Decreased adrenoceptor stimulation in heart failure rats reduces NGF expression by cardiac parasympathetic neurons

Autonomic Neuroscience: Basic and Clinical

Volumn 181, Issue 1, 2014, Pages 13-20

  Hasan, Wohaib ^a   Smith, Peter G ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Adrenergic receptor; Autonomic; Cardiac ganglion; Heart failure; Nerve growth factor; Parasympathetic

Indexed keywords

ADRENERGIC RECEPTOR; ISOPRENALINE; MESSENGER RNA; NERVE GROWTH FACTOR; NORADRENALIN; PHENYLEPHRINE; VASOACTIVE INTESTINAL POLYPEPTIDE; VESICULAR ACETYLCHOLINE TRANSPORTER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIAC PARASYMPATHETIC NEURON; CONTROLLED STUDY; CORONARY ARTERY LIGATION; GANGLION; HEART FAILURE; HEART GANGLION; HEART HEMODYNAMICS; HEART PERFORMANCE; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE CELL CULTURE; NEUROCHEMISTRY; NONHUMAN; PARASYMPATHETIC NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; SHAM PROCEDURE; SYMPATHETIC NERVE; SYMPATHETIC NERVE CELL;

ADRENERGIC RECEPTOR; AUTONOMIC; CARDIAC GANGLION; HEART FAILURE; NERVE GROWTH FACTOR; PARASYMPATHETIC;

ADRENERGIC ALPHA-AGONISTS; ADRENERGIC ANTAGONISTS; ADRENERGIC BETA-AGONISTS; ANIMALS; CELLS, CULTURED; HEART; HEART FAILURE; ISOPROTERENOL; MALE; NERVE GROWTH FACTOR; NERVE GROWTH FACTORS; NEURONS; PARASYMPATHETIC NERVOUS SYSTEM; PHENYLEPHRINE; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC; RNA, MESSENGER; TIME FACTORS; VASOACTIVE INTESTINAL PEPTIDE; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 84893935660     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2013.11.001     Document Type: Article

References (65)

