Skip to main content

Cell-to-Cell Communication

Permeability, Formation, Genetics, and Functions of the Cell-Cell Membrane Channel

  • Chapter
Membrane Physiology

Abstract

In formulating Cell Theory, Schleiden(1) wrote in 1838: “Every higher organism is an aggregate of fully circumscribed and self-contained unit beings, the cells.” This basic tenet has been extraordinarily fruitful and influential in biology and medicine, and in many aspects its usefulness continues unabated. However, since the mid-1960s it has become clear that cellular circumscription is generally not complete; a wide variety of cells turned out to be interconnected by membrane channels at their junction.(2,3) Small molecules pass freely from one cell interior to another through these junctional channels so that the connected cell ensemble, rather than the single cell, is the unit in many cellular functions; there is cell autonomy only in respect to the larger molecules that do not permeate the junctional channels.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Schleiden, M. J. 1838. Beiträge zur Phytogenesis. Müllers Arch. Anat. Physiol. Wiss. Med. 1838: 137–176.

    Google Scholar 

  2. Loewenstein, W. R. 1966. Permeability of membrane junctions. Ann. N.Y. Acad. Sci. 137: 441–472.

    Article  PubMed  CAS  Google Scholar 

  3. Loewenstein, W. R. 1975. Permeable junctions. Cold Spring Harbor Symp. Quant. Biol 40: 49–63.

    Article  Google Scholar 

  4. Furshpan, E. J., and D. D. Potter. 1968. Low resistance junctions between cells in embryos and tissue culture. Curr. Top. Dey. Biol. 3: 95–116.

    Article  CAS  Google Scholar 

  5. Singer, S. J., and G. L. Nicolson. 1972. The fluid mosaic model of the structure of cell membranes. Science 17: 720–729.

    Article  Google Scholar 

  6. Loewenstein, W. R. 1974. Cellular communication by permeable junctions. In: Cell Membranes: Biochemistry, Cell Biology and Pathology. G. Weissman and R. Claiborne, eds. H. P. Publ. Co., New York. pp. 105–114.

    Google Scholar 

  7. Goodenough, D. A., and J. P. Revel. 1970. A fine structural analysis of intercellular junctions in the mouse liver. J. Cell Biol. 45: 272–288.

    Article  PubMed  CAS  Google Scholar 

  8. McNutt, N. S., and R. S. Weinstein. 1973. Membrane ultrastructure and mammalian intercellular junction. Prog. Biophys. Mol. Biol. 26: 45–62.

    Article  PubMed  CAS  Google Scholar 

  9. Goodenough, D. A. 1975. The structure and permeability of isolated hepatocyte gap junctions. Cold Spring Harbor Symp. Quant. Biol. 40: 37–45.

    Article  Google Scholar 

  10. Peracchia, C., and M. E. Fernandez-Jaimovich. 1975. Isolation of intramembranous particles from gap junction. J. Cell Biol. 67: 330a.

    Google Scholar 

  11. Gilula, N. B., and M. L. Epstein. 1976. Cell-to-cell communication, gap junction and calcium. Symp. Soc. Exp. Biol. 30: 257–272.

    CAS  Google Scholar 

  12. Ito, S., E. Sato, and W. R. Loewenstein. 1974. Studies on the formation of a permeable cell membrane junction. II. Evolving junctional conductance and junctional insulation. J. Membr. Biol. 19: 339–355.

    Article  PubMed  CAS  Google Scholar 

  13. Loewenstein, W. R., and Y. Kanno. 1964. Studies on an epithelial (gland) cell junction. I. Modifications of surface membrane permeability. J. Cell Biol. 22: 565–586.

    Google Scholar 

  14. Pappas, G. D., and M. V. L. Bennett. 1966. Specialized junctions involved in electrical transmission between neurons. Ann. N.Y. Acad. Sci. 137: 495–511.

    Article  PubMed  CAS  Google Scholar 

  15. Rose, B. 1971. Intercellular communication and some structural aspects of cell junctions in a simple cell system. J. Membr. Biol. 5: 1–19.

    Article  CAS  Google Scholar 

  16. Sheridan, J. 1971. Dye movement and low resistance junctions between reaggregated embryonic cells. Del,. Biol. 26: 627–643.

