Complete recovery by nerve growth factor of neuropeptide content and function in capsaicin-impaired sensory neurons

Brain Research

Volumn 741, Issue 1-2, 1996, Pages 103-108

  Donnerer, J ^a   Amann, R ^a   Schuligoi, R ^a   Skofitsch, G ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

capsaicin; nerve growth factor; neuropeptide; neuroregeneration; primary afferent fiber; rat

Indexed keywords

ALLYL ISOTHIOCYANATE; CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; NERVE GROWTH FACTOR; SUBSTANCE P;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MALE; NERVE DEGENERATION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT; SCIATIC NERVE;

ANIMALS; BLOOD PROTEINS; CAPSAICIN; MALE; NERVE GROWTH FACTORS; NEURONS, AFFERENT; NEUROPEPTIDES; PERIPHERAL NERVOUS SYSTEM; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE;

EID: 0030602022     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(96)00905-5     Document Type: Article

References (33)

1. [1] Amann, R., Schuligoi, R., Herzeg, G. and Donnerer, J., Intraplantar injection of NGF into the rat hindpaw: local edema and effects on thermal nociceptive threshold, Pain, 64 (1995) 323-329.
2. [2] Amann, R., Sirinatsinghji, D.J.S., Donnerer, J., Liebmann, I. and Schuligoi, R., Stimulation by nerve growth factor of neuropeptide synthesis in the adult rat in vivo: bilateral response to unilateral intraplantar injection, Neurosci. Lett., 203 (1996) 171-174.
3. [3] Apfel, S.C., Arezzo, J.C., Brownlee, M., Federoff, H. and Kessler, J.A., Nerve growth factor administration protects against experimental diabetic sensory neuropathy, Brain Res., 634 (1994) 7-12.
4. [4] Brain, S.D. and Williams, T.J., Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability, Br. J. Pharmacol., 86 (1985) 855-860.
5. [5] Chung, K., Klein, C.M. and Coggeshall, R.E., The receptive part of the primary afferent axon is most vulnerable to systemic capsaicin in adult rats, Brain Res., 511 (1990) 222-226.
6. [6] Diamond, J., Coughlin, M., MacIntyre, L., Holmes, M. and Visheau, B., Evidence that endogenous nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats, Proc. NatL Acad. Sci. USA, 84 (1987) 6596-6600.
7. [7] Diamond, J., Holmes, M. and Coughlin, M., Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J. Neurosci., 12 (1992) 1454-1466.
8. [8] Donaldson, L.F., McQueen, D.S. and Seckl, J.R., Neuropeptide gene expression and capsaicin-sensitive primary afferents: maintenance and spread of adjuvant arthritis in the rat, J. Physiol., 486 (1995) 473-482.
9. [9] Donnerer, J., Schuligoi, R. and Stein, C., Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo, Neuroscience, 49 (1992) 693-698.
10. [10] Gamse, R., Leeman, S.E., Holzer, P. and Lembeck, F., Differential effects of capsaicin on the content of somatostatin, substance P, and neurotensin in the nervous system of the rat, Naunyn-Schmiedeberg's Arch. Pharmacol. 317 (1981) 140-148.
11. [11] Gamse, R., Petsche, U., Lembeck, F. and Jancso, G., Capsaicin applied to peripheral nerve inhibits axoplasmic transport of substance P and somatostatin, Brain Res., 239 (1982) 447-462.
12. [12] Gavazzi, I., Collateral sprouting and responsiveness to nerve growth factor of ageing neurons, Neurosci. Lett., 189 (1995) 47-50.
13. [13] Goedert, M., Stoeckel, K. and Otten, U., Biological importance of the retrograde axonal transport of nerve growth factor in sensory neurons, Proc. Natl. Acad. Sci. USA, 78 (1981) 5895-5898.
14. [14] Holzer, P., Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons, Pharmacol. Rev., 43 (1991) 143-201.
15. [15] Hu-Tsai, M., Winter, J., Emson, P.C. and Woolf, C.J., Neurite outgrowth and GAP-43 mRNA expression in cultured adult rat dorsal root ganglion neurons: effects of NGF or prior peripheral axotomy, J. Neurosci. Res., (1994) 634-645.
