The Role of Cyclic Nucleotides in Modulation of the Membrane Potential of the Schwann Cell of Squid Giant Nerve Fibre

Overview

Journal J Physiol

Specialty Physiology

Date 1985 Jun 1

PMID 2991504

Citations 6

Authors

P D Evans

V REALE

J Villegas

Affiliations

Soon will be listed here.

Abstract

The role of cyclic nucleotides in mediating the effects of nicotine cholinergic receptors has been investigated in Schwann cells of the giant nerve fibre of the squid. Elevation of cyclic AMP levels in this preparation by means of the phosphodiesterase inhibitor, theophylline, by the diterpene adenylate cyclase activator, forskolin, and by cyclic nucleotide analogues mimics the action of activating the nicotinic cholinergic receptors in producing a long-lasting hyperpolarization of the membrane potential of the Schwann cell. Theophylline and forskolin also potentiate the effects of carbachol and of neural stimulation on the Schwann cell. The results suggest that the nicotinic receptor of the squid Schwann cell is likely to mediate its effects via a mechanism that activates adenylate cyclase. The results are discussed in terms of the role of cyclic AMP in the complex multistep interaction between the giant axon of the squid and its surrounding Schwann-cell layer.

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References

Villegas J . Effects of acetylcholine and carbamylcholine on the axon and Schwann cell electrical potentials in the squid nerve fibre. J Physiol. 1974; 242(3):647-59. PMC: 1330656. DOI: 10.1113/jphysiol.1974.sp010728. View

Villegas J . Effects of tubocurarine and eserine on the axon-Schwann cell relationship in the squid nerve fibre. J Physiol. 1973; 232(1):193-208. PMC: 1350499. DOI: 10.1113/jphysiol.1973.sp010264. View

Villegas J . Characterization of acetylcholine receptors in the Schwann cell membrane of the squid nerve fibre. J Physiol. 1975; 249(3):679-89. PMC: 1309599. DOI: 10.1113/jphysiol.1975.sp011037. View

Villegas J, Sevcik C, BARNOLA F, Villegas R . Grayanotoxin, veratrine, and tetrodotoxin-sensitive sodium pathways in the Schwann cell membrane of squid nerve fibers. J Gen Physiol. 1976; 67(3):369-80. PMC: 2214968. DOI: 10.1085/jgp.67.3.369. View

Battelle B, Kravitz E . Targets of octopamine action in the lobster: cyclic nucleotide changes and physiological effects in hemolymph, heart and exoskeletal muscle. J Pharmacol Exp Ther. 1978; 205(2):438-48. View

Villegas J, JENDEN D . Acetylcholine content of the Schwann cell and axon in the giant nerve fibre of the squid. J Neurochem. 1979; 32(3):761-6. DOI: 10.1111/j.1471-4159.1979.tb04559.x. View

Patterson P . Environmental determination of autonomic neurotransmitter functions. Annu Rev Neurosci. 1978; 1:1-17. DOI: 10.1146/annurev.ne.01.030178.000245. View

Berridge M, Rapp P . A comparative survey of the function, mechanism and control of cellular oscillators. J Exp Biol. 1979; 81:217-79. DOI: 10.1242/jeb.81.1.217. View

Heumann R, Villegas J, Herzfeld D . Acetylcholine synthesis in the Schwann cell and axon in the giant nerve fiber of the squid. J Neurochem. 1981; 36(2):765-8. DOI: 10.1111/j.1471-4159.1981.tb01654.x. View

10.

Seamon K, Daly J . Forskolin: a unique diterpene activator of cyclic AMP-generating systems. J Cyclic Nucleotide Res. 1981; 7(4):201-24. View

11.

Villegas J . Axon/Schwann-cell relationships in the giant nerve fibre of the squid. J Exp Biol. 1981; 95:135-51. DOI: 10.1242/jeb.95.1.135. View

12.

Lasek R, Tytell M . Macromolecular transfer from glia to the axon. J Exp Biol. 1981; 95:153-65. DOI: 10.1242/jeb.95.1.153. View

13.

Currie D, Kelly J . Glial versus neuronal uptake of glutamate. J Exp Biol. 1981; 95:181-93. DOI: 10.1242/jeb.95.1.181. View

14.

Mudge A . Effect of non-neuronal cells on peptide content of cultured sensory neurones. J Exp Biol. 1981; 95:195-203. DOI: 10.1242/jeb.95.1.195. View

15.

POTTER D, Furshpan E, Landis S . Transmitter status in cultured rat sympathetic neurons: plasticity and multiple function. Fed Proc. 1983; 42(6):1626-32. View

16.

Huganir R, Greengard P . cAMP-dependent protein kinase phosphorylates the nicotinic acetylcholine receptor. Proc Natl Acad Sci U S A. 1983; 80(4):1130-4. PMC: 393542. DOI: 10.1073/pnas.80.4.1130. View

17.

Rougon G, Noble M, Mudge A . Neuropeptides modulate the beta-adrenergic response of purified astrocytes in vitro. Nature. 1983; 305(5936):715-7. DOI: 10.1038/305715a0. View

18.

Evans P . A modulatory octopaminergic neurone increases cyclic nucleotide levels in locust skeletal muscle. J Physiol. 1984; 348:307-24. PMC: 1199404. DOI: 10.1113/jphysiol.1984.sp015112. View

19.

Evans P . The role of cyclic nucleotides and calcium in the mediation of the modulatory effects of octopamine on locust skeletal muscle. J Physiol. 1984; 348:325-40. PMC: 1199405. DOI: 10.1113/jphysiol.1984.sp015113. View

20.

Neering I, McBurney R . Role for microsomal Ca storage in mammalian neurones?. Nature. 1984; 309(5964):158-60. DOI: 10.1038/309158a0. View