Electrophysiological evidence for tetrodotoxin-resistant sodium channels in slowly conducting dural sensory fibers

Journal of Neurophysiology

Volumn 81, Issue 2, 1999, Pages 413-424

  Strassman, A M ^a,c   Raymond, Strassman A ^b,c  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; MALE; NERVE CONDUCTION; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY GANGLION; SODIUM TRANSPORT;

EID: 0033062951     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.81.2.413     Document Type: Article

References (65)

1. AKOPIAN, A. N., SIVILOTTI, L., AND WOOD, J. N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379: 257-262, 1996.
2. ANDRES, K. H., VON DURING, M., MUSZYNSKI, K., AND SCHMIDT, R. F. Nerve fibres and their terminals of the dura mater encephali of the rat. Anat. Embryol. 175: 289-301, 1987.
3. ARBUCKLE, J. B. AND DOCHERTY, R. J. Expression of tetrodotoxin-resistant sodium channels in capsaicin-sensitive dorsal root ganglion neurons of adult rats. Neurosci. Lett. 185: 70-73, 1995.
4. BOSSU, J. L. AND FELTZ, A. Patch-clamp study of the tetrodotoxin-resistant sodium current in group C sensory neurones. Neurosci. Lett. 51: 241-246, 1984.
5. BURGESS, P. R. AND PERL, E. R. Myelinated afferent fibres responding specifically to noxious stimulation of the skin. J. Physiol. (Lond.) 190: 541-562, 1967.
6. CAFFREY, J. M., ENG, D. L., BLACK, J. A., WAXMAN, S. G., AND KOCSIS, J. D. Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res. 592: 283-297, 1992.
7. + currents in neurons from the guinea-pig jugular ganglion. J. Auton. Nerv. Syst. 56: 75-86, 1995.
8. COLQUHOUN, D. AND RITCHIE, J. M. The interaction at equilibrium between tetrodotoxin and mammalian non-myelinated nerve fibres. J. Physiol. (Lond.) 221: 533-553, 1972.
9. DICHTER, M. A. AND FISCHBACH, G. D. The action potential of chick dorsal root ganglion neurones maintained in cell culture. J. Physiol. (Lond.) 267: 281-298, 1977.
10. ELLIOTT, A. A. AND ELLIOTT, J. R. Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J. Physiol. (Lond.) 463: 39-56, 1993.
11. 2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurons via the cyclic AMP-protein kinase A cascade. J. Physiol. (Lond.) 495: 429-440, 1996.
12. GAUMANN, D. M., BRUNET, P. C., AND JIROUNEK, P. Clonidine enhances the effects of lidocaine on C-fiber action potential. Anesth. Analg. 74: 719-725, 1992.
13. GISSEN, A. J., COVINO, B. G., AND GREGUS, J. Differential sensitivities of mammalian nerve fibers to local anesthetic agents. Anesthesiology 53: 467-474, 1980.
14. GISSEN, A. J., COVINO, B. G., AND GREGUS, J. Differential sensitivity of fast and slow fibers in mammalian nerve. II. Margin of safety for nerve transmission. Anesth. Analg. 61: 561-569, 1982.
15. GOLD, M. S., DASTMALCHI, S., AND LEVINE, J. D. Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 71: 265-275, 1996a.
16. + current in nociceptors. Proc. Natl. Acad. Sci. USA 93: 1108-1112, 1996b.
17. GORKE, K. AND PIERAU, F. K. Spike potentials and membrane properties of dorsal root ganglion cells in pigeons. Pflügers Arch. 386: 21-28, 1980.
18. HEYER, E. AND MACDONALD, R. Calcium- and sodium-dependent action potentials of mouse spinal cord and dorsal root ganglion neurons in cell culture. J. Neurophysiol. 47: 641-655, 1982.
19. HOHEISEL, U., LEHMANN-WILLENBROCK, E., AND MENSE, S. Termination patterns of identified group II and III afferent fibres from deep tissues in the spinal cord of the cat. Neuroscience 28: 495-507, 1989.
20. HOHEISEL, U. AND MENSE, S. Observations on the morphology of axons and somata of slowly conducting dorsal root ganglion cells in the cat. Brain Res. 423: 269-278, 1987.
