Vagus nerve stimulation mitigates intrinsic cardiac neuronal and adverse myocyte remodeling postmyocardial infarction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 309, Issue 7, 2015, Pages H1198-H1206

  Beaumont, Eric ^a   Southerland, Elizabeth M ^a   Hardwick, Jean C ^b   Wright, Gary L ^a   Ryan, Shannon ^a   Li, Ying ^a   KenKnight, Bruce H ^c   Andrew Armour, J ^a,d   Ardell, Jeffrey L ^a,d  

^a East Tennessee State University   (United States)

^b ITHACA COLLEGE   (United States)

^c Cyberonics Inc   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autonomic regulation therapy; Guinea pig; Intrinsic cardiac nervous system; Myocardial infarction; Vagus nerve stimulation

Indexed keywords

NORADRENALIN; PROTEIN BAX;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ECHOCARDIOGRAPHY; EVOKED RESPONSE; GLYCOGENOLYSIS; GUINEA PIG; HEART FUNCTION; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART PROTECTION; INTRINSIC CARDIAC NERVOUS SYSTEM; MALE; MEMBRANE STEADY POTENTIAL; NERVOUS SYSTEM; NONHUMAN; POSTMYOCARDIAL INFARCTION; PRIORITY JOURNAL; SYNAPTIC EFFICACY; VAGUS NERVE STIMULATION; WESTERN BLOTTING; ANIMAL; AUTONOMIC NERVOUS SYSTEM; CARDIAC MUSCLE CELL; HEART; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; INNERVATION; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; BCL-2-ASSOCIATED X PROTEIN; EVOKED POTENTIALS; GLYCOGENOLYSIS; GUINEA PIGS; HEART; MEMBRANE POTENTIALS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEURONAL PLASTICITY; NOREPINEPHRINE; STROKE VOLUME; SYNAPTIC TRANSMISSION; VAGUS NERVE STIMULATION; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT;

EID: 84943153122     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00393.2015     Document Type: Article

References (75)

1. Ahonen A, Harkonen M, Juntunen J, Kormano M, Penttila A. Effects of myocardial infarction on adrenergic nerves of the rat heart muscle, a histochemical study. Acta Physiol Scand 93: 336-344, 1975.
2. Ajijola OA, Yagishita D, Patel KJ, Vaseghi M, Zhou W, Yamakawa K, So E, Lux RL, Mahajan A, Shivkumar K. Focal myocardial infarction induces global remodeling of cardiac sympathetic innervation: neural remodeling in a spatial context. Am J Physiol Heart Circ Physiol 305: H1031-H1040, 2013.
3. Antoni ML, Boden H, Hoogslag GE, Ewe SH, Auger D, Holman ER, van der Wall EE, Schalij MJ, Bax JJ, Delgado V. Prevalence of dyssynchrony and relation with long-term outcome in patients after acute myocardial infarction. Am J Cardiol 108: 1689-1696, 2011.
4. Ardell JL. Intrathoracic neuronal regulation of cardiac function In: Basic and Clinical Neurocardiology, edited by Armour JAArdell JL. New York: Oxford University Press, 2004, p. 118-152.
5. Ardell JL, Cardinal R, Vermeulen M, Armour JA. Dorsal spinal cord stimulation obtunds the capacity of intrathoracic extracardiac neurons to transduce myocardial ischemia. Am J Physiol Regul Integr Comp Physiol 297: R470-R477, 2009.
6. Armour JA. Myocardial ischaemia and the cardiac nervous system. Cardiovasc Res 41: 41-54, 1999.
7. Armour JA. Potential clinical relevance of the 'little brain' on the mammalian heart. Exp Physiol 93: 165-176, 2008.
8. Armour JA, Kember G. Cardiac sensory neurons. In: Basic and Clinical Neurocardiology, edited by Armour JA and Ardell JL. New York: Oxford University Press, 2004, p. 79-117.
9. Armour JA, Linderoth B, Arora RC, DeJongste MJ, Ardell JL, Kingma JG Jr, Hill M, Foreman RD. Long-term modulation of the intrinsic cardiac nervous system by spinal cord neurons in normal and ischaemic hearts. Auton Neurosci 95: 71-79, 2002.
10. Beaumont E, Salavatian S, Southerland EM, Vinet A, Jacquemet V, Armour JA, Ardell JL. Network interactions within the canine intrinsic cardiac nervous system: implications for reflex control of regional cardiac function. J Physiol 591: 4515-4533, 2013.
11. Billman GE. A comprehensive review and analysis of 25 years of data from an in vivo canine model of sudden cardiac death: implications for future anti-arrhythmic drug development. Pharmacol Ther 111: 808-835, 2006.
12. Bonaz B, Picq C, Sinniger V, Mayol JF, Clarencon D. Vagus nerve stimulation: from epilepsy to the cholinergic anti-inflammatory pathway. Neurogastroenterol Motil 25: 208-221, 2013.
13. Brack KE, Winter J, Ng GA. Mechanisms underlying the autonomic modulation of ventricular fibrillation initiation-tentative prophylactic properties of vagus nerve stimulation on malignant arrhythmias in heart failure. Heart Fail Rev 18: 389-408, 2013.
14. Buckley U, Shivkumar K, Ardell JL. Autonomic regulation therapy in heart failure. Curr Heart Fail Rep 12: 284-293, 2015.
15. Calvillo L, 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 58: 500-507, 2011.
16. Cardinal R, Ardell JL, Linderoth B, Vermeulen M, Foreman RD, Armour JA. Spinal cord activation differentially modulates ischaemic electrical responses to different stressors in canine ventricles. Auton Neurosci 111: 37-47, 2004.
17. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 95: 957-970, 2004.
18. Dawson TA, Li D, Woodward T, Barber Z, Wang L, Paterson DJ. Cardiac cholinergic NO-cGMP signaling following acute myocardial infarction and nNOS gene transfer. Am J Physiol Heart Circ Physiol 295: H990-H998, 2008.
19. De Ferrari GM. Vagal stimulation in heart failure. J Cardiovasc Transl Res 7: 310-320, 2014.
20. De Ferrari GM, Crijns HJ, Borggrefe M, Milasinovic G, Smid J, Zabel M, Gavazzi A, Sanzo A, Dennert R, Kuschyk J, Raspopovic S, Klein H, Swedberg K, Schwartz PJ; CardioFit Multicenter Trial Investigators. Chronic vagus nerve stimulation: a new and promising therapeutic approach for chronic heart failure. Eur Heart J 32: 847-855, 2011.
21. De Ferrari GM, Tuinenburg AE, Ruble S, Brugada J, Klein H, Butter C, Wright DJ, Schubert B, Solomon S, Meyer S, Stein K, Ramuzat A, Zannad F. Rationale and study design of the NEuroCardiac TherApy foR Heart Failure Study: NECTAR-HF. Eur J Heart Fail 16: 692-699, 2014.
22. De Ferrari GM, Vanoli E, Schwartz PJ. Cardiac vagal activity, myocardial ischemia and sudden death. In: Cardiac Electrophysiology: From Cell to Bedside (2nd ed.), edited by Zipes DP and Jalifa J. Philadelphia, PA: WB Sanders, 1995, p. 422-434.
23. Dell'Italia LJ. Translational success stories: angiotensin receptor 1 antagonists in heart failure. Circ Res 109: 437-452, 2011.
24. Dobaczewski M, de Haan JJ, Frangogiannis NG. The extracellular matrix modulates fibroblast phenotype and function in the infarcted myocardium. J Cardiovasc Transl Res 5: 837-847, 2012.
25. Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol 48: 504-511, 2010.
26. Florea VG, Cohn JN. The autonomic nervous system and heart failure. Circ Res 114: 1815-1826, 2014.
27. Foreman RD. Mechanisms of cardiac pain. Annu Rev Physiol 61: 143-167, 1999.
28. Fu LW, Longhurst JC. Regulation of cardiac afferent excitability in ischemia. Handb Exp Pharmacol 194: 185-225, 2009.
29. Fukuda K, Kanazawa H, Aizawa Y, Ardell JL, Shivkumar K. Cardiac innervation and sudden cardiac death. Circ Res 116: 2005-2019, 2015.
30. Gibbons DD, Southerland EM, Hoover DB, Beaumont E, Armour JA, Ardell JL. Neuromodulation targets intrinsic cardiac neurons to attenuate neuronally mediated atrial arrhythmias. Am J Physiol Regul Integr Comp Physiol 302: R357-R364, 2012.
31. Girasole AE, Palmer CP, Corrado SL, Marie Southerland E, Ardell JL, Hardwick JC. Angiotensin II potentiates adrenergic and muscarinic modulation of guinea pig intracardiac neurons. Am J Physiol Regul Integr Comp Physiol 301: R1391-R1399, 2011.
32. Gonzalez GE, Seropian IM, Krieger ML, Palleiro J, Lopez Verrilli MA, Gironacci MM, Cavallero S, Wilensky L, Tomasi VH, Gelpi RJ, Morales C. Effect of early versus late AT(1) receptor blockade with losartan on postmyocardial infarction ventricular remodeling in rabbits. Am J Physiol Heart Circ Physiol 297: H375-H386, 2009.
33. Hankes GH, Ardell JL, Tallaj J, Wei CC, Aban I, Holland M, Rynders P, Dillon R, Cardinal R, Hoover DB, Armour JA, Husain A, Dell'Italia LJ. Beta1-Adrenoceptor blockade mitigates excessive norepinephrine release into cardiac interstitium in mitral regurgitation in dog. Am J Physiol Heart Circ Physiol 291: H147-H151, 2006.
34. Hardwick JC, Baran CN, Southerland EM, Ardell JL. Remodeling of the guinea pig intrinsic cardiac plexus with chronic pressure overload. Am J Physiol Regul Integr Comp Physiol 297: R859-R866, 2009.
35. Hardwick JC, Mawe GM, Parsons RL. Evidence for afferent fiber innervation of parasympathetic neurons of the guinea-pig cardiac ganglion. J Auton Nerv Syst 53: 166-174, 1995.
36. Hardwick JC, Ryan SE, Beaumont E, Ardell JL, Southerland EM. Dynamic remodeling of the guinea pig intrinsic cardiac plexus induced by chronic myocardial infarction. Auton Neurosci 181: 4-12, 2014.
37. Hardwick JC, Ryan SE, Powers EN, Southerland EM, Ardell JL. Angiotensin receptors alter myocardial infarction-induced remodeling of the guinea pig cardiac plexus. Am J Physiol Regul Integr Comp Physiol 309: R179-R188, 2015.
38. Hardwick JC, Southerland EM, Ardell JL. Chronic myocardial infarction induces phenotypic and functional remodeling in the guinea pig cardiac plexus. Am J Physiol Regul Integr Comp Physiol 295: R1926-R1933, 2008.
39. Hardwick JC, Southerland EM, Girasole AE, Ryan SE, Negrotto S, Ardell JL. Remodeling of intrinsic cardiac neurons: effects of betaadrenergic receptor blockade in guinea pig models of chronic heart disease. Am J Physiol Regul Integr Comp Physiol 303: R950-R958, 2012.
40. Henning SL, Wambolt RB, Schonekess BO, Lopaschuk GD, Allard MF. Contribution of glycogen to aerobic myocardial glucose utilization. Circulation 93: 1549-1555, 1996.
41. Hoover DB, Ganote CE, Ferguson SM, Blakely RD, Parsons RL. Localization of cholinergic innervation in guinea pig heart by immunohistochemistry for high-affinity choline transporters. Cardiovasc Res 62: 112-121, 2004.
42. Hopkins DA, Macdonald SE, Murphy DA, Armour JA. Pathology of intrinsic cardiac neurons from ischemic human hearts. Anat Rec 259: 424-436, 2000.
43. 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 579: 2111-2118, 2005.
44. Katare RG, Ando M, Kakinuma Y, Arikawa M, Handa T, Yamasaki F, Sato T. Vagal nerve stimulation prevents reperfusion injury through inhibition of opening of mitochondrial permeability transition pore independent of the bradycardiac effect. J Thorac Cardiovasc Surg 137: 223-231, 2009.
45. Kember G, Ardell JL, Armour JA, Zamir M. Vagal nerve stimulation therapy: what is being stimulated? PLoS One 9: e114498, 2014.
46. Kember G, Armour JA, Zamir M. Dynamic neural networking as a basis for plasticity in the control of heart rate. J Theor Biol 317: 39-46, 2013.
47. Kember G, Armour JA, Zamir M. Neural control hierarchy of the heart has not evolved to deal with myocardial ischemia. Physiol Genomics 45: 638-644, 2013.
48. Lefkowitz RJ. A brief history of G-protein coupled receptors (Nobel lecture). Angew Chem Int Ed Engl 52: 6366-6378, 2013.
49. Levy MN. Sympathetic-parasympathetic interactions in the heart. Circ Res 29: 437-445, 1971.
50. Levy MN, Ng M, Martin P, Zieske H, Rogoff T. Sympathetic and parasympathetic interactions upon the left ventricle of the dog. Circ Res 19: 5-10, 1966.
51. 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 109: 120-124, 2004.
52. Mawe GM, Talmage EK, Lee KP, Parsons RL. Expression of choline acetyltransferase immunoreactivity in guinea pig cardiac ganglia. Cell Tissue Res 285: 281-286, 1996.
53. McAllen RM, Salo LM, Paton JF, Pickering AE. Processing of central and reflex vagal drives by rat cardiac ganglion neurones: an intracellular analysis. J Physiol 589: 5801-5818, 2011.
54. McGuirt AS, Schmacht DC, Ardell JL. Autonomic interactions for control of atrial rate are maintained after SA nodal parasympathectomy. Am J Physiol Heart Circ Physiol 272: H2525-H2533, 1997.
55. Mollema SA, Liem SS, Suffoletto MS, Bleeker GB, van der Hoeven BL, van de Veire NR, Boersma E, Holman ER, van der Wall EE, Schalij MJ, Gorcsan J, 3rd, Bax JJ. Left ventricular dyssynchrony acutely after myocardial infarction predicts left ventricular remodeling. J Am Coll Cardiol 50: 1532-1540, 2007.
56. Murphy E. Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection. Circ Res 94: 7-16, 2004.
57. Premchand RK, Sharma K, Mittal S, Monteiro R, Dixit S, Libbus I, DiCarlo LA, Ardell JL, Rector TS, Amurthur B, KenKnight BH, Anand IS. Autonomic regulation therapy via left or right cervical vagus nerve stimulation in patients with chronic heart failure: results of the ANTHEM-HF Trial. J Card Fail 20: 808-816, 2014.
58. Randall DC, Brown DR, McGuirt AS, Thompson GW, Armour JA, Ardell JL. Interactions within the intrinsic cardiac nervous system contribute to chronotropic regulation. Am J Physiol Regul Integr Comp Physiol 285: R1066-R1075, 2003.
59. Schwartz PJ. Vagal stimulation for the treatment of heart failure: a translational success story. Heart 98: 1687-1689, 2012.
60. Shen MJ, Zipes DP. Interventional and device-based autonomic modulation in heart failure. Heart Fail Clin 11: 337-348, 2015.
61. Shen MJ, Zipes DP. Role of the autonomic nervous system in modulating cardiac arrhythmias. Circ Res 114: 1004-1021, 2014.
62. Shinlapawittayatorn K, Chinda K, Palee S, Surinkaew S, Thunsiri K, Weerateerangkul P, Chattipakorn S, KenKnight BH, Chattipakorn N. Low-amplitude, left vagus nerve stimulation significantly attenuates ventricular dysfunction and infarct size through prevention of mitochondrial dysfunction during acute ischemia-reperfusion injury. Heart Rhythm 10: 1700-1707, 2013.
63. Southerland EM, Gibbons DD, Smith SB, Sipe A, Williams CA, Beaumont E, Armour JA, Foreman RD, Ardell JL. Activated cranial cervical cord neurons affect left ventricular infarct size and the potential for sudden cardiac death. Auton Neurosci 169: 34-42, 2012.
64. Southerland EM, Milhorn DM, Foreman RD, Linderoth B, DeJongste MJ, Armour JA, Subramanian V, Singh M, Singh K, Ardell JL. Preemptive, but not reactive, spinal cord stimulation mitigates transient ischemia-induced myocardial infarction via cardiac adrenergic neurons. Am J Physiol Heart Circ Physiol 292: H311-H317, 2007.
65. Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85: 1093-1129, 2005.
66. Stanley WC, Sabbah HN. Metabolic therapy for ischemic heart disease: the rationale for inhibition of fatty acid oxidation. Heart Fail Rev 10: 275-279, 2005.
67. Tong H, Imahashi K, Steenbergen C, Murphy E. Phosphorylation of glycogen synthase kinase-3beta during preconditioning through a phosphatidylinositol-3-kinase-dependent pathway is cardioprotective. Circ Res 90: 377-379, 2002.
68. Wang HJ, Wang W, Cornish KG, Rozanski GJ, Zucker IH. Cardiac sympathetic afferent denervation attenuates cardiac remodeling and improves cardiovascular dysfunction in rats with heart failure. Hypertension 64: 745-755, 2014.
69. Wang Q, Cheng Y, Xue FS, Yuan YJ, Xiong J, Li RP, Liao X, Liu JH. Postconditioning with vagal stimulation attenuates local and systemic inflammatory responses to myocardial ischemia reperfusion injury in rats. Inflamm Res 61: 1273-1282, 2012.
70. Wang Z, Yu L, Chen M, Wang S, Jiang H. Transcutaneous electrical stimulation of auricular branch of vagus nerve: a noninvasive therapeutic approach for post-ischemic heart failure. Int J Cardiol 177: 676-677, 2014.
71. Wang Z, Yu L, Wang S, Huang B, Liao K, Saren G, Tan T, Jiang H. Chronic intermittent low-level transcutaneous electrical stimulation of auricular branch of vagus nerve improves left ventricular remodeling in conscious dogs with healed myocardial infarction. Circ Heart Fail 7: 1014-1021, 2014.
72. Woodbury DM, Woodbury JW. Effects of vagal stimulation on experimentally induced seizures in rats. Epilepsia 31, Suppl 2: S7-S19, 1990.
73. Wu J, Chen P, Li Y, Ardell C, Der T, Shohet R, Chen M, Wright GL. HIF-1alpha in heart: protective mechanisms. Am J Physiol Heart Circ Physiol 305: H821-H828, 2013.
74. Zhang Y, Mazgalev TN. Arrhythmias and vagus nerve stimulation. Heart Fail Rev 16: 147-161, 2011.
75. Zucker IH, Patel KP, Schultz HD. Neurohumoral stimulation. Heart Fail Clin 8: 87-99, 2012.