Role of astrocytes in grey matter during stroke: A modelling approach

Brain Research

Volumn 1138, Issue 1, 2007, Pages 231-242

  Dronne, Marie Aimée ^a   Grenier, Emmanuel ^b   Dumont, Thierry ^c   Hommel, Marc ^d   Boissel, Jean Pierre ^a  

^a UNIVERSITÉ LYON 1   (France)

^b UNITÉ DE MATHÉMATIQUES PURES ET APPLIQUÉES   (France)

^c UNIVERSITÉ LYON 1   (France)

^d GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

Excitotoxicity; Glutamate; Ischaemia; Mathematical model; Potassium; Simulations

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID; POTASSIUM; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; EXCITOTOXICITY; EXTRACELLULAR SPACE; GRAY MATTER; HUMAN; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; NEUROPROTECTION; PRIORITY JOURNAL; STROKE;

EID: 33847235392     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.12.062     Document Type: Article

References (73)

1. Anderson C.M., and Swanson R.A. Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32 (2000) 1-14
2. Anderson M.F., Blomstrand F., Blomstrand C., Eriksson P.S., and Nilsson M. Astrocytes and stroke: networking for survival?. Neurochem. Res. 28 (2003) 293-305
3. Aschner M. Astrocytic functions and physiological reactions to injury: the potential to induce and/or exacerbate neuronal dysfunction-a forum position paper. Neurotoxicology 19 (1998) 7-17 (discussions 37-38)
4. Attwell D., Barbour B., and Szatkowski M. Nonvesicular release of neurotransmitter. Neuron 11 (1993) 401-407
5. Barber P.A., Auer R.N., Buchan A.M., and Sutherland G.R. Understanding and managing ischemic stroke. Can. J. Physiol. Pharmacol. 79 (2001) 283-296
6. Barres B.A., Chun L.L., and Corey D.P. Ion channel expression by white matter glia: I. Type 2 astrocytes and oligodendrocytes. Glia 1 (1988) 10-30
7. Benveniste H., Drejer J., Schousboe A., and Diemer N.H. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43 (1984) 1369-1374
8. Berger T., Walz W., Schnitzer J., and Kettenmann H. GABA- and glutamate-activated currents in glial cells of the mouse corpus callosum slice. J. Neurosci. Res. 31 (1992) 21-27
9. Bevan S., Chiu S.Y., Gray P.T., and Ritchie J.M. The presence of voltage-gated sodium, potassium and chloride channels in rat cultured astrocytes. Proc. R. Soc. Lond., B Biol. Sci. 225 (1985) 299-313
10. Busch E., Gyngell M.L., Eis M., Hoehn-Berlage M., and Hossmann K.A. Potassium-induced cortical spreading depressions during focal cerebral ischemia in rats: contribution to lesion growth assessed by diffusion-weighted NMR and biochemical imaging. J. Cereb. Blood Flow Metab. 16 (1996) 1090-1099
11. Chen Y., and Swanson R.A. Astrocytes and brain injury. J. Cereb Blood Flow Metab. 23 (2003) 137-149
12. Choi D.W. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci. 11 (1988) 465-469
13. Clausen T. Potassium and sodium transport and pH regulation. Can. J. Physiol. Pharmacol. 70 (1992) S219-S222 (Suppl.)
14. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., Kang J., Naus C.C., and Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 15735-15740
15. Danbolt N.C. The high affinity uptake system for excitatory amino acids in the brain. Prog. Neurobiol. 44 (1994) 377-396
16. Dirnagl U., Iadecola C., and Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22 (1999) 391-397
17. Dronne M.A., Boissel J.P., and Grenier E. A mathematical model of ion movements in grey matter during a stroke. J. Theor. Biol. 240 (2006) 599-615
18. Erecinska M., and Silver I.A. Ions and energy in mammalian brain. Prog. Neurobiol. 43 (1994) 37-71
19. Giffard R.G., Monyer H., and Choi D.W. Selective vulnerability of cultured cortical glia to injury by extracellular acidosis. Brain Res. 530 (1990) 138-141
20. Goldberg W.J., Kadingo R.M., and Barrett J.N. Effects of ischemia-like conditions on cultured neurons: protection by low Na+, low Ca2+ solutions. J. Neurosci. 6 (1986) 3144-3151
21. Gorji A. Spreading depression: a review of the clinical relevance. Brain Res. Brain Res. Rev. 38 (2001) 33-60
22. Haberg A., Qu H., Saether O., Unsgard G., Haraldseth O., and Sonnewald U. Differences in neurotransmitter synthesis and intermediary metabolism between glutamatergic and GABAergic neurons during 4 hours of middle cerebral artery occlusion in the rat: the role of astrocytes in neuronal survival. J. Cereb. Blood Flow Metab. 21 (2001) 1451-1463
23. Hansen A.J. The extracellular potassium concentration in brain cortex following ischemia in hypo- and hyperglycemic rats. Acta Physiol. Scand. 102 (1978) 324-329
24. Hansson E., Muyderman H., Leonova J., Allansson L., Sinclair J., Blomstrand F., Thorlin T., Nilsson M., and Ronnback L. Astroglia and glutamate in physiology and pathology: aspects on glutamate transport, glutamate-induced cell swelling and gap-junction communication. Neurochem. Int. 37 (2000) 317-329
25. Hertz L. Possible role of neuroglia: a potassium-mediated neuronal-neuroglial-neuronal impulse transmission system. Nature 206 (1965) 1091-1094
26. Hochachka P.W., and Mommsen T.P. Protons and anaerobiosis. Science 219 (1983) 1391-1397
27. Jabaudon D., Scanziani M., Gahwiler B.H., and Gerber U. Acute decrease in net glutamate uptake during energy deprivation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 5610-5615
28. Jensen A.M., and Chiu S.Y. Expression of glutamate receptor genes in white matter: developing and adult rat optic nerve. J. Neurosci. 13 (1993) 1664-1675
29. Kanner B.I. Sodium-coupled neurotransmitter transport: structure, function and regulation. J. Exp. Biol. 196 (1994) 237-249
30. Karwoski C.J., Lu H.K., and Newman E.A. Spatial buffering of light-evoked potassium increases by retinal Muller (glial) cells. Science 244 (1989) 578-580
31. Kato H., and Kogure K. Biochemical and molecular characteristics of the brain with developing cerebral infarction. Cell. Mol. Neurobiol. 19 (1999) 93-108
32. Kauppinen R.A., McMahon H.T., and Nicholls D.G. Ca2+-dependent and Ca2+-independent glutamate release, energy status and cytosolic free Ca2+ concentration in isolated nerve terminals following metabolic inhibition: possible relevance to hypoglycaemia and anoxia. Neuroscience 27 (1988) 175-182
33. Kristian T., and Siesjo B.K. Changes in ionic fluxes during cerebral ischaemia. Int. Rev. Neurobiol. 40 (1997) 27-45
34. Kuffler S.W., Nicholls J.G., and Orkand R.K. Physiological properties of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29 (1966) 768-787
35. Landis D.M. The early reactions of non-neuronal cells to brain injury. Annu. Rev. Neurosci. 17 (1994) 133-151
36. Lee J.M., Zipfel G.J., and Choi D.W. The changing landscape of ischaemic brain injury mechanisms. Nature 399 (1999) A7-A14
37. Lin J.H., Weigel H., Cotrina M.L., Liu S., Bueno E., Hansen A.J., Hansen T.W., Goldman S., and Nedergaard M. Gap-junction-mediated propagation and amplification of cell injury. Nat. Neurosci. 1 (1998) 494-500
38. Longuemare M.C., and Swanson R.A. Excitatory amino acid release from astrocytes during energy failure by reversal of sodium-dependent uptake. J. Neurosci. Res. 40 (1995) 379-386
39. Madl J.E., and Burgesser K. Adenosine triphosphate depletion reverses sodium-dependent, neuronal uptake of glutamate in rat hippocampal slices. J. Neurosci. 13 (1993) 4429-4444
40. Martins-Ferreira H., Nedergaard M., and Nicholson C. Perspectives on spreading depression. Brain Res. Brain Res. Rev. 32 (2000) 215-234
41. McLennan H. The autoradiographic localization of l-[3h]glutamate in rat brain tissue. Brain Res. 115 (1976) 139-144
42. Mies G., Iijima T., and Hossmann K.A. Correlation between peri-infarct DC shifts and ischaemic neuronal damage in rat. NeuroReport 4 (1993) 709-711
43. Montana V., Ni Y., Sunjara V., Hua X., and Parpura V. Vesicular glutamate transporter-dependent glutamate release from astrocytes. J. Neurosci. 24 (2004) 2633-2642
44. Namura S., Maeno H., Takami S., Jiang X.F., Kamichi S., Wada K., and Nagata I. Inhibition of glial glutamate transporter GLT-1 augments brain edema after transient focal cerebral ischemia in mice. Neurosci. Lett. 324 (2002) 117-120
45. Nedergaard M., and Hansen A.J. Characterization of cortical depolarizations evoked in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 13 (1993) 568-574
46. Nicholls D., and Attwell D. The release and uptake of excitatory amino acids. Trends Pharmacol. Sci. 11 (1990) 462-468
47. Nishizawa Y. Glutamate release and neuronal damage in ischemia. Life Sci. 69 (2001) 369-381
48. Orkand R.K., Nicholls J.G., and Kuffler S.W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29 (1966) 788-806
49. Rogers S.J., and Sherman D.G. Pathophysiology and treatment of acute ischemic stroke. Clin. Pharm. 12 (1993) 359-376
50. Rosenberg P.A., and Aizenman E. Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocyte-poor cultures of rat cerebral cortex. Neurosci. Lett. 103 (1989) 162-168
51. Rossi D.J., Oshima T., and Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403 (2000) 316-321
52. Rothstein J.D., Dykes-Hoberg M., Pardo C.A., Bristol L.A., Jin L., Kuncl R.W., Kanai Y., Hediger M.A., Wang Y., Schielke J.P., and Welty D.F. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16 (1996) 675-686
53. Sanchez-Prieto J., Sihra T.S., and Nicholls D.G. Characterization of the exocytotic release of glutamate from guinea-pig cerebral cortical synaptosomes. J. Neurochem. 49 (1987) 58-64
54. Seki Y., Feustel P.J., Keller Jr. R.W., Tranmer B.I., and Kimelberg H.K. Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker. Stroke 30 (1999) 433-440
55. Shapiro B.E. Osmotic forces and gap junctions in spreading depression: a computational model. J. Comput. Neurosci. 10 (2001) 99-120
56. Siesjo B.K. Pathophysiology and treatment of focal cerebral ischemia: Part I. Pathophysiology. J. Neurosurg. 77 (1992) 169-184
57. Simard M., and Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129 (2004) 877-896
58. Somjen G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81 (2001) 1065-1096
59. Sontheimer H. Astrocytes, as well as neurons, express a diversity of ion channels. Can. J. Physiol. Pharmacol. 70 (1992) S223-S238 (Suppl.)
60. Steinhauser C., and Gallo V. News on glutamate receptors in glial cells. Trends Neurosci. 19 (1996) 339-345
61. Storm-Mathisen J., Danbolt N.C., Rothe F., Torp R., Zhang N., Aas J.E., Kanner B.I., Langmoen I., and Ottersen O.P. Ultrastructural immunocytochemical observations on the localization, metabolism and transport of glutamate in normal and ischemic brain tissue. Prog. Brain Res. 94 (1992) 225-241
62. Swanson R.A. Astrocyte glutamate uptake during chemical hypoxia in vitro. Neurosci. Lett. 147 (1992) 143-146
63. Swanson R.A., Farrell K., and Stein B.A. Astrocyte energetics, function, and death under conditions of incomplete ischemia: a mechanism of glial death in the penumbra. Glia 21 (1997) 142-153
64. Szatkowski M., Barbour B., and Attwell D. Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348 (1990) 443-446
65. Takahashi M., Billups B., Rossi D., Sarantis M., Hamann M., and Attwell D. The role of glutamate transporters in glutamate homeostasis in the brain. J. Exp. Biol. 200 Pt 2 (1997) 401-409
66. Verkhratsky A., and Steinhauser C. Ion channels in glial cells. Brain Res. Brain Res. Rev. 32 (2000) 380-412
67. Walz W. Role of astrocytes in the clearance of excess extracellular potassium. Neurochem. Int. 36 (2000) 291-300
68. Walz W., and Hertz L. Ouabain-sensitive and ouabain-resistant net uptake of potassium into astrocytes and neurons in primary cultures. J. Neurochem. 39 (1982) 70-77
69. Walz W., and Hertz L. Functional interactions between neurons and astrocytes: II. Potassium homeostasis at the cellular level. Prog. Neurobiol. 20 (1983) 133-183
70. Walz W., and Hertz L. Intense furosemide-sensitive potassium accumulation in astrocytes in the presence of pathologically high extracellular potassium levels. J. Cereb. Blood Flow Metab. 4 (1984) 301-304
71. Walz W., and Hinks E.C. A transmembrane sodium cycle in astrocytes. Brain Res. 368 (1986) 226-232
72. Walz W., and Wuttke W.A. Independent mechanisms of potassium clearance by astrocytes in gliotic tissue. J. Neurosci. Res. 56 (1999) 595-603
73. Yi C.S., Fogelson A.L., Keener J.P., and Peskin C.S. A mathematical study of volume shifts and ionic concentration changes during ischemia and hypoxia. J. Theor. Biol. 220 (2003) 83-106