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Cited by 63Ion Transport and Channel RegulationNeuroscience and Neuropharmacology ResearchAmino Acid Enzymes and Metabolism

Two Distinct Modes of Hypoosmotic Medium-Induced Release of Excitatory Amino Acids and Taurine in the Rat Brain In Vivo

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Haskew-Layton, Renée E., Rudkouskaya, Alena, Jin, Yiqiang, Feustel, Paul J., Kimelberg, Harold K., Mongin, Alexander A.·2008·PLoS ONE
DOI 10.1371/journal.pone.0003543PMC PMC2568819
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Abstract

A variety of physiological and pathological factors induce cellular swelling in the brain. Changes in cell volume activate several types of ion channels, which mediate the release of inorganic and organic osmolytes and allow for compensatory cell volume decrease. Volume-regulated anion channels (VRAC) are thought to be responsible for the release of some of organic osmolytes, including the excitatory neurotransmitters glutamate and aspartate. In the present study, we compared the in vivo properties of the swelling-activated release of glutamate, aspartate, and another major brain osmolyte taurine. Cell swelling was induced by perfusion of hypoosmotic (low [NaCl]) medium via a microdialysis probe placed in the rat cortex. The hypoosmotic medium produced several-fold increases in the extracellular levels of glutamate, aspartate and taurine. However, the release of the excitatory amino acids differed from the release of taurine in several respects including: (i) kinetic properties, (ii) sensitivity to isoosmotic changes in [NaCl], and (iii) sensitivity to hydrogen peroxide, which is known to modulate VRAC. Consistent with the involvement of VRAC, hypoosmotic medium-induced release of the excitatory amino acids was inhibited by the anion channel blocker DNDS, but not by the glutamate transporter inhibitor TBOA or Cd2+, which inhibits exocytosis. In order to elucidate the mechanisms contributing to taurine release, we studied its release properties in cultured astrocytes and cortical synaptosomes. Similarities between the results obtained in vivo and in synaptosomes suggest that the swelling-activated release of taurine in vivo may be of neuronal origin. Taken together, our findings indicate that different transport mechanisms and/or distinct cellular sources mediate hypoosmotic medium-induced release of the excitatory amino acids and taurine in vivo.

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Authors
Haskew-Layton, R. E., Rudkouskaya, A., Jin, Y., Feustel, P. J., Kimelberg, H. K., & Mongin, A. A.
Affiliations
  • Cornell University (US)
  • Albany Medical College (US)
Corresponding author
Mongin, Alexander A.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2008-10-28
Volume
3
Issue
10
Pages
e3543
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0003543
PMC
PMC2568819
OpenAlex
W2053847470
Cited by
63
References
1
Citations by year
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FWCI
1.92
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Institutes of Health
  • National Institute of Neurological Disorders and Stroke (F31NS046961, R01NS035205, R21NS052516)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Keywords
hypoosmotic stress, volume-regulated anion channel, excitatory amino acids, glutamate release, aspartate release, taurine release, osmolytes, DNDS, hydrogen peroxide, astrocytes, synaptosomes, sodium chloride, glutamate transporters
MeSH terms
Animals, Astrocytes, Brain, Brain Edema, Cells, Cultured, Male, Neurons, Osmolar Concentration, Osmosis, Sodium Chloride, Synaptosomes, Taurine, Water-Electrolyte Balance, Rats, Sprague-Dawley, Excitatory Amino Acids, Rats

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