    CAS  Google Scholar 

  17. Azarnia, R., and W. R. Loewenstein. 1971. Intercellular communication and tissue growth. V. A cancer cell strain that fails to make permeable membrane junctions with normal cells. J. Membr. Biol. 6: 368–385.

    Article  Google Scholar 

  18. Azarnia, R., W. Michalke, and W. R. Loewenstein. 1972. Intercellular communication and tissue growth. VI. Failure of exchange of endogenous molecules between cancer cells with defective junctions and noncancerous cells. J. Membr. Biol. 10: 247–258.

    Article  PubMed  CAS  Google Scholar 

  19. Pollack, G. H. 1976. Intercellular coupling in the atrioventricular node and other tissues of the rabbit heart. J. Physiol. (Land.) 255: 275–298.

    CAS  Google Scholar 

  20. Kanno, Y., and W. R. Loewenstein. 1966. Cell-to-cell passage of large molecules. Nature 212: 629–630.

    Article  PubMed  CAS  Google Scholar 

  21. Potter, D. D., E. J. Furshpan, and E. S. Lennox. 1966. Connections between cells of the developing squid as revealed by electrophysiological methods. Proc. Natl. Acad. Sci. U.S.A. 55: 328–344.

    Article  PubMed  CAS  Google Scholar 

  22. Payton, B. W., M. V. L. Bennett, and G. D. Pappas. 1969. Permeability and structure of junctional membranes at an electrotonic synapse. Science 166: 16411656.

    Google Scholar 

  23. Johnson, R., and J. D. Sheridan. 1971. Junctions between cancer cells in culture: Ultrastructure and permeability. Science 174: 717–734.

    Article  PubMed  CAS  Google Scholar 

  24. Simpson, I., B. Rose, and W. R. Loewenstein. 1977. Size limit of molecules permeating the junctional membrane channels. Science 195: 294–296.

    Article  PubMed  CAS  Google Scholar 

  25. Oliveira-Castro, G. M., and W. R. Loewenstein. 1971. Junctional membrane permeability: Effects of divalent cations. J. Membr. Biol. 5:51–77.

    Google Scholar 

  26. Rose, B., and W. R. Loewenstein. 1975. Permeability of cell junction depends on local cytoplasmic calcium activity. Nature 254: 250–252.

    Article  PubMed  CAS  Google Scholar 

  27. Rose, B., and W. R. Loewenstein. 1976. Permeability of a cell junction and the local cytoplasmic free ionized calcium concentration. A study with aequorin. J. Membr. Biol. 28: 87–119.

    Article  PubMed  CAS  Google Scholar 

  28. Shimomura, O., and F. H. Johnson. 1969. Properties of the bioluminescent protein aequorin. Biochemistry 8: 3991–4008.

    Article  PubMed  CAS  Google Scholar 

  29. Rose, B., and W. R. Loewenstein. 1975. Calcium ion distribution in cytoplasm visualized by aequorin: Diffusion in the cytosol is restricted due to energized sequestering. Science 190:1204–1206.

    Google Scholar 

  30. Délèze, J., and W. R. Loewenstein. 1976. Permeability of a cell junction during intracellular injection of divalent cations. J. Membr. Biol. 28: 71–86.

    Article  PubMed  Google Scholar 

  31. Rose, B., I. Simpson, W. R. Loewenstein. 1977. Calcium ion produces graded changes in permeability of membrane channels in cell junction. Nature 267: 625627.

    Google Scholar 

  32. Loewenstein, W. R. 1967. Cell surface membranes in close contact. Role of calcium and magnesium ions. J. Colloid Interface Sci. 25: 34–46.

    Article  PubMed  CAS  Google Scholar 

  33. Loscalzo, J., G. H. Reed, and A. Weber. 1976. Conformational change and cooperativity in actin filaments free of tropomyosin. Proc. Natl. Acad. Sci. U.S.A. 72: 3412–3428.

    Article  Google Scholar 

  34. Haynes, D. 1977. Divalent cation-ligand interactions of phospholipid membranes. In: Metal-Ligand Interactions in Organic Chemistry and Biochemistry. Part II. B. Pullman and M. Goldblum, eds. Ninth Jerusalem Symp. D. Ridell, Dordrecht, Holland. pp. 189–212.

