Modulation of Cholinergic and Substance P-like Neurotransmission by Nitric Oxide in the Guinea-pig Ileum

Overview

Journal Br J Pharmacol

Publisher Wiley

Specialty Pharmacology

Date 1993 Oct 1

PMID 7694759

Citations 21

Authors

C U Wiklund

C Olgart

N P Wiklund

L E Gustafsson

Affiliations

Soon will be listed here.

Abstract

1. The role of endogenous nitric oxide (NO) as a modulator of enteric neurotransmission was investigated in longitudinal muscle myenteric plexus (LMMP) preparations of guinea-pig isolated ileum. 2. In tissues previously incubated with [3H]-choline, exogenous NO inhibited electrically-evoked [3H]-choline overflow as well as responses to exogenous agonists, indicating that NO has the potential of neuromodulation both pre- and postjunctionally. 3. A series of NO synthase inhibitors enhanced contractile responses to nerve stimulation indicating inhibitory neuromodulation by endogenous NO. 4. The potency order of the NO synthase inhibitors and their consistent effects after dexamethasone, on responses to nerve stimulation, indicate action on a constitutive NO synthase. 5. Responses enhanced by NO synthase inhibitors were inhibited by the substance P receptor antagonist, spantide, suggesting a neuromodulatory influence on substance P-like neurotransmission by the endogenous NO. 6. NO synthase inhibition did not modify contractile responses to application of acetylcholine or substance P, or [3H]-choline overflow, indicating that endogenous NO mainly has a prejunctional inhibitory action on substance P-like neurotransmission. Nor did it modify responses to direct electrical muscle stimulation in the presence of tetrodotoxin. This suggests a prejunctional enhancing effect by NO synthesis inhibition. 7. Evidence for endogenous NO modulation of acetylcholine release was obtained when NO synthase inhibition modified atropine-sensitive, nerve-mediated contractile responses. However, [3H]-choline overflow was unaltered by NO synthase inhibition. 8. NO synthase inhibition did not modify responses to inhibitory neurotransmission. 9. The findings suggest that endogenous NO inhibits substance P-like motor neurotransmission, probably via prejunctional mechanisms. Cholinergic transmission may also be reduced by endogenous NO, acting prejunctionally.

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References

Patthy A, Bajusz S, Patthy L . Preparation and characterization of Ng-mono-, di- and trimethylated arginines. Acta Biochim Biophys Acad Sci Hung. 1977; 12(3):191-6. View

Kilbinger H . Modulation by oxotremorine and atropine of acetylcholine release evoked by electrical stimulation of the myenteric plexus of the guinea-pig ileum. Naunyn Schmiedebergs Arch Pharmacol. 1977; 300(2):145-51. DOI: 10.1007/BF00505045. View

Palmer R, Ferrige A, Moncada S . Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987; 327(6122):524-6. DOI: 10.1038/327524a0. View

Rimele T, Sturm R, Adams L, Henry D, Heaslip R, Weichman B . Interaction of neutrophils with vascular smooth muscle: identification of a neutrophil-derived relaxing factor. J Pharmacol Exp Ther. 1988; 245(1):102-11. View

Martin W, Smith J, Lewis M, Henderson A . Evidence that inhibitory factor extracted from bovine retractor penis is nitrite, whose acid-activated derivative is stabilized nitric oxide. Br J Pharmacol. 1988; 93(3):579-86. PMC: 1853840. DOI: 10.1111/j.1476-5381.1988.tb10313.x. View

Palmer R, Rees D, Ashton D, Moncada S . L-arginine is the physiological precursor for the formation of nitric oxide in endothelium-dependent relaxation. Biochem Biophys Res Commun. 1988; 153(3):1251-6. DOI: 10.1016/s0006-291x(88)81362-7. View

Garthwaite J, Charles S, Chess-Williams R . Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature. 1988; 336(6197):385-8. DOI: 10.1038/336385a0. View

Gillespie J, 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; 95(4):1151-6. PMC: 1854279. DOI: 10.1111/j.1476-5381.1988.tb11750.x. View

Knowles R, Palacios M, Palmer R, Moncada S . Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci U S A. 1989; 86(13):5159-62. PMC: 297577. DOI: 10.1073/pnas.86.13.5159. View

10.

McCall T, Boughton-Smith N, Palmer R, Whittle B, Moncada S . Synthesis of nitric oxide from L-arginine by neutrophils. Release and interaction with superoxide anion. Biochem J. 1989; 261(1):293-6. PMC: 1138817. DOI: 10.1042/bj2610293. View

11.

Palacios M, Knowles R, Palmer R, Moncada S . Nitric oxide from L-arginine stimulates the soluble guanylate cyclase in adrenal glands. Biochem Biophys Res Commun. 1989; 165(2):802-9. DOI: 10.1016/s0006-291x(89)80037-3. View

12.

Li C, Rand M . Evidence for a role of nitric oxide in the neurotransmitter system mediating relaxation of the rat anococcygeus muscle. Clin Exp Pharmacol Physiol. 1989; 16(12):933-8. DOI: 10.1111/j.1440-1681.1989.tb02404.x. View

13.

Bredt D, Snyder S . Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci U S A. 1990; 87(2):682-5. PMC: 53329. DOI: 10.1073/pnas.87.2.682. View

14.

Gibson A, Mirzazadeh S, Hobbs A, Moore P . L-NG-monomethyl arginine and L-NG-nitro arginine inhibit non-adrenergic, non-cholinergic relaxation of the mouse anococcygeus muscle. Br J Pharmacol. 1990; 99(3):602-6. PMC: 1917344. DOI: 10.1111/j.1476-5381.1990.tb12976.x. View

15.

Ignarro L, Bush P, Buga G, Wood K, Fukuto J, Rajfer J . Nitric oxide and cyclic GMP formation upon electrical field stimulation cause relaxation of corpus cavernosum smooth muscle. Biochem Biophys Res Commun. 1990; 170(2):843-50. DOI: 10.1016/0006-291x(90)92168-y. View

16.

Ignarro L, Bush P, Buga G, Rajfer J . Neurotransmitter identity doubt. Nature. 1990; 347(6289):131-2. DOI: 10.1038/347131b0. View

17.

Bredt D, Hwang P, Snyder S . Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature. 1990; 347(6295):768-70. DOI: 10.1038/347768a0. View

18.

Gustafsson L, Wiklund C, Wiklund N, Persson M, Moncada S . Modulation of autonomic neuroeffector transmission by nitric oxide in guinea pig ileum. Biochem Biophys Res Commun. 1990; 173(1):106-10. DOI: 10.1016/s0006-291x(05)81028-9. View

19.

Rees D, Cellek S, Palmer R, Moncada S . Dexamethasone prevents the induction by endotoxin of a nitric oxide synthase and the associated effects on vascular tone: an insight into endotoxin shock. Biochem Biophys Res Commun. 1990; 173(2):541-7. DOI: 10.1016/s0006-291x(05)80068-3. View

20.

Rees D, Palmer R, Schulz R, HODSON H, Moncada S . Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol. 1990; 101(3):746-52. PMC: 1917753. DOI: 10.1111/j.1476-5381.1990.tb14151.x. View