Expression and functional role of mGluR3 and mGluR5 in human astrocytes and glioma cells: Opposite regulation of glutamate transporter proteins

European Journal of Neuroscience

Volumn 17, Issue 10, 2003, Pages 2106-2118

  Aronica, Eleonora ^a,b   Gorter, Jan A ^b,c   Ijlst Keizers, Helen ^a   Rozemuller, Annemieke J ^a   Yankaya, Bulent ^a   Leenstra, Sieger ^a   Troost, Dirk ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b STICHTING EPILEPSIE INSTELLINGEN NEDERLAND SEIN   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Cultures; Glioma; Glutamate transporters; Human astrocytes; Metabotropic glutamate receptors; Western blot

Indexed keywords

2 (2,3 DICARBOXYCYCLOPROPYL)GLYCINE; 3,5 DIHYDROXYPHENYLGLYCINE; CELL PROTEIN; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR AGONIST; GLUTAMATE TRANSPORTER; GROWTH FACTOR; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 5; PROTEIN EAAT3; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTE; CANCER CELL CULTURE; CELL CULTURE; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION; GENE FUNCTION; GLIOMA CELL; HORMONE RECEPTOR INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; RECEPTOR INTRINSIC ACTIVITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADULT; AGED; AGED, 80 AND OVER; AMINO ACID TRANSPORT SYSTEM X-AG; ASTROCYTES; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; EXCITATORY AMINO ACID TRANSPORTER 3; GENE EXPRESSION; GLIOBLASTOMA; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; GROWTH SUBSTANCES; HUMANS; IMMUNOPHENOTYPING; RECEPTORS, METABOTROPIC GLUTAMATE; SYMPORTERS; TUMOR CELLS, CULTURED;

EID: 0038810014     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02657.x     Document Type: Article

References (67)

