The presence and role of the tetrodotoxin-resistant sodium channel Nav1.9 (NaN) in nociceptive primary afferent neurons

Journal of Neuroscience

Volumn 22, Issue 17, 2002, Pages 7425-7433

  Fang, Xin ^a   Djouhri, Laiche ^a   Black, Joel A ^b,c   Dib Hajj, Sulayman D ^b,c   Waxman, Stephen G ^b,c   Lawson, Sally N ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

Action potential; Conduction velocity; DRG; Nav 1.9 (NaN); Pain; Sodium channel

Indexed keywords

SODIUM CHANNEL; TETRODOTOXIN;

AFFERENT NERVE GROUP 1; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DORSAL ROOT POTENTIAL; FEMALE; IMMUNOCYTOCHEMISTRY; MUSCLE SPINDLE AFFERENT NERVE; NERVE CONDUCTION; NERVE FIBER C; NOCICEPTION; NOCICEPTIVE RECEPTOR; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL;

EID: 0036759621     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-17-07425.2002     Document Type: Article

References (46)

1. Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257-262.
2. Amaya F, Decosterd I, Samad TA, Plumpton C, Tate S, Mannion RJ, Costigan M, Woolf CJ (2000) Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2. Mol Cell Neurosci 15:331-342.
3. Arbuckle JB, Docherty RJ (1995) Expression of tetrodotoxin-resistant sodium channels in capsaicin-sensitive dorsal root ganglion neurons of adult rats. Neurosci Lett 185:70-73.
4. Bessou P, Perl ER (1969) Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J Neurophysiol 32:1025-1043.
5. Black JA, Dib-Hajj S, McNabola K, Jeste S, Rizzo MA, Kocsis JD, Waxman SG (1996) Spinal sensory neurons express multiple sodium channel α-subunit mRNAs. Brain Res Mol Brain Res 43:117-131.
6. Caffrey JM, Eng DL, Black JA, Waxman SG, Kocsis JD (1992) Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res 592:283-297.
7. Catterall WA (1992) Cellular and molecular biology of voltage-gated sodium channels. Physiol Rev 72:S15-S48.
8. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN, Waxman SG (1999) A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 19:RC43:1-6.
9. Dib-Hajj SD, Tyrrell L, Black JA, Waxman SG (1998) NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci USA 95:8963-8968.
10. Djouhri L, Lawson SN (1999) Changes in somatic action potential shape in guinea-pig nociceptive primary afferent neurones during inflammation in vivo. J Physiol (Lond) 520[Pt 2]:565-576.
11. Djouhri L, Lawson SN (2001a) Increased conduction velocity of nociceptive primary afferent neurons during unilateral hindlimb inflammation in the anaesthetized guinea-pig. Neuroscience 102:669-679.
12. Djouhri L, Lawson SN (2001b) Differences in the size of the somatic action potential overshoot between nociceptive and non-nociceptive dorsal root ganglion neurons in the guinea-pig. Neuroscience 108:479-491.
13. Djouhri L, Bleazard L, Lawson SN (1998) Association of somatic action potential shape with sensory receptive properties in guinea pig dorsal root ganglion neurons. J Physiol (Lond) 513:857-872.
14. Elliott AA, Elliott JR (1993) Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol (Lond) 463:39-56.
15. Fjell J, Hjelmstrom P, Hormuzdiar W, Milenkovic M, Aglieco F, Tyrrell L, Dib-Hajj S, Waxman SG, Black JA (2000) Localization of the tetrodotoxin-resistant sodium channel NaN in nociceptors. NeuroReport 11:199-202.
16. Gallego R (1983) The ionic basis of action potentials in petrosal ganglion cells of the cat. J Physiol (Lond) 342:591-602.
17. Gee MD, Lynn B, Cotsell B (1996) Activity-dependent slowing of conduction velocity provides a method for identifying different functional classes of C-fibre in the rat saphenous nerve. Neuroscience 73:667-675.
18. Gee MD, Lynn B, Basile S, Pierau FK, Cotsell B (1999) The relationship between axonal spike shape and functional modality in cutaneous C-fibres in the pig and rat. Neuroscience 90:509-518.
19. Gold MS (1999) Inflammatory mediator-induced modulation of TTX-R INa: An underlying mechanism of inflammatory hyperalgesia. Proc West Pharmacol Soc 42:111-112.
20. Goldin AL, Barchi RL, Caldwell JH, Hofmann F, Howe JR, Hunter JC, Kallen RG, Mandel G, Meisler MH, Netter YB, Noda M, Tamkun MM, Waxman SG, Wood JN, Catterall WA (2000) Nomenclature of voltage-gated sodium channels. Neuron 28:365-368.
