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Long-Term Synergistic Regulation of Ionic Channels by C-Kinase and Ca2+/CaM-Type II Kinase

  • Daniel L. Alkon
  • Shigetaka Naito
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 221)

Abstract

The distinct molecular identities of ionic channels within biological membranes are now being revealed. The acetylcholine receptor, a ligandgated cation channel, was solubilized and purified from post-synaptic membranes of the ray Torpedo californica (Karlin, 1980; Changeux, 1981). Entire amino acid sequences for all of the acetylcholine receptor subunits were deduced from DNA sequence analysis of cDNA clones (Numa et al., 1983). Similarly, the voltage-sensitive Na+ channel from rat brain has been solubilized and purified to homogeneity, and shown to consist of α (Mr 260,000), β1 and β2(Mr 39,000 and 37,000, respectively) subunits (Agnew et al., 1980; Weigele and Barchi, 1982; Hartshorne and Catterall, 1984). Consistent with the heterogeneity of tetrodotoxin binding sites, presence of at least three distinct Na+ channels (I, II and III) in rat brain was suggested from a sequencing study of cDNA clones obtained from three distinct mRNAs for the α-subunit (Noda et al., 1986). The Ca2+ channel (a dihydropyridine-sensitive class) was also purified (Curtis and Catterall, 1985). None of the known K+ channels have yet been purified, probably due to the unavailability of high affinity neurotoxins and a K+ channel abundance which is small in comparison to that of the Na+ channel and the acetylcholine receptor.

