Skip to main content
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1995 Jan;114(2):428–432. doi: 10.1111/j.1476-5381.1995.tb13244.x

Pharmacological evidence that nitric oxide may be a retrograde messenger in the enteric nervous system.

S Y Yuan 1, J C Bornstein 1, J B Furness 1
PMCID: PMC1510253  PMID: 7533617

Abstract

1. The effects of inhibition of nitric oxide synthase on neuro-neuronal and neuromuscular transmission during motility reflexes in the small intestine of the guinea-pig were examined. 2. Isolated segments of intestine were secured in a three chambered organ bath so that different parts of the reflex pathways could be independently exposed to drug-containing solutions. Reflexes were evoked by distension or compression of the mucosa in two adjacent chambers and reflex responses were recorded from the circular muscle with intracellular microelectrodes in the third chamber. Thus, the actions of drugs at connections between sensory neurones and interneurones, between interneurones and other interneurones and at motor neurones could be distinguished. 3. NG-monomethyl-L-arginine (L-NMMA; 100 microM), an inhibitor of nitric oxide synthase, did not affect the ascending excitatory reflex when added to either the central stimulation chamber or the recording chamber. 4. In contrast, L-NMMA (100 microM) enhanced the descending inhibitory reflex when added to the chamber in which stimuli were applied. This effect was prevented by prior exposure to L-arginine (100 microM), which had no effect by itself. Conduction of reflexes between the stimulus chamber and the recording chamber was unaffected by the presence of L-NMMA in an intervening chamber. 5. L-NMMA (100 microM) added to the recording chamber depressed the descending inhibitory reflex, an effect that was prevented by previous exposure to L-arginine. 6. The nitric oxide donor, sodium nitroprusside (100 microM), added to the stimulus chamber, depressed both ascending excitatory and descending inhibitory reflexes.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
428

Selected References

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

  1. Bayliss W. M., Starling E. H. The movements and innervation of the small intestine. J Physiol. 1899 May 11;24(2):99–143. doi: 10.1113/jphysiol.1899.sp000752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bornstein J. C., Furness J. B., Smith T. K., Trussell D. C. Synaptic responses evoked by mechanical stimulation of the mucosa in morphologically characterized myenteric neurons of the guinea-pig ileum. J Neurosci. 1991 Feb;11(2):505–518. doi: 10.1523/JNEUROSCI.11-02-00505.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bornstein J. C., Hendriks R., Furness J. B., Trussell D. C. Ramifications of the axons of AH-neurons injected with the intracellular marker biocytin in the myenteric plexus of the guinea pig small intestine. J Comp Neurol. 1991 Dec 15;314(3):437–451. doi: 10.1002/cne.903140303. [DOI] [PubMed] [Google Scholar]
  4. Costa M., Furness J. B., Pompolo S., Brookes S. J., Bornstein J. C., Bredt D. S., Snyder S. H. Projections and chemical coding of neurons with immunoreactivity for nitric oxide synthase in the guinea-pig small intestine. Neurosci Lett. 1992 Dec 14;148(1-2):121–125. doi: 10.1016/0304-3940(92)90819-s. [DOI] [PubMed] [Google Scholar]
  5. Kunze W. A., Furness J. B., Bornstein J. C. Simultaneous intracellular recordings from enteric neurons reveal that myenteric AH neurons transmit via slow excitatory postsynaptic potentials. Neuroscience. 1993 Aug;55(3):685–694. doi: 10.1016/0306-4522(93)90434-h. [DOI] [PubMed] [Google Scholar]
  6. Lyster D. J., Bywater R. A., Taylor G. S., Watson M. J. Effects of a nitric oxide synthase inhibitor on non-cholinergic junction potentials in the circular muscle of the guinea pig ileum. J Auton Nerv Syst. 1992 Dec;41(3):187–196. doi: 10.1016/0165-1838(92)90058-o. [DOI] [PubMed] [Google Scholar]
  7. McConalogue K., Furness J. B. Projections of nitric oxide synthesizing neurons in the guinea-pig colon. Cell Tissue Res. 1993 Mar;271(3):545–553. doi: 10.1007/BF02913739. [DOI] [PubMed] [Google Scholar]
  8. Moncada S., Palmer R. M., Higgs E. A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991 Jun;43(2):109–142. [PubMed] [Google Scholar]
  9. Niel J. P., Bywater R. A., Taylor G. S. Apamin-resistant post-stimulus hyperpolarization in the circular muscle of the guinea-pig ileum. J Auton Nerv Syst. 1983 Nov;9(2-3):565–569. doi: 10.1016/0165-1838(83)90014-0. [DOI] [PubMed] [Google Scholar]
  10. Sanders K. M., Ward S. M. Nitric oxide as a mediator of nonadrenergic noncholinergic neurotransmission. Am J Physiol. 1992 Mar;262(3 Pt 1):G379–G392. doi: 10.1152/ajpgi.1992.262.3.G379. [DOI] [PubMed] [Google Scholar]
  11. Smith T. K., Bornstein J. C., Furness J. B. Distension-evoked ascending and descending reflexes in the circular muscle of guinea-pig ileum: an intracellular study. J Auton Nerv Syst. 1990 Mar;29(3):203–217. doi: 10.1016/0165-1838(90)90146-a. [DOI] [PubMed] [Google Scholar]
  12. Smith T. K., Furness J. B. Reflex changes in circular muscle activity elicited by stroking the mucosa: an electrophysiological analysis in the isolated guinea-pig ileum. J Auton Nerv Syst. 1988 Dec;25(2-3):205–218. doi: 10.1016/0165-1838(88)90025-2. [DOI] [PubMed] [Google Scholar]
  13. Stark M. E., Szurszewski J. H. Role of nitric oxide in gastrointestinal and hepatic function and disease. Gastroenterology. 1992 Dec;103(6):1928–1949. doi: 10.1016/0016-5085(92)91454-c. [DOI] [PubMed] [Google Scholar]
  14. Tamura K., Schemann M., Wood J. D. Actions of nitric oxide-generating sodium nitroprusside in myenteric plexus of guinea pig small intestine. Am J Physiol. 1993 Nov;265(5 Pt 1):G887–G893. doi: 10.1152/ajpgi.1993.265.5.G887. [DOI] [PubMed] [Google Scholar]
  15. Vincent S. R., Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience. 1992;46(4):755–784. doi: 10.1016/0306-4522(92)90184-4. [DOI] [PubMed] [Google Scholar]
  16. Yuan S. Y., Bornstein J. C., Furness J. B. Investigation of the role of 5-HT3 and 5-HT4 receptors in ascending and descending reflexes to the circular muscle of guinea-pig small intestine. Br J Pharmacol. 1994 Aug;112(4):1095–1100. doi: 10.1111/j.1476-5381.1994.tb13196.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Yuan S. Y., Furness J. B., Bornstein J. C. Post-stimulus depression of reflex changes in circular muscle activity in the guinea pig small intestine. J Auton Nerv Syst. 1992 Oct;40(3):171–180. doi: 10.1016/0165-1838(92)90198-p. [DOI] [PubMed] [Google Scholar]
  18. Yuan S. Y., Furness J. B., Bornstein J. C., Smith T. K. Mucosal distortion by compression elicits polarized reflexes and enhances responses of the circular muscle to distension in the small intestine. J Auton Nerv Syst. 1991 Sep;35(3):219–226. doi: 10.1016/0165-1838(91)90100-h. [DOI] [PubMed] [Google Scholar]

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

RESOURCES