JAK2/STAT3 pathways. Clin Sci (Lond). doi:10.1042/cs20150496
36. Liu XH, Zhang ZY, Sun S, Wu XD (2008) Ischemic postconditioning protects myocardium from ischemia/reperfusion injury through attenuating endoplasmic reticulum stress. Shock 30(4):422–427. doi:10.1097/SHK.0b013e318164ca29
37. Zhang GG, Teng X, Liu Y, Cai Y, Zhou YB, Duan XH, Song JQ, Shi Y, Tang CS, Yin XH, Qi YF (2009) Inhibition of endoplasm reticulum stress by ghrelin protects against ischemia/reperfusion injury in rat heart. Peptides 30(6):1109–1116. doi:10.1016/j.peptides.2009.03.024
38. Guo XF, Yang XJ (2015) Endoplasmic reticulum stress response in spontaneously hypertensive rats is affected by myocardial ischemia reperfusion injury. Exp Ther Med 9(2):319–326. doi:10.3892/etm.2014.2094
39. Tabas I, Ron D (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13(3):184–190. doi:10.1038/ncb0311-184
40. Fu HY, Okada K, Liao Y, Tsukamoto O, Isomura T, Asai M, Sawada T, Okuda K, Asano Y, Sanada S, Asanuma H, Asakura M, Takashima S, Komuro I, Kitakaze M, Minamino T (2010) Ablation of C/EBP homologous protein attenuates endoplasmic reticulum-mediated apoptosis and cardiac dysfunction induced by pressure overload. Circulation 122(4):361–369. doi:10.1161/circulationaha.109.917914
41. Zhang HM, Zhang Y (2014) Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. J Pineal Res 57(2):131–146. doi:10.1111/jpi.12162
42. Galano A, Tan DX, Reiter RJ (2013) On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK. J Pineal Res 54(3):245–257. doi:10.1111/jpi.12010
43. Wang H, Li L, Zhao M, Chen YH, Zhang ZH, Zhang C, Ji YL, Meng XH, Xu DX (2011) Melatonin alleviates lipopolysaccharide-induced placental cellular stress response in mice. J Pineal Res 50(4):418–426. doi:10.1111/j.1600-079X.2011.00860.x
44. Lin AM, Fang SF, Chao PL, Yang CH (2007) Melatonin attenuates arsenite-induced apoptosis in rat brain: involvement of mitochondrial and endoplasmic reticulum pathways and aggregation of alpha-synuclein. J Pineal Res 43(2):163–171. doi:10.1111/j.1600-079X.2007.00456.x
45. Lin AM, Feng SF, Chao PL, Yang CH (2009) Melatonin inhibits arsenite-induced peripheral neurotoxicity. J Pineal Res 46(1):64–70. doi:10.1111/j.1600-079X.2008.00629.x
46. Ji YL, Wang H, Meng C, Zhao XF, Zhang C, Zhang Y, Zhao M, Chen YH, Meng XH, Xu DX (2012) Melatonin alleviates cadmium-induced cellular stress and germ cell apoptosis in testes. J Pineal Res 52(1):71–79. doi:10.1111/j.1600-079X.2011.00921.x
47. Zhao H, Wu QQ, Cao LF, Qing HY, Zhang C, Chen YH, Wang H, Liu RY, Xu DX (2014) Melatonin inhibits endoplasmic reticulum stress and epithelial-mesenchymal transition during bleomycin-induced pulmonary fibrosis in mice. PLoS ONE 9(5):e97266. doi:10.1371/journal.pone.0097266
48. Nduhirabandi F, Du Toit EF, Blackhurst D, Marais D, Lochner A (2011) Chronic melatonin consumption prevents obesity-related metabolic abnormalities and protects the heart against myocardial ischemia and reperfusion injury in a prediabetic model of diet-induced obesity. J Pineal Res 50(2):171–182. doi:10.1111/j.1600-079X.2010.00826.x
49. Wang M, Meng XB, Yu YL, Sun GB, Xu XD, Zhang XP, Dong X, Ye JX, Xu HB, Sun YF, Sun XB (2014) Elatoside C protects against hypoxia/reoxygenation-induced apoptosis in H9c2 cardiomyocytes through the reduction of endoplasmic reticulum stress partially depending on STAT3 activation. Apoptosis 19(12):1727–1735. doi:10.1007/s10495-014-1039-3
50. Wang Z, Wang Y, Ye J, Lu X, Cheng Y, Xiang L, Chen L, Feng W, Shi H, Yu X, Lin L, Zhang H, Xiao J, Li X (2015) bFGF attenuates endoplasmic reticulum stress and mitochondrial injury on myocardial ischaemia/reperfusion via activation of PI3K/Akt/ERK1/2 pathway. J Cell Mol Med 19(3):595–607. doi:10.1111/jcmm.12346
51. Goodman MD, Koch SE, Fuller-Bicer GA, Butler KL (2008) Regulating RISK: A role for JAK-STAT signaling in postconditioning? Am J Physiol Heart Circ Physiol 295(4):H1649–1656. doi:10.1152/ajpheart.00692.2008
52. Cao SS, Kaufman RJ (2014) Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal 21(3):396–413. doi:10.1089/ars.2014.5851
53. Ding W, Yang L, Zhang M, Gu Y (2012) Reactive oxygen species-mediated endoplasmic reticulum stress contributes to aldosterone-induced apoptosis in tubular epithelial cells. Biochem Biophys Res Commun 418(3):451–456. doi:10.1016/j.bbrc.2012.01.037
54. Shi Z, Fu F, Yu L, Xing W, Su F, Liang X, Tie R, Ji L, Zhu M, Yu J, Zhang H (2015) Vasonatrin peptide attenuates myocardial ischemia–reperfusion injury in diabetic rats and underlying mechanisms. Am J Physiol Heart Circ Physiol 308(4):H281–290. doi:10.1152/ajpheart.00666.2014
55. Lau WW, Ng JK, Lee MM, Chan AS, Wong YH (2012) Interleukin-6 autocrine signaling mediates melatonin MT(1/2) receptor-induced STAT3 Tyr(705) phosphorylation. J Pineal Res 52(4):477–489. doi:10.1111/j.1600-079X.2011.00965.x
56. Wang Z, Liu D, Wang J, Liu S, Gao M, Ling EA, Hao A (2012) Cytoprotective effects of melatonin on astroglial cells subjected to palmitic acid treatment in vitro. J Pineal Res 52(2):253–264. doi:10.1111/j.1600-079X.2011.00952.x