Acetylcholine ameliorates endoplasmic reticulum stress in endothelial cells after hypoxia/ reoxygenation via M3 AChR-AMPK signaling

Cell Cycle

Volumn 14, Issue 15, 2015, Pages 2461-2472

  Bi, Xueyuan ^a   He, Xi ^a   Xu, Man ^a   Zhao, Ming ^a   Yu, Xiaojiang ^a   Lu, Xingzhu ^a   Zang, Weijin ^a  

^a MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Acetylcholine; AMPK; Apoptosis; Endoplasmic reticulum stress; Endothelial cells; Ischemia reperfusion injury; M3 AChR

Indexed keywords

4 DIPHENYLACETOXY 1 METHYLPIPERIDINE; ACETYLCHOLINE; CASPASE 12; DNA NUCLEOTIDYLEXOTRANSFERASE; GLUCOSE REGULATED PROTEIN 78; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MUSCARINIC M3 RECEPTOR; PROTEIN KINASE; 4-DIPHENYLACETOXY-1,1-DIMETHYLPIPERIDINIUM; CASP12 PROTEIN, HUMAN; ERN1 PROTEIN, HUMAN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78; PIPERIDINE DERIVATIVE; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; REOXYGENATION; SIGNAL TRANSDUCTION; TUNEL ASSAY; ULTRASTRUCTURE; ANTAGONISTS AND INHIBITORS; CELL LINE; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; REPERFUSION INJURY; RNA INTERFERENCE; UMBILICAL VEIN ENDOTHELIAL CELL;

ACETYLCHOLINE; AMP-ACTIVATED PROTEIN KINASES; APOPTOSIS; CASPASE 12; CELL HYPOXIA; CELL LINE; DNA NUCLEOTIDYLEXOTRANSFERASE; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; HEAT-SHOCK PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; PIPERIDINES; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, MUSCARINIC M3; REPERFUSION INJURY; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP;

EID: 84943748294     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.1080/15384101.2015.1060383     Document Type: Article

References (52)

