Calmodulin regulates current density and frequency-dependent inhibition of sodium channel Nav1.8 in DRG neurons

Journal of Neurophysiology

Volumn 96, Issue 1, 2006, Pages 97-108

  Choi, Jin Sung ^a,b   Hudmon, Andy ^a,b   Waxman, Stephen G ^a,b   Dib Hajj, Sulayman D ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; CALMODULIN BINDING PROTEIN; CALMODULIN INHIBITOR; GLUTAMINE; ISOLEUCINE; MUTANT PROTEIN; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; IMMUNOPRECIPITATION; IN VIVO STUDY; MALE; MEMBRANE CURRENT; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; SPINAL GANGLION;

ACTION POTENTIALS; ANIMALS; CALMODULIN; CALMODULIN-BINDING PROTEINS; CELLS, CULTURED; ELECTROPHYSIOLOGY; GANGLIA, SPINAL; GLUTAMINE; ISOLEUCINE; MALE; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNELS;

EID: 33745737497     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00854.2005     Document Type: Article

References (37)

1. Akopian AN, Sivilotti L, and Wood JN. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379: 257-262, 1996.
2. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S, Hill R, Stanfa LC, Dickenson AH, and Wood JN. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 2: 541-548, 1999.
3. Black JA, Dib-Hajj S, McNabola K, Jeste S, Rizzo MA, Kocsis JD, and Waxman SG. Spinal sensory neurons express multiple sodium channel alpha-subunit mRNAs. Mol Brain Res 43: 117-131, 1996.
4. 2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 22: 10277-10290, 2002.
5. + current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 23: 10338-10350, 2003.
6. Cardenas CA, Tripathi PK, Cardenas CG, de Armendi AJ, and Scroggs RS. Inactivation properties of use-dependent and use-resistant Nav1.8-like sodium currents in rat nociceptors. Soc Neurosci Abstr 62: 5, 2004.
7. Cummins TR, Aglieco F, Renganathan M, Herzog RI, Dib-Hajj SD, and Waxman SG. 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, 2001.
8. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN, and Waxman SG. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 19: RC43, 1999.
9. Cummins TR and Waxman SG. 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, 1997.
10. Deschenes I, Neyroud N, DiSilvestre D, Marban E, Yue DT, and Tomaselli GF. Isoform-specific modulation of voltage-gated Na(+) channels by calmodulin. Circ Res 90: E49-E57, 2002.
11. Dib-Hajj SD, Rush AM, Cummins TR, Hisama FM, Novella S, Tyrrell L, Marshall L, and Waxman SG. Gain-of-function mutation in Nav1.7 in familial erythromelalgia induces bursting of sensory neurons. Brain 128: 1847-1854, 2005.
12. Djouhri L, Fang X, Okuse K, Wood JN, Berry CM, and Lawson S. The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol 550: 739-752, 2003.
13. Elliott AA and Elliott JR. Characterization of TTX-sensitive and TTXresistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol 463: 39-56, 1993.
14. Erickson MG, Alseikhan BA, Peterson BZ, and Yue DT. Preassociation of calmodulin with voltage-gated Ca(2+) channels revealed by FRET in single living cells. Neuron 31: 973-985, 2001.
15. Garrido JJ, Fernandes F, Giraud P, Mouret I, Pasqualini E, Fache MP, Jullien F, and Dargent B. Identification of an axonal determinant in the C-terminus of the sodium channel Na(v)1.2. EMBO J 20: 5950-5961, 2001.
16. Hanley RM, Means AR, Ono T, Kemp BE, Burgin KE, Waxham N, and Kelly PT. Functional analysis of a complementary DNA for the 50-kilodalton subunit of calmodulin kinase II. Science 237: 293-297, 1987.
17. Herzog RI, Cummins TR, Ghassemi F, Dib-Hajj SD, and Waxman SG. Distinct repriming and closed-state inactivation kinetics of Nav1.6 and Nav1.7 sodium channels in mouse spinal sensory neurons. J Physiol 551: 741-750, 2003a.
18. Herzog RI, Liu C, Waxman SG, and Cummins TR. Calmodulin binds to the C terminus of sodium channels Nav1.4 and Nav1.6 and differentially modulates their functional properties. J Neurosci 23: 8261-8270, 2003b.
19. 2+ sensitivity of sodium channels. J Biol Chem 279: 45004-45012, 2004.
20. Liu C, Cummins TR, Tyrrell L, Black JA, Waxman SG, and Dib-Hajj SD. CAP-1A is a novel linker that binds clathrin and the voltage-gated sodium channel Na(v)1.8. Mol Cell Neurosci 28: 636-649, 2005.
21. Malik-Hall M, Poon WY, Baker MD, Wood JN, and Okuse K. Sensory neuron proteins interact with the intracellular domains of sodium channel Na(V)1.8. Mol Brain Res 110: 298-304, 2003.
22. 2+-sensitivity? Biochemistry 39: 1316-1323, 2000.
23. Ohya Y, Uno I, Ishikawa T, and Anraku Y. Purification and biochemical properties of calmodulin from Saccharomyces cerevisiae. Eur J Biochem 168: 13-19, 1987.
24. Payne ME, Fong YL, Ono T, Colbran RJ, Kemp BE, Soderling TR, and Means AR. Calcium/calmodulin-dependent protein kinase II. Characterization of distinct calmodulin binding and inhibitory domains. J Biol Chem 263: 7190-7195, 1988.
25. Renganathan M, Cummins TR, and Waxman SG. Contribution of Nav1.8 sodium channels to action potential electrogenesis in DRG neurons. J Neurophysiol 86: 629-640, 2001.
26. Rhoads AR and Friedberg F. Sequence motifs for calmodulin recognition. FASEB J 11: 331-340, 1997.
27. Rizzo MA, Kocsis JD, and Waxman SG. Slow sodium conductances of dorsal root ganglion neurons: intraneuronal homogeneity and interneuronal heterogeneity. J Neurophysiol 72: 2796-2815, 1994.
28. Rush AM, Brau ME, Elliott AA, and Elliott JR. Electrophysiological properties of sodium current subtypes in small cells from adult rat dorsal root ganglia. J Physiol 511: 771-789, 1998.
29. Rush AM, Dib-Hajj SD, and Waxman SG. Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurons. J Physiol 564: 803-815, 2005.
30. Sangameswaran L, Delgado SG, Fish LM, Koch BD, Jakeman LB, Stewart GR, Sze P, Hunter JC, Eglen RM, and Herman RC. Structure and function of a novel voltage-gated, tetrodoxtoxin-resistant sodium channel specific to sensory neurons. J Biol Chem 271: 5953-5956, 1996.
31. Tan HL, Kupershmidt S, Zhang R, Stepanovic S, Roden DM, Wilde AA, Anderson ME, and Balser JR. A calcium sensor in the sodium channel modulates cardiac excitability. Nature 415: 442-447, 2002.
32. Waxham MN, Tsai AL, and Putkey JA. A mechanism for calmodulin (CaM) trapping by CaM-kinase II defined by a family of CaM-binding peptides. J Biol Chem 273: 17579-17584, 1998.
33. Wood JN, Boorman JP, Okuse K, and Baker MD. Voltage-gated sodium channels and pain pathways. J Neurobiol 61: 55-71, 2004.
34. Wood JN and Waxman SG. New molecular targets for the treatment of neuropathic pain. In: From Neuroscience to Neurology: Neuroscience, Molecular Medicine and the Therapeutic Transformation of Neurology, edited by Waxman SG. Amsterdam: Elsevier Academic, 2005, p. 339-355.
35. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, Ishii T, Hirschberg B, Bond CT, Lutsenko S, Maylie J, and Adelman JP. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395: 503-507, 1998.
36. Young KA and Caldwell JH. Modulation of skeletal and cardiac voltage-gated sodium channels by calmodulin. J Physiol 565: 349 -370, 2005.
37. Zuhlke RD, Pitt GS, Deisseroth K, Tsien RW, and Reuter H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 399: 159-162, 1999.