Acetylcholine mediates AMPK-dependent autophagic cytoprotection in H9c2 cells during hypoxia/reoxygenation injury

Cellular Physiology and Biochemistry

Volumn 32, Issue 3, 2013, Pages 601-613

  Zhao, Mei ^a   Sun, Lei ^a   Yu, Xiao Jiang ^a   Miao, Yi ^a   Liu, Jin Jun ^a   Wang, Hao ^a   Ren, Jun ^b   Zang, Wei Jin ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF WYOMING COLLEGE OF HEALTH SCIENCES   (United States)

Author keywords

Acetylcholine; AMPK; Autophagy; Hypoxia reoxygenation; Muscarinic receptor

Indexed keywords

ACETYLCHOLINE; ATROPINE; CHLOROQUINE; CREATINE KINASE; DANSYLCADAVERINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LACTATE DEHYDROGENASE; SMALL INTERFERING RNA; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MUSCARINIC RECEPTOR;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOCHEMISTRY; CELL LINE; CELL SURVIVAL; CELL VIABILITY; ENZYME PHOSPHORYLATION; ENZYME RELEASE; HEART MUSCLE CELL; HEART PROTECTION; HYPOXIA; HYPOXIA REOXYGENATION INJURY; NICK END LABELING; PRIORITY JOURNAL; STAINING; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; CELL PROTECTION; CELL VACUOLE; CONTROLLED STUDY; REOXYGENATION; REPERFUSION INJURY; SCANNING ELECTRON MICROSCOPY;

ACETYLCHOLINE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ATROPINE; AUTOPHAGY; CELL HYPOXIA; CELL LINE; CELL SURVIVAL; CHLOROQUINE; CYTOPROTECTION; MICROTUBULE-ASSOCIATED PROTEINS; MUSCARINIC ANTAGONISTS; MYOCYTES, CARDIAC; PHOSPHORYLATION; RATS; RECEPTORS, MUSCARINIC; RNA INTERFERENCE; RNA, SMALL INTERFERING; TOR SERINE-THREONINE KINASES; UBIQUITIN-ACTIVATING ENZYMES;

EID: 84884996310     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000354464     Document Type: Article

References (44)

