Skip to main content
SpringerLink
Log in

Is the nexus necessary for cell-to-cell coupling of smooth muscle?

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Electronmicroscopic study of electrically coupled smooth muscles was undertaken to determine the distribution of nexuses in various types of smooth muscle. The study revealed that while nexal structures were commonplace in some types of smooth muscle, they were very rare or absent in others, even though in some cases these cells were only a few nanometers distant from one another. The persistence in thin section of these structures in the main circular muscle of dog intestine after poor fixation, fixation under strain, cell shrinkage, and metabolic damage of various sorts seems to rule out the thesis that they are labile. The absence of nexuses in longitudinal muscle of dog intestine examined both by thin section and by freeze fracture suggests that in this tissue they are absent or very rarein vivo and cannot account for electrical coupling.

Nexuses were discernible in thin sections of main circular muscle after a variety of experimental conditions of fixation. Metabolic inhibition orin vitro permanganate fixation partially destroyed nexal contacts. These procedures induced tissue, membrane apposition and an accompanying increase in the number of structures which resemble nexuses at low magnification (nexus-like structures). “Nexus-like” structures occurred in all smooth muscle fixed byin vitro permanganate associated with apposition of membranes and poor preservation of basement membrane. A technique ofin vitro permanganate fixation was developed which prevented tissue swelling; consequently “nexus-like” structures were absent in tissues so treated. The suggestion is made that some structures described in the literature as nexuses, following permanganate fixation, may represent “nexus-like” structures.

The balance of evidence suggests that nexuses need not be present for electrical coupling of some smooth muscle cells, in which other types of cell-to-cell contacts must be invoked.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Abe, Y., Tomita, T. 1968. Cable properties of smooth muscle.J. Physiol. (London) 196:87

    Google Scholar 

  2. Anderson, N.C., Jr. 1969. Voltage-clamp studies on uterine smooth muscle.J. Gen. Physiol. 54:145

    Google Scholar 

  3. Barr, L., Berger, W., Dewey, M.M. 1968. Electrical transmission at the nexus between smooth muscle cells.J. Gen. Physiol. 51:347

    Google Scholar 

  4. Batra, S.C., Daniel, E.E. 1970. Dissociation of the downhill calcium movements from sodium and potassium movements in rat uterus.Can. J. Physiol. Pharmacol. 48:768

    Google Scholar 

  5. Bergman, R.A. 1968. Uterine smooth muscle fibers in castrate and estrogen-treated rats.J. Cell Biol. 36:639

    Google Scholar 

  6. Daniel, E.E. 1960. The activation of various types of uterine muscle during stretch-induced contraction.Can. J. Biochem. Physiol. 38:1327

    Google Scholar 

  7. Daniel, E.E., Duchon, G., Henderson, R.M. 1971. The ultrastructural bases for coordination of intestinal motility.Am. J. Dig. Dis. 17:289

    Google Scholar 

  8. Daniel, E.E., Lodge, S. 1973. Electrophysiology of myometrium.In: Uterine Contraction. J. B. Josimovich, editor. p. 19. Wiley-Interscience, New York

    Google Scholar 

  9. Daniel, E.E., Lucien, P., Posey, V.A., Paton, D.M. 1974. A functional analysis of the myogenic control systems of the human fallopian tube.Am. J. Obstet. Gynecol. 121:1046

    Google Scholar 

  10. Daniel, E.E., Posey, V.A., Paton, D.M. 1974. A structural analysis of the myogenic control systems of the human fallopian tube.Am. J. Obstet. Gynecol. 121:1054

    Google Scholar 

  11. Daniel, E.E., Robinson, K. 1971. Effects of inhibitors of active transport on22Na and42K movements and on nucleotide levels in rat uteri at 25°C.Can. J. Physiol. Pharmacol. 49:178

    Google Scholar 

  12. Daniel, E.E., Robinson, K. 1971. Effects of inhibitors of metabolism on adenine nucleotides and on22Na and42K and net movements in rat uteri at 25°C.Can. J. Physiol. Pharmacol. 49:205

    Google Scholar 

  13. Daniel, E.E., Robinson, K. 1971. The effect of temperature on sodium movements in rat uteri and a model for control of their ion content.Can. J. Physiol. 49:240

    Google Scholar 

  14. Daniel, E.E., Robinson, K., Duchon, G., Henderson, R.M. 1971. The possible role of close contacts (nexuses) in the propagation of control electrical activity in the stomach and small intestine.Am. J. Dig. Dis. 16:611

    Google Scholar 

  15. Dewey, M.M., Barr, L. 1964. A study of the structure and distribution of the nexuses.J. Cell Biol. 23:553

    Google Scholar 

  16. Dewey, M.M., Barr, L. 1968. Structure of vertebrate in testinal smooth muscle.Hand. Physiol. 6:1629

    Google Scholar 

  17. Duchon, G., Henderson, R., Daniel, E.E. 1974. Circular muscle layers in the small intestine.In: Proceedings of the Fourth International Symposium on Gastrointestinal Motility. E.E. Daniel, editor. p. 635. Mitchell Press, Vancouver

