Skip to main content
Log in

Intercellular communication in smooth muscle

  • Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

The functioning of a group of cells as a tissue depends on intercellular communication; an example is the spread of action potentials through intestinal tissue resulting in synchronized contraction. Recent evidence for cell heterogeneity within smooth muscle tissues has renewed research into cell coupling.Electrical coupling is essential for propagation of action potentials in gastrointestinal smooth muscle.Metabolic coupling may be involved in generation of pacemaker activity. This review deals with the role of cell coupling in tissue function and some of the issues discussed are the relationship between electrical synchronization and gap junctions, metabolic coupling, and the role of interstitial cells of Cajal in coupling.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Amezcua, J. L., Palmer, R. M., de Souza, B. M., and Moncada, S., Nitric oxide synthesized from L-arginine regulates vascular tone in the coronary circulation of the rabbit. Br. J. Pharmac.97 (1989) 1119–1124.

    Article  CAS  Google Scholar 

  2. Barajas-López, C., Berezin, I., Daniel, E. E., and Huizinga, J. D., Pacemaker activity recorded in interstitial cells of Cajal of the gastrointestinal tract. Am. J. Physiol.257 (1989) C830-C835.

    Article  PubMed  Google Scholar 

  3. Bardakjian, B. L., and Diamant, N. E., Electronic models of oscillator to oscillator communication, in: Cell Interaction and Gap Junctions. Eds N. Sperelakis and W. C. Cole. CRC Press. Boca Raton 1989.

    Google Scholar 

  4. Bauer, A. J., Publicover, N. G., and Sanders, K. M., Origin and spread of slow waves in canine gastric antral circular muscle. Am. J. Physiol.249 (1985) G800-G806.

    CAS  PubMed  Google Scholar 

  5. Beny, J. L., and Connat, J. L., An electron microscopic study of smooth muscle cell dye coupling in the pig coronary arteries. Circ. Res.70 (1992) 49–55.

    Article  CAS  PubMed  Google Scholar 

  6. Berezin, I., Huizinga, J. D., and Daniel, E. E., Interstitial cells of Cajal in the canine colon: a special communication network at the inner border of the circular muscle. J. comp. Neurol.273 (1988) 42–51.

    Article  CAS  PubMed  Google Scholar 

  7. Berezin, I., Huizinga, J. D., Farraway, L., and Daniel, E. E., Innervation of interstitial cells of Cajal by vasoactive intestinal polypeptide containing nerves in canine colon. Can. J. Physiol. Pharmac.68 (1990) 922–932.

    Article  CAS  Google Scholar 

  8. Blennerhassett, M. G., and Garfield, R. E., Effect of gap junction number and permeability on intercellular coupling in rat myometrium. Am. J. Physiol.261 (1991) C1001-C1009.

    Article  CAS  PubMed  Google Scholar 

  9. Blennerhassett, M. G., Kannan, M. S., and Garfield, R. E., Functional characterization of cell-to-cell coupling in cultured rat aortic smooth muscle. Am. J. Physiol.252 (1987) C555-C569.

    Article  CAS  PubMed  Google Scholar 

  10. Brown, H. F., Electrophysiology of the sinoatrial node. Physiol. Rev.62 (1982) 505–530.

    Article  CAS  PubMed  Google Scholar 

  11. Cheung, D. W., and Daniel, E. E., Comparative study of the smooth muscle layers of the rabbit duodenum. J. Physiol., Lond.309 (1980) 13–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cole, W. C., and Garfield, R. E., Evidence for physiological regulation of myometrial gap junction permeability. Am. J. Physiol.251 (1986) C411-C420.

    Article  CAS  PubMed  Google Scholar 

  13. Cole, W. C., Garfield, R. E., and Kirkaldy, J. S., Gap junctions and direct intercellular communication between rat uterine smooth muscle cells. Am. J. Physiol.249 (1985) C20-C31.