21. HORN, R. Propagating calcium spikes in an axon of Aplysia. J. Physiol. (Lond.) 281: 513-534, 1978.
22. HUANG, J. H., THALHAMMER, J. G., RAYMOND, S. A., AND STRICHARTZ, G. R. Susceptibility to lidocaine of impulses in different somatosensory afferent fibers of rat sciatic nerve. J. Pharmacol. Exp. Ther. 282: 802-811, 1997.
23. IKEDA, S. R. AND SCHOFIELD, G. G. Tetrodotoxin-resistant sodium current of rat nodose neurones: monovalent cation selectivity and divalent cation block. J. Physiol. (Lond.) 389: 255-270, 1987.
24. 2+ currents of acutely isolated adult rat nodose ganglion cells. J. Neurophysiol. 55: 527-539, 1986.
25. JEFTINUA, S. The role of tetrodotoxin-resistant sodium channels of small primary afferent fibers. Brain Res. 639: 125-134, 1994.
26. KIRCHHOFF, C., LEAH, J. D., JUNG, S., AND REEH, P. W. Excitation of cutaneous sensory nerve endings in the rat by 4-aminopyridine and tetraethylammonium. J. Neurophysiol. 67: 125-131, 1992.
27. KOSTYUK, P. G., VESELOVSKY, N. S., AND TSYNPRENKO, A. Y. Ionic currents in the somatic membrane of rat dorsal root ganglion neurons I. Sodium currents. Neuroscience 6: 2423-2430, 1981.
28. LIANG, Y.-F. AND TERASHIMA, S.-I. Physiological properties and morphological characteristics of cutaneous and mucosal mechanical nociceptive neurons with A-delta peripheral axons in the trigeminal ganglia of crotaline snakes. J. Comp. Neurol. 328: 88-102, 1993.
29. LIANG, Y.-F., TERASHIMA, S.-I., AND ZHU, A-Q. Distinct morphological characteristics of touch, temperature, and mechanical nociceptive neurons in the crotaline trigeminal ganglia. J. Comp. Neurol. 360: 621-633, 1995.
30. LIGHT, A. R. AND PERL, E. R. Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J. Comp. Neurol. 186: 133-150, 1979.
31. LYNN, B. AND CARPENTER, S. E. Primary afferent units from the hairy skin of the rat hind limb. Brain Res. 238: 29-43, 1982.
32. LYNN, B., FAULSTROH, K., AND PIERAU, F.-K. The classification and properties of nociceptive afferent units from the skin of the anaesthetized pig. Eur. J. Neurosci. 7: 431-437, 1995.
33. MATSUDA, Y., YOSHIDA, S., AND YONEZAWA, T. Tetrodotoxin sensitivity and Ca component of action potentials of mouse dorsal root ganglion cells cultured in vitro. Brain Res. 154: 69-82 1978.
34. MCLEAN, M. J., BENNETT, P. B., AND THOMAS, R. M. Subtypes of dorsal root ganglion neurons based on different inward currents as measured by whole-cell voltage clamp. Mol. Cell. Biochem. 80: 95-107, 1988.
35. MEYER, R. A., DAVIS, K. D., COHEN, R. H., TREEDE, R.-D., AND CAMPBELL, J. N. Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey. Brain Res. 561: 252-261, 1991.
36. NODA, K., UEDA, Y., SUZUKI, K., AND YODA, K. Excitatory effects of algesic compounds on neuronal processes in murine dorsal root ganglion cell culture. Brain Res. 751: 348-351, 1997.
37. NOVAKOVIC, S. D., TZOLMAKA, E., MCGIVERN, J. G., HARAGUCHI, M., SANGAMESWARAN, L., GOGAS K. R.,. EGLEN, R. M., AND HUNTER, J. C. Distribution of the tetrodoloxin resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. J. Neurosci. 18: 2174-2187, 1998.
38. 2+ current in newborn rat dorsal root ganglia. Pflügers Arch. 420: 590-594, 1992a.
39. + channels in neurons of rat dorsal root ganglia. J. Memb. Biol. 129: 71-80, 1992b.
40. + channels in rat dorsal root ganglia. J. Physiol. (Lond.) 466: 9-37, 1993.
41. 2+ current of single isolated frog sensory neurons. Brain Res. 442: 223-228, 1988.
42. PERL, E. R. Myelinated afferent fibres innervating the primate skin and their response to noxious stimuli. J. Physiol. (Lond) 197: 593-615, 1968.
43. POZO, M. A., GALLEGO, R., GALLAR, J., AND BELMONTE, C. Blockade by calcium antagonists of chemical excitation and sensitization of polymodal nociceptors in the cat's cornea. J. Physiol. (Lond.) 450: 179-189, 1992.
44. QUASTHOFF, S., GROSSKREUTZ, J., SCHNEIDER, U., AND GRAFE, P. Calcium potentials and tetrodotoxin-resislant sodium potentials in unmyelinated C fibres of biopsied human sural nerve. Neuroscience 69: 955-965, 1995.
45. RANSOM, B. R. AND HOLZ, R. W. Ionic determinants of excitability in cultured mouse dorsal root ganglion and spinal cord cells. Brain Res. 136: 445-453, 1977.
46. RAYMOND, S. A., STEFFENSEN, S. C., GUGINO, L. D., AND STRICHARTZ, G. R. The role of length of nerve exposed to local anesthetics in impulse blocking action. Anesth. Analg. 68: 563-570, 1989.
47. RAYMOND, S. A. Subblocking concentrations of local anesthetics: effects on impulse generation and conduction in single myelinated sciatic nerve axons in frog. Anesth. Analg. 75: 906-921, 1992.
48. RAYMOND, S. A. AND GISSEN, A. J. Mechanisms of differential nerve block. In: Handbook of Experimental Pharmacology, edited by G. R. Strichartz. New York: Springer-Verlag, 1987, vol. 4, p. 95-164.
49. RETHELYI, M., LIGHT, A. R., AND PERL, E. R. Synaptic complexes formed by functionally defined primary afferent units with fine myelinated fibers. J. Comp. Neurol. 207: 381-393, 1982.
50. RITTER, A. M. AND MENDELL, L. M. Somal membrane properties of physiologically identified sensory neurons in the rat: effects of nerve growth factor. J. Neurophysiol. 68: 2033-2041, 1992.
51. RIZZO, M. A., KOCSIS, J. D., AND WAXMAN, S. G. Slow sodium conductances of dorsal root ganglion neurons: intraneuronal homogeneity and interneuronal heterogeneity. J. Neurophysiol. 72: 2796-2815, 1994.
52. ROY, M. L. AND NARAHASHI, T. Differential properties of tetrodotoxin-sensilive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J. Neurosci. 12: 2104-2111, 1992:
53. ROY, M. L., REUVENY, E., AND NARAHASHI, T. Single-channel analysis of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. Brain Res. 650: 341-346, 1994.
54. 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. Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J. Biol. Chem. 271: 5953-5956, 1996.
55. STEA, A. AND NURSE, C. A. Whole-cell currents in two subpopulations of cultured rat petrosal neurons with different tetrodotoxin sensitivities. Neuroscience 47: 727-736, 1992.
56. STOCKBRIDGE, L. L. AND ROSS, W. N. A TTX-resistant propagating calcium action potential. J. Neurophysiol. 56: 1669-1679, 1986.
57. STRASSMAN, A. M., RAYMOND, S. A., AND BURSTEIN, R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature 384: 560-564, 1996.
58. VILLIERE, V. AND MCLACHLAN, E. M. Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J. Neurophysiol. 76: 1924-1941, 1996.
59. + channel subtypes in central neurons. Neuron 3: 695-704, 1989.
60. YOSHIDA, S., MATSUDA, Y., AND SAMEJIMA, A. Tetrodotoxin-resistant sodium and calcium components of action potentials in dorsal root ganglion cells of the adult mouse. J. Neurophysiol. 41: 1096-1106, 1978.
61. YOSHIDA, S. Tetrodotoxin-resistant sodium channels. Cell. Mol. Neurobiol. 14: 227-244, 1994.
62. YOSHIDA, S. AND MATSUDA, Y. Studies on sensory neurons of the mouse with intracellular-recording and horseradish peroxidase-injection techniques. J. Neurophysiol. 42: 1134-1145, 1979.
63. YOSHIDA, S. AND MATSUDA, Y. Responses dependent on alkaline earth cations (Ca, Sr, Ba) in dorsal root ganglion cells of the adult mouse. Brain Res. 188: 593-597, 1980.
64. + currents recorded from acutely dissociated pelvic ganglion neurons of the adult rat. J. Neurophysiol. 76: 2508-2521, 1996.
65. + currents in dorsal root ganglion neurones innervating the rat urinary bladder. J. Physiol. (Lond.) 494: 1-16, 1996.