Effect of protein kinase A-induced phosphorylation on the gating mechanism of the brain Na+ channel: Model fitting to whole-cell current traces

Biophysical Journal

Volumn 77, Issue 1, 1999, Pages 204-216

  D'Alcantara, Pablo ^a   Schiffmann, Serge N ^a   Swillens, Stéphane ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; SODIUM CHANNEL; VOLTAGE GATED CHANNEL FORMING PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CATALYST; CHANNEL GATING; CHEMICAL MODIFICATION; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVATION; ION PERMEABILITY; MOLECULAR MODEL; NONHUMAN; PHOSPHORYLATION; RAT; SODIUM CURRENT;

EID: 0033015708     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)76882-7     Document Type: Article

References (47)

1. Aldrich, R. W., D. P. Corey, and C. F. Stevens. 1983. A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature. 306:436-441.
2. Aldrich, R. W., and C. F. Stevens. 1983. Inactivation of open and closed sodium channels determined separately. Cold Spring Harb. Symp. Quant. Biol. 48:147-153.
3. Armstrong, C. M. 1981. Sodium channels and gating currents. Physiol. Rev. 61:644-683.
4. Bean, B. P. 1981. Sodium channel inactivation in the crayfish giant axon. Must channels open before inactivating? Biophys. J. 35:595-614.
5. Cantrell, A. R., R. D. Smith, A. L. Goldin, T. Scheuer, and W. A. Catterall. 1997. Dopaminergic modulation of sodium current in hippocampal neurons via cAMP-dependent phosphorylation of specific sites in the sodium channel α subunit. J. Neurosci. 17:7330-7338.
6. Catterall, W. A. 1992. Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev. 72:S15-S48
7. Costa, M. R., J. E. Casnellie, and W. A. Catterall. 1982. Selective phosphorylation of the alpha subunit of the sodium channel by cAMP-dependent protein kinase. J. Biol. Chem. 257:7918-7921.
8. Costa, M. R., and W. A. Catterall. 1984. Cyclic AMP-dependent phosphorylation of the alpha subunit of the sodium channel in synaptic nerve ending particles. J. Biol. Chem. 259:8210-8218.
9. Cukierman, S. 1996. Regulation of voltage-dependent sodium channels. J. Membr. Biol. 151:203-214.
10. + channel. Neuron. 6:165-175.
11. Fraser, D. D., K. Hoehn, S. Weiss, and B. A. MacVicar. 1993. Arachidonic acid inhibits sodium currents and synaptic transmission in cultured striatal neurons. Neuron. 11:633-644.
12. Gershon, E., L. Weigl, I. Lotan, W. Schreibmayer, and N. Dascal. 1992. Protein kinase A reduces voltage-dependent Na+ current in Xenopus oocytes. J. Neurosci. 12:3743-3752.
13. + currents by enhancing inactivation from the closed state. Pflugers Arch. 429:245-252.
14. + currents in mouse neuroblastoma cells. J. Membrane Biol. 140:101-110.
15. Goldman, L. 1995. Sodium channel inactivation from closed states: evidence for an intrinsic voltage dependency. Biophys. J. 69:2369-2377.
16. Hamill, O. P., A. Marty, E. Neher, B. Sakmann, and F. J. Sigworth. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391:85-100.
17. Hebert, T. E., R. Monette, J. C. Stone, P. Drapeau, and R. J. Dunn. 1994. Insertion mutations of the RIIA Na+ channel reveal novel features of voltage gating and protein kinase A modulation. Pflugers Arch. 427: 500-509.
18. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer Associates Inc., Sunderland, MA.
19. + channels. J. Gen. Physiol. 106:1053-1068.
20. Hodgkin, A. L., and Huxley, A. F. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500-544.
21. Horn, R., J. Patlak, and C. F. Stevens. 1981. Sodium channels need not open before they inactivate. Nature. 291:426-427.
22. Horn, R., and C. A. Vandenberg. 1984. Statistical properties of single sodium channels. J. Gen. Physiol. 84:505-534.
23. Lauger, P., W. Stephan, and E. Frehland. 1980. Fluctuations of barrier structure in ionic channels. Biochim. Biophys. Acta. 602:167-180.
24. Li, M., J. W. West, Y. Lai, T. Scheuer, and W. A. Catterall. 1992. Functional modulation of brain sodium channels by cAMP-dependent phosphorylation. Neuron. 8:1151-1159.
