5-HT activates vagal afferent cell bodies in vivo: Role of 5-HT2 and 5-HT3 receptors

Neuroscience

Volumn 143, Issue 1, 2006, Pages 273-287

  Lacolley, P ^a   Owen, J R ^b   Sandock, K ^b   Lewis, T H J ^b   Bates, J N ^a   Robertson, T P ^b   Lewis, S J ^b  

^a UNIVERSITY OF IOWA   (United States)

^b Anatomic Pathology Service Department of Veterinary Pathobiology College of Veterinary   (United States)

Author keywords

5 HT; 5 HT2 receptors; 5 HT3 receptors; blood pressure; heart rate; vagal afferents

Indexed keywords

BEMESETRON; KETANSERIN; METHYSERGIDE MALEATE; SEROTONIN; SEROTONIN 2 ANTAGONIST; SEROTONIN 2 RECEPTOR; SEROTONIN 3 ANTAGONIST; SEROTONIN 3 RECEPTOR; TROPISETRON; UNCLASSIFIED DRUG; URETHAN; XYLAMIDINE TOSYLATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; EXPERIMENTAL RAT; HEART RATE; HEMODYNAMICS; IN VIVO STUDY; MALE; NERVE CELL MEMBRANE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL STIMULATION; NERVE ENDING; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; TACHYCARDIA; VAGUS NERVE;

ANALYSIS OF VARIANCE; ANIMALS; ATROPINE; BLOOD PRESSURE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; DRUG INTERACTIONS; HEART RATE; MALE; MUSCARINIC ANTAGONISTS; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SEROTONIN, 5-HT2; RECEPTORS, SEROTONIN, 5-HT3; SEROTONIN; SEROTONIN AGONISTS; SEROTONIN ANTAGONISTS; VAGUS NERVE;

EID: 33750522242     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.07.032     Document Type: Article

References (67)

1. Abboud F.M., Heistad D.D., Mark A.L., and Schmid P.G. Reflex control of the peripheral circulation. Prog Cardiovasc Dis 8 (1976) 371-403
2. Allen A.M., Chai S.Y., Sexton P.M., Lewis S.J., Verberne A.J.M., Jarrott B., Louis W.J., Clevers J., McKinley M.J., Paxinos G., and Mendholson F.A. Angiotensin II receptors and angiotensin converting enzyme in the medulla oblongata. Hypertension 9 (1987) 198-205
3. Andrade R., and Chaput Y. The electrophysiology of serotonin receptor subtypes. In: Petrouka S.J. (Ed). Serotonin receptor subtypes: basic and clinical aspects (1991), John Wiley Ltd, New York 103-124
4. Aviado D.M., and Guevara Aviado D. The Bezold-Jarisch reflex. A historical perspective of cardiopulmonary reflexes. Ann N Y Acad Sci 940 (2001) 48-58
5. Bacal K., and Kunze D.L. Dual effects of angiotensin II on calcium currents in neonatal rat nodose neurons. J Neurosci 14 (1994) 7159-7167
6. Broberger C., Holmberg K., Shi T.J., Dockray G., and Hokfelt T. Expression and regulation of cholecystokinin and cholecystokinin receptors in rat nodose and dorsal root ganglia. Brain Res 903 (2001) 128-140
7. Carrasco G., Cruz M.A., Gallardo V., Miguel P., Lagos M., and Gonzalez C. Plasma and platelet concentration and platelet uptake of serotonin in normal and pre-eclamptic pregnancies. Life Sci 62 (1998) 1323-1332
8. Christian E.P., Taylor G.E., and Weinreich D. Serotonin increases excitability of rabbit C-fiber neurons by two distinct mechanisms. J Appl Physiol 67 (1989) 584-591
9. Cordoba-Rodriguez R., Moore K.A., Kao J.P., and Weinreich D. Calcium regulation of a slow post-spike hyperpolarization in vagal afferent neurons. Proc Natl Acad Sci U S A 96 (1999) 7650-7657
10. 3 receptors are membrane ion-channels. Nature 339 (1989) 706-709
11. Emau P., Giri S.N., and Bruss M.L. Role of prostaglandins, histamine, and serotonin in the pathophysiology induced by Pasteurella hemolytica endotoxin in sheep. Circ Shock 12 (1984) 47-59
12. 3H]cGMP binding, by the rat vagus nerve. Brain Res 878 (2000) 240-246
13. Fozard J.R. Neuronal 5-HT receptors in the periphery. Neuropharmacology 23 (1984) 1473-1486
14. 3 receptors. In: Saxena P.R., Wallis D.I., Wouters W., and Bevan P. (Eds). Cardiovascular pharmacology of 5-hydroxytryptamine (1990), Kluwer, Dordrecht, The Netherlands 101-115
15. Gao X., Phillips P.A., Widdop R.E., Trinder D., Jarrott B., and Johnston C.I. Presence of functional vasopressin V1 receptors in rat vagal afferent neurones. Neurosci Letts 145 (1992) 79-82
16. Hoang C.J., and Hay M. Expression of metabotropic glutamate receptors in nodose ganglia and the nucleus of the solitary tract. Am J Physiol 281 (2001) H457-H462
17. Jacobs L., and Comroe Jr. J.H. Reflex apnea, bradycardia, and hypotension produced by serotonin and phenyldiguanide acting on the nodose ganglia of the cat. Circ Res 29 (1971) 145-155
18. Kereveur A., Callebert J., Humbert M., Herve P., Simonneau G., Launay J.M., and Drouet L. High plasma serotonin levels in primary pulmonary hypertension. Effect of long-term epoprostenol (prostacyclin) therapy. Arterioscler Thromb Vasc Biol 20 (2000) 2233-2239
19. Koike S., Hisa Y., Uno T., Murakami Y., Tamada Y., and Ibata Y. Nitric oxide synthase and NADPH-diaphorase in neurons of the rat, dog and guinea-pig nodose ganglia. Acta Otol 539 (1998) 110-112
20. Krstew E., Jarrott B., and Lawrence A.J. Bradykinin B2 receptors in nodose ganglia of rat and human. Eur J Pharmacol 348 (1998) 175-180
21. 2 receptors. Brain Res 1093 (2006) 105-115
22. Lacolley P.S., Owen J.R., Sandock K., Lewis T.H.J., Bates J.N., Robertson T.P., and Lewis S.J. Occipital artery injections of 5-5-HT may directly activate the cell bodies of vagal and glossopharyngeal afferent cell bodies in the rat. Neuroscience (2006) in press, doi: 10.1016/j.neuroscience.2006.08.047.
23. Laduron P.M. Axonal transport of receptors: coexistence with neurotransmitter and recycling. Biochem Pharmacol 33 (1984) 897-903
24. Laduron P.M. Axonal transport of opiate receptors in capsaicin-sensitive neurones. Brain Res 294 (1984) 157-160
25. Lawrence A.J., Krstew E., and Jarrott B. Functional dopamine D2 receptors on rat vagal afferent neurones. Br J Pharmacol 114 (1995) 1329-1334
26. Lawrence A.J., Krstew E., and Jarrott B. Actions of nitric oxide and expression of the mRNA encoding nitric oxide synthase in rat vagal afferent neurons. Eur J Pharmacol 315 (1996) 127-133
27. Lawrence A.J., Krstew E., and Jarrott B. Complex interactions between nitric oxide and adenosine receptors in the rat isolated nodose ganglion. Eur J Pharmacol 328 (1997) 83-88
28. Lewis S.J., Allen A.M., Verberne A.J.M., Figdor R., Jarrott B., and Mendelsohn F.A.O. Evidence for angiotensin II receptors on vagal afferents in the NTS. Eur J Pharmacol 125 (1986) 305-307
29. Lewis S.J., Cincotta M., Verberne A.J.M., Jarrott B., Lodge D., and Beart P.M. Receptor autoradiography with [3H]L-glutamate reveals the presence and axonal transport of glutamate receptors in vagal afferent neurons of the rat. Eur J Pharmacol 144 (1987) 413-415
30. Lewis S.J., Verberne A.J.M., Summers R.J., Beart P.M., and Cincotta M. Reduced glutamate binding in rat dorsal vagal complex after nodose ganglionectomy. Brain Res Bull 21 (1988) 913-916
31. Lewis S.J., Verberne A.J.M., Beart P.M., Jarrott B., Louis C., and Louis W.J. Histological and functional evidence for a degeneration of vagal afferent neurons following application of the excitotoxin kainic acid to the nodose ganglion. Neuroscience 34 (1989) 331-339
32. Lewis S.J., Hoque A., and Bates J.N. Differentiation of L- and D-S-nitrosothiol recognition sites. J Cardiovasc Pharmacol 46 (2005) 660-671
33. Lewis S.J., Graves J.E., Bates J.N., and Kooy N.W. Peroxynitrite elicits dysfunction of stereoselective S-nitrosocysteine recognition sites. J Cardiovasc Pharmacol 46 (2005) 637-645
34. Lewis S.J., Owen J.R., and Bates J.N. S-nitrosocysteine elicits hemodynamic responses similar to those of the Bezold-Jarisch reflex via activation of stereoselective recognition sites. Eur J Pharmacol 531 (2006) 254-258
35. Ling E.A., and Wong W.C. An electron microscopic study of the nodose (inferior vagal) ganglion cells in the monkey. J Neurocytol 17 (1988) 845-857
36. Maggi C.A., and Meli A. The sensory-efferent function of capsaicin-sensitive sensory neurons. Gen Pharmacol 19 (1988) 1-43
37. Maricq A.V., Peterson A.S., Brake A.J., Myers R.M., and Julius D. Primary structure and functional expression of the 5-HT3 receptor, a serotonin-gated channel. Science 254 (1991) 432-437
38. Mei N., Condamin M., and Boyer A. The composition of the vagus nerve of the cat. Cell Tissue Res 209 (1980) 423-431
39. Meller S.T., Lewis S.J., Ness T.J., Brody M.J., and Gebhart G.F. Vagal afferent-mediated inhibition of a nociceptive reflex by intravenous serotonin in the rat. I. Characterization. Brain Res 524 (1990) 90-100
40. 3 receptor subtypes. Brain Res 561 (1991) 61-68
41. Meller S.T., Lewis S.J., Ness T.J., Brody M.J., and Gebhart G.F. Neonatal capsaicin treatment abolishes the nociceptive responses to intravenous 5-HT in the rat. Brain Res 542 (1991) 212-218
42. Meller S.T., Lewis S.J., Brody M.J., and Gebhart G.F. Vagal afferent-mediated inhibition of a nociceptive reflex by i.v. serotonin in the rat. II. Role of 5-HT receptor subtypes. Brain Res 585 (1992) 71-86
43. Meller S.T., Lewis S.J., Brody M.J., and Gebhart G.F. Age, strain and anesthetic differences in the nociceptive responses to i.v. 5-HT in the rat. Brain Res 587 (1992) 88-94
44. Mendelowitz D., Reynolds P.J., and Andresen M.C. Heterogeneous functional expression of calcium channels at sensory and synaptic regions in nodose neurons. J Neurophysiol 73 (1995) 872-875
45. 3 receptors mediate inflammation-induced unmasking of functional tachykinin responses in vitro. J Appl Physiol 92 (2002) 2529-2534
46. Morelowska-Spierzak D., Pawlak D., and Buczko W. Influence of captopril on the serotonin-induced vasopressor effect in tail artery isolated from two-kidney, one-clip renal hypertensive rats. Pol J Pharmacol 47 (1995) 417-422
47. 3 receptors on vagal cardiopulmonary afferents. Brain Res 1059 (2005) 167-172
48. Palkovits M., and Zaborsky L. Neuroanatomy of central cardiovascular control. Nucleus tract solitarii: afferent and efferent neuronal connections in relation to the baroreceptor reflex arc. Prog Brain Res 47 (1977) 1-34
49. Probst W.C., Snyder L.A., Schuster D.I., Brosius J., and Sealfon S.C. Sequence alignment of the G-protein coupled receptor superfamily. DNA Cell Biol 11 (1992) 1-20
50. Pugh W.W., and Kalia M. Differential uptake of peroxidase (HRP) and peroxidase-lectin (HRP-WGA) conjugate injected in the nodose ganglion of the cat. J Histochem Cytochem 30 (1982) 887-894
51. 3 receptors. Trends Neurosci 9 (1986) 424-428
52. Ruggiero D.A., Mtui E.P., Otake K., and Anwar M. Central and primary visceral afferents to nucleus tractus solitarii may generate nitric oxide as a membrane-permeant neuronal messenger. J Comp Neurol 364 (1996) 51-67
53. Simasko S.M., Wiens J., Karpiel A., Covasa M., and Ritter R.C. Cholecystokinin increases cytosolic calcium in a subpopulation of cultured vagal afferent neurons. Am J Physiol 283 (2002) R1303-R1313
54. Snitsarev V., Whiteis C.A., Abboud F.M., and Chapleau M.W. Mechanosensory transduction of vagal and baroreceptor afferents revealed by study of isolated nodose neurons in culture. Auton Neurosci 98 (2002) 59-63
55. Spyer K.M. Neural organization and control of the baroreceptor reflex. Rev Physiol Biochem Pharmacol 88 (1981) 23-124
56. Ten Tusscher M.P., Klooster J., and Vrensen G.F. Satellite cells as blood-ganglion cell barrier in autonomic ganglia. Brain Res 490 (1980) 95-102
57. Teramoto Y., Urano T., Nagai N., Takada Y., Ikeda K., and Takada A. Plasma levels of 5-HT and 5-HIAA increased after intestinal ischemia/reperfusion in rats. Jpn J Physiol 48 (1998) 333-339
58. Thoren P. Role of cardiac vagal C-fibers in cardiovascular control. Rev Physiol Biochem Pharmacol 86 (1979) 1-94
59. Verberne A.J.M., Lewis S.J., Jarrott B., and Louis W.J. Bezold-Jarisch reflex is inhibited by excitotoxin-induced destruction of primary afferent neurons. Eur J Pharmacol 139 (1987) 365-367
60. Wallenstein S., Zucker C.L., and Fleiss J.C. Some statistical methods useful in circulation research. Circ Res 47 (1980) 1-9
61. 125I]-pindolol binding to β-adrenoceptors on rat nodose ganglion after chronic isoprenaline treatment. J Auton Nerv Syst 60 (1996) 12-16
62. 3 receptors on vagal afferents mediating the Bezold-Jarisch reflex. Brain Res 873 (2000) 302-305
63. Widdop R.E., Krstew E., and Jarrott B. Electrophysiological responses of angiotensin peptides on the rat isolated nodose ganglion. Clin Exp Hypertension A 14 (1992) 597-613
64. Winer B.J. Statistical principles of experimental design (1971), McGraw-Hill, New York 752-809
65. Wittstein I.S., Thiemann D.R., Lima J.A., Baughman K.L., Schulman S.P., Gerstenblith G., Wu K.C., Rade J.J., Bivalacqua T.J., and Champion H.C. Neurohumoral features of myocardial stunning due to sudden emotional stress. N Engl J Med 352 (2005) 539-548
66. Zhang L., Jones S., Brody K., Costa M., and Brookes S.J. Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. Am J Physiol 286 (2004) G983-G991
67. Zifa E., and Fillion G. 5-Hydroxytryptamine receptors. Pharmacol Rev 44 (1992) 401-458