M3-mAChR stimulation exerts anti-apoptotic effect via activating the HIF-1α/HO-1/VEGF signaling pathway in H9c2 rat ventricular cells

Journal of Cardiovascular Pharmacology

Volumn 60, Issue 5, 2012, Pages 474-482

  Hui, Yang ^a,b   Zhao, Yanli ^a,c   Ma, Ning ^a   Peng, Yahui ^a,b   Pan, Zhenwei ^a   Zou, Chaoxia ^a,b   Zhang, Pengxia ^d   Du, Zhimin ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b State Province Key Laboratories of Biomedicine Pharmaceutics of China   (China)

^c QINGHAI UNIVERSITY   (China)

^d JIAMUSI UNIVERSITY   (China)

Author keywords

acetylcholine receptors (muscarinic) M3; apoptosis; heme oxygenase 1; hypoxia inducible factor 1; vascular endothelial growth factor

Indexed keywords

4 DIPHENYLACETOXY 1 METHYLPIPERIDINE; ETOPOSIDE; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIFICIGUAT; MUSCARINIC M3 RECEPTOR; VASCULOTROPIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; HEART MUSCLE CELL; HEART PROTECTION; HEART VENTRICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STABLE EXPRESSION;

ANIMALS; APOPTOSIS; CARBACHOL; CARDIOTONIC AGENTS; CELL CULTURE TECHNIQUES; CELL LINE; ETOPOSIDE; HEART VENTRICLES; HEME OXYGENASE (DECYCLIZING); HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOBLOTTING; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, MUSCARINIC M3; SIGNAL TRANSDUCTION; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84870061073     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0b013e31826c1c13     Document Type: Article

References (40)

1. Jaiswal N, Lambrecht G, Mutschler E, et al. Effect of M2 muscarinic receptor antagonist 4-DAMP on prostaglandin synthesis and mechanical function in the isolated rabbit heart. Gen Pharmacol. 1989;20:497-502. (Pubitemid 19161432)
2. Akahane K, Furukawa Y, Karasawa Y, et al. Muscarinic receptor subtypes mediating negative chrono-and inotropic responses in isolated, blood-perfused dog right atria. J Auton Pharmacol. 1990;10:39-48. (Pubitemid 20109707)
3. Sharma VK, Colecraft HM, Rubin LE, et al. Does mammalian heart contain only the M2 muscarinic receptor subtype? Life Sci. 1997;60:1023-1029. (Pubitemid 27165571)
4. Sharma VK, Colecraft HM, Wang DX, et al. Molecular and functional identification of m1 muscarinic acetylcholine receptors in rat ventricular myocytes. Circ Res. 1996;79:86-93. (Pubitemid 26196321)
5. Colecraft HM, Egamino JP, Sharma VK, et al. Signaling mechanisms underlying muscarinic receptor mediated increase in contraction rate in cultured heart cells. J Biol Chem. 1998;273:32158-32166. (Pubitemid 29177161)
6. Brodde OE, Michel MC. Adrenergic and muscarinic receptors in the human heart. Pharmacol Rev. 1999;51:651-690.
7. Yang CM, Yeh HM, Sung TC, et al. Characterization of muscarinic receptor subtypes in canine left ventricular membranes. J Recept Res. 1992;12:427-449.
8. Shi H, Wang H, Lu Y, et al. Choline modulates cardiac membrane repolarization by activating an M3 muscarinic receptor and its coupled K+ channel. J Membr Biol. 1999;169:55-64. (Pubitemid 29211074)
9. Shi H, Wang H, Wang Z. Identification and characterization of multiple subtypes of muscarinic acetylcholine receptors and their physiological functions in canine hearts. Mol Pharmacol. 1999;55:497-507. (Pubitemid 29128106)
10. Wang H, Shi H, Lu Y, et al. Pilocarpine modulates the cellular electrical properties of mammalian hearts by activating a cardiac M3 receptor and a K+ current. Br J Pharmacol. 1999;126:1725-1734. (Pubitemid 29213089)
11. Wang H, Han H, Zhang L, et al. Expression of multiple subtypes of muscarinic receptors and cellular distribution in the human heart. Mol Pharmacol. 2001;59:1029-1036. (Pubitemid 32381581)
12. Camusso JJ, Sterin-Borda L, Rodriguez M, et al. Pharmacological evidence for the existence of different subtypes of muscarinic acetylcholine receptors for phosphoinositide hydrolysis in neonatal versus adult rat atria. J Lipid Mediat Cell Signal. 1995;12:1-10.
13. Dheina S, van Koppenb CJ, Broddea OE. Muscarinic receptors in the Mammalian Heart. Pharmacol Res. 2001;44:161-182.
14. Liu Y, Wang Y, Ma ML, et al. Cardiac-hemodynamic effects of M3 receptor agonist on rat and rabbit hearts. Yao Xue Xue Bao. 2001;36:84-87. (Pubitemid 33695841)
15. Wang H, Lu Y, Wang Z. Function of cardiac M3 receptors. Auton Autacoid Pharmacol. 2007;27:1-11.
16. De Sarno P, Shestopal SA, King TD, et al. Muscarinic receptor activation protects cells from apoptotic effects of DNA damage, oxidative stress, and mitochondrial inhibition. J Biol Chem. 2003;278:11086-11093. (Pubitemid 36792660)
17. Tobin AB, Budd DC. The anti-apoptotic response of the Gq/11-coupled muscarinic receptor family. Biochem Soc Trans. 2003;31:1182-1185. (Pubitemid 38030935)
18. Budd DC, McDonald J, Emsley N, et al. The C-terminal tail of the M3-muscarinic receptor possesses anti-apoptotic properties. J Biol Chem. 2003;278:19565-19573. (Pubitemid 36799355)
19. Budd DC, Spragg EJ, Ridd K, et al. Signalling of the M3-muscarinic receptor to the anti-apoptotic pathway. Biochem J. 2004;381:43-49. (Pubitemid 38932209)
20. Solyakov L, Sayan E, Riley J, et al. Regulation of p53 expression, phosphorylation and subcellular localization by a G-protein-coupled receptor. Oncogene. 2009;28:3619-3630.
21. Liu Y, Sun HL, Wu H, et al. Protective effect of M3 receptor on H2O2-induced apoptosis of rat myocardial cells in vitro. Yao Xue Xue Bao. 2004;39:887-891. (Pubitemid 40193182)
22. Hirota K, Fukuda R, Takabuchi S, et al. Induction of hypoxia-inducible factor 1 activity by muscarinic acetylcholine receptor signaling. J Biol Chem. 2004;279:41521-41528. (Pubitemid 39313593)
23. Drechsler Y, Dolganiuc A, Norkina O, et al. Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 MAPK activation in monocytes. J Immunol. 2006;177:2592-2600. (Pubitemid 44201018)
24. Turkseven S, Kruger A, Mingone CJ, et al. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol. 2005;289:H701-H707. (Pubitemid 41129386)
25. Slack BE, Siniaia MS. Adhesion-dependent redistribution of MAP kinase and MEK promotes muscarinic receptor-mediated signaling to the nucleus. J Cell Biochem. 2005;95:366-378. (Pubitemid 41420205)
26. Pönicke K, Heinroth-Hoffmann I, Brodde OE. Demonstration of functional M3-muscarinic receptors in ventricular cardiomyocytes of adult rats. Br J Pharmacol. 2003;138:156-160. (Pubitemid 36194215)
27. Willmy-Matthes P, Leineweber K, Wangemann T, et al. Existence of functional M3-muscarinic receptors in the human heart. Naunyn Schmiedebergs Arch Pharmacol. 2003;368:316-319. (Pubitemid 37372555)
28. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol. 1992;12:5447-5454.
29. Ema M, Taya S, Yokotani N, et al. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci U S A. 1997;94:4273-4278.
30. Dachs GU, Patterson AV, Firth JD, et al. Targeting gene expression to hypoxic tumor cells. Nat Med. 1997;3:515-520. (Pubitemid 27198648)
31. Bruick RK. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci U S A. 2000;97:9082-9087. (Pubitemid 30626677)
32. Merighi S, Benini A, Mirandola P, et al. Hypoxia inhibits paclitaxelinduced apoptosis through adenosine-mediated phosphorylation of Bad in glioblastoma cells. Mol Pharmacol. 2007;72:162-172. (Pubitemid 46998535)
33. Chen JK, Hu LJ, Wang J, et al. Hypoxia-induced BAX overexpression and radiation killing of hypoxic glioblastoma cells. Radiat Res. 2005;163:644-653. (Pubitemid 40734763)
34. Piret JP, Mottet D, Raes M, et al. Is HIF-1alpha a pro-or an antiapoptotic protein? Biochem Pharmacol. 2002;64:889-892.
35. Wang GL, Jiang BH, Rue EA, et al. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A. 1995;92:5510-5514.
36. Kim HL, Yeo EJ, Chun YS, et al. A domain responsible for HIF-1alpha degradation by YC-1, a novel anticancer agent. Int J Oncol. 2006;29:255-260.
37. Yeo EJ, Chun YS, Cho YS, et al. YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1. J Natl Cancer Inst. 2003;95:516-525.
38. Sun HL, Liu YN, Huang YT, et al. YC-1 inhibits HIF-1 expression in prostate cancer cells: contribution of Akt/NF-kappaB signaling to HIF-1alpha accumulation during hypoxia. Oncogene. 2007;26:3941-3951.
39. Li SH, Shin DH, Chun YS, et al. A novel mode of action of YC-1 in HIF inhibition: stimulation of FIH-dependent p300 dissociation from HIF-1 {alpha}. Mol Cancer Ther. 2008;7:3729-3738.
40. Yang B, Lin H, Xu C, et al. Choline produces cytoprotective effects against ischemic myocardial injuries: evidence for the role of cardiac m3 subtype muscarinic acetylcholine receptors. Cell Physiol Biochem. 2005;16:163-174. (Pubitemid 41643017)