Activation of M3 cholinoceptors attenuates vascular injury after ischaemia/reperfusion by inhibiting the Ca 2+/calmodulin-dependent protein kinase II pathway

British Journal of Pharmacology

Volumn 172, Issue 23, 2015, Pages 5619-5633

  Lu, Xing Zhu ^a   Bi, Xue Yuan ^a   He, Xi ^a   Zhao, Ming ^a   Xu, Man ^a   Yu, Xiao Jiang ^a   Zhao, Zheng Hang ^a   Zang, Wei Jin ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; MUSCARINIC M3 RECEPTOR; PHOSPHOLAMBAN; REACTIVE OXYGEN METABOLITE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CALCIUM EXCHANGE PROTEIN; SUPEROXIDE; 4-DIPHENYLACETOXY-1,1-DIMETHYLPIPERIDINIUM; CHOLINE; CHOLINERGIC RECEPTOR STIMULATING AGENT; PIPERIDINE DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; BLOOD VESSEL REACTIVITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; MALE; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RECEPTOR UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; COMPLICATION; DOSE RESPONSE; DRUG EFFECTS; INTRAVENOUS DRUG ADMINISTRATION; ISCHEMIA; METABOLISM; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; STRUCTURE ACTIVITY RELATION; VASCULAR SYSTEM INJURIES;

ADMINISTRATION, INTRAVENOUS; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CHOLINE; CHOLINERGIC AGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ISCHEMIA; MALE; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M3; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; VASCULAR SYSTEM INJURIES;

EID: 84949532924     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13183     Document Type: Article