1. Al-Shawi R., Hafner A., Olsen J., Chun S., Raza S., Thrasivoulou C., Lovestone S., Killick R., Simons P., Cowen T. Neurotoxic and neurotrophic roles of proNGF and the receptor sortilin in the adult and ageing nervous system. Eur. J. Neurosci. 2008, 27:2103-2114.
2. Azevedo E.R., Parker J.D. Parasympathetic control of cardiac sympathetic activity: normal ventricular function versus congestive heart failure. Circulation 1999, 100:274-279.
3. Backs J., Haunstetter A., Gerber S.H., Metz J., Borst M.M., Strasser R.H., Kubler W., Haass M. The neuronal norepinephrine transporter in experimental heart failure: evidence for a posttranscriptional downregulation. J. Mol. Cell. Cardiol. 2001, 33:461-472.
4. Bibevski S., Dunlap M.E. Evidence for impaired vagus nerve activity in heart failure. Heart Fail. Rev. 2011, 16:129-135.
5. Bierl M.A., Isaacson L.G. Increased NGF proforms in aged sympathetic neurons and their targets. Neurobiol. Aging 2007, 28:122-134.
6. Bierl M.A., Jones E.E., Crutcher K.A., Isaacson L.G. 'Mature' nerve growth factor is a minor species in most peripheral tissues. Neurosci. Lett. 2005, 380:133-137.
7. Binkley P.F., Nunziata E., Haas G.J., Nelson S.D., Cody R.J. Parasympathetic withdrawal is an integral component of autonomic imbalance in congestive heart failure: demonstration in human subjects and verification in a paced canine model of ventricular failure. J. Am. Coll. Cardiol. 1991, 18:464-472.
8. Bohm M., La Rosee K., Schwinger R.H., Erdmann E. Evidence for reduction of norepinephrine uptake sites in the failing human heart. J. Am. Coll. Cardiol. 1995, 25:146-153.
9. Carswell S., Hoffman E.K., Clopton-Hartpence K., Wilcox H.M., Lewis M.E. Induction of NGF by isoproterenol, 4-methylcatechol and serum occurs by three distinct mechanisms. Brain Res. Mol. Brain Res. 1992, 15:145-150.
10. Clarke G.L., Bhattacherjee A., Tague S.E., Hasan W., Smith P.G. β-Adrenoceptor blockers increase cardiac sympathetic innervation by inhibiting autoreceptor suppression of axon growth. J. Neurosci. 2010, 30:12446-12454.
11. Colangelo A.M., Johnson P.F., Mocchetti I. beta-Adrenergic receptor-induced activation of nerve growth factor gene transcription in rat cerebral cortex involves CCAAT/enhancer-binding protein delta. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10920-10925.
12. Colangelo A.M., Mallei A., Johnson P.F., Mocchetti I. Synergistic effect of dexamethasone and beta-adrenergic receptor agonists on the nerve growth factor gene transcription. Brain Res. Mol. Brain Res. 2004, 124:97-104.
13. Culmsee C., Semkova I., Krieglstein J. NGF mediates the neuroprotective effect of the beta2-adrenoceptor agonist clenbuterol in vitro and in vivo: evidence from an NGF-antisense study. Neurochem. Int. 1999, 35:47-57.
14. Dal Toso R., De Bernardi M.A., Brooker G., Costa E., Mocchetti I. Beta adrenergic and prostaglandin receptor activation increases nerve growth factor mRNA content in C6-2B rat astrocytoma cells. J. Pharmacol. Exp. Ther. 1988, 246:1190-1193.
15. Deneke T., Chaar H., de Groot J.R., Wilde A.A., Lawo T., Mundig J., Bosche L., Mugge A., Grewe P.H. Shift in the pattern of autonomic atrial innervation in subjects with persistent atrial fibrillation. Heart Rhythm. 2011, 8:1357-1363.
16. Donohue T., Smith P. Parasympathetic withdrawal in heart failure involves reduced vagal prejunctional inhibition of sympathetic nerves. Experimental Biology Abstracts 2009.
17. Du X.J., Dart A.M., Riemersma R.A., Oliver M.F. Failure of the cholinergic modulation of norepinephrine release during acute myocardial ischemia in the rat. Circ. Res. 1990, 66:950-956.
18. Dunlap M.E., Bibevski S., Rosenberry T.L., Ernsberger P. Mechanisms of altered vagal control in heart failure: influence of muscarinic receptors and acetylcholinesterase activity. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H1632-H1640.
19. Eckberg D.L., Drabinsky M., Braunwald E. Defective cardiac parasympathetic control in patients with heart disease. N. Engl. J. Med. 1971, 285:877-883.
20. Furukawa Y., Tomioka N., Sato W., Satoyoshi E., Hayashi K., Furukawa S. Catecholamines increase nerve growth factor mRNA content in both mouse astroglial cells and fibroblast cells. FEBS Lett. 1989, 247:463-467.
21. Hasan W., Smith P.G. Nerve growth factor expression in parasympathetic neurons: regulation by sympathetic innervation. Eur. J. Neurosci. 2000, 12:4391-4397.
