Modulation of rat parasympathetic cardiac ganglion phenotype and NGF synthesis by adrenergic nerves

Autonomic Neuroscience: Basic and Clinical

Volumn 145, Issue 1-2, 2009, Pages 17-26

  Hasan, Wohaib ^a,b   Smith, Peter G ^a,b  

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

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Guanethidine; Nerve growth factor; Parasympathetic nervous system; ProNGF; Stellate ganglionectomy

Indexed keywords

ACETYLCHOLINE; CATECHOLAMINE; GUANETHIDINE; NERVE GROWTH FACTOR; NEUROTROPHIN; PARGYLINE; VESICULAR MONOAMINE TRANSPORTER;

ADRENERGIC NERVE; ADRENERGIC TRANSMISSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; GANGLIONECTOMY; IMMUNOREACTIVITY; MALE; NEUROCHEMISTRY; NEUROTRANSMISSION; NONHUMAN; NORADRENERGIC NERVE; PARASYMPATHETIC GANGLION; PARASYMPATHETIC NERVE CELL; PHENOTYPE; POSTGANGLIONIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; REGULATORY MECHANISM; STELLATE GANGLION; SYMPATHECTOMY; SYMPATHETIC INNERVATION;

ADRENERGIC FIBERS; ANIMALS; GANGLIA, PARASYMPATHETIC; HEART; MALE; NERVE GROWTH FACTOR; PHENOTYPE; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 58149457557     PISSN: 15660702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.autneu.2008.10.012     Document Type: Article

References (72)