References (56)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G Protein-Coupled Receptors. Br J Pharmacol 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, et al. (2013c). The Concise Guide to PHARMACOLOGY 2013/14: Ion Channels. Br J Pharmacol 170: 1607-1651.
4. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, et al. (2013d). The Concise Guide to PHARMACOLOGY 2013/14: Ligand-Gated Ion Channels. Br J Pharmacol 170: 1582-1606.
5. 3 muscarinic receptors to the vasodilator response to acetylcholine in the human forearm vascular bed. Br J Clin Pharmacol 66: 300-303.
6. Banz Y, Rieben R, (2012). Role of complement and perspectives for intervention in ischemia-reperfusion damage. Ann Med 44: 205-217.
7. Bell JR, Vila-Petroff M, Delbridge LM, (2014). CaMKII-dependent responses to ischemia and reperfusion challenges in the heart. Front Pharmacol 5: 96.
8. 3 receptor in endothelium-dependent vasodilatation in mouse arteries. J Cardiovasc Pharmacol 51: 505-512.
9. Bi XY, He X, Zhao M, Yu XJ, Zang WJ, (2013). Role of endothelial nitric oxide synthase and vagal activity in the endothelial protection of atorvastatin in ischemia/reperfusion injury. J Cardiovasc Pharmacol 61: 391-400.
10. Borer KE, Bailey SR, Harris PA, Elliott J, (2013). Contractile responses of isolated equine digital arteries under hypoxic or hyperoxic conditions in vitro: role of reactive oxygen species and Rho kinase. J Vet Pharmacol Ther 36: 267-274.
11. Colucci R, Fornai M, Duranti E, Antonioli L, Rugani I, Aydinoglu F, et al. (2013). Rosuvastatin prevents angiotensin II-induced vascular changes by inhibition of NAD(P)H oxidase and COX-1. Br J Pharmacol 169: 554-566.
12. Erickson JR, (2014). Mechanisms of CaMKII activation in the heart. Front Pharmacol 5: 59.
13. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, et al. (2008). A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133: 462-474.
14. Gandhirajan RK, Meng S, Chandramoorthy HC, Mallilankaraman K, Mancarella S, Gao H, et al. (2013). Blockade of NOX2 and STIM1 signaling limits lipopolysaccharide-induced vascular inflammation. J Clin Invest 123: 887-902.
15. 2+-ATPase activity and inhibiting endoplasmic reticulum stress. J Cardiovasc Pharmacol 62: 143-153.
16. Hadri L, Kratlian RG, Benard L, Maron BA, Dorfmuller P, Ladage D, et al. (2013). Therapeutic efficacy of AAV1.SERCA2a in monocrotaline-induced pulmonary arterial hypertension. Circulation 128: 512-523.
17. Harvey RD, (2012). Muscarinic receptor agonists and antagonists: effects on cardiovascular function. Handb Exp Pharmacol 208: 299-316.
18. He X, Zhao M, Bi XY, Zang WJ, (2013). Delayed preconditioning prevents ischemia/reperfusion induced endothelial injury in rats: role of ROS and eNOS. Lab Invest 93: 168-180.
19. Herranz B, Marquez S, Guijarro B, Aracil E, Aicart-Ramos C, Rodriguez-Crespo I, et al. (2013). Integrin-linked kinase regulates vasomotor function by preventing endothelial nitric oxide synthase uncoupling role in atherosclerosis. Circ Res 110: 439-449.
20. 2+ exchanger-mediated mitochondrial calcium overload. Cell Calcium 51: 402-410.
21. 2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu Rev Biochem 71: 473-510.
22. Johansson S, Povlsen GK, Edvinsson L, (2012). Expressional changes in cerebrovascular receptors after experimental transient forebrain ischemia. PLoS ONE 7: e41852.
23. Kalogeris T, Baines CP, Krenz M, Korthuis RJ, (2012). Cell biology of ischemia/reperfusion injury. Int Rev Cell Mol Biol 298: 229-317.
24. Kawagishi H, Finkel T, (2014). Unraveling the truth about antioxidants: ROS and disease: finding the right balance. Nat Med 20: 711-713.
25. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs reporting guidelines working group. Br J Pharmacol 160: 1577-1579.
26. Lamping KG, Wess J, Cui Y, Nuno DW, Faraci FM, (2004). Muscarinic (M) receptors in coronary circulation gene-targeted mice define the role of M2 and M3 receptors in response to acetylcholine. Arterioscler Thromb Vasc Biol 24: 1253-1258.
27. Lawoko G, Jarlebark L, Heilbronn E, (1995). Ligand-binding properties of an unusual nicotinic acetylcholine receptor subtype on isolated outer hair cells from guinea pig cochlea. Neurosci Lett 195: 64-68.
28. 2+/calmodulin-dependent protein kinase II δ mediates myocardial ischemia/reperfusion injury through nuclear factor-kappa B. Circ Res 112: 935-944.
29. Lipskaia L, Hadri L, Lopez JJ, Hajjar RJ, Bobe R, (2013). Benefit of SERCA2a gene transfer to vascular endothelial and smooth muscle cells: a new aspect in therapy of cardiovascular diseases. Curr Vasc Pharmacol 11: 465-479.