22. Hasan W., Smith P.G. Modulation of rat parasympathetic cardiac ganglion phenotype and NGF synthesis by adrenergic nerves. Auton. Neurosci. 2009, 145:17-26.
23. Hasan W., Jama A., Donohue T., Wernli G., Onyszchuk G., Al-Hafez B., Bilgen M., Smith P.G. Sympathetic hyperinnervation and inflammatory cell NGF synthesis following myocardial infarction in rats. Brain Res. 2006, 1124:142-154.
24. Hayes V.Y., Isackson P.J., Fabrazzo M., Follesa P., Mocchetti I. Induction of nerve growth factor and basic fibroblast growth factor mRNA following clenbuterol: contrasting anatomical and cellular localization. Exp. Neurol. 1995, 132:33-41.
25. Henze M., Hart D., Samarel A., Barakat J., Eckert L., Scrogin K. Persistent alterations in heart rate variability, baroreflex sensitivity, and anxiety-like behaviors during development of heart failure in the rat. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H29-H38.
26. Henze M., Tiniakov R., Samarel A., Holmes E., Scrogin K. Chronic fluoxetine reduces autonomic control of cardiac rhythms in rats with congestive heart failure. Am. J. Physiol. Heart Circ. Physiol. 2013, 304:H444-H454.
27. Hill M.R., Wallick D.W., Mongeon L.R., Martin P.J., Levy M.N. Vasoactive intestinal polypeptide antagonists attenuate vagally induced tachycardia in the anesthetized dog. Am. J. Physiol. 1995, 269:H1467-H1472.
28. Ishibashi H., Umezu M., Jang I.S., Ito Y., Akaike N. Alpha 1-adrenoceptor-activated cation currents in neurones acutely isolated from rat cardiac parasympathetic ganglia. J. Physiol. 2003, 548:111-120.
29. Kanazawa H., Ieda M., Kimura K., Arai T., Kawaguchi-Manabe H., Matsuhashi T., Endo J., Sano M., Kawakami T., Kimura T., Monkawa T., Hayashi M., Iwanami A., Okano H., Okada Y., Ishibashi-Ueda H., Ogawa S., Fukuda K. Heart failure causes cholinergic transdifferentiation of cardiac sympathetic nerves via gp130-signaling cytokines in rodents. J. Clin. Invest. 2010, 120:408-421.
30. Kaye D.M., Vaddadi G., Gruskin S.L., Du X.J., Esler M.D. Reduced myocardial nerve growth factor expression in human and experimental heart failure. Circ. Res. 2000, 86:E80-E84.
31. Kimura K., Kanazawa H., Ieda M., Kawaguchi-Manabe H., Miyake Y., Yagi T., Arai T., Sano M., Fukuda K. Norepinephrine-induced nerve growth factor depletion causes cardiac sympathetic denervation in severe heart failure. Auton. Neurosci. 2010, 156:27-35.
32. Kinugawa T., Dibner-Dunlap M.E. Altered vagal and sympathetic control of heart rate in left ventricular dysfunction and heart failure. Am. J. Physiol. 1995, 268:R310-R316.
33. Kreusser M.M., Buss S.J., Krebs J., Kinscherf R., Metz J., Katus H.A., Haass M., Backs J. Differential expression of cardiac neurotrophic factors and sympathetic nerve ending abnormalities within the failing heart. J. Mol. Cell. Cardiol. 2008, 44:380-387.
34. Kruger C., Kalenka A., Haunstetter A., Schweizer M., Maier C., Ruhle U., Ehmke H., Kubler W., Haass M. Baroreflex sensitivity and heart rate variability in conscious rats with myocardial infarction. Am. J. Physiol. 1997, 273:H2240-H2247.
35. La Rovere M.T., Bigger J.T., Marcus F.I., Mortara A., Schwartz P.J. Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators. Lancet 1998, 351:478-484.
36. Lechat P., Hulot J.S., Escolano S., Mallet A., Leizorovicz A., Werhlen-Grandjean M., Pochmalicki G., Dargie H. Heart rate and cardiac rhythm relationships with bisoprolol benefit in chronic heart failure in CIBIS II Trial. Circulation 2001, 103:1428-1433.
37. Levy M.N. Autonomic interactions in cardiac control. Ann. N. Y. Acad. Sci. 1990, 601:209-221.
38. 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.
39. Liu Y.H., Yang X.P., Nass O., Sabbah H.N., Peterson E., Carretero O.A. Chronic heart failure induced by coronary artery ligation in Lewis inbred rats. Am. J. Physiol. 1997, 272:H722-H727.
40. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods 2001 Dec, 25(4):402-408.
41. Lobos E., Gebhardt C., Kluge A., Spanel-Borowski K. Expression of nerve growth factor (NGF) isoforms in the rat uterus during pregnancy: accumulation of precursor proNGF. Endocrinology 2005, 146:1922-1929.
42. Loiacono R.E., Story D.F. Effect of alpha-adrenoceptor agonists and antagonists on cholinergic transmission in guinea-pig isolated atria. Naunyn Schmiedebergs Arch. Pharmacol. 1986, 334:40-47.
43. Lombardi F., Mortara A. Heart rate variability and cardiac failure. Heart 1998, 80:213-214.