16. [16] Jeanjean, A.P., Maloteaux, J.M. and Laduron, P.M., IL-1β-like Freund's adjuvant enhances axonal transport of opiate receptors in sensory neurons, Neurosci. Lett., 177 (1994) 75-78.
17. [17] Johanson, S.O., Crouch, M.F. and Hendry, I.A., Retrograde axonal transport of signal transduction proteins in rat sciatic nerve, Brain Res., 690 (1995) 55-63.
18. [18] Kashiba, H., Ueda, Y. and Senba, E., Coexpression of preprotachykinin-A, α-calcitonin gene-related peptide, somatostatin, and neurotrophin receptor family messenger RNAs in rat dorsal root ganglion neurons, Neuroscience, 70 (1996) 179-189.
19. [19] Lembeck, F. and Donnerer, J., Time course of capsaicin-induced functional impairments in comparison with changes in neuronal substance P content, Naunyn-Schmiedeberg's Arch. Pharmacol., 316 (1981) 240-243.
20. [20] Lembeck, F., Donnerer, J., Tsuchiya, M. and Nagahisa, A., The non-peptide tachykinin antagonist, CP-96,345, is a potent inhibitor of neurogenic inflammation, Br. J. Pharmacol., 105 (1992) 527-530.
21. [21] Lewin, G.R., Rueff, A. and Mendell, L.M., Peripheral and central mechanisms of NGF-induced hyperalgesia, Eur. J. Neurosci., 6 (1994) 1903-1912.
22. [22] Lindsay, R.M. and Harmar, A.J., Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons, Nature, 337 (1989) 362-364.
23. [23] Lindsay, R.M., Lockett, C., Stemberg, J. and Winter, J., Neuropeptide expression in cultures of adult sensory neurons: modulation of substance P and calcitonin gene-related peptide levels by nerve growth factor, Neuroscience, 33 (1989) 53-65.
24. [24] Maggi, C.A., Santicioli, P., Geppetti, P., Giuliani, S., Patacchini, R., Frilli, S., Grassi, J. and Meli, A., Involvement of a peripheral site of action in the early phase of neuropeptide depletion following capsaicin desensitization, Brain Res., 436 (1987) 402-406.
25. [25] Maggi, C.A., Astolfi, M., Donnerer, J. and Amann, R., Which mechanisms account for the sensory neuron blocking action of capsaicin on primary afferents in the rat urinary bladder, Neurosci. Lett., 110 (1990) 267-272.
26. [26] Miller, M.S., Buck, S.H., Sipes, G., Yamamura, H.I. and Burks, T.F., Regulation of substance P by nerve growth factor: disruption by capsaicin, Brain Res., 250 (1982) 193-196.
27. [27] Mohiuddin, L., Fernandez, K., Tomlinson, D.R. and Fernyhough, P., Nerve growth factor and neurotrophin-3 enhance neurite outgrowth and up-regulate the levels of messenger RNA for growth-associated protein GAP-43 and T α1 α-tubulin in cultured adult rat sensory neurones, Neurosci. Lett., 185 (1995) 20-23.
28. [28] Otten, U., Lorez, H.P. and Businger, F., Nerve growth factor antagonizes the neurotoxic action of capsaicin on primary sensory neurons, Nature, 301 (1983) 515-517.
29. [29] Sango, K., Verdes, J.M., Hikawa, N., Horie, H., Tanaka, S., Inoue, S., Sotelo, J.R. and Takenaka, T., Nerve growth factor (NGF) restores depletions of calcitonin gene-related peptide and substance P in sensory neurons from diabetic mice in vitro, J. Neural. Sci., 126 (1994) 1-5.
30. [30] Szolcsányi, J., Sensory receptors and the antinociceptive effects of capsaicin. In R. Hakanson and F. Sundler (Eds.), Tachykinin Antagonists. Elsevier, Amsterdam, 1985. pp. 45-56.
31. [31] Taylor, D.C.M., Pierau, F.K. and Szolcsanyi, J., Capsaicin-induced inhibition of axoplasmic transport is prevented by nerve growth factor, Cell Tissue Res., 240 (1985) 569-573.
32. [32] Verge, V.M.K., Richardson, P.M., Wiesenfeld-Hallin, Z. and Ḧkfelt, T., Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons, J. Neurosci., 15 (1995) 2081-2096.
33. [33] Yasuda, T., Sobue, G., Ito, T., Mitsuma, T. and Takahashi, A., Nerve growth factor enhances neurite arborization of adult sensory neurons; a study in single-cell culture, Brain Res., 524 (1990) 54-63.