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Intercellular communication and tissue growth

IV. Conductance of membrane junctions of normal and cancerous cells in culture

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Summary

Epithelial cells of normal rat (adult) liver and hamster embryo in tissue culture communicate through membrane junctions: the membrane regions of cell contact are highly ion-permeable. Cancerous counterparts of these cells, cells from Morris' and Reuber's liver tumors and from x-ray-transformed embryo cultures, do not communicate under the same experimental conditions. These cells also fail to communicate with contiguous normal cells. Cancerous fibroblastic cells from a variety of tissues, including cells transformed by virus, x-radiation and chemicals, communicate as well as their normal counterparts; this is so for long- and short-term cell cultures. Communication in some fibroblastic cells is sensitive to components of blood serum: normal and transformed hamster embryo fibroblasts, which communicate when cultured in medium containing fetal calf serum, appear to lose communication in medium containing calf serum; the converse holds for hamster (adult) fibroblasts and 3T3 cells.

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References

  • Abercrombie, M. 1966. Contact inhibition: The phenomenon and its biological implications.Nat. Cancer Inst. Monogr. 26:249.

    Google Scholar 

  • —, and E. J. Ambrose. 1958. Interference microscope studies of cell contacts in tissue culture.Expl. Cell Res. 15:332.

    Google Scholar 

  • —, J. E. M. Heaysman, and H. M. Karhauser. 1957. Social behaviour of cells in tissue culture. III Mutual influence of sarsoma cells and fibroblasts.Expl. Cell Res. 13:276.

    Google Scholar 

  • Bennett, M. V. L. 1966. Physiology of electrotonic junctions.In: Conference on Biological Membranes, Recent Progress.Ann. N. Y. Acad. Sci. 137:509.

  • Berwald, Y., and L. Sachs. 1965.In vitro transformation of normal cells to tumor cells by carcinogenic hydrocarbons.J. Nat. Cancer Inst. 35:641.

    PubMed  Google Scholar 

  • Borek, C., and L. Sachs. 1966a. In vitro cell transformation by x-radiation.Nature 210:276.

    PubMed  Google Scholar 

  • Borek, C., and L. Sachs. 1966b. The difference in contact inhibition of cell replication between normal cells and cells transformed by different carcinogens.Proc. Nat. Acad. Sci. 56:1705.

    Google Scholar 

  • ——. 1967. Cell susceptibility to transformation by x-irradiation and fixation of the transformed state.Proc. Nat. Acad. Sci. 57:1522.

    PubMed  Google Scholar 

  • Coman, D. R. 1944. Decreased mutual adhesiveness, a property of cells from squamous cell carcinomas.Cancer Res. 4:625.

    Google Scholar 

  • Coon, H. G., and M. C. Weiss. 1969. A quantitative comparison of formation of spontaneous and virus-produced viable hybrids.Proc. Nat. Acad. Sci. 62:852.

    PubMed  Google Scholar 

  • Curtis, A. S. G., and M. F. Greaves. 1965. The inhibition of aggregation by a pure serum protein.J. Embryol. Exp. Morphol. 13:309.

    PubMed  Google Scholar 

  • Defendi, V., R. I. Carp, and R. V. Gilden. 1966. Cellular antigens induced by viruses.In: Viruses Inducing Cancer. W. J. Burdette, editor. p. 269. Univ. Utah Press, Salt Lake City.

    Google Scholar 

  • Eagle, H. 1960. The sustained growth of human and animal cells in protein-free environment.Proc. Nat. Acad. Sci. 46:427.

    Google Scholar 

  • —, V. I. Oyama, M. Levy, and A. E. Freeman. 1957. Myo-inositol as an essential growth factor for normal and malignant human cells in tissue culture.J. Biol. Chem. 226:191.

    PubMed  Google Scholar 

  • Fischer, H. W., T. T. Puck, and G. Sato. 1957. Molecular growth requirements of single mammalian cells: The action of fetuin in promoting cell attachment to glass.Proc. Nat. Acad. Sci. 44:4.

    Google Scholar 

  • Furshpan, E. J., and D. D. Potter. 1968. Low resistance junctions between cells in embryos and tissue culture.Curr. Topics Devel. Biol. 3:95.

    Google Scholar 

  • Ham, R. G. 1965. Clonal growth of mammalian cells in a chemically defined, synthetic medium.Proc. Nat. Acad. Sci. 53:288.

