Membrane properties and electrogenesis in the distal axons of small dorsal root ganglion neurons in vitro

Journal of Neurophysiology

Volumn 108, Issue 3, 2012, Pages 729-740

  Vasylyev, Dmytro V ^a,b   Waxman, Stephen G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

Action potential; Resting potential; Sodium channels; Tetrodotoxin

Indexed keywords

SODIUM CHANNEL; TETRODOTOXIN;

ANIMAL CELL; ARTICLE; ELECTROGENESIS; ELECTROPHYSIOLOGY; IN VITRO STUDY; MEMBRANE STEADY POTENTIAL; NERVE CELL MEMBRANE; NERVE ENDING; NERVE FIBER; NERVE POTENTIAL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL GANGLION; VOLTAGE CLAMP;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; AXONS; CELL MEMBRANE; CELLS, CULTURED; GANGLIA, SPINAL; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNELS; TETRODOTOXIN;

EID: 84865652029     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00091.2012     Document Type: Article

References (54)

1. Akopian AN, Sivilotti L, Wood JN. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379: 257-262, 1996.
2. Amir R, Devor M. Ongoing activity in neuroma afferents bearing retrograde sprouts. Brain Res 630: 283-288, 1993.
3. Black JA, Renganathan M, Waxman SG. Sodium channel Nav1.6 is expressed along nonmyelinated axons and it contributes to conduction. Brain Res Mol Brain Res 105: 19-28, 2002.
4. Black JA, Waxman SG. Molecular identities of two tetrodotoxin-resistant sodium channels in corneal axons. Exp Eye Res 75: 193-199, 2002.
5. Blair NT, Bean BP. Role of tetrodotoxin-resistant Na current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 23: 10338-10350, 2003.
6. 2 current in the action potentials of nociceptive sensory neurons. J Neurosci 22: 10277-10290, 2002.
7. Brock JA, Pianova S, Belmonte C. Differences between nerve terminal impulses of polymodal nociceptors and cold sensory receptors of the guinea-pig cornea. J Physiol 533: 493-501, 2001.
8. Caffrey JM, Eng DL, Black JA, Waxman SG, Kocsis JD. Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res 592: 283-297, 1992.
9. Carr RW, Pianova S, Brock JA. The effects of polarizing current on nerve terminal impulses recorded from polymodal and cold receptors in the guinea-pig cornea. J Gen Physiol 120: 395-405, 2002.
10. Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltagegated sodium channels. Pharmacol Rev 57: 397-409, 2005.
11. Choi JS, Waxman SG. Physiological interactions between Nav1.7 and Nav1.8 sodium channels: a computer simulation study. J Neurophysiol 106: 3173-3184, 2011.
12. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN, Waxman SG. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 19: RC43, 1999.
13. Cummins TR, Howe JR, Waxman SG. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel. J Neurosci 18: 9607-9619, 1998.
14. Cummins TR, Rush AM, Estacion M, Dib-Hajj SD, Waxman SG. Voltageclamp and current-clamp recordings from mammalian DRG neurons. Nat Protoc 4: 1103-1112, 2009.
15. Cummins TR, Sheets PL, Waxman SG. The roles of sodium channels in nociception: implications for mechanisms of pain. Pain 131: 243-257, 2007.
16. Cummins TR, 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.
17. Dib-Hajj SD, Choi JS, Macala LJ, Tyrrell L, Black JA, Cummins TR, Waxman SG. Transfection of rat or mouse neurons by biolistics or electroporation. Nat Protoc 4: 1118-1126, 2009.
18. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. Sodium channels in normal and pathological pain. Annu Rev Neurosci 33: 325-347, 2010.
19. Dib-Hajj SD, Rush AM, Cummins TR, Hisama FM, Novella S, Tyrrell L, Marshall L, Waxman SG. Gain-of-function mutation in Nav1.7 in familial erythromelalgia induces bursting of sensory neurons. Brain 128: 1847-1854, 2005.
20. Donnelly DF. Spontaneous action potential generation due to persistent sodium channel currents in simulated carotid body afferent fibers. J Appl Physiol 104: 1394-1401, 2008.
21. Elliott AA, Elliott JR. Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol 463: 39-56, 1993.
22. Estacion M, Dib-Hajj SD, Benke PJ, Te Morsche RH, Eastman EM, Macala LJ, Drenth JP, Waxman SD. Nav1.7 gain-of-function mutations as a continuum: A1632E displays physiological changes associated with erythromelalgia and paroxysmal extreme pain disorder mutations and produces symptoms of both disorders. J Neurosci 28: 11079-11088, 2008.
23. Faber CG, Hoeijmakers JG, Ahn HS, Cheng X, Han C, Choi JS, Estacion M, Lauria G, Vanhoutte EK, Gerrits MM, Dib-Hajj S, Drenth JP, Waxman SG, Merkies IS. Gain of function Nav1.7 mutations in idiopathic small fiber neuropathy. Ann Neurol 71: 26-39, 2012.
24. Harper AA, Lawson SN. Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 359: 31-46, 1985a.
25. Harper AA, Lawson SN. Electrical properties of rat dorsal root ganglion neurones with different peripheral nerve conduction velocities. J Physiol 359: 47-63, 1985b.
26. Harty TP, Dib-Hajj SD, Tyrrell L, Blackman R, Hisama FM, Rose JB, Waxman SG. Nav1.7 mutant A863P in erythromelalgia: effects of altered activation and steady-state inactivation on excitability of nociceptive dorsal root ganglion neurons. J Neurosci 26: 12566-12575, 2006.
27. Herzog RI, Cummins TR, Ghassemi F, Dib-Hajj SD, 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, 2003.
28. Hudmon A, Choi JS, Tyrrell L, Black JA, Rush AM, Waxman SG, Dib-Hajj SD. Phosphorylation of sodium channel Nav1.8 by p38 mitogenactivated protein kinase increases current density in dorsal root ganglion neurons. J Neurosci 28: 3190-3201, 2008.
29. Jamieson J, Boyd HD, McLachlan EM. Simulations to derive membrane resistivity in three phenotypes of guinea pig sympathetic postganglionic neuron. J Neurophysiol 89: 2430-2440, 2003.
30. Kocsis JD, Ruiz JA, Waxman SG. Maturation of mammalian myelinated fibers: changes in action-potential characteristics following 4-aminopyridine application. J Neurophysiol 50: 449-463, 1983.
31. Kocsis JD, Waxman SG, Hildebrand C, Ruiz JA. Regenerating mammalian nerve fibres: changes in action potential waveform and firing characteristics following blockage of potassium conductance. Proc R Soc Lond B Biol Sci 217: 77-87, 1982.
32. Kostyuk PG, Veselovsky NS, Tsyndrenko AY. Ionic currents in the somatic membrane of rat dorsal root ganglion neurons-I. Sodium currents. Neuro-science 6: 2423-2430, 1981.
33. Lang PM, Hilmer VB, Grafe P. Differential contribution of sodium channel subtypes to action potential generation in unmyelinated human C-type nerve fibers. Anesthesiology 107: 495-501, 2007.
34. Meyer RA, Raja SN, Campbell JN, Mackinnon SE, Dellon AL. Neural activity originating from a neuroma in the baboon. Brain Res 325: 255-260, 1985.
35. Moalem-Taylor G, Lang PM, Tracey DJ, Grafe P. Post-spike excitability indicates changes in membrane potential of isolated C-fibers. Muscle Nerve 36: 172-182, 2007.
