Vagus nerve stimulation protects against ventricular fibrillation independent of muscarinic receptor activation

Cardiovascular Research

Volumn 91, Issue 3, 2011, Pages 437-446

  Brack, Kieran E ^a   Coote, John H ^b   Ng, G André ^a,c  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c GLENFIELD HOSPITAL   (United Kingdom)

Author keywords

Acetylcholine; Nitric oxide; Vagal stimulation; Ventricular Fibrillation

Indexed keywords

4,5 DIAMINOFLUORESCEIN DIACETATE; ACETYLCHOLINE; ATROPINE; HEXAMETHONIUM; MUSCARINIC RECEPTOR; NITRIC OXIDE; OCTOXINOL; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIARRHYTHMIC ACTIVITY; ARTERY ENDOTHELIUM; ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; EVENT RELATED POTENTIAL; EXPERIMENTAL RABBIT; GANGLION BLOCK; HEART VENTRICLE FIBRILLATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; VAGUS NERVE STIMULATION; VENTRICULAR FIBRILLATION THRESHOLD;

ACETYLCHOLINE; ANIMALS; ENDOTHELIUM, VASCULAR; GANGLIONIC BLOCKERS; HEART RATE; HEART VENTRICLES; MALE; MUSCARINIC ANTAGONISTS; MYOCARDIUM; NITRERGIC NEURONS; NITRIC OXIDE; PARASYMPATHETIC FIBERS, POSTGANGLIONIC; PEPTIDE FRAGMENTS; RABBITS; RECEPTORS, MUSCARINIC; REFRACTORY PERIOD, ELECTROPHYSIOLOGICAL; TIME FACTORS; VAGUS NERVE; VAGUS NERVE STIMULATION; VASOACTIVE INTESTINAL PEPTIDE; VENTRICULAR FIBRILLATION; VENTRICULAR FUNCTION;

EID: 79960776522     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr105     Document Type: Article

References (51)