21. Handwerker HO, Kilo S, Reeh PW (1991) Unresponsive afferent nerve fibres in the sural nerve of the rat. J Physiol (Lond) 435:229-242.
22. Harper AA, Lawson SN (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglia. J Physiol (Lond) 359:31-46.
23. + current affects resting potential and response to depolarization in simulated spinal sensory neurons. J Neurophysiol 86:1351-1364.
24. Koerber HR, Mendell LM (1992) Functional heterogeneity of dorsal root ganglion cells. In: Sensory Neurons: Diversity, Development and Plasticity (Scott SA, ed), pp 77-96. Oxford: Oxford UP.
25. Kostyuk PG, Veselovsky NS, Tsyndrenko AY (1981) Ionic currents in the somatic membrane of rat dorsal root ganglion neurons. I. Sodium currents. Neuroscience 6:2423-2430.
26. Lawson SN (2002) Phenotype and function of somatic primary afferent nociceptive neurons with C-, Aδ-, or Aα/β-fibres. J Exp Physiol 87:239-244.
27. Lawson SN, Harper AA, Harper EI, Garson JA, Anderton BH (1984) A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurons. J Comp Neurol 228:263-272.
28. Lawson SN, Crepps BA, Perl ER (1997) Relationship of substance P to afferent characteristics of dorsal root ganglion neurones in guinea pig. J Physiol (Lond) 505:177-191.
29. Light AR, Perl ER (1993) Peripheral sensory systems. In: Peripheral Neuropathy (Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF, eds), pp 149-165. Philadelphia: Saunders.
30. v1.9/NaN to the cell membrane. J Biol Chem 276:46553-46561.
31. McCleskey EW, Gold MS (1999) Ion channels of nociception. Annu Rev Physiol 61:835-856.
32. Meyer RA, Davis KD, Cohen RH, Treede RD, Campbell JN (1991) Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey. Brain Res 561:252-261.
33. Renganathan M, Cummins TR, Hormuzdiar WN, Waxman SG (2000) α-SNS produces the slow TTX-resistant sodium current in large cutaneous afferent DRG neurons. J Neurophysiol 84:710-718.
34. Ritter AM, Mendell LM (1992) Somal membrane properties of physiologically identified sensory neurons in the rat: Effects of nerve growth factor. J Neurophysiol 68:2033-2041.
35. Roy ML, Narahashi T (1992) Differential properties of tetrodotoxinsensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J Neurosci 12:2104-2111.
36. Rush AM, Brau ME, Elliott AA, Elliott JR (1998) Electrophysiological properties of sodium current subtypes in small cells from adult rat dorsal root ganglia. J Physiol (Lond) 511:771-789.
37. Sangameswaran L, Delgado SG, Fish LM, Koch BD, Jakeman LB, Stewart GR, Sze P, Hunter JC, Eglen RM, Herman RC (1996) Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J Biol Chem 271:5953-5956.
38. Sangameswaran L, Fish LM, Koch BD, Rabert DK, Delgado SG, Ilnicka M, Jakeman LB, Novakovic S, Wong K, Sze P, Tzoumaka E, Stewart GR, Herman RC, Chan H, Eglen RM, Hunter JC (1997) A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J Biol Chem 272:14805-14809.
39. Schmidt RF (1996) The articular polymodal nociceptor in health and disease. Prog Brain Res 113:53-81.
40. Sleeper AA, Cummins TR, Dib-Hajj SD, Hormuzdiar W, Tyrrell L, Waxman SG, Black JA (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.
41. Stefanini M, De Martino C, Zamboni L (1967) Fixation of ejaculated spermatozoa for electron microscopy. Nature 216:173-175.
42. Tate S, Benn S, Hick C, Trezise D, John V, Mannion RJ, Costigan M, Plumpton C, Grose D, Gladwell Z, Kendall G, Dale K, Bountra C, Woolf CJ (1998) Two sodium channels contribute to the TTX-R sodium current in primary sensory neurons. Nat Neurosci 1:653-655.
43. v1.9/NaN in dorsal root ganglion neurons and is developmentally regulated. J Neurosci 21:9629-9637.
44. Waddell PJ, Lawson SN (1990) Electrophysiological properties of sub-populations of rat dorsal root ganglion neurons in vitro. Neuroscience 36:811-822.
45. Waddell PJ, Lawson SN, McCarthy PW (1989) Conduction velocity changes along the processes of rat primary sensory neurons. Neuroscience 30:577-584.
46. Waxman SG (1999) The molecular pathophysiology of pain: Abnormal expression of sodium channel genes and its contributions to hyperexcitability of primary sensory neurons. Pain [Suppl] 6:S133-S140.