    Google Scholar 

  35. Peracchia, C., and A. Dulhunty. 1976. Low resistance junctions in crayfish. Structural changes with functional uncoupling. J. Cell Biol. 70: 419–439.

    Article  PubMed  CAS  Google Scholar 

  36. Loewenstein, W. R., and R. D. Penn. 1967. Intercellular communication and tissue growth. II. Tissue regeneration. J. Cell Biol. 33: 235–242.

    Article  PubMed  CAS  Google Scholar 

  37. Penn, R. D. 1966. Ionic communication between liver cells. J. Cell Biol. 29:171–173.

    Google Scholar 

  38. Loewenstein, W. R. 1968. Some reflections on growth and differentiation. Perspect. Biol. Med. 11: 260–272.

    PubMed  CAS  Google Scholar 

  39. Loewenstein, W. R. 1968. Communication through cell junctions. Implications in growth control and differentiation. Dev. Biol. 19 (Suppl. 2): 151–183.

    Google Scholar 

  40. Slack, C., and J. P. Palmer, 1969. The permeability of intercellular junctions in the early embryo of Xenopus laevis, studies with fluorescent tracer. Exp. Cell Res. 55: 416–431.

    Article  PubMed  CAS  Google Scholar 

  41. Warner, A. E. 1973. Electrical properties of the actoderm in the amphibian embryo during induction and early development of the nervous system. J. Physiol. (Lond.) 235: 267–286.

    CAS  Google Scholar 

  42. Lehninger, A. L., E. Carafoli, and C. S. Rossi. 1967. Energy-linked ion movements in mitochondrial systems. Adv. Enzymol. 29: 259–320.

    PubMed  CAS  Google Scholar 

  43. Moore, L., T. Chen, H. R. Knapp, and E. J. Landon. 1975. Energy-dependent calcium sequestration activity in rat liver microsomes. J. Biol. Chem. 250: 4562–4568.

    PubMed  CAS  Google Scholar 

  44. Baker, P. F., and A. C. Crawford. 1972. Mobility and transport of magnesium in squid giant axons. J. Physiol. (Lond.) 227: 855–871.

    CAS  Google Scholar 

  45. Loewenstein. W. R., M. Nakas, and S. J. Socolar. 1967. Junctional membrane uncoupling. Permeability transformations at a cell membrane junction. J. Gen. Physiol. 50:1865–1891.

    Google Scholar 

  46. Politoff, A. L., S. J. Socolar, and W. R. Loewenstein. 1969. Permeability of a cell membrane junction. Dependence on energy metabolism. J. Gen. Physiol. 53: 498515.

    Google Scholar 

  47. Rose, B., and W. R. Loewenstein. 1971. Junctional membrane permeability. Depression by substitution of Li for extracellular Na, and by long-term lack of Ca and Mg; restoration by cell repolarization. J. Membr. Biol. 5: 20–50.

    Article  CAS  Google Scholar 

  48. Délèze, J. 1970. The recovery of resting potential and input resistance in sheep heart injured by knife or laser. J. Physiol. (Lond.) 208: 547–564.

    Google Scholar 

  49. Délèze, J. 1975. The site of healing over after local injury in the heart. In: Recent Advances in Studies on Cardiac Structure and Metabolism, Vol. 5. A. Fleckenstein and N. S. Dhalla, eds. Univ. Park Press, Baltimore. pp. 223–235.

    Google Scholar 

  50. de Mello, W. C. 1975. Effect of intracellular injection of calcium and strontium on cell communication in heart. J. Physiol. (Lond.) 250: 231–245.

    Google Scholar 

  51. Ito, S., E. Sato, and W. R. Loewenstein. 1974. Studies on the formation of a permeable cell membrane junction. I. Coupling under various conditions of membrane contact. Colchicine, cytochalasin B, dinitrophenol. J. Membr. Biol. 19: 305–337.

    Article  PubMed  CAS  Google Scholar 

  52. Ito, S., and W. R. Loewenstein. 1969. Ionic communication between early embryonic cells. Del). Biol. 19: 228–243.

    Article  CAS  Google Scholar 

  53. Johnson, R., M. Hammer, J. Sheridan, and J. P. Revel. 1974. Gap junction formation between reaggregated Novikoff hepatoma cells. Proc. Natl. Acad. Sci. U.S.A. 71: 4536–4540.