Keywords

Hair Cell Acetylcholine Receptor Associative Learning Phorbol Ester Outward Current 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Abrams, T. W., Castellucci, V. F., Camardo, J. S., Kandel, E. R. and Lloyd, P. E., Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel, Proc. Nat. Acad. Sci. USA, 81:7956–7960 (1984).CrossRefGoogle Scholar
  2. Acosta-Urquidi, J., Alkon, D. L. and Neary, J. T., Ca2+-dependent protein kinase injection in a photoreceptor mimics biophysical effects of associative learning, Science, 224:1254–1257 (1984).CrossRefGoogle Scholar
  3. Agnew, W. S., Moore, A. C., Levinson, S. R. and Raftery, M. A., Identification of a large molecular weight peptide associated with a tetrodotoxin binding protein from the electroplax of Electrophorus electricus, Bio-chem. Biophys. Res. Commun. 92:860–866 (1980).CrossRefGoogle Scholar
  4. Alkon, D. L., Voltage-dependent calcium and potassium ion conductances: A contingency mechanism for an associative learning model, Science, 205: 810–816 (1979).CrossRefGoogle Scholar
  5. Alkon, D. L., Membrane depolarization accumulates during acquisition of an associative behavioral change, Science, 210:1375–1376 (1980).CrossRefGoogle Scholar
  6. Alkon, D. L., Calcium-mediated reduction of ionic currents: A biophysical memory trace, Science, 226:1037–1045 (1984).CrossRefGoogle Scholar
  7. Alkon, D. L., Acosta-Urquidi, J., Olds, J., Kuzma, G. and Neary, J. T., Protein kinase injection reduces voltage-dependent potassium currents, Science, 219:303–306 (1983).CrossRefGoogle Scholar
  8. Alkon, D. L., Kubota, M., Neary, J. T., Naito, S., Coulter, D. and Rasmussen, H., C-kinase activation prolongs Ca2+-dependent inactivation of K+ currents, Biochem. Biophys. Res. Commun., 134:1215–1222 (1986).CrossRefGoogle Scholar
  9. Alkon, D. L., Lederhendler, I. and Shoukimas, J. J., Primary changes of membrane currents during retention of associative learning, Science, 215:693–695 (1982).CrossRefGoogle Scholar
  10. Alkon, D. L., Sakakibara, M., Forman, R., Harrigan, J., Lederhendler, I. and Farley, J., Reduction of two voltage-dependent K+ currents mediates retention of a learned association, Behav. Neural Biol., 44:278–300 (1985).CrossRefGoogle Scholar
  11. Bownds, M. D., Dawes, J., Miller, J. and Stahlman, M., Phosphorylation of frog photoreceptor membranes induced by light, Nature, 237:125–127 (1972).Google Scholar
  12. Castellucci, V. F., Kandel, E. R., Schwartz, J. H., Wilson, F. D., Nairn, A. C. and Greengard, P., Intracellular injection of the catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia, Proc. Nat. Acad. Sci. USA, 77:7492–7496 (1980).CrossRefGoogle Scholar
  13. Changeux, J.-P., The acetylcholine receptor: An “allosteric” membrane protein, Harvey Lect., 75:85–254 (1981).Google Scholar
  14. Coronado, R. and LaTorre, R., Phospholipid bilayers made from monolayers on patch-clamp pipettes, Biophys. J., 43:231–236 (1983).CrossRefGoogle Scholar
  15. Costa, M. R. C., Casnellie, J. E. and Catterall, W. A., Selective phosphorylation of the α-subunit of the sodium channel by cAMP-dependent protein kinase, J. Biol. Chem., 257:7918–7921 (1982).Google Scholar
  16. Costa, M. R. C. and Catterall, W. A., Phosphorylation of the α subunit of the sodium channel by protein kinase C, Cell. Mol. Neurobiol., 4:291–297 (1984).CrossRefGoogle Scholar
  17. Coulter, D. A., Kubota, M., Disterhoft, J. F., Moore, J. W. and Alkon, D. L., Conditioning-specific reduction of CA1 afterhyperpolarization amplitude and duration in rabbit hippocampal slices, Soc. Neurosci. Abstr., 11:981 (1985).Google Scholar
  18. Crow, T. J. and Alkon, D. L., Associative behavioral modification in Her-missenda: cellular correlates, Science, 209:412–414 (1980).CrossRefGoogle Scholar
  19. Curtis, B. M. and Catterall, W. A., Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules, Biochemistry, 23:2113–2118 (1984).CrossRefGoogle Scholar
  20. DePeyer, J. E., Cachelin, A. B., Levitan, I. B. and Reuter, H., Ca2+-acti-vated K+ conductance in internally perfused snail neurons is enhanced by protein phosphorylation, Proc. Nat. Acad. Sci. USA, 79:4207–4211 (1982).CrossRefGoogle Scholar
  21. DeRiemer, S. A., Strong, J. A., Albert, K. A., Greengard, P. and Kaczmarek, L. K., Enhancement of calcium current in Aplysia neurones by phorbol ester and protein kinase C, Nature, 313:313–316 (1985).CrossRefGoogle Scholar
  22. Disterhoft, J. F., Coulter, D. A. and Alkon, D. L., Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro, Proc. Nat. Acad. Sci. USA, in press (1986).Google Scholar
  23. Ewald, D. A., Williams, A. and Levitan, I. B., Modulation of single Ca2+-dependent K+ channel activity by protein phosphorylation, Nature, 315: 503–506 (1985).CrossRefGoogle Scholar
  24. Farley, J. and Alkon, D. L., Associative neural and behavioral change in Hermissenda: consequences of nervous system orientation for light and pairing specificity, J. Neurophysiol. 48:785–807 (1982).Google Scholar
  25. Farley, J. and Auerbach, S., Protein kinase C activation induces conductance changes in Hermissenda photoreceptors like those seen in associative learning, Nature, 319:220–223 (1986).CrossRefGoogle Scholar
  26. Goh, Y., Lederhendler, I. and Alkon, D. L., Input and output changes of an identified neural pathway are correlated with associative learning in Hermissenda, J. Neurosci., 5:536–543 (1985).Google Scholar
  27. Hartshorne, R. P. and Catterall, W. A., The sodium channel from rat brain: purification and subunit composition, J. Biol. Chem., 259:1667–1675 (1984).Google Scholar
  28. Huganir, R. L. and Greengard, P., cAMP-dependent protein kinase phosphory-lates the nicotinic acetylcholine receptor, Proc. Nat. Acad. Sci. USA, 80:1130–1134 (1983).CrossRefGoogle Scholar
  29. Huganir, R. L., Miles, K. and Greengard, P., Phosphorylation of the nicotinic acetylcholine receptor by an endogenous tyrosine-specific protein kinase, Proc. Nat. Acad. Sci. USA, 81:6968–6972 (1984).CrossRefGoogle Scholar
  30. Kaczmarek, L. K., Jennings, K. and Strumwasser, F., Neurotransmitter modulation, phosphodiesterase inhibitor effects, and cyclic AMP correlates of afterdischarge in peptidergic neurons, Proc. Nat. Acad. Sci. USA, 75:5200–5204 (1978).CrossRefGoogle Scholar
  31. Kaczmarek, L. K., Jennings, K. R., Strumwasser, F., Nairn, A. C., Walter, U., Wilson, F. D. and Greengard, P., Microinjection of catalytic sub-unit of cyclic-AMP-dependent protein kinase enhances calcium action potentials of bag cell neurons in cell culture, Proc. Nat. Acad. Sci. USA, 77:7487–7491 (1980).CrossRefGoogle Scholar
  32. Kaibuchi, K., Takai, Y., Sawamura, M., Hoshijima, M., Fujikura, T. and Nishizuka, Y., Synergistic functions of protein phosphorylation and calcium mobilization, J. Biol. Chem., 258:6701–6704 (1983).Google Scholar
  33. Karlin, A., Molecular properties of nicotinic acetylcholine receptors. In, The Cell Surface and Neuronal Function (Eds. Poste, G., Nicolson, G., and Cotman, C. W.) Elsevier/North Holland, Amsterdam, pp. 191–260 (1980).Google Scholar
  34. Kojima, I., Kojima, K., Kreutter, D. and Rasmussen, H., The temporal integration of the aldosterone secretory response to angiotension occurs via two intracellular pathways, J. Biol. Chem., 259:14448–14457 (1984).Google Scholar
  35. Krueger, B. K., Forn, J. and Greengard, P., Depolarization-induced phosphorylation of specific proteins, mediated by calcium ion influx, in rat brain synaptosomes, J. Biol. Chem., 252:2764–2773 (1977).Google Scholar
  36. Kubota, M., Alkon, D. L., Naito, S. and Rasmussen, H., Regulation of membrane currents by injection of C-kinase, Soc. Neurosci. Abstr., in press (1986).Google Scholar
  37. Lederhendler, I., Gart, S. and Alkon, D. L., Classical conditioning of Her-missenda: origin of a new response. J. Neurosci., in press (1986).Google Scholar
  38. Lemos, J. R., Novak-Hofer, I. and Levitan, I. B., Phosphoproteins associated with the regulation of a specific potassium channel in the identified Aplysia neurons R15, J. Biol. Chem., 260:3207–3214 (1985).Google Scholar
  39. Levitan, I. B., Phosphorylation of ion channels, J. Memb. Biol., 87:177–190 (1985).CrossRefGoogle Scholar
  40. Levitan, I. B., Harmar, A. J. and Adams, W. B., Synaptic and hormonal modulation of a neuronal oscillator: a search for molecular mechanisms, J. Exp. Biol., 81:131–151 (1979).Google Scholar
  41. Malenka, R. C., Madison, D. V., Andrade, R. and Nicoll, R. A., Phorbol esters mimic some cholinergic actions in hippocampal pyramidal neurons, J. Neurosci., 6:475–480 (1986).Google Scholar
  42. Neary, J. T. and Alkon, D. L., Protein phosphorylation/dephosphorylation and the transient, voltage-dependent potassium conductance in Hermissenda crassicornis, J. Biol. Chem., 258:8979–8983 (1983).Google Scholar
  43. Neary, J. T., Crow, T. and Alkon, D. L., Change in a specific phosphoprotein band following associative learning in Hermissenda, Nature, 293:658–660 (1981).CrossRefGoogle Scholar
  44. Noda, M., Ikeda, T., Kayano, T., Suzuki, H., Takeshima, H. Kurasaki, M., Takahashi, H. and Numa, S., Existence of distinct sodium messenger channel RNAs in rat brain, Nature, 320:188–192 (1986).CrossRefGoogle Scholar
  45. Numa, S., Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Furutani, Y. and Kikyotani, S., Molecular structure of the nicotinic acetylcholine receptor, Cold Spring Harbor Symp. Quant. Biol., 48:57–69 (1983).CrossRefGoogle Scholar
  46. Rane, S. G. and Dunlap, K., Kinase C activator 1, 2-oleoylacetylglycerol attenuates voltage-dependent Ca2+ current in sensory neurons, Proc. Nat. Acad. Sci. USA, 83:184–188 (1986).CrossRefGoogle Scholar
  47. Sakakibara, M., Alkon, D. L., Neary, J. T., DeLorenzo, R., Gould, R. and Heldman, E., Ca2+-mediated reduction of K+ currents is enhanced by injection of IP3 or neuronal Ca2+/calmodulin kinase type II, Soc. Neurosci. Abstr., 11:956 (1985).Google Scholar
  48. Sakakibara, M., Alkon, D. L., DeLorenzo, R., Goldenring, J. R., Neary, J. T. and Heldman, E., Modulation of calcium-mediated inactivation of ionic currents by Ca2+/calmodulin-dependent protein kinase II, Bio-phys. J., in press (1986).Google Scholar
  49. Shuster, M. J., Camardo, J. S., Siegelbaum, S. A. and Kandel, E. R., Cyclic AMP-dependent protein kinase closes the serotonin-sensitive K+ channels of Aplysia sensory neurons in cell free membrane patches, Nature, 313:392–395 (1985).CrossRefGoogle Scholar
  50. Suarez-Isla, B. A., Wan, K., Lindstrom, J. and Montal, M., Single channel recordings from purified acetylcholine receptors reconstituted in bi-layers formed at the tip of patch pipets, Biochemistry, 22:2319–2323 (1983).CrossRefGoogle Scholar
  51. Szuts, E. Z., Light stimulates phosphorylation of two large membrane proteins in frog photoreceptors, Biochemistry, 24:4176–4984 (1985).CrossRefGoogle Scholar
  52. Wane, J. A., Johnson, P. C., Smith, M. and Salzman, E. W., Aequorin detects increased cytoplasmic calcium in platelets stimulated with phorbol ester or diacylglycerol, Biochem. Biophys. Res. Commun., 133:98–104 (1985).CrossRefGoogle Scholar
  53. Weigele, J. B. and Barchi, R. L., Functional reconstitution of the purified sodium channel protein from rat sarcolemma, Proc. Nat. Acad. Sci. USA, 79:3651–3655 (1982).CrossRefGoogle Scholar
  54. Wilmsen, U., Methfessel, C., Hanke, W. and Boheim, G., In, Physical Chemistry of Transmembrane Ion Motions, Elsevier/North Holland, Amsterdam. pp. 479–485 (1983).Google Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • Daniel L. Alkon
    • 1
  • Shigetaka Naito
    • 1
  1. 1.Section on Neural Systems, Laboratory of BiophysicsNational Institute of Neurological and Communicative Disorders and Stroke, National Institutes of Health at the Marine Biological LaboratoryWoods HoleUSA

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