Physiological Roles of Gap Junctional Communication in Reproduction

  • Robert C. Burghardt
  • William H. Fletcher

Abstract

The uterus exhibits a unique structural and physiological plasticity when responding to ovarian cues with orderly cycles of tissue differentiation, glandular secretion, and regional turnover of terminally differentiated cells. These cyclic changes are programmed to be developmentally synchronous with blastocyst development, such that arrival of a blastocyst in the uterus, followed by interaction of blastocyst trophectoderm with uterine epithelial cells, results in the progressive phases of implantation.

Keywords

Cortisol Adenosine Theophylline Lanthanum Stim 

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References

  1. 1.
    Loeb, L., 1908, The production of deciduomata and the relation between the ovaries and the formation of the decidua, J.A.M.A. 50:1897–1901Google Scholar
  2. 2.
    Reynolds, S. R. M., 1949, Physiology of the Uterus, 2nd, ed., Harper & Brothers, New YorkGoogle Scholar
  3. 3.
    Loewenstein, W. R., 1981, Junctional intercellular communication: The cell-to-cell membrane channel, Physiol. Rev. 61:829–913.PubMedGoogle Scholar
  4. 4.
    Hertzberg, E. L., Lawrence, T. S., Gilula, N. B., 1981, Gap junctional communication, Annu. Rev. Physiol43:479–491CrossRefGoogle Scholar
  5. 5.
    Peracchia, C., 1980, Structural correlates of gap junction permeation, Int. Rev. Cvtol66:81–146Google Scholar
  6. 6.
    Bennett, M. V. L., Goodenough, D. A., 1978, Gap junctions, electronic coupling and intercellular communication, Neurosci Res. Prog. Bull. 16:373–486Google Scholar
  7. 7.
    Hertzberg, E. L., Lawrence, T. S., Gilula, N. B., 1981, Gap junctional communication, Annu. Rev. Physiol. 43:479–491CrossRefGoogle Scholar
  8. 8.
    Larsen, W. J.,Risinger, M. A., 1985, The dynamic life histories of intercellular membrane junctions, in: Modern Cell Biology, Volume 4 (B. Satir, ed.), Alan R. Liss, New York, pp. 151– 216Google Scholar
  9. 9.
    Loewenstein, W. R., 1968, Junctional intercellular communication and the control of growth, Biochim. Biophys Acta 560:1–65Google Scholar
  10. 10.
    Pitts, J. D., Finbow, M. E., 1986, The gap junctionJ. Cell Sci (Suppi) 4:239–266Google Scholar
  11. 11.
    Sheridan, J. D., Atkinson, M. M., 1985, Physiological roles of permeable junctions: Some possibilities, Annu. Rev. Physiol. 47:337–353PubMedCrossRefGoogle Scholar
  12. 12.
    Bennett, M. V. L., Trinkaus, J. P., 1970, Electrical coupling between embryonic cells by way of extracellular space and specialized junctions, J. Cell Biol. 44:592–606PubMedCrossRefGoogle Scholar
  13. 13.
    Gilula, N. B., Reeves, O. R., Steinbach, A., 1972, Metabolic coupling, ionic coupling and cell contacts, Nature 235:262–265PubMedCrossRefGoogle Scholar
  14. 14.
    Simpson, J., Rose, B., Loewenstein, W. R., 1977, Size limit of molecules permeating the junctional membrane channels, Science 195:294–296PubMedCrossRefGoogle Scholar
  15. 15.
    Dewey, M. M., Barr, L., 1964, Intercellular connection between smooth muscle cells: The nexus, Science 137:670–672CrossRefGoogle Scholar
  16. 16.
    Furshpan, E. J., Potter, D. D., 1962, Intracellular and extracellular responses of several regions of the Mauthner cell of the goldfish, J. Neurophysiol. 25:732–771PubMedGoogle Scholar
  17. 17.
    Trachtenberg, M. C., Pollen, D. A., 1970, Neuroglia: Biophysical properties and physiological function, Science 167:1248–1252PubMedCrossRefGoogle Scholar
  18. 18.
    Fletcher, W. H., Byus, C. V., Walsh, D. A., 1987, Receptor-mediated action without receptor occupancy: A function for cell—cell communication in ovarian function, in: Regulation of Ovarian and Testicular Function( V. B. Mahesh, D. S. Dhindsa, E. Anderson, S. P. Kalra, eds.), Plenum Press, New York, pp. 299–323Google Scholar
  19. 19.
    Loewenstein, W. R., 1968, Communication through cell junctions. Implications in growth control and differentiation, Dev. Biol. 19:(Suppl. 2): 151–183Google Scholar
  20. 20.
    Lawrence, T. S., Beers, W. H., and Gilula, N. B., 1978, Transmission of hormonal stimulation by cell-to-cell communication, Nature 272:501–506PubMedCrossRefGoogle Scholar
  21. 21.
    Azarnia, R., and Larsen, W. J., 1976, Intercellular communication and cancer, in: Intercellular Communication( W. C. DeMello, ed.), Plenum Press, New York, pp. 145–172Google Scholar
  22. 22.
    Yotti, L. P., Chang, C. C., Trosko, J. E., 1979, Elimination of metabolic cooperation in Chinese hamster cells by a tumor promoter, Science 206:1089–1091PubMedCrossRefGoogle Scholar
  23. 23.
    Entomoto, T., and Yamasaki, H., 1984, Lack of intercellular communication between chemically transformed and surrounding nontransformed BALBc/3T3 cells, Cancer Res 44:5200–5203Google Scholar
  24. 24.
    Janssen-Timmen, U., Traub, O., Dermietzel, R., Rabes, H. M., and Willecke, K., 1986, Reduced number of gap junctions in rat hepatocarcinomas detected by monoclonal antibody, Carcinogenesis 7:1475–1482PubMedCrossRefGoogle Scholar
  25. 25.