    Google Scholar 

  18. El-Sharkawy, T.Y., Daniel, E.E. 1975. Electrical activity of small intestinal smooth muscle and its temperature dependence.Am. J. Physiol. 229:1268

    Google Scholar 

  19. El-Sharkawy, T.Y., Daniel, E.E. 1975. Electrogenic sodium pumping in rabbit small intestinal smooth muscle.Am. J. Physiol. 229:1277

    Google Scholar 

  20. El-Sharkawy, T.Y., Daniel, E.E. 1975. The ionic mechanisms of the intestinal electrical control activity.Am. J. Physiol. 229:1287

    Google Scholar 

  21. Gabella, G. 1972. Innervation of the intestinal muscular coat.J. Neurocytol. 1:341

    Google Scholar 

  22. Gabella, G. 1972. Intercellular junctions between circular and longitudinal intestinal muscle layer.Z. Zellforsch. mikrosk. Anat. 125:191

    Google Scholar 

  23. Garfield, R.E., Daniel, E.E. 1975. Relation of membrane vesicles to volume control and Na+ transport in smooth muscle: Effect of metabolic and transport inhibition on fresh tissues.J. Mechanochem. Cell Motil. (in press)

  24. Garfield, R.E., Daniel, E.E. 1975. Relation of membrane vesicles to volume control and Na+ transport in smooth muscle: Studies on Na+-rich tissues.J. Mechanochem. Cell Motil. (in press)

  25. Garfield, R.E., Daniel, E.E. 1975. Light and dark smooth muscle cells in rat myometrium.Can. J. Physiol. Pharmacol. (in press)

  26. Goodenough, D.A. 1974. Bulk isolation of mouse hepatocyte gap junctions. Characterization of the principal protein, connexin.J. Cell Biol. 61:557

    Google Scholar 

  27. Goodenough, D.A., Gilula, N.B. 1974. The splitting of hepatocyte gap junctions andzonulae occludentes with hypertonic disaccharides.J. Cell Biol. 61:575

    Google Scholar 

  28. Goodenough, D.A., Stoeckenius, W. 1972. The isolation of mouse hepatocyte gap junctions. Preliminary chemical characterization and X-ray diffraction.J. Cell Biol. 54:646

    Google Scholar 

  29. Hashimoto, K., Miller, F., Bereston, E.S. 1972. Occurrence of gap junctions between fibroblasts. 1. Colloid milium. Histochemical and electron microscope studies.Arch. Dermatol. 105:684

    Google Scholar 

  30. Henderson, R.M., Duchon, G., Daniel, E.E. 1971. Cell contacts in duodenal smooth muscle layers.Am. J. Physiol. 221:564

    Google Scholar 

  31. Henderson, R.M. 1974. Cell contacts in vascular and other smooth muscle.Proc. Can. Fed. Biol. Soc. 17:137

    Google Scholar 

  32. Karnovsky, M.J. 1967. The ultrastructural basis of capillary permeability studied with peroxidase as a tracer.J. Cell Biol. 35:213

    Google Scholar 

  33. Kefalides, N.A. 1969. The chemistry and structure of basement membrane.Arthritis Rheum. 12:427

    Google Scholar 

  34. Kuriyama, H., Osa, T., Toida, H. 1967. Electrophysiological study of the intestinal smooth muscle of the guinea pig.J. Physiol. (London) 191:239

    Google Scholar 

  35. Loewenstein, W.R., Nakas, M., Socolar, S.J. 1967. Junctional membrane uncoupling: permeability transformations at a cell membrane junction.J. Gen. Physiol. 50:1865

    Google Scholar 

  36. Malhotra, S.K., Tewari, J.P., Tu, J.C. 1975. Functional characterization of types of plasma membranes in cerebral cortex.J. Neurobiol. 6:57

    Google Scholar 

  37. Matler, A. 1973. A morphometric study in the nexus of rat cardiac muscle.J. Cell Biol. 56:690

    Google Scholar 

  38. McCann, F.V., Stibitz, G.R., Hugenenin, J. 1973. Studies of impedance in cardiac tissue using sucrose gap and computer techniques. 1. The influence of sucrose and oil as insulating media.Biophys. J. 13:1183

    Google Scholar 

  39. McNutt, N.S., Weinstein, R.S. 1970. The ultrastructure of the nexus. A correlated thin-section and freeze-cleave study.J. Cell Biol. 47:667

    Google Scholar 

  40. Melton, C.E. 1956. Electrical activity in the uterus of the rat.Endocrinology 58:139

    Google Scholar 

  41. Nelson, P.C., Peacock, J.H. 1973. Transmission of an active electrical response between fibroblasts (L cells) in cell culture.J. Gen. Physiol. 62:25