1. Ibanez B, Fuster V, Jimenez-Borreguero J, Badimon JJ: Lethal myocardial reperfusion injury: a necessary evil? Int J Cardiol 2010;151: 3-11.
2. Yellon DM, Hausenloy DJ: Myocardial reperfusion injury. N Engl J Med 2007;357: 1121-1135.
3. Tucka J, Bennett M, Littlewood T: Cell death and survival signalling in the cardiovascular system. Front Biosci 2012;17: 248-261.
4. Kroemer G, Marino G, Levine B: Autophagy and the integrated stress response. Mol Cell 2010;40: 280-293.
5. Takemura G, Kanamori H, Goto K, Maruyama R, Tsujimoto A, Fujiwara H, Seishima M, Minatoguchi S: Autophagy maintains cardiac function in the starved adult. Autophagy 2009;5: 1034-1036.
6. Hariharan N, Zhai P, Sadoshima J: Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal 2011;14: 2179-2190.
7. Levine B, Klionsky DJ: Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004;6: 463-477.
8. Petrovski G, Das S, Juhasz B, Kertesz A, Tosaki A, Das DK: Cardioprotection by endoplasmic reticulum stress-induced autophagy. Antioxid Redox Signal 2011;14: 2191-2200.
9. Jiang M, Liu K, Luo J, Dong Z: Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury. Am J Pathol 2010;176: 1181-1192.
10. Pattison JS, Osinska H, Robbins J: Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res 2011;109: 151-160.
11. Yitzhaki S, Huang C, Liu W, Lee Y, Gustafsson AB, Mentzer RM Jr, Gottlieb RA: Autophagy is required for preconditioning by the adenosine A1 receptor-selective agonist CCPA. Basic Res Cardiol 2009;104: 157-167.
12. Gurusamy N, Lekli I, Mukherjee S, Ray D, Ahsan MK, Gherghiceanu M, Popescu LM, Das DK: Cardioprotection by resveratrol: a novel mechanism via autophagy involving the mTORC2 pathway. Cardiovasc Res 2010;86: 103-112.
13. Sroka K: On the genesis of myocardial ischemia. Z Kardiol 2004;93: 768-783.
14. Cisternas JR, Valenti VE, Alves TB, Ferreira C, Petenusso M, Breda JR, Pires AC, Tassi N, de Abreu LC: Cardiac baroreflex is already blunted in eight weeks old spontaneously hypertensive rats. Int Arch Med 2010;3: 2.
15. Schwartz PJ, De Ferrari GM, Sanzo A, Landolina M, Rordorf R, Raineri C, Campana C, Revera M, Ajmone- Marsan N, Tavazzi L, Odero A: Long term vagal stimulation in patients with advanced heart failure: first experience in man. Eur J Heart Fail 2008;10: 884-891.
16. Zhang Y, Kakinuma Y, Ando M, Katare RG, Yamasaki F, Sugiura T, Sato T: Acetylcholine inhibits the hypoxia-induced reduction of connexin43 protein in rat cardiomyocytes. J Pharmacol Sci 2006;101: 214-222.
17. Kakinuma Y, Ando M, Kuwabara M, Katare RG, Okudela K, Kobayashi M, Sato T: Acetylcholine from vagal stimulation protects cardiomyocytes against ischemia and hypoxia involving additive non-hypoxic induction of HIF-1alpha. Febs Lett 2005;579: 2111-2118.
18. Kawada T, Yamazaki T, Akiyama T, Inagaki M, Shishido T, Zheng C, Yanagiya Y, Sugimachi M, Sunagawa K: Vagosympathetic interactions in ischemia-induced myocardial norepinephrine and acetylcholine release. Am J Physiol Heart Circ Physiol 2001;280:H216-H221.
19. Uemura K, Li M, Tsutsumi T, Yamazaki T, Kawada T, Kamiya A, Inagaki M, Sunagawa K, Sugimachi M: Efferent vagal nerve stimulation induces tissue inhibitor of metalloproteinase-1 in myocardial ischemia-reperfusion injury in rabbit. Am J Physiol Heart Circ Physiol 2007;293:H2254-H2261.
20. Lu J, Zang WJ, Yu XJ, Jia B, Chorvatova A, Sun L: Effects of postconditioning of adenosine and acetylcholine on the ischemic isolated rat ventricular myocytes. Eur J Pharmacol 2006;549: 133-139.
21. 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.
22. Miao Y, Zhou J, Zhao M, Liu JJ, Sun L, Yu XJ, He X, Pan XY, Zang WJ: Acetylcholine attenuates hypoxia/reoxygenation-induced mitochondrial and cytosolic ROS formation in H9c2 cells via M2 acetylcholine receptor. Cell Physiol Biochem 2013;31: 189-198.
23. Swanlund JM, Kregel KC, Oberley TD: Investigating autophagy: quantitative morphometric analysis using electron microscopy. Autophagy 2010;6: 270-277.
24. Burman C, Ktistakis NT: Autophagosome formation in mammalian cells. Semin Immunopathol 2010;32: 397-413.
25. Harvey RD: Muscarinic receptor agonists and antagonists: effects on cardiovascular function. Handb Exp Pharmacol 2012;208: 299-316.
26. Xie Z, He C, Zou MH: AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy 2011;7: 1254-1255.
27. Ando M, Katare RG, Kakinuma Y, Zhang D, Yamasaki F, Muramoto K, Sato T: Efferent vagal nerve stimulation protects heart against ischemia-induced arrhythmias by preserving connexin43 protein. Circulation 2005;112: 164-170.
28. Tsutsumi T, Ide T, Yamato M, Kudou W, Andou M, Hirooka Y, Utsumi H, Tsutsui H, Sunagawa K: Modulation of the myocardial redox state by vagal nerve stimulation after experimental myocardial infarction. Cardiovasc Res 2008;77: 713-721.
29. Zordoky BN, El-Kadi AO: H9c2 cell line is a valuable in vitro model to study the drug metabolizing enzymes in the heart. J Pharmacol Toxicol Methods 2007;56: 317-322.
30. Watkins SJ, Borthwick GM, Arthur HM: The H9c2 cell line and primary neonatal cardiomyocyte cells show similar hypertrophic responses in vitro. In Vitro Cell Dev Biol Anim 2011;47: 125-131.
31. Nishida K, Yamaguchi O, Otsu K: Crosstalk between autophagy and apoptosis in heart disease. Circ Res 2008;103: 343-351.
32. Loos B, Genade S, Ellis B, Lochner A, Engelbrecht AM: At the core of survival: autophagy delays the onset of both apoptotic and necrotic cell death in a model of ischemic cell injury. Exp Cell Res 2011;317: 1437-1453.
33. Sadoshima J: The role of autophagy during ischemia/reperfusion. Autophagy 2008;4: 402-403.
34. Sala-Mercado JA, Wider J, Undyala VV, Jahania S, Yoo W, Mentzer RJ, Gottlieb RA, Przyklenk K: Profound cardioprotection with chloramphenicol succinate in the swine model of myocardial ischemia-reperfusion injury. Circulation 2010;122:S179-S184.
35. Yan W, Zhang H, Bai X, Lu Y, Dong H, Xiong L: Autophagy activation is involved in neuroprotection induced by hyperbaric oxygen preconditioning against focal cerebral ischemia in rats. Brain Res 2011;1402: 109-121.
36. Bibevski S, Dunlap ME: Evidence for impaired vagus nerve activity in heart failure. Heart Fail Rev 2011;16: 129-135.
37. Li M, Zheng C, Sato T, Kawada T, Sugimachi M, Sunagawa K: Vagal nerve stimulation markedly improves long-term survival after chronic heart failure in rats. Circulation 2004;109: 120-124.
38. Mizushima N: Methods for monitoring autophagy. Int J Biochem Cell Biol 2004;36: 2491-2502.
39. Mizushima N, Yoshimori T, Levine B: Methods in mammalian autophagy research. Cell 2010;140: 313-326.
40. Takagi H, Matsui Y, Sadoshima J: The role of autophagy in mediating cell survival and death during ischemia and reperfusion in the heart. Antioxid Redox Signal 2007;9: 1373-1381.
41. Sciarretta S, Hariharan N, Monden Y, Zablocki D, Sadoshima J: Is autophagy in response to ischemia and reperfusion protective or detrimental for the heart? Pediatr Cardiol 2011;32: 275-281.
42. Hamacher-Brady A, Brady NR, Gottlieb RA: Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 2006;281: 29776-29787.
43. Papandreou I, Lim AL, Laderoute K, Denko NC: Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ 2008;15: 1572-1581.
44. Shi WY, Xiao D, Wang L, Dong LH, Yan ZX, Shen ZX, Chen SJ, Chen Y, Zhao WL: Therapeutic metformin/AMPK activation blocked lymphoma cell growth via inhibition of mTOR pathway and induction of autophagy. Cell Death Dis 2012;3:e275.