    Hertzberg, E. L., Spray, D. C., and Bennett, M. V. L., 1985, Reduction of gap junctional conductance by microinjection of antibodies against the 27-kDa liver gap junction polypeptide, Proc. Natl. Acad. Sci. U.S.A. 82:2412–2416PubMedCrossRefGoogle Scholar
  26. 26.
    Peracchia, C., Peracchia, L. L., 1980, Gap junction dynamics: Reversible effects of divalent cations, J. Cell Biol. 87:708–718Google Scholar
  27. 27.
    Peracchia, C., Peracchia, L. L., 1980, Gap junction dynamics: Reversible effects of hydrogen ions, J. Cell Biol. 87:719–727Google Scholar
  28. 28.
    Goshima, K., 1969, Synchronized beating of and electrotonic transmission between myocardial cells mediated by heterotypic strain cells in monolayer culture, Exp. Cell Res. 65:161–169CrossRefGoogle Scholar
  29. 29.
    Walsh, D. A., Cooper, R. H., 1979, The physiological regulation and function of cAMP- dependent protein kinases, in: Biochemical Actions of Hormones, Volume 6 ( G. Litwack, ed.), Academic Press, New York, pp. 1–75Google Scholar
  30. 30.
    Beebe, S. J., Corbin, J. D., 1986, Cyclic nucleotide-dependent protein kinases, in: The Enzymes, Volume 17 ( P. D. Boyer, ed.) Academic Press, New York, pp. 43–111Google Scholar
  31. 31.
    Fletcher, W. H., Byus, C. V., 1982, Direct cytochemical localization of catalytic subunits dissociated from cAMP-dependent protein kinase in Reuber H-35 hepatoma cells. I. Development and validation of fluorescinated inhibitor, J. Cell Biol. 93:719–726PubMedCrossRefGoogle Scholar
  32. 32.
    Byus, C. V., Fletcher, W. H., 1982, Direct cytochemical localization of catalytic subunits dissociated from cAMP-dependent protein kinase in Reuber H-35 hepatoma cells. II. Temporal and spatial kinetics, J. Cell Biol 93:727–734Google Scholar
  33. 33.
    Fletcher, W. H., Van Patten, S. M., Cheng, H.-C., Walsh, D. A., 1986, Cytochemical identification of the regulatory subunit of the cAMP protein kinase by use of fluorescently labeled catalytic subunit, J. Biol. Chem. 261:5504–5513PubMedGoogle Scholar
  34. 34.
    Van Patten, S. M., Fletcher, W. H., Walsh, D. A., 1986, The inhibitor protein of the cAMP- dependent protein kinase-catalytic subunit interaction, J. Biol. Chem. 261:5514–5523PubMedGoogle Scholar
  35. 35.
    Murray, S. A., Fletcher, W. H., 1984, Hormone-induced intercellular signal transfer dissociates cyclic AMP-dependent protein kinase, J. Cell Biol. 98:1710PubMedCrossRefGoogle Scholar
  36. 36.
    Fletcher, W. H., Greenan, J. R. T., 1985, Receptor mediated action without receptor occupancy, Endocrinology 116:1660–1662Google Scholar
  37. 37.
    Ware, C. F., Coffman, F., Green, L. M., Fletcher, W. H., 1988, Hierarchy of molecular mechanisms controlling the sensitivity of tumor cells to cytolysis by lumphotoxin and tumor necrosis factor, in: Proceedings of International Conference on Tumor Necrosis Factor/ Cachepin, Lymphotoxin and Related Cytotoxins( B. Bonavida, G. Gifford, H. Kirchner, and N. Old, eds.), F. Karger, Basel, pp. 26–31Google Scholar
  38. 38.
    Fletcher, W. H., Shiu, W. W., Ishida, T. A., Haviland, D. L., and Ware, C. F., 1987, Resistance to the cytolytic action of lymphotoxin and tumor necrosis factor coincides with the presence of gap junctions uniting target cells, J. Immunol. 139:956–962PubMedGoogle Scholar
  39. 39.
    Anderson, W. A., Kang, Y.-H., DeSombre, E., 1975, Estrogen and antagonist-induced changes in endometrial topography of immature and cycling rats, J. Cell Biol. 64:692–703PubMedCrossRefGoogle Scholar
  40. 40.
    Psychoyos, A., 1973, Endocrine control of egg-implantation, in: Handbook of Physiology, Endocrinology, Volume 2, part 2 ( R. O. Greep and E. B. Astwood, eds.), American Physiological Society, Washington, DC, pp. 187–215Google Scholar
  41. 41.
    Winterhager, E., Kuhnel, W., 1982, Alterations in intercellular junctions of the uterine epithelium during preimplantation phase in the rabbit, Cell Tissue Res 224:517–526PubMedCrossRefGoogle Scholar
  42. 42.
    Murphy, C. R., Swift, J. G., Mukherjee, T. M., Rogers, A. W., 1982, Reflexive gap junctions on uterine luminal epithelial cells, Acta Anat. 112: 92–96PubMedCrossRefGoogle Scholar
  43. 43.
    Herr, J. C., 1976, Reflexive gap junctions. Gap junctions between processes arising from the same ovarian decidual cell, J. Cell Biol. 69:495–501PubMedCrossRefGoogle Scholar
  44. 44.
    Herr, J. C., Heidger, P. M., 1978, A freeze-fracture study of exocytosis and reflexive gap junctions in human ovarian decidual cells, Am. J. Anat. 152:29–44PubMedCrossRefGoogle Scholar
  45. 45.
    Lawn, A. M., Wilson, E. W., and Finn, C. A., 1971, The ultrastructure of human decidual and predecidual cells, J. Reprod. Fertil. 26:85–90PubMedCrossRefGoogle Scholar
  46. 46.
    Murphy, C. R., Swift, J. G., Mukherjee, T. M., Rogers, A. W., 1981, Effects of ovarian hormones on cell membranes in the rat uterus. II. Freeze-fracture studies on tight junctions of the lateral plasma membrane of the luminal epithelium, Cell Biophysics 3:57–69PubMedCrossRefGoogle Scholar
  47. 47.