    Google Scholar 

  42. Oki, M., Daniel, E.E. 1974. Ultrastructural basis for electrical coupling in the dog stomach.In: Proceedings of the Fourth International Symposium on Gastrointestinal Motility. E.E. Daniel, editor. p. 85. Mitchell Press, Vancouver

    Google Scholar 

  43. Oliveira-Castro, G.M., Loewenstein, W.R. 1971. Junctional membrane permeability. Effects of divalent cations.J. Membrane Biol. 5:51

    Google Scholar 

  44. Politoff, A.L., Socolar, S.J., Loewenstein, W.R. 1969. Permeability of a cell membrane junction.J. Gen. Physiol. 53:498

    Google Scholar 

  45. Prosser, C.L. 1974. Smooth muscle.Annu. Rev. Physiol. 36:503

    Google Scholar 

  46. Rangachari, P.K., Paton, D.M., Daniel, E.E. 1973. Regulation of cellular volume in rat myometrium.Biochim. Biophys. Acta 323:297

    Google Scholar 

  47. Revel, J.P., Olson, W., Karnovsky, M.J. 1967. A twenty-angstrom gap junction with a hexagonal array of subunits in smooth muscle.J. Cell Biol. 35:112A

    Google Scholar 

  48. Revel, J.R., Yee, A.G., Hudspeth, A.J. 1971. Gap junctions between electronically coupled cells in tissue culture and in brown fat.Proc. Nat. Acad. Sci. USA 68:2924

    Google Scholar 

  49. Sanger, J.W., McCann, F.V. 1968. Ultrastructure of the myocardium of the moth,Hyalophora cecropia.J. Insect Physiol. 14:1105

    Google Scholar 

  50. Sarna, S.K., Daniel, E.E., Kingma, Y.J. 1971. Simulation of slow wave electrical activity of small intestine.Am. J. Physiol. 221:166

    Google Scholar 

  51. Sarna, S.K., Daniel, E.E., Kingma, Y.J. 1972. Simulation of the electric control activity of the stomach by an array of relaxation oscillators.Am. J. Dig. Dis. 17:299

    Google Scholar 

  52. Spira, A.W. 1971. The nexus in the intercalated disc of the canine heart: Quantitative data for an estimation of its resistance.J. Ultrastruc. Res. 34:409

    Google Scholar 

  53. Stibitz, G.R., McCann, F.V. 1974. Studies of impedance in cardiac tissue using sucrose gap and computer techniques. II. Circuit stimulation of passive electrical properties and cell-to-cell transmission.Biophys. J. 14:75

    Google Scholar 

  54. Taxi, J. 1965. Contribution à l'étude des connexions des neurones moteurs du système nerveux autonome.Ann. Sci. Natur. Zool. 7:413

    Google Scholar 

  55. Tewari, J.P., Malhotra, S.K., Tu, J.C. 1971. A study of the structure of mitochondrial membranes by freeze-etch and freeze-fracture techniques.Cytobios 4:97

    Google Scholar 

  56. Tomita, T. 1966. Electrical responses of smooth muscle to external stimulation in hypertonic solution.J. Physiol. (London) 183:450

    Google Scholar 

  57. Tomita, T. 1969. The longitudinal tissue impedance of the smooth muscle of guinea pigtaenia coli.J. Physiol. (London) 201:145

    Google Scholar 

  58. Tomita, T. 1973. Electrical properties of mammalian smooth muscle.In: Smooth Muscle. E. Bülbring, A. Brading, A. Jones, T. Tomita, editors, p. 197. Edward Arnold, London

    Google Scholar 

  59. van Breemen, C., Daniel, E.E., van Breemen, D. 1966. Calcium distribution and exchange in the rat uterus.J. Gen. Physiol. 49:1265

    Google Scholar 

Download references

Author information

Author notes

  1. S. K. Malhotra

    Present address: Biological Sciences Electron Microscopy Laboratory, University of Alberta, Edmonton, Canada

  2. M. Oki

    Present address: Department of Anatomy, Yamaguchi University, Ube, Japan

Authors and Affiliations

  1. Department of Pharmacology, The University of Alberta, Edmonton, Canada

    E. E. Daniel, V. P. Daniel, G. Duchon, R. E. Garfield, M. Nichols, S. K. Malhotra & M. Oki

Authors
  1. E. E. Daniel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. P. Daniel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Duchon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. E. Garfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Nichols
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. K. Malhotra
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Oki
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Daniel, E.E., Daniel, V.P., Duchon, G. et al. Is the nexus necessary for cell-to-cell coupling of smooth muscle?. J. Membrain Biol. 28, 207–239 (1976). https://doi.org/10.1007/BF01869698

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869698

Keywords

Search

Navigation