Skip to main content
Log in

Neuronal membrane remodelling during the oestrus cycle: a freeze-fracture study in the arcuate nucleus of the rat hypothalamus

  • Published:
Journal of Neurocytology

Summary

Freeze-fracture methodology was used to study the organization of the neuronal plasma membrane in the rat arcuate nucleus, an oestrogen sensitive area of the hypothalamus. The quantitative evaluation of freeze-fracture replicas of the perikarya, dendritic shafts and dendritic spines revealed that the numerical density of intramembranous particles varied during the ovarian cycle. The number of small (< 10 nm) particles was decreased, and the number of large (> 10 nm) particles was increased, in the P-face of the perikaryal plasma membranes in prooestrus and oestrus when compared to dioestrus. This change was associated with a significant increase in the number of exo-endocytotic images in the perikaryal plasma membrane in prooestrus. Changes in intramembranous particles during the ovarian cycle were not detected in arcuate nucleus dendritic shafts and dendritic spines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arimatsu, Y. (1983) Short- and long-term influences of neonatal sex steroids on α-bungarotoxin binding capacity in the mouse amygdala.Neuroscience 9, 873–7.

    Google Scholar 

  • Biegon, A., Bercovitz, H. &Samuel, D. (1980) Serotonin receptor concentration during the estrous cycle of the rat.Brain Research 187, 221–5.

    Google Scholar 

  • Biegon, A., Fischette, C. T., Rainbow, T. C. &McEwen, B. S. (1982) Serotonin receptor modulation by estrogen in discrete brain nuclei.Neuroendocrinology 35, 287–91.

    Google Scholar 

  • Branton, D., Bullivant, S., Gilula, N. B., Karnovsky, M. J., Moor, H., MÜhlethaler, K., Northcote, D. H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L. A., Steere, R. L. &Weinstein, R. S. (1975) Freeze-etching nomenclature.Science 190, 54–6.

    Google Scholar 

  • Brawer, J. R. (1971) The role of arcuate nucleus in the brain-pituitary-gonad axis.Journal of Comparative Neurology 143, 411–46.

    Google Scholar 

  • Brawer, J. R., Naftolin, F., Martin, J. &Sonnenschein, C. (1987) Effects of a single injection of estradiol valerate on the hypothalamic arcuate nucleus and on reproductive function in the female rat.Endocrinology 103, 501–12.

    Google Scholar 

  • Brown, D. (1981) Polyvinyl alcohol coating: an improvement of the freeze-fracture technique.Journal of Microscopy 121, 283–7.

    Google Scholar 

  • Deliconstantinos, G. &Fotiou, S. (1986) Sex steroid and prostaglandin interactions upon the purified rat myometrial plasma membranes.Molecular and Cellular Endocrinology 45, 149–56.

    Google Scholar 

  • Di Paolo, T., Poyet, P. &Labrie, F. (1982) Effect of prolactin and estradiol on rat striatal dopamine receptors.Life Sciences 31, 2921–9.

    Google Scholar 

  • Drouva, S. V., Laplante, E., Gautron, J. P. &Kordon, C. (1984a) Effects of 17β-estradiol on LH-RH release from rat mediobasal hypothalamic slices.Neuroendocrinology 38, 152–7.

    Google Scholar 

  • Drouva, S. V., Leblanc, P., Laplante, E., L'heritier, A. &Kordon, C. (1984b) Effect of 17 β-estradiol on phospholipids methylation on rat pituitary membranes.Society for Neuroscience Abstracts 10, part 1, 91.

    Google Scholar 

  • Duncan, D. B. (1955) Multiple range and multiple F tests.Biometrics 11, 1–42.

    Google Scholar 

  • Dyer, R. G., Pritchetti, C. J. &Cross, B. A. (1972) Unit activity in the diencephalon of female rats during the oestrus cycle.Journal of Endocrinology 53, 151–60.

    Google Scholar 

  • Fischette, C. T., Biegon, A. &McEwen, B. S. (1983) Sex differences in serotonin 1 receptor binding in rat brain.Science 222, 333–5.

    Google Scholar 

  • Garcia-Segura, L. M., Baetens, D. &Naftolin, F. (1985) Sex differences and maturational changes in arcuate nucleus neuronal plasma membrane organization.Developmental Brain Research 19, 146–9.

    Google Scholar 

  • Garcia-Segura, L. M., Baetens, D. &Naftolin, F. (1986a) Synaptic remodelling in arcuate nucleus after injection of estradiol valerate in adult female rats.Brain Research 366, 131–6.

    Google Scholar 

  • Garcia-Segura, L. M., De Cozar, M., Moreno, M. C. &Monreal, J. (1986b) Freeze-fracture characterization of proteolipid protein and basic protein of central nervous system myelin incorporated to liposomes.Brain Research 380, 261–6.

    Google Scholar 

  • Garcia-Segura, L. M., Olmos, G., Tranque, P., Aguilera, P. &Naftolin, F. (1987a) Nuclear pores in rat hypothalamic arcuate neurons: sex differences and changes during the oestrus cycle.Journal of Neurocytology 16, 469–75.

    Google Scholar 

  • Garcia-Segura, L. M., Olmos, G., Tranque, P. &Naftolin, F. (1987b) Rapid effects of gonadal steroids upon hypothalamic neuronal membrane ultrastructure.Journal of Steroid Biochemistry 27, 615–23.

    Google Scholar 

  • Garcia-Segura, L. M. &Perrelet, A. (1984) Postsynaptic membrane domains in the molecular layer of the cerebellum: a correlation between presynaptic inputs and postsynaptic plasma membrane organization.Brain Research 321, 255–66.

    Google Scholar 

  • Ke, F.-C. &Ramirez, V. D. (1987) Membrane mechanism mediates progesterone stimulatory effect on LHRH release from superfused rat hypothalamiin vitro.Neuroendocrinology 45, 514–7.

    Google Scholar 

  • Kelly, M. J., Moss, R. L., Dudley, C. A. &Fawcett, C. P. (1977) The specificity of the response of preopticseptal area neurons to estrogen: 17-α-estradiol vs 17-β-estradiol and the response of extrahypothalamic neurons.Experimental Brain Research 30, 43–52.

    Google Scholar 

  • King, J. C., Williams, T. H. &Gerall, A. A. (1974) Transformations of hypothalamic arcuate neurons. I. Changes associated with stages of the estrous cycle.Cell and Tissue Research 153, 497–515.

    Google Scholar 

  • Koenig, H., Goldstone, A. &Lu, C. Y. (1982) Testosterone induces a rapid stimulation of endocytosis, amino acid and hexose transport in mouse kidney cortex.Biochemical and Biophysical Research Communications 106, 346–53.

    Google Scholar 

  • Koenig, H., Goldstone, A. &Lu, C. Y. (1983a) Androgenic stimulation of endocytosis, amino acid and hexose transport in mouse kidney cortex involves increased calcium fluxes.Biochimica et Biophysica Acta 762, 366–71.

    Google Scholar 

  • Koenig, H., Goldstone, A. &Lu, C. Y. (1983b) Polyamines regulate calcium fluxes in a rapid plasma membrane response.Nature 305, 530–4.

    Google Scholar 

  • Leranth, C., Sakamoto, H., MacLusky, N. J., Shanabrough, M. &Naftolin, F. (1985) Estrogen responsive cells in the arcuate nucleus of the rat contain glutamic acid decarboxylase (GAD): an electron microscopic immunocytochemical study.Brain Research 331, 376–81.

    Google Scholar 

  • Marchesi, V. T., Tillack, T. W., Jackson, R. L., Segrest, J. P. &Scott, R. E. (1972) Chemical characterization and surface orientation of the major glycoprotein of the human erythrocyte membrane.Proceedings of the National Academy of Sciences (USA) 69, 1445–9.

    Google Scholar 

  • Matsumoto, A. &Arai, Y. (1980) Sexual dimorphism in ‘wiring pattern’ in the hypothalamic arcuate nucleus and its modifications by neonatal hormonal environment.Brain Research 190, 238–42.

    Google Scholar 

  • Matsumoto, A. &Arai, Y. (1981) Neuronal plasticity in the deafferented hypothalamic arcuate nucleus of adult female rats and its enhancement by treatment with estrogen.Journal of Comparative Neurology 197, 197–205.

    Google Scholar 

  • Miller, M. M., Silver, J. &Billiar, R. B. (1984) Effects of gonadal steroids on thein vivo binding of [125α-bungarotoxin to the suprachiasmatic nucleus.Brain Research 290, 67–75.

    Google Scholar 

  • Moor, H. &Mühlethaler, K. (1963) Fine structure of frozen-etched yeast cells.Journal of Cell Biology 17, 609–28.

    Google Scholar 

  • Morrell, J. I., Krieger, M. S. &Pfaff, D. W. (1986) Quantitative autoradiographic analysis of estradiol retention by cells in the preoptic area, hypothalamus and amygdala.Experimental Brain Research 62, 343–54.

    Google Scholar 

  • Moss, R. L. &Law, O. T. (1971) The estrous cycle: its influence on single unit activity in the forebrain.Brain Research 30, 435–8.

    Google Scholar 

  • Nabekura, J., Oomura, Y., Minami, T., Mizuno, Y. &Fukuda, A. (1986) Mechanism of the rapid effect of 17-β-estradiol on medial amygdala neurons.Science 233, 226–8.

    Google Scholar 

  • Naftolin, F. &Brawer, J. R. (1978) The effect of estrogen on hypothalamic structure and function.American Journal of Obstetrics and Gynecology 132, 758–65.

    Google Scholar 

  • Naftolin, F., Brown-Grant, K. &Corker, C. (1972) Plasma and pituitary luteinizing hormone and peripheral plasma oestradiol concentrations in the normal oestrus cycle of the rat and after experimental manipulation of the cycle.Journal of Endocrinology 53, 17–30.

    Google Scholar 

  • Naftolin, F., Bruhlmann-Papazyan, M., Baetens, D. &Garcia-Segura, L. M. (1985) Neurons with whorl bodies have increased numbers of synapses.Brain Research 329, 289–93.

    Google Scholar 

  • Naftolin, F. &McLusky, N. J. (1984) Aromatization hypothesis revisited. InSexual Differentiation: Basic and Clinical Aspects (edited bySerio, M., Motta, M., Zanisi, M. &Martini, L.), pp. 79–92. New York: Raven Press.

    Google Scholar 

  • Olmos, G., Aguilera, P., Tranque, P., Naftolin, F. &Garcia-Segura, L. M. (1987) Estrogen-induced synaptic remodelling in adult rat brain is accompanied by the reorganization of neuronal membranes.Brain Research 425, 57–64.

    Google Scholar 

  • Orsini, J. C. (1985) Direct effect of androgens on lateral hypothalamic neuronal activity in the male rat. II. A pressure ejection study.Brain Research Bulletin 15, 547–52.

    Google Scholar 

  • Pfaff, D. &Keiner, M. (1973) Atlas of estradiolconcentrating cells in the central nervous system of the female rat.Journal of Comparative Neurology 151, 121–58.

    Google Scholar 

  • Pietras, R. J. &Szego, C. M. (1975) Endometrial cell calcium and oestrogen action.Nature 253, 357–9.

    Google Scholar 

  • Pinto Da Silva, P. (1972) Translational mobility of the membrane intercalated particles of human erythrocyte ghosts, pH-dependent, reversible aggregation.Journal of Cell Biology 53, 777–87.

    Google Scholar 

  • Rambo, C. O. &Szego, C. M. (1983) Estrogen action at endometrial membranes: alterations in luminal surface detectable within seconds.Journal of Cell Biology 97, 679–85.

    Google Scholar 

  • Raviazza, L., Nicoletti, F., Pozzi, O. &Barbaccia, M. L. (1985) Repeated daily treatments with estradiol increase the [3H] imipramine binding in male rat frontal cortex.European Journal of Pharmacology 107, 395–6.

    Google Scholar 

  • Rehavi, M., Sepcuti, H. &Weizman, A. (1987) Upregulation of imipramine binding and serotonin uptake by estradiol in female rat brain.Brain Research 410, 135–9.

    Google Scholar 

  • Sibbald, J. R., Sirett, N. E. &Hubbard, J. I. (1987) The influence of the estrous cycle, persistent estrus, ovariectomy and estrogen replacement, on the numbers and frequency of spontaneously active neurons in slices of the rat preoptic regionin vitro.Neuroscience Letters 76, 323–8.

    Google Scholar 

  • Stockert, M. &De Robertis, E. (1985) Effect of ovariectomy and estrogen on [3H] imipramine binding to different regions of the rat brain.European Journal of Pharmacology 119, 255–7.

    Google Scholar 

  • Stolinski, C. &Breathnach, A. S. (1975)Freeze-Fracture Replication of Biological Tissues, pp. 79–82 London: Academic Press.

    Google Scholar 

  • Teyler, T. J., Vardaris, R. M., Lewis, D. &Rawitch, A. B. (1980) Gonadal steroids: effects on excitability of hippocampal pyramidal cells.Science 209, 1017–9.

    Google Scholar 

  • Tsuruo, Y., Hisano, S., Okamura, Y., Tsukamoto, N. &Daikoku, S. (1984) Hypothalamic substance P-containing neurons. Sex-dependent topographical differences and ultrastructural transformations associated with stages of the estrous cycle.Brain Research 305, 331–41.

    Google Scholar 

  • Uphouse, L., Williams, J., Eckols, K. &Sierra, V. (1986) Variations in binding of [3H]5-HT to cortical membranes during the female rat estrous cycle.Brain Research 381, 376–81.

    Google Scholar 

  • Vail, W. J., Papahadjopoulos, D. &Moscarello, M. A. (1974) Interaction of a hydrophobic protein with liposomes. Evidence for particles seen in freeze-fracture replicas as being proteins.Biochimica et Biophysica Acta 345, 463–7.

    Google Scholar 

  • Walsh, R. J., Brawer, J. R. &Naftolin, F. (1982) Early postnatal development of the arcuate nucleus in normal and sexually reversed male and female rats.Journal of Anatomy 135, 733–44.

    Google Scholar 

  • Wilkinson, M., Bhanot, R., Wilkinson, D. A. &Brawer, J. R. (1983) Prolonged estrogen treatment induces changes in opiate, benzodiazepine and β-adrenergic binding sites in female rat hypothalamus.Brain Research Bulletin 11, 279–81.

    Google Scholar 

  • Wuttke, W. (1974) Preoptic unit activity and gonadotropin release.Experimental Brain Research 19, 205–16.

    Google Scholar 

  • Yu, J. &Branton, D. (1976) Reconstitution of intramembrane particles in recombinants of erythrocyte protein Band3 and lipid: effects of spectrin-actin association.Proceedings of the National Academy of Sciences (USA) 73, 3891–5.

    Google Scholar 

  • Zambrano, D. (1969) The arcuate complex of the female rat during the sexual cycle. An electron microscopic study.Zeitschrift für Zellforschung und mikroskopische Anatomie 93, 560–70.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garcia-Segura, L.M., Hernandez, P., Olmos, G. et al. Neuronal membrane remodelling during the oestrus cycle: a freeze-fracture study in the arcuate nucleus of the rat hypothalamus. J Neurocytol 17, 377–383 (1988). https://doi.org/10.1007/BF01187859

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01187859

Keywords

Navigation