30. 2+ handling as a common mechanism. Can J Physiol Pharmacol 86: 860-865.
31. Luczak ED, Anderson ME, (2014). CaMKII oxidative activation and the pathogenesis of cardiac disease. J Mol Cell Cardiol 73: 112-116.
32. Luo M, Guan X, Luczak ED, Lang D, Kutschke W, Gao Z, et al. (2013). Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J Clin Invest 123: 1262-1274.
33. 2+ exchanger in developing rats. Cell Physiol Biochem 34: 313-324.
34. 2+/calmodulin-dependent protein kinase II. Br J Pharmacol 157: 705-715.
35. Martinez-Revelles S, Jimenez-Altayo F, Caracuel L, Perez-Asensio FJ, Planas AM, Vila E, (2008). Endothelial dysfunction in rat mesenteric resistance artery after transient middle cerebral artery occlusion. J Pharmacol Exp Ther 325: 363-369.
36. Matsumoto T, Kobayashi T, Ishida K, Taguchi K, Kamata K, (2010). Enhancement of mesenteric artery contraction to 5-HT depends on Rho kinase and Src kinase pathways in the ob/ob mouse model of type 2 diabetes. Br J Pharmacol 160: 1092-1104.
37. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
38. del Monte F, Lebeche D, Guerrero JL, Tsuji T, Doye AA, Gwathmey JK, et al. (2004). Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc Natl Acad Sci U S A 101: 5622-5627.
39. 3 muscarinic receptors in human pulmonary arteries. Br J Pharmacol 119: 149-157.
40. Paillard M, Tubbs E, Thiebaut PA, Gomez L, Fauconnier J, Da Silva CC, et al. (2013). Depressing mitochondria-reticulum interactions protects cardiomyocytes from lethal hypoxia-reoxygenation injury. Circulation 128: 1555-1565.
41. 3 subtype of muscarinic acetylcholine receptor promotes cardioprotection via the suppression of miR376b5p. PLoS ONE 7: e32571.
42. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledge base of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-D1106.
43. Pesic S, Grbovic L, Jovanovic A, (2002). Acetylcholine-induced contractions in the perforating branch of the human internal mammary artery: protective role of the vascular endothelium. Pharmacology 64: 182-188.
44. 2+/calmodulin-activated protein kinase II. Free Radic Biol Med 65: 234-243.
45. Szadujkis-Szadurska K, Slupski M, Szadujkis-Szadurski R, Szadujkis-Szadurski L, Jasiñski M, Kolodziejska R, (2010). The role of the endothelium in the regulation of vascular smooth muscle cell contractions induced by angiotensin II after ischemia and reperfusion. Arch Pharm Res 33: 1019-1024.
46. 2+-exchangers in coronary artery endothelium versus smooth muscle. J Cell Mol Med 11: 129-138.
47. Tabrizi-Fard MA, Maurer TS, Fung HL, (1999). In vivo disposition of 3-nitro-L-tyrosine in rats: implications on tracking systemic peroxynitrite exposure. Drug Metab Dispos 27: 429-431.
48. Takhtfooladi MA, Jahanshahi A, Sotoudeh A, Daneshi MH, Khansari M, Takhtfooladi HA, (2013). The antioxidant role of N-acetylcysteine on the testicular remote injury after skeletal muscle ischemia and reperfusion in rats. Pol J Pathol 64: 204-209.
49. Wang J, Chen S, Ma X, Cheng C, Xiao X, Chen J, et al. (2013). Effects of endothelial progenitor cell-derived microvesicles on hypoxia/reoxygenation induced endothelial dysfunction and apoptosis. Oxid Med Cell Longev 2013: 572729.
50. 3 muscarinic acetylcholine receptors has cardioprotective effects against ischaemia-induced arrhythmias. Clin Exp Pharmacol Physiol 39: 343-349.
51. Wang S, Han HM, Pan ZW, Hang PZ, Sun LH, Jiang YN, et al. (2012b). Choline inhibits angiotensin II-induced cardiac hypertrophy by intracellular calcium signal and p38 MAPK pathway. Naunyn Schmiedebergs Arch Pharmacol 385: 823-831.
52. Wu X, Xu T, Li D, Zhu S, Chen Q, Hu W, et al. (2013). ERK/PP1a/PLB/SERCA2a and JNK pathways are involved in luteolin-mediated protection of rat hearts and cardiomyocytes following ischemia/reperfusion. PLoS ONE 8: e82957.
53. Yousif MH, Benter IF, Akhtar S, (2003). Inhibition of calcium/calmodulin-dependent protein kinase II normalizes diabetes-induced abnormal vascular reactivity in the rat perfused mesenteric vascular bed. Auton Autacoid Pharmacol 23: 27-33.
54. 3 receptors induces delayed cardioprotection by preserving phosphorylated connexin43 and up-regulating cyclooxygenase-2 expression. Br J Pharmacol 159: 1217-1225.
55. Zhao M, He X, Bi XY, Yu XJ, Gil Wier W, Zang WJ, (2013). Vagal stimulation triggers peripheral vascular protection through the cholinergic anti-inflammatory pathway in a rat model of myocardial ischemia/reperfusion. Basic Res Cardiol 108: 345.
56. Zhao Z, Fefelova N, Shanmugam M, Bishara P, Babu GJ, Xie LH, (2011). Angiotensin II induces after depolarizations via reactive oxygen species and calmodulin kinase II signaling. J Mol Cell Cardiol 50: 128-136.