1. Asmus S.E., Tian H., and Landis S.C. Induction of cholinergic function in cultured sympathetic neurons by periosteal cells: cellular mechanisms. Dev. Biol. 235 (2001) 1-11
2. Azevedo E.R., and Parker J.D. Parasympathetic control of cardiac sympathetic activity: normal ventricular function versus congestive heart failure. Circulation 100 (1999) 274-279
3. Baluk P., and Gabella G. Some parasympathetic neurons in the guinea-pig heart express aspects of the catecholaminergic phenotype in vivo. Cell Tissue Res. 261 (1990) 275-285
4. Brodde O.E. Beta-adrenoceptor blocker treatment and the cardiac beta-adrenoceptor-G-protein(s)-adenylyl cyclase system in chronic heart failure. Naunyn Schmiedebergs Arch. Pharmacol. 374 (2007) 361-372
5. Carswell S., Hoffman E.K., Clopton-Hartpence K., Wilcox H.M., and Lewis M.E. Induction of NGF by isoproterenol, 4-methylcatechol and serum occurs by three distinct mechanisms. Brain Res. Mol. Brain Res. 15 (1992) 145-150
6. Chang C.C., Costa E., and Brodie B.B. Interaction of guanethidine with adrenergic neurons. J. Pharmacol. Exp. Ther. 147 (1965) 303-312
7. Cheng Z., Powley T.L., Schwaber J.S., and Doyle F.J. Vagal afferent innervation of the atria of the rat heart reconstructed with confocal microscopy. J. Comp. Neurol. 381 (1997) 1-17
8. Chun L.L., and Patterson P.H. Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth, and differentiation of catecholamine production. J. Cell Biol. 75 (1977) 694-704
9. Colangelo A.M., Mallei A., Johnson P.F., and Mocchetti I. Synergistic effect of dexamethasone and beta-adrenergic receptor agonists on the nerve growth factor gene transcription. Brain Res. Mol. Brain Res. 124 (2004) 97-104
10. Culmsee C., Semkova I., and 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. 35 (1999) 47-57
11. Dal Toso R., De Bernardi M.A., Brooker G., Costa E., and Mocchetti I. Beta adrenergic and prostaglandin receptor activation increases nerve growth factor mRNA content in C6-2B rat astrocytoma cells. J. Pharmacol. Exp. Ther. 246 (1988) 1190-1193
12. Dunlap M.E., Bibevski S., Rosenberry T.L., and Ernsberger P. Mechanisms of altered vagal control in heart failure: influence of muscarinic receptors and acetylcholinesterase activity. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H1632-1640
13. Fan Q., and Smith P.G. Decreased vasoactive intestinal polypeptide-immunoreactivity of parasympathetic neurons and target innervation following long-term sympathectomy. Regul. Pept. 48 (1993) 337-343
14. Ferrari A.U., Franzelli C., Daffonchio A., Perlini S., and Dirienzo M. Sympathovagal interplay in the control of overall blood pressure variability in unanesthetized rats. Am. J. Physiol. 270 (1996) H2143-2148
15. Forsgren S., Moravec M., and Moravec J. Catecholamine-synthesizing enzymes and neuropeptides in rat heart epicardial ganglia; an immunohistochemical study. Histochem. J. 22 (1990) 667-676
16. Furshpan E.J., MacLeish P.R., O'Lague P.H., and Potter D.D. Chemical transmission between rat sympathetic neurons and cardiac myocytes developing in microcultures: evidence for cholinergic, adrenergic, and dual-function neurons. Proc. Natl. Acad. Sci. USA 73 (1976) 4225-4229
17. Furshpan E.J., Landis S.C., Matsumoto S.G., and Potter D.D. Synaptic functions in rat sympathetic neurons in microcultures. I. Secretion of norepinephrine and acetylcholine. J. Neurosci. 6 (1986) 1061-1079
18. Goldstein D.S. Functional neuroimaging of sympathetic innervation of the heart. Ann. N. Y. Acad. Sci. 1018 (2004) 231-243
19. Goldstein D.S., Robertson D., Esler M., Straus S.E., and Eisenhofer G. Dysautonomias: clinical disorders of the autonomic nervous system. Ann. Intern. Med. 137 (2002) 753-763
20. Habecker B.A., and Landis S.C. Noradrenergic regulation of cholinergic differentiation. Science 264 (1994) 1602-1604
21. Hansson M., Kjorell U., and Forsgren S. Increased immunoexpression of atrial natriuretic peptide in the heart conduction system of the rat after cardiac sympathectomy. J. Molec. Cell Cardiol. 30 (1998) 2047-2057
22. Hasan W., and Smith P.G. Nerve growth factor expression in parasympathetic neurons: regulation by sympathetic innervation. Eur. J. Neurosci. 12 (2000) 4391-4397
23. Hasan W., Zhang R., Liu M., Warn J.D., and Smith P.G. Coordinate expression of NGF and alpha-smooth muscle actin mRNA and protein in cutaneous wound tissue of developing and adult rats. Cell Tissue Res. 300 (2000) 97-109
24. Hasan W., Smith H.J., Ting A.Y., and Smith P.G. Estrogen alters trkA and p75 neurotrophin receptor expression within sympathetic neurons. J. Neurobiol. 65 (2005) 192-204
25. Hassall C.J., and Burnstock G. Intrinsic neurones and associated cells of the guinea-pig heart in culture. Brain Res. 364 (1986) 102-113
26. Hayes V.Y., Isackson P.J., Fabrazzo M., Follesa P., and Mocchetti I. Induction of nerve growth factor and basic fibroblast growth factor mRNA following clenbuterol: contrasting anatomical and cellular localization. Exp. Neurol. 132 (1995) 33-41
27. Himura Y., Felten S.Y., Kashiki M., Lewandowski T.J., Delehanty J.M., and Liang C.S. Cardiac noradrenergic nerve terminal abnormalities in dogs with experimental congestive heart failure. Circulation 88 (1993) 1299-1309
28. Horackova M., Huang M.H., Armour J.A., Hopkins D.A., and Mapplebeck C. Cocultures of adult ventricular myocytes with stellate ganglia or intrinsic cardiac neurones from guinea pigs: spontaneous activity and pharmacological properties. Cardiovasc. Res. 27 (1993) 1101-1108
29. Horackova M., Armour J.A., and Byczko Z. Distribution of intrinsic cardiac neurons in whole-mount guinea pig atria identified by multiple neurochemical coding. A confocal microscope study. Cell Tissue Res. 297 (1999) 409-421
30. Huang M.H., Sylven C., Pelleg A., Smith F.M., and Armour J.A. Modulation of in situ canine intrinsic cardiac neuronal activity by locally applied adenosine, ATP, or analogues. Am. J. Physiol. 265 (1993) R914-922
31. Jacobowitz D. Histochemical studies of the relationship of chromaffin cells and adrenergic nerve fibers to the cardiac ganglia of several species. J. Pharmacol. Exp. Ther. 158 (1967) 227-240
32. Kniazeva L.A., Iarygin V.N., and Pylaev A.S. Cytofluorimetric study of the small, intensely fluorescent cells of the rat atria in pharmacological sympathectomy. Biulleten' eksperimental'noi biologii i meditsiny 94 (1982) 90-92
33. Kohn J., Aloyz R.S., Toma J.G., Haak-Frendscho M., and Miller F.D. Functionally antagonistic interactions between the TrkA and p75 neurotrophin receptors regulate sympathetic neuron growth and target innervation. J. Neurosci. 19 (1999) 5393-5408
34. Korsching S., and Thoenen H. Developmental changes of nerve growth factor levels in sympathetic ganglia and their target organs. Dev. Biol. 126 (1988) 40-46
35. Kummer W., Fink L., Dvorakova M., Haberberger R., and Bohle R.M. Rat cardiac neurons express the non-coding R-exon (exon 1) of the cholinergic gene locus. Neuroreport 9 (1998) 2209-2212
36. Lee R., Kermani P., Teng K.K., and Hempstead B.L. Regulation of cell survival by secreted proneurotrophins. Science 294 (2001) 1945-1948
37. Levy M.N. Autonomic interactions in cardiac control. Ann. N. Y. Acad. Sci. 601 (1990) 209-221
38. Lockhart S.T., Mead J.N., Pisano J.M., Slonimsky J.D., and Birren S.J. Nerve growth factor collaborates with myocyte-derived factors to promote development of presynaptic sites in cultured sympathetic neurons. J. Neurobiol. 42 (2000) 460-476
39. Loffelholz K., and Pappano A.J. The parasympathetic neuroeffector junction of the heart. Pharmacol. Rev. 37 (1985) 1-24
40. Loiacono R.E., and Story D.F. Effect of alpha-adrenoceptor agonists and antagonists on cholinergic transmission in guinea-pig isolated atria. Naunyn Schmiedebergs Arch. Pharmacol. 334 (1986) 40-47
41. Lu B., Pang P.T., and Woo N.H. The yin and yang of neurotrophin action. Nat. Rev. Neurosci. 6 (2005) 603-614
42. Matsumoto S.G., Sah D., Potter D.D., and Furshpan E.J. Synaptic functions in rat sympathetic neurons in microcultures. IV. Nonadrenergic excitation of cardiac myocytes and the variety of multiple-transmitter states. J. Neurosci. 7 (1987) 380-390
43. Mawe G.M., Talmage E.K., Lee K.P., and Parsons R.L. Expression of choline acetyltransferase immunoreactivity in guinea pig cardiac ganglia. Cell Tissue Res. 285 (1996) 281-286
44. Maxwell R.A. Guanethidine after twenty years: a pharmacologist's perspective. Br. J. Clin. Pharmacol. 13 (1982) 35-44
45. Mione M.C., Sancesario G., D'Angelo V., and Bernardi G. Increase of dopamine beta-hydroxylase immunoreactivity in non-noradrenergic nerves of rat cerebral arteries following long-term sympathectomy. Neurosci. Lett. 123 (1991) 167-171
46. Moravec M., Moravec J., and Forsgren S. Catecholaminergic and peptidergic nerve components of intramural ganglia in the rat heart. An immunohistochemical study. Cell Tissue Res. 262 (1990) 315-327
47. Nihei M., Lee J.K., Honjo H., Yasui K., Uzzaman M., Kamiya K., Opthof T., and Kodama I. Decreased vagal control over heart rate in rats with right-sided congestive heart failure: downregulation of neuronal nitric oxide synthase. Circ. J. 69 (2005) 493-499
48. Ogita H., Shimonagata T., Fukunami M., Kumagai K., Yamada T., Asano Y., Hirata A., Asai M., Kusuoka H., Hori M., and Hoki N. Prognostic significance of cardiac (123)I metaiodobenzylguanidine imaging for mortality and morbidity in patients with chronic heart failure: a prospective study. Heart (British Cardiac Society) 86 (2001) 656-660
49. Pardini B.J., Lund D.D., and Schmid P.G. Organization of the sympathetic postganglionic innervation of the rat heart. J. Auton. Nerv. Syst. 28 (1989) 193-201
50. Paton J.F., Boscan P., Pickering A.E., and Nalivaiko E. The yin and yang of cardiac autonomic control: vago-sympathetic interactions revisited. Brain Res. Brain Res. Rev. 49 (2005) 555-565
51. Pauza D.H., Pauziene N., Pakeltyte G., and Stropus R. Comparative quantitative study of the intrinsic cardiac ganglia and neurons in the rat, guinea pig, dog and human as revealed by histochemical staining for acetylcholinesterase. Ann. Anat. 184 (2002) 125-136
52. Randall D.C., Brown D.R., Mcardiac ganglionuirt A.S., Thompson G.W., Armour J.A., and Ardell J.L. Interactions within the intrinsic cardiac nervous system contribute to chronotropic regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285 (2003) R1066-1075
53. Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 (2006) 1545-1564
54. Rush R.A., Chie E., Liu D., Tafreshi A., Zettler C., and Zhou X.F. Neurotrophic factors are required by mature sympathetic neurons for survival, transmission and connectivity. Clin. Exp. Pharm. Physiol. 24 (1997) 549-555
55. Samina Riaz S., and 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. 85 (2000) 179-188
56. Seabrook G.R., Fieber L.A., and Adams D.J. Neurotransmission in neonatal rat cardiac ganglion in situ. Am. J. Physiol. 259 (1990) H997-1005
57. Semkova I., Schilling M., Henrich-Noack P., Rami A., and 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. 717 (1996) 44-54
58. Singh S., Johnson P.I., Javed A., Gray T.S., Lonchyna V.A., and Wurster R.D. Monoamine- and histamine-synthesizing enzymes and neurotransmitters within neurons of adult human cardiac ganglia. Circulation 99 (1999) 411-419
59. Slavikova J., Kuncova J., Reischig J., and Dvorakova M. Catecholaminergic neurons in the rat intrinsic cardiac nervous system. Neurochem. Res. 28 (2003) 593-598
60. Smith P.G. Role of the sympathetic nervous system in functional maturation of Muller's smooth muscle in the rat. J. Pharmacol. Exp. Ther. 235 (1985) 330-334
61. Smith, P.G., 2008. Autonomic Neuroplasticity: Development. In: Squire L.A.T., Bloom F., Gage F., and Spitzer N., (Ed.), New Encyclopedia of Neuroscience, 4th ed. Elsevier, Oxford. pp. in press.
62. Smith P.G., and Fan Q. Sympathetic nerve trajectories to rat orbital targets: role of connective tissue pathways. J. Comp. Neurol. 365 (1996) 69-78
63. Smith P.G., Bruckert J.W., and Mills E. Reinnervation of Muller's smooth muscle by atypical sympathetic pathways following neonatal ganglionectomy in the rat: structural and functional investigations of enhanced neuroplasticity. Neuroscience 23 (1987) 781-793
64. Smith P.G., Warn J.D., Steinle J.J., Krizsan-Agbas D., and Hasan W. Modulation of parasympathetic neuron phenotype and function by sympathetic innervation. Auton. Neurosci. 96 (2002) 33-42
65. Sroka K. On the genesis of myocardial ischemia. Zeitschrift fur Kardiologie 93 (2004) 768-783
66. Tseng W.Y., Tsao C.F., Ko C.C., and Huang H.T. Local capsaicin application to the stellate ganglion and stellatectomy attenuate neurogenic inflammation in rat bronchi. Auton. Neurosci. 94 (2001) 25-33
67. Ungerer M., Parruti G., Bohm M., Puzicha M., DeBlasi A., Erdmann E., and Lohse M.J. Expression of beta-arrestins and beta-adrenergic receptor kinases in the failing human heart. Circ. Res. 74 (1994) 206-213
68. Ungerer M., Hartmann F., Karoglan M., Chlistalla A., Ziegler S., Richardt G., Overbeck M., Meisner H., Schomig A., and Schwaiger M. Regional in vivo and in vitro characterization of autonomic innervation in cardiomyopathic human heart. Circulation 97 (1998) 174-180
69. Warn J.D., Fan Q., and Smith P.G. Decreased neuronal nitric oxide synthase-immunoreactivity and NADPH-diaphorase activity in rat pterygopalatine ganglion parasympathetic neurons and cerebrovascular innervation following long-term sympathectomy. Neurosci. Lett. 232 (1997) 25-28
70. Weihe E., Schutz B., Hartschuh W., Anlauf M., Schafer M.K., and Eiden L.E. Coexpression of cholinergic and noradrenergic phenotypes in human and nonhuman autonomic nervous system. J. Comp. Neurol. 492 (2005) 370-379
71. Wetzel G.T., and Brown J.H. Presynaptic modulation of acetylcholine release from cardiac parasympathetic neurons. Am. J. Physiol. 248 (1985) H33-39
72. Yang B., Slonimsky J.D., and Birren S.J. A rapid switch in sympathetic neurotransmitter release properties mediated by the p75 receptor. Nat. Neurosci. 5 (2002) 539-545