    Murphy, C. R., Swift, J. G., Mukherjee, T. M., Rogers, A. W., 1982, The structure of tight junctions between uterine luminal epithelial cells at different stages of pregnancy in the rat, Cell Tissue Res 223:281–286PubMedCrossRefGoogle Scholar
  48. 48.
    Murphy, C. R., Swift, J. G., Need, J. A., Mukherjee, T. M., and Rogers, A. W., 1982, A freeze- frature electron microscopic study of tight junctions of epithelial cells in the human uterus, AnatEmbryol 163:367–370CrossRefGoogle Scholar
  49. 49.
    Winterhager, E., Brummer, F., Dermietzel, R., Hulser, D. F., and Denker, H.-W., 1988, Gap junction formation in rabbit uterine epithelium in response to embryo recognition, Dev. Biol. 126:203–211PubMedCrossRefGoogle Scholar
  50. 50.
    Enders, A. E., and Schlafke, S., 1967, A morphological analysis of the early implantation in the rat, J. Anat. 120:1850–225Google Scholar
  51. 51.
    Potts, D. M., 1969, The ultrastructure of egg implantation, Adv. Reprod. Physiol 4:241–267. 307Google Scholar
  52. 52.
    Tachi, S., and Tachi, C., 1979, Ultrastructural studies on maternal–embryonic cell interaction during experimentally induced implantation of rat blastocysts to the endometrium of the mouse, Dev. Biol. 68:203–223PubMedCrossRefGoogle Scholar
  53. 53.
    Lejeune, B., Van Hoeck, J., Leroy, F., 1981, Transmitter role of the luminal uterine epithelium in the induction of decidualization in rats, J. Reprod. Fertil. 61:235–240PubMedCrossRefGoogle Scholar
  54. 54.
    Moulton, B. C., Koenig, B. B., 1986, Biochemical responses of the luminal epithelium and uterine sensitization, Ann. N.Y. Acad. Sci. 476:95–109PubMedCrossRefGoogle Scholar
  55. 55.
    Furchgott, R. F., 1983, Role of endothelium in responses of vascular smooth muscle, Circ. Res. 53:557–573PubMedGoogle Scholar
  56. 56.
    Finn, C. A., Porter, D. G., 1975, The Uterus, Elek Science, LondonGoogle Scholar
  57. 57.
    DeFeo, V. J., 1967, Decidualization, in: Cellular Biology of the Uterus( R. M. Wynn, ed.), Meredith Publishing, New York, pp. 191–290Google Scholar
  58. 58.
    Kleinfeld, R. G., Morrow, H. A., and DeFeo, V. J., 1976, Intercellular junctions between decidual cells in the growing deciduoma of the pseudopregnant rat uterus, Biol. Reprod. 15:593–603PubMedCrossRefGoogle Scholar
  59. 59.
    O’Shea, J. D., Kleinfeld, R. G., and Morrow, H. A., 1983, Ultrastructure of decidualization in the pseudopregnant rat, Am. J. Anat. 166:271–298PubMedCrossRefGoogle Scholar
  60. 60.
    Finn, C. A., and Lawn, A. M., 1967, Specialized junctions, between decidual cells in the uterus of the pregnant mouse, J. Ultrastruct. Res. 20:321–327PubMedCrossRefGoogle Scholar
  61. 61.
    Finn, C. A., 1971, The biology of decidual cells, Adv. Reprod. Physiol. 5:1–26PubMedGoogle Scholar
  62. 62.
    Bernhard, O., Rachman, F., 1980, Immunological aspects of the decidual reaction, Prog. Reprod. Biol. 7:135–142Google Scholar
  63. 63.
    Gibori, G., Rothchild, I., Pepe, G. J., Morishige, W. K., and Lam, P., 1974, Luteotrophic action of decidual tissue in the rat, Endocrinology 95:1113–1118PubMedCrossRefGoogle Scholar
  64. 64.
    Jayatilak, P. G., Glaser, L. A., Basuray, R., Kelly, P. A., Gibori, G., 1985, Identification and partial characterization of a prolactin-like hormone produced by rat decidual tissue, Proc. Natl. Acad. Sci. U.S.A. 82:217–221PubMedCrossRefGoogle Scholar
  65. 65.
    Golander, A., Hurley, T., Barrett, J., Hize, A., Handwerger, S., 1978, Prolactin synthesis by human chorion-decidual tissue: A possible source of amniotic fluid prolactin, Science 202:311–312PubMedCrossRefGoogle Scholar
  66. 66.
    Tomita, K., McCoshen, J. A., Friesen, H. G., Tyson, J. E., 1982, Quantitative comparison between biological and immunological activities of prolactin derived from human fetal and maternal sources, J. Clin. Endocrinol. Metab. 55:269–271CrossRefGoogle Scholar
  67. 67.
    Handwerger, S., Barry, S., Markoff, E., Barrett, J., Conn, P. M., 1983, Stimulation of the synthesis and release of decidual prolactin by a placental polypeptide, Endocrinology 112:1370–1374PubMedCrossRefGoogle Scholar
  68. 68.
    Markoff, E., Howell, S., Handwerger, S., 1983, Inhibition of decidual prolactin by a decidual peptide, J. Clin. Endocrinol. Metab. 56:962–968PubMedCrossRefGoogle Scholar
  69. 69.
    Moulton, B. C., Koenig, B. B., 1986, Hormonal control of phospholipid methylation in uterine luminal epithelial cells during sensitivity to deciduogenic stimuli, Endocrinology 118:244–249PubMedCrossRefGoogle Scholar
  70. 70.
    Hirata, F., Axelrod, J., 1980, Phospholipid methylation and biological signal transmission, Science 209:1082–1090PubMedCrossRefGoogle Scholar
  71. 71.
