Summary
Electrical uncoupling of crayfish septate axons with acidification has been shown to cause a substantial increase in [Ca2+]i which closely matches in percent the increase in junctional resistance. To determine the origin of [Ca2+]i increase, septate axons have been exposed either to drugs that influence Ca2+ release from internal stores, caffeine and ryanodine, or to treatments that affect Ca2+ entry. A large increase in junctional resistance and [Ca2+]i maxima above controls resulted from addition of caffeine (10–30mm) to acetate solutions, while a substantial decrease in both parameters was observed when exposure to acetate-caffeine was preceded by caffeine pretreatment. In contrast, ryanodine (1–10 μm) always caused a significant decrease in junctional resistance and [Ca2+]i maxima when applied either together with acetate or both before and with acetate. Calcium channel blockers such as La3+, Cd2+ and nisoldipine had no effect, while an increase in the [Ca2+] of acetate solutions either decreased junctional resistance and [Ca2+]i maxima or had no effect. The data suggest that cytoplasmic acidification causes an increase in [Ca2+]i by releasing Ca2+ from caffeine and ryanodine-sensitive Ca2+ stores. The increase in [Ca2+]i results in a decrease in gap junction conductance.
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References
Alvarez-Leefmans, F.J., Rink, T.J., Tsien, R.Y. 1981. Free calcium ions in neurons ofHelix aspersa measured with ionselective microelectrodes.J. Physiol. (London) 315:531–548
Ammann, D., Oesch, U., Bührer, T., Simon, W. 1987. Design of ionophores for ion-selective microsensors.Can. J. Physiol. Pharmacol. 65:879–884
Bennett, M.V.L. 1966. Physiology of electrotonic junctions.Ann. N.Y. Acad. Sci. 37:509–539
Bennett, M.V.L., Verselis, R.L., White, R.L., Spray, D.C. 1988. Gap junctional conductance: Gating.In: Gap Junctions. E.L. Hertzberg and R.G. Johnson, editors. pp. 207–304. Alan R. Liss, New York
Butcher, R.W., Sutherland, E.W. 1962. Adenosine 3′, 5′-phosphate in biological materials: I. Purification and properties of cyclic 3′,5′-nucleotide phosphodiesterase and use of this enzyme to characterize adenosine 3′,5′-phosphate in human urine.J. Biol. Chem. 237:1244–1250
Chapman, R.A., Miller, D.J. 1974. The effects of caffeine on the contraction of the frog heart.J. Physiol. (London) 242:589–613
Connett, R.J. 1978. Association of increased pH i with calcium ion release in skeletal muscle.Am. J. Physiol. 234:C110-C114
Delay, M.B., Ribalet, B., Vergara, J. 1986. Caffeine potentiation of calcium release in frog skeletal muscle fibers.J. Physiol. (London) 375:535–559
Fairhurst, A.S., Hasselbach, W. 1970. Calcium efflux from a heavy sarcotubular fraction. Effect of ryanodine, caffeine and magnesium.Eur. J. Biochem. 13:504–509
Fill, M., Coronado, R. 1988. Ryanodine receptor channel of sarcolplasmic reticulum.Trends Neurosci. 11:453–457
Imagawa, T., Smith, J.S., Coronado, R., Campbell, K.P. 1987. Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum in the Ca2+-permeable pore of the calcium release channel.J. Biol. Chem. 262:16636–16643
Johnston, M.F., Ramon, F. 1981. Electronic coupling in internally perfused crayfish segmented axons.J. Physiol. (London) 317:509–518
Lea, T.J., Ashley, C.C. 1981. Carbon dioxide or bicarbonate ions release Ca2+ from internal stores in crustacean myofibrillar bundles.J. Membrane Biol. 61:115–125
Lipscombe, D., Madison, D.V., Poenie, M., Reuter, H., Tsien, R.Y., Tsien, R.W. 1988. Spatial distribution of calcium channels and cytosolic calcium transients in growth cones and cell bodies of sympathetic neurons.Proc. Natl. USA 85:2398–2402
Loewenstein, W.R. 1966. Permeability of membrane junctions.Ann. N.Y. Acad. Sci. 137:441–472
Loewenstein, W.R. 1981. Junctional intercellular communication: The cell-to-cell membrane channel.Physiol. Rev. 61:829–913
McGrew, S.G., Wolleben, C., Siegl, P., Inui, M., Fleischer, S. 1989. Positive cooperativity of ryanodine binding to the calcium release channel of sarcoplasmic reticulum from heart and skeletal muscle.Biochemistry 28:1686–1691
Meissner, G., Henderson, J.S. 1987. Rapid calcium release from cardiac sarcoplasmic reticulum vesicles is dependent on Ca++ and is modulated by Mg++, adenine nucleotide and calmodulin.J. Biol. Chem. 262:3065–3073
