Nitric oxide is an autocrine regulator of Na+ currents in axotomized C- type DRG neurons

Journal of Neurophysiology

Volumn 83, Issue 4, 2000, Pages 2431-2442

  Renganathan, M ^a   Cummins, T R ^a   Hormuzdiar, W N ^a   Black, J A ^a   Waxman, S G ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; HYDROXYSTILBAMINE METHANESULFONATE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; TETRODOTOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; CONTROLLED STUDY; FEMALE; NERVE FIBER TRANSECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SODIUM CURRENT; SPINAL GANGLION; VOLTAGE CLAMP;

EID: 0034117195     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.4.2431     Document Type: Article

References (49)

1. AIMI, Y., FUJIMURA, M., VINCENT, S. R., AND KIMURA, H. Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J. Comp. Neurol. 306: 382-392, 1991.
2. AKOPIAN, A. N., SOUSLOVA, V., ENGLAND, S., OKUSE, K., OGATA, N., URE, J., SMITH, A., KERR, B. J., MCMAHON, S. B., BOYCE, S., HILL, R., STANFA, L. C., DICKENSON, A. H., AND WOOD, J. N. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat. Neurosci. 2: 541-548, 1999.
3. BREDT, D. S. AND SNYDER, S. H. Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 63: 175-195, 1994a.
4. BREDT, D. S. AND SNYDER, S. H. Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron 13: 301-313, 1994b.
5. 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.
6. CHOI, Y., RAJA, S. N., MOORE, L. C., AND TOBIN, J. R. Neuropathic pain in rats is associated with altered nitric oxide synthase activity in neural tissue. J. Neurol. Sci. 138: 14-20, 1996.
7. CUMMINS, T. R., DIB-HAJJ, S. D., BLACK, J. A., AKOPIAN, A. N., WOOD, J. N., AND WAXMAN, S. G. A novel persistent tetrodotoxin-resistent sodium current in SNS-null and wild-type small primary sensory neurons. J. Neurosci. 19: RC43: 1-6, 1999.
8. CUMMINS, T. R. AND WAXMAN, S. G. 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.
9. DEVOR, M., GOVRIN-LIPPMANN, R., FRANK, I., AND RABER, P. Proliferation of primary sensory neurons in adult rat dorsal root ganglion and the kinetics of retrograde cell loss after sciatic nerve section. Somatosens. Res. 3: 139-167, 1985.
10. DIB-HAJJ, S., BLACK, J. A., FELTS, P., AND WAXMAN, S. G. Down-regulation of transcripts for Na channel alpha-SNS in spinal sensory neurons following axotomy. Proc. Natl. Acad. Sci. USA 93: 14950-14954, 1996.
11. DIB-HAJJ, S. D., TYRRELL, L., BLACK, J. A., AND WAXMAN, S. G. 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, 1998.
12. 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.
13. + channel inactivation and bursting discharge in a simple model axon: implications for neuropathic pain. Brain Res. 754: 221-226, 1997.
14. FERREIRA, S. H., DUARTE, I. D., AND LORENZETTI, B. B. The molecular mechanism of action of peripheral morphine analgesia: stimulation of the cGMP system via nitric oxide release. Eur. J. Pharmacol 201: 121-122, 1991.
15. FIALLOS-ESTRADA, C. E., KUMMER, W., MAYER, B., BRAVO, R., ZIMMERMANN, M., AND HERDEGEN, T. Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-JUN co-expression in rat dorsal root ganglion neurons following sciatic nerve transection. Neurosci. Lett. 150: 169-173, 1993.
16. HAMILL, O. P., MARTY, A., NEHER, E., SAKMANN, B., AND SIGWORTH, F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. Arch. Eur. J. Physiol. 391: 85-100, 1981.
17. HALEY, J. E., DICKENSON, A. H., AND SCHACHTER, M. Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat. Neuropharmacology 31: 251-258, 1992.
18. HOLSCHER, C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity [see comments]. Trends Neurosci. 20: 298-303, 1997.
19. HOLTHUSEN, H. AND ARNDT, J. O. Nitric oxide evokes pain at nociceptors of the paravascular tissue and veins in humans. J. Physiol. (Lond.) 487: 253-258, 1995.
20. IALENTI, A., IANARO, A., MONCADA, S., AND DI ROSA, M. Modulation of acute inflammation by endogenous nitric oxide. Eur. J. Pharmacol. 211: 177-182, 1992.
21. JIA, L., BONAVENTURA, C., BONAVENTURA, J., AND STAMLER, J. S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control [see comments]. Nature 380: 221-226, 1996.
22. JEFTINIJA, S. The role of tetrodotoxin-resistant sodium channels of small primary afferent fibers. Brain Res. 639: 125-134, 1994.
23. LANKFORD, K. L., WAXMAN, S. G., AND KOCSIS, J. D. Mechanisms of enhancement of neurite regeneration in vitro following a conditioning sciatic nerve lesion. J. Comp. Neurol 391: 11-29, 1998.
