Neonatal capsaicin treatment results in prolonged mitochondrial damage and delayed cell death of B cells in the rat trigeminal ganglia

Neuroscience

Volumn 113, Issue 4, 2002, Pages 925-937

  Szöke, É ^a   Seress, L ^b   Szolcsanyi J ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Nerve growth factor; Neurodegeneration; Neuroprotection; Nociception; Sensory neuron; Vanilloid receptor

Indexed keywords

ALLYL ISOTHIOCYANATE; CAPSAICIN; NERVE GROWTH FACTOR;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BRAIN MITOCHONDRION; CELL COUNT; CELL DEATH; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DRUG INSTILLATION; ELECTRON MICROSCOPE; EXTRAVASATION; EYE; HISTOGRAM; MITOCHONDRION SWELLING; NEUROGENIC INFLAMMATION; NEUROTOXICITY; NEWBORN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SENSORY NERVE CELL; TRIGEMINUS GANGLION;

ANIMALS; ANIMALS, NEWBORN; CAPSAICIN; CELL DEATH; MITOCHONDRIA; MITOCHONDRIAL SWELLING; NEURONS; RATS; RATS, WISTAR; TRIGEMINAL GANGLION;

EID: 0037056055     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00208-7     Document Type: Article

References (62)

1. Andres K.H. Untersuchungen über den Feinbau von Spinalganglien. Z. Zellforsch. Mikrosk. Anat. 55:1961;1-48.
2. Arvidsson M.E., Ygge J. A quantitative study of the effects of neonatal capsaicin treatment and of subsequent peripheral nerve transection in the adult rat. Brain Res. 397:1986;130-136.
3. Bevan S., Szolcsányi J. Sensory neuron-specific actions of capsaicin: mechanisms and applications. Trends Pharmacol. Sci. 11:1990;330-333.
4. Caramia F., Angeletti P.U., Levi-Montalcini R., Carratelli L. Mitochondrial lesions of developing sympathetic neurons induced by bretylium tosylate. Brain Res. 40:1972;237-246.
5. Cassarino D.S., Bennett J.P. Jr. An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 29:1999;1-25.
6. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channels in the pain pathway. Nature. 389:1997;816-824.
7. Chard P.S., Bleakman D., Savidge J.R., Miller R.J. Capsaicin-induced neurotoxicity in cultured dorsal root ganglion neurons: involvment of calcium-activated proteases. Neuroscience. 65:1995;1099-1108.
8. Chiba T., Masuko S., Kawano H. Correlation of mitochondrial swelling after capsaicin treatment and substance P and somatostatin immunoreactivity in small neurons of dorsal root ganglion in the rat. Neurosci. Lett. 64:1986;311-316.
9. Chung K., Klein C.M., 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.
10. Dedov V.N., Roufogalis B.D. Mitochondrial calcium accumulation following activation of vanilloid (VR1) receptors by capsaicin in dorsal root ganglion neurons. Neuroscience. 95:2000;183-188.
11. Duchen M.R. Mitochondria and calcium: from cell signalling to cell death. J. Physiol. 529:2000;57-68.
12. 3 purinoceptor and IB4 binding sites. Eur. J. Neurosci. 11:1999;946-968.
13. Helliwell R.J., McLatchie L.M., Clarke M., Winter J., Bevan S., McIntyre P. Capsaicin sensitivity is associated with the expression of the vanilloid (capsaicin) receptor (VR1) mRNA in adult rat sensory ganglia. Neurosci. Lett. 250:1998;177-180.
14. Himes B.T., Tessler A. Death of some dorsal root ganglion neurons and plasticity of others following sciatic nerve section in adult and neonatal rats. J. Comp. Neurol. 284:1989;215-230.
15. Hiura A. Neuroanatomical effects of capsaicin on the primary afferent neurons. Arch. Histol. Cytol. 63:2000;199-215.
16. Hiura A., Ishizuka H. Changes in features of degenerating primary sensory neurons with time after capsaicin treatment. Acta Neuropathol. 78:1989;35-46.
17. Hiura A., Sakamoto Y. Quantitative estimation of the effect of capsaicin on the mouse primary sensory neurons. Neurosci. Lett. 76:1987;101-106.
18. Holje H., Hilderbrand C., Fried K. Proportion of unmyelinated axons in the rat inferior alveolar nerve and mandibular molar pulps after neonatal administration of capsaicin. Brain. Res. 266:1983;133-136.
19. Holzer, P., 1992. Capsaicin: Selective toxicity for thin primary sensory neurons. In: Herke, H., Huchs, F. (Eds.), Handbook of Experimental Pharmacology. Selective Neurotoxicity, Vol. 102. Springer, Heidelberg, pp. 419-481.
20. Ichikawa H., Sugimoto T. VR1-immunoreactive primary sensory neurons in the rat trigeminal ganglion. Brain Res. 890:2001;148-188.
21. Jancsó G., Karcsu S., Király E., Szebeni A., Tóth L., Bacsy E., Joó F., Párducz A. Neurotoxin induced nerve cell degeneration: possible involvement of calcium. Brain Res. 295:1984;211-216.
22. Jancsó G., Király E. Sensory neurotoxins: chemically induced selective destruction of primary sensory neurons. Brain Res. 210:1981;83-89.
23. Jancsó G., Király E., Jancsó-Gábor A. Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature. 270:1977;741-743.
24. Jancsó G., Király E., Such G., Joó F., Nagy A. Neurotoxic effect of capsaicin in mammals. Acta Physiol. Hung. 69:1987;295-313.
25. Jancsó N., Jancsó-Gábor A., Szolcsányi J. Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br. J. Pharmacol. 31:1967;138-151.
26. Jancsó-Gábor A., Szolcsányi J., Jancsó N. Stimulation and desenzitization of the hypothalamic heat-sensitive structures by capsaicin in rats. J. Physiol. 208:1970;449-459.
27. Joó F., Szolcsányi J., Jancsó-Gábor A. Mitochondrial alterations in the spinal ganglion cells of the rat accompanying the long-lasting sensory disturbance induced by capsaicin. Life Sci. 8:1969;621-626.
28. Kai-Kai M.A., Che Y-M. Distribution of arginine-vasopressin in the trigeminal dorsal root ganglia and spinal cord of the rat: depletion by capsaicin. Comp. Biochem. Physiol. A. Comp. Physiol. 110:1995;71-78.
29. Königsmark, B.W., 1970. Methods for counting of neurons. In: Nauta, W.J.H., Ebbesson, S.O.E. (Eds.), Contemporary Research Methods in Neuroanatomy. Springer-Verlag, New York, pp. 315-340.
30. Lawson S.N. The morphological consequences of neonatal treatment with capsaicin on primary afferent neurones in adult rats. Acta Physiol. Hung. 69:1987;315-321.
31. Lawson, S.N., Harper, A.A., 1984. Neonatal capsaicin is not a specific neurotoxin for sensory C-fibres or small dark cells of rat dorsal root ganglia. In: Chahl, L.A., Szolcsányi, J., Lembeck, F. (Eds.), Antidromic Vasodilatation an Neurogenic Inflammation. Akadémia Kiadó, Budapest, pp. 111-118.
32. Lewin G.R., Mendell L.M. Regulation of cutaneous C-fiber heat nociceptors by nerve growth factor in the developing rat. J. Neurophysiol. 71:1994;941-949.
33. Lieberman, A.R., 1976. Sensory ganglia. In: Landon, D.N. (Ed.), The Peripheral Nerve. Chapman and Hall, London, pp. 178-188.
34. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 79:1999;1431-1568.
35. Lynn, B., Carpenter, S.E., Pini, A., 1984. Capsaicin and cutaneous afferents. In: Chahl, L.A., Szolcsányi, J., Lembeck, F. (Eds.), Antidromic Vasodilatation an Neurogenic Inflammation. Akadémia Kiadó, Budapest, pp. 83-92.
36. Manning P.T., Powers C.W., Schmidt R.E., Johnson E.M. Jr. Guanethidine-induced destruction of peripheral sympathetic neurons occurs by an immune-mediated mechanism. J. Neurosci. 3:1983;714-724.
37. Manning P.T., Russell J.H., Johnson E.M. Jr. Immunosuppressive agents prevent guanethidine-induced destruction of rat sympathetic neurons. Brain Res. 241:1982;131-143.
38. Marsh S.J., Stansfeld C.E., Brown D.A., Davey R., McCarthy D. The mechanism of action of capsaicin on sensory C-type neurons and their axons in vitro. Neuroscience. 23:1987;275-290.
39. McCarthy M., Kent C., Mayhew T.M. Effects of neonatal capsaicin administration on the number and volume of neurons in left and right T10 dorsal root ganglia in the rat. J. Neurocytol. 28:1999;161-169.
40. McDougal D.B. Jr., McDougal S.H., Johnson E.M. Jr. Effect of capsaicin upon fluoride sensitive acid phosphatases in selected ganglia and spinal cord upon neuronal size and number in dorsal root ganglion. Brain Res. 331:1985;63-70.
