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Structural and developmental differences between three types of Na channels in dorsal root ganglion cells of newborn rats

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Summary

The changes in Na current during development were studied in the dorsal root ganglion (DRG) cells using the whole-cell patch-clamp technique. Cells obtained from rats 1–3 and 5–8 days after birth were cultured and their Na currents were compared. On top of the two types of Na currents reported in these cells (fast-FA current and slow-S current) a new fast current was found (FN). The main characteristics of the three currents are: (i) The voltages of activation are −37, −36, and −23 mV for the FN, FA and S currents, respectively. (ii) The activation and inactivation kinetics of FN and FA currents are about five times faster than those of the S current. (iii) The voltages at which inactivation reaches 50% are −139, −75 and −23 mV for the FN, FA and S currents, respectively.

The kinetics and voltage-dependent parameters of the three currents and their density do not change during the first eight days after birth. However, their relative frequency in the cells changes. In the 1–3 day-old rats the precent of cells with S, FA, and mixed S+FN currents is 22, 18, and 60% of the cells, respectively. In the 5–8 day-old, the percent of cells with S, FA, and FN+S is 10, 66 and 22%. The relative increase in the frequency of cells with FA current during development can contribute to the ease of action potential generation compared with cells with FN currents, which are almost completely inactivated under physiological conditions. The predominance of FA cells also results in a significant decrease in the relative frequency of cells with the high-threshold, slow current.

Antibodies directed against a part of the S4 region of internal repeat I of the sodium channel (C +1 , amino acids 210–223, eel channel numbering) were found to shift the voltage dependence of FA current inactivation (but not of FN or S currents) to more negative potentials. The effect was found only when the antibodies were applied externally. The results suggest that FN, FA and S types of Na currents are generated by channels, which are different in the topography of the C +1 region in the membrane.

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References

  1. Aldrich, R.W., Corey, D.P., Stevens, C.F. 1983. A reinterpretation of mammalian sodium channel gating based on single channel recording.Nature (London) 306:436–441

    Google Scholar 

  2. Almers, W., McClesky, E.W. 1984. Non-selective conductance in calcium channels of frog muscle: Calcium selectivity in single-file pore.J. Physiol. (London) 353:585–608

    Google Scholar 

  3. Armstrong, C. 1981. Sodium currents and gating currents.Physiol. Rev. 61:644–683

    PubMed  Google Scholar 

  4. Barchi, R.L. 1988. Probing the molecular structure of the voltage dependent sodium channel.Annu. Rev. Neurosci. 11:455–489

    PubMed  Google Scholar 

  5. Bossu, J.L., Feltz, A. 1984. Patch-clamp study of the tetrodotoxin-resistent sodium current in group C sensory neurons.Neurosci. Lett. 51:241–246

    PubMed  Google Scholar 

  6. Catterall, W.A. 1988. Structure and function of voltage sensitive ion channels.Science 242:50–61

    PubMed  Google Scholar 

  7. Drews, G., Rack, M. 1988. Modification of sodium and gating currents by amino group specific cross-linking and monofunctional reagents.Biophys. J. 54:383–391

    PubMed  Google Scholar 

  8. Edgar, D., Bard, Y.A., Thoenen, H. 1981. Subpopulations of cultured sympathetic neurons differ in their requirements for survival factors.Nature (London) 289:294–295

    Google Scholar 

  9. Fedlova, S.A., Kostyuk, P.G., Vaselovsky, N.S. 1985. Two types of calcium currents in the somatic membrane of newborn rat dorsal root ganglion neurons.J. Physiol. (London) 359:431–446

    Google Scholar 

  10. Gilly, W.F., Brismar, T. 1989. Properties of appropriately and inappropriately expressed sodium channel in squid giant axons and its somata.J. Neurosci. 9:1362–1374

    PubMed  Google Scholar 

  11. Gordon, D., Catterall, W.A. 1987. Identification of an intracellular domain of the sodium channel having multiple c-AMP dependent phosphorylation sites.J. Biol. Chem. 262:17530–17535

    PubMed  Google Scholar 

  12. Gordon, D., Merrick, D., Auld, V., Dunn, R., Goldin, A.L., Davidson, N., Catterall, W.A. 1987. Tissue specific expression of the RI and RII sodium channel subtypes.Proc. Natl. Acad. Sci. USA 84:308–313