24. LARSON, A. A. AND KITTO, K. F. Sensitization to the behavioral effect of kainic acid in the mouse is mediated by nitric oxide. J. Pharmacol. Exp. Ther. 275: 544-550, 1995.
25. LAWAND, N. B., WILLIS, W. D., AND WESTLUND, K. N. Blockade of joint inflammation and secondary hyperalgesia by L-NAME, a nitric oxide synthase inhibitor. Neuroreport 8: 895-899, 1997.
26. LI, Z., CHAPLEAU, M. W., BATES, J. N., BIELEFELDT, K., LEE, H. C., AND ABBOUD, F. M. Nitric oxide as an autocrine regulator of sodium currents in baroreceptor neurons. Neuron 20: 1039-1049, 1998.
27. MACHELSKA, H., LABUZ, D., PRZEWLOCKI, R., AND PRZEWLOCKA, B. Inhibition of nitric oxide synthase enhances antinociception mediated by mu, delta and kappa opioid receptors in acute and prolonged pain in the rat spinal cord. J. Pharmacol. Exp. Ther. 282: 977-984, 1997.
28. MELEAN, 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.
29. MONCADA, S. Nitric oxide: discovery and impact on clinical medicine. J. R. Soc. Med. 92: 164-169, 1999.
30. MONCADA, S. AND HIGGS, A. The L-arginine-nitric oxide pathway. New Eng. J. Med. 329: 2002-2012, 1993.
31. MONCADA, S., HIGGS, A., AND FURCHGOTT, R. International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol. Rev. 49: 137-142, 1997.
32. MOORE, P. K., OLUYOMI, A. O., BABBEDGE, R. C., WALLACE, P., AND HART, S. L. L-NG-nitro arginine methyl ester exhibits antinociceptive activity in the mouse. Br. J. Pharmacol 102: 198-202, 1991.
33. REDFORD, E. J., KAPOOR, R., AND SMITH, K. J. Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 120: 2149-2157, 1997.
34. 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.
35. ROY, M. L. AND NARAHASHI, T. Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J. Neurosci. 12: 2104-2111, 1992.
36. RUSH, A. M., BRAU, M. E., ELLIOTT, A. A., AND ELLIOTT, J. R. Electrophysiological properties of sodium current subtypes in small cells from adult rat dorsal root ganglia. J. Physiol. (Lond.) 511: 771-789, 1998.
37. SALTER, M., STRIJBOS, P. J., NEALE, S., DUFFY, C., FOLLENFANT, R. L., AND GARTHWAITE, J. The nitric oxide-cyclic GMP pathway is required for nociceptive signalling at specific loci within the somatosensory pathway. Neuroscience 73: 649-655, 1996.
38. + current heterogeneity in rat nodose neurons and its impact on neuronal discharge. J. Neurophysiol. 78: 3198-3209, 1997
39. SHRAGER, P., CUSTER, A. W., KAZARINOVA, K., RASBAND, M. N., AND MATTSON, D. Nerve conduction block by nitric oxide that is mediated by the axonal environment. J. Neurophysiol. 79: 529-536, 1998.
40. STEEL, J. H., TERENGHI, G., CHUNG, J. M., NA, H. S., CARLTON, S. M., AND POLAK, J. M. Increased nitric oxide synthase immunoreactivity in rat dorsal root ganglia in a neuropathic pain model. Neurosci. Lett. 169: 81-84, 1994.
41. + conductance in rat optic nerve axons. Proc. Natl. Acad. Sci. USA 90: 6976-6980, 1993.
42. TATE, S., BENN, S., HICK, C., TREZISE, D., JOHN, V., MANNION, R. J., COSTIGAN, M., PLUMPTON, C., GROSE, D., GLADWELL, Z., KENDALL, G., DALE, K., BOUNTRA, C., AND WOOLF, C. J. Two sodium channels contribute to the TTX-R sodium current in primary sensory neurons. Nat. Neurosci. 1: 653-655, 1998.
43. THOMAS, D. A., REN, K., BESSE, D., RUDA, M. A., AND DUBNER, R. Application of nitric oxide synthase inhibitor, N omega-nitro-L-arginine methyl ester, on injured nerve attenuates neuropathy-induced thermal hyperalgesia in rats. Neurosci. Lett. 210: 124-126, 1996.
44. VERGE, V. M., XU, Z., XU, X. J., WIESENFELD-HALLIN, Z., AND HOKFELT, T. Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc. Natl. Acad. Sci. USA 89: 11617-11621, 1992.
45. WAXMAN, S. G., DIB-HAJJ, S., CUMMINS, T. R., AND BLACK, J. A. Sodium channels and pain. Proc. Natl. Acad. Sci. USA 96: 7635-7639, 1999.
46. WAXMAN, S. G., KOCSIS, J. D., AND BLACK, J. A. Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J. Neurophysiol. 72: 466-470, 1994.
47. WIESENFELD-HALLIN, Z., HAO, J. X., XU, X. J., AND HOKFELT, T. Nitric oxide mediates ongoing discharges in dorsal root ganglion cells after peripheral nerve injury. J. Neurophysiol. 70: 2350-2353, 1993.
48. YIP, H. K., RICH, K. M., LAMPE, P. A., AND JOHNSON, E. M., JR. The effects of nerve growth factor and its antiserum on the postnatal development and survival after injury of sensory neurons in rat dorsal root ganglia. J. Neurosci. 4: 2986-2992, 1984.
49. ZHANG, X., VERGE, V., WIESENFELD-HALLIN, Z., JU, G., BREDT, D., SNYDER, S. H., AND HOKFELT, T. Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J. Comp. Neurol. 335: 563-575, 1993.