Advertisement

Cellular and Molecular Neurobiology

, Volume 16, Issue 2, pp 213–223 | Cite as

Potential neuronal mechanisms of estrogen actions in synaptogenesis and synaptic plasticity

  • F. Naftolin
  • C. Leranth
  • T. L. Horvath
  • L. M. Garcia-Segura
Article

Summary

1. Studies conducted on the rat arcuate nucleus, an area involved in the development and control of LH and FSH secretion, have shown the existence of hormonally regulated developmental sex differences in synaptic patterns and estrogen-induced synaptic plasticity during adult life. Several questions raised by these findings are examined in this review:

2. The mechanisms of estrogen-regulated developmental synaptogenesis. These include the role of glycocalyx glycoproteins in neuronal membranes, neural cell adhesion molecules, and insulin-like growth factor I.

3. The relationship among circulating estrogen, gonadotropin levels, and hypothalamic synaptic plasticity. Recent evidence for the role of GABAergic and dopaminergic synaptic inputs and POMC projections from the arcuate nucleus to the GnRH cells is discussed.

4. The synaptologic basis of age-related failure of positive feedback. The role of the cumulative effect of repeated preovulatory synaptic retraction and reapplication cycles on sensescent constant estrus is analyzed.

Key words

estradiol arcuate nucleus gonadotropin releasing hormone ovarian cycle synaptogenesis synaptic plasticity GABA dopamine β-endorphin neural cell adhesion molecule insulin-like growth factor I 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acheson, A., Sunshine, J. L., and Ruthishauser, U. (1991). NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions.J. Cell Biol. 114143–153.PubMedGoogle Scholar
  2. 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.PubMedGoogle Scholar
  3. Doherty, P., Cohen, J., and Walsh, F. S. (1990). Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysiallic acid.Neuron 5209–219.PubMedGoogle Scholar
  4. DueSNOW;as, M., Luquin, S., Chowen, J. A., Torres-Aleman, I., Naftolin, F., and Garcia-Segura, L. M. (1994). Gonadal hormone regulation of insulin-like growth factor-I-like immunoreactivity in hypothalamic astroglia of developing and adult rats.Neuroendocrinology 59528–538.PubMedGoogle Scholar
  5. Edelman, G. M. (1986). Cell adhesion molecules in neural histogenesis.Annu. Rev. Physiol. 48417–430.PubMedGoogle Scholar
  6. Garcia-Segura, L. M., Baetens, D., and Naftolin, F. (1986). Synaptic remodeling in the arcuate nucleus after injection of estradiol valerate in adult female rats.Brain Res. 366131–136.PubMedGoogle Scholar
  7. Garcia-Segura, L. M., Perez, 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.PubMedGoogle Scholar
  8. Garcia-Segura, L. M., Perez, J., Jones, E., and Naftolin, F. (1991). Loss of sexual dimorphism in rat arcuate nucleus neuronal membranes with reproductive aging.Exp. Neurol. 112125–128.PubMedGoogle Scholar
  9. Garcia-Segura, L. M., Chowen J. A., Párducz, A., and Naftolin, F. (1994). Gonadal hormones as promoters of structural synaptic plasticity: Cellular mechanisms.Prog. Neurobiol. 44279–307.PubMedGoogle Scholar
  10. Garcia-Segura, L. M., CaSNOW;as, B., Parducz, A., Rougon, G., Theodosis, D., Naftolin, F., and Torres-Aleman, I. (1995). Estradiol promotion of changes in the morphology of astrologia growing in culture depends on the expression of polysialic acid on neural membranes.Glia 13209–216.PubMedGoogle Scholar
  11. Knobil, E. (1980). The neuroendocrine control of the menstrual cycle.Rec. Prog. Horm. Res. 3653–88.PubMedGoogle Scholar
  12. Leranthal, C., Naftolin, F., Shanabrough, M., and Horvath, T. L. H. (1994). Electron microscopic double and triple labeling immunocytochemistry in the elucidation of synaptological interactions between ovarian steroid-sensitive neutrons and circuits. InMethods in Neuroscience (P. M. Conn, Ed.) (in press).Google Scholar
  13. Lewis, C. E., and Naftolin, F. (1994). Morphological effects of estradiol valerate on presynaptic catecholaminergic and GABAergic nerve terminals.Soc. Neurosci. Abstr. 20(1):100.Google Scholar
  14. Lu, J. K. H., Matt, D. W., and LaPolt, P. S. (1990). Modulatory effects of estrogens and progestins on female reproductive aging. InOvarian Secretions and Cardiovascular and Neurological Function (F. Naftolin, J. N. Gutmann, A. H. DeCherney, and P. M. Sarrel, Eds.), Raven Press, New York, pp. 287–296.Google Scholar
  15. MacLusky, N. J., and Naftolin, F. (1981). Sexual differentiation of the central nervous system.Science 2111294–1303.PubMedGoogle Scholar
  16. Matsumoto, A., and Arai, Y. (1976a). Effect of estrogen on early postnatal development of synaptic formation in the hypothalamic arcuate nucleus of female rats.Neurosci. Lett. 279–82.Google Scholar
  17. Matsumoto, A., and Arai, Y. (1976b). Developmental changes in synaptic formation in the hypothalamic arcuate nucleus of female rats.Cell Tissue Res. 169143–156.PubMedGoogle Scholar
  18. Matsumoto, A., and Arai, Y. (1977). Precoccious puberty and synaptogenesis in the hypothalamic arcuate nucleus in pregnant serum gonadotrophin (PMSG) treated immature female rats.Brain Res. 129275–278.PubMedGoogle Scholar
  19. Mitsushima, D., Hei, D. L., and Terasawa, E. (1994). Gamma-aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty.Proc. Natl. Acad. Sci. USA 91395–399.PubMedGoogle Scholar
  20. Naftolin, F., and MacLusky, N. J. (1984). Aromatization hypothesis revisited. InSexual Differentiation: Basic and Clinical Aspects (M. Serio, M. Motta, M. Zanisi, and L. Martini, Eds.), Raven Press, New York. pp. 79–82.Google Scholar
  21. Naftolin, F., Garcia-Segura, L. M., Keefe, D., Leranth, C., MacLusky, N. J., and Brawer, J. R. (1990). Estrogen effect on the synaptology and neural membranes of the rat hypothalamic arcuate nucleus.Biol. Reprod. 4221–28.PubMedGoogle Scholar
  22. Ojeda, S. R., and Urbanski, H. F. (1993). Intracellular regulatory mechanisms of LHRH secretion and the onset of female puberty. InNeuroendocrine Control of the Hypothalamic-Pituitary System (H. Imura, Ed.), Japan Scientific Press, Tokyo, pp. 49–64.Google Scholar
  23. 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.PubMedGoogle Scholar
  24. Párducz, A., Pérez, J., and Garcia-Segura, L. M. (1993). Estradiol induces plasticity of GABAergic synapses in the hypothalamus.Neuroscience 53395–401.PubMedGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. Pons, S., and Torres-Aleman, I. (1993). Estradiol modulates insulin-like growth factor I receptors and binding proteins in neurons from the hypothalamus.J. Neuroendocrinol. 5267–271.PubMedGoogle Scholar
  27. Rougon, G. (1993). Structure, metabolism and cell biology of polysialic acids.Eur. J. Cell Biol. 61197–207.PubMedGoogle Scholar
  28. Ruf, K. B. (1973). How does the brain control the process of puberty?Z. Neurol. 20495–105.Google Scholar
  29. Ruthishauser, U. (1992). NCAM and its polysialic acid moiety: A mechanism for pull/push regulation of cell interactions during development?Development (Suppl.) 99–104.Google Scholar
  30. Toran-Allerand, C. D. (1976). Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: Implication for sexual differentiation.Brain Res. 106407–412.PubMedGoogle Scholar
  31. Toran-Allerand, C. D., Ellis, L., and Pfenninger, K. H. (1988). Estrogen and insulin synergism in neurite growth enhancementin vitro: Mediation of steroid effects by interactions with growth factors?Dev. Brain Res. 4187–100.Google Scholar
  32. Walsh, R., Brawer, J., and Naftolin, F. (1982). Early postnatal development of the arcuate nucleus in normal sexually reversed male and female rats.J. Anat. 135733–734.PubMedGoogle Scholar
  33. Wise, P. M., Weiland, N. G., Scarbrough, K., Larson, G. H., and Lloyd, J. M. (1990). Effects of aging on reproductive neuroendocrine function. InSexual Differentiation: Basic and Clinical Aspects (M. Serio, M. Motta, M. Zanisi, and L. Martini, Eds.), Raven Press, New York, pp. 287–296.Google Scholar
  34. Witkin, J. W., and Silverman, A. J. (1985). Synaptology of luteinzing hormone-releasing hormone neurons in rat preoptic area.Peptides 6263–271.PubMedGoogle Scholar
  35. 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.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • F. Naftolin
    • 1
  • C. Leranth
    • 1
  • T. L. Horvath
    • 1
  • L. M. Garcia-Segura
    • 2
  1. 1.Department of Obstetrics and GynecologyYale University School of MedicineNew Haven
  2. 2.Instituto Cajal, CSICMadridSpain

Personalised recommendations