Summary
Incubation of the salivary glands of the larvae ofDrosophila hydei in a control medium containing 2×10−3 m cyclic adenosine monophosphate (cAMP) induces a considerable increase in passive electrical cel communication. This is caused by a decrease in permeabilty of the nonjunctional membrane part, together with an increase of the permeability of the low-resistance junctions. Similar changes in intercellular communication in the salivary gland ofDrosophila hydei were seen in a majority of experiments in which 10−3 m dibutyryl cycli adenosine monophosphate (dBcAMP), 5×10−3 m theophylline or ecdysterone (100 μg/ml) were added to the control medium. Hyperpolarization of the gland cells can be observed concomitant with the increase in communication. A hypothesis is discussed for a possible molecular regulation of passive electrical cell communication in which the intracellular cAMP level plays a significant part.
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Azarnia, R., Michalke, W., Loewenstein, W. R. 1972. Intercelular communication and tissue growth. VI. Failure of exchange of endogenous molecules between cancer cells with defective junctions and noncancerous cells.J. Membrane Biol. 10:247
Bär, K. P., Hechter, O. 1969. Adenyl cyclase and hormone action. III. Calcium requirement for ACTH stimulation of adenyl cyclase.Biochem. Biophys. Res. Commun. 35:681
Borle, A. B. 1974. Cyclic AMP stimulation of calcium efflux from kidney, liver, and heart mitochondria.J. Membrane Biol. 16:221
Bradham, L. S., Holt, D. A., Sims, M. 1970. The effect of Ca2+ on the adenyl cyclase of calf brain.Biochim. Biophys. Acta 201:250
Burger, M. M., Bombik, B. M., Breckenridge, B. McL., Sheppard, J. R. 1972. Growth control and cyclic alterations of cyclic AMP in the cell cycle.Nature, New Biol. 239:161
Bürk, R. R. 1968. Reduced adenyl cyclase activity in a polyoma virus transformed cell line.Nature 219:1272
Bürk, R. P., Pitts, J. D., Subak-Sharpe, J. H. 1968. Exchange between hamster cells in culture.Exp. Cell Res. 53:297
Chiappe de Cingolani, G. E., Van den Bosch, H., Van Deenen, L. L. M. 1972. Phospholipase A and lysophospholipase activities in isolated fat cells: Effect of cyclic 3′5′-AMP.Biochim. Biophys. Acta 260:387
Cox, R. P., Kraus, M. R., Balis, M. E., Dancis, J. 1972. Communication between normal and enzyme deficient cells in tissue culture.Exp. Cell Res. 74:251
Frank, W. 1972. Cyclic 3′∶5′ AMP and cell proliferation in cultures of embryonic rat cells.Exp. Cell Res. 71:238
Friedman, N., Dambach, G. 1973. Relationship between cyclic AMP induced membrane potential changes and gluconeogenesis.Abstr. Ninth Int. Congr. Biochem. 8c2
Friedman, N., Park, C. R. 1968. Early effects of 3′,5′ adenosine monophosphate on the fluxes of calcium and potassium in the perfused liver of normal and adrenolectomized rats.Proc. Nat. Acad. Sci. 61:504
Froehlich, J. E., Rachmeler, M. 1972. Effect of adenosine 3′,5′ cyclic monophosphate on cell proliferation.J. Cell Biol. 55:19
Furshpan, E. J., Potter, D. D. 1968. Low-resistance junctions between cells in embryos and tissue culture.Curr. Top. Devel. Biol. 3:95
Gilula, N. B., Reeves, O. R., Steinbach, A. 1972. Metabolic coupling, ionic coupling and cell contacts.Nature 235:262
Hax, W. M. A., Demel, R. A., Spies, F., Vossenberg, J. B. J., Linnemans, W. A. M. 1974. Increased phospholipase A activity and formation of communicative contacts betweenAcanthamoeba castellanii cells. Effect of 3′,5′-cyclic AMP.Exp. Cell Res. (To be published)
Hax, W. M. A., van Venrooij, G. E. P. M., Denier van der Gon, J. J., Elbers, P. F. 1973. Cell communication induced by lysolecithin.J. Membrane Biol. 13:61
Honda, F., Imamura, H. 1968. Inhibition of cyclic 3′,5′-nucleotide phosphodiesterase by phenothiazine and reserpine derivatives.Biochim. Biophys. Acta 161:267
Hsie, A. W., Puck, T. T. 1971. Morphological transformation of Chinese hamster cells by dibutyryl adenosine cyclic 3′,5′-monophosphate and testosterone.Proc. Nat. Acad. Sci. 68:358
Imre, S. 1972. The effect of cAMP on phospholipid metabolism.Acta Biochim. Biophys. Acad. Sci. Hung. 7:247
Kelly, L. A., Koritz, S. B. 1971. Bovine adrenal cortical adenyl cyclase and its stimulation by adrenocorticotropic hormone and NaF.Biochim. Biophys. Acta 237:141
