Neuronal and glial handling of glutamate and glutamine during hypoosmotic stress: A biochemical and quantitative immunocytochemical analysis using the rat cerebellum as a model

Neuroscience

Volumn 72, Issue 3, 1996, Pages 743-755

  Nagelhus, E A ^a   Lehmann, A ^b   Ottersen, O P ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b ASTRAZENECA R AND D   (Sweden)

Author keywords

cerebellum; glutamate; glutamine; hypoosmotic stress

Indexed keywords

GLUTAMIC ACID; GLUTAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; ELECTRON MICROSCOPY; GLIA CELL; IMMUNOCYTOCHEMISTRY; MALE; NERVE CELL; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; RAT;

EID: 0029928379     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00003-6     Document Type: Article

References (67)

1. Amiry-Moghaddam M., Nagelhus E. and Ottersen O. P. (1994) Light-and electronmicroscopic distribution of taurine, an organic osmolyte, in rat renal tubule cells. Kidney Int. 45, 10-22.
2. Arieff A. I., Llach F. and Massry S. G. (1976) Neurological manifestations and morbidity of hyponatremia: correlation with brain water and electrolytes. Medicine 55, 121-129.
3. Ballanyi K. and Grafe P. (1988) Cell volume regulation in the nervous system. Renal Physiol. Biochem. 3-5, 142-157.
4. Baxter C. F., Wasterlain C. G., Hallden K. L. and Pruess S. F. (1986) Effect of altered blood plasma osmolalities on regional brain amino acid concentrations and focal seizure susceptibility in the rat. J. Neurochem. 47, 617-624.
5. Bender A. S., Mantelle L. L. and Norenberg M. D. (1994) Stimulation of calcium uptake in cultured astrocytes by hypoosmotic stress-effect of cyclic AMP. Brain Res. 645, 27-35.
6. 2+ on glutamine synthesis and distribution in rat brain cortex slices: a possible linkage of glutamine synthetase with cerebral transport processes and energetics in the astrocytes. J. Neurochem. 48, 1157-1164.
7. Benveniste H., Drejer J., Schousboe A. and Diemer N. H. (1984) Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43, 1369-1374.
8. Blackstad T. W., Karagülle T. and Ottersen O. P. (1990) Morforel, a computer program for two-dimensional analysis of micrographs of biological specimens, with emphasis on immunogold preparations. Comput. Biol. Med. 20, 15-34.
9. Brookes N. (1992) Effect of pH on glutamine content derived from exogenous glutamate in astrocytes. J. Neurochem. 59, 1017-1023.
10. Cooper A. J. L. and Plum F. (1987) Biochemistry and physiology of brain ammonia. Physiol. Rev. 67, 440-519.
11. Davanger S., Storm-Mathisen J. and Ottersen O. P. (1994) Colocalization of glutamate and glycine in bipolar cell terminals of the human retina. Exp. Brain Res. 98, 342-354.
12. Dila C. J. and Pappius H. M. (1972) Cerebral water and electrolytes. An experimental model of inappropriate secretion of antidiuretic hormone. Archs Neurol. 26, 85-90.
13. Erecińska M. and Silver I. A. (1990) Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 35, 245-296.
14. Erecińska M., Zaleska M. M., Nelson D., Nissim I. and Yudkoff M. (1990) Neuronal glutamine utilization: glutamine/glutamate homeostasis in synaptosomes. J. Neurochem. 54, 2057-2069.
15. Ericson A. C., Blomqvist A., Craig A. D. (Bud), Ottersen O. P. and Broman J. (1995) Evidence for glutamate as neurotransmitter in trigemino-and spinothalamic tract terminals in the nucleus submedius of cats. Eur. J. Neurosci. 7, 305-317.
16. Fishman R. A. (1975) Brain edema. New Engl. J. Med. 293, 706-711.
17. Fonnum F. (1984) Glutamate: a transmitter in mammalian brain. J. Neurochem. 42, 1-11.
18. Holliday M. A., Kalayci M. N. and Harrah J. (1968) Factors that limit brain volume changes in response to acute and sustained hyper-and hyponatremia. J. clin. Invest. 47, 1916-1928.
19. Huxtable R. J. (1992) The physiological actions of taurine. Physiol. Rev. 72, 101-163.
20. Kimelberg H. K., Goderie S. K., Higman S., Pang S. and Waniewski R. A. (1990) Swelling-induced release of glutamate, aspartate and taurine from astrocyte cultures. J. Neurosci. 10, 1583-1591.
21. Laake J. H., Gundersen V., Nordbø G., Ottersen O. P. and Storm-Mathisen J. (1986) An antiserum against glutamine. In Excitatory Amino Acids (eds Roberts P. J., Storm-Mathisen J. and Bradford H. F.), pp. 448-450. Macmillan, London.
22. Law R. O. (1994) Regulation of mammalian brain cell volume. J. exp. Zool. 268, 90-96.