    Article  PubMed  CAS  Google Scholar 

  54. Edidin, M. 1974. Rotational and translational diffusion in membranes. Annu. Rev. Biophys. Bioeng. 3: 179201.

    Google Scholar 

  55. Schlesinger, J., D. Axelrod, D. E. Koppel, W. W. Webb, and E. L. Elson. 1977. Lateral transport of a lipid probe and labeled proteins on a cell membrane. Science 195:4275–4287.

    Google Scholar 

  56. Azarnia, R., W. J. Larsen, and W. R. Loewenstein. 1974. The membrane junctions in communicating and non-communicating cells, their hybrids and segregants. Proc. Natl. Acad. Sci. U.S.A. 71: 880–884.

    Article  PubMed  CAS  Google Scholar 

  57. Azarnia, R., and W. R. Loewenstein. 1977. Intercellular communication and tissue growth. VIII. A genetic analysis of junctional communication and cancerous growth. J. Membr. Biol. 34: 1–37.

    Article  PubMed  CAS  Google Scholar 

  58. Larsen, W. J., R. Azarnia, and W. R. Loewenstein. 1977. Intercellular communication and tissue growth. IX. Junctional membrane structure of hybrids between communication-competent and communication-incompetent cells. J. Membr. Biol. 34: 39–54.

    Article  PubMed  CAS  Google Scholar 

  59. Jamakosmanovic, A., and W. R. Loewenstein. 1968. Intercellular communication and tissue growth. III. Thyroid cancer. J. Cell Biol. 38: 556–561.

    Article  PubMed  CAS  Google Scholar 

  60. Lewis, S. A., D. C. Eaton, and J. M. Diamond. 1976. The mechanism of Na+ transport in rabbit urinary bladder. J. Membr. Biol. 28: 41–70.

    Article  PubMed  CAS  Google Scholar 

  61. Nagel, W. 1976. Intercellular junctions of frog skin epithelial cells. Nature 264: 469–471.

    Article  PubMed  CAS  Google Scholar 

  62. Furshpan, E. J., and D. D. Potter. 1959. Transmission at the giant motor synapses of the crayfish. J. Physiol. (Lond.) 145:289–325.

    Google Scholar 

  63. Woodbury, J. W., and W. E. Crill. 1961. In: Nervous Inhibition. E. Flong, ed. Pergamon, Oxford.

    Google Scholar 

  64. Weidmann, S. 1952. The electrical constants of Purkinje fibers. J. Physiol. (Lond.) 118: 348–360.

    CAS  Google Scholar 

  65. Weidmann, S. 1966. The diffusion of radio potassium across intercalated disks of mammalian cardiac muscle. J. Physiol. (Lond.) 187: 323–342.

    CAS  Google Scholar 

  66. Barr, L., M. M. Dewey, and W. Berger. 1965. Propagation of the action potentials and the structure of the nexus in cardiac muscle. J. Gen. Physiol. 48: 797–823.

    Article  PubMed  CAS  Google Scholar 

  67. Dewey, M. M., and L. Barr. 1964. A study of the structure and distribution of the nexus. J. Cell Biol. 23: 553–585.

    Article  PubMed  CAS  Google Scholar 

  68. Ito, S., and N. Hori. 1966. Electrical characteristics of Triturus egg cells during cleavage. J. Gen. Physiol. 49:1019–1027.

    Google Scholar 

  69. Sheridan, J. 1968. Electrophysiological evidence for low resistance junctions in the early chick embryo. J. Cell Biol. 37: 650–659.

    Article  PubMed  CAS  Google Scholar 

  70. Wolpert, L. 1971. Positional information and pattern formation. Curr. Top. Dev. Biol. 6: 883–224.

    Google Scholar 

  71. Crick, F. H. C. 1970. Diffusion in embryogenesis. Nature 225:420–422.

    Google Scholar 

  72. Loewenstein, W. R. 1969. Transfer of information through cell junctions and growth control. In: EighthCanadian Cancer Conference, Honey Harbour. J. F. Morgan, ed. Pergamon, Toronto. pp. 162–170.

    Google Scholar 

  73. Burton, A. C. 1971. Cellular communication, contact inhibition, cell clocks, and cancer. Perspect. Biol. Med. 14: 301–318.

