Abstract
In the present experiments the effect of systemic capsaicin treatment on the retrograde labelling of sensory ganglion cells was studied following the injection of choleratoxin B subunit-horseradish peroxidase conjugate (CTX-HRP) into intact and chronically transected peripheral nerves. In the control rats CTX-HRP injected into intact sciatic nerves labelled medium and large neurons with a mean cross-sectional area of 1041 ± 39 µm2. However, after injection of the conjugate into chronically transected sciatic nerves of the control rats, many small cells were also labelled, shifting the mean cross-sectional area of the labelled cells to 632 ± 118 µm2. Capsaicin pretreatmen. per se induced a moderate but significant decrease in the mean cross-sectional area of the labelled neurons (879 ± 79 µm2). More importantly, systemic pretreatment with capsaicin prevented the peripheral nerve lesion-induced labelling of small cells. Thus, the mean cross-sectional areas of labelled neurons relating to the intact and transected sciatic nerves, respectively, did not differ significantly. These findings provide direct evidence for a phenotypic switch of capsaicin-sensitive nociceptive neurons after peripheral nerve injury, and suggest that lesion-induced morphological changes in the spinal cord may be related to specific alterations in the chemistry of C-fibre afferent neurons rather than to a sprouting response of A-fibre afferents.
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Aldskogius, H., Arvidsson, J., Grant, G. (1985) The reaction of primary sensory neurons to peripheral nerve injury with particular emphasis on transganglionic changes. Brain Res. 357, 27–46.
Ambrus, A., Jancsó, G. (1994) Capsaicin sensitivity of primary sensory neurones and its regulation. In: Besson, J. M., Guilband, G., Ollat, H. (eds). Peripheral Neurons in Nociception: Physio-pharmacological Aspects. John Libbey Eurotext, Paris, pp. 71–87.
Bennett, D. L., French, J., Priestley, J. V., McMahon, S. B. (1996) NGF but not NT-3 or BDNF prevents the A fiber sprouting into lamina II of the spinal cord that occurs following axotomy. Mol. Cell. Neurosci. 8, 211–220.
Chung, K., Klein, C. M., Coggeshall, R. E. (1990) The receptive part of the primary afferent axon is most vulnerable to systemic capsaicin in adult rats. Brain Res. 511, 222–226.
Chung, K., Schwen, R. J., Coggeshall, R. E. (1985) Ureteral axon damage following subcutaneous administration of capsaicin in adult rats. Neurosci. Lett. 53, 221–226.
Dray, A., Urban, L., Dickenson, A. (1994) Pharmacology of chronic pain. Trends Phar. 15, 190–197.
Gamse, R., Petsche, U., Lembeck, F., Jancsó, G. (1982) Capsaicin applied to peripheral nerve inhibits axoplasmic transport of substance P and somatostatin. Brain Res. 239, 447–462.
Hökfelt, T., Zhang, X., Wiesenfeld-Hallin, Z. (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci. 17, 22–30.
Jancsó, G. (1992) Pathobiological reactions of C-fibre primary sensory neurones to peripheral nerve injury. Exp. Physiol. 77, 405–431.
Jancsó, G., Király, E., Jancsó-Gábor, A. (1977) Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 270, 741–743.
Jancsó, G., Király, E., Joó, F., Such, G., Nagy, A. (1985) Selective degeneration by capsaicin of a subpopulation of primary sensory neurons in the adult rat. Neurosci. Lett. 59, 209–214.
Jancsó, G., Király, E., Such, G., Joó, F., Nagy, A. (1987) Neurotoxic effect of capsaicin in mammals. Acta Physiol. Hung. 69, 295–313.
Jancsó, G., Lawson, S. N. (1990) Transganglionic degeneration of capsaicin-sensitive C-fiber primary afferent terminals. Neuroscience 39, 501–511.
Mannion, R. J., Doubell, T. P., Coggeshall, R. E., Woolf, C. J. (1996) Collateral sprouting of uninjured primary afferent A-fibers into the superficial dorsal horn of the adult rat spinal cord after topical capsaicin treatment to the sciatic nerve. J. Neurosci. 16, 5189–5195.
Mesulam, M. M. (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26, 106–117.
Miller, M. S., Buck, S. H., Sipes, I. G., Yamamura, H. I., Burks, T. F. (1982) Regulation of substance P by nerve growth factor: disruption by capsaicin. Brain Res. 250, 193–196.
Ritter, S., Dinh, T. T. (1988) Capsaicin-induced neuronal degeneration: silver impregnation of cell bodies, axons, and terminals in the central nervous system of the adult rat. J. Comp. Neurol. 271, 79–90.
Robertson, B., Grant, G. (1985) A comparison between wheat germ agglutinin and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurones in the rat with some observations in the cat. Neuroscience 14, 895–905.
Tong, Y. G., Wang, H. F., Ju, G., Grant, G., Hökfelt, T., Zhang, X. (1999) Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J. Comp. Neurol. 404, 143–158.
Verge, V. M., Gratto, K. A., Karchewski, L. A., Richardson, P. M. (1996) Neurotrophins and nerve injury in the adult. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 351, 423–430.
Waxman, S. G. (1999) The molecular pathophysiology of pain: abnormal expression of sodium channel genes and its contributions to hyperexcitability of primary sensory neurons. Pain Suppl. 6, S133–S140.
Woolf, C. J., Shortland, P., Coggeshall, R. E. (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355, 75–78.
Woolf, C. J., Shortland, P., Reynolds, M., Ridings, J., Doubell, T., Coggeshall, R. E. (1995) Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J. Comp. Neurol. 360, 121–134.
Zhang, X., Xu, Z. O., Shi, T. J., Landry, M., Holmberg, K., Ju, G., Tong, Y. G., Bao, L., Cheng, X. P., Wiesenfeld-Hallin, Z., Lozano, A., Dostrovsky, J., Hökfelt, T. (1998) Regulation of expression of galanin and galanin receptors in dorsal root ganglia and spinal cord after axotomy and inflammation. Ann. N. Y. Acad. Sci. 863, 402–413.
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Dedicated to Professor József Hámori on the occasion of his 70th birthday.
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Jancső, G., Sántha, P. & Gecse, K. Peripheral Nerve Lesion-Induced Uptake and Transport of Choleragenoid by Capsaicin-Sensitive C-Fibre Spinal Ganglion Neurons. BIOLOGIA FUTURA 53, 77–84 (2002). https://doi.org/10.1556/ABiol.53.2002.1-2.9
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DOI: https://doi.org/10.1556/ABiol.53.2002.1-2.9