Rescue of α-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo

Journal of Neurophysiology

Volumn 79, Issue 5, 1998, Pages 2668-2676

  Dib Hajj, S D ^b   Black, J A ^b   Cummins, T R ^b   Kenney, A M ^b   Kocsis, J D ^b   Waxman, S G ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; SODIUM; SODIUM CHANNEL; TETRODOTOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IN SITU HYBRIDIZATION; NERVE FIBER TRANSECTION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM CURRENT; SPINAL GANGLION;

EID: 0031840375     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.79.5.2668     Document Type: Article

References (51)

1. AGUAYO, L. G. AND WHITE, G. Effects of nerve growth factor on TTX-and capsaicin-sensitivity in adult rat sensory neurons. Brain Res. 570: 61-67, 1992.
2. AKOPIAN, A. N., SIVILOTTI, L., AND WOOD, J. N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379: 258-262, 1996.
3. BANDTLOW, C. E., HEUMANN, R., SCHWAB, M. E., AND THEONEN, H. Cellular localization of nerve growth factor synthesis by in situ hybridization. EMBO J. 6: 891-899, 1987.
4. BENHAM, F. J., HODOKINSON, S., AND DAVIES, K. E. A glyceraldehyde-3-phosphate dehydrogenase pseudogene on the short arm of the human X chromosome defines a multigene family. EMBO J. 3: 2635-2640, 1984.
5. BHATTACHARYYA, A., WATSON, F. L., BRADLESS, T. A., POMEROY, S. L., STILES, C. D., AND SEGAL, R. A. Trk receptors function as rapid retrograde signal carriers in the adult nervous system. J. Neurosci. 17: 7007-7016, 1997.
6. BLACK, J. A., DIB-HAJJ, S., MCNABOLA, K., JESTE, S., RIZZO, M. A., KOCSIS, AND WAXMAN, S. G. Spinal sensory neurons express multiple sodium channel α-subunit mRNAs. Mol. Brain Res. 43: 117-131, 1996.
7. + channel III and SNS gene expression in spinal sensory neurons. Neuroreport 8: 2331-2335, 1997.
8. BLACK, J. A., YOKOYAMA, S., HIGASHIDA, H., RANSOM, B. R., AND WAXMAN, S. G. Sodium channel mRNAs I, II and II in the CNS: cell-specific expression. Mol. Brain Res. 22: 275-289, 1994a.
9. BLACK, J. A., YOKOYAMA, S., WAXMAN, S. G., OH, Y., ZUR, K. B., SONTHEIMER, H., HIGASHIDA, H., AND RANSOM, B. R. Sodium channel mRNAs in cultured spinal cord astrocytes: in situ hybridization in identified cell types. Mol. Brain Res. 23: 235-245, 1994b.
10. 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.
11. CHENG, S., FOCKLER, C., BARNES, W. M., AND HIGUCHI, R. Effective amplification of long targets from cloned inserts and human genomic DNA. Proc. Natl. Acad. Sci. USA 91: 5695-5699, 1992.
12. CHOMCZYNSKI, P. AND SACCHI, N. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159, 1987.
13. 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.
14. D'ARCANGELO, G., PARDISO, K., SHEPHERD, D., BREHM, P., HALEGOUA, S., AND MANDEL, G. Neuronal growth factor regulation of two different sodium channel types through distinct signal transduction pathways. J. Cell Biol. 122: 915-921, 1993.
15. DIB-HAJJ, S., BLACK, J. A., FELTS, P. A., AND WAXMAN, S. G. Down-regulation of transcripts for Na channel α-SNS in spinal sensory neurons following axotomy. Proc. Natl. Acad. Sci. USA 93: 14950-14954, 1996.
16. DISTEFANO, P. S., FRIEDMAN, B., RADZIEJEWSKI, C., ALEXANDER, C., BOLAND, P., AND SCHICK, C. M. The neurotrophins BDNF, NT-3 and NGF display distinct paterns of retrograde axonal transport inperipheral and central neurons. Neuron 8: 983-993, 1993.
17. 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.
18. ERCOLANI, L., FLORENCE, B., DENARO, M., AND ALEXANDER, M. Isolation and complete sequence of a functional human glyceraldehyde-3-phosphate dehydrogenase gene. J. Biol. Chem. 263: 15335-15341, 1988.
19. FANGER, G. R., JONES, J. R., AND MAUE, R. A. Differential regulation of neruonal sodium channel expression by endogenous and exogenous tyrosine kinase receptors expressed in rat pheochromocytoma cells. J. Neurosci. 15: 202-213, 1995.
20. FITZGERALD, M., WALL, P. D., GOEDERT, M., AND EMSON, P. C. Nerve growth factor conteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res. 332: 131-141, 1985.
21. A mRNA have functional receptors. J. Neurosci. 14: 5429-5436, 1994.
22. HEUMANN, R., KORSCHING, S., BANDTLOW, C., AND THEONEN, H. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J. Cell Biol. 104: 1623-1631, 1987.
23. HINSON, A. W., Gu, X. Q., DIB-HAJJ, S., BLACK, J. A., AND WAXMAN, S. G. Schwann cells modulate sodium channel expression in spinal sensory neurons in vitro. Glia 21: 339-349, 1997.
24. HONMOU, O., UTZSCHNEIDER, D. A., RIZZO, M. A., BOWE, C. M., WAXMAN, S. G., AND KOCSIS, J. D. Delayed depolarization and slow sodium currents in cutaneous afferents. J. Neurophysiol. 71: 1627-1637, 1994.
25. KALMAN, D., WONG, B., HORVAI, A. E., CLINE, M. J., AND O'LAGUE, P. H. Nerve growth factor acts through cAMP-dependent protein kinase to increase the number of sodium channels in PC12 cell. Neuron 2: 355-366, 1990.
26. KASHIBA, H., NOGUCHI. K., UEDA, Y., AND SENBA, E. Coexpression of trk family members and low-affinity neurotrophin receptors in rat dorsal root ganglion neurons. Mol. Brain Res. 30: 158-164, 1995.
27. KINOSHITA, T., IMAMURA, J., NAGAI, H., AND SHIMOTOHNO, Quantification of gene expression over a wide range by the polymerase chain reaction. Anal. Biochem. 206: 231-235, 1992.
28. KOSTYUK, P. G., VESELOVSKY, N. S., AND TSYANDRYENKO, A. Y. Ionic currents in the somatic membrane of rat dorsal root ganglion neurons. I. Sodium currents. Neuroscience 6: 2423-2430, 1981.
29. MATHESON, C. R., CARNAHAN, J., URICH, J. L., BOANGEL, D., ZHANG, T. J., AND YAN, Q. Glial cell line-derived neurotrophic factor (GDNF) is a neurotrophic factor for sensory neurons: comparison with the effects of the neurotrophins. J. Neurobiol. 32: 22-32, 1997.
30. + channels by nerve growth factor. Proc. Natl. Acad. Sci. USA 85: 924-928, 1988.
31. 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.
32. MCMAHON, S. B., ARMANINI, M. P., LING, L. H., AND PHILLIPS, H. S. Expression and coexpression of trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12: 1161-1171, 1994.
33. MENDELL, L. M. Neurotrophic factors and the specification of neural function. Neuroscientist 1: 26-34, 1995.
34. MEYER, M., MATSUOKA, I., WETMORE, C., OLSON, L., AND THEONEN, H. Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J. Cell Biol. 119: 45-54, 1992.
35. MUNSON, J. B., SHELTON, D. L., AND MCMAHON, S. B. Adult mammalian sensory and motor neurons: roles of endogenous neurotrophins and rescue by exogenous neurotrophins after axotomy. J. Neurosci. 17: 470-476, 1997.
36. + channels in neurons of the rat dorsal root ganglia. Dev. Brain Res. 65: 93-100, 1992.
37. A receptor-mediated conductances and sodium currents in cutaneous afferent neurons. J. Neurophysiol. 78: 31-41, 1997.
38. RITTER, A. M., LEWIN, G. R., KREMER, N. E., AND MENDELL, L. M. Requirements for nerve growth factor in the development of myelinated nociceptors in vivo. Nature 350: 300-302,1991.
39. RITTER, A. M. AND MENDELL, L. M. The somal membrane properties of physiologically identified sensory neruons in the rat: effects of nerve growth factor. J. Neurophysiol. 68: 2033-2041, 1992.
40. 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.
41. + currents in cutaneous afferent dorsal root ganglion neurones following axotomy. Neurobiol. Dis. 2: 87-96, 1995.
42. 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.
43. RUDY, B., KIRSCHENBAUM, B., RUKENSTEIN, A., AND GREENE, L. A. Nerve growth factor increases the number of functional Na cahnnels and induces TTX-resistant Na channels in PC12 pheochromocytoma cells. J. Neurosci. 7: 1613-1625, 1987.
44. SANGAMESWARAN, L., DELGADO, S. G., FISH, L. M., KOCH, 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.
45. SOUSLOVA, V., Fox, M., WOOD, J., AND AKOPIAN, A. Cloning and characterization of mouse sensory neuron tetrodotoxin-resistant voltage-gated sodium channel gene, Scn10a. Genomics 41: 201-209, 1997.
46. SUCHER, N. J., BROSE, N., DEITCHER, D. L., AWOBULUYI, M., GASIC, G. P., BADING, H., CEPKO, C. L., GREENBERG, M. E., JAHN, R., HEINEMANN, S. F., AND LIPTON, S. Expression of endogenous NMDAR1 transcripts without receptor protein suggests post-transcriptional control in PC12 cells. J. Biol. Chem. 268: 22299-22304, 1993.
47. TOLEDO-ARAL, J. J., BREHM, P., HALEGOUA, S., AND MANDEL, G. A single pulse of nerve growth factor triggers long-term neuronal excitability through sodium channel gene induction. Neuron 14: 607-611, 1995.
48. VERGE, V.M.K., RICHARDSON, P. M., WEISENFELD-HALLIN, Z., AND HOKFELT, T. Differential effect of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J. Neurosci. 15: 2081-2096, 1995.
49. WAXMAN, S. G., KOCSIS, J. D., AND BLACK, J. A. Type III sodium channel mRNA is expressed in embronic but not adult spinal sensory neurons, and is reexpressed following axotomy. J. Neurophysiol. 72: 466-470, 1994.
50. WONG, J. AND OBLINGER, M. M. NGF rescues substance P expression but not neurofilament or tubulin gene expression in axotomized sensory neurons. J. Neurosci. 11: 543-552, 1991.
51. ZUR, K. B., OH, Y., WAXMAN, S. G., AND BLACK, J. A. Differential up-regulation of sodium channel α-and β1-subunit MRNAs in cultured embryonic DRG neurons following exposure to NGF. Mol. Brain Res. 30: 97-103, 1995.