    PubMed  Google Scholar 

  13. Gordon, R.D., Fieles, W.E., Schotland, D.L., Hogue-Angeletti, R., Barchi, R.L. 1987. Topographical localization of the C-terminal region of the voltage dependent sodium channel fromElectrophorus electricus using antibodies raised against a synthetic peptide.Proc. Natl. Acad. Sci. USA 84:308–313

    PubMed  Google Scholar 

  14. Gordon, R.D., Li, Y., Fieles, W.E., Schotland, D.L., Barchi, R.L. 1988. Topological localization of a segment of the eel voltage dependent sodium channel primary sequence (AA927-938) that discriminates models of tertiary structure.J. Neurosci. 8:3742–3749

    PubMed  Google Scholar 

  15. Gottman, K., Dietzel, I.D., Lux, H.D., Huck, S., Rohrer, H. 1988. Development of inward currents in chick sensory and autonomic neuronal precursor cells in culture.J. Neurosci. 8:3722–3733

    PubMed  Google Scholar 

  16. Guyton, A.C. 1981. Medical Physiology. Chap. 48. pp. 595. Sounders, Philadelphia

    Google Scholar 

  17. Hamill, O.P., Marty, A., Neher, E., Sakman, B., Sigworth, F.J. 1981. Improved patch clamp techniques for high-resolution current recording from cells and cell-free membrane patches.Pfluegers Arch. 391:85–100

    Google Scholar 

  18. Harper, A.A., Lawson, J.N. 1985. Conduction velocities related to morphological cell type in rat dorsal root ganglia.J. Physiol. (London) 359:31–46

    Google Scholar 

  19. Harper, A.A., Lawson, J.N. 1985. Electrical properties of dorsal root ganglion neurons with different peripheral nerve conduction velocities.J. Physiol. (London) 359:47–63

    Google Scholar 

  20. Hess, P., Lansman, J.B., Tsien, R.W. 1986. Calcium channel selectivity for divalent and monovalent cations.J. Gen. Physiol. 88:293–319

    Google Scholar 

  21. Heyer, E.J., Mcdonald, R.L. 1982. Calcium and sodium dependent action potentials of mouse spinal cord and dorsal root ganglion neurons in cell culture.J. Neurophysiol. 47:641–655

    PubMed  Google Scholar 

  22. Hille, B. 1984. Ionic Currents of Excitable Membrane. Sinauer, Sunderland (MA)

    Google Scholar 

  23. Hille, B., Woodhull, A.M., Shapiro, B.I. 1975. Negative surface charge near sodium currents of nerve: Divalent ions, monovalent ions and pH.Phil. Trans. R. Soc. London B 270:301–318

    Google Scholar 

  24. Hodgkin, A.L., Huxley, A.F. 1952. A quantitative description of membrane currents and its application to conduction and excitation in nerve.J. Physiol. (London) 117:500–544

    Google Scholar 

  25. Huang, J.M.C., Tanguy, J., Yeh, J.Z. 1987. Removal of sodium inactivation and block of sodium channels by chloramine-T in crayfish and squid giant axons.Biophys. J. 52:155–163

    PubMed  Google Scholar 

  26. Ikeda, S.R., Schofield, G.G. 1987. Tetrodotoxin resistant sodium current at nodose neurons; monovalent cation selectivity and divalent cation block.J. Physiol. (London) 389:255–270

    Google Scholar 

  27. Kameyama, M., Hofmann, F., Trautwein, W. 1985. On the mechanism of beta-adrenergic regulation of the Ca channel in the guinea-pig heart.Pfuegers Arch. 405:285–293

    Google Scholar 

  28. Kayano, T., Noda, M., Flockerzi, V., Takahashi, H., Numa, S. 1988. Primary structure of rat brain sodium channel III deduced from the cDNA sequence.FEBS Lett. 228:187–194

    PubMed  Google Scholar 

  29. Kostyuk, P.G., Shuba, Ya.M., Savahenko, A.N. 1988. Three types of calcium currents in the membrane of mouse sensory neurons.Pfluegers Arch. 411:661–669

    Google Scholar 

  30. Kostyuk, P.G., Vaselovsky, N.S., Tsynderenko, A.Y. 1981. Ionic currents in the somatic membrane of the rat dorsal root ganglion neurons. I. Sodium currents. II. Calcium currents.Neuroscience 6:2423–2438

    PubMed  Google Scholar 

  31. Krafte, D.S., Snutch, T.P., Leonard, J.P., Davidson, N., Lester, H.A. 1988. Evidence for the involvement of more than one mRNA species in controlling the inactivation process of rat and rabbit brain Na channels expressed inXenopus oocytes.J. Neurosci. 8:2859–2868

    PubMed  Google Scholar 

  32. Lee, K.S., Akaike, N., Brown, A.M. 1977. Trypsin inhibits the action of tetrodotoxin on neurons.Nature (London) 265:751–753

    Google Scholar 

  33. Lucas, J.H., Gross, G.W., Tramp, B.F., Balentine, J.D., Berezesky, I.K., Young, W., Gilad, G.M., Bernstein, J.S. 1988. Cellular and molecular correlates of central nervous system trauma.J. Neurotrauma 5:209–258

    Google Scholar 

  34. Matsuda, Y., Yoshida, S., Yonezawa, T. 1978. Tetrodotoxin sensitivity and calcium component of action potentials of mouse dorsal root ganglion cell cultured in-vitro.Brain Res. 154:69–82

    PubMed  Google Scholar 

  35. McLean, M.J., Bennet, P.B., Thomas, R.M. 1988. Subtypes of dorsal root ganglion neurons based on different inward currents as measured by whole cell voltage clamp.Molec. Cell. Biochem. 80:95–107

    PubMed  Google Scholar 

  36. Meiri, H., Omri, G., Zeitoun, I., Savion, N. 1986. Environmental factors that influence the differentiation and the development of voltage dependent sodium channels in cultured dorsal root ganglion cells of newborn rats.Exp. Brain Res. 13:231–245

    Google Scholar 

  37. Meiri, H., Sammar, M., Schwartz, A. 1989. Production and use of synthetic peptide antibodies to map a region associated with sodium channel inactivation.Methods Enzymol. 178:714–739

    PubMed  Google Scholar 

  38. Meiri, H., Spira, G., Sammar, M., Namir, M., Schwartz, A., Komoriya, A., Kosower, E.M., Palti, Y. 1987. Mapping a region associated with Na channel inactivation using antibodies to synthetic peptide corresponding to a part of the channel.Proc. Natl. Acad. Sci. USA 84:5058–5062

    PubMed  Google Scholar 

  39. Merrifield, R.B. 1965. Solid phase synthesis.Science 150:178–185

    PubMed  Google Scholar 

  40. Messner, D.J., Feller, D.J., Scheuer, T., Catterall, W.A. 1986. Functional properties of rat brain sodium channel lacking the beta1 or beta2 subunits.J. Biol. Chem. 26:14882–14890

    Google Scholar 

  41. Meves, H., Rubly, N., Stampfli, R. 1988. The action of arginine-specific reagents on ionic and gating currents of frog myelinated nerve.Biochem. Biophys. Acta. 943:1–12

    PubMed  Google Scholar 

  42. Noda, M., Ikeda, T., Kayano, T., Suzuki, H., Takashima, H., Kuraski, M., Takahashi, H., Nakayama, H., Numa, S. 1986. Existence of distinct sodium channel messenger RNAs in rat brain.Nature (London) 320:188–192

    Google Scholar 

  43. Noda, M., Shimizu, S., Tannabe, T., Takai, T., Kayano, T., Ikeda, T., Takahashi, H., Nakayama, H., Kanaoka, Y., Miniamino, N., Kangawa, K., Matsuo, H., Raftery, M.A., Miyata, T., Numa, S. 1984. Primary structure of electrophorus sodium channel deduced from c-DNA sequence.Nature (London) 312:121–127

    Google Scholar 

  44. O'Dowd, D.K., Ribera, A.B., Spitzer, N.C. 1987. Development of voltage-dependent calcium, sodium and potassium currents inXenopus spinal neurons.J. Neurosci.,8:792–805

    Google Scholar 

  45. Okun, L.M. 1972. Isolated dorsal root ganglion neurons in culture: Cytological maturation and extension of electrically active processes.J. Neurobiol. 3:111–151

    PubMed  Google Scholar 

  46. Omri, G., Meiri, H. 1990. Characterization of sodium currents in mammalian sensory neurons cultured in serum-free defined medium with and without NGF.J. Membrane Biol. 115:13–29

    Google Scholar 

  47. Orozco, C.B., Epstein, C.J., Rapoport, S.I. 1988. Voltage activated sodium conductance in cultured normal and trisomy-16 dorsal root ganglion neurons from fetal mouse.Dev. Brain Res. 3:265–274

    Google Scholar 

  48. Oxford, G.S. 1978. Removal of sodium channel inactivation in squid giant axons by N-bromoacetamide.J. Gen. Physiol. 71:227–247

    PubMed  Google Scholar 

  49. Palti, Y., Cohen-Armon, M. 1982. Numerical method for correcting the series resistance error in voltage clamp experiments.Isr. J. Med. Sci. 18:19–24

    PubMed  Google Scholar 

  50. Papazian, D.M., Schwartz, T.L., Temple, B.L., Jan, Y.N., Jan, L.Y. 1984. Cloning of genomic and complimentary DNA from shaker a putative potassium channel gene fromDrosophila.Science 237:749–753

    Google Scholar 

  51. Purves, D., Lichtman, J.W. 1985. Principles of Neuronal Development, Chapter 7. Trophic effects of targets on neurons. pp. 155–178. Sinauer, Sunderland (MA)

    Google Scholar 

  52. Rojas, E., Rudy, B. 1976. Destructive of the sodium conductance inactivation by a specific protease in perfused nerve fibers fromLoligo.J. Physiol. (London) 262:501–531

    Google Scholar 

  53. Sackmann, B., Methfessel, C., Mishina, M., Takahashi, T., Takai, T., Kuraski, M., Fukuda, K., Numa, S. 1985. Role of acetycholine receptor subunits in gating of the channel.Nature (London) 318:538–543

    Google Scholar 

  54. Schmidt, J., Rossie, S., Catterall, W.A. 1985. A large intracellular pool of inactive Na channel alpha subunits in developing rat brain.Proc. Natl. Acad. Sci. USA 82:4847–4851

    PubMed  Google Scholar 

  55. Scott, B.S., Edwards, B.A.V. 1980. Electric membrane properties of adult mouse DRG neurons and the effect of culturing duration.J. Neurobiol. 11:291–301

    PubMed  Google Scholar 

  56. Spalding, B.C. 1980. Properties of toxin resistant sodium channels produced by chemical modification in frog skeletal muscles.J. Physiol. (London) 305:485–500

    Google Scholar 

  57. Spitzer, N.C. 1979. Ion channels in development.Annu. Rev. Neurosci. 2:363–397

    PubMed  Google Scholar 

  58. Stolc, S., Nemcek, V., Boska, D. 1988. Potential clamp of isolated dialyzed neuron: Minimalization of the effect of series resistance.Gen. Physiol. Biophys. 7:303–312

    PubMed  Google Scholar 

  59. Stuhmer, W., Conti, F., Suzuki, H., Wang, X., Wang, X., Noda, M., Numa, S. 1989. Structural parts involved in activation and inactivation of the sodium channel.Nature (London) 339:597–603

    Google Scholar 

  60. Tanabe, T., Takeshima, H., Mikawi, A., Flocherzi, V., Takahashi, H., Kangawa, K., Kayima, M., Matsuo, H., Hirose, T., Numa, S. 1987. Primary structure of the receptor for calcium channel blockers from skeletal muscle.Nature (London) 328:313–318

    Google Scholar 

  61. Trimmer, S., Jr., Cooperman, S.S., Tomiko, S.A., Zhou, J., Crean, S.M., Boyk, M.B., Galle, R.G., Sheng, Z., Barchi, R.L., Sigworth, F.J., Goodman, R.H., Agnew, W.S., Mandel, G. 1989. Primary structure and functional expression of a mammalian skeletal muscle sodium channel.Neuron 3:33–49

    PubMed  Google Scholar 

  62. Vassilev, P.M., Scheur, T., Catterall, W.A. 1988. Identification of an intracellular peptide segment involved in sodium channel inactivation.Science 241:1658–1661

    PubMed  Google Scholar 

  63. Weiss, R.E., Horn, R. 1986. Functional differences between two classes of sodium currents in developing rat skeletal muscle.Science 233:361–364

    PubMed  Google Scholar 

  64. Yoshida, S., Matsuda, Y., Samejima, A. 1978. Tetrodotoxin-resistant sodium and calcium component, of action potentials in DRG cells of the adult mouse.J. Neurophysiol. 41:1096–1106

    PubMed  Google Scholar 

  65. Zeitoun, I., Meiri, H., Omri, G., Palti, Y. 1987. The development of different types of Na channels in rat DRG cells.Proc. Int. Biophys. Cong. 9:143

    Google Scholar 

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Schwartz, A., Palti, Y. & Meiri, H. Structural and developmental differences between three types of Na channels in dorsal root ganglion cells of newborn rats. J. Membrain Biol. 116, 117–128 (1990). https://doi.org/10.1007/BF01868670

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