Inhibition of astroglial glutamate transport by polyunsaturated fatty acids: Evidence for a signalling role of docosahexaenoic acid

Neurochemistry International

Volumn 54, Issue 8, 2009, Pages 535-543

  Grintal, Barbara ^a,b   Champeil Potokar, Gaëlle ^a   Lavialle, Monique ^a   Vancassel, Sylvie ^a   Breton, Sylvie ^b   Denis, Isabelle ^a  

^a INRA   (France)

^b Saint Hubert   (France)

Author keywords

Arachidonic acid; Astrocytes; Brain; Docosahexaenoic acid; Glutamate uptake; Polyunsaturated fatty acids; Rat

Indexed keywords

ALPHA TOCOPHEROL; ARACHIDONIC ACID; ASPARTIC ACID; CELL SURFACE PROTEIN; DOCOSAHEXAENOIC ACID; EXCITATORY AMINO ACID TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; POLYUNSATURATED FATTY ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; BRAIN MEMBRANE; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; EXCITOTOXICITY; IMMUNOBLOTTING; LIPID PEROXIDATION; MACROGLIA; NERVE CELL CULTURE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; WESTERN BLOTTING;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; ARACHIDONIC ACID; ASPARTIC ACID; ASTROCYTES; BIOTINYLATION; CELL MEMBRANE; CELLS, CULTURED; DOCOSAHEXAENOIC ACIDS; EXCITATORY AMINO ACID TRANSPORTER 1; FATTY ACIDS, UNSATURATED; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; LIPID METABOLISM; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; VITAMIN E;

RATTUS;

EID: 64049119297     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2009.02.018     Document Type: Article

References (41)