1. Nolan J, Batin PD, Andrews R, Lindsay SJ, Brooksby P, Mullen H et al. Prospective study of heart rate variability and mortality in chronic heart failure-results of the United Kingdom heart failure evaluation and assessment of risk trial (UK-Heart). Circulation 1998;98:1510-1516.
2. La Rovere MT, Pinna GD, Maestri R, Robbi E, Caporotondi A, Guazzotti G et al. Prognostic implications of baroreflex sensitivity in heart failure patients in the betablocking era. J Am Coll Cardiol 2009;53:193-199.
3. La Rovere MT, Bigger JT, Marcus FI, Mortara A, Schwartz PJ. Baroreflex sensitivity and heart rate variability in prediction of total cardiac mortality after myocardial infarction. Lancet 1998;351:478-484.
4. Schwartz PJ. The autonomic nervous system and sudden death. Eur Heart J 1998;19: F72-F80.
5. Higgins CB, Vatner SF, Braunwald E. Parasympathetic control of the heart. Pharmacol Rev 1973;25:119-124.
6. Loffelholtz K, Pappano AJ. The parasympathetic neuroeffector junction of the heart. Pharmacol Rev 1985;37:1-24.
7. Casedi B. Vagal control of myocardial contractility in humans. Exp Physiol 2001;86: 817-823.
8. Eidenbrodt. Uber herzeizung und ihr verhaeltins zum blutdruck. Akademie der Wissenschaften (Vienna). Sitzungsberichte 1895;38:345-359.
9. Vanoli E, De Ferrari GM, Strama-Badiale M, Hull SS, Foreman RD, Schwartz PJ. Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardium. Circ Res 1991;68:1471-1481.
10. Ng GA, Brack KE, Coote JH. Effects of direct sympathetic and vagus nerve stimulation on the physiology of the whole heart - a novel model of isolated Langendorff perfused rabbit heart with intact autonomic nerves. Exp Physiol 2001;86:319-329.
11. Ng GA, Brack KE, Patel VH, Coote JH. Autonomic modulation of electrical restitution alternans and ventricular fibrillation initiation in the isolated heart. Cardiovasc Res 2007;73:750-760.
12. Weiss JN, Chen PS, Qu Z, Karagueuzian HS, Lin SF, Garfinkel A. Electrical restitution and cardiac fibrillation. J Cardiovasc Electrophysiol 2002;13:292-295.
13. Brack KE, Patel VH, Coote JH, Ng GA. Nitric oxide mediate the vagal protective effect on ventricular fibrillation via effects on action potential duration in the isolated rabbit hear. J Physiol 2007;583:695-704.
14. Brack KE, Patel VH, Mantravadi R, Coote JH, Ng GA. Direct evidence of nitric oxide release from neuronal nitric oxide synthase activation in the left ventricle as a result of cervical vagus nerve stimulation. J Physiol 2009;587:3045-3054.
15. Herring N, Danson EJ, Paterson DJ. Cholinergic control of heart rate by nitric oxide is site specific. News Physiol Sci 2002;17:202-206.
16. Henning RJ, Sawmiler DR. Vasoactive intestinal peptide: cardiovascular effects. Cardiovasc Res 2001;49:27-37.
17. Fahrenkrug J. VIP and autonomic neurotransmission. Pharmac Ther 1989;41:515-545.
18. Berthoud HR, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Auton Neurosci 2000;85:1-17.
19. Hoover DB, Shepherd AV, Southerland EM, Armour JA, Ardell JL. Neurochemical diversity of afferent neurones that transduce sensory signals from dog ventricular myocardium. Autonom Neurosci 2008;414:38-45.
20. Patel VH, Brack KE, Coote JH, Ng GA. A novel method of measuring nitric oxidedependent fluorescence using 4,5-diamiofluorescein (DAF-2) in the isolated Langendorff-perfused rabbit heart. Pflugers Arch 2008;456:635-645.
21. Hogan K, Markos F. Vasoactive intestinal polypeptide receptor antagonism enhances the vagally induced increase in cardiac interval of the rat atrium in vitro. Exp Physiol 2006;91:641-646.
22. Hassanabad ZF, Furman BL, Parratt JR, Aughey E. Coronary endothelium dysfunction increases the severity of ischaemia-induced ventricular arrhythmia in rat isolated perfused hearts. Basic Res Cardiol 1998;93:241-249.
23. Li K, Rouleau JL, Andries LJ, Brutsaert DL. Effect of dysfunctional vascular endothelium on myocardial performance in isolated papillary muscles. Circ Res 1993;72: 768-777.
24. Evans CH, Murray JG. Histological and functional studies on the fibre composition of the vagus nerve in the rabbit. J Anat 1954;88:320-337.
25. Jumrussirikul P, Dinerman J, Dawson TM, Dawson VL, Ekelund U, Georgakopoulos D et al. Interaction between neuronal nitric oxide synthase and inhibitory G protein activity in heart rate regulation in conscious mice. J Clin Invest 1998;102:1279-1285.
26. Patel VH, Brack KE, Kundu S, Coote JH, Ng GA. The effect of nitric oxide on electrical restitution and ventricular fibrillation in the isolated rabbit heart: mechanism underlying the antifibrillatory effects of vagus nerve activity. Eur Heart J 2004; 25(Supp. 1):68. [abstract].
27. Ulphani JS, Cain JH, Inderyas F, Gordon D, Gikas PV, Shade G et al. Quantitative analysis of parasympathetic innervations of the porcine heart. Heart Rhythm 2010;7: 1113-1119.
