Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1986 Oct;379:61–82. doi: 10.1113/jphysiol.1986.sp016241

Peptidergic modulation of the membrane potential of the Schwann cell of the squid giant nerve fibre.

P D Evans, V Reale, J Villegas
PMCID: PMC1182885  PMID: 2435897

Abstract

The effects of a range of neuropeptides were investigated on the membrane potential of the Schwann cells of the giant nerve fibre of the tropical squid. Vasoactive intestinal peptide (VIP) produced a dose-dependent, long-lasting hyperpolarization of the Schwann-cell membrane potential. Among peptides structurally related to VIP, similar effects were produced by peptide histidine isoleucine (PHI) but not by secretin and glucagon. Substance P and somatostatin also hyperpolarized the Schwann-cell membrane potential but via receptor systems distinct from those activated by VIP. Methionine enkephalin ([Met]-enkephalin) blocked the actions of all the above peptides as well as the effects of DL-octopamine and carbachol. The actions of [Met]-enkephalin upon the VIP responses were antagonized by naloxone. VIP produces its effects on the Schwann-cell membrane potential via a receptor system that is independent from those described previously which mediate the effects of carbachol and DL-octopamine. However, VIP can potentiate the effects of the latter systems. The actions of VIP on the Schwann cell are unlikely to be mediated via changes in adenosine 3',5'-cyclic monophosphate (cyclic AMP) levels and are insensitive to changes in the level of extracellular calcium in the superfusate. The actions of VIP are, however, potentiated in the presence of low concentrations of lithium ions suggesting that the VIP receptor may mediate its effects by inducing the hydrolysis of polyphosphatidylinositols in the Schwann-cell membrane. Evidence is presented for the existence of an endogenous VIP-like component in the normal hyperpolarizing action of giant-axon activity on the membrane potential of the Schwann cell.