1. Alessandri J.M., Guesnet P., Vancassel S., Astorg P., Denis I., Langelier B., Aid S., Poumes-Ballihaut C., Champeil-Potokar G., and Lavialle M. Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reprod. Nutr. Dev. 44 (2004) 509-538
2. Barbour B., Szatkowski M., Ingledew N., and Attwell D. Arachidonic acid induces a prolonged inhibition of glutamate uptake into glial cells. Nature 342 (1989) 918-920
3. Bazan N.G. Synaptic lipid signaling: significance of polyunsaturated fatty acids and platelet-activating factor. J. Lipid Res. 44 (2003) 2221-2233
4. Berry C.B., Hayes D., Murphy A., Wiessner M., Rauen T., and McBean G.J. Differential modulation of the glutamate transporters GLT1, GLAST and EAAC1 by docosahexaenoic acid. Brain Res. 1037 (2005) 123-133
5. Berry C.B., and McBean G.J. An investigation into the role of calcium in the modulation of rat synaptosomal d-[H-3]aspartate transport by docosahexaenoic acid. Brain Res. 973 (2003) 107-114
6. Champeil-Potokar G., Chaumontet C., Guesnet P., Lavialle M., and Denis I. Docosahexaenoic acid (22:6n-3) enrichment of membrane phospholipids increases gap junction coupling capacity in cultured astrocytes. Eur. J. Neurosci. 24 (2006) 3084-3090
7. Champeil-Potokar G., Denis I., Goustard-Langelier B., Alessandri J.-M., Guesnet P., and Lavialle M. Astrocytes in culture require docosahexaenoic acid to restore the n-3/n-6 polyunsaturated fatty acid balance in their membrane phospholipids. J. Neurosci. Res. 75 (2004) 96-106
8. Contreras M.A., Greiner R.S., Chang M.C., Myers C.S., Salem Jr. N., and Rapoport S.I. Nutritional deprivation of alpha-linolenic acid decreases but does not abolish turnover and availability of unacylated docosahexaenoic acid and docosahexaenoyl-CoA in rat brain. J. Neurochem. 75 (2000) 2392-2400
9. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 65 (2001) 1-105
10. DeMar J.C., Ma K.Z., Bell J.M., and Rapoport S.I. Half-lives of docosahexaenoic acid in rat brain phospholipids are prolonged by 15 weeks of nutritional deprivation of n-3 polyunsaturated fatty acids. J. Neurochem. 91 (2004) 1125-1137
11. Fedorova I., and Salem Jr. N. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot. Essent. Fatty Acids 75 (2006) 271-289
12. Green J.T., Orr S.K., and Bazinet R.P. The emerging role of group VI calcium-independent phospholipase A(2) in releasing docosahexaenoic acid from brain phospholipids. J. Lipid Res. 49 (2008) 939-944
13. Hogyes E., Nyakas C., Kiliaan A., Farkas T., Penke B., and Luiten P.G.M. Neuroprotective effect of developmental docosahexaenoic acid supplement against excitotoxic brain damage in infant rats. Neuroscience 119 (2003) 999-1012
14. Kondo K., Hashimoto H., Kitanaka J., Sawada M., Suzumura A., Marunouchi T., and Baba A. Expression of glutamate transporters in cultured glial cells. Neurosci. Lett. 188 (1995) 140-142
15. Lauritzen I., Blondeau N., Heurteaux C., Widmann C., Romey G., and Lazdunski M. Polyunsaturated fatty acids are potent neuroprotectors. EMBO J. 19 (2000) 1784-1793
16. Lundy D.F., and McBean G.J. Pre-incubation of synaptosomes with arachidonic acid potentiates inhibition of [3H]d-aspartate transport. Eur. J. Pharmacol. 291 (1995) 273-279
17. Lundy D.F., and McBean G.J. Inhibition of the high-affinity uptake of d-[3H]aspartate in rate by l-alpha-aminoadipate and arachidonic acid. J. Neurol. Sci. 139 Suppl (1996) 1-9
18. Magistretti P.J. Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209 (2006) 2304-2311
19. Manzoni C., and Mennini T. Arachidonic acid inhibits 3H-glutamate uptake with different potencies in rodent central nervous system regions expressing different transporter subtypes. Pharmacol. Res. 35 (1997) 149-151
20. Martin D.S.D., Spencer P., Horrobin D.F., and Lynch M.A. Long-term potentiation in aged rats is restored when the age-related decrease in polyunsaturated fatty acid concentration is reversed. Prostaglandins Leukot. Essent. Fatty Acids 67 (2002) 121-130
21. McGahon B.M., Martin D.S., Horrobin D.F., and Lynch M.A. Age-related changes in synaptic function: analysis of the effect of dietary supplementation with omega-3 fatty acids. Neuroscience 94 (1999) 305-314
22. Michael-Titus A.T. Omega-3 fatty acids and neurological injury. Prostaglandins Leukot. Essent. Fatty Acids 77 (2007) 295-300
23. Mirnikjoo B., Brown S.E., Kim H.F., Marangell L.B., Sweatt J.D., and Weeber E.J. Protein kinase inhibition by omega-3 fatty acids. J. Biol. Chem. 276 (2001) 10888-10896
24. Rao J.S., Ertley R.N., Demar J.C., Rapoport S.I., Bazinet R.P., and Lee H.J. Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex. Mol. Psychiatry 12 (2007) 151-157
25. Robinson M.B. Acute regulation of sodium-dependent glutamate transporters: a focus on constitutive and regulated trafficking. Handb. Exp. Pharmacol. (2006) 251-275
26. 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
27. Sattler R., and Rothstein J.D. Regulation and dysregulation of glutamate transporters. Handb. Exp. Pharmacol. (2006) 277-303
28. +-dependent glutamate transporters by cyclic AMP analogs and neurons. Mol. Pharmacol. 53 (1998) 355-369
29. 2+. Br. J. Pharmacol. 139 (2003) 1014-1022
30. Strokin M., Sergeeva M., and Reiser G. Prostaglandin synthesis in rat brain astrocytes is under the control of the n-3 docosahexaenoic acid, released by group VIB calcium-independent phospholipase A2. J. Neurochem. 102 (2007) 1771-1782
31. Susarla B.T.S., Seal R.P., Zelenaia O., Watson D.J., Wolfe J.H., Amara S.G., and Robinson M.B. Differential regulation of GLAST immunoreactivity and activity by protein kinase C: evidence for modification of amino and carboxyl termini. J. Neurochem. 91 (2004) 1151-1163
32. Swanson R.A., Liu J., Miller J.W., Rothstein J.D., Farrell K., Stein B.A., and Longuemare M.C. Neuronal regulation of glutamate transporter subtype expression in astrocytes. J. Neurosci. 17 (1997) 932-940
33. Tilleux S., and Hermans E. Down-regulation of astrocytic GLAST by microglia-related inflammation is abrogated in dibutyryl cAMP-differentiated cultures. J. Neurochem. 105 (2008) 2224-2236
34. Trotti D., Danbolt N.C., and Volterra A. Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration?. Trends Pharmacol. Sci. 19 (1998) 328-334
35. Trotti D., Rizzini B.L., Rossi D., Haugeto O., Racagni G., Danbolt N.C., and Volterra A. Neuronal and glial glutamate transporters possess an SH-based redox regulatory mechanism. Eur. J. Neurosci. 9 (1997) 1236-1243
36. Trotti D., Volterra A., Lehre K.P., Rossi D., Gjesdal O., Racagni G., and Danbolt N.C. Arachidonic acid inhibits a purified and reconstituted glutamate transporter directly from the water phase and not via the phospholipid membrane. J. Biol. Chem. 270 (1995) 9890-9895
37. Vermeiren C., Najimi M., Maloteaux J.-M., and Hermans E. Molecular and functional characterisation of glutamate transporters in rat cortical astrocytes exposed to a defined combination of growth factors during in vitro differentiation. Neurochem. Int. 46 (2005) 137-147
38. Volterra A., Trotti D., Cassutti P., Tromba C., Salvaggio A., Melcangi R.C., and Racagni G. High sensitivity of glutamate uptake to extracellular free arachidonic acid levels in rat cortical synaptosomes and astrocytes. J. Neurochem. 59 (1992) 600-606
39. Volterra A., Trotti D., Floridi S., and Racagni G. Reactive oxygen species inhibit high-affinity glutamate uptake: molecular mechanism and neuropathological implications. Ann. NY Acad. Sci. 738 (1994) 153-162
40. Volterra A., Trotti D., and Racagni G. Glutamate uptake is inhibited by arachidonic acid and oxygen radicals via two distinct and additive mechanisms. Mol. Pharmacol. 46 (1994) 986-992
41. Zerangue N., Arriza J.L., Amara S.G., and Kavanaugh M.P. Differential modulation of human glutamate transporter subtypes by arachidonic acid. J. Biol. Chem. 270 (1995) 6433-6435