    PubMed  Google Scholar 

  • Higashino, S., C. Borek, and W. R. Loewenstein. 1969. Lack of communication between cancerous epithelial cells in tissue culture.Fed. Proc. 28: abs. 2375, 684.

    Google Scholar 

  • Holley, R. W., and J. A. Kiernan. 1968. Contact inhibition of cell division in 3T3 cells.Proc. Nat. Acad. Sci. 60:300.

    PubMed  Google Scholar 

  • Holmes, R. 1967. Preparation from human serum of an alpha-one protein which induces the immediate growth of unadapted cells in vitro.J. Cell Biol. 32:297.

    PubMed  Google Scholar 

  • Ito, S., and W. R. Loewenstein. 1969. Ionic communication between early embryonic cells.Devel. Biol. 19:228.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Kanno, Y., and H. Matsui. 1968. Cellular uncoupling in cancerous stomach epithelium.Nature 218:775.

    Google Scholar 

  • Lieberman, I., and P. Ove. 1957. Purification of a serum protein required by a mammalian cell in tissue culture.Biochim. Biophys. Acta 25:449.

    PubMed  Google Scholar 

  • Lilien, J. E. 1968. Specific enhancement of cell aggregation in vitro.Devel. Biol. 17:657.

    Google Scholar 

  • Loewenstein, W. R. 1966. Permeability of membrane junctions.In: Conference on Biological Membranes, Recent Progress.Ann. N. Y. Acad. Sci. 137:441.

    PubMed  Google Scholar 

  • — 1967a. On the genesis of cellular communication.Devel. Biol. 15:503.

    Google Scholar 

  • — 1967b. Cell surface membranes in close contact. Role of calcium and magnesium ions.J. Colloid Interface Sci. 25:34.

    PubMed  Google Scholar 

  • — 1968a. Some reflections on growth and differentiation.Perspect. Biol. Med. 11: 260.

    PubMed  Google Scholar 

  • Loewenstein, W. R. 1968b. Communication through cell junctions. Implications in growth and differentation.In: The Emergence of Order in Developing Systems. M. Locke, editor.Devel. Biol. 19:Sup. 2, 151.

  • Loewenstein, W. R. 1969. Transfer of information through cell junctions and growth control. In: Candian Cancer Conference: Proc. 8th Canad. Cancer Res. Conf., 1968, Honey Harbour, Ontario. J. F. Morgan, editor. p. 162. Pergamon Press, Toronto.

    Google Scholar 

  • —, and Y. Kanno. 1964. Studies on an epithelial (gland) cell junction. I. Modifications of surface membrane permeability.J. Cell Biol. 22:565.

    PubMed  Google Scholar 

  • ——. 1966. Intercellular communication and the control of tissue growth. Lack of communication between cancer cells.Nature 209:1248.

    PubMed  Google Scholar 

  • ——. 1967., Intercellular communication and tissue growth I. Cancerous growth.J. Cell Biol. 33:225.

    PubMed  Google Scholar 

  • —, and R. D. Penn. 1967. Intercellular communication and tissue growth. II. Tissue regeneration.J. Cell Biol. 33:235.

    PubMed  Google Scholar 

  • —, S. J. Socolar, S. Higashino, Y. Kanno, and N. Davidson. 1965. Intercellular communication: renal, urinary bladder, sensory, and salivary gland cells.Science 149:295.

    Google Scholar 

  • Mc Cutcheon, M., D. R. Coman, and F. B. Moore. 1948. Studies on invasiveness of cancer. Adhesiveness of malignant cells in various human adenocarcinomas.Cancer 1:460.

    Google Scholar 

  • Medina, D., and L. Sachs. 1963. Studies on lytic interaction and cell transformation with a large and small-plaque mutant of polyoma virus.Virology 19:127.

    Google Scholar 

  • Morris, H. P. 1965. Studies on the development, biochemistry and biology of experimental hepatomas.Advanc. Cancer Res. 9:227.

    Google Scholar 

  • Moscona, A. A. 1961. Tissue reconstruction from dissociated cells in growth in living systems.In: Growth in Living, Systems. M. X. Zarrow, editor. p. 197. Basic Books, New York.

    Google Scholar 

  • —, and M. H. Moscona. 1966. Aggregation of embryonic cells in serum-free medium and its inhibition at suboptimal temperatures.Expl. Cell Res. 41:697.

