Maturation of cutaneous sensory neurons from normal and NGF- overexpressing mice

Journal of Neurophysiology

Volumn 83, Issue 3, 2000, Pages 1722-1732

  Ritter, Amy M ^a   Woodbury, C Jeffery ^a   Albers, Kathryn ^b   Davis, Brian M ^b   Koerber, H Richard ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL CELL; ARTICLE; CELL MATURATION; FEMALE; GENE OVEREXPRESSION; MALE; MOUSE; NERVE CONDUCTION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SKIN CONDUCTANCE;

EID: 0034059324     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.3.1722     Document Type: Article

References (56)

1. AIRAKSINEN, M. S., KOLTZENBURG, M., LEWIN, G. R., MASU, Y., HELBIG, C., WORL, E., BREM, G., TOYKA, K. V., THOENEN, H., AND MEYER, M. Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron 16: 287-295, 1996.
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. ALBERS, K., WRIGHT, D. E., AND DAVIS, B. M. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14: 1422-1432, 1994.
4. AVERILL, S., MCMAHON, S. B., CLARY, D. O., REICHANRDT, L. F., AND PRIESTLEY, J. V. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci. 7: 1484-1494, 1995.
5. BENNETT, D.L.H., AVERILL, S., CLARY, D. O., PRIESTLEY, J. V., AND MCMAHON, S. B. Postnatal changes in the expression of the trkA high-affinity NGF receptor in primary sensory neurons. Eur. J. Neurosci. 8: 2204-2208, 1996.
6. + channel III and SNS gene expression in spinal sensory neurons. Neuroreport 8: 2331-2335, 1997.
7. BLACK, J. A. AND WAXMAN, S. G. Sodium channel expression: a dynamic process in neurons and non-neuronal cells. Dev. Neurosci. 18: 139-152, 1996.
8. CAMERON, A. A., LEAH, J. D., AND SNOW, P. J. The electrophysiological and morphological characteristics of feline dorsal root ganglion cells. Brain Res. 362: 1-6, 1986.
9. CARROLL, P., LEWIN, G. R., KOLTZENBURG, M., TOYKA, K. V., AND THOENEN, H. A role for BDNF in mechanosensation. Nature Neurosci. 1: 42-46, 1998.
10. COGGESHALL, R. E., POVER, C. M., AND FITZGERALD, M. Dorsal root ganglion cell death and surviving cell numbers in relation to the development of sensory innervation in the at hindlimb. Dev. Brain Res. 82: 193-212, 1994.
11. DAVIES, A. M. The role of neurotrophins during successive stages of sensory neuron development. Prog. Growth Factor Res. 5: 263-289, 1994.
12. DAVIES, A. M., BANDTLOW, C., HEUMANN, R., KORSCHING, S., ROHRER, H., AND THOENEN, H. Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326: 353-358, 1987.
13. DAVIS, B. M., LEWIN, G. R., MENDELL, L. M., JONES, M. E., AND ALBERS, K. M. Altered expression of nerve growth factor in the skin of transgenic mice leads to changes in responses to mechanical stimuli. Neuroscience 56: 789-792, 1993.
14. DIB-HAJJ, S. D., BLACK, J. A., CUMMINS, T. R., KENNEY, A. M., KOCSIS, J. D., AND WAXMAN, S. G. Rescue of α-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo. J. Neurophysiol. 79: 2668-2676, 1998.
15. DIB-HAJJ, S. D., 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. FELTS, P. A., YOKOYAMA, S., DIB-HAJJ, S., BLACK, J. A., AND WAXMAN, S. G. Sodium channel α-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Mol. Brain Res. 45: 71-82, 1997.
17. FITZGERALD, M. Spontaneous and evoked activity of fetal primary afferents in vivo. Nature 326: 603-604, 1987a.
18. FITZGERALD, M. Cutaneous primary afferent properties in the hind limb of the neonatal rat. J. Physiol. (Lond.) 383: 79-92, 1987b.
19. FITZGERALD, M., BUTCHER, T., AND SHORTLAND, P. Developmental changes in the laminar termination of A fibre cutaneous sensory afferents in the rat spinal cord dorsal horn. J. Comp. Neurol. 348: 225-233, 1994.
20. FITZGERALD, M. AND FULTON, B. P. The physiological properties of developing sensory neurons. In: Sensory Neurons: Diversity, Development and Plasticity, edited by S. A. Scott. Oxford, UK: Oxford Univ. Press, 1992, p. 287-306.
21. FITZGERALD, M., SHAW, A., AND MACINTOSH, N. Postnatal development of the cutaneous flexor reflex: comparative study of preterm infants and newborn rat pups. Dev. Med. Child Neurol. 30: 520-526, 1988.
22. FULTON, B. P. Postnatal changes in conduction velocity and soma action potential parameters of rat dorsal root ganglion neurones. Neurosci. Lett. 73: 125-130, 1987.
23. GORKE, K. AND PIERAU, F.-K. Spike potentials and membrane properties of dorsal root ganglion cells in pigeons. Pflügers Arch. 386: 21-28, 1980.
24. GOODNESS, T. P., ALBERS, K. M., DAVIS, F. E., AND DAVIS, B. M. Overexpression of nerve growth factor in skin increases sensory neuron size and modulates Trk receptor expression. Eur. J. Neurosci. 9: 1574-1585, 1997.
25. HARPER, A. A. AND LAWSON, S. N. Electrical properties of rat dorsal root ganglion neurons with differenl peripheral conduction velocities. J. Physiol. (Lond.) 359: 47-63, 1985.