    Kennedy, T. G.,1983, Embryonic signals and the initiation of blastocyst implantation, Aust. J. Biol. Sci 36:521–543.Google Scholar
  72. 72.
    Kennedy, T. G., 1985, Evidence for the involvement of prostaglandins throughout the decidual cell reaction in the rat, Biol. Reprod. 33:140–146PubMedCrossRefGoogle Scholar
  73. 73.
    Kennedy, T. G., 1983, Prostaglandin E2, adenosine 3’:5’-cyclic monophosphate and changes in endometrial vascular permeability in rat uteri sensitized for the decidual cell reaction, Biol. Reprod. 29:1069–1076PubMedCrossRefGoogle Scholar
  74. 74.
    Johnson, R., Hammer, M., Sheridan, J., Reval, J. P., 1974, Gap junction formation between reaggregating Novikoff hepatoma cells, Proc. Natl. Acad. Sci. U.S.A. 71:4536–4543PubMedCrossRefGoogle Scholar
  75. 75.
    Flagg-Newton, J. L., 1980, The permeability of the cell-to-cell membrane channel and its regulation in mammalian cell junction, In Vitro 16:1043–1048PubMedCrossRefGoogle Scholar
  76. 76.
    Flagg-Newton, J. L., Loewenstein, W. R., 1981, Cell junction and cyclic AMP: II. Modulations of junctional membrane permeability, dependent on serum and cell density, J. Membr. Biol. 63:121–131Google Scholar
  77. 77.
    Flagg-Newton, J. L., Dahl, G., Loewenstein, W. R., 1981, Cell junction and cyclic AMP: I. Upregulation of junctional membrane permeability and junctional membrane particles by administration of cyclic nucleotide or phosphodiesterase inhibitor, J. Membr. Biol. 63:105–121PubMedGoogle Scholar
  78. 78.
    Azarnia, R., Dahl, G., Loewenstein, W. R., 1981, Cell junction and cyclic AMP: III. Promotion of junctional membrane permeability and junctional membrane particles in a junction deficient cell type, J. Membr. Biol. 63:133–146Google Scholar
  79. 79.
    Radu, A., Dahl, G., Loewenstein, W. R., 1982, Hormonal regulation of cell junction per-meability: Upregulation by catecholamine and prostaglandin E1, J. Membr. Biol. 70:239–251Google Scholar
  80. 80.
    Hertzberg, E. L., 1985, Antibody probes in the study of gap junctional communication, Annu. Rev. Physiol. 47:305–318PubMedCrossRefGoogle Scholar
  81. 81.
    Tadvalkar, G., Pinto da Silva, P., 1983, In vitro, rapid assembly of gap junctions is induced by cytoskeletal disrupters, J. Cell Biol. 96:1279–1287PubMedCrossRefGoogle Scholar
  82. 82.
    Zor, U., 1983, Role of cytoskeletal organization in the regulation of adenylate cyclase-cyclic adenosine monophosphate by hormones, Endocrinol. Rev. 4:1–21CrossRefGoogle Scholar
  83. 83.
    Child Health and Human Development, 1981, An Evaluation and Assessment of the State of the Sciences, NIH Publication No. (PHS) 825–2304, National Institutes of Health, BethesdaGoogle Scholar
  84. 84.
    Bengtsson, B., Chow, E. M. H., Marshall, J. M., 1984, Calcium dependency of pregnant rat myometrium: Comparison of circular and longitudinal muscle, Biol. Reprod. 30:869–878PubMedCrossRefGoogle Scholar
  85. 85.
    Leroy, M.-J., Ferre, F., Filliatreau, F. G., Cabrol, D., Breuiller, M., 1986, Cyclic AMP metabolism in the inner and outer layers of human myometrium near term, Acta Physiol. Hung. 67:83–94PubMedGoogle Scholar
  86. 86.
    Csapo, A. I., 1956, Progesterone “block,” Am. J. Anat 98:273–291PubMedCrossRefGoogle Scholar
  87. 87.
    Huszar, G., Roberts, J. M., 1981, Biochemistry and pharmacology of the myometrium and labor: Regulation at the cellular and molecular levels, Am. J. Obstet. Gynecol. 142:225–237Google Scholar
  88. 88.
    Carsten, M. E., Miller, J. D., 1987, A new look at uterine muscle contraction, Am. J. Obstet. Gynecol. 157:1303–1315PubMedGoogle Scholar
  89. 89.
    Garfield, R. E., Sims, S. M., Daniel, E. E., 1977, Gap Junctions: Their presence and necessity in myometrium during parturition, Science 198:958–960.PubMedCrossRefGoogle Scholar
  90. 90.
    Garfield, R. E., Rabideau, S., Challis, J. R. G., and Daniel, E. E., 1979, Hormonal control of gap junctions in sheep myometrium, Biol. Reprod. 21:999–1007PubMedCrossRefGoogle Scholar
  91. 91.
    Garfield, R. E., Daniel, E. E., Dukes, M., and Fitzgerald, J. D., 1982, Changes in gap junctions in myometrium of guinea pig at parturition and abortion, Can. J. Physiol. Pharmacol. 60:335- 341Google Scholar
  92. 92.
    Demianczuk, N., Towell, M. E., Garfield, R. E., 1984, Myometrial electrophysiologic activity and gap junctions in the pregnant rabbit, Am. J. Obstet. Gynecol. 149:485–491PubMedGoogle Scholar
  93. 93.
    Garfield, R. E., Hayashi, R. H., 1981, Appearance of gap junctions in the myometrium of women during labor, Am. J. Obstet. Gynecol. 140:254–260PubMedGoogle Scholar
  94. 94.
    Krishnamurti, C. R., Kitts, D. D., Kitts, W. D., Tompkins, J. G., 1982, Myoelectric changes in the uterus of the sheep around parturition, J. Reprod. Fertil. 64:59–67CrossRefGoogle Scholar
  95. 95.
