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

References

• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Wang J, Chen S, Ma X, Cheng C, Xiao X, Chen J, Liu S, Zhao B, Chen Y. Effects of endothelial progenitor cell-derived microvesicles on hypoxia/reoxygenation-induced endothelial dysfunction and apoptosis. Oxid Med Cell Longev 2013; 2013:572729; PMID:24288585; http://dx.doi.org/10.1155/2013/572729
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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/annurev-physiol-030212-183707
   PubMed Web of Science ®Google Scholar
• 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]
   PubMed Web of Science ®Google Scholar
• Calvillo 1, 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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 α 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Khurana S, Chacon I, Xie G, Yamada M, Wess J, Raufman JP Kennedy RH. Vasodilatory effects of cholinergic agonists are greatly diminished in aorta from M3R−/− mice. Eur J Pharmacol 2004; 493:127–32; PMID:15189773; http://dx.doi.org/10.1016/j.ejphar.2004.04.012
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Chen K, Li G, Geng F, Zhang Z, Li J, Yang M, Dong L, Gao F. Berberine reduces ischemia/reperfusion-induced 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Yoon MJ, Lee AR, Jeong SA, Kim YS, Kim JY, Kwon YJ, Choi KS. Release of Ca2+ from the endoplasmic reticulum and its subsequent influx into mitochondria trigger celastrol-induced paraptosis in cancer cells. Oncotarget 2014; 5:6816–31; PMID:25149175
   PubMed Web of Science ®Google Scholar
• He X, Bi XY, Lu XZ, Zhao M, Yu XJ, Sun L, Xu M, Wier WG, Zang WJ. Reduction of mitochondria-endoplasmic 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]
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Li DL, Liu JJ, Liu BH, Hu H, Sun L, Xu HF, Yu XJ, Ma X, Ren J, et al. Acetylcholine inhibits hypoxia-induced tumor necrosis factor-α 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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 NFκB-p65-dependent mechanism. Cell Cycle 2013; 12:1901–13; PMID:23708521; http://dx.doi.org/10.4161/cc.24929
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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-1α dependent superoxide dismutase. Cell Physiol Biochem 2014; 34:1614–25; PMID:25402826; http://dx.doi.org/10.1159/000366364
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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]
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar