Skip to main content
SpringerLink
Log in

Morphology of astroglia in colony cultures following transient exposure to potassium ion, hypoösmolarity and vasopressin

  • Published:
Journal of Neurocytology

Summary

Brain swelling is the major cause of delayed neuronal damage following injury to the central nervous system. Swelling of mouse astroglial cells was studied in colony cultures by light and electron microscopy. Swelling of suspended astroglial cells was studied by flow cytometry. Swelling caused by hypoösmolar solution was more pronounced than that caused by 15 or 60mm K+. Under both conditions swelling in both immature and mature astroglia was followed by a regulatory volume decrease. Arginine vasopressin caused mild astroglial swelling and atrial natriuretic peptide did not significantly affect cell volume. All changes in extracellular environment were associated with changes in the morphology of microvilli and varying amounts of membrane ruffling. Immature cells exhibited a delayed response to the application of atrial natriuretic peptide and less membrane ruffling following exposure to 60mm K+ than mature astroglia. These nonspecific morphological changes are likely associated with changes in membrane ion pump activity.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albrecht-Buehler, G. (1990) In defense of ‘nonmolecular’ cell biology.International Review of Cytology 120, 191–241.

    PubMed  Google Scholar 

  • Albrecht-Buehler, G. &Bushnell, A. (1982) Reversible compression of cytoplasm.Experimental Cell Research 140, 173–89.

    PubMed  Google Scholar 

  • Barron, K. D., Dentinger, M. P., Kimelberg, H. K., Nelson, L. R., Bourke, R. S., Keegan, S., Mankes, R. &Cragoe, E. J. (1988) Ultrastructural features of a brain injury model in cat. I. Vascular and neuroglial changes and the prevention of astroglial swelling by a fluorenyl(aryloxy) alkanoic acid derivative (l-644,711).Acta Neuropathologica 75, 295–307.

    PubMed  Google Scholar 

  • Beaumont, K. &Tan, P. K. (1990) Effects of atrial and brain natriuretic peptides upon cyclic GMP levels, potassium transport, and receptor binding in rat astrocytes.Journal of Neuroscience Research 25, 256–62.

    PubMed  Google Scholar 

  • Bender, A. S. &Hertz, L. (1987) Inhibition of [3H] diazepam binding in primary cultures of astrocytes by atrial natriuretic peptide and by a cyclic GMP analog.Brain Research 436, 189–92.

    PubMed  Google Scholar 

  • Chaussy, L., Baethmann, A. &Lubitz, W. (1981) Electrical sizing of nerve and glia cells in the study of cell volume regulation. InCerebral Microcirculation and Metabolism (edited byCervos-Navarro, J. &Fritschka, E.) pp. 29–40. New York: Raven Press.

    Google Scholar 

  • Chen, W. T. (1981) Mechanism of retraction of the trailing edge during fibroblast movement.Journal of Cell Biology 90, 187–200.

    PubMed  Google Scholar 

  • Cholewinski, A. J. &Wilkin, G. P. (1988) Peptide receptors on astrocytes: evidence for regional heterogeneity.Biochemical Society Transactions 16, 429–32.

    PubMed  Google Scholar 

  • Clegg, J. S. (1984) Properties and metabolism of the aqueous cytoplasm and its boundaries.American Journal of Physiology 246, R133-R151.

    PubMed  Google Scholar 

  • Clegg, J. S. (1988) Contrasting views on the organization of cytoplasm.Scanning Microscopy 2, 915–24.

    PubMed  Google Scholar 

  • Cornell-Bell, A. H. &Finkbeiner, S. M. (1991) Ca2+ waves in astrocytes.Cell Calcium 12, 185–204.

    PubMed  Google Scholar 

  • Cornell-Bell, A. H., Thomas, P. G. &Smith, S. J. (1990) The excitatory neurotransmitter glutamate causes filopodia formation in cultured hippocampal astrocytes.Glia 3, 322–34.

    PubMed  Google Scholar 

  • De Vente, J., Manshanden, C. G., Sikking, R. A., Ramaekers, F. C. S. &Steinbusch, H. W. M. (1990) A functional parameter to study heterogeneity of glial cells in rat brain slices: cyclic guanosine monophosphate production in atrial natriuretic factor (ANF)-responsive cells.Glia 3, 43–54.