25. Li, M., J. W. West, R. Numann, B. J. Murphy, T. Scheuer, and W. A. Catterall. 1993. Convergent regulation of sodium channels by protein kinase C and cAMP-dependent protein kinase. Science. 261:1439-1442.
26. Marban, E., T. Yamagishi, and G. F. Tomaselli. 1998. Structure and function of voltage-gated sodium channels. J. Physiol. Lond. 508: 647-657.
27. McPhee, J. C., D. S. Ragsdale, T. Scheuer, W. A. Catterall. 1995. A critical role for transmembrane segment IVS6 of the sodium channel α subunit in fast inactivation. J. Biol. Chem. 270:12025-12034.
28. Murphy, B. J., S. Rossie, J. K. De, and W. A. Catterall. 1993. Identification of the sites of selective phosphorylation and dephosphorylation of the rat brain Na+ channel alpha subunit by cAMP-dependent protein kinase and phosphoprotein phosphatases. J. Biol. Chem. 268:27355-27362.
29. Nicoll, R. A., R. C. Malenka, and J. A. Kauer. 1990. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev. 70:513-565.
30. Numann, R., W. A. Catterall, and T. Scheuer. 1991. Functional modulation of brain sodium channels by protein kinase C phosphorylation. Science. 254:115-118.
31. + current in rat hippocampal neurones via protein kinase C. J. Physiol. Lond. 503:479-488.
32. + channels. Physiol. Rev. 71:1047-1080.
33. Rossie, S., and W. A. Catterall. 1987. Cyclic-AMP-dependent phosphorylation of voltage-sensitive sodium channels in primary cultures of rat brain neurons. J. Biol. Chem. 262:12735-12744.
34. Sarkar, S. N., A. Adhikari, and S. K. Sikdar. 1995. Kinetic characterization of rat brain type IIA sodium channel alpha-subunit stably expressed in a somatic cell line. J. Physiol. Lond. 488:633-645.
35. Schiffmann, S. N., P. M. Lledo, and J. D. Vincent. 1995. Dopamine D1 receptor modulates the voltage-gated sodium current in rat striatal neurones through a protein kinase A. J. Physiol. Lond. 483:95-107.
36. Schiffmann, S. N., F. Desdouits, R. Menu, P. Greengard, J.-D. Vincent, J.-J. Vanderheagen, and J.-A. Girault. 1998. Modulation of the voltage-gated sodium current in rat striatal neurons by DARPP-32, an inhibitor of protein phosphatase. Eur. J. Neurosci. 10:1312-1320.
37. Sigg, D., and F. Bezanilla. 1997. Total charge movement per channel. The relation between gating charge displacement and the voltage sensitivity of activation. J. Gen. Physiol. 109:27-39.
38. Sigworth, F. J. 1995. Charge movement in the sodium channel. J. Gen. Physiol. 106:1047-1051.
39. Smith, R. D., and A. L. Goldin. 1992. Protein kinase A phosphorylation enhances sodium channel currents in Xenopus oocytes. Am. J. Physiol. 263:C660-C666
40. Smith, R. D., and A. L. Goldin. 1997. Phosphorylation at a single site in the rat brain sodium channel is necessary and sufficient for current reduction by protein kinase A. J. Neurosci. 17:6086-6093.
41. Stevens, C. F. 1978. Interactions between intrinsic membrane protein and electric field. An approach to studying nerve excitability. Biophys. J. 22:295-306.
42. Stimers, J. R., F. Bezanilla, and R. E. Taylor. 1985. Sodium channel activation in the squid giant axon. Steady state properties. J. Gen. Physiol. 85:65-82.
43. Surmeier, D. J., J. Eberwine, C. J. Wilson, Y. Cao, A. Stefani, and S. T. Kitai. 1992. Dopamine receptor subtypes colocalize in rat striatonigral neurons. Proc. Natl. Acad. Sci. USA. 89:10178-10182.
44. Vandenberg, C. A., and R. Horn. 1984. Inactivation viewed through single sodium channels. J. Gen. Physiol. 84:535-564.
45. Vandenberg, C. A., and F. Bezanilla. 1991. A sodium channel gating model based on single channel, macroscopic ionic, and gating currents in the squid giant axon. Biophys. J. 60:1511-1533.
46. + channel required for modulation by protein kinase C. Science. 254:866-868.
47. Zhang, X. F., X. T. Hu, and F. J. White. 1998. Whole-cell plasticity in cocaine withdrawal: reduced sodium currents in nucleus accumbens neurons. J. Neurosci. 18:488-498.