Skip to main content
Log in

Inward rectification by hyperpolarization-activated Na current in the marine ciliate Euplotes vannus

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

The ionic mechanisms underlying inward or anomalous rectification have been studied in the marine hypotrichous ciliate Euplotes vannus. Inward-current pulses of moderate amplitude elicited time-dependent rectification that started from a hyperpolarization peak and was expressed as a depolarizing sag towards rest. Voltage-clamp analysis showed that this depolarization is caused by the activation of a complex inward current that does not inactivate with time. The current is carried by a major Na and a minor K component. The Na-current component has been identified by its concentration-dependent reduction in low extra-cellular Na solutions and the capability of Li2+ as Na substitute to carry the current, though with a slightly reduced amplitude. The K-current component has been isolated from the total current after the replacement of Na2+ within the experimental solution. It was blocked in media that contained 10 mmol/liter TEA, a well-known blocker for K inwardly rectifying currents. TEA was only effective at membrane potentials close to or negative to the potassium equilibrium potential. The inward current was reduced after the injection of the Ca chelator EGTA into the cell. Also the elimination of the ciliary membrane, by deciliating cells with ethanol, reduced the amplitude of the inwardly rectifying currents. Both experiments indicate a regulatory function of Ca22+ in inward rectification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Angstadt, J.D., Calabrese, R.L. 1989. A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J. Neurosci. 9:2846–2857

    Google Scholar 

  • Ballanyi, K., Deitmer, J.W. 1984. Concentration-dependent effects of Ba22+ on action potential and membrane currents in the ciliate Stylonychia. Comp. Biochem. Physiol. 78A:575–581

    Google Scholar 

  • De Peyer, J.E., Machemer, H. 1978. Hyperpolarizing and depolarizing mechanoreceptor potentials in Stylonychia. J. Comp. Physiol. 127:255–266

    Google Scholar 

  • Deitmer, J.W. 1981. Voltage and time characteristics of the potassium mechanoreceptor current in the ciliate Stylonychia. J. Comp. Physiol. 141:173–182

    Google Scholar 

  • Deitmer, J.W. 1982. The effects of tetraethylammonium and other agents on the potassium mechanoreceptor current in the ciliateStylonychia. J. Exp. Biol. 96:239–249

    Google Scholar 

  • DiFrancesco, D., Torotora, P. 1991. Direct activation of cardiac pace-maker channels by intracellular cyclic AMP. Nature 351:145–147

    Google Scholar 

  • Kamondi, A., Reiner, P.B. 1991. Hyperpolarization-activated inward current in histaminergic tuberomammillary neurons of the rat hypothalamus. J. Neurophysiol. 66:1902–1911

    Google Scholar 

  • Krüppel, T., Lueken, W. 1988. Membrane excitability and membrane currents in the marine ciliate Euplotes vannus. Eur. J. Protistol. 24:11–21

    Google Scholar 

  • Krüppel, T., Lueken, W. 1990. Calcium-dependent sodium current in the marine ciliate Euplotes vannus. J. Membrane Biol. 116:79–86

    Google Scholar 

  • Latorre, R., Miller, C. 1983. Conduction and selectivity in potassium channels. J. Membrane Biol. 71:11–30

    Google Scholar 

  • Lueken, W., Gaertner, M., Breer, H. 1983. Mating-type-specific loss of conjugation competence by irritation in Euplotes vannus. J. Exp. Zool. 226:11–17

    Google Scholar 

  • Machemer, H., Ogura, A. 1979. Ionic conductances of membranes in ciliated and deciliated Paramecium. J. Physiol. 296:49–60

    Google Scholar 

  • Matsuda, H., Saigusa, A., Irisawa, H. 1987. Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg22+. Nature 325:156–159

    Google Scholar 

  • McCormick, D.A., Pape, H-C. 1990. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol. 431:291–318

    Google Scholar 

  • Mukai, M., Kyogoku, L, Kuno, M. 1992. Calcium-dependent inactivation of inwardly rectifying K2+ channel in a tumor mast cell line. Am. J. Physiol. 256:C84-C90

    Google Scholar 

  • Naitoh, Y., Eckert, R. 1968. Electrical properties of Paramecium caudatum: Modifications by bound and free cations. Z. vergl. Physiologie 61:427–452