    PubMed  Google Scholar 

  • Doczi, T., Joo, F., Szerdahelyi, P. &Bodosi, M. (1988) Regulation of brain water and electrolyte contents: the opposite actions of central vasopressin and atrial natriuretic factor (ANF).Acta Neurochirurgica Supplement 43, 186–8.

    Google Scholar 

  • El-Achkar, P., Langley, O. K. &Mersel, M. (1989) Effect of cell surface trypsinization on ethanolamine base exchange enzymatic activity of astrocyte primary cultures and derived spontaneously transformed cell lines.Biochemical and Biophysical Research Communications 159, 1055–64.

    PubMed  Google Scholar 

  • Fedoroff, S., Neal, J., Opas, M. &Kalnins, V. I. (1984) Astrocyte cell lineage. III. The morphology of differentiating mouse astrocytes in colony culture.Journal of Neurocytology 13, 1–20.

    PubMed  Google Scholar 

  • Fedoroff, S., Ahmed, I. &Wang, E. (1990) The relationship of the expression of statin, the nuclear protein of nonproliferating cells, to the differentiation and cell cycle of astroglia in cultures andin situ.Journal of Neuroscience Research 26, 1–15.

    PubMed  Google Scholar 

  • Friede, R. L. (1989)Developmental Neuropathology, 2nd ed. Berlin: Springer-Verlag.

    Google Scholar 

  • Friedl, A., Harmening, C., Schmalz, F., Schuricht, B., Schiller, M. &Hamprecht, B. (1989) Elevation by atrial natriuretic factors of cyclic GMP levels in astrogliarich cultures from murine brain.Journal of Neurochemistry 52, 589–97.

    PubMed  Google Scholar 

  • Ghadially, F. N. (1988)Ultrastructural Pathology of the Cell and Matrix, 3rd ed. London: Butterworths.

    Google Scholar 

  • Gilles, F. H. (1983) Neuronal damage: inconstancy during gestation. InThe Developing Human Brain. Growth and Epidemiologie Neuropathology (edited byGilles, F. H., Leviton, A. &Dooling, E. C.) pp. 227–243. Boston: John Wright PSG Inc.

    Google Scholar 

  • Henn, F. A., Deering, J. &Anderson, D. (1980) Receptor studies on isolated astroglial cell fractions prepared with and without trypsin.Neurochemical Research 5, 459–64.

    PubMed  Google Scholar 

  • Hirano, A. (1969) The fine structure of brain in edema. InThe Structure and Function of Nervous Tissue, Vol. 2 (edited byBourne, G. H.) pp. 69–135. New York: Academic Press.

    Google Scholar 

  • Ibaragi, M. &Niwa, M. (1989) Atrial natriuretic peptide and angiotensin II binding sites in cerebral capillaries of spontaneously hypertensive rats.Cellular and Molecular Neurobiology 9, 221–32.

    PubMed  Google Scholar 

  • Kempski, O., Chaussy, L., Gross, U., Zimmer, M. &Baethmann, A. (1983) Volume regulation and metabolism of suspended C6 glioma cells: anin vitro model to study cytotoxic brain edema.Brain Research 279, 217–28.

    PubMed  Google Scholar 

  • Kimelberg, H. K. &Frangakis, M. V. (1985) Furosemide- and bumetanide-sensitive ion transport and volume control in primary astrocyte cultures from rat brain.Brain Research 361, 125–34.

    PubMed  Google Scholar 

  • Kimelberg, H. K. &O'Connor, E. (1988) Swelling of astrocytes causes membrane potential depolarization.Glia 1, 219–24.

    PubMed  Google Scholar 

  • Kimelberg, H. K. &Ransom, B. R. (1986) Physiological and pathological aspects of astrocyte swelling. InAstrocytes. Cell Biology and Pathology of Astrocytes, Vol. 3 (edited byFedoroff, S. &Vernadakis, A.) pp. 129–66. Orlando, FL: Academic Press.

    Google Scholar 

  • Koyama, Y., Sugimoto, T., Shigenaga, Y., Baba, A. &Iwata, H. (1991) A morphological study on glutamate-induced swelling of cultured astrocytes: involvement of calcium and chloride ion mechanisms.Neuroscience Letters 124, 235–8.

    PubMed  Google Scholar 

  • Lodin, Z., Booher, J., Kasten, F. H. &Hartman, J. (1971) Effects of increased extracellular potassium on intracellular transport in cultured nerve and glial cells.Neurobiology 1, 86–95.

    Google Scholar 

  • Mcgann, L. E., Walterson, M. L. &Hogg, L. M. (1988) Light scattering and cell volumes in osmotically stressed and frozen-thawed cells.Cytometry 9, 33–8.

    PubMed  Google Scholar 

  • Okuma, A. &Yamada, H. (1978) Brain edema in immature animals. An experimental study in rats.Child's Brain 4, 321–38.

    PubMed  Google Scholar 

  • Olson, J. E., Sankar, R., Holtzman, D., James, A. &Fleischhacker, D. (1986) Energy dependent volume regulation in primary cultured cerebral astrocytes.Journal of Cellular Physiology 128, 209–15.

    PubMed  Google Scholar 

  • Parsons, D. F., Cole, R. W. &Kimelberg, H. K. (1989) Shape, size, and distribution of cell structures by 3-D graphics reconstruction and stereology. I. The regulatory volume decrease of astroglial cells.Cell Biophysics 14, 27–12.

    PubMed  Google Scholar 

  • Raichle, M. E. (1981) Hypothesis: a central neuroendocrine system regulates brain ion homeostatis and volume. InNeurosecretion and Brain Peptides (edited byMartin, J. B., Reichlin, S., &Bick, K. L.) pp. 329–36. New York: Raven Press.

    Google Scholar 

  • Ravid, R., Swaab, D. F., Van Der Woude, T. P. &Boer, G. J. (1986) Immunocytochemically-stained vasopressin binding sites in rat brain. Ventricular application of vasopressin/accurel in the Brattleboro rat.Journal of the Neurological Sciences 76, 317–33.

    PubMed  Google Scholar 

  • Rosenberg, G. A., Estrada, E. &Kyner, W. T. (1988) The effect of arginine vasopressin and V1 receptor antagonist on brain water in cat.Neuroscience Letters 95, 241–5.

    PubMed  Google Scholar 

  • Teoh, R., Kum, W., Cockram, C. S., Young, J. D. &Nicholls, M. G. (1989) Mouse astrocytes possess specific ANP receptors which are linked to cGMP production.Clinical and Experimental Pharmacology and Physiology 16, 323–7.

    PubMed  Google Scholar 

  • Tholey, G., Ledig, M., Bloch, S. &Mandel, P. (1985) Glutamine synthetase and energy metabolism enzymes in cultured chick glial cells: modulation by dibutyryl cyclic AMP, hydrocortisone, and trypsinization.Neurochemical Research 10, 191–200.

    PubMed  Google Scholar 

  • Van Rossum, G. D. V., Russo, M. A. &Schisselbauer, J. C. (1987) Role of cytoplasmic vesicles in volume maintenance.Current Topics in Membranes and Transport 30, 45–74.

    Google Scholar 

  • Walz, W. (1987) Swelling and potassium uptake in cultured astrocytes.Canadian Journal of Physiology and Pharmacology 65, 1051–7.

    PubMed  Google Scholar 

  • Wasterlain, C. G. &Torack, R. M. (1968) Cerebral edema in water intoxication. II. An ultrastructural study.Archives of Neurology 19, 79–87.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, The University of Saskatchewan, Saskatoon, Canada

    M. R. Del Bigio & S. Fedoroff

  2. Department of Microbiology, The University of Saskatchewan, Saskatoon, Canada

    L. F. Qualtiere

Authors
  1. M. R. Del Bigio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Fedoroff
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. F. Qualtiere
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Del Bigio, M.R., Fedoroff, S. & Qualtiere, L.F. Morphology of astroglia in colony cultures following transient exposure to potassium ion, hypoösmolarity and vasopressin. J Neurocytol 21, 7–18 (1992). https://doi.org/10.1007/BF01206894

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01206894

Keywords

Search

Navigation