    Garfield, R. E., Daniel, E. E., 1974, The structural basis of electrical coupling (cell-to-cell contacts) in rat myometrium, Gynecol. Invest. 5:284–300PubMedCrossRefGoogle Scholar
  96. 96.
    Berezin, I., Daniel, E. E., Garfield, R. E., 1982, Ovarian hormones are not necessary for postpartum regression of gap junctions, Can. J. Physiol. Pharmacol. 60:1567–1572PubMedCrossRefGoogle Scholar
  97. 97.
    Garfield, R. E., Sims, S. M., Kannan, M. S., Daniel, E. E., 1978, Possible role of gap junctions in activation of myometrium during parturition, Am. J. Physiol. 235:C168–C179PubMedGoogle Scholar
  98. 98.
    Garfield, R. E., Merrett, D., Grover, A. K., 1980, Gap junction formation and regulation in myometrium, Am. J. Physiol. 239:C217–C228PubMedGoogle Scholar
  99. 99.
    Merk, F. B., Kwan, P. W. L., Leav, I., 1980, Gap junctions in the myometrium of hypo- physectomized estrogen-treated rats, Cell Biol. Int. Rep. 4:287–294PubMedCrossRefGoogle Scholar
  100. 100.
    Burghardt, R. C., Matheson, R. L., Gaddy, D., 1984, Gap junction modulation in rat uterus. I. Effects of estrogen on myometrial and serosal cells, Biol. Reprod. 30:239–248PubMedCrossRefGoogle Scholar
  101. 101.
    Zervos, A. S., Hope, J., Evans, W. H., 1985, Preparation of a gap junction fraction from uteri of pregnant rats: The 28-kD polypeptides of uterus, liver, and heart gap junctions are homologous, J. Cell Biol. 101:1363–1370.Google Scholar
  102. 102.
    Dahl, G., Azarina, R., Werner, R., 1980, De novo construction of cell-to-cell channels, In Vitro 16:1068–1075PubMedCrossRefGoogle Scholar
  103. 103.
    Dahl, G., Werner, R., Azarnia, R. 1983, Studies on the biogenesis of cell-cell channels, Methods Enzymol 98:537–545PubMedCrossRefGoogle Scholar
  104. 104.
    Werner, R., Miller, T., Azarnia, R., Dahl, G., 1985, Translation and functional expression of cell-cell channel mRNA in Xenopus oocytes, J. Membr. Biol. 87:253–268PubMedCrossRefGoogle Scholar
  105. 105.
    Turin, L., Warner, A. E., 1980, Intracellular pH in early Xenopus embryos: Its effect on current flow between blastomeres, J. Physiol. (Lond.) 300:489–504Google Scholar
  106. 106.
    Paul, D. L., 1986, Molecular cloning of cDNA for rat liver gap junction protein, J. Cell Biol. 103:123–134PubMedCrossRefGoogle Scholar
  107. 107.
    Kumar, N. M., Gilula, N. B., 1986, Cloning and characterization of human and rat liver cDNAs coding for a gap junction protein, J. Cell Biol. 103:767–776PubMedCrossRefGoogle Scholar
  108. 108.
    Byer, E. C., Paul, D. L., Goodenough, D. A., 1987, Connexin43: A protein from rat heart homologous to a gap junction protein from liver, J. Cell Biol. 105:2621–2629CrossRefGoogle Scholar
  109. 109.
    Dahl, G., Miller, T., Paul, D., Voellmy, R., Werner, R.. 1987, Expression of functional cell– cell channels from cloned rat liver gap junction complementary DNA, Science 236:1290–1293PubMedCrossRefGoogle Scholar
  110. 110.
    Fuchs, A. R., 1978, Hormonal control of myometrial function during pregnancy and parturition, Acta Endocrinol (Kbh.) [Suppl.] 221:1–70Google Scholar
  111. 111.
    Frank, R. T., Bonham, C., Gustavson, R. G., 1925, A new method of assaying the potency of female sex hormone based upon its effect on spontaneous contraction of the uterus of the white rat, Am. J. Physiol. 74:395–399Google Scholar
  112. 112.
    Reynolds, S. R. M., Allen, W. M., 1932, The effect of progestin-containing extracts of corpora lutea on uterine motility in the unanesthetized rabbit, with observations onpseudopregnancy, Am. J. Physiol. 102:39–55Google Scholar
  113. 113.
    Bedford, C. A., Challis, J. R. G., Harrison, F. A., Heup, R. B., 1972, The role of estrogen and progesterone in the onset of parturition in various species, J. Reprod. Fertil. [Suppl.] 16:1–23Google Scholar
  114. 114.
    Csapo, A. I., 1975, The “see-saw” theory of the regulatory mechanism of pregnancy, Am. J. Obstet. Gynecol. 121:578–581Google Scholar
  115. 115.
    Bergman, R. A., 1968, Uterine smooth muscle fibers in castrate and estrogen-treated rats, J. Cell Biol. 36:639–648PubMedCrossRefGoogle Scholar
  116. 116.
    Daniel, E. E., Daniel, V. P., Duchon, G., Garfield, R. E., Nichols, M., Malhotra, S. K., and Oki, M., 1976, Is the nexus necessary for cell-to-cell coupling of smooth muscle? J. Membr. Biol. 28:207–239PubMedCrossRefGoogle Scholar
  117. 117.
    Dahl, G., Berger, W., 1978, Nexus formation in the myometrium during parturition and induced by estrogen, Cell Biol. Int. Rep. 2:381–387PubMedCrossRefGoogle Scholar
  118. 118.
    Garfield, R. E., Puri, C. P., Csapo, A. I., 1982, Endocrine, structural, and functional changes in the uterus during premature labor, Am. J. Obstet. Gynecol. 142:21–27PubMedGoogle Scholar
  119. 119.
    MacKenzie, L. W., Garfield, R. E., 1985, Effects of 17β-estradiol on myometrial gap junctions and pregnancy in the rat, Can. J. Physiol. Pharmacol. 64:462–466CrossRefGoogle Scholar
  120. 120.
    Burghardt, R. C., Mitchell, P. A., Kurten, R. C., 1984, Gap junction modulation in rat uterus. II. Effects of antiestrogens on myometrial and serosal cells, Biol. Reprod. 30:249–255PubMedCrossRefGoogle Scholar
  121. 121.
    Burghardt, R. C., Gaddy-Kurten, D., Burghardt, R. L., Kurten, R. C., and Mitchell, P. A., 1987, Gap junction modulation in rat uterus. III. Structurea-ctivity relationships of estrogen receptor- binding ligands on myometrial and serosal cells, Biol. Reprod. 36:741–751PubMedCrossRefGoogle Scholar
  122. 122.
    Markaverich, B. M., Clark, J. H., 1979, Two binding sites for estradiol in rat uterine nuclei: Relationship to uterotropic response, Endocrinology 105:1458–1462PubMedCrossRefGoogle Scholar
  123. 123.
    Clark, J. H., and Markaverich, B. M., 1984, The agonistic and antagonistic actions of estriol, J. Steroid Biochem. 20:1005–1013PubMedCrossRefGoogle Scholar
  124. 124.
    Korach, K. S., Fox-Davies, C. Quarmby, V. E., and Swaisgood, M. H., 1985, Diethylstilbestrol metabolites and analogs. Biochemical probes for differential stimulation of uterine estrogen responses, J. Biol. Chem. 260:15420–15426PubMedGoogle Scholar
  125. 125.
    Garfield, R. E., Kannan, M. S., Daniel, E. E., 1980, Gap junction formation in myometrium: Control by estrogens, progesterone, and prostaglandins, Am. J. Physiol. 238:C81–C89PubMedGoogle Scholar
  126. 126.
    MacKenzie, L. W., Puri, C. P., Garfield, R. E., 1983, Effect of estradiol-17β and prostaglandins on rat myometrial gap junctions, Prostaglandins 26:925–941PubMedCrossRefGoogle Scholar
  127. 127.
    MacKenzie, L. W., Garfield, R. E., 1985, Hormonal control of gap junctions in the myo-metrium, Am. J. Physiol. 248:C296–C308PubMedGoogle Scholar
  128. 128.
    Wathes, D. C., Porter, D. G., 1982, Effect of uterine distention and oestrogen treatment on gap junction formation in the myometrium of the rat, J. Reprod. Fertil. 65:497–505PubMedCrossRefGoogle Scholar
  129. 129.
    Ikeda, M., Shibata, Y., Yamamoto, T., 1987, Rapid formation of myometrial gap junctions during parturition in the unilaterally implanted rat uterus, Cell Tissue Res 248:297–303PubMedCrossRefGoogle Scholar
  130. 130.
    Kloeck, F. K., Jung, H., 1973, In vitrorelease of prostaglandins from the human myometrium under the influence of stretching, Am. J. Obstet. Gynecol. 115:1066–1069Google Scholar
  131. 131.
    Puri, C. P., Garfield, R. E., 1982, Changes in hormone levels and gap junctions in the rat uterus during pregnancy and parturition, Biol. Reprod. 27:967–975PubMedCrossRefGoogle Scholar
  132. 132.
    Verhoeff, A., Garfield, R. E., Ramondt, J., Wallenburg, H. C. S., 1985, Electrical and mechanical uterine activity and gap junctions in peripartal sheep, Am. J. Obstet. Gynecol. 153:447–454Google Scholar
  133. 133.
    Liggins, G. C., Fairclough, R. J., Grieves, S. A., Kendall, J. Z., and Knox, B. S., 1973, The mechanism of parturition in the ewe, Recent Prog. Horm. Res. 29:111–137PubMedGoogle Scholar
  134. 134.
    Kitts, D. D., Anderson, G. B., Bon Durant, R. H., Kindahl, H., and Stabenfeldt, G. H., 1985, Studies on the endocrinology of parturition: Steroidogenesis in coexisting genetically dissimilar ovine fetuses, concomitant with the temporal patterns of maternal C18 and C19 steroids and prostaglandin F2α release, Biol. Reprod. 33:67–78PubMedCrossRefGoogle Scholar
  135. 135.
    Kendall, J. Z., Challis, J. R. G., Hart, I. C., Jones, C. T., Mitchell, M. D., Ritchie, J. W. K., Robinson, J. S., and Thorburn, G. D., 1977, Steroid and prostaglandin concentrations in the plasma of pregnant ewes during infusion of adrenocorticotrophin or dexamethasone to intact or hypophysectomized foetuses, J. Endocrinol. 75:59–71PubMedCrossRefGoogle Scholar
  136. 136.
    Alexandrova, M., and Soloff, M. S., 1980, Oxytocin receptors and parturition. I. Control of oxytocin receptor concentration in the rat myometrium at term, Endocrinology 106:730–735PubMedCrossRefGoogle Scholar
  137. 137.
    Saito, Y., Sakamoto, H., MacLusky, N. J., and Naftolin, F., 1985, Gap junctions and myometrial steroid hormone receptors in pregnant and postpartum rats: A possible cellular basis for the progesterone withdrawal hypothesis, Am. J. Obstet. Gynecol. 151:805–812PubMedGoogle Scholar
  138. 138.
    Giannopoulos, G., and Tulchinsky, D., 1979, Cytoplasmic and nuclear progestin receptors in human myometrium during the menstrual cycle and in pregnancy at term, J. Clin. Endocrinol. Metab. 49:100–106PubMedCrossRefGoogle Scholar
  139. 139.
    Casey, M. L., and MacDonald, P. C., 1984, Endocrinology of preterm birth, Clin. Obstet. Gynecol. 27:562–571PubMedCrossRefGoogle Scholar
  140. 140.