44. Lund D.D., Schmid P.G., Roskoski R. Neurochemical indices of autonomic innervation of heart in different experimental models of heart failure. Adv. Exp. Med. Biol. 1983, 161:179-198.
45. Markos F., Snow H.M. Vagal postganglionic origin of vasoactive intestinal polypeptide (VIP) mediating the vagal tachycardia. Eur. J. Appl. Physiol. 2006, 98:419-422.
46. Mulder P., Barbier S., Chagraoui A., Richard V., Henry J.P., Lallemand F., Renet S., Lerebours G., Mahlberg-Gaudin F., Thuillez C. Long-term heart rate reduction induced by the selective I(f) current inhibitor ivabradine improves left ventricular function and intrinsic myocardial structure in congestive heart failure. Circulation 2004, 109:1674-1679.
47. Ng J., Villuendas R., Cokic I., Schliamser J.E., Gordon D., Koduri H., Benefield B., Simon J., Murthy S.N., Lomasney J.W., Wasserstrom J.A., Goldberger J.J., Aistrup G.L., Arora R. Autonomic remodeling in the left atrium and pulmonary veins in heart failure: creation of a dynamic substrate for atrial fibrillation. Circ. Arrhythm. Electrophysiol. 2011, 4:388-396.
48. Nihei M., Lee J.K., Honjo H., Yasui K., Uzzaman M., Kamiya K., Opthof T., Kodama I. Decreased vagal control over heart rate in rats with right-sided congestive heart failure: downregulation of neuronal nitric oxide synthase. Circ. J. 2005, 69:493-499.
49. Ondicova K., Mravec B. Multilevel interactions between the sympathetic and parasympathetic nervous systems: a minireview. Endocr. Regul. 2010, 44:69-75.
50. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001 May 1, 29(9):e45.
51. Porter T.R., Eckberg D.L., Fritsch J.M., Rea R.F., Beightol L.A., Schmedtje J.F., Mohanty P.K. Autonomic pathophysiology in heart failure patients. Sympathetic-cholinergic interrelations. J. Clin. Invest. 1990, 85:1362-1371.
52. Qin F., Vulapalli R.S., Stevens S.Y., Liang C.S. Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H363-H371.
53. Ramchandra R., Hood S.G., Denton D.A., Woods R.L., McKinley M.J., McAllen R.M., May C.N. Basis for the preferential activation of cardiac sympathetic nerve activity in heart failure. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:924-928.
54. Roskoski R., Schmid P.G., Mayer H.E., Abboud F.M. In vitro acetylcholine biosynthesis in normal and failing guinea pig hearts. Circ. Res. 1975, 36:547-552.
55. Sabbah H.N. Electrical vagus nerve stimulation for the treatment of chronic heart failure. Cleve. Clin. J. Med. 2011, 78(Suppl. 1):S24-S29.
56. Sabbah H.N., Ilsar I., Zaretsky A., Rastogi S., Wang M., Gupta R.C. Vagus nerve stimulation in experimental heart failure. Heart Fail. Rev. 2011, 16:171-178.
57. Samina Riaz S., Tomlinson D.R. Pharmacological modulation of nerve growth factor synthesis: a mechanistic comparison of vitamin D receptor and beta(2)-adrenoceptor agonists. Brain Res. Mol. Brain Res. 2000, 85:179-188.
58. Semkova I., Schilling M., Henrich-Noack P., Rami A., Krieglstein J. Clenbuterol protects mouse cerebral cortex and rat hippocampus from ischemic damage and attenuates glutamate neurotoxicity in cultured hippocampal neurons by induction of NGF. Brain Res. 1996, 717:44-54.
59. Vanhoutte P.M., Levy M.N. Prejunctional cholinergic modulation of adrenergic neurotransmission in the cardiovascular system. Am. J. Physiol. 1980, 238:H275-H281.
60. Wernli G., Hasan W., Bhattacherjee A., van Rooijen N., Smith P.G. Macrophage depletion suppresses sympathetic hyperinnervation following myocardial infarction. Basic Res. Cardiol. 2009, 104:681-693.
61. Wetzel G.T., Brown J.H. Presynaptic modulation of acetylcholine release from cardiac parasympathetic neurons. Am. J. Physiol. 1985, 248:H33-H39.
62. Xu Z.J., Adams D.J. Alpha-adrenergic modulation of ionic currents in cultured parasympathetic neurons from rat intracardiac ganglia. J. Neurophysiol. 1993, 69:1060-1070.
63. Xu X.L., Zang W.J., Lu J., Kang X.Q., Li M., Yu X.J. Effects of carvedilol on M2 receptors and cholinesterase-positive nerves in adriamycin-induced rat failing heart. Auton. Neurosci. 2006, 130:6-16.
64. Yang T., Levy M.N. Sequence of excitation as a factor in sympathetic-parasympathetic interactions in the heart. Circ. Res. 1992, 71:898-905.
65. Zhang Y., Popovic Z.B., Bibevski S., Fakhry I., Sica D.A., Van Wagoner D.R., Mazgalev T.N. Chronic vagus nerve stimulation improves autonomic control and attenuates systemic inflammation and heart failure progression in a canine high-rate pacing model. Circ. Heart Fail. 2009, 2:692-699.