1. Agrawal, S.K., Theriault, E. & Fehlings, M.G. (1998) Role of group I metabotropic glutamate receptors in traumatic spinal cord white matter injury. J. Neurotrauma, 15, 929-941.
2. Anderson, C.M. & Swanson, R.A. (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia, 32, 1-14.
3. Aronica, E., van Vliet, E.A., Mayboroda, O.A., Troost, D., da Silva, F.H. & Gorter, J.A. (2000) Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur. J. Neurosci., 12, 2333-2344.
4. Aronica, E., Catania, M.V., Geurts, J., Yankaya, B. & Troost, D. (2001a) Immunohistochemical localization of group I and II metabotropic glutamate receptors in control and amyotrophic lateral sclerosis human spinal cord: upregulation in reactive astrocytes. Neuroscience, 105, 509-520.
5. Aronica, E., Yankaya, B., Jansen, G.H., Leenstra, S., van Veelen, C.W., Gorter, J.A. & Troost, D. (2001b) Ionotropic and metabotropic glutamate receptor protein expression in glioneuronal tumours from patients with intractable epilepsy. Neuropathol. Appl. Neurobiol., 27, 223-237.
6. Balazs, R., Miller, S., Romano, C., de Vries, A., Chun, Y. & Cotman, C.W. (1997) Metabotropic glutamate receptor mGluR5 in astrocytes: pharmacological properties and agonist regulation. J. Neurochem., 69, 151-163.
7. Biber, K., Laurie, D.J., Berthele, A., Sommer, B., Tolle, T.R., Gebicke-Harter, P.J., van Calker, D. & Boddeke, H.W. (1999) Expression and signaling of group I metabotropic glutamate receptors in astrocytes and microglia. J. Neurochem., 72, 1671-1680.
8. Boxall, S.J., Thompson, S.W., Dray, A., Dickenson, A.H. & Urban, L. (1996) Metabotropic glutamate receptor activation contributes to nociceptive reflex activity in the rat spinal cord in vitro. Neuroscience, 74, 13-20.
9. Bruno, V., Battaglia, G., Casabona, G., Copani, A., Caciagli, F. & Nicoletti, F. (1998) Neuroprotection by glial metabotropic glutamate receptors is mediated by transforming growth factor-beta. J. Neurosci., 18, 9594-9600.
10. Cai, Z., Schools, G.P. & Kimelberg, H.K. (2000) Metabotropic glutamate receptors in acutely isolated hippocampal astrocytes: developmental changes of mGluR5 mRNA and functional expression. Glia, 29, 70-80.
11. Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
12. Ciccarelli, R., Sureda, F.X., Casabona, G., Di Iorio, P., Caruso, A., Spinella, F., Condorelli, D.F., Nicoletti, F. & Caciagli, F. (1997) Opposite influence of the metabotropic glutamate receptor subtypes mGlu3 and -5 on astrocyte proliferation in culture. Glia, 21, 390-398.
13. Ciccarelli, R., Di Iorio, P., Bruno, V., Battaglia, G., D'Alimonte, I., D'Onofrio, M., Nicoletti, F. & Caciagli, F. (1999) Activation of A(1) adenosine or mGlu3 metabotropic glutamate receptors enhances the release of nerve growth factor and S-100beta protein from cultured astrocytes. Glia, 27, 275-281.
14. Condorelli, D.F., Dell'Albani, P., Corsaro, M., Giuffrida, R., Caruso, A., Trovato Salinaro, A., Spinella, F., Nicoletti, F., Albanese, V. & Giuffrida Stella, A.M. (1997) Metabotropic glutamate receptor expression in cultured rat astrocytes and human gliomas. Neurochem. Res., 22, 1127-1133.
15. Condorelli, D.F., Conti, F., Gallo, V., Kirchhoff, F., Seifert, G., Steinhauser, C., Verkhratsky, A. & Yuan, X. (1999) Expression and functional analysis of glutamate receptors in glial cells. Adv. Exp. Med. Biol., 468, 49-67.
16. Conti, F., Melone, M., De Biasi, S., Minelli, A., Brecha, N.C. & Ducati, A. (1998) Neuronal and glial localization of GAT-1, a high-affinity gamma-aminobutyric acid plasma membrane transporter, in human cerebral cortex: with a note on its distribution in monkey cortex. J. Comp. Neurol., 396, 51-63.
17. De Groot, C.J., Langeveld, C.H., Jongenelen, C.A., Montagne, L., Van Der Valk, P. & Dijkstra, C.D. (1997) Establishment of human adult astrocyte cultures derived from postmortem multiple sclerosis and control brain and spinal cord regions: immunophenotypical and functional characterization. J. Neurosci. Res., 49, 342-354.
18. D'Onofrio, M., Cuomo, L., Battaglia, G., Ngomba, R.T., Storto, M., Kingston, A.E., Orzi, F., De Blasi, A., Di Iorio, P., Nicoletti, F. & Bruno, V. (2001) Neuroprotection mediated by glial group-II metabotropic glutamate receptors requires the activation of the MAP kinase and the phosphatidylinositol-3-kinase pathways. J. Neurochem., 78, 435-445.
19. Dunlop, J., Lou, Z. & McIlvain, H.B. (1999) Properties of excitatory amino acid transport in the human U373 astrocytoma cell line. Brain Res., 839, 235-242.
20. Ferraguti, E, Corti, C., Valerio, E., Mion, S. & Xuereb, J. (2001) Activated astrocytes in areas of kainate-induced neuronal injury upregulate the expression of the metabotropic glutamate receptors 2/3 and 5. Exp. Brain Res., 137, 1-11.
