Abstract
The reorganization of the GABAergic system was studied by means of immunohistochemistry after the symmetrical and asymmetrical (unilateral) extirpation of the brain of the anneli. Eisenia fetida. GABA-immunoreactive neurons were first observed in the wound tissue on the 3rd postoperative day. Thereafter the number of labelled cells gradually increased, and by postoperative days 76–80 all GABA-immunoreactive cells (approx. 140 neurons) could be found in their final positions in the symmetrically regenerated brain. After asymmetrical brain extirpation, nearly all cells (70–75) could be detected in the regenerating hemisphere by postoperative days 50–56. In the early stages of the asymmetrical regeneration of the brain, more GABAergic cells were concentrated dorsally and laterally in the preganglion than during the symmetrical type of regeneration.
In both types of regeneration, the immunoreactive neurons in the regenerated brain originated in part from undifferentiated neuroblasts situated in different parts of the body, and in part from dividing neurons localized mainly in the pharyngeal nerve plexus.
Both exogenous GABA and picrotoxin, applied during the early stages (days 10–12) of brain regeneration, inhibited the development of the wound tissue and the migration of the neuroblasts and the enteric neurons. At the same time, exogenous GABA application accelerated the proliferation of the pharyngeal neurons. No effect on the process of regeneration could be demonstrated when exogenous GABA and picrotoxin were given together.
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Antonopoulos, J., Pappas, I. S., Pamavelas, J. G. (1997) Activation of the GABAA receptor inhibits the proliferative effects of bFGF in cortical progenitor cells. Eur. J. Neurosci. 9, 291–298.
Baguna, J., Romero, R., Saló, E., Collet, J., Auladell, C., Ribas, M., Riutort, M., Garcia-Fernandez, J., Burgaya, F., Boeno, D. (1990) Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians. In: Marthy, H. (ed.). Experimental Embryology in Aquatic Plants and Animals. Plenum Press, New York, pp. 129–162.
Bánvölgyi, T., Barna, J., Csoknya, M., Lengvári, I., Hámori, J. (1994) The number of ganglion cells in the intact and regenerated nervous system in the earthworm (Lumbricus terrestris). Acta Biol. Hung. 45, 179–187.
Barr, H. J. (1964) Regeneration and natural selection. Am. Natural J. 118, 183–186.
Bautz, A., Schilt, J. (1986) Somatostatin-like peptide and regeneration capacities in planarians. Gen. Comp. Endocrinol. 64, 267–272.
Boer, H., Schot, L. P. C., Roubos, E. W., terMaat, A., Loddel, J. C., Reichelt, D. (1979) ACTH-like immunoreactivity in two electrotonically coupled giant neurons in the pond snai. Lymnaea stagnalis. Cell Tissue Res. 202, 231–240.
Bollner, T., Beesley, P. W., Thorndyke, M. C. (1993) Distribution of GABA-like immunoreactivity during post-metamorphic development and regeneration of the central nervous system in the ascidi-a. Ciona intestinalis. Cell Tissue Res. 272, 553–561.
Chole, R. N., Morell, R. J., Zipser, B. (1989) Glial processes, identified through their glial-specific 130 kD surface glycoprotein, are juxtaposed to sites of neurogenesis in the leech germinal plate. Glia 2, 446–457.
Cornec, J. P. (1984) Modification ultrastructurales aprés amputation dans le territoire de régénération postérieure de l’Hirudiné Rhynchobdell. Helobdella stagnalis: mise en place et évolution du bouchon cicatriciel. Arch. Anat. microsc. Morphol. Exp. 73, 269–289.
Csoknya, M., Lengvári, I., Hiripi, L., Elekes, K., Vincze, J., Szelier, M., Hámori, J. (1993) Serotonin content during the regeneration of nervous system in earthworm (Lumbricus terrestris L., Oligochaeta). Acta Biol. Szeged 39, 39–49.
Csoknya, M., Barna, J., Hiripi, L., Hámori, J., Elekes, K. (2001) Reorganization of monoaminergic systems in the earthworm (Eisenia fetida), following brain extirpation. J. Exp. Zool. (submitted).
Gardner, C. R., Walker, R. J. (1982) The roles of putative neurotransmitters and neuromodulators in annelids and related invertebrates. Prog. Neurobiol. 18, 81–120.
Ghosh, A., Greenberg, M. E. (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15, 89–103.
Golding, D. W. (1967) Nerosecretion and regeneration i. Nereis. I. Regeneration and the role of the supraesophageal ganglion. Gen. Comp. Endocrin. 8, 348–355.
Gustafsson, M. K. S. (1976) Observations on the histogenesis of nervous tissue i. Diphyllobothrium dendriticum Nitzsch, 1824 (Cestoda, Pseudophyllidea). Z. Parasitenk. 50, 313–321.
Herlant-Meewis, H., Deligne, J. (1965) Influence of the nervous system on regeneration in Annelids. In: Kiortsis, V. and Trampusch, H. A. L. (eds). Regeneration in Animals and Related Problems. North-Holland Publ. Co., Amsterdam, pp. 228–238.
Hibbard, E. (1963) Regeneration in the severed spinal cord of the cordate larvae o. Petromyzon mar-inus. Exp. Neurol. 7, 175–185.
Hulsebosch, C. E., Bittner, G. D. (1981) Regeneration of axons and nerve cell bodies in the CNS of Annelids. J. Comp. Neurol. 198, 77–88.
Javois, L. C., Bode, P. M., Bode, H. R. (1988) Patterning of the head in hydra as visualized by a monoclonal antibody. II. The initiation and localization of head structures in regenerating pieces of tissue. Dev. Biol. 129, 390–399.
Kelemen, J. (1965) Methode zur Impregnation des in Paraffin eingebetteten Nervengewebes. Acta Neuropath. 4, 431–435.
Koritsánszky, S., Hartwig, H. G. (1974) The regeneration of the monoaminergic system in the cerebral ganglion of the earthworm. Allolobophora caliginosa. A morphological and microspectrofluo-rometrical analysis. Cell Tissue Res. 151, 171–186.
Kurabuchi, S., Kishida, Y. (1992) Effect of delay in anterior or posterior amputation on regeneration of short fragments of planaria. Zool. Sci. 9, 575–581.
Lauder, J. M. (1993) Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci. 16, 233–240.
Laurie, D. H., Wisden, W., Seeburg, P. H. (1992) The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci. 12, 4151–4172.
Lender, T. (1974) The role of neurosecretion in freshwater planarian. In: Riser, N. W. and Morse, M. P. (eds). Biology of the Turbellarian. McGraw-Hill Book Co., New York, pp. 460–475.
Lyckman, A. W., Bittner, G. D. (1992) Axonal conduction and electrical coupling in regenerating earthworm giant axons. Exp. Neurol. 117, 299–306.
Lyckman, A. W., Heildelbaugh, S. M., Bittner, G. D. (1992) Analysis of neuritic outgrowth from severed giant axons i. Lumbricus terrestris. J. Comp. Neurol. 318, 426–438.
Martelly, I., Moraczewsky, J., Franquiner, R., Castagne, M. (1987) Protein kinase C activity in a freshwater planarian (Dugesia gonocephala). Comp. Biochem. Physiol. 86B, 405–409.
Meier, E., Hertz, L., Schousboe, A. (1991) Neurotransmitters as developmental signals. Neurochem. Int. 19, 1–15.
Mhatre, M. C., Ticku, M. K. (1994) Chronic GABA treatment downregulates the GABAA receptor a2 and a3 subunit mRNAS as well as polypeptide expression in primary cultured cerebral cortical neurons. Mol. Brain Res. 24, 159–165.
Michler-Stuke, A., Wolff, J. R. (1987) Facilitation and inhibition of neurite elongation by GABA in chick tectal neurons. In: Redburn, D. A. and Schousboe, A. (eds), Neurotrophic Activity of GABA During Development. Neurol. Neurobiol. Vol. 32. Alan, R. Liss, New York, pp. 253–266.
Millott, N. (1943) The visceral nervous system of the earthworm: I. Nerves controlling the tone of the alimentary canal. Proc. Roy. Soc. Lond. B. 131, 271–295.
Muller, K. J., Carbonetto, S. (1979) The morphological and physiological properties of a regenerating synapse in the CNS of the leech. J. Comp. Neurol. 185, 485–516.
Murate, M., Kishimoto, Y., Sugiyama, T., Fujisawa, T., Takahashi-Iwanaga, H., Iwanaga, T. (1997) Hydra regeneration from recombined ectodermal and endodermal tissue. II. Differential stability in the ectodermal and endodermal epithelial organization. J. Cell Sci. 110, 1919–1934.
Needham, A. E. (1952). Regeneration and Wound Healing. John Wiley and Sons, Inc. New York.
Redburn, D. A., Schousboe, A. (eds), (1987) Neurotrophic activity of GABA during development. Neurol. Neurobiol. 32, 1–27.
Reuter, M., Gustafsson, M. (1996) Neuronal signal substances in asexual multiplication and development in flatworms. Cell. Mol. Neurobiol. 16, 591–616.
Reuter, M., Sheiman, I. M., Gustafsson, M. K. S., Halton, D. W., Maule, A. G., Shaw, C. (1996) Development of the nervous system i. Dugesia tigrina during regeneration after fission and decapitation. Invertebr. Repr. Dev. 29, 199–211.
Seshan, K. R., Bittner, G. D. (1987) Developmental and other factors affecting regeneration of crayfish CNS axons. J. Comp. Neurol. 262, 535–545.
Telkes, I., Csoknya, M., Buzás, P., Gábriel, R., Hámori, J., Elekes, K. (1996) GABA-immunoreactive neurons in the central and peripheral nervous system of the earthworm. Lumbricus terrestris (Oligochaeta, Annelida). Cell Tissue Res. 285, 463–475.
Thorey, I. S., Zipser, B. (1991) The segmentation of the leech nervous system is prefigured by myo-genic cells at the embryonic midline expressing a muscle-matrix protein. J. Neurosci. 11, 1786–1799.
Van Eden, C. G., Mrzljak, L., Voorn, P., Uylings, H. B. M. (1989) Prenatal development of GABAergic neurons in the neocortex of the rat. J. Comp. Neurol. 289, 213–227.
Zimmermann, P. (1967) Fluoreszenzmikroskopische Studien über die Verteilung und Regeneration der Faserglia be. Lumbricus terrestris L. Z. Zellforsch. 81, 190–220.
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Dedicated to Professor József Hámori on the occasion of his 70th birthday.
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Csoknya, M., Barna, J. & Elekes, K. Reorganization of the Gabaergic System Following Brain Extirpation in the Earthworm (Eisenia Fetida, Annelida, Oligochaeta). BIOLOGIA FUTURA 53, 43–58 (2002). https://doi.org/10.1556/ABiol.53.2002.1-2.6
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DOI: https://doi.org/10.1556/ABiol.53.2002.1-2.6