41. Mendell L.M. Neurotrophin action on sensory neurons in adults: an extension of the neurotrophic hypothesis. Pain. 6:1999;127-132.
42. Michael G.J., Priestley J.V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its down regulation by axotomy. J. Neurosci. 19:1999;1844-1854.
43. Nagy J.I., Vincent W.M., Staines A., Fibiger H.C., Reisine T.D., Yamamura H.I. Neurotoxic action of capsaicin on spinal substance P neurons. Brain Res. 186:1980;435-444.
44. Nagy J.I., Iversen L.L., Goedert M., Chapman D., Hunt S.P. Dose-dependent effects of capsaicin on primary sensory neurons in the neonatal rat. J. Neurosci. 3:1983;399-406.
45. Otten U., Lorez H.P., Businger F. Nerve growth factor antagonize the neurotoxic action of capsaicin on primary sensory neurones. Nature. 301:1983;515-517.
46. Scadding J.W. The permanent anatomical effects of neonatal capsaicin on somatosensory nerves. J. Anat. 131:1980;473-484.
47. Shu X., Mendell L.M. Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci. Lett. 274:1999;159-162.
48. Sugimoto T., Takayama A., Xiao C., Takano-Yamamoto T., Ichikawa H. Electron microscopic demonstration of nick end-labeled DNA fragments during capsaicin-induced apoptosis of trigeminal primary neurons in neonatal rats. Brain Res. 818:1999;147-152.
49. Sugimoto T., Xiao C., Ichikawa H. Neonatal primary neuronal death induced by capsaicin and axotomy involves an apoptotic mechanism. Brain Res. 807:1998;147-154.
50. Szallasi A., Blumberg P.M. Vanilloid (capsaicin) receptors and mechanisms. Pharmacol. Rev. 51:1999;159-211.
51. Szallasi A., Joó F., Blumberg P. Duration of desensitization and ultrastructural changes in dorsal root ganglia of rats treated with resiniferatoxin, an ultrapotent capsaicin analog. Brain Res. 503:1989;68-72.
52. Szolcsányi, J., 1982. Capsaicin type pungent agents producing pyrexia. In: Milton, A.S. (Ed.), Handbook of Experimental Pharmacology, Pyretics and Antipyretics, Vol. 60. Springer-Verlag, Berlin, pp. 437-478.
53. Szolcsányi, J., 1990. Capsaicin, irritation and desensitization. Neurophysiological basis and future perspectives. In: Green, B.G., Mason, J.R., Kare, M.R. (Eds.), Irritation, Chemical Senses, Vol. 2. Marcel Dekker, New York, pp. 141-168.
54. Szolcsányi, J., 1996. Neurogenic Inflammation: reevaluation of axon reflex theory. In: Geppetti, P., Holzer, P. (Eds.). Neurogenic Inflammation. CRC, Boca Raton, FL, pp. 35-44.
55. Szolcsányi J., Anton F., Reeh P.W., Handwerker H.O. Selective excitation by capsaicin of mechano-heat sensitive nociceptors in rat skin. Brain Res. 446:1988;262-268.
56. Szolcsányi J., Jancsó-Gábor A., Joó F. Functional and fine structural characteristics of the sensory neuron blocking effect of capsaicin. Naunyn-Schmiedeberg's Arch. Pharmacol. 287:1975;157-169.
57. Szolcsányi J., Joó F., Jancsó-Gábor A. Mitochondrial changes in preoptic neurones after capsaicin desensitization of the hypothalamic thermodetectors in rats. Nature. 299:1971;116-117.
58. Szolcsányi J., Szallasi A., Szallasi Z., Joó F., Blumberg P.M. Resiniferatoxin: an ultrapotent selective modulator of capsaicin-sensitive primary afferent neurons. J. Pharmacol. Exp. Ther. 255:1990;923-928.
59. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Baumann B.E., Basbaum A.I., Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 21:1998;531-543.
60. Welk E., Fleisher E., Petsche U., Handwerker H.O. Afferent C-fibres in rats after neonatal capsaicin treatment. Pflug. Arch. 400:1984;66-71.
61. Winter J., Forbes C.A., Sternberg J., Lindsay R.M. Nerve growth factor (NGF) regulates adult rat cultured dorsal root ganglion neuron responses to the excitotoxin capsaicin. Neuron. 1:1988;973-981.
62. Winter, J., Woolf, C., Lynn, B., 1993. Degenerative and regenerative responses of sensory neurones to capsaicin-induced damage. In: Wood, J.N. (Ed.), Capsaicin in the Study of Pain. Academic, New York, pp. 139-160.