    PubMed  CAS  Google Scholar 

  74. Burton, A. C. 1975. The role of biochemical rhythms in contact inhibition of cellular division. In: Cellular Membranes and Tumor Cell Behavior. Williams & Wilkins, Baltimore. pp. 249–266.

    Google Scholar 

  75. Socolar, S. J. 1973. Cell coupling in epithelia. Exp. Eye Res. 15: 693–698.

    Article  PubMed  CAS  Google Scholar 

  76. Loewenstein, W. R. 1975. Intercellular communications in normal and neoplastic tissues. In: Cellular Membranes and Tumor Cell Behavior. Williams & Wilkins, Baltimore. pp. 239–248.

    Google Scholar 

  77. Borek, C., S. Higashino, and W. R. Loewenstein. 1969. Intercellular communication and tissue growth. IV. Conductance of membrane junctions of normal and cancerous cells in culture. J. Membr. Biol. 1: 274–293.

    Article  Google Scholar 

  78. Sheridan, J. 1970. Low resistance junctions between cancer cells in various solid tumors. J. Cell Biol. 45: 91–99.

    Article  PubMed  CAS  Google Scholar 

  79. Azamia, R., and W. R. Loewenstein. 1976. Intercellular communication and tissue growth. VII. A cancer cell strain with retarded formation of permeable membrane junction and reduced exchange of a 330-dalton molecule. J. Membr. Biol. 30:175–186.

    Google Scholar 

  80. Subak-Sharpe, H., R. R. Burk, and J. D. Pitts. 1969. Metabolic cooperation between biochemically marked mammalian cells in culture. J. Cell Sci. 4: 353–360.

    PubMed  CAS  Google Scholar 

  81. Cox, R. P., M. R. Kraus, M. E. Balis, and J. Dancis. 1970. Evidence of transfer of enzyme product as the basis of metabolic cooperation between tissue culture fibroblasts of Lesch-Nyhan disease and normal cells. Proc. Natl. Acad. Sci. U.S.A.67:1573–1579.

    Google Scholar 

  82. Pitts, J. D. 1971. Growth control in cell culture. In: Ciba Foundation Symposium. G. Wolstenholme and J. Knight, eds. Churchill, Livingston, London. p. 89

    Google Scholar 

  83. Gilula, N. B., O. R. Reeves, and A. Steinbach. 1972. Metabolic coupling, ionic coupling and cell contacts. Nature 235:262–265.

    Google Scholar 

  84. Pitts, J. D. 1975. How do animal cells communicate? Nature255:371.

    Google Scholar 

  85. Loewenstein, W. R., and S. J. Socolar. 1978. Methods for studying cell-cell communication. In: Methods in Membrane Biology,Vol. 6. E. Korn, ed. Plenum, New York.

    Google Scholar 

  86. Weiss, M. C., J. Todaro, and H. Green. 1968. Properties of a hybrid between lives sensitive and insensitive to contact inhibition of cell division. J. Cell. Physiol.71:105–108.

    Article  PubMed  CAS  Google Scholar 

  87. Klein, G., V. Bregula, F. Wiener, and H. Harris. 1971. The analysis of malignancies by cell fusion. I. Hybrids between tumor cells and L cell derivatives. J. Cell Sci.8:659–672.

    Google Scholar 

  88. Harris, H. 1971. Cell fusion and the analysis of malignancy. Proc. R. Soc. Lond. 179: 1–20.

    Article  PubMed  CAS  Google Scholar 

  89. Azarnia, R., and W. R. Loewenstein. 1973. Parallel correction of cancerous growth and of a genetic defect of cell-to-cell communication. Nature 241: 445–457.

    Article  Google Scholar 

  90. Loewenstein, W. R. 1978. Junctional intercellular communication and growth control. B.B.A. Rev. Cancer. In press.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1980 Springer Science+Business Media New York

About this chapter

Cite this chapter

Loewenstein, W.R. (1980). Cell-to-Cell Communication. In: Andreoli, T.E., Hoffman, J.F., Fanestil, D.D. (eds) Membrane Physiology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-1718-1_18

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-1718-1_18

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-1720-4

  • Online ISBN: 978-1-4757-1718-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics