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Neuroplastic changes in the hypothalamic arcuate nucleus: The estradiol effect is accompanied by increased exoendocytotic activity of neuronal membranes

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Summary

1. In the rat hypothalamic arcuate nucleus, estradiol induces coordinated changes in the number of axosomatic synapses, the amount of glial ensheathing, and the ultrastructure of the membrane of neuronal somas. In the present study we used conventional electron microscopy and freeze-fracture to examine cellular mechanisms responsible for the estradiol-induced chages at the membrane level.

2. In freeze-fracture replicas taken 10–60 min and 24 hr after injection of 17β-estradiol to adult ovariectomized females, it was found that there was a rapid increase in the number of exoendocytotic images that reached a plateau by 30 min.

3. In thin sections from animals injected 24 hr earlier we demonstrated a significant increase in coated vesicles in the periphery of the neurons and coated pits in the perikaryal membranes and decreased axosomatic synapses.

4. We conclude that these morphological alterations are signaling estrogen-induced transport and/or turnover of perikaryal membrane constituents and extracellular components which may affect interneuronal and neuroglial interactions.

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References

  • Altman, J. (1971). Coated vesicles and synaptogenesis. A developmental study in the cerebellar cortex of the rat.Brain Res. 30311–322.

    PubMed  Google Scholar 

  • Arnold, A. P., and Gorski, R. A. (1984). Gonadal steroid induction of structural sex differences in the central nervous system.A. Rev. Neurosci. 7413–442.

    Google Scholar 

  • Bailey, C. H., Chen, M., Keller, F., and Kandel, E. R. (1992). Serotonin-mediated endocytosis of apCAM: An early step of learning-related synaptic growth in Aplysia.Science 256645–649.

    PubMed  Google Scholar 

  • Bonfanti, L., Olive, S., Pulain, D. A., and Theodosis, D. T. (1992). Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: An immunohistochemical study.Neuroscience 49419–436.

    PubMed  Google Scholar 

  • Calverley, R. K. S., and Jones, D. G. (1987). A serial-section study of perforated synapses in rat neocortex.Cell Tissue Res. 247565–572.

    PubMed  Google Scholar 

  • Farquhar, M. G. (1983). Multiple pathways of exocytosis, endocytosis, and membrane recycling: Validation of a Golgi route.Fed. Proc. 42 2407–2413.

    PubMed  Google Scholar 

  • Frankfurt, M., Gould, E., Woolley, C. S., and McEwen, B. S. (1990). Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: A Golgi study in the adult rat.Neuroendocrinology 51530–535.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., and Perrelet, A. (1984). Postsynaptic membrane domains in the molecular layer of the cerebellum: a correlation between presynaptic inputs and postsynaptic plasma membrane organization.Brain Res. 321 255–266.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., Baetens, D., and Naftolin, F. (1985). Sex differences and maturational changes in arcuate nucleus neuronal plasma membrane organization.Dev. Brain. Res. 19146–149.

    Google Scholar 

  • Garcia-Segura, L. M., Baetens, D., and Naftolin, F. (1986). Synaptic remodelling in arcuate nucleus after injection of estradiol valerate in adult female rats.Brain Res. 366131–136.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., Olmos, G., Tranque, P., and Naftolin, F. (1987). Rapid effects of gonadal steroids upon hypothalamic neuronal membrane ultrastructure.J. Steroid Biochem. 27615–623.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., Hernandez, P., Olmos, G., Tranque, P. A., and Naftolin, F. (1988a). Neuronal membrane remodelling during the oestrus cycle: A freeze-fracture study in the arcuate nucleus of the rat hypothalamus.J. Neurocytol. 17377–383.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., Pérez, J., Tranque, P. A., Olmos, G., and Naftolin, F. (1988b). Sexual differentiation of the neuronal plasma membrane: Neonatal levels of sex steroids modulate the number of exo-endocytotic images in the developing rat arcuate neurons.Neurosci Lett. 9119–23.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., Pérez, J., Tranque, P. A., Olmos, G., and Naftolin, F. (1989). Sex differences in plasma membrane concanavalin A binding in the rat arcuate neurons.Brain Res. Bull. 22651–655.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., Chowen, J. A., Párducz, A., and Naftolin, F. (1994a). Gonadal hormones as promoters of structural synaptic plasticity: Cellular mechanisms. Progress inNeurobiology 44279–307.

    PubMed  Google Scholar 

  • Garcia-Segura, L. M., Luquín, S., Párducz, A., and Naftolin, F. (1994b). Gonadal hormone regulation of glial fibrillary acidic protein immunoreactivity and glial ultrastructure in the rat neuroendocrine hypothalamus.Glia 1059–69.

    PubMed  Google Scholar 

  • Goldstein, J. L., Anderson, R. G. W., and Brown, M. S. (1979). Coated pits, coated vesicles, and receptor-mediated endocytosis.Nature 279679–685.

    PubMed  Google Scholar 

  • Gould, E., Woolley, C. S., Frankfurt, M., and McEwen, B. S. (1990). Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood.J. Neurosci. 101286–1291.

    PubMed  Google Scholar 

  • Güldner, F. H. (1982). Sexual dimorphisms of axo-spine synapses and postsynaptic density material in the suprachiasmatic nucleus of the rat.Neurosci. Lett. 28145–150.

    PubMed  Google Scholar 

  • Leedy, M. G., Beattie, M. S., and Bresnahan, J. C. (1987). Testosterone induced plasticity of synaptic inputs to adult mammalian motoneurons.Brain Res. 424386–390.

    PubMed  Google Scholar 

  • Lewis, C. E., and Naftolin, F. (1994). Morphological effects of estradiol valerate on presynaptic catecholaminergic and GABAergic nerve terminals. 4th Annual Meeting of the Society for Neuroscience Abstract 47.2, p. 21.

  • Madeira, M. D., Sousa, N., and Paula-Barbosa, M. M. (1991). Sexual dimorphism in the mossy fiber synapses of the rat hippocampus.Exp. Brain Res. 87537–545.

    PubMed  Google Scholar 

  • Matsumoto, A. (1991). Synaptogenic action of sex steroids in developing and adult neuroendocrine brain.Psychoneuroendocrinology 1625–40.

    PubMed  Google Scholar 

  • Matsumoto, A., and Arai, Y. (1980). Sexual dimorphism in “wiring pattern” in the hypothalamic arcuate nucleus and its modification by neonatal hormonal environment. Brain Res.190238–242.

    PubMed  Google Scholar 

  • Matsumoto, A., and Arai, Y. (1986). Male-female difference in synaptic organization of the ventromedial nucleus of the hypothalamus.Neuroendocrinology 42233–236.

    Google Scholar 

  • Naftolin, F. (1981). Understanding the bases of sexual differences.Science 2111263–1264.

    PubMed  Google Scholar 

  • Naftolin, F., Garcia-Segura, L. M., Keefe, D., Leranth, C., Maclusky, N. J., and Braver, J. R. (1990). Estrogen effects on the synaptology and neural membranes of the rat hypothalamic arcuate nucleus.Biol. Reprod. 4221–28.

    PubMed  Google Scholar 

  • Naftolin, F., Leranth, C., Pérez, J., and Garcia-Segura, L. M. (1993). Estrogen induces synaptic plasticity in adult primate neurons.Neuroendocrinology 57935–939.

    PubMed  Google Scholar 

  • Olmos, G., Aguilera, P., Tranque, P., Naftolin, F., and Garcia-Segura, L. M. (1987). Estrogen-induced synaptic remodelling in adult rat brain is accompanied by the reorganization of neuronal membranes.Brain Res. 42557–64.

    PubMed  Google Scholar 

  • Olmos, G., Naftolin, F., Pérez, J., Tranque, P. A., and Garcia-Segura, L. M. (1989). Synaptic remodelling in the rat arcuate nucleus during the estrous cycle.Neuroscience 32663–667.

    PubMed  Google Scholar 

  • Párducz, A., and Garcia-Segura, L. M. (1993). Sexual differences in the synaptic connectivity in the rat denatate gyrus.Neurosci. Lett. 16153–56.

    PubMed  Google Scholar 

  • Párducz, A., Pérez, J., and Garcia-Segura, L. M. (1993). Estradiol induces plasticity of GABAergic synapses in the hypothalamus.Neuroscience 53395–401.

    PubMed  Google Scholar 

  • Pérez, J., Naftolin, F., and Garcia-Segura, L. M. (1990). Sexual differentiation of synaptic connectivity and neuronal plasma membrane in the arcuate nucleus of the rat hypothalamus.Brain Res. 527116–122.

    PubMed  Google Scholar 

  • Pérez, J., Luquín, S., Naftolin, F., and Garcia-Segura, L. M. (1993). The role of estradiol and progesterone in phased synaptic remodelling of the rat arcuate nucleus.Brain Res. 60838–44.

    PubMed  Google Scholar 

  • Raisman, G., and Field, P. M. (1973). Sexual dimorphism in the neuropil of the preoptic area of the rat and its dependence on neonatal androgen.Brain Res. 541–29.

    PubMed  Google Scholar 

  • Regoeczi, E., Chindemi, P. A., DeBanne, M., and Charlwood, P. A. (1982). Partial resialylation of human asilotransferrin type 3 in the rat.Proc. Natl. Acad. Sci. USA 792226–2230.

    PubMed  Google Scholar 

  • Silva, W. I., Andres, A., Schook, W., and Puszkin, S. (1986). Evidence for the presence of muscarinic acetylcholine receptors in bovine brain coated vesicles.J. Biol. Chem. 26114788–14796.

    PubMed  Google Scholar 

  • Somogyi, P., and Hodgson, A. J. (1985). Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex.J. Histochem. Cytochem. 33249–257.

    PubMed  Google Scholar 

  • Theodosis, D. T., Rougon, G., and Poulain, D. A. (1991). Retention of embryonic features by an adult neuronal system capable of plasticity: polysialylated neural cell adhesion molecule in the hypothalamus-neurohypophysial system.Proc. Natl. Acad. Sci. USA 885494–5498.

    PubMed  Google Scholar 

  • Witkin, J. W., Ferin, M., Popilskis, S. J., and Silverman, A.-J. (1991). Effects of gonadal steroids on the ultrastructure of GnRH neurons in the rhesus monkey: Synaptic input and glial apposition.Endocrinology 1291083–1092.

    PubMed  Google Scholar 

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Párducz, A., Szilágyi, T., Hoyk, S. et al. Neuroplastic changes in the hypothalamic arcuate nucleus: The estradiol effect is accompanied by increased exoendocytotic activity of neuronal membranes. Cell Mol Neurobiol 16, 259–269 (1996). https://doi.org/10.1007/BF02088180

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  • DOI: https://doi.org/10.1007/BF02088180

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