23. Lehmann A. (1989) Effects of microdialysis-perfusion with anisoosmotic media on extracellular amino acids in the rat hippocampus and skeletal muscle. J. Neurochem. 53, 525-535.
24. Lehmann A., Carlström C., Nagelhus E. A. and Ottersen O. P. (1991) Elevation of taurine in hippocampal extracellular fluid and cerebrospinal fluid of acutely hypoosmotic rats: contribution by influx from blood? J. Neurochem. 56, 690-697.
25. Lien Y.-H. H., Shapiro J. I. and Chan L. (1991) Study of brain electrolytes and organic osmolytes during correction of chronic hyponatremia. J. clin. Invest. 88, 303-309.
26. Liu C.-J., Grandes P., Matute C., Cuénod M. and Streit P. (1989) Glutamate like immunoreactivity revealed in rat olfactory bulb, hippocampus and cerebellum by monoclonal antibody and sensitive staining method. Histochemistry, 90, 427-445.
27. Martinez Hernandez A., Bell K. P. and Norenberg M. D. (1977) Glutamine synthetase: glial localization in the brain. Science 195, 1356-1358.
28. Melton J. E. and Nattie E. E. (1983) Brain and CSF water and ions during dilutional and isosmotic hyponatremia in the rat. Am. J. Physiol. 244, 724-732.
29. Melton J. E., Patlak C. S., Pettigrew K. D. and Cserr H. F. (1987) Volume regulatory loss of Na, Cl, and K from rat brain during acute hyponatremia. Am. J. Physiol. 252, 661-669.
30. Miller S., Cotman C. W. and Bridges R. J. (1992) 1-Aminocyclopentane-trans-1,3-dicarboxylic acid induces glutamine synthetase activity in cultured astrocytes. J. Neurochem. 58, 1967-1970.
31. Nagelhus E. A., Amiry-Moghaddam M., Lehmann A. and Ottersen O. P. (1994) Taurine as an organic osmolyte in the intact brain: immunocytochemical and biochemical studies. In Taurine in Health and Disease (eds Huxtable R. J. and Michalk D.), Vol. 359, pp. 325-334. Plenum Press, New York.
32. Nagelhus E. A., Lehmann A. and Ottersen O. P. (1993) Neuronal-glial exhange of taurine during hypo osmotic stress: a combined immunocytochemical and biochemical analysis in rat cerebellar cortex. Neuroscience 54, 615-631.
33. Norenberg M. D. (1979) Distribution of glutamine synthetase in the rat central nervous system. J. Histochem. Cytochem. 27, 756-762.
34. Norenberg M. D. and Martinez Hernandez A. (1979) Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res. 161, 303-310.
35. O'Connor E. R. and Kimelberg H. K. (1993) Role of calcium in astrocyte volume regulation and in the release of ions and amino acids. J. Neurosci. 13, 2638-2650.
36. Ottersen O. P. (1987) Postembedding light-and electron microscopic immunocytochemistry of amino acids: description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp. Brain Res. 69, 167-174.
37. Ottersen O. P. (1988) Quantitative assessment of taurine-like immunoreactivity in different cell types and processes in rat cerebellum: an electronmicroscopic study based on a postembedding immunogold labelling procedure. Anat. Embryol. 178, 407-421.
38. Ottersen O. P. (1989) Postembedding immunogold labelling of fixed glutamate: an electron microscopic analysis of the relationship between gold particle density and antigen concentration. J. Chem. Neuroanat. 2, 57-66.
39. Ottersen O. P., Zhang N. and Walberg F. (1992) Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 46, 519-534.
40. Pasantes Morales H., Alavez S., Sánchez-Olea R. and Morán J. (1993) Contribution of organic and inorganic osmolytes to volume regulation in rat brain cells in culture. Neurochem. Res. 18, 445-452.
41. Pasantes Morales H., Chacón E., Sánchez Olea R. and Morán J. (1994) Volume regulation in cultured neurons: pivotal role of taurine. In Taurine in Health and Disease (eds Huxtable R. J. and Michalk D.), Vol. 359, pp. 317-323. Plenum Press, New York.
42. Pollock A. S. and Arieff A. I. (1980) Abnormalities of cell volume regulation and their functional consequenses. Am. J. Physiol. 239, 195-205.
43. Riggs J. E. (1989) Neurologic manifestations of fluid and electrolyte disturbances. Neurol. Clin. 7, 509-523.
44. Rymer M. M. and Fishman R. A. (1973) Protective adaption of brain to water intoxication. Archs Neurol. 28, 49-54.
45. Schousboe A. and Pasantes-Morales H. (1992) Role of taurine in neural cell volume regulation. Can. J. Physiol. Pharmac. 70, 356-361.
46. Solís J. M., Herranz A. S, Herreras O., Lerma J. and Martín del Rio R. (1988) Does taurine act as an osmoregulatory substance in the rat brain? Neurosci. Lett. 91, 53-58.
47. Somogyi P., Halasy K., Somogyi J., Storm-Mathisen J. and Ottersen O. P. (1986) Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience 19, 1045-1050.
