VIP- and PACAP-mediated nonadrenergic, noncholinergic inhibition in longitudinal muscle of rat distal colon: Involvement of activation of charybdotoxin- and apamin-sensitive K+ channels

British Journal of Pharmacology

Volumn 119, Issue 4, 1996, Pages 623-630

  Kishi, Masami ^a   Takeuchi, Tadayoshi ^a   Suthamnatpong, Naowarat ^a   Ishii, Toshiaki ^a   Nishio, Hideaki ^a   Hata, Fumiaki ^a   Takewaki, Tadashi ^b  

^a Osaka Prefecture University   (Japan)

^b GIFU UNIVERSITY   (Japan)

Author keywords

Apamin; Charybdotoxin; NANC inhibition; PACAP; Rat distal colon; VIP

Indexed keywords

APAMIN; CHARYBDOTOXIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; DESCENDING COLON; ELECTROSTIMULATION; HYPERPOLARIZATION; INTESTINE MUSCLE; MALE; MUSCLE FIBER MEMBRANE POTENTIAL; MUSCLE RELAXATION; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0029966990     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1476-5381.1996.tb15719.x     Document Type: Article

References (50)

1. ARCHER, S.L., HUANG, J.M.C., HAMPL, V., NELSON, D.P., SHULTZ, P.J. & WEIR, E.K. (1994). Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin-sensitive K channel by cGMP-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A., 91, 7583-7587.
2. ARIMURA, A., SOMOGYVARI, A., MIYATA, A., MIZUNO, K., COY, D.H. & KITADA, C. (1991). Tissue distribution of PACAP as determined by RIA: Highly abundant in the rat brain and testes. Endocrinology, 129, 2787-2789.
3. BIANCANI, P., WALSH, J. & BEHAR, J. (1985). Vasoactive intestinal peptide: a neurotransmitter for relaxation of the rabbit internal anal sphincter. Gastroenterology, 89, 867-874.
4. BOLOTINA, V.M., NAJIBI, S., PALACINO, J.J., PAGANO, P.J. & COHEN, R.A. (1994). Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature, 368, 850-853.
5. CASTLE, N.A., HAYLETT, D.G. & JENKINSON, D.H. (1989). Toxins in the characterization of potassium channels. Trends Neurosci., 12, 59-66.
6. + channel opening mediates hyperpolarizations by nitric oxide donors and IJPs in opossum esophagus. Am. J. Physiol., 268, G831-G842.
7. CHRISTINCK, F., JURY, J., CAYABYAB, F.S. & DANIEL, E.E. (1991). Nitric oxide may be the final mediator of nonadrenergic, noncholinergic inhibitory junction potentials in the gut. Can. J. Physiol. Pharmacol., 69, 1448-1458.
8. COWAN, C.L., PALACINO, J.J., NAJIBI, S. & COHEN, R.A. (1993). Potassium channel-mediated relaxation to acetylcholine in rabbit arteries. J. Pharmacol. Exp. Ther., 266, 1482-1489.
9. DALZIEL, H.H., THORNBURY, K.D., WARD, S.M. & SANDERS, K.M. (1991). Involvement of nitric oxide synthetic pathway in inhibitory junction potentials in canine proximal colon. Am. J. Physiol., 260, G789-G792.
10. DU, C., MURRAY, J., BATES, J.N. & CONKLIN, J.L. (1991). Nitric oxide: mediator of NANC hyperpolarization of opossum esophageal smooth muscle. Am. J. Physiol., 261, G1012-G1016.
11. + channel modulated by a functionally associated protein kinase. Nature, 369, 563-565.
12. +-channel activity by protein phosphorylation. Nature, 315, 503-506.
13. GOYAL, R.K., RATTAN, S. & SAID, S.I. (1980). VIP as possible neurotransmitter of non-cholinergic non-adrenergic inhibitory neurons. Nature, 288, 378-380.
14. GRIDER, J.R. (1993). Interplay of VIP and nitric oxide in regulation of the descending relaxation phase of peristalsis. Am. J. Physiol., 264, G334-G340.
15. GRIDER, J.R., CABLE, M.B., SAID, S.I. & MAKHLOUF, M. (1985). Vasoactive intestinal peptide as a neural mediator of gastric relaxation. Am. J. Physiol., 248, G73-G78.
