Control of intercellular communication by voltage dependence of gap junctional conductance

The junctional conductance between coupled amphibian blastomeres exhibits a high degree of voltage dependence, as previously described in voltage clamp studies (Spray, D.C., A.L. Harris, and M.V.L. Bennett (1981) J. Gen. Physiol. 77: 77–95; Harris, A.L., D.C. Spray, and M.V.L. Bennett (1981) J. Gen. Physiol. 77: 95–117). The present study examines the properties which this voltage dependence confers on electrotonic coupling between cells. The effects of applied pulses and ramps of current are studied experimentally and are modeled by calculation. During sufficiently large current pulses applied to one cell of a pair, the cells uncouple and then recouple after termination of the pulses. Ramps of current applied to one of the cells can give voltage-current (V-I) relations with a region of hysteresis within which the cells are stably coupled or stably uncoupled depending on previous history. Intrinsically generated currents are able to cause bistability of coupling in the absence of externally applied current. Calculations from the parameters of junctional conductance defined under voltage clamp fully account for these findings and illustrate how junctional and nonjunctional conductances affect the V-I relations in the region of bistability. Recordings from several cells within a small group show that boundaries of intercellular communication can be altered by applied current, a finding that also can be accounted for by voltage dependence of junctional conductance. The “Appendix” examines quantitatively the criteria required for bistability of coupling and the relevance of bistability for intercellular signaling. The plasticity of coupling which the voltage dependence of junctional conductance confers on cells offers an intriguing mechanism by which patterns of intercellular communication could be determined and changed in developing tissues.

[1]  E. Neher,et al.  Local anaesthetics transiently block currents through single acetylcholine‐receptor channels. , 1978, The Journal of physiology.

[2]  D. Spray,et al.  Control of Intercellular Communication via Gap Junctions , 1982 .

[3]  C. Goodman,et al.  Transient Dye Coupling Between Developing Neurons Reveals Patterns of Intercellular Communication During Embryogenesis , 1982 .

[4]  D C Spray,et al.  Gap junctional conductance is a simple and sensitive function of intracellular pH. , 1981, Science.

[5]  M. Spira,et al.  Synaptic organization of expansion motoneurons ofNavanax inermis , 1980, Brain Research.

[6]  P. Elias,et al.  Vitamin-A-induced mucous metaplasia. An in vitro system for modulating tight and gap junction differentiation , 1976, The Journal of cell biology.

[7]  L. Wolpert.  Positional information and the spatial pattern of cellular differentiation. , 1969, Journal of theoretical biology.

[8]  T. Lentz.  Organization and Development of the Embryo , 1970, The Yale Journal of Biology and Medicine.

[9]  R. Flickinger,et al.  A study of the metabolism of amphibian neural crest cells during their migration and pigmentation in vitro. , 1949, The Journal of experimental zoology.

[10]  N. Spitzer.  Voltage‐ and stage‐development uncoupling of Rohon‐Beard neurones during embryonic development of Xenopus tadpoles , 1982, The Journal of physiology.

[11]  M. Fuortes,et al.  Electrical Connections between Visual Cells in the Ommatidium of Limulus , 1965, Science.

[12]  D C Spray,et al.  Equilibrium properties of a voltage-dependent junctional conductance , 1981, The Journal of general physiology.

[13]  D C Spray,et al.  Kinetic properties of a voltage-dependent junctional conductance , 1981, The Journal of general physiology.

[14]  M. Spira,et al.  Permeability of gap junctions between embryonic cells of Fundulus: a reevaluation. , 1978, Developmental biology.

[15]  L. Jaffe,et al.  The role of ionic currents in establishing developmental pattern. , 1981, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  W. Loewenstein,et al.  Permeability of cell junction depends on local cytoplasmic calcium activity , 1975, Nature.

[17]  M. V. Bennett,et al.  Voltage threshold in excitable cells depends on stimulus form. , 1970, Journal of Neurophysiology.

[18]  T. G. Smith,et al.  The functional organization within the ommatidium of the lateral eye of limulus. , 1969, Progress in brain research.

[19]  M. Bennett,et al.  Electrical Coupling in Development , 1981 .

[20]  S. J. Socolar,et al.  Uncoupling Cell Junctions in a Glandular Epithelium by Depolarizing Current , 1971, Science.

[21]  JOHN W. Moore.  Membranes, ions, and impulses , 1976 .

[22]  M. V. Bennett,et al.  Gap junctions, electrotonic coupling, and intercellular communication. , 1978, Neurosciences Research Program bulletin.

[23]  M. Poo,et al.  Electrophoresis and diffusion in the plane of the cell membrane. , 1979, Biophysical journal.

[24]  D. Spray,et al.  Gap junctions and development , 1981, Trends in Neurosciences.

[25]  N. S. Mcnutt,et al.  NEXUS JUNCTIONS BETWEEN DIVIDING AND INTERPHASE GRANULOSA CELLS OF THE RAT OVARY , 1972, The Journal of cell biology.

[26]  A Gierer,et al.  Biological features and physical concepts of pattern formation exemplified by hydra. , 1977, Current topics in developmental biology.

[27]  C. Stevens,et al.  Sodium channels need not open before they inactivate , 1981, Nature.

[28]  N. Gilula,et al.  Transmission of hormonal stimulation by cell-to-cell communication , 1978, Nature.

[29]  M. Finbow,et al.  Junctional Permeability and Its Consequences , 1977 .

[30]  D. Potter,et al.  Transmission at the giant motor synapses of the crayfish , 1959, The Journal of physiology.

[31]  A. Warner,et al.  The function of the sodium pump during differentiation of amphibian embryonic neurones. , 1979, The Journal of physiology.

[32]  D. Potter,et al.  Low-resistance junctions between cells in embryos and tissue culture. , 1968, Current topics in developmental biology.

[33]  D. Potter,et al.  Chapter 4 Low-Resistance Junctions Between Cells in Embryos and Tissue Culture , 1968 .

[34]  B. Rose,et al.  Junctional Membrane Permeability: Restoration by Repolarizing Current , 1970, Science.

[35]  C. Goodman,et al.  Embryonic development of identified neurones: differentiation from neuroblast to neurone , 1979, Nature.

[36]  M. Bennett,et al.  PHYSIOLOGY OF ELECTROTONIC JUNCTIONS * , 1966, Annals of the New York Academy of Sciences.

[37]  D. Spray,et al.  Voltage dependence of junctional conductance in early amphibian embryos. , 1979, Science.

[38]  A. Warner,et al.  Alterations in resting membrane properties during neural plate stages of development of the nervous system. , 1976, The Journal of physiology.

[39]  D. Purves,et al.  Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech , 1970, The Journal of physiology.

[40]  D. Spray,et al.  Gap junctional conductance: comparison of sensitivities to H and Ca ions. , 1982, Proceedings of the National Academy of Sciences of the United States of America.