Up-regulation of low-threshold tetrodotoxin-resistant Na + current via activation of a cyclic AMP/protein kinase A pathway in nociceptor-like rat dorsal root ganglion cells

Neuroscience

Volumn 186, Issue , 2011, Pages 13-20

  Scroggs, R S ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

A 803467; Hyperalgesia; Inflammation; NaV1.8; NaV1.9; Sensory neuron

Indexed keywords

A 803467; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; SEROTONIN; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; MEMBRANE CURRENT; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SODIUM CURRENT; SPINAL GANGLION; UPREGULATION;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; GANGLIA, SPINAL; MALE; MEMBRANE POTENTIALS; NOCICEPTORS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; TETRODOTOXIN; UP-REGULATION;

EID: 79957998071     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.046     Document Type: Article

References (32)

1. Akopian A.N., Sivilotti L., Wood J.N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 1996, 379:257-262.
2. Amaya F., Decosterd I., Samad T.A., Plumpton C., Tate S., Mannion R.J., Costigan M., Woolf C.J. Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2. Mol Cell Neurosci 2000, 15:331-342.
3. Amaya F., Wang H., Costigan M., Allchorne A.J., Hatcher J.P., Egerton J., Stean T., Morisset V., Grose D., Gunthorpe M.J., Chessell I.P., Tate S., Green P.J., Woolf C.J. The voltage-gated sodium channel Na(v)1.9 is an effector of peripheral inflammatory pain hypersensitivity. J Neurosci 2006, 26:12852-12860.
4. Baker M.D. Protein kinase C mediates up-regulation of tetrodotoxin-resistant, persistent Na+ current in rat and mouse sensory neurons. J Physiol 2005, 567(3):851-867.
5. Baker M.D., Chandra S.Y., Ding Y., Waxman S.G., Wood J.N. GTP-induced tetrodotoxin-resistant Na+ current regulates excitability in mouse and rat small diameter sensory neurones. J Physiol 2003, 548(3):373-382.
6. Black J.A., Waxman S.G. Molecular identities of two tetrodotoxin-resistant sodium channels in corneal axons. Exp Eye Res 2002, 75:193-199.
7. Blair N.T., Bean B.P. Role of tetrodotoxin-resistant Na+ current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 2003, 23:10338-10350.
8. Boess F.G., Martin I.L. Molecular biology of 5-HT receptors. Neuropharmacology 1994, 33:275-317.
9. Cardenas L.M., Cardenas C.G., Scroggs R.S. 5HT increases excitability of nociceptor-like rat dorsal root ganglion neurons via cAMP-coupled TTX-R Na+ channels. J Neurophysiol 2001, 86:241-248.
10. Cardenas C.G., Del Mar L.P., Scroggs R.S. Variation in serotonergic inhibition of calcium channel currents in four types of rat sensory neurons differentiated by membrane properties. J Neurophysiol 1995, 74:1870-1879.
11. Cardenas C.G., Del Mar L.P., Cooper B.Y., Scroggs R.S. 5HT4 receptors couple positively to tetrodotoxin-insensitive sodium channels in a subpopulation of capsaicin sensitive rat sensory neurons. J Neurosci 1997, 17:7181-7189.
12. Coggeshall R.E., Tate S., Carlton S.M. Differential expression of tetrodotoxin-resistant sodium channels NaV1.8 and NaV1.9 in normal and inflamed rats. Neuroscience letters 2004, 355:45-48.
13. Coste B., Osorio N., Padilla F., Crest M., Delmas P. Gating and modulation of presumptive NaV1.9 channels in enteric and spinal sensory neurons. Mol Cell Neurosci 2004, 26:123-134.
14. Cummins T.R., Dib-Hajj S.D., Black J.A., Akopian A.K., Wood J.N., Waxman S.G. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 1999, 19(RC43):1-6.
15. d'Alcantara P., Cardenas L.M., Swillens S., Scroggs R.S. Reduced transition between open and inactivated channel states underlies 5HT increased INa+ in rat nociceptors. Biophys J 2002, 83:5-21.
16. Fang X., Djouhri L., Black J.A., Dib-Hajj S.D., Waxman S.G., Lawson S.N. The presence and role of the tetrodotoxin-resistant sodium channel NaV1.9 in nociceptive primary afferent neurons. J Neurosci 2002, 22:7425-7433.
17. Gold M.S., Zhang L., Wrigley D.L., Traub R.J. Prostaglandin E2 modulates TTX-R INa in rat colonic sensory neurons. J Neurophysiol 2002, 88:1512-1522.
18. Herzog R.I., Cummins T.R., Waxman S.G. Persistent TTX-resistant Na+ current affects resting potential and response to depolarization in simulated spinal sensory neurons. J Neurophysiol 2001, 86:1351-1364.
19. Jarvis M.E., Honore P., Shieh C., Chapman M., Joshi S., Zhang X.F., Kort M., Carroll W., Marron B., Atkinson R., Thomas J., Liu D., Krambis M., Liu Y., McGaraughty S., Chu K., Roeloffs R., Zhong C., Mikusa J.P., Hernandez G., Gauvin D., Wade C., Zhu C., Pai M., Scanio M., Shi L., Drizin I., Gregg R., Matulenko M., Hakeem A., Gross M., Johnson M., Marsh K., Wagoner P.K., Sullivan J.P., Faltynek C.R., Krafte D.S. A-803467, a potent and selective NaV1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat. Proc Natl Acad Sci USA 2007, 104:8520-8525.
20. John V.H., Main M.J., Powell A.J., Gladwell Z.M., Hick C., Sidhu H.S., Clare J.J., Tate S., Trezise D.J. Heterologous expression and functional analysis of rat NaV1.8 (SNS) voltage-gated sodium channels in the dorsal root ganglion neuroblastoma cell line ND7-23. Neuropharmacology 2004, 46:425-438.
21. Keh S.M., Facer P., Simpson K.D., Sandhu G., Saleh H.A., Anand P. Increased nerve fiber expression of sensory sodium channels Nav1.7, Nav1.8, And Nav1.9 in rhinitis. Laryngoscope 2008, 118:573-579.
22. Maingret F., Coste B., Padilla F., Clerc N., Crest M., Korogod S.M., Delmas P. Inflammatory mediators increase NaV1.9 current and excitability in nociceptors through a coincident detection mechanism. J Gen Physiol 2008, 131:211-225.
23. Maruyama H., Yamamoto M., Matsutomi T., Zheng T., Nakata Y., Wood J.N., Ogata N. Electrophysiological characterization of the tetrodotoxin-resistant Na+ channel, NaV1.9, in mouse dorsal root ganglion neurons. Pflugers Arch 2004, 449:76-87.
24. Ostman J.A., Nassar M.A., Wood J.N., Baker M.D. GTP up-regulated persistent Na+ current and enhanced nociceptor excitability require NaV1.9. J Physiol 2008, 586(4):1077-1087.
25. Padilla F., Couble M.L., Coste B., Maingret F., Clerc N., Crest M., Ritter A.M., Magloire H., Delmas P. Expression and localization of the Nav1.9 sodium channel in enteric neurons and in trigeminal sensory endings: implication for intestinal reflex function and orofacial pain. Mol Cell Neurosci 2007, 35:138-152.
26. Priest B.T., Murphy B.A., Lindia J.A., Diaz C., Abbadie C., Ritter A.M., Liberator P., Iyer I.M., Kash S.F., Kohler M.G., Kaczorowski G.J., MacIntyre D.E., Martin W.J. Contribution of the tetrodotoxin-resistant voltage-gated sodium channel NaV1.9 to sensory transmission and nociceptive behavior. Proc Natl Acad Sci 2005, 102:9382-9387.
27. Rush A.M., Waxman S.G. PGE2 increases the tetrodotoxin-resistant NaV1.9 sodium current in mouse DRG neurons via G-proteins. Brain Res 2004, 1023:264-271.
28. Scroggs R.S. Serotonin upregulates low- and high-threshold tetrodotoxin-resistant sodium channels in the same subpopulation of rat nociceptors. Neuroscience 2010, 165:1293-1300.
29. Strickland A.M., Martindale J.C., Woodhams P.L., Reeve A.J., Chessell I.P., McQueen D.S. Changes in the expression of NaV1.7, NaV1.8 and NaV1.9 in a distinct population of dorsal root ganglia innervating the rat knee joint in a model of chronic inflammatory joint pain. Eur J Pain 2008, 12:564-572.
30. Tripathi P., Cardenas C.A., Cardenas C.G., Trujillo L., de Armendi A.J., Scroggs R.S. Analysis of the variation in use-dependent inactivation of tetrodotoxin-resistant Na+ currents recorded from rat sensory neurons. Neuroscience 2006, 143:923-938.
31. Warren C.A., Mok L., Gordon S., Fouad A.F., Gold M.S. Quantification of neural protein in extirpated tooth pulp. J Endod 2008, 34:7-10.
32. Wells J.E., Bingham V., Rowland K.C., Hatton J. Expression of Nav1.9 channels in human dental pulp and trigeminal ganglion. J Endod 2007, 33:1172-1176.