Skip to main content
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1994 Jun;112(2):676–682. doi: 10.1111/j.1476-5381.1994.tb13129.x

Nitric oxide-mediated inhibitory response of rat proximal colon: independence from changes in membrane potential.

N Suthamnatpong 1, M Hosokawa 1, T Takeuchi 1, F Hata 1, T Takewaki 1
PMCID: PMC1910383  PMID: 7521262

Abstract

1. We studied the relation of nitric oxide-mediated relaxation of smooth muscle to changes in membrane potential of cells in the proximal colon of rats. 2. The resting membrane potential and electrical field stimulation (EFS)-induced junction potentials were recorded from the circular and longitudinal muscle cells. 3. Localized distension with a small balloon caused relaxation of the circular muscle on the anal side of the distended region (descending relaxation). Relaxation of the longitudinal muscle was also induced by EFS. 4. Inhibitory junction potentials (i.j.ps) were recorded from all circular muscle cells tested, but rarely from the longitudinal muscle cells. 5. The i.j.ps were recorded only in the presence of atropine but relaxations of both muscles were induced even in the absence of atropine. 6. Apamin (100 nM) completely abolished the i.j.ps recorded in both circular and longitudinal muscle cells, but had no significant effect on the relaxations of either. 7. In contrast to apamin, Ng nitro-L-arginine (10 microM) inhibited the relaxations of both muscles, but did not affect the i.j.ps. 8. Exogenously added nitric oxide (0.1-10 microM) induced relaxations of both muscles concentration-dependently, but did not affect the membrane potentials at these concentrations. 9. These data strongly suggest that nitric oxide-mediated relaxation of rat proximal colon is not associated with the i.j.ps of the cell membrane.

