Subunit dependence of Na channel slow inactivation and open channel block in cerebellar neurons

Biophysical Journal

Volumn 92, Issue 6, 2007, Pages 1938-1951

  Aman, Teresa K ^a   Raman, Indira M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL; SODIUM CHANNEL; SODIUM ION; TETRODOTOXIN; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL TRANSPORT; CEREBELLUM NUCLEUS; CONTROLLED STUDY; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; EXPERIMENTAL MODEL; HYPERPOLARIZATION; MOUSE; MUTAGENESIS; NEUROSCIENCE; NONHUMAN; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PURKINJE CELL;

MUS;

EID: 33947635133     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.093500     Document Type: Article

References (65)

1. Thach, W. 1968. Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J. Neurophysiol. 31:785-797.
2. McDevitt, C. J., T. J. Ebner, and J. R. Bloedel. 1987. Relationships between simultaneously recorded Purkinje cells and nuclear neurons. Brain Res. 425:1-13.
3. Llinas, R., and M. Sugimori. 1980. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. 305:171-195.
4. Jahnsen, H. 1986. Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J. Physiol. 372:129-147.
5. Raman, I. M., and B. P. Bean. 1997. Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci. 17:4517-4526.
6. Raman, I. M., and B. P. Bean. 1999. Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J. Neurosci. 19:1663-1674.
7. Raman, I. M., and B. P. Bean. 2001. Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys. J. 80:729-737.
8. Martina, M., G. L. Yao, and B. P. Bean. 2003. Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons. J. Neurosci. 23:5698-5707.
9. Akemann, W., and T. Knopfel. 2006. Interaction of Kv3 potassium channels and resurgent sodium current influences the rate of spontaneous firing of Purkinje neurons. J. Neurosci. 26:4602-4612.
10. Raman, I. M., A. E. Gustafson, and D. Padgett. 2000. Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J. Neurosci. 20:9004-9016.
11. Afshari, F. S., K. Ptak, Z. M. Khaliq, T. M. Grieco, N. T. Slater, D. R. McCrimmon, and I. M. Raman. 2004. Resurgent Na currents in four classes of neurons of the cerebellum. J. Neurophysiol. 92:2831-2843.
12. Llinas, R., and M. Muhlethaler. 1988. Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J. Physiol. 404:241-258.
13. Khaliq, Z. M., and I. M. Raman. 2005. Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J. Neurosci. 25:454-463.
14. Monsivais, P., B. A. Clark, A. Roth, and M. Hausser. 2005. Determinants of action potential propagation in cerebellar Purkinje cell axons. J. Neurosci. 25:464-472.
15. Aizenman, C. D., and D. J. Linden. 1999. Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. J. Neurophysiol. 82:1697-1709.
16. Vassilev, P. M., T. Scheuer, and W. A. Catterall. 1988. Identification of an intracellular peptide segment involved in sodium channel inactivation. Science. 241:1658-1661.
17. Stuhmer, W., F. Conti, H. Suzuki, X. D. Wang, M. Noda, N. Yahagi, H. Kubo, and S. Numa. 1989. Structural parts involved in activation and inactivation of the sodium channel. Nature. 339:597-603.
18. Cannon, S. C. 1996. Sodium channel defects in myotonia and periodic paralysis. Annu. Rev. Neurosci. 19:141-164.
19. Baukrowitz, T., and G. Yellen. 1995. Modulation of K+ current by frequency and external [K+]: a tale of two inactivation mechanisms. Neuron. 15:951-960.
20. Townsend, C., and R. Horn. 1997. Effect of alkali metal cations on slow inactivation of cardiac Na+ channels. J. Gen. Physiol. 110:23-33.
21. Chen, Y., F. H. Yu, D. J. Surmeier, T. Scheuer, and W. A. Catterall. 2006. Neuromodulation of Na+ channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron. 49:409-420.
22. Schaller, K. L., and J. H. Caldwell. 2000. Developmental and regional expression of sodium channel isoform NaCh6 in the rat central nervous system. J. Comp. Neurol. 420:84-97.
23. Felts, P. A., S. Yokoyama, S. Dib-Hajj, J. A. Black, and S. G. Waxman. 1997. Sodium channel a-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res. Mol. Brain Res. 45:71-82.
24. Chung, Y. H., K. M. Joo, M. J. Kim, and C. I. Cha. 2003. Age-related changes in the distribution of Na(v)1.1 and Na(v)1.2 in rat cerebellum. Neuroreport. 14:841-845.
25. Vega-Saenz de Miera, E. C., B. Rudy, M. Sugimori, and R. Llinas. 1997. Molecular characterization of the sodium channel subunits expressed in mammalian cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA. 94:7059-7064.
26. Kuo, C. C., and S. Y. Liao. 2000. Facilitation of recovery from inactivation by external Na+ and location of the activation gate in neuronal Na+ channels. J. Neurosci. 20:5639-5646.
27. Raman, I. M., L. K. Sprunger, M. H. Meisler, and B. P. Bean. 1997. Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron. 19:881-891.
28. Grieco, T. M., and I. M. Raman. 2004. Production of resurgent current in NaV1.6-null Purkinje neurons by slowing sodium channel inactivation with beta-pompilidotoxin. J. Neurosci. 24:35-42.
29. Levin, S. I., Z. M. Khaliq, T. K. Aman, T. M. Grieco, J. A. Kearney, I. M. Raman, and M. H. Meisler. 2006. Impaired motor function in mice with cell-specific knockout of sodium channel Scn8a (NaV1.6) in cerebellar Purkinje neurons and granule cells. J. Neurophysiol. 96:785-793.
30. Zhou, W., and A. L. Goldin. 2004. Use-dependent potentiation of the Nav1.6 sodium channel. Biophys. J. 87:3862-3872.
31. Rush, A. M., S. D. Dib-Hajj, and S. G. Waxman. 2005. Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurones. J. Physiol. 564:803-815.
32. Do, M. T., and B. P. Bean. 2004. Sodium currents in subthalamic nucleus neurons from Nav1.6-null mice. J. Neurophysiol. 92:726-733.
33. Enomoto, A., J. M. Han, C. F. Hsiao, N. Wu, and S. H. Chandler. 2006. Participation of sodium currents in burst generation and control of membrane excitability in mesencephalic trigeminal neurons. J. Neurosci. 26:3412-3422.
34. Leao, R. N., M. M. Naves, K. E. Leao, and B. Walmsley. 2006. Altered sodium currents in auditory neurons of congenitally deaf mice. Eur. J. Neurosci. 24:1137-1146.
35. Cummins, T. R., and F. J. Sigworth. 1996. Impaired slow inactivation in mutant sodium channels. Biophys. J. 71:227-236.
36. Balser, J. R., H. B. Nuss, N. Chiamvimonvat, M. T. Perez-Garcia, E. Marban, and G. F. Tomaselli. 1996. External pore residue mediates slow inactivation in μ1 rat skeletal muscle sodium channels. J. Physiol. 494:431-442.
37. Todt, H., S. C. Dudley, Jr., J. W. Kyle, R. J. French, and H. A. Fozzard. 1999. Ultra-slow inactivation in μ1 Na+ channels is produced by a structural rearrangement of the outer vestibule. Biophys. J. 76:1335-1345.
38. Ong, B. H., G. F. Tomaselli, and J. R. Balser. 2000. A structural rearrangement in the sodium channel pore linked to slow inactivation and use dependence. J. Gen. Physiol. 116:653-662.
39. Struyk, A. F., and S. C. Cannon. 2002. Slow inactivation does not block the aqueous accessibility to the outer pore of voltage-gated Na channels. J. Gen. Physiol. 120:509-516.
40. Vedantham, V., and S. C. Cannon. 2000. Rapid and slow voltage-dependent conformational changes in segment IVS6 of voltage-gated Na(+) channels. Biophys. J. 78:2943-2958.
41. Westenbroek, R. E., D. K. Merrick, and W. A. Catterall. 1989. Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons. Neuron. 3:695-704.
42. Schaller, K. L., and J. H. Caldwell. 2003. Expression and distribution of voltage-gated sodium channels in the cerebellum. Cerebellum. 2:2-9.
43. Krzemien, D. M., K. L. Schaller, S. R. Levinson, and J. H. Caldwell. 2000. Immunolocalization of sodium channel isoform NaCh6 in the nervous system. J. Comp. Neurol. 420:70-83.
44. Khaliq, Z. M., N. W. Gouwens, and I. M. Raman. 2003. The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J. Neurosci. 23:4899-4912.
45. Van Wart, A., and G. Matthews. 2006. Impaired firing and cell-specific compensation in neurons lacking nav1.6 sodium channels. J. Neurosci. 26:7172-7180.
46. Yu, F. H., R. E. Westenbroek, I. Silos-Santiago, K. A. McCormick, D. Lawson, P. Ge, H. Ferriera, J. Lilly, P. S. DiStefano, W. A. Catterall, T. Scheuer, and R. Curtis. 2003. Sodium channel β4, a new disulfidelinked auxiliary subunit with similarity to β2. J. Neurosci. 23:7577-7585.
47. Chen, C., and S. C. Cannon. 1995. Modulation of Na+ channel inactivation by the β1 subunit: a deletion analysis. Pflugers Arch. 431:186-195.
48. Qu, Y., L. L. Isom, R. E. Westenbroek, J. C. Rogers, T. N. Tanada, K. A. McCormick, T. Scheuer, and W. A. Catterall. 1995. Modulation of cardiac Na+ channel expression in Xenopus oocytes by β1 subunits. J. Biol. Chem. 270:25696-25701.
49. Isom, L. L., D. S. Ragsdale, K. S. De Jongh, R. E. Westenbroek, B. F. Reber, T. Scheuer, and W. A. Catterall. 1995. Structure and function of the β 2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell. 83:433-442.
50. Qu, Y., R. Curtis, D. Lawson, K. Gilbride, P. Ge, P. S. DiStefano, I. Silos-Santiago, W. A. Catterall, and T. Scheuer. 2001. Differential modulation of sodium channel gating and persistent sodium currents by the β1, β2, and β3 subunits. Mol. Cell. Neurosci. 18:570-580.
51. Chen, C., V. Bharucha, Y. Chen, R. E. Westenbroek, A. Brown, J. D. Malhotra, D. Jones, C. Avery, P. J. Gillespie 3rd, K. A. Kazen-Gillespie, K. Kazarinova-Noyes, P. Shrager, T. L. Saunders, R. L. Macdonald, B. R. Ransom, T. Scheuer, W. A. Catterall, and L. L. Isom. 2002. Reduced sodium channel density, altered voltage dependence of inactivation, and increased susceptibility to seizures in mice lacking sodium channel β2-subunits. Proc. Natl. Acad. Sci. USA. 99:17072-17077.
52. Grieco, T. M., J. D. Malhotra, C. Chen, L. L. Isom, and I. M. Raman. 2005. Open-channel block by the cytoplasmic tail of sodium channel β4 as a mechanism for resurgent sodium current. Neuron. 45:233-244.
53. Carr, D. B., M. Day, A. R. Cantrell, J. Held, T. Scheuer, W. A. Catterall, and D. J. Surmeier. 2003. Transmitter modulation of slow, activitydependent alterations in sodium channel availability endows neurons with a novel form of cellular plasticity. Neuron. 39:793-806.
54. Plummer, N. W., J. Galt, J. M. Jones, D. L. Burgess, L. K. Sprunger, D. C. Kohrman, and M. H. Meisler. 1998. Exon organization, coding sequence, physical mapping, and polymorphic intragenic markers for the human neuronal sodium channel gene SCN8A. Genomics. 54:287-296.
55. Cantrell, A. R., and W. A. Catterall. 2001. Neuromodulation of Na+ channels: an unexpected form of cellular plasticity. Nat. Rev. Neurosci. 2:397-407.
56. Grissmer, S., and M. Cahalan. 1989. TEA prevents inactivation while blocking open K+ channels in human T lymphocytes. Biophys. J. 55:203-206.
57. Choi, K. L., R. W. Aldrich, and G. Yellen. 1991. Tetraethylammonium blockade distinguishes two inactivation mechanisms in voltage-activated K+ channels. Proc. Natl. Acad. Sci. USA. 88:5092-5095.
58. Hoshi, T., W. N. Zagotta, and R. W. Aldrich. 1991. Two types of inactivation in Shaker K+ channels: effects of alterations in the carboxy-terminal region. Neuron. 7:547-556.
59. Yellen, G., D. Sodickson, T. Y. Chen, and M. E. Jurman. 1994. An engineered cysteine in the external mouth of a K+ channel allows inactivation to be modulated by metal binding. Biophys. J. 66:1068-1075.
60. Khaliq, Z. M., and I. M. Raman. 2006. Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J. Neurosci. 26:1935-1944.
61. Czubayko, U., F. Sultan, P. Thier, and C. Schwarz. 2001. Two types of neurons in the rat cerebellar nuclei as distinguished by membrane potentials and intracellular fillings. J. Neurophysiol. 85:2017-2029.
62. McKay, B. E., M. L. Molineux, W. H. Mehaffey, and R. W. Turner. 2005. Kv1 K+ channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J. Neurosci. 25:1481-1492.
63. Aizenman, C. D., P. B. Manis, and D. J. Linden. 1998. Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron. 21:827-835.
64. Aizenman, C. D., and D. J. Linden. 2000. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat. Neurosci. 3:109-111.
65. Pugh, J. R., and I. M. Raman. 2006. Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron. 51:113-123.