Regulatory role of voltage-gated Na+ channel β subunits in sensory neurons

Frontiers in Pharmacology

Volumn 2 NOV, Issue , 2011, Pages

  Chahine, Mohamed ^a,b   O'Leary, Michael E ^c  

^a CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

; Pain; peripheral nervous system; Subunit; Voltage gated sodium channel

Indexed keywords

NEUROTOXIN; VOLTAGE GATED SODIUM CHANNEL BETA 1 SUBUNIT; VOLTAGE GATED SODIUM CHANNEL BETA 2 SUBUNIT;

ACTION POTENTIAL; ARTICLE; CELL POPULATION; CELLULAR DISTRIBUTION; CHANNEL GATING; CYTOSKELETON; EXTRACELLULAR MATRIX; HUMAN; MOLECULAR CLONING; MYELINATION; NERVE EXCITABILITY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SENSORY GATING; SENSORY NERVE CELL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

EID: 84858203214     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2011.00070     Document Type: Article

References (79)

1. Akopian, A. N., Sivilotti, L.,and Wood, J. N. (1996). A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379, 257-262.
2. Aman, T. K., Grieco-Calub, T. M., Chen, C., Rusconi, R., Slat, E. A., Isom, L. L., and Raman, I. M. (2009). Regulation of persistent Na current by interactions between beta subunits of voltage-gated Na channels. J. Neurosci. 29, 2027-2042.
3. Amaya, F., Decosterd, I., Samad, T. A., Plumpton, C., Tate, S., Mannion, R. J., Costigan, M., and Woolf, C. J. (2000). Diversity of expression of the sensory neuron-specific TTXresistant voltage-gated sodium ion channels SNS and SNS2. Mol. Cell. Neurosci. 15, 331-342.
4. + channel α?subunit with novel gating properties. Neuron 1, 449-461.
5. Bant, J. S., and Raman, I. M. (2010). Control of transient, resurgent, and persistent current by open-channel block by Na channel beta4 in cultured cerebellar granule neurons. Proc. Natl. Acad. Sci. U.S.A. 107, 12357-12362.
6. Black, J. A., Cummins, T. R., Plumpton, C., Chen, Y. H., Hormuzdiar, W., Clare, J. J., and Waxman, S. G. (1999). Upregulation of a silent sodium channel after peripheral, but not central, nerve injury in DRG neurons. J. Neurophysiol. 82, 2776-2785.
7. Black, J. A., Dib-Hajj, S., McNabola, K., Jeste, S., Rizzo, M. A., Kocsis, J. D., and Waxman, S. G. (1996). Spinal sensory neurons express multiple sodium channel alpha-subunit mRNAs. Brain Res. Mol. Brain Res. 43, 117-131.
8. Brackenbury, W. J., Djamgoz, M. B., and Isom, L. L. (2008). An emerging role for voltage-gated Na+ channels in cellular migration: regulation of central nervous system development and potentiation of invasive cancers. Neuroscientist 14, 571-583.
9. Casula, M. A., Facer, P., Powell, A. J., Kinghorn, I. J., Plumpton, C., Tate, S. N., Bountra, C., Birch, R., and Anand, P. (2004). Expression of the sodium channel β3 subunit in injured human sensory neurons. Neuroreport 15, 1629-1632.
10. Catterall, W. A. (2000). From ionic currents to molecular mechanisms: the structure and function of voltagegated sodium channels. Neuron 26, 13-25.
11. Catterall, W. A., Goldin, A. L., and Waxman, S. G. (2003). International Union of Pharmacology. XXXIX. Compendium of voltage-gated ion channels: sodium channels. Pharmacol. Rev. 55, 575-578.
12. Catterall, W. A., Goldin, A. L., and Waxman, S. G. (2005). International Union of Pharmacology. XLVII. Nomenclature and structurefunction relationships of voltagegated sodium channels. Pharmacol. Rev. 57, 397-409.
13. Chahine, M., Chatelier, A., Babich, O., and Krupp, J. J. (2008). Voltagegated sodium channels in neurological disorders. CNS Neurol. Disord. Drug Targets 7, 144-158.