Full text

PDF
676

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amano M., Goto A., Sakai A., Achiha M., nee Hara, Takahashi N., Hara C., Ogawa N. Comparison of the anticonflict effect of buspirone and its major metabolite 1-(2-pyrimidinyl)-piperazine (1-PP) in rats. Jpn J Pharmacol. 1993 Apr;61(4):311–317. doi: 10.1254/jjp.61.311. [DOI] [PubMed] [Google Scholar]
  2. Arnold W. P., Mittal C. K., Katsuki S., Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3':5'-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3203–3207. doi: 10.1073/pnas.74.8.3203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnette M. S., Barone F. C., Fowler P. J., Grous M., Price W. J., Ormsbee H. S. Human lower oesophageal sphincter relaxation is associated with raised cyclic nucleotide content. Gut. 1991 Jan;32(1):4–9. doi: 10.1136/gut.32.1.4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barnette M., Torphy T. J., Grous M., Fine C., Ormsbee H. S., 3rd Cyclic GMP: a potential mediator of neurally- and drug-induced relaxation of opossum lower esophageal sphincter. J Pharmacol Exp Ther. 1989 May;249(2):524–528. [PubMed] [Google Scholar]
  5. Boeckxstaens G. E., Pelckmans P. A., Bogers J. J., Bult H., De Man J. G., Oosterbosch L., Herman A. G., Van Maercke Y. M. Release of nitric oxide upon stimulation of nonadrenergic noncholinergic nerves in the rat gastric fundus. J Pharmacol Exp Ther. 1991 Feb;256(2):441–447. [PubMed] [Google Scholar]
  6. Boeckxstaens G. E., Pelckmans P. A., Bult H., De Man J. G., Herman A. G., Van Maercke Y. M. Non-adrenergic non-cholinergic relaxation mediated by nitric oxide in the canine ileocolonic junction. Eur J Pharmacol. 1990 Nov 6;190(1-2):239–246. doi: 10.1016/0014-2999(90)94132-h. [DOI] [PubMed] [Google Scholar]
  7. Brayden J. E. Membrane hyperpolarization is a mechanism of endothelium-dependent cerebral vasodilation. Am J Physiol. 1990 Sep;259(3 Pt 2):H668–H673. doi: 10.1152/ajpheart.1990.259.3.H668. [DOI] [PubMed] [Google Scholar]
  8. Bult H., Boeckxstaens G. E., Pelckmans P. A., Jordaens F. H., Van Maercke Y. M., Herman A. G. Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature. 1990 May 24;345(6273):346–347. doi: 10.1038/345346a0. [DOI] [PubMed] [Google Scholar]
  9. Carl A., Sanders K. M. Ca2+-activated K channels of canine colonic myocytes. Am J Physiol. 1989 Sep;257(3 Pt 1):C470–C480. doi: 10.1152/ajpcell.1989.257.3.C470. [DOI] [PubMed] [Google Scholar]
  10. Chen G., Suzuki H. Some electrical properties of the endothelium-dependent hyperpolarization recorded from rat arterial smooth muscle cells. J Physiol. 1989 Mar;410:91–106. doi: 10.1113/jphysiol.1989.sp017522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chen G., Suzuki H., Weston A. H. Acetylcholine releases endothelium-derived hyperpolarizing factor and EDRF from rat blood vessels. Br J Pharmacol. 1988 Dec;95(4):1165–1174. doi: 10.1111/j.1476-5381.1988.tb11752.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Christinck F., Jury J., Cayabyab F., Daniel E. E. Nitric oxide may be the final mediator of nonadrenergic, noncholinergic inhibitory junction potentials in the gut. Can J Physiol Pharmacol. 1991 Oct;69(10):1448–1458. doi: 10.1139/y91-217. [DOI] [PubMed] [Google Scholar]
  13. Dalziel H. H., Thornbury K. D., Ward S. M., Sanders K. M. Involvement of nitric oxide synthetic pathway in inhibitory junction potentials in canine proximal colon. Am J Physiol. 1991 May;260(5 Pt 1):G789–G792. doi: 10.1152/ajpgi.1991.260.5.G789. [DOI] [PubMed] [Google Scholar]
  14. Desai K. M., Sessa W. C., Vane J. R. Involvement of nitric oxide in the reflex relaxation of the stomach to accommodate food or fluid. Nature. 1991 Jun 6;351(6326):477–479. doi: 10.1038/351477a0. [DOI] [PubMed] [Google Scholar]
  15. Garland C. J., McPherson G. A. Evidence that nitric oxide does not mediate the hyperpolarization and relaxation to acetylcholine in the rat small mesenteric artery. Br J Pharmacol. 1992 Feb;105(2):429–435. doi: 10.1111/j.1476-5381.1992.tb14270.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gillespie J. S., Sheng H. Influence of haemoglobin and erythrocytes on the effects of EDRF, a smooth muscle inhibitory factor, and nitric oxide on vascular and non-vascular smooth muscle. Br J Pharmacol. 1988 Dec;95(4):1151–1156. doi: 10.1111/j.1476-5381.1988.tb11750.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hamaguchi M., Ishibashi T., Imai S. Involvement of charybdotoxin-sensitive K+ channel in the relaxation of bovine tracheal smooth muscle by glyceryl trinitrate and sodium nitroprusside. J Pharmacol Exp Ther. 1992 Jul;262(1):263–270. [PubMed] [Google Scholar]
  18. Hata F., Ishii T., Kanada A., Yamano N., Kataoka T., Takeuchi T., Yagasaki O. Essential role of nitric oxide in descending inhibition in the rat proximal colon. Biochem Biophys Res Commun. 1990 Nov 15;172(3):1400–1406. doi: 10.1016/0006-291x(90)91605-r. [DOI] [PubMed] [Google Scholar]
  19. Hata F., Kataoka T., Takeuchi T., Yagasaki O., Yamano N. Differences in control of descending inhibition in the proximal and distal regions of rat colon. Br J Pharmacol. 1990 Dec;101(4):1011–1015. doi: 10.1111/j.1476-5381.1990.tb14198.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Huang A. H., Busse R., Bassenge E. Endothelium-dependent hyperpolarization of smooth muscle cells in rabbit femoral arteries is not mediated by EDRF (nitric oxide). Naunyn Schmiedebergs Arch Pharmacol. 1988 Oct;338(4):438–442. doi: 10.1007/BF00172124. [DOI] [PubMed] [Google Scholar]
  21. Kanada A., Hata F., Suthamnatpong N., Maehara T., Ishii T., Takeuchi T., Yagasaki O. Key roles of nitric oxide and cyclic GMP in nonadrenergic and noncholinergic inhibition in rat ileum. Eur J Pharmacol. 1992 Jun 5;216(2):287–292. doi: 10.1016/0014-2999(92)90372-b. [DOI] [PubMed] [Google Scholar]
  22. Komori K., Lorenz R. R., Vanhoutte P. M. Nitric oxide, ACh, and electrical and mechanical properties of canine arterial smooth muscle. Am J Physiol. 1988 Jul;255(1 Pt 2):H207–H212. doi: 10.1152/ajpheart.1988.255.1.H207. [DOI] [PubMed] [Google Scholar]
  23. Li C. G., Rand M. J. Evidence that part of the NANC relaxant response of guinea-pig trachea to electrical field stimulation is mediated by nitric oxide. Br J Pharmacol. 1991 Jan;102(1):91–94. doi: 10.1111/j.1476-5381.1991.tb12137.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Murray J., Du C., Ledlow A., Bates J. N., Conklin J. L. Nitric oxide: mediator of nonadrenergic noncholinergic responses of opossum esophageal muscle. Am J Physiol. 1991 Sep;261(3 Pt 1):G401–G406. doi: 10.1152/ajpgi.1991.261.3.G401. [DOI] [PubMed] [Google Scholar]
  25. Nagao T., Vanhoutte P. M. Hyperpolarization contributes to endothelium-dependent relaxations to acetylcholine in femoral veins of rats. Am J Physiol. 1991 Oct;261(4 Pt 2):H1034–H1037. doi: 10.1152/ajpheart.1991.261.4.H1034. [DOI] [PubMed] [Google Scholar]
  26. Plane F., Garland C. J. Differential effects of acetylcholine, nitric oxide and levcromakalim on smooth muscle membrane potential and tone in the rabbit basilar artery. Br J Pharmacol. 1993 Oct;110(2):651–656. doi: 10.1111/j.1476-5381.1993.tb13861.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rand V. E., Garland C. J. Endothelium-dependent relaxation to acetylcholine in the rabbit basilar artery: importance of membrane hyperpolarization. Br J Pharmacol. 1992 May;106(1):143–150. doi: 10.1111/j.1476-5381.1992.tb14307.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rattan S., Sarkar A., Chakder S. Nitric oxide pathway in rectoanal inhibitory reflex of opossum internal anal sphincter. Gastroenterology. 1992 Jul;103(1):43–50. doi: 10.1016/0016-5085(92)91093-j. [DOI] [PubMed] [Google Scholar]
  29. Shikano K., Long C. J., Ohlstein E. H., Berkowitz B. A. Comparative pharmacology of endothelium-derived relaxing factor and nitric oxide. J Pharmacol Exp Ther. 1988 Dec;247(3):873–881. [PubMed] [Google Scholar]
  30. Stark M. E., Bauer A. J., Szurszewski J. H. Effect of nitric oxide on circular muscle of the canine small intestine. J Physiol. 1991 Dec;444:743–761. doi: 10.1113/jphysiol.1991.sp018904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Suthamnatpong N., Hata F., Kanada A., Takeuchi T., Yagasaki O. Mediators of nonadrenergic, noncholinergic inhibition in the proximal, middle and distal regions of rat colon. Br J Pharmacol. 1993 Feb;108(2):348–355. doi: 10.1111/j.1476-5381.1993.tb12808.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Suthamnatpong N., Maehara T., Kanada A., Takeuchi T., Hata F. Dissociation of cyclic GMP level from relaxation of the distal, but not the proximal colon of rats. Jpn J Pharmacol. 1993 Aug;62(4):387–393. doi: 10.1254/jjp.62.387. [DOI] [PubMed] [Google Scholar]
  33. Takewaki T., Ohashi O. Non-cholinergic excitatory transmission to intestinal smooth muscle cells. Nature. 1977 Aug 25;268(5622):749–750. doi: 10.1038/268749a0. [DOI] [PubMed] [Google Scholar]
  34. Tare M., Parkington H. C., Coleman H. A., Neild T. O., Dusting G. J. Hyperpolarization and relaxation of arterial smooth muscle caused by nitric oxide derived from the endothelium. Nature. 1990 Jul 5;346(6279):69–71. doi: 10.1038/346069a0. [DOI] [PubMed] [Google Scholar]
  35. Thornbury K. D., Ward S. M., Dalziel H. H., Carl A., Westfall D. P., Sanders K. M. Nitric oxide and nitrosocysteine mimic nonadrenergic, noncholinergic hyperpolarization in canine proximal colon. Am J Physiol. 1991 Sep;261(3 Pt 1):G553–G557. doi: 10.1152/ajpgi.1991.261.3.G553. [DOI] [PubMed] [Google Scholar]
  36. Toda N., Baba H., Okamura T. Role of nitric oxide in non-adrenergic, non-cholinergic nerve-mediated relaxation in dog duodenal longitudinal muscle strips. Jpn J Pharmacol. 1990 Jun;53(2):281–284. doi: 10.1254/jjp.53.281. [DOI] [PubMed] [Google Scholar]
  37. Torphy T. J., Fine C. F., Burman M., Barnette M. S., Ormsbee H. S., 3rd Lower esophageal sphincter relaxation is associated with increased cyclic nucleotide content. Am J Physiol. 1986 Dec;251(6 Pt 1):G786–G793. doi: 10.1152/ajpgi.1986.251.6.G786. [DOI] [PubMed] [Google Scholar]
  38. Tøttrup A., Svane D., Forman A. Nitric oxide mediating NANC inhibition in opossum lower esophageal sphincter. Am J Physiol. 1991 Mar;260(3 Pt 1):G385–G389. doi: 10.1152/ajpgi.1991.260.3.G385. [DOI] [PubMed] [Google Scholar]
  39. Ward S. M., Dalziel H. H., Bradley M. E., Buxton I. L., Keef K., Westfall D. P., Sanders K. M. Involvement of cyclic GMP in non-adrenergic, non-cholinergic inhibitory neurotransmission in dog proximal colon. Br J Pharmacol. 1992 Dec;107(4):1075–1082. doi: 10.1111/j.1476-5381.1992.tb13409.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ward S. M., McKeen E. S., Sanders K. M. Role of nitric oxide in non-adrenergic, non-cholinergic inhibitory junction potentials in canine ileocolonic sphincter. Br J Pharmacol. 1992 Apr;105(4):776–782. doi: 10.1111/j.1476-5381.1992.tb09056.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES