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. 1980 Jan 1;75(1):79–105. doi: 10.1085/jgp.75.1.79

Giant smooth muscle cells of Beroe. Ultrastructure, innervation, and electrical properties

PMCID: PMC2215185  PMID: 6102109

Abstract

Beroe muscle fibers are single cells which may be 20-40 micrometer in diameter in mature specimens. Longitudinal muscles may be 6 cm or more long. There is no striation pattern and the muscles were observed to contract in a tonic fashion when stretched. They are innervated by a nerve net, and external recording revealed what are probably nerve net impulses. Intracellular stimulation of the muscles themselves was found to initiate large propagating action potentials which were recorded intracellularly. The action potentials were insensitive to tetrodotoxin (10(-5) g/ml), tetraethylammonium ions (50 mM), MnCl2 (25 mM), and low concentrations of verapamil (2 X 10(-6) g/ml). Full-size action potentials were recorded in sodium- or calcium-deficient salines, but were small and graded in salines deficient in both sodium and calcium. Cable analysis yielded mean values for lambda (1.95 mm), Ri (154 omega cm), Rm (9,253 omega cm2), and tau m (13.9 ms). The conduction velocity depended primarily on fiber diameter and maximum rate of rise of the action potential and could be predicted from the theoretical analysis of Hunter et al. (1975 Prog. Biophys. Mol. Biol. 30: 99-144). The calculated membrane capacity (less than microF/cm2) indicates little infolding of the surface membrane, a conclusion which is in agreement with anatomical studies.

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Selected References

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  1. Abe Y., Tomita T. Cable properties of smooth muscle. J Physiol. 1968 May;196(1):87–100. doi: 10.1113/jphysiol.1968.sp008496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian R. H., Peachey L. D. The membrane capacity of frog twitch and slow muscle fibres. J Physiol. 1965 Nov;181(2):324–336. doi: 10.1113/jphysiol.1965.sp007764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson N. C., Ramon F., Snyder A. Studies on calcium and sodium in uterine smooth muscle excitation under current-clamp and voltage-clamp conditions. J Gen Physiol. 1971 Sep;58(3):322–339. doi: 10.1085/jgp.58.3.322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brading A., Bülbring E., Tomita T. The effect of sodium and calcium on the action potential of the smooth muscle of the guinea-pig taenia coli. J Physiol. 1969 Feb;200(3):637–654. doi: 10.1113/jphysiol.1969.sp008713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cranefield P. F., Aronson R. S., Wit A. L. Effect of verapamil on the noraml action potential and on a calcium-dependent slow response of canine cardiac Purkinje fibers. Circ Res. 1974 Feb;34(2):204–213. doi: 10.1161/01.res.34.2.204. [DOI] [PubMed] [Google Scholar]
  6. Devine C. E., Somlyo A. V., Somlyo A. P. Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscles. J Cell Biol. 1972 Mar;52(3):690–718. doi: 10.1083/jcb.52.3.690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. FATT P., KATZ B. The electrical properties of crustacean muscle fibres. J Physiol. 1953 Apr 28;120(1-2):171–204. doi: 10.1113/jphysiol.1953.sp004884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fay F. S., Delise C. M. Contraction of isolated smooth-muscle cells--structural changes. Proc Natl Acad Sci U S A. 1973 Mar;70(3):641–645. doi: 10.1073/pnas.70.3.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gabella G. Cellular structures and electrophysiological behaviour. Fine structure of smooth muscle. Philos Trans R Soc Lond B Biol Sci. 1973 Mar 15;265(867):7–16. doi: 10.1098/rstb.1973.0004. [DOI] [PubMed] [Google Scholar]
  10. Golenhofen K., Lammel E. Selective suppression of some components of spontaneous activity in various types of smooth muscle by iproveratril (Verapamil). Pflugers Arch. 1972;331(3):233–243. [PubMed] [Google Scholar]
  11. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HODGKIN A. L., HUXLEY A. F., KATZ B. Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol. 1952 Apr;116(4):424–448. doi: 10.1113/jphysiol.1952.sp004716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hernandez-Nicaise M. L. Le système nerveux des Cténaires. I. Structure et ultrastructure des réseaux epithéliaux. Z Zellforsch Mikrosk Anat. 1973 Feb 12;137(2):223–250. [PubMed] [Google Scholar]
  14. Hernandez-Nicaise M. L. Le systéme nerveux des eténaires. II. Les éléments nerveux intra-mésogléens des béroidés et des cydippidés. Z Zellforsch Mikrosk Anat. 1973;143(1):117–133. [PubMed] [Google Scholar]
  15. Hernandez-Nicaise M. L. The nervous system of ctenophores. III. Ultrastructure of synapses. J Neurocytol. 1973 Sep;2(3):249–263. doi: 10.1007/BF01104029. [DOI] [PubMed] [Google Scholar]
  16. Hodgkin A. L., Nakajima S. Analysis of the membrane capacity in frog muscle. J Physiol. 1972 Feb;221(1):121–136. doi: 10.1113/jphysiol.1972.sp009743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hunter P. J., McNaughton P. A., Noble D. Analytical models of propagation in excitable cells. Prog Biophys Mol Biol. 1975;30(2-3):99–144. doi: 10.1016/0079-6107(76)90007-9. [DOI] [PubMed] [Google Scholar]
  18. JENERICK H. P. Muscle membrane potential, resistance, and external potassium chloride. J Cell Physiol. 1953 Dec;42(3):427–448. doi: 10.1002/jcp.1030420309. [DOI] [PubMed] [Google Scholar]
  19. KURIYAMA H., TOMITA T. THE RESPONSES OF SINGLE SMOOTH MUSCLE CELLS OF GUINEA-PIG TAENIA COLI TO INTRACELLULARLY APPLIED CURRENTS, AND THEIR EFFECT ON THE SPONTANEOUS ELECTRICAL ACTIVITY. J Physiol. 1965 May;178:270–289. doi: 10.1113/jphysiol.1965.sp007627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kuroda T. The effects of D600 and verapamil on action potential in the X-organ neuron of the crayfish. Jpn J Physiol. 1976;26(2):189–202. doi: 10.2170/jjphysiol.26.189. [DOI] [PubMed] [Google Scholar]
  21. Moreton R. B. Electrophysiology and ionic movements in the central nervous system of the snail, Helix aspersa. J Exp Biol. 1972 Oct;57(2):513–541. doi: 10.1242/jeb.57.2.513. [DOI] [PubMed] [Google Scholar]
  22. Rosen M. R., Ilvento J. P., Gelband H., Merker C. Effects of verapamil on electrophysiologic properties of canine cardiac Purkinje fibers. J Pharmacol Exp Ther. 1974 May;189(2):414–422. [PubMed] [Google Scholar]
  23. Suarez-Kurtz G., Sorenson A. L. Effects of verapamil on excitation-contraction coupling in single crab muscle fibers. Pflugers Arch. 1977 Apr 25;368(3):231–239. doi: 10.1007/BF00585201. [DOI] [PubMed] [Google Scholar]
  24. Tomita T. Electrophysiology of mammalian smooth muscle. Prog Biophys Mol Biol. 1975;30(2-3):185–203. doi: 10.1016/0079-6107(76)90009-2. [DOI] [PubMed] [Google Scholar]
  25. Tomita T. Membrane capacity and resistance of mammalian smooth muscle. J Theor Biol. 1966 Nov;12(2):216–227. doi: 10.1016/0022-5193(66)90114-7. [DOI] [PubMed] [Google Scholar]
  26. Vassort G. Voltage-clamp analysis of transmembrane ionic currents in guinea-pig myometrium: evidence for an initial potassium activation triggered by calcium influx. J Physiol. 1975 Nov;252(3):713–734. doi: 10.1113/jphysiol.1975.sp011167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wald F. Ionic differences between somatic and axonal action potentials in snail giant neurones. J Physiol. 1972 Jan;220(2):267–281. doi: 10.1113/jphysiol.1972.sp009706. [DOI] [PMC free article] [PubMed] [Google Scholar]

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