16. GRIDER, J.R., KATSOULIS, S., SCHMIDT, W.E. & JIN, J.-G. (1994). Regulation of the descending relaxation phase of intestinal peristalsis by PACAP. J. Autonom. Nerv. Syst., 50, 151-159.
17. GRIDER, J.R., MURTHY, K.S., JIN, J.-G. & MAKHLOUF, G.M. (1992). Stimulation of nitric oxide from muscle cells by VIP: prejunctional enhancement of VIP release. Am. J. Physiol., 262, G774-G778.
18. GRIDER, J.R. & RIVIER, J.R. (1990). Vasoactive intestinal peptide (VIP) as transmitter of inhibitory neurons of the gut: evidence from use of selective VIP antagonists and VIP antiserum. J. Pharmacol. Exp. Ther., 253, 738-742.
19. HATA, F., ISHII, T., KANADA, A., YAMANO, N., KATAOKA, T., TAKEUCHI, T. & YAGASAKI, O. (1990). Essential role of nitric oxide in descending inhibition in the rat proximal colon. Biochem. Biophys. Res. Commun., 172, 1400-1406.
20. HIRAMATSU, T., KUME, H., YAMAKI, K. & TAKAGI, K. (1995). Inhibition of pituitary adenylate cyclase activating polypeptide induced relaxation of guinea-pig tracheal smooth muscle by charybdotoxin. Arzneim.-Forsch./Drug Res., 45, 689-692.
21. HOSOYA, M., ONDA, H., OGI, K., MASUDA, Y., MIYAMOTO, Y., OHTAKI, T., OKAZAKI, H., ARIMURA, A. & FUJINO, M. (1993). Molecular cloning and functional expression of rat cDNAs encoding the receptor for pituitary adenylate cyclase activating polypeptide (PACAP). Biochem. Biophys. Res. Commun., 194, 133-143.
22. ISHIHARA, T., SHIGEMOTO, R., TAKAHASHI, K. & NAGATA, S. (1992). Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide. Neuron, 8, 811-819.
23. JIN, J.-G., KATSOULIS, S., SCHMIDT, W.E. & GRIDER, J.R (1994). Inhibitory transmission in tenia coli mediated by distinct vasoactive intestinal peptide and apamin-sensitive pituitary adenylate cyclase activating peptide receptors. J. Pharmacol. Exp. Ther., 270, 433-439.
24. KATSOULIS, S., SCHMIDT, W.E., FOLSCH, U.R., JIN, J.-G. & GRIDER, J.R. (1994). Inhibitory neurotransmission by PACAP in guinea pig stomach is mediated by VIP/PACAP-II receptors and by distinct apamin-sensitive receptors. Gastroenterology, 106, A519.
25. KOMORI, S. & OHASHI, H. (1990). Effects of vasoactive intestinal peptide on transmission from excitatory and inhibitory nerves to smooth muscle cells in chicken rectum. Eur. J. Pharmacol., 175, 21-28.
26. 2-adrenoceptor agonist, UK-14,304. Br. J. Pharmacol., 107, 256-261.
27. LEFEBVRE, R.A., SMITS, G.J.M. & TIMMERMANS, J.-P. (1995). Study of NO and VIP as non-adrenergic non-cholinergic neurotransmitters in the pig gastric fundus. Br. J. Pharmacol., 116, 2017-2026.
28. LI, C.G. & RAND, M.J. (1990). Nitric oxide and vasoactive intestinal polypeptide mediate non-adrenergic. non-cholinergic inhibitory transmission to smooth muscle of the rat gastric fundus. Eur. J. Pharmacol., 191, 303-309.
29. MAEHARA, T., FUJITA, A., SUTHAMNATPONG, N., TAKEUCHI, T. & HATA, F. (1994). Differences in relaxant effects of cyclic GMP on skinned muscle preparations from the proximal and distal colon of rats. Eur. J. Pharmacol., 261, 163-170.
30. MARTINS, S.L.R., DE OLIVEIRA, R.B. & BALLEJO, G. (1995). Rat duodenum nitrergic-induced relaxations are cGMP-independent and apamin-sensitive. Eur. J. Pharmacol., 284, 265-270.
31. MEERA, P., ANWER, K., MONGA, M., OBERTI, C., STEFANI, E., TORO, L. & SANBORN, B.M. (1995). Relaxin stimulates myometrial calcium-activated potassium channel activity via protein kinase A. Am. J. Physiol., 269, C312-C317.
32. MIDDLETON, S.J., CUTHBERT, A.W., SHORTHOUSE, M. & HUNTER, J.O. (1993). Nitric oxide affects mammalian distal colonic smooth muscle by tonic neural inhibition. Br. J. Pharmacol., 108, 974-979.