48. Somogyi P., Hodgson A. J., Smith A. D., Nunzi M. G., Gorio A. and Wu J.-U. (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin-or cholecystokinin-immunoreactive material. J. Neurosci. 4, 2590-2603.
49. Sterns R. H., Baer J., Ebersol S., Thomas D., Lohr J. W. and Kamm D. E. (1993) Organic osmolytes in acute hyponatremia. Am. J. Physiol. 264, 833-836.
50. Strange K. (1994) Regulation of solute and water balance and cell volume in the central nervous system. J. Am. Soc. Neprol. 3, 12-27.
51. Thurston J. H., Hauhart R. E., Jones E. M. and Ater J. L. (1975) Effects of salts and water on carbohydrate and energy metabolism and levels of selected amino acids in the brains of young mice. J. Neurochem. 24, 953-957.
52. Thurston J. H., Hauhart R. E. and Nelson, J. S. (1987) Adaptive decreases in amino acids (taurine in particular), creatine, and electrolytes prevent cerebral edema in chronically hyponatremic mice: rapid correction (experimental model of central pontine myelinolysis) causes dehydration and shrinkage of brain. Metab. Brain Dis. 2, 223-241.
53. Thurston J. H., Sherman W. R., Hauhart R. E. and Kloepper R. F. (1989) Myo-inositol: a newly identified nonnitrogenous osmoregulatory molecule in mammalian brain. Pedriatric Res. 26, 482-485.
54. Torp R., Andiné P., Hagberg H., Karagülle T., Blackstad T. W. and Ottersen O. P. (1991) Cellular and subcellular redistribution of glutamate-, glutamine-, and taurine-like immunoreactivities during forebrain ischemia: a semiquantitative electron microscopic study in rat hippocampus. Neuroscience 41, 433-447.
55. Torp R., Arvin B., Le Peillet E., Chapman A. G., Ottersen O. P. and Meldrum B. S. (1993) Effect of ischemia a reperfusion on the extra- and intracellular distribution of glutamate, glutamine, aspartate and GABA in the rat hippocampus, with note on the effect of the sodium channel blocker BW 1003C87. Exp. Brain Res. 96, 365-376.
56. Trachtman H. (1992) Cell volume regulation: a review of cerebral adaptive mechanisms and implications for clinical treatment of osmolal disturbances - II. Pediat. Nephrol. 6, 104-112.
57. van Gelder N. M. (1990) Neuronal discharge hypersynchrony and the intracranial water balance in relation to glutamic acid and taurine redistribution: migraine and epilepsy. In Taurine: Functional Neurochemistry, Physiology, and Cardiology (eds Pasantes Morales H., Martin D. L., Shain W. and Martín del Rio R.), pp. 1-20. Wiley-Liss, New York.
58. van Gelder N. M. and Barbeau A. (1985) The osmoregulatory function of taurine and glutamic acid. In Taurine: Biological Actions and Clinical Perspectives (eds Oja S. S., Ahtee L., Kontro P. and Paasonen M. K.), pp. 149-163. Liss, New York.
59. Verbalis J. G. and Drutarosky M. D. (1988) Adaption to chronic hypoosmolality in rats. Kidney Int. 34, 351-360.
60. Verbalis J. G. and Gullans S. R. (1991) Hyponatremia causes large sustained reductions in brain content of multiple organic osmolytes in rats. Brain Res. 567, 274-282.
61. Wade J. V., Olson J. P., Samson F. E., Nelson S. R. and Pazdernik T. L. (1988) A possible role for taurine in osmoregulation within the brain. J. Neurochem. 51, 740-745.
62. Wang B.-L. and Larsson L.-I. (1985) Simultaneous demonstration of multiple antigens by indirect immunofluorescence or immunogold staining. Novel light and electron microscopical double and triple staining method employing primary antibodies from the same species. Histochemistry, 83, 47-46.
63. Wasterlain C. G. and Posner J. B. (1968) Cerebral edema in water intoxication - I. Clinical and chemical observations Archs Neurol. 19, 71-78.
64. Wedler F. C. and Ley B. W. (1994) Kinetic, ESR, and trapping evidence for in vivo binding of Mn(II) to glutamine synthetase in brain cells. Neurochem. Res. 19, 139-144.
65. Wedler F. C., Vichnin M. C., Ley B. W., Tholey G., Ledig M. and Copin J.-C. (1994) Effects of Ca(II) ions on Mn(II) dynamics in chick glia and rat astrocytes: potential regulation of glutamine synthetase. Neurochem. Res. 19, 145-151.
66. Yannet H. (1940) Changes in the brain resulting from depletion of extracellular electrolytes. Am. J. Physiol. 128, 683-689.
67. Zhang N., Laake J., Nagelhus E., Storm-Mathisen J. and Ottersen O. P. (1991) Distribution of glutamine-like immunoreactivity in the cerebellum of rat and baboon (Papio anubis) with reference to the issue of metabolic compartmentation. Anat. Embryol. 184, 213-223.