Abstract
1. Radioimmunological techniques were used in isolated guinea-pig inferior mesenteric ganglion (IMG)-colon preparations to determine whether opioid peptides and neurotensin8-13 (NT8-13), the C-terminal region of NT1-13 recognized by neurotensin receptors, modulate distension-induced release of substance P (SP)- and vasoactive intestinal polypeptide (VIP)-like immunoreactive (LI) material. 2. Colonic distension significantly increased the amount of SP- and VIP-LI material released in the ganglionic superfusate. A low-Ca2+ (0.1 mM), high-Mg2+ (15 mM) solution blocked their release. 3. In vivo capsaicin pretreatment abolished release of SP-LI material during colonic distension but had no significant effect on distension-induced release of VIP-LI material. 4. The addition of [Leu5]enkephalin, [Met5]enkephalin, PL017 (a mu-receptor agonist) and DPDPE (a delta-receptor agonist) to the ganglion side of a two-compartment chamber blocked distension-induced release of SP-LI material. The addition of naloxone and ICI-174,864 (a delta-receptor antagonist) to the ganglion compartment reversed the inhibitory effect of the mu- and delta-receptor agonists. 5. Addition of [Leu5]enkephalin and [Met5]enkephalin to the ganglion compartment had no significant effect on release of VIP-LI material during colonic distension. 6. Addition of NT8-13 to the ganglion compartment significantly increased in the amount of SP-LI material released during colonic distension but had no affect on distension-induced release of VIP-LI material. 7. The results suggest the hypothesis that under in vivo conditions, enkephalinergic nerves decrease and neurotensinergic nerves increase the release of SP from peripheral branches of primary afferent sensory nerves.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baron R., Jänig W., McLachlan E. M. The afferent and sympathetic components of the lumbar spinal outflow to the colon and pelvic organs in the cat. II. The lumbar splanchnic nerves. J Comp Neurol. 1985 Aug 8;238(2):147–157. doi: 10.1002/cne.902380203. [DOI] [PubMed] [Google Scholar]
- Chang K. J., Wei E. T., Killian A., Chang J. K. Potent morphiceptin analogs: structure activity relationships and morphine-like activities. J Pharmacol Exp Ther. 1983 Nov;227(2):403–408. [PubMed] [Google Scholar]
- Chavkin C., James I. F., Goldstein A. Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science. 1982 Jan 22;215(4531):413–415. doi: 10.1126/science.6120570. [DOI] [PubMed] [Google Scholar]
- Crowcroft P. J., Szurszewski J. H. A study of the inferior mesenteric and pelvic ganglia of guinea-pigs with intracellular electrodes. J Physiol. 1971 Dec;219(2):421–441. doi: 10.1113/jphysiol.1971.sp009670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dalsgaard C. J., Hökfelt T., Schultzberg M., Lundberg J. M., Terenius L., Dockray G. J., Goldstein M. Origin of peptide-containing fibers in the inferior mesenteric ganglion of the guinea-pig: immunohistochemical studies with antisera to substance P, enkephalin, vasoactive intestinal polypeptide, cholecystokinin and bombesin. Neuroscience. 1983 May;9(1):191–211. doi: 10.1016/0306-4522(83)90056-8. [DOI] [PubMed] [Google Scholar]
- Dalsgaard C. J., Vincent S. R., Hökfelt V. T., Christensson I., Terenius L. Separate origins for the dynorphin and enkephalin immunoreactive fibers in the inferior mesenteric ganglion of the guinea pig. J Comp Neurol. 1983 Dec 20;221(4):482–489. doi: 10.1002/cne.902210410. [DOI] [PubMed] [Google Scholar]
- Dun N. J., Jiang Z. G. Non-cholinergic excitatory transmission in inferior mesenteric ganglia of the guinea-pig: possible mediation by substance P. J Physiol. 1982 Apr;325:145–159. doi: 10.1113/jphysiol.1982.sp014141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dun N. J., Kiraly M. Capsaicin causes release of a substance P-like peptide in guinea-pig inferior mesenteric ganglia. J Physiol. 1983 Jul;340:107–120. doi: 10.1113/jphysiol.1983.sp014752. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elfvin L. G., Dalsgaard C. J. Retrograde axonal transport of horseradish perioxidase in afferent fibers of the inferior mesenteric ganglion of the guinea pig. Identification of the cells of origin in dorsal root ganglia. Brain Res. 1977 Apr 22;126(1):149–153. doi: 10.1016/0006-8993(77)90221-9. [DOI] [PubMed] [Google Scholar]
- Gamse R., Wax A., Zigmond R. E., Leeman S. E. Immunoreactive substance P in sympathetic ganglia: distribution and sensitivity towards capsaicin. Neuroscience. 1981;6(3):437–441. doi: 10.1016/0306-4522(81)90136-6. [DOI] [PubMed] [Google Scholar]
- Heym C., Reinecke M., Weihe E., Forssmann W. G. Dopamine-beta-hydroxylase-, neurotensin-, substance P-, vasoactive intestinal polypeptide- and enkephalin-immunohistochemistry of paravertebral and prevertebral ganglia in the cat. Cell Tissue Res. 1984;235(2):411–418. doi: 10.1007/BF00217867. [DOI] [PubMed] [Google Scholar]
- Hökfelt T., Elfvin L. G., Schultzberg M., Goldstein M., Nilsson G. On the occurrence of substance P-containing fibers in sympathetic ganglia: immunohistochemical evidence. Brain Res. 1977 Aug 19;132(1):29–41. doi: 10.1016/0006-8993(77)90704-1. [DOI] [PubMed] [Google Scholar]
- Katayama Y., North R. A. Does substance P mediate slow synaptic excitation within the myenteric plexus? Nature. 1978 Jul 27;274(5669):387–388. doi: 10.1038/274387a0. [DOI] [PubMed] [Google Scholar]
- Kondo H., Kuramoto H., Wainer B. H., Yanaihara N. Evidence for the coexistence of acetylcholine and enkephalin in the sympathetic preganglionic neurons of rats. Brain Res. 1985 Jun 3;335(2):309–314. doi: 10.1016/0006-8993(85)90483-4. [DOI] [PubMed] [Google Scholar]
- Kosterlitz H. W. The Wellcome Foundation lecture, 1982. Opioid peptides and their receptors. Proc R Soc Lond B Biol Sci. 1985 Jul 22;225(1238):27–40. doi: 10.1098/rspb.1985.0048. [DOI] [PubMed] [Google Scholar]
- Kuo D. C., Krauthamer G. M., Yamasaki D. S. The organization of visceral sensory neurons in thoracic dorsal root ganglia (DRG) of the cat studied by horseradish peroxidase (HRP) reaction using the cryostat. Brain Res. 1981 Mar 9;208(1):187–191. doi: 10.1016/0006-8993(81)90630-2. [DOI] [PubMed] [Google Scholar]
- Love J. A., Szurszewski J. H. The electrophysiological effects of vasoactive intestinal polypeptide in the guinea-pig inferior mesenteric ganglion. J Physiol. 1987 Dec;394:67–84. doi: 10.1113/jphysiol.1987.sp016860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lundberg J. M., Rökaeus A., Hökfelt T., Rosell S., Brown M., Goldstein M. Neurotensin-like immunoreactivity in the preganglionic sympathetic nerves and in the adrenal medulla of the cat. Acta Physiol Scand. 1982 Jan;114(1):153–155. doi: 10.1111/j.1748-1716.1982.tb06965.x. [DOI] [PubMed] [Google Scholar]
- Matthews M. R., Cuello A. C. Substance P-immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1668–1672. doi: 10.1073/pnas.79.5.1668. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matthews M. R., Cuello A. C. The origin and possible significance of substance P immunoreactive networks in the prevertebral ganglia and related structures in the guinea-pig. Philos Trans R Soc Lond B Biol Sci. 1984 Aug 14;306(1128):247–276. doi: 10.1098/rstb.1984.0087. [DOI] [PubMed] [Google Scholar]
- Micevych P. E., Yaksh T. L., Go V. L. Opiate-mediated inhibition of the release of cholecystokinin and substance P, but not neurotensin from cat hypothalamic slices. Brain Res. 1982 Nov 4;250(2):283–289. doi: 10.1016/0006-8993(82)90422-x. [DOI] [PubMed] [Google Scholar]
- Mo N., Dun N. J. Cholecystokinin octapeptide depolarizes guinea pig inferior mesenteric ganglion cells and facilitates nicotinic transmission. Neurosci Lett. 1986 Mar 14;64(3):263–268. doi: 10.1016/0304-3940(86)90339-3. [DOI] [PubMed] [Google Scholar]
- Nishi S., Koketsu K. Early and late after discharges of amphibian sympathetic ganglion cells. J Neurophysiol. 1968 Jan;31(1):109–121. doi: 10.1152/jn.1968.31.1.109. [DOI] [PubMed] [Google Scholar]
- Parkman H. P., Ma R. C., Stapelfeldt W. H., Szurszewski J. H. Direct and indirect mechanosensory pathways from the colon to the inferior mesenteric ganglion. Am J Physiol. 1993 Sep;265(3 Pt 1):G499–G505. doi: 10.1152/ajpgi.1993.265.3.G499. [DOI] [PubMed] [Google Scholar]
- Peters S., Kreulen D. L. Vasopressin-mediated slow EPSPs in a mammalian sympathetic ganglion. Brain Res. 1985 Jul 22;339(1):126–129. doi: 10.1016/0006-8993(85)90630-4. [DOI] [PubMed] [Google Scholar]
- Reinecke M., Forssmann W. G., Thiekötter G., Triepel J. Localization of neurotensin-immunoreactivity in the spinal cord and peripheral nervous system of the guinea pig. Neurosci Lett. 1983 May 27;37(1):37–42. doi: 10.1016/0304-3940(83)90501-3. [DOI] [PubMed] [Google Scholar]
- Saria A., Ma R. C., Dun N. J. Neurokinin A depolarizes neurons of the guinea pig inferior mesenteric ganglia. Neurosci Lett. 1985 Sep 30;60(2):145–150. doi: 10.1016/0304-3940(85)90235-6. [DOI] [PubMed] [Google Scholar]
- Schultzberg M., Hökfelt T., Terenius L., Elfvin L. G., Lundberg J. M., Brandt J., Elde R. P., Goldstein M. Enkephalin immunoreactive nerve fibres and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neuroscience. 1979;4(2):249–270. doi: 10.1016/0306-4522(79)90087-3. [DOI] [PubMed] [Google Scholar]
- Schumann M. A., Kreulen D. L. Action of cholecystokinin octapeptide and CCK-related peptides on neurons in inferior mesenteric ganglion of guinea pig. J Pharmacol Exp Ther. 1986 Nov;239(2):618–625. [PubMed] [Google Scholar]
- Stapelfeldt W. H., Szurszewski J. H. Central neurotensin nerves modulate colo-colonic reflex activity in the guinea-pig inferior mesenteric ganglion. J Physiol. 1989 Apr;411:347–365. doi: 10.1113/jphysiol.1989.sp017577. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stapelfeldt W. H., Szurszewski J. H. Neurotensin facilitates release of substance P in the guinea-pig inferior mesenteric ganglion. J Physiol. 1989 Apr;411:325–345. doi: 10.1113/jphysiol.1989.sp017576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takemori A. E., Ho B. Y., Naeseth J. S., Portoghese P. S. Nor-binaltorphimine, a highly selective kappa-opioid antagonist in analgesic and receptor binding assays. J Pharmacol Exp Ther. 1988 Jul;246(1):255–258. [PubMed] [Google Scholar]
- Tsunoo A., Konishi S., Otsuka M. Substance P as an excitatory transmitter of primary afferent neurons in guinea-pig sympathetic ganglia. Neuroscience. 1982;7(9):2025–2037. doi: 10.1016/0306-4522(82)90117-8. [DOI] [PubMed] [Google Scholar]
- Vonvoigtlander P. F., Lahti R. A., Ludens J. H. U-50,488: a selective and structurally novel non-Mu (kappa) opioid agonist. J Pharmacol Exp Ther. 1983 Jan;224(1):7–12. [PubMed] [Google Scholar]
- Yaksh T. L., Abay E. O., 2nd, Go V. L. Studies on the location and release of cholecystokinin and vasoactive intestinal peptide in rat and cat spinal cord. Brain Res. 1982 Jun 24;242(2):279–290. doi: 10.1016/0006-8993(82)90311-0. [DOI] [PubMed] [Google Scholar]