Full text

PDF
61

Selected References

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

  1. Berridge M. J., Downes C. P., Hanley M. R. Lithium amplifies agonist-dependent phosphatidylinositol responses in brain and salivary glands. Biochem J. 1982 Sep 15;206(3):587–595. doi: 10.1042/bj2060587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  3. Besson J., Rotsztejn W., Laburthe M., Epelbaum J., Beaudet A., Kordon C., Rosselin G. Vasoactive intestinal peptide (VIP): brain distribution, subcellular localization and effect of deafferentation of the hypothalamus in male rats. Brain Res. 1979 Apr 6;165(1):79–85. doi: 10.1016/0006-8993(79)90046-5. [DOI] [PubMed] [Google Scholar]
  4. Chneiweiss H., Glowinski J., Prémont J. Vasoactive intestinal polypeptide receptors linked to an adenylate cyclase, and their relationship with biogenic amine- and somatostatin-sensitive adenylate cyclases on central neuronal and glial cells in primary cultures. J Neurochem. 1985 Mar;44(3):779–786. doi: 10.1111/j.1471-4159.1985.tb12883.x. [DOI] [PubMed] [Google Scholar]
  5. Christophe J. P., Conlon T. P., Gardner J. D. Interaction of porcine vasoactive intestinal peptide with dispersed pancreatic acinar cells from the guinea pig. Binding of radioiodinated peptide. J Biol Chem. 1976 Aug 10;251(15):4629–4634. [PubMed] [Google Scholar]
  6. Couvineau A., Laburthe M. The rat liver vasoactive intestinal peptide binding site. Molecular characterization by covalent cross-linking and evidence for differences from the intestinal receptor. Biochem J. 1985 Jan 15;225(2):473–479. doi: 10.1042/bj2250473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Daly J. W. Forskolin, adenylate cyclase, and cell physiology: an overview. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;17:81–89. [PubMed] [Google Scholar]
  8. Dockray G. J., Reeve J. R., Jr, Shively J., Gayton R. J., Barnard C. S. A novel active pentapeptide from chicken brain identified by antibodies to FMRFamide. Nature. 1983 Sep 22;305(5932):328–330. doi: 10.1038/305328a0. [DOI] [PubMed] [Google Scholar]
  9. ERSPAMER V., ANASTASI A. Structure and pharmacological actions of eledoisin, the active endecapeptide of the posterior salivary glands of Eledone. Experientia. 1962 Feb 15;18:58–59. doi: 10.1007/BF02138250. [DOI] [PubMed] [Google Scholar]
  10. El-Salhy M., Falkmer S., Kramer K. J., Speirs R. D. Immunohistochemical investigations of neuropeptides in the brain, corpora cardiaca, and corpora allata of an adult lepidopteran insect, Manduca sexta (L). Cell Tissue Res. 1983;232(2):295–317. doi: 10.1007/BF00213788. [DOI] [PubMed] [Google Scholar]
  11. Etgen A. M., Browning E. T. Activators of cyclic adenosine 3':5'-monophosphate accumulation in rat hippocampal slices: action of vasoactive intestinal peptide (VIP). J Neurosci. 1983 Dec;3(12):2487–2493. doi: 10.1523/JNEUROSCI.03-12-02487.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Evans P. D., Reale V., Villegas J. The role of cyclic nucleotides in modulation of the membrane potential of the Schwann cell of squid giant nerve fibre. J Physiol. 1985 Jun;363:151–167. doi: 10.1113/jphysiol.1985.sp015701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Evans T., McCarthy K. D., Harden T. K. Regulation of cyclic AMP accumulation by peptide hormone receptors in immunocytochemically defined astroglial cells. J Neurochem. 1984 Jul;43(1):131–138. doi: 10.1111/j.1471-4159.1984.tb06688.x. [DOI] [PubMed] [Google Scholar]
  14. Fredholm B. B., Lundberg J. M. VIP-induced cyclic AMP formation in the cat submandibular gland. Potentiation by carbacholine. Acta Physiol Scand. 1982 Jan;114(1):157–159. doi: 10.1111/j.1748-1716.1982.tb06966.x. [DOI] [PubMed] [Google Scholar]
  15. Greenberg M. J., Price D. A. Invertebrate neuropeptides: native and naturalized. Annu Rev Physiol. 1983;45:271–288. doi: 10.1146/annurev.ph.45.030183.001415. [DOI] [PubMed] [Google Scholar]
  16. Ip N. Y., Baldwin C., Zigmond R. E. Regulation of the concentration of adenosine 3',5'-cyclic monophosphate and the activity of tyrosine hydroxylase in the rat superior cervical ganglion by three neuropeptides of the secretin family. J Neurosci. 1985 Jul;5(7):1947–1954. doi: 10.1523/JNEUROSCI.05-07-01947.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jensen R. T., Gardner J. D. The cellular basis of action of gastrointestinal peptides. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;17:375–382. [PubMed] [Google Scholar]
  18. Koh S. W., Chader G. J. Elevation of intracellular cyclic AMP and stimulation of adenylate cyclase activity by vasoactive intestinal peptide and glucagon in the retinal pigment epithelium. J Neurochem. 1984 Dec;43(6):1522–1526. doi: 10.1111/j.1471-4159.1984.tb06072.x. [DOI] [PubMed] [Google Scholar]
  19. Koh S. W., Kyritsis A., Chader G. J. Interaction of neuropeptides and cultured glial (Müller) cells of the chick retina: elevation of intracellular cyclic AMP by vasoactive intestinal peptide and glucagon. J Neurochem. 1984 Jul;43(1):199–203. doi: 10.1111/j.1471-4159.1984.tb06697.x. [DOI] [PubMed] [Google Scholar]
  20. Laburthe M., Breant B., Rouyer-Fessard C. Molecular identification of receptors for vasoactive intestinal peptide in rat intestinal epithelium by covalent cross-linking. Evidence for two classes of binding sites with different structural and functional properties. Eur J Biochem. 1984 Feb 15;139(1):181–187. doi: 10.1111/j.1432-1033.1984.tb07992.x. [DOI] [PubMed] [Google Scholar]