Meldolesi, J., Volpe, P., Pozaan, T. 1988. The intracellular distribution of calcium.Trends Neurosci. 11:449–452
Nagasaki, K., Kasai, M. 1983. Fast release of calcium from sarcoplasmic reticulum vesicles monitored by chloretetracycline fluorescence.J. Biochem. (Tokyo) 94:1101–1109
Peracchia, C. 1973. Low resistance junctions in crayfish: 1. Two arrays of globules in junctional membranes.J. Cell Biol. 57:54–65
Peracchia, C. 1980. Structural correlates of gap junction permeation.Int. Rev. Cytol. 66:81–146
Peracchia, C. 1987a. Permeability and regulation of gap junction channels in cells and in artificial lipid bilayers.In: Cell-to-Cell Communications. W.C. DeMello, editor. pp. 65–102. Plenum, New York
Peracchia, C. 1987b. Calmodulin-like proteins and communicating junctions-electrical uncoupling of crayfish septate axons is inhibited by the calmodulin inhibitor W7 and is not affected by cyclic nucleotides.Pfluegers Arch. 408:379–385
Peracchia, C. 1988. The calmodulin hypothesis for gap junction regulation six years later.In: Gap Junctions. E.L. Hertzberg and R.G. Johnson, editors. pp. 267–282. Alan R. Liss, New York
Peracchia, C. 1989. Participation of caffeine-and ryanodine-sensitive Ca2+-stores in low pH i -induced uncoupling of crayfish axons.Soc. Neurosci. Abstr. 15:1302
Peracchia, C. 1990. Increase in gap junction resistance with acidification in crayfish septate axons is closely related to changes in intracellular calcium but not hydrogen ion concentration.J. Membrane Biol. 113:75–92
Peracchia, C., Dulhunty, A.F. 1976. Low resistance junctions in crayfish. Structural changes with functional uncoupling.J. Cell. Biol. 70:419–439
Peracchia, C., Robertson, J.D., 1971. Increase in osmiophilia of axonal membranes of crayfish as a result of electrical stimulation, asphyxia, or treatment with reducing agents.J. Cell. Biol. 51:223–239
Ramon, F., Rivera, A. 1987. Gap junction channel modulation. A physiological viewpoint.Prog. Biophys. 48:127–153
Rose, B., Loewenstein, W.R. 1976. Permeability of a cell junction and the local cytoplasmic free ionized calcium concentration: A study with acquorin.J. Membrane Biol. 28:87–119
Rose, B., Rick, R. 1978. Intracellular pH, intracellular free Ca, and junctional cell-cell coupling.J. Membrane Biol. 44:377–415
Rousseau, E., Meissner, G. 1989. Single cardiac sarcoplasmic reticulum Ca2+-release channel: Activation by caffeine.Am. J. Physiol. 256:H328-H333
Rousseau, E., Smith, J.S., Meissner, G. 1987. Ryanodine modifies conductance and gating behavior of single Ca++ release channel.Am. J. Physiol. 253:C364-C368
Schefer, U., Ammann, D., Pretsch, E., Oesch, U., Simon, W. 1986. Neutral carrier based Ca++-sensitive electrode with detection limit in the subnanomolar range.Anal. Chem. 58:2282–2285
Smith, D.S., Imagawa, T., Ma, J., Fill, M., Campbell, K.P., Coronado, R. 1988. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum.J. Gen. Physiol. 92:1–26
Spray, D.C., Harris, A.L., Bennett, M.V.L. 1981. Gap junctional conductance is a simple and sensitive function of intracellular pH.Science 211:712–715
Stephenson, E.W. 1981. Activation of fast skeletal muscle: Contribution of studies on skinned fibers.Am. J. Physiol. 240:C1-C19
Sutko, J.L., Willerson, J.T., Templeton, G.H., Besch, H.R., Jr. 1979. Ryanodine: Its alteration of cat papillary muscle contratile state and responsiveness to inotropic interventions and a suggested mechanism of action.J. Pharmacol. Exp. Ther. 209:37–47
Turin, L., Warner, A.E. 1977. Carbon dioxide reversibly abolishes ionic communication between cells of early embryo.Nature (London) 270:56–57
Turin, L., Warner, A.E. 1980. Intracellular pH in earlyXenopus embryos: Its effect on current flow between blastomers.J. Physiol. (London) 300:489–504
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Peracchia, C. Effects of caffeine and raynodine on low pHi-induced changes in gap junction conductance and calcium concentration in crayfish septate axons. J. Membrain Biol. 117, 79–89 (1990). https://doi.org/10.1007/BF01871567
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DOI: https://doi.org/10.1007/BF01871567