28. Cersosimo RO, Bartuluchi M, De Los Santos C, Benovehi I, Pomata H, Caraballo RH. Vagus nerve stimulation: effectiveness and tolerability in patients with epileptic encephaolopathies. Childs Ner Syst 2011;27:787-792.
29. Zheng C, Li M, Imagaki M, Kawada T, Sumagawa K, Sugimachi M. Vagal stimulation markedly suppresses arrhythmia in conscious rats with chronic heart failure after myocardial. Conf Proc IEEE Eng Med Biol Soc 2005;7:7072-7075.
30. 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.
31. Schwartz PJ, De Ferrari GM, Sanzo A, Landolina M, Rordorff R, Raineri C et al. Long term vagal stimulation in patients with advanced heart failure: first experience in man. Eur J Heart Fail 2008;10:884-891.
32. De Ferrari G, Crijins HJGM, Borggrefe M, Milasinovic G, Smid J, Zabel M et al. Chronic vagus nerve stimulation: a new and promising therapeutic approach for chronic heart failure. Eur Heart J 2011;32:847-855.
33. Shvilkin A, Danilo P, Chevalier P, Chang F, Cohen IS, Rosen MR. Vagal released vasoactive intestinal peptide can promote vagaotonic tachycardia in the isolated innervated rat heart. Cardiovasc Res 1994;28:1769-1773.
34. Feliciano L, Henning RJ. Vagal nerve stimulation during muscarinic and beta-adrenergic blockade causes significant coronary artery dilation. JANS 1998;68:78-88.
35. Murthy KS, Teng B, Jin J, Makhlouf GM. G protein-dependent activation of smooth muscle eNOS via natriuretic peptide clearance receptor. AJP 1998;275: C1409-C1416.
36. Dvorakova M, Lips KS, Bruggmann D, Slavikova J, Kuncova J, Kummer W. Developmental changes in the expression of nicotinic acetylcholine receptor a-subunits in the rat heart. Cell Tissue Res 2005;319:201-209
37. Haberberger RV, Henrich M, Lips KS, KummerW. Nicotinic receptor alpha7-subunits are coupled to the stimulation of nitric oxide synthase in rate dorsal root ganglion neurones. Histochem Cell Biol 2003;120:173-181.
38. Paz Y, Frolkis I, Pevni D, Shapira I, Yuhas Y, Iaina A et al. Effect of tumor necrosis factor-alpha on endothelium and inducible nitric oxide synthase messenger ribonucleic acid expression and nitric oxide synthesis in ischemic and nonischemic isolated rat heart. J Am Coll Cardiol 2003;42:1299-1305.
39. Massion PB, Dessy C, Desjarins F, Palet M, Havaux X, Belge C et al. Cardiomyocyte-restricted overexpression of endothelial nitric oxide (NOS3) attenuates beta-adrenergic stimulation and reinforces vagal inhibition of cardiac contraction. Circulation 2004;110:2666-2672.
40. Miethke A, Feussner M, Planitzer G, Richter H, Gutsmann M, Gossrau R. Localization of NOS-1 in the sarcolemma region of a subpopulation of atrial cardiomyocytes including myoendocrine cells and NOS-3 in vascular and endocardial endothelial cells of the rat heart. Acta Histochem 2003;105:43-55.
41. Sosunov AA, Hassell CJ, Loesch A, Turmaine M, Burnstock G. Ultrastructural investigation of nitric oxide synthase-immunoreactive nerve associated with coronary blood vessels of rat guinea-pig. Cell Tissue Res 1995;280:575-582.
42. Singh S, Gray T, Wurster RD. Nitric oxide and carbon monoxide synthesizing enzymes and soluble guanylyl cyclise within neurones of human cardiac ganglia. Auton Neurosci 2009;142:93-98.
43. Richardson RJ, Grkovic I, Anderson CR. Immunohistochemical analysis of intracardiac ganglia of the rat heart. Cell Tissue Res 2003;314:337-350.
44. Tobin M, Kahonen M, Braund P, Nieminen T, Hajat C, Tomaszewski M et al. Gender and effects of a common genetic variant in the NOS1 regulator NOS1AP on cardiac repolarization in 3761 individuals from two independent populations. Int J Epidemiol 2008;37:1132-1141.
45. Chang KC, Bartg AS, Sasano T, Kizana E, Kashiwakura Y, Zhang Y et al. CAPON modulates cardiac repolarization via neuronal nitric oxide synthase signalling in the heart. PNAS 2008;105:4477-4482.
46. Arking DE, Pfeufer A, Post W, Kao WH, Newton-Cheh C, Ikeda M et al. A common genetic variant in the NOS1 regulator NOS1AP modulates cardiac repolarization. Nat Genet 2006;38:644-651.
47. Crottie L, Monti MC, Insolia R, Peljto A, Goosen A, Brink PA et al. NOS1AP is a genetic modifier of long-QT syndrome. Circulation 2009;120:1657-1663.
48. Kollman BS, Verrier RL, Lown B. The effect of vagus nerve stimulation upon vulnerability of the canine ventricle: role of sympathetic-parasympathetic interactions. Circulation 1975;52:578-585.
49. Burton FL, Cobbe SM. Effect of sustained stretch on dispersion of ventricular fibrillation intervals in normal rabbit hearts. Cardiovasc Res 1998;39:351-359.
50. Kent KM, Smith ER, Redwood DR, Epstein SE. Electrical stability of acutely ischemic myocardium: influences of heart rate and vagal stimulation. Circ 1973;47:291-298.
51. Mantravadi R, Gabris B, Liu T, Choi BR, de Groat WC, Ng GA et al. Autonomic nerve stimulation reverses ventricular repolarization sequence in Rabbit hearts. Circ Res 2007;100:e72-e80.