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Acta Biologica Hungarica

, Volume 53, Issue 1–2, pp 167–175 | Cite as

Age-Related Mitochondrial Damage in The B-Type Cells of the Rat Trigeminal Ganglia

  • L. SeressEmail author
  • Éva Szőke
  • G. Czéh
Article

Abstract

Aging is associated with signs of sensory impairment and neurological symptoms. Advancing age is characterized by increased thresholds of thermal, tactile and vibratory sensations. One important cause of the sensory disturbances has been stated to be the loss of neurons. Decreases have been observed in the number of peripheral nerve fibers and in the number of neurons in the spinal ganglia of rats.

In the present study, the cytoplasmic organelles of the neurons of the trigeminal ganglia were examined in young and senescent rats in order to reveal the cause of cell loss during aging. Mitochondrial alterations, swelling and loss of internal cristae were observed from 23 week of age in the B-type neurons of the trigeminal ganglia. Other cytoplasmic elements were intact. Mitochondrial damage was never seen in A-type neurons and satellite glial cells.

It was concluded that the ultrastructural changes in the mitochondria of the B-type cells may contribute to the nervous disturbances that occur in senescent individuals. The diminution of mitochondrial damage and the protection of B-type neurons through the use of nerve growth factors may prevent the sensory impairment late in life.

Keywords

Aging capsaicin mitochondrial alterations sensory disturbances sensory ganglia 

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References

  1. 1.
    Andres, K. H. (1961) Untersuchungen über den Feinbau von Spinalganglien. Z. Zellforsch. Mikrosk. Anat. 55, 1–48.CrossRefGoogle Scholar
  2. 2.
    Berg, B. N., Wolf, A., Simms, H. S. (1962) Degenerative lesions of spinal roots and peripheral nerves in aging rats. Gerontologia (Basel) 6, 72–80.CrossRefGoogle Scholar
  3. 3.
    Bergman, E., Ulfhake, B. (1998) Loss of primary sensory neurons in the very old rat: neuron number estimates using the disector method and confocal optical sectioning. J. Comp. Neurol. 396, 211–222.CrossRefGoogle Scholar
  4. 4.
    Bevan, S., Szolcsányi, J. (1990) Sensory neuron-specific actions of capsaicin: mechanisms and applications. Trends Pharmacol. Sci. 11, 330–333.CrossRefGoogle Scholar
  5. 5.
    Biedenbach, M. A., Kalu, D. N., Herbert, D. C. (1992) Effects of aging and food restriction on the trigeminal ganglion: a morphometric study. Mech. Ageing Dev. 65, 111–125.CrossRefGoogle Scholar
  6. 6.
    van den Bosch de Aguilar, P., Vanneste, J. (1981) Ultrastructural study of the neurons of the spinal ganglia during aging in the rat. Acta Anat. (Basel) 110, 59–70.CrossRefGoogle Scholar
  7. 7.
    Caramia, F., Angeletti, P. U., Levi-Montalcini, R., Carratelli, L. (1972) Mitochondrial lesions of developing sympathetic neurons induced by bretylium tosylate. Brain Res. 40, 237–246.CrossRefGoogle Scholar
  8. 8.
    Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., Julius, D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824.CrossRefGoogle Scholar
  9. 9.
    Cavanagh, J. B. (1964) The significance of the “dying back” process in experimental and human neurological disease. Int. Rev. Exp. Pathol. 3, 219–267.PubMedGoogle Scholar
  10. 10.
    Chiba, T., Masuko, S., Kawano, H. (1986) 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, 311–316.CrossRefGoogle Scholar
  11. 11.
    Dedov, V. N., Roufogalis, B. D. (2000) Mitochondrial calcium accumulation following activation of vanilloid (VR1) receptors by capsaicin in dorsal root ganglion neurons. Neurosci 95, 183–188.CrossRefGoogle Scholar
  12. 12.
    Duchen, L. W., Scaravilli, F. (1977) Quantitative and electron microscopic studies of sensory ganglion cells of the Sprawling mutant mouse. J. Neurocytol. 6, 465–481.CrossRefGoogle Scholar
  13. 13.
    Dyck, P. J., Karnes, J., O’Brian, P. C., Zimmerman, I. (1984) Detection thresholds of cutaneous sensations in humans. In: Dyck, P. J., Thomas, P. K., Lambert, E. H., Bunge, R. (eds), Peripheral Neuropathy. Saunders, Philadelphia, pp. 1103–1138.Google Scholar
  14. 14.
    Emery, L., Singhal, R. (1973) Changes associated with growth in the cells of the dorsal root ganglion in children. Dev. Med. Child. Neurol. 15, 460–466.CrossRefGoogle Scholar
  15. 15.
    Gardner, E. (1940) Decrease in human neurones with ages. Anat. Rec. 77, 529–536.CrossRefGoogle Scholar
  16. 16.
    Gilmore, S. A. (1972) Spinal nerve root degeneration in aging laboratory rats: a light microscopic study. Anat. Rec. 174, 251–257.CrossRefGoogle Scholar
  17. 17.
    Goemaere-Vanneste, J., van den Bosch de Aguilar, P. (1987) Study of the peripheral nerve fibers during aging in the rat. Cellule 74, 263–279.PubMedGoogle Scholar
  18. 18.
    Hatai, S. (1902) Number and size of the spinal ganglion cells and dorsal root fibers in the white rat at different ages. J. Comp. Neurol. 12, 107–124.CrossRefGoogle Scholar
  19. 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.Google Scholar
  20. 20.
    Jancsó, G., Király, E., Jancsó-Gábor, A. (1977) Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 270, 741–743.CrossRefGoogle Scholar
  21. 21.
    Jancsó-Gábor, A., Szolcsányi, J., Jancsó, N. (1970) Stimulation and desensitization of the hypothalamic heat-sensitive structures by capsaicin in rats. J. Physiol. 208, 449–459.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Jancsó, N., Jancsó-Gábor, A., Szolcsányi, J. (1967) Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br. J. Pharmacol. 31, 138–151.Google Scholar
  23. 23.
    Jellinger, K. (1973) Neuroaxonal dystrophy: Its natural history and related disorders. In: Jimmernan H. M. (ed.), Progress is Neuropathology. Grune and Stratton, London, pp. 129–180.Google Scholar
  24. 24.
    Joó, F., Szolcsányi, J., Jancsó-Gábor, A. (1969) Mitochondrial alterations in the spinal ganglion cells of the rat accompanying the long-lasting sensory disturbance induced by capsaicin. Life Sci. 8, 621–626.CrossRefGoogle Scholar
  25. 25.
    Lawson, S. N. (1979) The postnatal development of large light and small dark neurons in mouse dorsal root ganglia: a statistical analysis of cell numbers and size. J. Neurocytol. 8, 275–294.CrossRefGoogle Scholar
  26. 26.
    Lieberman, A. R. (1976) Sensory ganglia. In: Landon, D. N. (ed.), The Peripheral Nerve. Chapman and Hall, London, pp. 178–188.Google Scholar
  27. 27.
    Manning, P. T., Powers, C. W., Schmidt, R. E., Johnson, E. M., Jr. (1983) Guanethidine-induced destruction of peripheral sympathetic neurons occurs by an immune-mediated mechanism. J. Neurosci. 3, 714–724.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Manning, P. T., Russell, J. H., Johnson, E. M., Jr. (1982) Immunosuppressive agents prevent guanethidine-induced destruction of rat sympathetic neurons. Brain Res. 241, 131–143.CrossRefGoogle Scholar
  29. 29.
    Marsh, S. J., Stansfeld, C. E., Brown, D. A., Davey, R., McCarthy, D. (1987) The mechanism of action of capsaicin on sensory C-type neurons and their axons in vitro. Neuroscience 23, 275–290.CrossRefGoogle Scholar
  30. 30.
    Mezey, É., Tóth, Z. E., Cortright, D. N., Arzubi, M. K., Krause, J. E., Elde, R., Guo, A., Blumberg, P. M., Szallasi, Á. (2000) Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc. Natl. Acad. Sci. 97, 3655–3660.CrossRefGoogle Scholar
  31. 31.
    de Neeling, J. N., Beks, P. J., Bertelsmann, F. W., Heine, R. J., Bouter, L. M. (1994) Sensory thresholds in older adults: reproducibility and reference values. Muscle Nerve. 17, 454–461.CrossRefGoogle Scholar
  32. 32.
    Scharf, J. H., Blumenthal, H. J. (1967) Current aspects on the age-dependent involution of the sensory peripheral nervous system. Z. Zellforsch. Mikrosk. Anat. 78, 280–302.CrossRefGoogle Scholar
  33. 33.
    Sugimoto, T., Xiao, C., Ichikawa, H. (1998) Neonatal primary neuronal death induced by capsaicin and axotomy involves an apoptotic mechanism. Brain Res. 807, 147–154.CrossRefGoogle Scholar
  34. 34.
    Szallasi, A., Blumberg, P. M. (1999) Vanilloid (capsaicin) receptors and mechanisms. Pharmacol. Rev. 51, 159–211.PubMedGoogle Scholar
  35. 35.
    Szallasi, A., Joó, F., Blumberg, P. (1989) Duration of desensitization and ultrastructural changes in dorsal root ganglia of rats treated with resiniferatoxin, an ultrapotent capsaicin analog. Brain Res. 503, 68–72.CrossRefGoogle Scholar
  36. 36.
    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.CrossRefGoogle Scholar
  37. 37.
    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 and Basel, pp. 141–168.Google Scholar
  38. 38.
    Szolcsányi, J., Jancsó-Gábor, A., Joó, F. (1975) Functional and fine structural characteristics of the sensory neuron blocking effect of capsaicin. Naunyn-Schmiedeberg’s Arch. Pharmacol. 287, 157–169.CrossRefGoogle Scholar
  39. 39.
    Szolcsányi, J., Szallasi, A., Szallasi, Z., Joó, F., Blumberg, P. M. (1990) Resiniferatoxin: an ultrapotent selective modulator of capsaicin-sensitive primary afferent neurons. J. Pharmacol. Exp. Ther. 255, 923–928.PubMedGoogle Scholar
  40. 40.
    Szolcsányi, J., Szőke, É., Seress, L. (1998) Reevaluation of the neurotoxic effect of neonatal capsaicin treatment on rat’s trigeminal sensory neurons. Soc. Neurosci. Abstr. 24, 91.12.Google Scholar
  41. 41.
    Szőke, É., Seress, L., Szolcsányi, J. (1998) Reevaluation of the neurotoxic effect of neonatal capsaicin treatment on the basis of morphometrical studies. Neurobiology 6, 477–478.PubMedGoogle Scholar
  42. 42.
    Thomas, P. K., King, R. H., Sharma, A. K. (1980) Changes with age in the peripheral nerves of the rat. An ultrastructural study. Acta Neuropathol. (Berlin), 52, 1–6.CrossRefGoogle Scholar
  43. 43.
    Vanneste, J., van den Bosch de Aguilar, P. (1981) Mitochondrial alterations in the spinal ganglion neurons in ageing rats. Acta Neuropathol. (Berlin), 54, 83–87.CrossRefGoogle Scholar

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© Akadémiai Kiadó, Budapest 2002

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Central Electron Microscopic LaboratoryUniversity of PécsPécsHungary
  2. 2.Neuropharmacology Research Group of the Hungarian Academy of Sciences, Department of Pharmacology and Pharmacotherapy, Faculty of MedicineUniversity of PécsPécsHungary

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