Leenders, H. J., Wullems, G. J., Berendes, H. D. 1970. Competitive interaction of adenosine 3′,5′-monophosphate on gene activation by ecdysterone.Exp. Cell Res. 63:159
Loewentein, W. R. 1966. Permeability of membrane junctions.Ann. N.Y. Acad. Sci. 137:441
Loewenstein, W. R. 1967a. Cell surface membranes in close contact. Role of calcium and magnesium ions.J. Colloid Interface Sci. 2534
Loewenstein, W. R. 1967b. On the genesis of cellular communication.Devel. Biol. 15:503
Loewenstein, W. R. 1968. Emergence of order in tissues and organs. Communication through cell junctions. Implications in growth control and differentiation.Devel. Biol. 19 (suppl. 2): 151
Loewenstein, W. R., Nakas, M., Socolar, S. J. 1967. Junctional membrane uncoupling. Permeability transformations at a cell membrane junction.J. Gen. Physiol. 50:1865
Otten, J., Johnson, G. S., Pastan, I. 1971. Cyclic AMP levels in fibroblasts: Relationship to growth rate and contact inhibition of growth.Biochem. Biophys. Res. Commun. 44:1192
Peery, C. V., Johnson, G. S., Pastan, I. 1971. Adenyl cyclase in normal and transformed fibroblasts in tissue culture. Activation by prostaglandines.J. Biol. Chem. 18:5785
Poels, C. L. M. 1970. Time sequence in the expression of various developmental characters induced by ecdysterone inDrosophila hydei.Devel. Biol. 23:210
Poels, C. L. M. 1972. Mucopolysaccharide secretion fromDrosophila salivary gland cells as a consequence of hormone induced gene activity.Cell Diff. 1:63
Politoff, A. L., Socolar, S. J., Loewenstein, W. R. 1969. Permeability of a cell membrane junction. Dependence on energy metabolism.J. Gen. Physiol. 53:498
Rasmussen, H. 1970. Cell communication, calcium ion, and cyclic adenosine monophosphate.Science 170:404
Rensing, L., Hardeland, R. 1972. Effect of adenosine 3′,5′-cyclic monophosphate on membrane potential, nuclear volume and puff size inDrosophila salivary gland in vitro.Exp. Cell Res. 73:311
Robison, G. A., Butcher, R. W., Sutherland, E. W. 1971. Cyclic AMP. Academic Press, New York
Rose, B. 1970. Junctional membrane permeability: Restoration by repolarizing current.Science 169:607
Rose, B., Loewenstein, W. R. 1969. Depression of junctional membrane permeability by substitution of lithium for extracellular sodium.Biochim. Biophys. Acta 173:146
Rose, B., Loewenstein, W. R. 1971. Junctional membrane permeability. Depression by substitution of Lif for extracellular Na, and by long-term lack of Ca and Mg; restoration by cell repolarization.J. Membrane Biol. 5:20
Rubin, R. P., Carchman, R. A., Jaanus, S. B. 1972. Role of calcium and adenosine cyclic 3′,5′ phosphate in action of adrenocorticotropin.Nature, New Biol. 240:150
Seifert, W., Paul, D. 1972. Levels of cyclic AMP in sparse and dense cultures of growing and quiescent 3T3 cells.Nature, New Biol. 240:281
Sheppard, J. R. 1971. Restoration of contact-inhibited growth to transformed cells by dibutyryl adenosine 3′,5′-cyclic monophosphate.Proc. Nat. Acad. Sci. 68:1316
Sheppard, J. R. 1972. Difference in the cyclic adenosine 3′,5′-monophosphate levels in normal and transformed cells.Nature, New Biol.236:14
Smets, L. A. 1972. Contact-inhibition of transformed cells incompletely restored by dibutyryl cyclic AMP.Nature, New Biol. 239:123
Socolar, S. J., Politoff, A. L. 1971. Uncoupling cell junctions in a glandular epithelium by depolarizing current.Science 172:492
Sutherland, E. W. 1970. On the biological role of cAMP.J. Amer. Med. Soc. 2141281
Teel, R. W., Hall, R. G. 1973. Effects of dibutyryl cyclic AMP on the restoration of contact inhibition in tumor cells and its relationship to cell density and the cell cycle.Exp. Cell Res. 76:390
Venrooij, G. E. P. M. van, Hax, W. M. A., Dantzig, G. F. van, Prijs, V., Denier van der Gon, J. J. 1974. Model approaches for the evaluation of electrical cell coupling in the salivary gland of the larva ofDrosophila hydei. The influence of lysolecithin on the electrical coupling.J. Membrane Biol. 19:229
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Hax, W.M.A., van Venrooij, G.E.P.M. & Vossenberg, J.B.J. Cell communication: A cyclic-AMP mediated phenomenon. J. Membrain Biol. 19, 253–266 (1974). https://doi.org/10.1007/BF01869981
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DOI: https://doi.org/10.1007/BF01869981