14. Chahine, M., Ziane, R., Vijayaragavan, K., and Okamura, Y. (2005). Regulation of Na(v) channels in sensory neurons. Trends Pharmacol. Sci. 26, 496-502.
15. Chen, C., Westenbroek, R. E., Xu, X., Edwards, C. A., Sorenson, D. R., Chen, Y., McEwen, D. P., O'Malley, H. A., Bharucha, V., Meadows, L. S., Knudsen, G. A., Vilaythong, A., Noebels, J. L., Saunders, T. L., Scheuer, T., Shrager, P., Catterall, W. A., and Isom, L. L. (2004). Mice lacking sodium channel β1 subunits display defects in neuronal excitability, sodium channel expression, and nodal architecture. J. Neurosci. 24, 4030-4042.
16. Chen, Y., Yu, F. H., Sharp, E. M., Beacham, D., Scheuer, T.,and Catterall, W. A. (2008). Functional properties and differential neuromodulation of Na(v)1.6 channels. Mol. Cell. Neurosci. 38, 607-615.
17. Coward, K., Jowett, A., Plumpton, C., Powell, A., Birch, R., Tate, S., Bountra, C., and Anand, P. (2001). Sodium channel β1 and β2 subunits parallel SNS/PN3 αsubunit changes in injured human sensory neurons. Neuroreport 12, 483-488.
18. Cummins, T. R., Aglieco, F., Renganathan, M., Herzog, R. I., Dib-Hajj, S. D., and Waxman, S. G. (2001). Nav1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons. J. Neurosci. 21, 5952-5961.
19. Cummins, T. R., Dib-Hajj, S. D., Herzog, R. I., and Waxman, S. G. (2005). Nav1.6 channels generate resurgent sodium currents in spinal sensory neurons. FEBS Lett. 579, 2166-2170.
20. Cummins, T. R., Sheets, P. L., and Waxman, S. G. (2007). The roles of sodium channels in nociception:implications for mechanisms of pain. Pain 131, 243-257.
21. Cummins, T. R., and Waxman, S. G. (1997). Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J. Neurosci. 17, 3503-3514.
22. Dib-Hajj, S., Black, J. A., Felts, P., and Waxman, S. G. (1996). Downregulation of transcripts for Na channel α-SNS in spinal sensory neurons following axotomy. Proc. Natl. Acad. Sci. U.S.A. 93, 14950-14954.
23. Dib-Hajj, S. D., Black, J. A., Cummins, T. R., Kenney, A. M., Kocsis, J. D., and Waxman, S. G. (1998). Rescue of α-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo. J. Neurophysiol. 79, 2668-2676.
24. Dib-Hajj, S. D., Fjell, J., Cummins, T. R., Zheng, Z., Fried, K., LaMotte, R., Black, J. A., and Waxman, S. G. (1999). Plasticity of sodium channel expression in DRG neurons in the chronic constriction injury model of neuropathic pain. Pain 83, 591-600.
25. Do, M. T., and Bean, B. P. (2004). Sodium currents in subthalamic nucleus neurons from Nav1.6-null mice. J. Neurophysiol. 92, 726-733.
26. Fertleman, C. R., Baker, M. D., Parker, K. A., Moffatt, S., Elmslie, F. V., Abrahamsen, B., Ostman, J., Klugbauer, N., Wood, J. N., Gardiner, R. M., and Rees, M. (2006). SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52, 767-774.
27. Fukuoka, T., Kobayashi, K., Yamanaka, H., Obata, K., Dai, Y., and Noguchi, K. (2008). Comparative study of the distribution of the alpha-subunits of voltage-gated sodium channels in normal and axotomized rat dorsal root ganglion neurons. J. Comp. Neurol. 510, 188-206.
28. Gastaldi, M., Robaglia-Schlupp, A., Massacrier, A., Planells, R., and Cau, P. (1998). mRNA coding for voltagegated sodium channel beta2 subunit in rat central nervous system: cellular distribution and changes following kainate-induced seizures. Neurosci. Lett. 249, 53-56.
29. Grieco, T. M., Afshari, F. S., and Raman, I. M. (2002). A role for phosphorylation in the maintenance of resurgent sodium current in cerebellar Purkinje neurons. J. Neurosci. 22, 3100-3107.