33. MIYATA, A., ARIMURA, A., DAHL, R.R., MINAMINO, N., UEHARA, A., JIANG, L., CULLER, M.D. & COY, D.H. (1989). Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem. Biophys. Res. Commun., 164, 567-574.
34. NURKO, S. & RATTAN, S. (1988). Role of vasoactive intestinal polypeptide in the internal anal sphincter of the opossum. J. Clin. Invest., 81, 1146-1153.
35. Ca channels by PKA in pregnant and nonpregnant myometrium. Am. J. Physiol., 266, C1459-C1463.
36. RATTAN, S. & CHAKDER, S. (1992). Role of nitric oxide as a mediator of internal anal sphincter relaxation. Am. J. Physiol., 262, G107-G112.
37. ROBERTSON, BE., SCHUBERT, R., HESCHELER, J. & NELSON, M.T. (1993). cGMP-dependent protein kinase activates Ca-activated K channels in cerebral artery smooth muscle cells. Am. J. Physiol., 265, C299-C303.
38. SADOSHIMA, J., AKAIKE, N., KANAIDE, H. & NAKAMURA, M. (1988). Cyclic AMP modulates Ca-activated K channel in cultured smooth muscle cells of rat aorta. Am. J. Physiol., 255, H754-H759.
39. SCHWORER, H., CLEMENS, A., KATSOULIS, S., KOHLER, H., CREUTZFELDT, W. & SCHMIDT, W.E. (1993). Pituitary adenylate cyclase-activating peptide is a potent modulator of human colonic motility. Scand. J. Gastroenterol., 28, 625-632.
40. SCHWORER, H., KATSOULIS, S., CREUTZFELDT, W. & SCHMIDT, W.E. (1992). Pituitary adenylate cyclase-activating peptide, a novel VIP-like gut-brain peptide, relaxes the guinea-pig taenia caeci via apamin-sensitive potassium channels. Naunyn-Schmiedeberg's Arch. Pharmacol., 346, 511-514.
41. SHUTTLEWORTH, C.W.R. & KEEF, K.D. (1995). Roles of peptides in enteric neuromuscular transmission. Regulat. Pept., 56, 101-120.
42. SPENGLER, D., WAEBER, C., PANTALONI, C., HOLSBOER, F., BOCKAERT, J., SEEBURG, P.H. & JOURNOT, L. (1993). Differential signal transduction by five splice variants of the PACAP receptor. Nature, 365, 170-175.
43. STARK, M.E., BAUER, A.J. & SZURZEWSKI, J.H. (1991). Effect of nitric oxide on circular muscle of the canine small intestine. J. Physiol., 444, 743-761.
44. SUTHAMNATPONG, N., HATA, F., KANADA, A., TAKEUCHI, T. & YAGASAKI, O. (1993a). Mediators of nonardrenergic, noncholinergic inhibition in the proximal, middle and distal regions of rat colon. Br. J. Pharmacol., 108, 348-355.
45. SUTHAMNATPONG, N., HOSOKAWA, M., TAKEUCHI, T., HATA, F. & TAKEWAKI, T. (1994). Nitric oxide-mediated inhibitory response of rat proximal colon: independence from changes in membrane potential. Br. J. Pharmacol., 112, 676-682.
46. SUTHAMNATPONG, N., MAEHARA, T., KANADA, A., TAKEUCHI, T. & HATA, F. (1993b). Dissociation of cyclic GMP level from relaxation of the distal, but not the proximal colon of rats. Jpn. J. Pharmacol., 62, 387-393.
47. TAKEUCHI, T., KISHI, M., ISHII, T., NISHIO, H. & HATA, F. (1996). Nitric oxide-mediated relaxation without concomitant change in cyclic GMP content of rat proximal colon. Br. J. Pharmacol., 117, 1204-1208.
48. TAKEWAKI, T. & OHASHI, H. (1977). Non-cholinergic, excitatory transmission to intestinal smooth muscle cells. Nature, 268, 749-750.
49. THORNBURY, K.D., WARD, S.M., DALZIEL, H.H., CARL, A., WESTFALL, D.P. & SANDERS, K.M. (1991). Nitric oxide and nitrosocysteine mimic nonadrenergic, noncholinergic hyperpolarization in canine proximal colon. Am. J. Physiol., 261, G553-G557.
50. WHITE, R.E., LEE, A.B., SHCHERBATKO, A.D., LINCOLN, T.M., SCHONBRUNN, A. & ARMSTRONG, D.L. (1993). Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature, 361, 263-266.