21. Fine, S.M., Angel, R.A., Perry, S.W., Epstein, L.G., Rothstein, J.D., Dewhurst, S. & Gelbard, H.A. (1996) Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. Implications for pathogenesis of HIV-1 dementia. J. Biol. Chem., 271, 15 303-15 306.
22. Furuta, A., Rothstein, J.D. & Martin, L.J. (1997) Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J. Neurosci., 17, 8363-8375.
23. Gasparini, F., Lingenhohl, K., Stoehr, N., Flor, P.J., Heinrich, M., Vranesic, I., Biollaz, M., Allgeier, H., Heckendom, R., Urwyler, S., Varney, M.A., Johnson, E.C., Hess, S.D., Rao, S.P., Sacaan, A.I., Santori, E.M., Velicelebi, G. & Kuhn, R. (1999) 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology, 38, 1493-1503.
24. Gegelashvili, G., Civenni, G., Racagni, G., Danbolt, N.C., Schousboe, I. & Schousboe, A. (1996) Glutamate receptor agonists up-regulate glutamate transporter GLAST in astrocytes. Neuroreport, 8, 261-265.
25. Gegelashvili, G., Danbolt, N.C. & Schousboe, A. (1997) Neuronal soluble factors differentially regulate the expression of the GLT1 and GLAST glutamate transporters in cultured astroglia. J. Neurochem., 69, 2612-2615.
26. Gegelashvili, G., Dehnes, Y., Danboh, N.C. & Schousboe, A. (2000) The high-affinity glutamate transporters GLT1, GLAST, and EAAT4 are regulated via different signalling mechanisms. Neurochem. Int., 37, 163-170.
27. Gegelashvili, G., Robinson, M.B., Trotti, D. & Rauen, T. (2001) Regulation of glutamate transporters in health and disease. Prog. Brain Res., 132, 267-286.
28. Gorter, J.A., Van Vliet, E.A., Proper, E.A., De Graan, P.N., Ghijsen, W.E., Lopes Da Silva, F.H. & Aronica, E. (2002) Glutamate transporters alterations in the reorganizing dentate gyrus are associated with progressive seizure activity in chronic epileptic rats. J. Comp. Neurol., 442, 365-377.
29. Kimura, K., Hattori, S., Kabuyama, Y., Shizawa, Y., Takayanagi, J., Nakamura, S., Toki, S., Matsuda, Y., Onodera, K. & Fukui, Y. (1994) Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem., 269, 18 961-18 967.
30. Kleihues, P. & Cavanee, W.K. (2000) World Health Organization classification of tumours. In Pathology and Genetics of Tumours of the Nervous System. Astrocytic tumours. IARC Press, Lyon. pp. 9-52.
31. Kondoh, T., Nishizaki, T., Aihara, H. & Tamaki, N. (2001) NMDA-responsible, APV-insensitive receptor in cultured human astrocytes. Life Sci., 68, 1761-1767.
32. Litschig, S., Gasparini, F., Rueegg, D., Stoehr, N., Flor, P.J., Vranesic, I., Prezeau, L., Pin, J.P., Thomsen, C. & Kuhn, R. (1999) CPCCOEt, a noncompetitive metabotropic glutamate receptor 1 antagonist, inhibits receptor signaling without affecting glutamate binding. Mol. Pharmacol., 55, 453-461.
33. Meldrum, B.S. (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J. Nutr., 130, 1007S-1015S.
34. Miller, S., Kesslak, J.P., Romano, C. & Cotman, C.W. (1995a) Roles of metabotropic glutamate receptors in brain plasticity and pathology. Ann. N.Y. Acad. Sci., 757, 460-474.
35. Miller, S., Romano, C. & Cotman, C.W. (1995b) Growth factor upregulation of a phosphoinositide-coupled metabotropic glutamate receptor in cortical astrocytes. J. Neurosci., 15, 6103-6109.
36. Miller, S., Sehati, N., Romano, C. & Cotman, C.W. (1996) Exposure of astrocytes to thrombin reduces levels of the metabotropic glutamate receptor mGluR5. J. Neurochem., 67, 1435-1447.
37. Minoshima, T. & Nakanishi, S. (1999) Structural organization of the mouse metabotropic glutamate receptor subtype 3 gene and its regulation by growth factors in cultured cortical astrocytes. J. Biochem. (Tokyo), 126, 889-896.
38. Nakanishi, S. (1994) Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron, 13, 1031-1037.
39. Ohishi, H., Ogawa-Meguro, R., Shigemoto, R., Kaneko, T., Nakanishi, S. & Mizuno, N. (1994) Immunohistochemical localization of metabotropic glutamate receptors, mGluR2 and mGluR3, in rat cerebellar cortex. Neuron, 13, 55-66.
40. Palos, T.P., Ramachandran, B., Boado, R. & Howard, B.D. (1996) Rat C6 and human astrocytic tumor cells express a neuronal type of glutamate transporter. Brain Res. Mol. Brain Res., 37, 297-303.
41. Petralia, R.S., Wang, Y.X., Niedzielski, A.S. & Wenthold, R.J. (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience, 71, 949-976.
42. Pin, J.P. & Duvoisin, R. (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology, 34, 1-26.
43. Romano, C., Sesma, M.C.T.M., O'Malley, K., Van den Pol, A.N. & Olney, J.W. (1995) Distribution of metabotropic glutamate receptor mGluR immunoreactivity in rat brain. J. Comp. Neurol., 355, 455-469.
44. Romano, C., Yang, W.L. & O'Malley, K.L. (1996) Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J. Biol. Chem., 271, 28612-28616.
45. Rothstein, J.D., Martin, L., Levey, A.I., Dykes-Hoberg, M., Jin, L., Wu, D., Nash, N. & Kuncl, R.W. (1994) Localization of neuronal and glial glutamate transporters. Neuron, 13, 713-725.
46. Schaffhauser, H., Richards, J.G., Cartmell, J., Chaboz, S., Kemp, J.A., Klingelschmidt, A., Messer, J., Stadler, H., Woltering, T. & Mutel, V. (1998) In vitro binding characteristics of a new selective group II metabotropic glutamate receptor radioligand, [3H]LY354740, in rat brain. Mol. Pharmacol., 53, 228-233.
47. Schlag, B.D., Vondrasek, J.R., Munir, M., Kalandadze, A., Zelenaia, O.A., Rothstein, J.D. & Robinson, M.B. (1998) Regulation of the glial Na+-dependent glutamate transporters by cyclic AMP analogs and neurons. Mol. Pharmacol., 53, 355-369.
48. Schoepp, D.D., Goldsworthy, J., Johnson, B.G., Salhoff, C.R. & Baker, S.R. (1994) 3,5-dihydroxyphenylglycine is a highly selective agonist for phosphoinositide-linked metabotropic glutamate receptors in the rat hippocampus. J. Neurochem., 63, 769-772.
49. Schoepp, D.D., Jane, D.E. & Monn, J.A. (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology, 38, 1431-1476.
50. Schools, G.P. & Kimelberg, H.K. (1999) mGluR3 and mGluR5 are the predominant metabotropic glutamate receptor mRNAs expressed in hippocampal astrocytes acutely isolated from young rats. J. Neurosci. Res., 58, 533-543.
51. Schweitzer, C., Kratzeisen, C., Adam, G., Lundstrom, K., Malherbe, P., Ohresser, S., Stadler, H., Wichmann, J., Woltering, T. & Mutel, V. (2000) Characterization of [(3)H]-LY354740 binding to rat mGlu2 and mGlu3 receptors expressed in CHO cells using semliki forest virus vectors. Neuropharmacology, 39, 1700-1706.
52. Seifert, G. & Steinhauser, C. (2001) Ionotropic glutamate receptors in astrocytes. Prog. Brain Res., 132, 287-299.
53. Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P.J., Neki, A., Abe, T., Nakanishi, S. & Mizuno, N. (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci., 17, 7503-7522.
54. Sims, K.D. & Robinson, M.B. (1999) Expression patterns and regulation of glutamate transporters in the developing and adult nervous system. Crit. Rev. Neurobiol., 13, 169-197.
55. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. & Klenk, D.C. (1985) Measurement of protein using bicinchoninic acid. [Published erratum appears in Anal. Biochem. 1987 May 15; 163(1), 279.] Anal. Biochem., 150, 76-85.
56. Steinhauser, C. & Gallo, V. (1996) News on glutamate receptors in glial cells. Trends Neurosci., 19, 339-345.
57. Swanson, R.A., Liu, J., Miller, J.W., Rothstein, J.D., Farrell, K., Stein, B.A. & Longuemare, M.C. (1997) Neuronal regulation of glutamate transporter subtype expression in astrocytes. J. Neurosci., 17, 932-940.
58. Tanaka, K. (2000) Functions of glutamate transporters in the brain. Neurosci. Res., 37, 15-19.
59. Testa, C.M., Standaert, D.G., Young, A.B. & Penney, J.B. Jr (1994) Metabotropic glutamate receptor mRNA expression in the basal ganglia of the rat. J. Neurosci., 14, 3005-3018.
60. Ulas, J., Satou, T, Ivins, K.J., Kesslak, J.P., Cotman, C.W. & Balazs, R. (2000) Expression of metabotropic glutamate receptor 5 is increased in astrocytes after kainate-induced epileptic seizures. Glia, 30, 352-361.
61. Verkhratsky, A. & Steinhauser, C. (2000) Ion channels in glial cells. Brain Res. Brain Res. Rev., 32, 380-412.
62. Wang, C., Pralong, W.F., Schulz, M.F., Rougon, G., Aubry, J.M., Pagliusi, S., Robert, A. & Kiss, J.Z. (1996) Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: a critical role in regulating polysialic acid-neural cell adhesion molecule expression and cell migration. J. Cell Biol., 135, 1565-1581.
63. Winder, D.G. & Conn, P.J. (1996) Roles of metabotropic glutamate receptors in glial function and glial-neuronal communication. J. Neurosci. Res., 46, 131-137.
64. Wroblewska, B., Santi, M.R. & Neale, J.H. (1998) N-acetylaspartylglutamate activates cyclic AMP-coupled metabotropic glutamate receptors in cerebellar astrocytes. Glia, 24, 172-179.
65. Yao, R. & Cooper, G.M. (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science, 267, 2003-2006.
66. Ye, Z.C., Rothstein, J.D. & Sontheimer, H. (1999) Compromised glutamate transport in human glioma cells: reduction-mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange. J. Neurosci., 19, 10 767-10 777.
67. Zelenaia, O., Schlag, B.D., Gochenauer, G.E., Ganel, R., Song, W., Beesley, J.S., Grinspan, J.B., Rothstein, J.D. & Robinson, M.B. (2000) Epidermal growth factor receptor agonists increase expression of glutamate transporter GLT-1 in astrocytes through pathways dependent on phosphatidylinositol 3-kinase and transcription factor NF-kappaB. Mol. Pharmacol., 57, 667-678.