    Article  CAS  PubMed  Google Scholar 

  14. Conklin, J. L., and Du, C., Pathways of slow-wave propagation in proximal colon of cats. Am. J. Physiol.258 (1990) G894-G903.

    CAS  PubMed  Google Scholar 

  15. Connor, J. A., Kreulen, D., Prosser, C. L., and Weigel, R., Interaction between longitudinal and circular muscle in intestine of cat. J. Physiol., Lond.273 (1977) 665–689.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Daniel, E. E., Gap junctions and smooth muscle, in: Cell to Cell Communication, pp. 149–184. Ed W. C. De Mello. CRC Press, Boca Raton 1991.

    Google Scholar 

  17. Daniel, E. E., Daniel, V. P. Duchon, G., Garfield, R. E., Nichols, M., Malhotra, S. K., and Oki, M., Is the nexus necessary for cell-to-cell coupling of smooth muscle? J. membr. Biol.28 (1976) 207–239.

    Article  CAS  PubMed  Google Scholar 

  18. Daniel, E. E., and Posey Daniel, V., Neuromuscular structures in opossum esophagus: role of interstitial cells of Cajal. Am. J. Physiol.246 (1984) G305-G315.

    CAS  PubMed  Google Scholar 

  19. Gabella, G., Smooth muscle cell junctions and structural aspects of contraction. Br. med. Bull.35 (1979) 213–218.

    Article  CAS  PubMed  Google Scholar 

  20. Garfield, R. E., Cell-to-Cell communication in smooth muscle, in: Calcium and contractile activity, pp. 143–150. Eds A. K. Grover and E. E. Daniel. The Humana Press, Clifton 1985.

    Chapter  Google Scholar 

  21. Garfield, R. E., Blennerhassett, M. G., and Miller, S. M., Control of myometrial contractility: role and regulation of gap junctions. Oxford Reviews of Reproductive Biology10 (1988) 436–490.

    CAS  PubMed  Google Scholar 

  22. Garfield, R. E., Thilander, G., Blennerhassett, M. G., and Sakai, N., An update on the question: are gap junctions necessary for cell to cell coupling of smooth muscle? Can. J. Physiol. Pharmac. (1992) in press.

  23. Hallett, M. B., The unpredictability of cellular behavior: trivial or of fundamental importance to cell biology? Perspect. Biol. Med.33 (1989) 110–119.

    Article  CAS  PubMed  Google Scholar 

  24. Hertzberg, E. L., Lawrence, T. S., and Gilula, N. B., Gap junctional communication. A. Rev. Physiol.43 (1981) 479–491.

    Article  CAS  Google Scholar 

  25. Hooper, M. L., and Subak Sharpe, J. H., Metabolic cooperation between cells. Int. Rev. Cytol.69 (1981) 45–104.

    Article  CAS  PubMed  Google Scholar 

  26. Huizinga, J. D., Action potentials in gastrointestinal smooth muscle. Can. J. Physiol. Pharmacol.69 (1981) 1133–1142.

    Article  Google Scholar 

  27. Huizinga, J. D., Berezin, I., Daniel, E. E., and Chow, E., Inhibitory innervation of colonic smooth muscle cells and interstitial cells of Cajal. Can. J. Physiol. Pharmac.68 (1990) 447–454.

    Article  CAS  Google Scholar 

  28. Huizinga, J. D., and Chow, E., Electrotonic current spread in colonic smooth muscle. Am. J. Physiol.254 (1988) G702-G710.

    CAS  PubMed  Google Scholar 

  29. Huizinga, J. D., and Den Hertog, A., Inhibition of fundic strips from guinea-pig stomach: the effect of theophylline on the membrane potential, muscle contraction and ion fluxes. Eur. J. Pharmacol.57 (1979) 1–11.