  21. Leung M. K., Stefano G. B. Isolation and identification of enkephalins in pedal ganglia of Mytilus edulis (Mollusca). Proc Natl Acad Sci U S A. 1984 Feb;81(3):955–958. doi: 10.1073/pnas.81.3.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lundberg J. M., Anggård A., Hökfelt T., Kimmel J. Avian pancreatic polypeptide (APP) inhibits atropine resistant vasodilation in cat submandibular salivary gland and nasal mucosa: possible interaction with VIP. Acta Physiol Scand. 1980 Oct;110(2):199–201. doi: 10.1111/j.1748-1716.1980.tb06651.x. [DOI] [PubMed] [Google Scholar]
  23. Lundberg J. M. Evidence for coexistence of vasoactive intestinal polypeptide (VIP) and acetylcholine in neurons of cat exocrine glands. Morphological, biochemical and functional studies. Acta Physiol Scand Suppl. 1981;496:1–57. [PubMed] [Google Scholar]
  24. Lundberg J. M., Hedlund B., Bartfai T. Vasoactive intestinal polypeptide enhances muscarinic ligand binding in cat submandibular salivary gland. Nature. 1982 Jan 14;295(5845):147–149. doi: 10.1038/295147a0. [DOI] [PubMed] [Google Scholar]
  25. Magistretti P. J., Schorderet M. VIP and noradrenaline act synergistically to increase cyclic AMP in cerebral cortex. Nature. 1984 Mar 15;308(5956):280–282. doi: 10.1038/308280a0. [DOI] [PubMed] [Google Scholar]
  26. O'Shea M., Schaffer M. Neuropeptide function: the invertebrate contribution. Annu Rev Neurosci. 1985;8:171–198. doi: 10.1146/annurev.ne.08.030185.001131. [DOI] [PubMed] [Google Scholar]
  27. Osborne N. N., Patel S., Dockray G. Immunohistochemical demonstration of peptides, serotonin and dopamine-beta-hydroxylase-like material in the nervous system of the leech Hirudo medicinalis. Histochemistry. 1982;75(4):573–583. doi: 10.1007/BF00640607. [DOI] [PubMed] [Google Scholar]
  28. Reale V., Evans P. D., Villegas J. Octopaminergic modulation of the membrane potential of the Schwann cell of the squid giant nerve fibre. J Exp Biol. 1986 Mar;121:421–443. doi: 10.1242/jeb.121.1.421. [DOI] [PubMed] [Google Scholar]
  29. Robberecht P., Conlon T. P., Gardner J. D. Interaction of porcine vasoactive intestinal peptide with dispersed pancreatic acinar cells from the guinea pig. Structural requirements for effects of vasoactive intestinal peptide and secretin on cellular adenosine 3':5'-monophosphate. J Biol Chem. 1976 Aug 10;251(15):4635–4639. [PubMed] [Google Scholar]
  30. Rostene W. H., Fischette C. T., McEwen B. S. Modulation by vasoactive intestinal peptide (VIP) of serotonin receptors in membranes from rat hippocampus. J Neurosci. 1983 Dec;3(12):2414–2419. doi: 10.1523/JNEUROSCI.03-12-02414.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rostène W. H. Neurobiological and neuroendocrine functions of the vasoactive intestinal peptide (VIP). Prog Neurobiol. 1984;22(2):103–129. doi: 10.1016/0301-0082(84)90022-4. [DOI] [PubMed] [Google Scholar]
  32. Rougon G., Noble M., Mudge A. W. Neuropeptides modulate the beta-adrenergic response of purified astrocytes in vitro. Nature. 1983 Oct 20;305(5936):715–717. doi: 10.1038/305715a0. [DOI] [PubMed] [Google Scholar]
  33. Said S. I., Mutt V. Isolation from porcine-intestinal wall of a vasoactive octacosapeptide related to secretin and to glucagon. Eur J Biochem. 1972 Jul 13;28(2):199–204. doi: 10.1111/j.1432-1033.1972.tb01903.x. [DOI] [PubMed] [Google Scholar]
  34. Said S. I., Rosenberg R. N. Vasoactive intestinal polypeptide: abundant immunoreactivity in neural cell lines and normal nervous tissue. Science. 1976 May 28;192(4242):907–908. doi: 10.1126/science.1273576. [DOI] [PubMed] [Google Scholar]
  35. Schot L. P., Boer H. H., Swaab D. F., Van Noorden S. Immunocytochemical demonstration of peptidergic neurons in the central nervous system of the pond snail Lymnaea stagnalis with antisera raised to biologically active peptides of vertebrates. Cell Tissue Res. 1981;216(2):273–291. doi: 10.1007/BF00233620. [DOI] [PubMed] [Google Scholar]
  36. Seamon K. B., Wetzel B. Interaction of forskolin with dually regulated adenylate cyclase. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;17:91–99. [PubMed] [Google Scholar]
  37. Suzuki Y., McMaster D., Huang M., Lederis K., Rorstad O. P. Characterization of functional receptors for vasoactive intestinal peptide in bovine cerebral arteries. J Neurochem. 1985 Sep;45(3):890–899. doi: 10.1111/j.1471-4159.1985.tb04077.x. [DOI] [PubMed] [Google Scholar]
  38. Tatemoto K., Mutt V. Isolation and characterization of the intestinal peptide porcine PHI (PHI-27), a new member of the glucagon--secretin family. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6603–6607. doi: 10.1073/pnas.78.11.6603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Villegas J. Axon-Schwann cell interaction in the squid nerve fibre. J Physiol. 1972 Sep;225(2):275–296. doi: 10.1113/jphysiol.1972.sp009940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Villegas J. Axon/Schwann-cell relationships in the giant nerve fibre of the squid. J Exp Biol. 1981 Dec;95:135–151. doi: 10.1242/jeb.95.1.135. [DOI] [PubMed] [Google Scholar]
  41. Villegas J. Characterization of acetylcholine receptors in the Schwann cell membrane of the squid nerve fibre. J Physiol. 1975 Aug;249(3):679–689. doi: 10.1113/jphysiol.1975.sp011037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Villegas J. Effects of tubocurarine and eserine on the axon-Schwann cell relationship in the squid nerve fibre. J Physiol. 1973 Jul;232(1):193–208. doi: 10.1113/jphysiol.1973.sp010264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Villegas J., Sevcik C., Barnola F. V., Villegas R. Grayanotoxin, veratrine, and tetrodotoxin-sensitive sodium pathways in the Schwann cell membrane of squid nerve fibers. J Gen Physiol. 1976 Mar;67(3):369–380. doi: 10.1085/jgp.67.3.369. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES