Neuroregulation by vasoactive intestinal peptide (VIP) of mucus secretion in ferret trachea: Activation of BKCa channels and inhibition of neurotransmitter release

British Journal of Pharmacology

Volumn 126, Issue 1, 1999, Pages 147-158

  Liu, Yu Chih ^a   Patel, Hema J ^a   Khawaja, Aamir M ^b   Belvisi, Maria G ^c   Rogers, Duncan F ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^c SANOFI   (France)

Author keywords

Acetylcholine release; Airways; Cholinergic nerve; Ferret trachea; Iberiotoxin; Mucus secretion; Potassium channel; Vasoactive intestinal peptide

Indexed keywords

ACETYLCHOLINE; APAMIN; CHOLINE; GLIBENCLAMIDE; IBERIOTOXIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM ION; SULFUR 35; TACHYKININ; TRITIUM; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE ANTIBODY;

ACETYLCHOLINE RELEASE; ANIMAL TISSUE; ARTICLE; CHOLINERGIC TRANSMISSION; FERRET; MALE; MUCUS SECRETION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; TRACHEA;

ACETYLCHOLINE; ADRENERGIC AGENTS; ANIMALS; ANTIBODIES; ATROPINE; CHYMOTRYPSIN; DOSE-RESPONSE RELATIONSHIP, DRUG; FERRETS; MALE; MUCUS; MUSCARINIC ANTAGONISTS; NEUROTRANSMITTER AGENTS; PEPTIDES; PHENTOLAMINE; PIPERIDINES; POTASSIUM CHANNELS; PROPRANOLOL; RECEPTORS, ADRENERGIC; RECEPTORS, CHOLINERGIC; RECEPTORS, TACHYKININ; TRACHEA; TRITIUM; VASOACTIVE INTESTINAL PEPTIDE;

EID: 0032892939     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0702288     Document Type: Article

References (67)

1. AIZAWA, H., INOUE, H., SHIGYO, M., TAKATA, S., KOTO, H., MATSUMOTO, K. & IIARA, N. (1994). VIF antagonists enhance excitatory cholinergic neuro-transmission in the human airway. Lung, 17, 159-167.
2. ALBERTS, P., BARTFAI, T. & STJARNE, L. (1982). The effects of atropine on [3H]acetylchoIine secretion from guinea-pig myenteric plexus evoked electrically or by high potassium. J. Physiot., 32,93-112.
3. BANKS, B.E.C., BROWN, C., BURNSTOCK, G.M., CLARET, M., COCKS, T.M. & JENKINSON, D.U. (1979). Apamin blocks certain neurotransmitter-induced increases in potassium permeability. Atoure, 282,415-417.
4. BARANIUK, J.N., LUNDGREN, J.D., OKAYAMA, M., MULLOL, J., MERIDA, M., SHELHAMER, J.H. & KALINER, M.A. (1990). Vasoactive intestinal peptide in human nasal mucosa. J. Clin. Invest., 86, 825-831.
5. BARNES, P.J. (1996). Neuroeffector mechanisms: the interface between inflammation and neuronal responses. J. Allergy Clin. Immunol, 98, 1187-1198.
6. BARNES, P.J. & DIXON, C.Nl'.S. (1984). The effect of inhaled vasoactive intestinal peptide on bronchial hyperreactivity in man. Am. Rev. Respir. Dis., 13, 162- 166.
7. BELVISI, M.G., PATEL, H.J., TAKAHASHI, T., P.J. BARNES & GIEMBYCZ, M.A. (1996). Paradoxical facilitation of acetylcholine release from parasympathetic nerves innervating guinea-pig trachea by isoprenaline. Br. J. Pharmacol., 11, 1413-1420.
8. BORSON, D.B., CHARLIN, M., GOLD, B.D. & NADEL, J.A. (1984). Neural regulation of 35SO4-macromolecule secretion from trachea! glands of ferrets. J. Appl. Physio!.. 57, 457-466.
9. BOWDEN, J.J. & GIBBINS, I.L. (1992). Vasoactive intestinal peptide and neuropeptide Y co-exist in non-adrenergic sympathetic neurons to guinea pig trachea. J. Anton. Nerv. Syst., 38, l -20.
10. CAUGHEY, G.H., LEIDIG, F., VIRO, N.F. & NADEL, J.A. (1988). Substance P and vasoactive intestinal peptide degradation by mast cell tryptase and chymase. J. Pharmacol. Exp. Thcr., 24, 133-137.
11. CHATELAIN, C, POCHON, N. & LACROIX, J.S. (1995). Functional effects of phosphoramidon and captopril on exogenous neuropeptides in human nasal mucosa. Ear. Arch. Otorhinolaryngol., 25,83-85.
12. COLE, S.J., SAID, S.I. & REID, L.M. (1981). Inhibition by vasoactive intestinal peptide of glycoconjugate and lysozyme secretion by human airways in vitro. Am. Rev. Respir. Dis., 12, 531-536.
13. DAVIES, J.R., CORBISHLEY, CM. & RICHARDSON, P.S. (1990). The uptake of radiolabelled precursors of mucus glycoconjugates by secretory tissues in the feline trachea. J. PhysioL, 42, 19-30.
14. DECKERS, I.A., RAMPART, M., BULT, H. &. HERMAN, A.G. (1989). Evidence for the involvement of prostaglandins in modulation of acetylcholine release from bronchial tissue. Eur. J. Pharmacol., 16,415-418.
15. DEFFEBACH, M.E., ISLAMI, H., PRICE, A-, WEBBER, S.E. & WIDDICOMBE, J.G. (1990). Prostaglandins alter methacholineinduced secretion in ferret in vitro trachea. Am. J. Physittl., 25, L75-L80.
16. DEY, R.D., ALTERMUS, J.B., ROOD, A., MAYER, B, SAID, S.I. & COBURN, R.F. (1996). Neurochemical characterization of intrinsic neurons in ferret trachéal plexus. Am. J. Respir. Cell Mol. Biol., 14, 207-216.
17. DEY, R.D., HOFFPAUR, J. & SAID, S.I. (1988). Co-localization of VIP- and SP-containing nerves in cat bronchi. Neuroscience, 24, 275-281.
18. DEY, R.D., SHANNON JR, W.A. & SAID, S.I. (1981). Localization of VIP-immunoreactive nerves in airways and pulmonary vessels of dog, cat and human subjects. Cell Tissue Res., 22, 231-238.
19. DEY, R.D. & ZHU, W. (I994). Origin of galanin in verves of cat airways and colocalization with vasoactive intestinal peptide. Cell Tissue Res., 27, 193-200.
20. ELLIS, J.L. & FARMER, S.G. (1989a). Effects of peptidases on nonadrenergic, non-cholinergic inhibitory responses of trachéal smooth muscle: a comparison with effects on VIP- and PHIinduced relaxation. Br. J. Pharmacol., 96, 521-526.
21. ELLIS, J.L. & FARMER, S.G. (1989b). The effects of vasoactive intestinal peptide (VIP) antagonists, and VIP and peptide histidine isoleucine antisera on non-adrenergic, non-cholinergic relaxations of trachéal smooth muscle. Br. J. Pharmacol., 96, 52-528.
22. FISCHER, A.W. & HOFFMANN, B. (1996). Nitric oxide synthasc in neurons and nerve fibers of lower airways and in vagal sensory ganglia of man. Am. J. Respir. Cril. Care Afed., 15-4, 209-216.
23. FISCHER, A., KUMMER, W., COURAUD, J.-Y., ALDER, D., BRANSCHEID, D. & HEYM, C. (1992). Immunohistochemical localization of receptors for vasoactive intestinal peptide and substance P in human trachea. Lab. Invest., 67, 387-393.
24. GARCIA, M.L., GALVEZ, A., GARCIA-CALVO, M., KING, V.F., VASQUEZ, J. & KACZOROWSKI, G.J. (1991). Use of toxins to study potassium channels. J. Bioeuerget. Biomcmb., 23,615 -646.
25. GASHI, A.A., BORSON, D.B., FINKBEINER, W.E., NADEL, J.A. & BASBAUM, C.B. (1986). Neuropeptides degranulate serous cells of ferret trachéal glands. Am. J. Physio!., 25, C223-C229.
26. GASHI, A.A. BORSON, D.B., FINKBEINER, W.E., NADEL, J.A. & BASBAUM, C.B. (1987). Neuropeptides degranulate serous cells of ferret trachéal glands. Am. J. PhysioL, 25, C2223-C2229.
27. G1USEPPE, N.C., LOADER, J.E., GRAVES, J.P. & LARSEN, G.L (1995). Modulation of acetylcholine release in rabbit airways in vitro. Am. J. PhysioL, 12, L432-L437.
28. HOWARTH, P.H., SPRINGALL, D.R., REDINGTON, A.E., DJUKANOVIC, R., HOLGATE, S.T. & POLAK, J.M. (1995). Neuropeptidecontaining nerves in endobronchial biopsies from asthmatic and nonasthmatic subjects. Am. J. Respir. Cell Mol. BioL, 13, 288296.
29. LAITINEN, A., PARTANEN, M., HERVONEN, A., PELTO-HUIKKO, M. & LAITINEN, L.A. (1985). VIP-Iike immunoreactive nerves in human respiratory tract: light and electronic microscopic study. Hisiochemistry. 82, 313-319.
30. LAMMERS, J.W., BARNES, P.J. & CHUNG, K.F. (1992). Nonadrenergic, noncholinergic airway inhibitory nerves. Eur. Respir. J., 5, 23-246.
31. LAZARUS, S.C., BASBAUM, C.B., BARNES, P.J. & GOLD, W.M. (1986). cAMP immunocytochemistry provides evidence for functional VIP receptors in trachea. Am. J. Physio!., 25, Cl 15-C119.
32. LEROUX, P., VAUDRY, H., FOURNIER, A., ST-PIERRE, S. & PELLETIER, G. (I984). Characterization and localization of vasoactive intestinal peptide receptors in the rat lung. Endocrinology, 114, 1506-1512.
33. LI, CG. & RAND, M.J. (1991). Evidence that part of the NANC relaxant response of guinea-pig trachea to electrical field stimulation is mediated by nitric oxide. Br. J. PharnmcoL, 10, 91-94.
34. LIU, A., LI, P.S. & ZHANG, Z.J. (I993a). A clinical study on determination of plasma vasoactive intestinal peptide and the relationship between plasma vasoactive intestinal peptide and bronchial responsiveness in asthmatics. Cliiinç Hua Nei Ko Tsa Chili. 32, 165-166.
35. LIU, A., LI, P.S. & ZHANG, Z.J. (1993b). A clinical study on the effect of non-adrenergic non-cholinergic nerves in asthma. Chung Hua Nei Ko Tsa Chili, 32, 223-225.
36. MARTIN, J.G., WANG, A., ZACOUR, M. & BIGGS, D.F. (1990). The effects of vasoactive intestinal polypcptidc on cholinergic neurotransmission in an isolated innervated guinea pig trachéal preparation. Respir. PhysioL, 79, 111-121.
37. MCLEAN, S., GANONG, A., SEYMOUR, P.A., SNIDER, R.M., DESAI, M.C., ROSEN, T., BRYCE, O.K., LONGO, K.P., REYNOLDS, L.S., ROBINSON, G., SCHMIDT, A.W., SIOK, C. & HEYM, J. (1993). Pharmacology of CP-99,994: a non-peptide antagonist of the tachykinin neurokinin-1 receptor. J. Pharmacol. Exp. Ther., 26, 472-479.
38. ME1NI, S., MAK, J.C.W., ROHDE, J.A.L. & ROGERS, D.F. (1993). Tachykinin control of ferret airways: mucus secretion, bronchoconstriction and receptor mapping. Neuropeptides, 24, 81 -89.
39. MULLOL, J., RIEVES, R.D., BARANIUK, J.N., LUNDGREN, J.D., MERIDA, M., HAUSFELD, J.M., SHELHAMER, J.H. & KALINER, M.A. (1992). The effects of neuropeptides on mucous glycoprotein secretion from human nasal mucosa in vitro. Neuropeptides, 21, 231-238.
40. NIKI, I., KELLY, R.P., ASHCROFT, S.J.H. & ASHCROFT, P.M. (1989). ATP-sensitive K-channels in HIT T15 /5-cells studies by patchclamp methods, 86Rb efflux and glibenclamide binding. Pflügers Arch., 41, 47-55.
41. OLLERENSHAW, S.J., JARVIS, D., SULLIVAN, C.E. & WOOLCOCK, A.J. (1991). Substance P immunoreactive nerves in airways from asthmatics and non-asthmatics. Eur. Respir. J., 4, 67-682.
42. OLLERENSHAW, S.J., JARVIS, D., WOOLCOCK, A., SULLIVAN, C. & SCHEIBNER, T. (1989). Absence of immunoreactive vasoactive intestinal polypeptide in tissue from the lungs of patients with asthma. N. Engl. J. Med., 32, 1244-1248.
43. PATEL, HJ., BARNES, P.J., TAKAHASHI, T., TADJKARIMI, S., YACOUB, M.H. & BELVISI, M.G. (1995). Evidence for prejunctional muscarinic autoreceptor in human and guinea-pig trachea. Am. J. Respir. Cril. Care Med., 15, 872-878.
44. PAUL, S., GAO, Q.S., HUANG, H., SUN, M., THOMPSON, A., RENNARD, S. & LANDER, D. (1995). Catalytic autoantibodies to vasoactive intesinal peptide. Chest, 10, S125-S126.
45. PEATFIELD, A.C., BARNES, P.J., BRATCHER, C., NADEL, J.A. & DAVIS, B. (1983). Vasoactive intestinal peptide stimulates trachéal submucosal gland secretion in ferret. Am. Rev. Respir. Dis., 12,89-93.
46. RAMNARINE, S.I., HIRAYAMA, Y., BARNES, P.J. & ROGERS, D.F. (1994). Sensory-efferent neural control of mucus secretion: characterisation using tachykinin receptor antagonists in ferret trachea in vitro. Br. J. Pharmacol., 11, 1183-1190.
47. RAMNARINE, S.I., K.HAWAJA, A.M., BARNES, P.J. & ROGERS, D.F. (1996). Nitric- oxide inhibition of basal and neurogenic mucus secretion in ferret trachea in vitro. Br. J. Pharmacol., 11, 9981002.
48. RAMNARINE, S.I., LIU, Y.-C. & ROGERS, D.F. (1998). Neuroregulation of mucus secretion by opioid receptors and KATP and BKCa channels in ferret trachea in vitro. Br. J. Pharmacol., 12, 1631 1638.
49. RAMNARINE, S.I. & ROGERS, D.F. (1994). Non-adrenergic, noncholinergic neural control of mucus secretion in the airways. Pulm. Pharmacol., 7, 19-33
50. ROBINSON, N.P., YENNING, L., KYLE, H. & WIDDICOMBE, J.G. (1986). Quantitation of the secretory cells of the ferret tracheobronchial tree. J Anal., 14, 173-188.
51. ROGERS, D.F. (1997). Neural control of airway secretions. In: Autonomie Control of the Respiratory System, ed. Barnes, P.J. pp. 201-227. Amsterdam: Harwood Academic Publishers GmbH.
52. SASAKI, T., SHIMURA, S., SASAKI, H & TAKISHIMA, T. (1989). Effect of epithelium on mucus secretion from feline trachea! submucosal glands. J. Appl. Physiol., 60, 1237-1247.
53. + channels and block neurosecretion. Proc. Natl. Acad. Sei. U.S.A., 87, 3489-3492.
54. SEKIZAWA, K., TAMAOKI, J., GRAF, P.D. & NADEL, J.A. (1988). Modulation of cholinergic neurotransmission by vasoactive intestinal peptide in ferret trachea. J. Appl. Physiol., 64, 24332437.
55. SIIIGYO, M., AIZAWA, H., KOTO, H., MATSUMOTO, K., TAKATA, S. & HARA, N. (1997). Pre- and post-junctional effects of VIP-like peptides in guinea pig trachéal smooth muscle. Respiration, 64, 59-65
56. SHIMURA, S., SASAKI, T., IKEDA, K., SASAKI, II. & TAKISHIMA, T. (1988). VIP augments cholinergic-induced glycoconjugate secretion in trachéal submucosal glands. J. Appl. Physiol., 65, 24372544.
57. SHVILKIN, A., DANILO JR, P., CHEVALIER, P., CHANG, F., COHEN, I.S. & ROSEN, M.R. (1994). Vagal release of vasoactive intestinal peptide can promote vagotonic tachycardia in the isolated innervated rat heart. Cardiovas. Res.. 28, 1769-1773.
58. STRETTON, C.D., BELVISI, M.G. & BARNES, P.J. (1991). Modulation of neural bronchoconstrictor responses in the guinea pig respiratory tract by vasoactive intestinal peptide. Neitropcptides, 18, 149-157.
59. TUCKER, J.F., BRAVE, J.R., CHARALAMBOUS, L., HOBBS, A.J. & GIBSON, A. (1990). L-N-nitro arginine inhibits non-adrenergic, non-cholinergic relaxations of guinea-pig isolated trachéal smooth muscle. Br. J. Pharmacol., 10, 663-664.
60. USDIN, T.B., BONNER, T.I. & MEZEY, E. (1994). Two receptors for vasoactive intestinal polypeptide with similar specificity and complementary distributions. Endocrinology, 13, 2662-2680.
61. WAGNER, U., BREDENBRÖKER, D., STORM, B., TACKENBERG, B., FEHMANN, H.-C. & VON WICHERT, P. (1998). Effects of VIP and related peptides on airway mucus secretion from isolated rat trachea. Peptides, 19, 241-245.
62. WALTERS, E.H., O'BYRNE, P.M., FABBRI, L.M., GRAF, P.D., HOLTZMAN, M.J. & NADEL, J.A. (1984). Control of neurotransmission by prostaglandins in canine trachealis smooth muscle. J. Appl. Pharmacol., 57, 129-133.
63. WARD, J.K., BELVISI, M.G., FOX, A.J., MIURA, M., TADJKARIMI, S., YACOUB, M.H. & BARNES, P.J. (1993). Modulation of cholinergic neural bronchoconstriction by endogenous nitric oxide and vasoactive intestinal peptide in human airways in vitro. J. Clin. Invest., 92, 736-743.
64. WEBBER, S.E. & WIDDICOME, J.G. (1987). The effect of vasoactive intestinal peptide on smooth muscle tone and mucus secretion from the ferret trachea. Br. J. Pharmacol., 91, 139-148.
65. WESSLER, L, HELLW1G, D. & RACKE, K. (1990). Epithelium-derived inhibition of [3H]acetylcholine release from the isolated guineapig trachea. Naunyn-Schmiedeberg's Arch. Pharmacol., 34, 387-393.
66. WESSLER, I., KLEIN, A., POHAN, D., MACLAGAN, J. & RACKE, K. (1991). Release of [3H]acetylchoIine from the isolated rat or guinea-pig trachea evoked by preganglionic nerve stimulation; a comparison with transmural stimulation. Naunyn-Schmiedeberg's Arch. Pharmacol., 34, 403-411.
67. WIDDICOMBE, J.G. (1996). Neuroregulation of the nose and bronchi. Clin. Exp. Allergy, 26 (suppl. 3), 32-35.