    Article  CAS  PubMed  Google Scholar 

  30. Huizinga, J. D., Farraway, L., and Den Hertog, A., Effect of voltage and cyclic AMP on frequency of slow wave type action potentials in colonic smooth muscle. J. Physiol., Lond.442 (1991) 31–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Huizinga, J. D., Shin, A., and Chow, E., Electrical coupling and pacemaker activity in colonic smooth muscle. Am. J. Physiol.255 (1988) C653-C660.

    Article  CAS  PubMed  Google Scholar 

  32. Kanna, M. S., and Daniel, E. E., Formation of gap junctions by treatment in vitro with potassium conductance blockers. J. Cell Biol.78 (1978) 338–348.

    Article  Google Scholar 

  33. Kannan, M. S., Jager, L. P., Daniel, E. E., and Garfield, R. E., Effects of 4-aminopyridine and tetraethylammonium chloride on the electrical activity and cable properties of canine tracheal smooth muscle. J. Pharmac. exp. Ther.227 (1983) 706–715.

    CAS  Google Scholar 

  34. Larson, D. M., Haudenschild, C. C., and Beyer, E. C., Gap junction messenger RNA expression by vascular wall cells. Circ. Res.66 (1990) 1074–1080.

    Article  CAS  PubMed  Google Scholar 

  35. Lash, J. A., Critser, E. S., and Pressler, M. L., Cloning of a gap junctional protein from vascular smooth muscle and expression in two-cell mouse embryos. J. biol. Chem.265 (1990) 13113–13117.

    Article  CAS  PubMed  Google Scholar 

  36. Lawrence, T. S., Beers, W. H., and Gilula, N. B., Transmission of hormonal stimulation by cell-to-cell communication. Nature272 (1978) 501–506.

    Article  CAS  PubMed  Google Scholar 

  37. Liu, L. W. C., Daniel, E. E., and Huizinga, J. D., Colonic circular muscle without the network of interstitial cells of Cajal can generate slow waves through different mechanisms. Gastroenterology99 (II) (1990) 1215. (Abstract)

    Article  Google Scholar 

  38. Liu, L. W. C., Daniel, E. E., and Huizinga, J. D., Excitability of canine colon circular muscle disconnected from the network of interstitial cell of Cajal. Can. J. Physiol. Pharmac.70(2) (1992) 289–295.

    Article  CAS  Google Scholar 

  39. Meda, P., Chanson, M., Pepper M., Giordano, E., Bosco, D., Traub, O., Willecke, K., el Aoumari, A., Gros, D., Beyer, E. C., Orci, L., and Spray, D. C., In vivo modulation of connexin, 43 gene expression and junctional coupling of pancreatic B-cells. Exp. Cell Res.192 (1991) 469–480.

    Article  CAS  PubMed  Google Scholar 

  40. Miller, S. M., Garfield, R. E., and Daniel, E. E., Improved propagation in myometrium associated with gap junctions during parturition. Am. J. Physiol.256 (1989) C130-C141.

    Article  CAS  PubMed  Google Scholar 

  41. Moore, L. K., Beyer, E. C., and Burt, J. M., Characterization of gap junction channels in A7r5 vascular smooth muscle cells. Am. J. Physiol.260 (1991) C975-C981.

    Article  CAS  PubMed  Google Scholar 

  42. Perez Armendariz, M., Roy, C., Spray, D. C., and Bennett, M. V., Biophysical properties of gap junctions between freshly dispersed pairs of mouse pancreatic beta cells. Biophys. J.59 (1991) 76–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Peterson, O. H., and Findlay, I., Electrophysiology of the pancreas. Physiol. Rev.67 (1987) 1054–1116.

    Article  Google Scholar 

  44. Risek, B., Guthrie, S., Kumar, N. B., Modulation of gap junction transcript and protein expression during pregnancy in the rat. J. Cell Biol.110 (1990) 269–282.

    Article  CAS  PubMed  Google Scholar 

  45. Rumessen, J. J., and Thuneberg, L., Interstitial cells of Cajal in human small intestine. Ultrastructural identification and organization between the main smooth muscle layers. Gastroenterology100 (1991) 1417–1431.

    Article  CAS  PubMed  Google Scholar 

  46. Safranyos, R. G., and Caveney, S., Rates of diffusion of fluorescent molecules via cell-to-cell membrane channels in a developing tissue. J. Cell Biol.100 (1985) 736–747.

    Article  CAS  PubMed  Google Scholar 

  47. Seltzer, Z., and Devor, M., Ephaptic transmission in chronically damaged peripheral nerves. Neurology29 (1979) 1061–1064.

    Article  CAS  PubMed  Google Scholar 

  48. Serio, R., Barajas-López, C., Daniel, E. E., Berezin, I., and Huizinga, J. D., Slow-wave activity in colon: role of network of submucosal interstitial cells of Cajal. Am. J. Physiol.260 (1991) G636-G645.

    CAS  PubMed  Google Scholar 

  49. Sims, S. M., Daniel, E. E., and Garfield, R. E., Improved electrical coupling in uterine smooth muscle is associated with increased numbers of gap junctions at parturition. J. gen. Physiol.80 (1982) 353–375.

    Article  CAS  PubMed  Google Scholar 

  50. Sperelakis, N., Propagation mechanisms in heart. A. Rev. Physiol.41 (1979) 441–457.

    Article  CAS  Google Scholar 

  51. Sperelakis, N., Electric field model: An alternate mechanism for cell-to-cell propagation in cardiac muscle and smooth muscle. J. Gastroint. Motil.3 (1991) 1–19.

    Google Scholar 

  52. Spray, D. C. and Bennett, M. V., Physiology and pharmacology of gap junctions. A. Rev. Physiol.47 (1985) 281–303.

    Article  CAS  Google Scholar 

  53. Spray, D. C., and Burt, J. M., Structure-activity relations of the cardiac gap junction channel. Am. J. Physiol.258 (1990) C195-C205.

    Article  CAS  PubMed  Google Scholar 

  54. Spray, D. C., Harris, A. L., and Bennett, M. V., Voltage dependence of junctional conductance in early amphibian embryos. Science204 (1979) 432–434.

    Article  CAS  PubMed  Google Scholar 

  55. Suenson, M., Ephaptic impulse transmission between ventricular myocardial cells in vitro. Acta physiol. scand.120 (1984) 445–455.

    Article  CAS  PubMed  Google Scholar 

  56. Tang, C. M., Orkand, P. M., and Orkand, R. K., Coupling and uncoupling of amphibian neuroglia. Neurosci. Lett.54 (1985) 237–242.

    Article  CAS  PubMed  Google Scholar 

  57. Thuneberg, L., Interstitial cells of Cajal: intestinal pacemaker cells? Adv. Anat. Embryol. Cell Biol.71 (1982) 1–130.

    Article  CAS  PubMed  Google Scholar 

  58. Thuneberg, L., Interstitial Cells of Cajal, in: Handbook of Physiology, The Gastrointestinal System, pp. 349–386. Eds G. S. Schultz, J. D. Wood and B. B. Rauner. American Physiological Society, Bethesda, U.S.A. 1989.

    Google Scholar 

  59. Veenstra, R. D., and DeHaan, R. L., Measurement of single channel currents from cardiac gap junctions. Science233 (1986) 972–974.

    Article  CAS  PubMed  Google Scholar 

  60. Zamir, O., and Hanani, M., Intercellular dye-coupling in intestinal smooth muscle. Are gap junctions required for intercellular coupling? Experientia46 (1990) 1002–1005.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huizinga, J.D., Liu, L.W.C., Blennerhassett, M.G. et al. Intercellular communication in smooth muscle. Experientia 48, 932–941 (1992). https://doi.org/10.1007/BF01919140

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01919140

Key words

Navigation