    Google Scholar 

  • Novikoff, A. B.. 1957. A transplantable rat liver tumor induced by 4-dimethylaminoazobenzene.Cancer Res. 17:1010.

    PubMed  Google Scholar 

  • Novikoff, A. B., and L. Biempica. 1966. Cytochemical and electron microscopical examination of Morris 5123 and Reuber H-35 hepatomas after several years of transplantation.GANN Mongraph I, p. 65.

  • Orr, C. W., and S. Roseman. 1969. Intercellular adhesion. II. Purification and properties of a horse serum protein that promotes neural retina cell aggregation.J. Membrane Biol. 1:125.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Pitot, H. C., C. Periano, P. A. Morse, and V. R. Potter. 1964. Hepatomas in tissue culture compared with adapting liver in vivo.Nat. Cancer Inst. Monogr. 13:229.

    PubMed  Google Scholar 

  • Politoff, A. L., S. J. Socolar, and W. R. Loewenstein. 1969. Permeability of a cell membrane junction dependence on energy metabolism.J. Gen. Physiol. 53:498.

    PubMed  Google Scholar 

  • Potter, D. D., E. T. Furshpan, and E. J. Lennox. 1966. Connections between cells of the developing squid as revealed by electrophysiological methods.Proc. Nat. Acad. Sci. 55:328.

    PubMed  Google Scholar 

  • Sheridan, J. D. 1968. Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo.J. Cell. Biol. 37:650.

    PubMed  Google Scholar 

  • Stoker, M. G. P. 1964. Regulation of growth and orientation in hamster cells transformed by polyoma virus.Virology 24:165.

    PubMed  Google Scholar 

  • — 1967. Transfer of growth inhibition between normal and virus transformed cells; autoradiographic studies using marked cells.J. Cell Sci. 2:293.

    PubMed  Google Scholar 

  • —, M. Sheaver, and C. O'Neill. 1966. Growth inhibition of polyoma-transformed cells by contact with static normal fibroblasts.J. Cell Sci. 1:297.

    PubMed  Google Scholar 

  • Temin, H. M.. 1967a. Studies on carcinogenesis by avian sarcoma viruses. VI. Differential multiplication of uninfected and of converted cells in response to insulin.J. Cell. Comp. Physiol. 69:377.

    Google Scholar 

  • Temin, H. M. 1967b. Control of factors in serum of multiplication of uninfected cells and cells infected and converted by avian sarcoma viruses.In: Growth Regulatory Substances for Animal Cells in Culture. V. Defendi, editor. Wistar Institute Press, Philadelphia.

    Google Scholar 

  • —, and H. Rubin. 1958. Characteristics of an assay for Rous sarcoma virus and Rous sarcoma cells in tissue culture.Virology 6:669.

    PubMed  Google Scholar 

  • Todaro, G. J., H. Green, and B. D. Goldberg. 1964. Transformation of properties of an established cell line by SV-40 and polyoma virus.Proc. Nat. Acad. Sci. 51:66.

    PubMed  Google Scholar 

  • —, K. Habel, and H. Green. 1965. Antigenic and cultural properties of cells doubly transformed by polyoma virus and SV-40.Virology 27:179.

    PubMed  Google Scholar 

  • —, G. K. Lazar, and H. Green. 1965. The initiation of cell division in a contact-inhibited mammalian cell line.J. Cell. Comp. Physiol. 66:325.

    Google Scholar 

  • Vogt, M., and R. Dulbecco. 1960. Virus-cell interaction with a tumor-producing virus.Proc. Nat. Acad. Sci. 46:365.

    Google Scholar 

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Author notes

  1. Carmia Borek

    Present address: Irvington House Institute and Dept. of Pathology, New York University Medical Center, 10016, New York, New York

Authors and Affiliations

  1. Cell Physics Laboratory, Department of Physiology, Columbia University, College of Physicians & Surgeons, 10032, New York, New York

    Carmia Borek, S. Higashino & W. R. Loewenstein

Authors
  1. Carmia Borek
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  2. S. Higashino
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  3. W. R. Loewenstein
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Additional information

The preceding papers of this series appeared in the Journal of Cell Biology.

Trainee of the National Institutes of Health, National Cancer Institute, Grant CA 05011.

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Borek, C., Higashino, S. & Loewenstein, W.R. Intercellular communication and tissue growth. J. Membrain Biol. 1, 274–293 (1969). https://doi.org/10.1007/BF01869786

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