1. Kalogeris T, Baines CP, Krenz M, Korthuis RJ. Cell biology of ischemia/reperfusion injury. Int Rev Cell Mol Biol 2012; 298: 229-317; PMID: 22878108; http://dx. doi. org/10. 1016/B978-0-12-394309-5. 00006-7.
2. Bi XY, He X, Zhao M, Yu XJ, Zang WJ. Role of endothelial nitric oxide synthase and vagal activity in the endothelial protection of atorvastatin in ischemia/reperfusion injury. J Cardiovasc Pharmacol 2013; 61: 391-400; PMID: 23364605; http://dx. doi. org/10. 1097/FJC. 0b013e318286baf3.
3. Xie P, Duan Y, Guo X, Hu L, Yu M. SalA attenuates hypoxia-induced endothelial endoplasmic reticulum stress and apoptosis via down-regulation of VLDL receptor expression. Cell Physiol Biochem 2015; 35: 17-28; PMID: 25547648; http://dx. doi. org/10. 1159/000369671.
4. Wang J, Chen S, Ma X, Cheng C, Xiao X, Chen J, Liu S, Zhao B, Chen Y. Effects of endothelial progenitor cellderived microvesicles on hypoxia/reoxygenation-induced endothelial dysfunction and apoptosis. OxidMed Cell Longev 2013; 2013: 572729; PMID: 24288585; http://dx. doi. org/10. 1155/2013/572729.
5. Vemula P, Gautam B, Abela GS, Wang DH. Myocardial ischemia/reperfusion injury: potential of TRPV1 agonists as cardioprotective agents. Cardiovasc Hematol Disord Drug Targets 2014; 14: 71-8; PMID: 24304232; http://dx. doi. org/10. 2174/1871529_13666131129103759.
6. Turer AT, Hill JA. Pathogenesis of myocardial ischemia-reperfusion injury and rationale for therapy. Am J Cardiol 2010; 106: 360-8; PMID: 20643246; http://dx. doi. org/10. 1016/j. amjcard. 2010. 03. 032.
7. Liu XH, Zhang ZY, Sun S, Wu XD. Ischemic postconditioning protects myocardium from ischemia/reperfusion injury through attenuating endoplasmic reticulum stress. Shock 2008; 30: 422-27; PMID: 18323739; http://dx. doi. org/10. 1097/SHK. 0b013e318164ca29.
8. Wang Z, Wang Y, Ye J, Lu X, Cheng Y, Xiang L, Chen L, Feng W, Shi H, Yu X, et al. bFGF attenuates endoplasmic reticulum stress and mitochondrial injury on myocardial ischaemia/reperfusion via activation of PI3K/Akt/ERK1/2 pathway. J Cell Mol Med 2015; 19: 595-607; PMID: 25533999; http://dx. doi. org/10. 1111/jcmm. 12346.
9. Guo XF, Yang XJ. Endoplasmic reticulum stress response in spontaneously hypertensive rats is affected by myocardial ischemia reperfusion injury. Exp Ther Med 2015; 9: 319-326; PMID: 25574192; http://dx. doi. org/10. 3892/etm. 2014. 2094.
10. Zhang GG, Teng X, Liu Y, Cai Y, Zhou YB, Duan XH, Song JQ, Shi Y, Tang CS, Yin XH, et al. Inhibition of endoplasm reticulum stress by ghrelin protects against ischemia/reperfusion injury in rat heart. Peptides 2009; 30: 1109-1116; PMID: 19406177; http://dx. doi. org/10. 1016/j. peptides. 2009. 03. 024.
11. Groenendyk J, Agellon LB, Michalak M. Coping with endoplasmic reticulum stress in the cardiovascular system. Annu Rev Physiol 2013; 75: 49-67; PMID: 23020580; http://dx. doi. org/10. 1146/annurevphysiol-030212-183707.
12. He X, Zhao M, Bi X, Sun L, Yu X, Zhao M, Zang W. Novel strategies and underlying protective mechanisms of modulation of vagal activity in cardiovascular diseases. Br J Pharmacol 2015; PMID: 25378088; http://dx. doi. org/10. 1111/bph. 13010 [Epub ahead of print].
13. Calvillo I, Vanoli E, Andreoli E, Besana A, Omodeo E, Gnecchi M, Zerbi P, Vago G, Busca G, Schwartz PJ. Vagal stimulation, through its nicotinic action, limits infarct size and the inflammatory response to myocardial ischemia and reperfusion. J Cardiovasc Pharmacol 2011; 58: 500-7; PMID: 21765369; http://dx. doi. org/10. 1097/FJC. 0b013e31822b7204.
14. Zhao M, He X, Bi XY, Yu XJ, Gil Wier W, Zang WJ. Vagal stimulation triggers peripheral vascular protection through the cholinergic anti-inflammatory pathway in a rat model of myocardial ischemia/reperfusion. Basic Res Cardiol 2013; 108: 345; PMID: 23519622; http://dx. doi. org/10. 1007/s00395-013-0345-1.
15. Liu JJ, Li DL, Zhou J, Sun L, Zhao M, Kong SS, Wang YH, Yu XJ, Zhou J, Zang WJ. Acetylcholine prevents angiotensin II-induced oxidative stress and apoptosis in H9c2 cells. Apoptosis 2011; 16: 94-103; PMID: 20963497; http://dx. doi. org/10. 1007/s10495-010-0549-x.
16. Miao Y, Bi XY, Zhao M, Jiang HK, Liu JJ, Li DL, Yu XJ, Yang YH, Huang N, Zang WJ. Acetylcholine inhibits tumor necrosis factor a activated endoplasmic reticulum apoptotic pathway via EGFR-PI3K signaling in cardiomyocytes. J Cell Physiol 2015; 230: 767-74; PMID: 25201632; http://dx. doi. org/10. 1002/jcp. 24800.
17. Zhao M, Sun L, Yu XJ, Miao Y, Liu JJ, Wang H, Ren J, Zang WJ. Acetylcholine mediates AMPK-dependent autophagic cytoprotection in H9c2 cells during hypoxia/reoxygenation injury. Cell Physiol Biochem 2013; 32: 601-13; PMID: 24021916; http://dx. doi. org/10. 1159/000354464.
18. Song P, Zou MH. Regulation of NAD(P)H oxidases by AMPK in cardiovascular systems. Free Radic Biol Med 2012; 52: 1607-19; PMID: 22357101; http://dx. doi. org/10. 1016/j. freeradbiomed. 2012. 01. 025.
19. Dong Y, Zhang M, Liang B, Xie Z, Zhao Z, Asfa S, Choi HC, Zou MH. Reduction of AMP-activated protein kinase alpha2 increases endoplasmic reticulum stress and atherosclerosis in vivo. Circulation 2010; 121: 792-803; PMID: 20124121; http://dx. doi. org/10. 1161/CIRCULATIONAHA. 109. 900928.
20. Kataoka Y, Shibata R, Ohashi K, Kambara T, Enomoto T, Uemura Y, Ogura Y, Yuasa D, Matsuo K, Nagata T, et al. Omentin prevents myocardial ischemic injury through AMP-activated protein kinase-and Akt-dependent mechanisms. J Am Coll Cardiol 2014; 63: 2722-33; PMID: 24768874; http://dx. doi. org/10. 1016/j. jacc. 2014. 03. 032.
21. Viollet B, Horman S, Leclerc J, Lantier L, Foretz M, Billaud M, Giri S, Andreelli F. AMPK inhibition in health and disease. Crit Rev Biochem Mol Biol 2010; 45: 276-95; PMID: 20522000; http://dx. doi. org/10. 3109/10409238. 2010. 488215.
22. Zhuo XZ, Wu Y, Ni YJ, Liu JH, Gong M, Wang XH, Wei F, Wang TZ, Yuan Z, Ma AQ, et al. Isoproterenol instigates cardiomyocyte apoptosis and heart failure via AMPK inactivation-mediated endoplasmic reticulum stress. Apoptosis 2013; 18: 800-10; PMID: 23620435; http://dx. doi. org/10. 1007/s10495-013-0843-5.
23. -/¡ mice. Eur J Pharmacol 2004; 493: 127-32; PMID: 15189773; http://dx. doi. org/10. 1016/j. ejphar. 2004. 04. 012.
24. Groenendyk J, Sreenivasaiah PK, Kim do H, Agellon LB, Michalak M. Biology of endoplasmic reticulum stress in the heart. Circ Res 2010; 107: 1185-97; PMID: 21071716; http://dx. doi. org/10. 1161/CIRCRESAHA. 110. 227033.
25. Wang Y, Gao E, Tao L, Lau WB, Yuan Y, Goldstein BJ, Lopez BL, Christopher TA, Tian R, Koch W, et al. AMP-activated protein kinase deficiency enhances myocardial ischemia/reperfusion injury but has minimal effect on the antioxidant/antinitrative protection of adiponectin. Circulation 2009; 119: 835-44; PMID: 19188503; http://dx. doi. org/10. 1161/CIRCULATIONAHA. 108. 815043.
26. Chen K, Li G, Geng F, Zhang Z, Li J, Yang M, Dong L, Gao F. Berberine reduces ischemia/reperfusioninduced myocardial apoptosis via activating AMPK and PI3K-Akt signaling in diabetic rats. Apoptosis 2014; 19: 946-57; PMID: 24664781; http://dx. doi. org/10. 1007/s10495-014-0977-0.