    Garfield, R. E., and Baulieu, E. E., 1987, The antiprogesterone steroid RU 486: A short pharmacological and clinical review, with emphasis on the interruption of pregnancy, Baillieres Clin. Endocrinol. Metab. 1:207–221PubMedCrossRefGoogle Scholar
  141. 141.
    Baulieu, E. E., and Ulmann, A., 1986, Antiprogesterone activity of RU 486 and its contragestive and other applications, Hum. Reprod. 1:107–110PubMedGoogle Scholar
  142. 142.
    Williams, K. I., 1984, Prostaglandin synthesis and uterine contractility, in: Uterine Contractility( S. Bottari, J. P. Thomas, A. Vokaer, and R. Vokaer, eds.), Masson, New York, pp. 282–288Google Scholar
  143. 143.
    Ham, E. A., Cirillo, V. J., Zanetti, M. E., and Kuehl, F. A., Jr., 1975, Estrogen directed synthesis of specific prostaglandins in uterus, Proc. Natl. Acad. Sci. U.S.A. 72:1420–1424PubMedCrossRefGoogle Scholar
  144. 144.
    Thorburn, G. D., Challis, J. R. G., 1979, Endocrine control of parturition, Physiol. Rev. 59:863–918Google Scholar
  145. 145.
    Taylor, M. J., Webb, R., Mitchell, M. D., Robinson, J. S., 1982, Effect of progesterone withdrawal in sheep during late pregnancy, J. Endocrinol. 92:85–93PubMedCrossRefGoogle Scholar
  146. 146.
    Hahn, D. W., McGuire, J. L., Carraher, R. P., Demers, L. M., 1985, Influence of ovarian steroids on prostaglandin- and leukotriene-induced uterine contractions, Am. J. Obstet. Gynecol. 153:87–91PubMedGoogle Scholar
  147. 147.
    Revel, J. P., Yancey, S. B., Meyer, D. J., and Nicholson, B., 1980, Cell junctions and intercellular communication, In Vitro 16:1010–1017.PubMedCrossRefGoogle Scholar
  148. 148.
    Dahl, G., Asarnia, R., Werner, R., 1981, Induction of cell-cell channel formation by mRNA, Nature 303:435–439Google Scholar
  149. 149.
    Fallon, R. F., Goodenough, D. A., 1981, Five hour half-life of mouse liver gap junction protein, J. Cell Biol 90:521–526Google Scholar
  150. 150.
    Traub, O., Druge, P. M., Willecke, K., 1983, Degradation and resynthesis of gap junction protein in plasma membranes of regenerating liver after partial hepatectomy or cholestasis, Proc. Natl. Acad. Sci. U.S.A. 80:755–759PubMedCrossRefGoogle Scholar
  151. 151.
    Greipp, E. B., and Revel, J. P., 1977, Gap junctions in development, in: Intercellular Communication( W. C. DeMello, ed.), Plenum Press, New York, pp. 1–32Google Scholar
  152. 152.
    Larsen, W. J., Tung, H. N., 1978, Origin and fate of cytoplasmic gap junctional vesicles in rabbit granulosa cells, Tissue Cell 10:585–598PubMedGoogle Scholar
  153. 153.
    Garfield, R. E., 1985, Cell-to-cell communication in smooth muscle, in: Calcium and Contractility:Smooth Muscle ( A. K. Grover and E. E. Daniel, eds.), Humana Press, Clifton Manor, NJ, pp. 143–173Google Scholar
  154. 154.
    Burghardt, R. C., Anderson, E., 1979, Hormonal modulation of ovarian interstitial cells with particular reference to gap junctions, J. Cell Biol. 81:104–114PubMedCrossRefGoogle Scholar
  155. 155.
    Burghardt, R. C., Anderson, E., 1981, Hormonal modulation of gap junctions in rat ovarian follicles, Cell Tissue Res 214:181–193PubMedCrossRefGoogle Scholar
  156. 156.
    Burghardt, R. C., Matheson, R. L., 1982, Gap junction amplification in rat ovarian granulosa cells. I. A direct response to follicle stimulating hormone, Dev. Biol. 94:206–215PubMedCrossRefGoogle Scholar
  157. 157.
    Yee, S. B., Revel, J. P., 1978, Loss and reappearance of gap junctions in regenerating livers, J. Cell Biol. 78:554–564PubMedCrossRefGoogle Scholar
  158. 158.
    Lane, N. J., Swales, L. S., 1980, Dispersal of junctional particles, not internalization, during the in vivo disappearance of gap junctions, Cell 19:579–586PubMedCrossRefGoogle Scholar
  159. 159.
    Lee, W. M., Cran, D. G., and Lane, N. J., 1982, Carbon dioxide induced disassembly of gap junctional plaques, J. Cell Sci. 57:215–228PubMedGoogle Scholar
  160. 160.
    Spray, D. C., Harris, A. L., and Bennett, M. V. L., 1982, Comparison of pH and calcium dependence of gap junctional conductance, in: Intracellular pH: Its Measurement, Regulation, and Utilization in Cellular Functions, Alan R. Liss, New York, pp. 445–461Google Scholar
  161. 161.
    Spray, D. C., White, R. L., Mazet, F., and Bennett, M. V. L., 1985, Regulation of gap junctional conductance, Am. J. Physiol. 248:H753–H764PubMedGoogle Scholar
  162. 162.
    Spray, D. C., Stern, J. H., Harris, A. L., and Bennett, M. V. L., 1982, Gap junctional conduc-tance: Comparison of sensitivities to H and Ca ions, Proc. Natl. Acad. Sci. U.S.A. 79:441–445PubMedCrossRefGoogle Scholar
  163. 163.
    in’t Veld, P., Schuit, F., and Pipeleers, D., 1985, Gap junctions between pancreatic B-cells are modulated by cyclic AMP, Eur. J. Cell Biol. 36:269–276Google Scholar
  164. 164.
    Azarnia, R., Russell, T. R., 1985, Cyclic AMP effects on cell-to-cell junctional membrane permeability during adipocyte differentiation of 3T3-L1 fibroblasts, J. Cell Biol. 100:265–269PubMedCrossRefGoogle Scholar
  165. 165.
    De Mello, W. C., 1983, The role of cAMP and Ca on the modulation of junctional conductance: An integrated hypothesis, Cell Biol. Int. Rep. 7:1033–1040PubMedCrossRefGoogle Scholar
  166. 166.
    Saez, J. C., Spray, D. C., Nairn, A. C., Hertzberg, E., Greengard, P., and Bennett, M. V. L., 1986, cAMP increases junctional conductance and stimulates phosphorylation of the 27-kDa principal gap junction polypeptide, Proc. Natl. Acad. Sci. U.S.A. 83:2473–2477.Google Scholar
  167. 167.
    Traub, O., Look, J., Paul, D., Willecke, K., 1987, Cyclic adenosine monophosphate stimulates biosynthesis and phosphorylation of the 26-kDa gap junction protein in cultured mouse hepatocytes, Eur. J. Cell Biol. 43:48–54PubMedGoogle Scholar
  168. 168.
    Enomoto, T., Sasaki, Y., Shiba, Y., Kanno, Y., Yamasaki, H., 1981, Tumor promotors cause a rapid and reversible inhibition of the formation and maintenance of electrical cell coupling in culture, Proc. Natl Acad. Sci. U.S.A. 78:5628–5632PubMedCrossRefGoogle Scholar
  169. 169.
    Kanno, Y., 1985, Modulation of cell communication and carcinogenesis, Jpn. J. Physiol 35:693–707PubMedCrossRefGoogle Scholar
  170. 170.
    Yada, T., Rose, B., Loewenstein, W. R., 1985, Diacylglycerol downregulates junctional membrane permeability. TMB-8 blocks this effect, J. Membr. Biol. 88:217–232Google Scholar
  171. 171.
    Takeda, A., Hashimoto, E., Yamamura, H., and Shimazu, T., 1987, Phosphorylation of liver gap junction protein by protein kinase C, FEBS Lett 210:169–172PubMedCrossRefGoogle Scholar
  172. 172.
    Atkinson, M. M., Menko, A. S., Johnson, R. G., Sheppard, J. R., and Sheridan, J. D., 1981, Rapid and reversible reduction of junctional permeability in cells infected with a temperature- sensitive mutant of avian sarcoma virus, J. Cell Biol. 91:573–578PubMedCrossRefGoogle Scholar
  173. 173.
    Azarnia, R., Loewenstein, W. R., 1984, Intercellular communication and the control of growth: X. Alteration of junctional permeability by the srcgene. A study with temperature- sensitive mutant Rous sarcoma virus, J. Membr. Biol. 82:191–205Google Scholar
  174. 174.
    Azarnia, R., Loewenstein, W. R., 1984, Intercellular communication and the control of growth: XI. Alteration of junctional permeability by the src gene in a revertant cell with normal cytoskeleton, J. Membr. Biol. 82:207–212Google Scholar
  175. 175.
    Sugimoto, Y., Whitman, M., Cantley, L. C., and Erikson, R. L., 1984, Evidence that Rous sarcoma virus transforming gene product phosphorylates phosphotidylinositol and diacylglycerol, Proc. Natl. Acad. Sci. U.S.A. 81:2117–2121PubMedCrossRefGoogle Scholar
  176. 176.
    Berridge, M. J., 1987, Inositol trisphosphate and diacylglycerol: Two interacting second mes-sengers, Annu. Rev. Biochem. 56:159–193PubMedCrossRefGoogle Scholar
  177. 177.
    Atkinson, M. M., Sheridan, J. D., 1985, Reduced junctional permeability in cells transformed by different viral oncogenes, in: Gap Junctions( M. V. L. Bennett and D. C. Spray, eds.), Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 205–213Google Scholar
  178. 178.
    Cole, W. C., Garfield, R. E., and Kirkaldy, J. S., 1985, Gap junctions and direct intercellular communication between rat uterine smooth muscle cells, Am. J. Physiol. 18:C20–C31Google Scholar
  179. 179.
    Cole, W. C., Garfield, R. E., 1985, Alterations in coupling in uterine smooth muscle, in: Gap Junctions( M. V. L. Bennett and D. C. Spray, eds.), Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 215–230Google Scholar
  180. 180.
    Cole, W. C., Garfield, R. E., 1986, Evidence for the physiological regulation of myometrial gap junction permeability, Am. J. Physiol. 251:C411–C420PubMedGoogle Scholar
  181. 181.
    Huszar, G., 1986, Cellular regulation of myometrial contractility and essentials of tocolytic therapy, in: The Physiology and Biochemistry of the Uterus in Pregnancy and Labor( G. Huszar, ed.), CRC press, Boca Raton, FL, pp. 107–126Google Scholar
  182. 182.
    Nishikori, K., Weisbrodt, N. W., Sherwood, O. D., and Sanborn, B. M., 1983, Effects of relaxin on rat uterine myosin light chain kinase activity and myosin light chain phosphorylation, J. Biol. Chem. 258:2468–2474PubMedGoogle Scholar
  183. 183.
    Scheid, C. R., Honeyman, T. W., Fay, F. S., 1979, Mechanism of β-adrenergic relaxation of smooth muscle, Nature 277:32–36PubMedCrossRefGoogle Scholar
  184. 184.
    Darnell, J. E., Lodish, H. F., Baltimore, D., 1986, Molecular Cell Biology, W. H. Freeman, New YorkGoogle Scholar

Copyright information

© Plenum Press, New York 1990

Authors and Affiliations

  • Robert C. Burghardt
    • 1
  • William H. Fletcher
    • 2
  1. 1.Department of Veterinary Anatomy, College of Veterinary MedicineTexas A&M UniversityCollege StationUSA
  2. 2.Department of Anatomy, School of MedicineLoma Linda University and Jerry L. Pettis Memorial Veterans Medical CenterLoma LindaUSA

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