30. Grieco, T. M., Malhotra, J. D., Chen, C., Isom, L. L., and Raman, I. M. (2005). Open-channel block by the cytoplas-mic tail of sodium channel β4as a mechanism for resurgent sodium current. Neuron 45, 233-244.
31. Grieco, T. M., and Raman, I. M. (2004). Production of resurgent current in NaV1.6-null Purkinje neurons by slowing sodium channel inactivation with beta-pompilidotoxin. J. Neurosci. 24, 35-42.
32. Ho, C., and O'Leary, M. E. (2011). Single-cell analysis of sodium channel expression in dorsal root ganglion neurons. Mol. Cell. Neurosci. 46, 159-166.
33. Ho, C., Zhao, J., Malinowski, S., Chahine, M., and O'Leary, M. E. (2011). Differential expression of sodium channel β subunits and Na channel regulation in subpopulations of dorsal root ganglion sensory neurons. Society of Neurosciences Meeting.
34. Huth, T., Rittger, A., Saftig, P., and Alzheimer, C. (2011). beta-Site APPcleaving enzyme 1 (BACE1) cleaves cerebellar Na+ channel beta4subunit and promotes Purkinje cell firing by slowing the decay of resurgent Na+ current. Pflugers Arch. 461, 355-371.
35. Isom, L. L. (2001). Sodium channel beta subunits: anything but auxiliary. Neuroscientist 7, 42-54.
36. Isom, L. L. (2002). β subunits: players in neuronal hyperexcitability? Novartis Found. Symp. 241, 124-138.
37. Isom, L. L., De Jongh, K. S., Patton, D. E., Reber, B. F., Offord, J., Charbonneau, H., Walsh, K., Goldin, A. L., and Catterall, W. A. (1992). Primary structure and functional expression of the β1 subunit of the rat brain sodium channel. Science 256, 839-842.
38. Isom, L. L., Ragsdale, D. S., De Jongh, K. S., Westenbroek, R. E., Reber, B. F. X., Scheuer, T., and Catterall, W. A. (1995). Structure and function of the β2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell 83, 433-442.
39. Jarecki, B. W., Piekarz, A. D., Jackson, J. O., and Cummins, T. R. (2010). Human voltage-gated sodium channel mutations that cause inherited neuronal and muscle channelopathies increase resurgent sodium currents. J. Clin. Invest. 120, 369-378.
40. Jarecki, B. W., Sheets, P. L., Jackson, J. O., and Cummins, T. R. (2008). Paroxysmal extreme pain disorder mutations within the D3/S4-S5 linker of Nav1.7 cause moderate destabilization of fast inactivation. J. Physiol. 586, 4137-4153.
41. Kazen-Gillespie, K. A., Ragsdale, D. S., D'Andrea, M. R., Mattei, L. N., Rogers, K. E., and Isom, L. L. (2000). Cloning, localization, and functional expression of sodium channel β1A subunits. J. Biol. Chem. 275, 1079-1088.
42. Kim, C. H., Oh, Y., Chung, J. M., and Chung, K. (2001). The changes in expression of three subtypes of TTX sensitive sodium channels in sensory neurons after spinal nerve ligation. Brain Res. Mol. Brain Res. 95, 153-161.
43. Kim, C. H., Oh, Y., Chung, J. M., and Chung, K. (2002). Changes in three subtypes of tetrodotoxin sensitive sodium channel expression in the axotomized dorsal root ganglion in the rat. Neurosci. Lett. 323, 125-128.
44. Krafte, D. S., Snutch, T. P., Leonard, J. P., Davidson, N., and 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 in Xenopus oocytes. J. Neurosci. 8, 2859-2868.
45. Krzemien, D. M., Schaller, K. L., Levinson, S. R., and Caldwell, J. H. (2000). Immunolocalization of sodium channel isoform NaCh6 in the nervous system. J. Comp. Neurol. 420, 70-83.
46. + channel Scn1b gene regulates dorsal root ganglion nociceptor excitability in vivo. J. Biol. Chem. 286, 22913-22923.
47. Lopez-Santiago, L. F., Meadows, L. S., Ernst, S. J., Chen, C., Malhotra, J. D., McEwen, D. P., Speelman, A., Noebels, J. L., Maier, S. K., Lopatin, A. N.,and Isom, L. L. (2007). Sodium channel Scn1b null mice exhibit prolonged QT and RR intervals. J. Mol. Cell. Cardiol. 43, 636-647.
48. Lopez-Santiago, L. F., Pertin, M., Morisod, X., Chen, C., Hong, S., Wiley, J., Decosterd, I., and Isom, L. L. (2006). Sodium channel β2 subunits regulate tetrodotoxin-sensitive sodium channels in small dorsal root ganglion neurons and modulate the response to pain. J. Neurosci. 26, 7984-7994.
49. Morgan, K., Stevens, E. B., Shah, B., Cox, P. J., Dixon, A. K., Lee, K., Pinnock, R. D., Hughes, J., Richardson, P. J., Mizuguchi, K., and Jackson, A. P. (2000). β3: an additional auxiliary subunit of the voltagesensitive sodium channel that modulates channel gating with distinct kinetics. Proc. Natl. Acad. Sci. U.S.A. 97, 2308-2313.
50. + channel β1 subunit mRNA: differential expression in rat spinal sensory neurons. Brain Res. Mol. Brain Res. 30, 357-361.
51. O'Leary, M. E. (1998). Characterization of the isoform-specific differences in the gating of neuronal and muscle sodium channels. Can. J. Physiol. Pharmacol. 76, 1041-1050.
52. Patino, G. A., Claes, L. R., LopezSantiago, L. F., Slat, E. A., Dondeti, R. S., Chen, C., O'Malley, H. A., Gray, C. B., Miyazaki, H., Nukina, N., Oyama, F., De, J. P., and Isom, L. L. (2009). A functional null mutation of SCN1B in a patient with Dravet syndrome. J. Neurosci. 29, 10764-10778.
53. Pertin, M., Ji, R. R., Berta, T., Powell, A. J., Karchewski, L., Tate, S. N., Isom, L. L., Woolf, C. J., Gilliard, N., Spahn, D. R., and Decosterd, I. (2005). Upregulation of the voltagegated sodium channel β2 subunit in neuropathic pain models: characterization of expression in injured and non-injured primary sensory neurons. J. Neurosci. 25, 10970-10980.
54. Qin, N., D'Andrea, M. R., Lubin, M. L., Shafaee, N., Codd, E. E., and Correa, A. M. (2003). Molecular cloning and functional expression of the human sodium channel β1B subunit,a novel splicing variant of the β1 subunit. Eur. J. Biochem. 270, 4762-4770.
55. Qu, Y., Curtis, R., Lawson, D., Gilbride, K., Ge, P., Distefano, P. S., SilosSantiago, I., Catterall, W. A., and Scheuer, T. (2001). Differential modulation of sodium channel gating and persistent sodium currents by the β1,β2,and β3 subunits. Mol. Cell. Neurosci. 18, 570-580.
56. Raman, I. M., and Bean, B. P. (1997). Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci. 17, 4517-4526.
57. Raman, I. M., and Bean, B. P. (1999). Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J. Neurosci. 19, 1663-1674.
58. Raman, I. M., and Bean, B. P. (2001). Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys. J. 80, 729-737.
59. Raman, I. M., Sprunger, L. K., Meisler, M. H.,and Bean, B. P. (1997).Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19, 881-891.
60. Rush, A. M., Cummins, T. R., and Waxman, S. G. (2007). Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J. Physiol. 579, 1-14.
61. Sangameswaran, L., Delgado, S. G., Fish, L. M., Koch, B. D., Jakeman, L. B., Stewart, G. R., Sze, P., Hunter, J. C., Eglen, R. M., and Herman, R. C. (1996). Structure and function of a novel voltage-gated, tetrodotoxinresistant sodium channel specific to sensory neurons. J. Biol. Chem. 271, 5953-5956.
62. Shah, B. S., Stevens, E. B., Gonzalez, M. I., Bramwell, S., Pinnock, R. D., Lee, K., and Dixon, A. K. (2000). beta3, a novel auxiliary subunit for the voltage-gated sodium channel, is expressed preferentially in sensory neurons and is upregulated in the chronic constriction injury model of neuropathic pain. Eur. J. Neurosci. 12, 3985-3990.
63. Shah, B. S., Stevens, E. B., Pinnock, R. D., Dixon, A. K., and Lee, K. (2001). Developmental expression of the novel voltage-gated sodium channel auxiliary subunit β3, in rat CNS. J. Physiol. 534, 763-776.
64. Sleeper, A. A., Cummins, T. R., DibHajj, S. D., Hormuzdiar, W., Tyrrell, L., Waxman, S. G., and Black, J. A. (2000). Changes in expression of two tetrodotoxin-resistant sodium channels and their currents in dorsal root ganglion neurons after sciatic nerve injury but not rhizotomy. J. Neurosci. 20, 7279-7289.
65. Takahashi, N., Kikuchi, S., Dai, Y., Kobayashi, K., Fukuoka, T., and Noguchi, K. (2003). Expression of auxiliary beta subunits of sodium channels in primary afferent neurons and the effect of nerve injury. Neuroscience 121, 441-450.
66. Theile, J. W., and Cummins, T. R. (2011). Inhibition of Nav{beta}4 peptide-mediated resurgent sodium currents in Nav1.7 channels by carbamazepine, riluzole and anandamide. Mol. Pharmacol. 80, 724-734.
67. Theile, J. W., Jarecki, B. W., Piekarz, A. D., and Cummins, T. R. (2011). Nav1.7 mutations associated with paroxysmal extreme pain disorder, but not erythromelalgia, enhance Navbeta4 peptide-mediated resurgent sodium currents. J. Physiol. 589, 597-608.
68. Tzoumaka, E., Tischler, A. C., Sangameswaran, L., Eglen, R. M., Hunter, J. C., and Novakovic, S. D. (2000). Differential distribution of the tetrodotoxin-sensitive rPN4/NaCh6/Scn8a sodium channel in the nervous system. J. Neurosci. Res. 60, 37-44.
69. Ulzheimer, J. C., Peles, E., Levinson, S. R., and Martini, R. (2004). Altered expression of ion channel isoforms at the node of Ranvier in P0-deficient myelin mutants. Mol. Cell. Neurosci. 25, 83-94.
70. Vijayaragavan, K., O'Leary, M. E., and Chahine, M. (2001). Gating properties of Nav1.7 and Nav1.8 peripheral nerve sodium channels. J. Neurosci. 21, 7909-7918.
71. Vijayaragavan, K., Powell, A. J., Kinghorn, I. J., and Chahine, M. (2004). Role of auxiliary β1-, β2-, and β?-subunits and their interaction with Na(v)1.8 voltage-gated sodium channel. Biochem. Biophys. Res. Commun. 319, 531-540.
72. Watanabe, E., Fujikawa, A., Matsunaga, H., Yasoshima, Y., Sako, N., Yamamoto, T., Saegusa, C., and Noda, M. (2000). Nav2/NaG channel is involved in control of salt-intake behavior in the CNS. J. Neurosci. 20, 7743-7751.
73. Watanabe, U., Shimura, T., Sako, N., Kitagawa, J., Shingai, T., Watanabe, E., Noda, M., and Yamamoto, T. (2003). A comparison of voluntary salt-intake behavior in Nax-gene deficient and wild-type mice with reference to peripheral taste inputs. Brain Res. 967, 247-256.
74. Waxman, S. G., Kocsis, J. D., and Black, J. A. (1994). Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J. Neurophysiol. 72, 466-470.
75. + channel α subunits in a somatic cell line. Neuron 8, 59-70.
76. Yu, F. H., and Catterall, W. A. (2003). Overview of the voltage-gated sodium channel family. Genome Biol. 4, 207.
77. Yu, F. H., Mantegazza, M., Westenbroek, R. E., Robbins, C.A., Kalume, F., Burton, K. A., Spain, W. J., McKnight, G. S., Scheuer, T., and Catterall, W. A. (2006). Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat. Neurosci. 9, 1142-1149.
78. Yu, F. H., Westenbroek, R. E., SilosSantiago, I., McCormick, K. A., Lawson, D., Ge, P., Ferriera, H., Lilly, J., Distefano, P. S., Catterall, W. A., Scheuer, T., and Curtis, R. (2003). Sodium channel β4, a new disulfide-linked auxiliary subunit with similarity to β2. J. Neurosci. 23, 7577-7585.
79. + channels by auxiliary {beta}-subunits. J. Neurophysiol. 106, 608-619.