36. Morita K, Katayama Y. Bullfrog dorsal root ganglion cells having tetrodotoxin-resistant spikes are endowed with nicotinic receptors. J Neurophysiol 62: 657-664, 1989.
37. Persson AK, Black JA, Gasser A, Cheng X, Fischer TZ, Waxman SG. Sodium-calcium exchanger and multiple sodium channel isoforms in intraepidermal nerve terminals. Mol Pain 6: 84, 2010.
38. Quasthoff S, Grosskreutz J, Schroder JM, Schneider U, Grafe P. Calcium potentials and tetrodotoxin-resistant sodium potentials in unmyelinated C fibres of biopsied human sural nerve. Neuroscience 69: 955-965, 1995.
39. Rall W, Burke RE, Holmes WR, Jack JJ, Redman SJ, Segev I. Matching dendritic neuron models to experimental data. Physiol Rev 72: S159-S186, 1992.
40. Rang HP, Ritchie JM. Depolarization of nonmyelinated fibers of the rat vagus nerve produced by activation of protein kinase C. J Neurosci 8: 2606-2617, 1988.
41. Renganathan M, Cummins TR, Waxman SG. Contribution of Nav1.8 sodium channels to action potential electrogenesis in DRG neurons. J Neurophysiol 86: 629-640, 2001.
42. Renganathan M, Dib-Hajj S, Waxman SG. Nav1.5 underlies the 'third TTX-R sodium current' in rat small DRG neurons. Brain Res Mol Brain Res 106: 70-82, 2002.
43. Ritter AM, Mendell LM. Somal membrane properties of physiologically identified sensory neurons in the rat: effects of nerve growth factor. J Neurophysiol 68: 2033-2041, 1992.
44. Rush AM, Craner MJ, Kageyama T, Dib-Hajj SD, Waxman SG, Ranscht B. Contactin regulates the current density and axonal expression of tetrodotoxin-resistant but not tetrodotoxin-sensitive sodium channels in DRG neurons. Eur J Neurosci 22: 39-49, 2005a.
45. Rush AM, Cummins TR, Waxman SG. Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol 579: 1-14, 2007.
46. Rush AM, Dib-Hajj SD, Liu S, Cummins TR, Black JA, Waxman SG. A single sodium channel mutation produces hyperor hypoexcitability in different types of neurons. Proc Natl Acad Sci USA 103: 8245-8250, 2006.
47. Rush AM, Dib-Hajj SD, Waxman SG. Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurones. J Physiol 564: 803-815, 2005b.
48. Serra J, Bostock H, Sola R, Aleu J, Garcia E, Cokic B, Navarro X, Quiles C. Microneurographic identification of spontaneous activity in C-nociceptors in neuropathic pain states in humans and rats. Pain 153: 42-55, 2012.
49. Serra J, Sola R, Aleu J, Quiles C, Navarro X, Bostock H. Double and triple spikes in C-nociceptors in neuropathic pain states: an additional peripheral mechanism of hyperalgesia. Pain 152: 343-353, 2011.
50. Snape A, Pittaway JF, Baker MD. Excitability parameters and sensitivity to anemone toxin ATX-II in rat small diameter primary sensory neurones discriminated by Griffonia simplicifolia isolectin IB4. J Physiol 588: 125-137, 2010.
51. Steffens H, Hoheisel U, Eek B, Mense S. Tetrodotoxin-resistant conductivity and spinal effects of cutaneous C-fibre afferents in the rat. Neurosci Res 39: 413-419, 2001.
52. Strassman AM, Raymond SA. Electrophysiological evidence for tetrodotoxin-resistant sodium channels in slowly conducting dural sensory fibers. J Neurophysiol 81: 413-424, 1999.
53. Waddell PJ, Lawson SN. Electrophysiological properties of subpopulations of rat dorsal root ganglion neurons in vitro. Neuroscience 36: 811-822, 1990.
54. Waxman SG, Black JA, Kocsis JD, Ritchie JM. Low density of sodium channels supports action potential conduction in axons of neonatal rat optic nerve. Proc Natl Acad Sci USA 86: 1406-1410, 1989.