    Google Scholar 

  • Naitoh, Y., Eckert, R. 1973. Sensory mechanisms in Paramecium II. Ionic basis of the hyperpolarizing mechanoreceptor potential. J. Exp. Biol. 59:53–65

    Google Scholar 

  • Oertel, D., Schein, S.J., Kung, C. 1978. A potassium conductance activated by hyperpolarization in Paramecium. J. Membrane Biol. 43:169–185

    Google Scholar 

  • Ogura, A., Machemer, H. 1980. Distribution of mechanoreceptor channels in the Paramecium surface membrane. J. Comp. Physiol. 135:233–242

    Google Scholar 

  • Partridge, L.D., Swandulla, D. 1988. Calcium-activated non-specific cation channels. TINS 11:69–72

    Google Scholar 

  • Phillips, C.L., Bacigalupo, J., O'Day, P.M. 1992. Inward rectification in Limulus photoreceptors. Visual Neurosci. 8:19–25

    Google Scholar 

  • Preston, R., Saimi, Y., Kung, C. 1990. Evidence for two K2+ currents activated upon hyperpolarization of Paramecium tetraurelia. J. Membrane Biol. 115:41–50

    Google Scholar 

  • Preston, R.R., Saimi, Y., Kung, C. 1992a. Calcium current activated upon hyperpolarization of Paramecium tetraurelia. J.Gen. Physiol. 100:233–251

    Google Scholar 

  • Preston, R.R., Saimi, Y., Kung, C. 1992b. Calcium-dependent inacti vation of the calcium current activated upon hyperpolarization of Paramecium tetraurelia. J. Gen. Physiol. 100:253–268

    Google Scholar 

  • Rudy, B. 1988. Diversity and ubiquity of K channels. Neuroscience 25:729–749

    Google Scholar 

  • Saimi, Y. 1986. Calcium-dependent sodium currents in Paramecium: mutational manipulations and effects of hyper and depolarization. J. Membrane Biol. 92:227–236

    Google Scholar 

  • Saimi, Y., Kung, C. 1980. A Ca-induced Na-current in Paramecium. J. Exp. Biol. 88:305–325

    Google Scholar 

  • Satow, Y., Kung, C. 1974. Genetic dissection of active electrogenesis in Paramecium aurelia. Nature 247:69–71

    Google Scholar 

  • Satow, Y., Kung, C. 1977. A regenerative hyperpolarization in Paramecium. J. Comp. Physiol. 119:99–110

    Google Scholar 

  • Spain, W.J., Schwindt, P.C., Crill, W.E. 1987. Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 57:1555–1576

    Google Scholar 

  • Thompson, H., Aldrich, W. 1980. Membrane potassium channels. In: The Cell Surface and Neuronal Function. C.W. Cotman, G. Poste, and G.L. Nicolson, editors, pp. 49–85. Elsevier North-Holland, Amsterdam

    Google Scholar 

  • Tokimasa, T., Akasu, T. 1990. Cyclic AMP regulates an inward rectifying sodium-potassium current in dissociated bull-frog sympathetic neurones. J. Physiol. 420:409–429

    Google Scholar 

  • Valbonesi, A., Ortenzi, C., Luporini, P. 1988. An integrated study of the species problem in the Euplotes crassus-minutavannus group. J. Protozool. 35:38–45

    Google Scholar 

  • Valbonesi, A., Ortenzi, C., Luporini, P. 1992. The species problem in a ciliate with a high multiple mating type system, Euplotes crassus. J. Protozool. 39:45–54

    Google Scholar 

  • Vandenberg, C.A. 1987. Inward rectification of a potassium channel in cardiac ventricular cells depends on internal magnesium ions. Proc. Natl. Acad. Sci. USA 84:2560–2564

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

The author is grateful to Harald Mikoleit for technical assistance and preparing the figures and to Prof. W. Lueken for his critical comments. This work was supported by Deutsche Forschungsgemeinschaft, SFB 171, C7.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krüppel, T. Inward rectification by hyperpolarization-activated Na current in the marine ciliate Euplotes vannus . J. Membarin Biol. 133, 263–270 (1993). https://doi.org/10.1007/BF00232025

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00232025

KeyWords

Navigation