27. Terai K, Hiramoto Y, Masaki M, Sugiyama S, Kuroda T, Hori M, Kawase I, Hirota H. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol Cell Biol 2005; 25: 9554-75; PMID: 16227605; http://dx. doi. org/10. 1128/MCB. 25. 21. 9554-9575. 2005.
28. Oakes SA, Papa FR. The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol 2015; 10: 173-94; PMID: 25387057; http://dx. doi. org/10. 1146/annurev-pathol-012513-104649.
29. Macaluso M, Caracciolo V, Rizzo V, Sun A, Montanari M, Russo G, Bellipanni G, Khalili K, Giordano A. Integrating role of T antigen, Rb2/p130, CTCF and BORIS in mediating non-canonical endoplasmic reticulum-dependent death pathways triggered by chronic ER stress in mouse medulloblastoma. Cell Cycle 2012; 11: 1841-50; PMID: 22544282; http://dx. doi. org/10. 4161/cc. 20242.
30. Estrada IA, Donthamsetty R, Debski P, Zhou MH, Zhang SL, Yuan JX, Han W, Makino A. STIM1 restores coronary endothelial function in type 1 diabetic mice. Circ Res 2012; 111: 1166-75; PMID: 22896585; http://dx. doi. org/10. 1161/CIRCRESAHA. 112. 275743.
31. Park IJ, Kim MJ, Park OJ, Choe W, Kang I, Kim SS, Ha J. Cryptotanshinone induces ER stress-mediated apoptosis in HepG2 and MCF7 cells. Apoptosis 2012; 17: 248-57; PMID: 22113823; http://dx. doi. org/10. 1007/s10495-011-0680-3.
32. Dong S, Teng Z, Lu FH, Zhao YJ, Li H, Ren H, Chen H, Pan ZW, Lv YJ, Yang BF, et al. Post-conditioning protects cardiomyocytes from apoptosis via PKC(epsilon)-interacting with calcium-sensing receptors to inhibit endo(sarco)plasmic reticulum-mitochondria crosstalk. Mol Cell Biochem 2010; 341: 195-206; PMID: 20383739; http://dx. doi. org/10. 1007/s11010-010-0450-5.
33. Yoon MJ, Lee AR, Jeong SA, Kim YS, Kim JY, Kwon YJ, Choi KS. Release of Ca2C from the endoplasmic reticulum and its subsequent influx into mitochondria trigger celastrol-induced paraptosis in cancer cells. Oncotarget 2014; 5: 6816-31; PMID: 25149175.
34. He X, Bi XY, Lu XZ, Zhao M, Yu XJ, Sun L, Xu M, Wier WG, Zang WJ. Reduction of mitochondriaendoplasmic reticulum interactions by acetylcholine protects human umbilical vein endothelial cells from hypoxia/reoxygenation injury. Arterioscler Thromb Vasc Biol 2015; PMID: 25977565; http://dx. doi. org/10. 1161/ATVBAHA. 115. 305469 [Epub ahead of print].
35. Petkovich BW, Vega J, Thomas S. Vagal modulation of hypertension. Curr Hypertens Rep 2015; 17: 532; PMID: 25794951; http://dx. doi. org/10. 1007/s11906-015-0532-6.
36. Schwartz PJ, De Ferrari GM, Sanzo A, Landolina M, Rordorf R, Raineri C, Campana C, Revera M, Ajmone-Marsan N, Tavazzi L, et al. Long term vagal stimulation in patients with advanced heart failure: first experience in man. Eur J Heart Fail 2008; 10: 884-91; PMID: 18760668; http://dx. doi. org/10. 1016/j. ejheart. 2008. 07. 016.
37. Kim MH, Kim MO, Heo JS, Kim JS, Han HJ. Acetylcholine inhibits long-term hypoxia-induced apoptosis by suppressing the oxidative stress-mediated MAPKs activation as well as regulation of Bcl-2, c-IAPs, and caspase-3 in mouse embryonic stem cells. Apoptosis 2008; 13: 295-304; PMID: 18049903; http://dx. doi. org/10. 1016/10. 1007/s10495-007-0160-y.
38. Miao Y, Zhou J, Zhao M, Liu J, Sun L, Yu X, He X, Pan X, Zang W. Acetylcholine attenuates hypoxia/reoxygenation-induced mitochondrial and cytosolic ROS formation in H9c2 cells via M2 acetylcholine receptor. Cell Physiol Biochem 2013; 31: 189-98; PMID: 23407103; http://dx. doi. org/10. 1159/000343360.