26. HOLMBERG, H. AND SCHOUENBORG, J. Postnatal development of the nociceptive withdrawal reflexes in the rat: a behavioural and electromyographic study. J. Physiol. (Lond.) 493: 239-252, 1996.
27. KOERBER, H. R., DRUZINSKY, R. E., AND MENDELL, L. M. Properties of somata of spinal dorsal root ganglion cells. J. Neurophysiol. 73: 693-702, 1988.
28. KOLTZENBURG, M., STUCKY, C. L., AND LEWIN, G. R. Receptive properties of mouse sensory neurons innervating hairy skin. J. Neurophysiol. 78: 1841-1850, 1997.
29. KOSTYUK, P. G., VESELOVSKY, N. S., AND TSYNDRENKO, A. Y. Ionic currents in the somatic membrane of rat dorsal root ganglion neurons. I. Sodium currents. Neuroscience 6: 2423-2430, 1981.
30. LAWSON, S. N. Neuropeptides in morphologically and functionally identified primary afferent neurons in dorsal root ganglia: substance P, CGRP and somatostatin. Prog. Brain Res. 104: 161-173, 1995.
31. LAWSON, S. N., MCCARTHY, P. W., AND PRABHAKAR, E. Electrophysiological properties of neurones with CGRP-like immunoreactivity in rat dorsal root ganglia. J. Comp. Neurol. 365: 355-366, 1996.
32. LEEM, J. W., WILLIS, W. D., AND CHUNG, J. M. Cutaneous sensory receptors in the rat foot. J. Neurophysiol. 69: 1684-1699, 1993.
33. LYNN, B. AND CARPENTER, S. E. Primary afferent units from the hairy skin of the rat hind limb. Brain Res. 238: 29-43, 1982.
34. MCMAHON, S. B., BENNETT, K.L.H., PRIESTLEY, J. V., AND SHELTON, D. L. Expression and coexpression of trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12: 1161-1171, 1994.
35. MENDELL, L. M., ALBERS, K. M., AND DAVIS, B. M. Neurotrophins, nociceptors, and pain. Microsc. Res. Tech. 45: 252-261, 1999.
36. MENDELSON, B., ALBERS, K. M., GOODNESS, T. P., AND DAVIS, B. M. Overexpression of nerve growth factor in epidermis of transgenic mice preserves excess sensory neurons but does not alter the somatotopic organization of cutaneous nerve projections. Neurosci. Lett. 211: 68-72, 1996.
37. MIRNICS, K. AND KOERBER, H. R. Properties of individual embryonic primary afferents and their spinal projections in the rat. J. Neurophysiol. 78: 1590-1600, 1997.
38. MOLLIVER, D. C. AND SNIDER, W. D. Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J. Comp. Neurol. 381: 428-438, 1997.
39. MORITA, K. AND KATAYAMA, Y. Bullfrog dorsal root ganglion cells having tetrodotoxin-resistant spikes are endowed with nicotinic receptors. J. Neurophysiol. 62: 657-664, 1989.
40. A-receptor-mediated conductance and sodium currents in cutaneous afferent neurons. J. Neurophysiol 78: 31-42, 1997.
41. PAYNE, J., MIDDLETON, J., AND FITZGERALD, M. The pattern and timing of cutaneous hair follicle innervation in the rat pup and human fetus. Dev. Brain Res. 61: 173-182, 1991.
42. 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.
43. RITTER, A. M., WOODBURY, C. J., DAVIS, B. M., ALBERS, K. A., AND KOERBER, H. R. Correlation of anatomical and functional properties of identified cutaneous fibers in wildtype and NGF overexpressing mice. Soc. Neurosci. Abstr. 24: 1042, 1998.
44. RIZZO, M. A., KOCSIS, J. D., AND WAXMAN, S. G. Sodium conductances of dorsal root ganglion neurons: intraneuronal homogeneity and interneuronal heterogeneity. J. Neurophysiol. 72: 2796-2815, 1994.
45. ROSE, R. D., KOERBER, H. R., SEDIVEC, M. J., AND MENDELL, L. M. Somal action potential duration differs in identified primary afferents. Neurosci. Lett. 63: 259-264, 1986.
46. 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.
47. 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.
48. STUCKY, C. L., KOLTZENBURG, M., SCHNEIDER, M., ENGLE, M. G., ALBERS, K. M., AND DAVIS, B. M. Overexpression of nerve growth factor in skin selectively affects the survival and functional properties of nociceptors. J. Neurosci. 19: 8509-8516, 1999.
49. TRAUB, R. J. AND MENDELL, L. M. The spinal projection of individual identified A and C-fibres. J. Neurophysiol. 59: 41-55, 1988.
50. VILLIÈRE, 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.
51. WADDELL, P. J. AND LAWSON, S. N. Electrophysiological properties of subpopulations of rat dorsal root ganglion neurons in vitro. Neurosci. 36: 811-822, 1990.
52. 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: 446-470, 1994.
53. WENG, H.-R. AND SCHOUENBORG, J. On the cutaneous receptors contributing to withdrawal reflex pathways in the decerebrate spinal rat. Exp. Brain Res. 118: 71-77, 1998.
54. WRIGHT, D. E. AND SNIDER, W. D. Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. J. Comp. Neurol. 351: 329-338, 1995.
55. 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.
56. 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.