39. Li DL, Liu JJ, Liu BH, Hu H, Sun L, Xu HF, Yu XJ, Ma X, Ren J, et al. Acetylcholine inhibits hypoxiainduced tumor necrosis factor-a production via regulation of MAPKs phosphorylation in cardiomyocytes. J Cell Physiol 2011; 226: 1052-9; PMID: 20857413; http://dx. doi. org/10. 1002/jcp. 22424.
40. Millott R, Dudek E, Michalak M. The endoplasmic reticulum in cardiovascular health and disease. Can J Physiol Pharmacol 2012; 90: 1209-17; PMID: 22897133; http://dx. doi. org/10. 1139/y2012-058.
41. Zhou B, Li H, Liu J, Xu L, Zang W, Wu S, Sun H. Intermittent injections of osteocalcin reverse autophagic dysfunction and endoplasmic reticulum stress resulting from diet-induced obesity in the vascular tissue via the NFkB-p65-dependent mechanism. Cell Cycle 2013; 12: 1901-13; PMID: 23708521; http://dx. doi. org/10. 4161/cc. 24929.
42. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011; 13: 184-90; PMID: 21364565; http://dx. doi. org/10. 1038/ncb0311-184.
43. DuRose JB, Tam AB, Niwa M. Intrinsic capacities of molecular sensors of the unfolded protein response to sense alternate forms of endoplasmic reticulum stress. Mol Biol Cell. 2006; 17: 3095-107; PMID: 16672378; http://dx. doi. org/10. 1091/mbc. E06-01-0055.
44. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, Wang J, Song B, Yau GD, Kaufman RJ. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 2007; 13: 351-64; PMID: 17765679; http://dx. doi. org/10. 1016/j. devcel. 2007. 07. 005.
45. Ofek K, Soreq H. Cholinergic involvement and manipulation approaches in multiple system disorders. Chem Biol Interact 2013; 203: 113-9; PMID: 22898318; http://dx. doi. org/10. 1016/j. cbi. 2012. 07. 007.
46. Sun L, Zang WJ, Wang H, Zhao M, Yu XJ, He X, Miao Y, Zhou J. Acetylcholine promotes ROS detoxification against hypoxia/reoxygenation-induced oxidative stress through FoxO3a/PGC-1a dependent superoxide dismutase. Cell Physiol Biochem 2014; 34: 1614-25; PMID: 25402826; http://dx. doi. org/10. 1159/000366364.
47. Wei K, Liu L, Xie F, Hao X, Luo J, Min S. 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 2015; 12: 83-91; PMID: 25552923; http://dx. doi. org/10. 7150/ijms. 10101.
48. Lu XZ, Bi XY, He X, Zhao M, Xu M, Yu XJ, Zhao ZH, Zang WJ. Activation of M3 muscarinic acetylcholine receptors attenuates ischaemia/reperfusion-induced vascular injury via inhibition of the ROS-mediated CaMKII pathway. Br J Pharmacol 2015; PMID: 25953628; http://dx. doi. org/10. 1111/bph. 13183 [Epub ahead of print].
49. Kawada T, Akiyama T, Shimizu S, Kamiya A, Uemura K, Li M, Shirai M, Sugimachi M. Detection of endogenous acetylcholine release during brief ischemia in the rabbit ventricle: a possible trigger for ischemic preconditioning. Life Sci 2009; 85: 597-601; PMID: 19733187; http://dx. doi. org/10. 1016/j. lfs. 2009. 08. 015.
50. Engel AG, Shen XM, Selcen D, Sine S. New horizons for congenital myasthenic syndromes. Ann N Y Acad Sci 2012; 1275: 54-62; PMID: 23278578; http://dx. doi. org/10. 1111/j. 1749-6632. 2012. 06803. x.
51. Sugimoto K, Fujii S, Takemasa T, Yamashita K. Detection of intracellular nitric oxide using a combination of aldehyde fixatives with 4, 5-diaminofluorescein diacetate. Histochem Cell Biol 2000; 113: 341-7; PMID: 0883393; http://dx. doi. org/10. 1007/s004180000151.
52. He X, Zhao M, Bi XY, Yu XJ, Zang WJ. Delayed preconditioning prevents ischemia/reperfusion-induced endothelial injury in rats: role of ROS and eNOS. Lab Invest 2013; 93: 168-80; PMID: 23147223; http://dx. doi. org/10. 1038/labinvest. 2012. 160.