Glutamate in the immune system: Glutamate receptors in immune cells, potent effects, endogenous production and involvement in disease

Nerve-Driven Immunity: Neurotransmitters and Neuropeptides in the Immune System

Volumn , Issue , 2012, Pages 121-162

  Ganor, Yonatan ^a   Levite, Mia ^b  

^a INSTITUT COCHIN   (France)

^b The Academic College of TLV Yaffo   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84894229739     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-7091-0888-8_4     Document Type: Chapter

References (124)

1. Affaticati P, Mignen O, Jambou F, Potier MC, Klingel-Schmitt I, Degrouard J, Peineau S, Gouadon E, Collingridge GL, Liblau R, Capiod T, Cohen-Kaminsky S (2011) Sustained calcium signalling and caspase-3 activation involve NMDA receptors in thymocytes in contact with dendritic cells. Cell Death Differ 18(1):99-108
2. Andrews PI, Mc Namara JO (1996) Rasmussen’s encephalitis: an autoimmune disorder? Curr Opin Neurobiol 6(5):673-678
3. Andrews PI, Dichter MA, Berkovic SF, Newton MR, Mc Namara JO (1996) Plasmapheresis in Rasmussen’s encephalitis. Neurology 46(1):242-246
4. Antozzi C, Granata T, Aurisano N, Zardini G, Confalonieri P, Airaghi G, Mantegazza R, Spreafico R (1998) Long-term selective IgG immuno-adsorption improves Rasmussen’s encephalitis. Neurology 51(1):302-305
5. Arcella A, Carpinelli G, Battaglia G, D’Onofrio M, Santoro F, Ngomba RT, Bruno V, Casolini P, Giangaspero F, Nicoletti F (2005) Pharmacological blockade of group II metabotropic glutamate receptors reduces the growth of glioma cells in vivo. Neuro Oncol 7(3):236-245
6. Armstrong N, Sun Y, Chen GQ, Gouaux E (1998) Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395(6705):913-917
7. Baranzini SE, Laxer K, Saketkhoo R, Elkins MK, Parent JM, Mantegazza R, Oksenberg JR (2002) Analysis of antibody gene rearrangement, usage, and specificity in chronic focal encephalitis. Neurology 58(5):709-716
8. Boldyrev AA, Kazey VI, Leinsoo TA, Mashkina AP, Tyulina OV, Johnson P, Tuneva JO, Chittur S, Carpenter DO (2004) Rodent lymphocytes express functionally active glutamate receptors. Biochem Biophys Res Commun 324(1):133-139
9. Bonsi P, Cuomo D, De Persis C, Centonze D, Bernardi G, Calabresi P, Pisani A (2005) Modulatory action of metabotropic glutamate receptor (mGluR) 5 on mGluR1 function in striatal cholinergic interneurons. Neuropharmacology 49(Suppl 1):104-113
10. Cahalan MD, Wulff H, Chandy KG (2001) Molecular properties and physiological roles of ion channels in the immune system. J Clin Immunol 21(4):235-252
11. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA, Zhang D (2002) Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415(6873):793-798
12. Chiocchetti A, Miglio G, Mesturini R, Varsaldi F, Mocellin M, Orilieri E, Dianzani C, Fantozzi R, Dianzani U, Lombardi G (2006) Group I mGlu receptor stimulation inhibits activation-induced cell death of human T lymphocytes. Br J Pharmacol 148(6):760-768 Chu Z, Hablitz JJ (2000) Quisqualate induces an inward current via mGluR activation in neocorti-cal pyramidal neurons. Brain Res 879(1-2):88-92
13. Cohen-Kashi Malina K, Ganor Y, Levite M, Teichberg VI (2006) Autoantibodies against an extracellular peptide of the GluR3 subtype of AMPA receptors activate both homomeric and heteromeric AMPA receptor channels. Neurochem Res 31(10):1181-1190
14. Collard CD, Park KA, Montalto MC, Alapati S, Buras JA, Stahl GL, Colgan SP (2002) Neutrophil-derived glutamate regulates vascular endothelial barrier function. J Biol Chem 277 (17):14801-14811
15. Collingridge GL, Singer W (1990) Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci 11(7):290-296
16. Dalmau J, Lancaster E, Martinez-Hernandez E, Rosenfeld MR, Balice-Gordon R (2011) Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis. Lancet Neurol 10(1):63-74
17. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65(1):1-105
18. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, Chen HS, Lipton SA, Nakanishi N (1998) Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393 (6683):377-381
19. Dickman KG, Youssef JG, Mathew SM, Said SI (2004) Ionotropic glutamate receptors in lungs and airways: molecular basis for glutamate toxicity. Am J Respir Cell Mol Biol 30(2):139-144
20. Divino Filho JC, Hazel SJ, Furst P, Bergstrom J, Hall K (1998) Glutamate concentration in plasma, erythrocyte and muscle in relation to plasma levels of insulin-like growth factor (IGF)-I, IGF binding protein-1 and insulin in patients on haemodialysis. J Endocrinol 156(3):519-527
21. Droge W, Eck HP, Betzler M, Schlag P, Drings P, Ebert W (1988) Plasma glutamate concentration and lymphocyte activity. J Cancer Res Clin Oncol 114(2):124-128
22. Droge W, Murthy KK, Stahl-Hennig C, Hartung S, Plesker R, Rouse S, Peterhans E, Kinscherf R, Fischbach T, Eck HP (1993) Plasma amino acid dysregulation after lentiviral infection. AIDS Res Hum Retroviruses 9(9):807-809
23. Eck HP, Drings P, Droge W (1989a) Plasma glutamate levels, lymphocyte reactivity and death rate in patients with bronchial carcinoma. J Cancer Res Clin Oncol 115(6):571-574
24. Eck HP, Frey H, Droge W (1989b) Elevated plasma glutamate concentrations in HIV-1-infected patients may contribute to loss of macrophage and lymphocyte functions. Int Immunol 1(4):367-372
25. Endoh T (2004) Characterization of modulatory effects of postsynaptic metabotropic glutamate receptors on calcium currents in rat nucleus tractus solitarius. Brain Res 1024(1-2):212-224
26. Ferrarese C, Aliprandi A, Tremolizzo L, Stanzani L, De Micheli A, Dolara A, Frattola L (2001) Increased glutamate in CSF and plasma of patients with HIV dementia. Neurology 57(4):671-675
27. Florance NR, Davis RL, Lam C, Szperka C, Zhou L, Ahmad S, Campen CJ, Moss H, Peter N, Gleichman AJ, Glaser CA, Lynch DR, Rosenfeld MR, Dalmau J (2009) Anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis in children and adolescents. Ann Neurol 66(1): 11-18
28. Foster AC, Fagg GE (1984) Acidic amino acid binding sites in mammalian neuronal membranes: their characteristics and relationship to synaptic receptors. Brain Res 319(2):103-164
29. Gahring L, Carlson NG, Meyer EL, Rogers SW (2001) Granzyme B proteolysis of a neuronal glutamate receptor generates an autoantigen and is modulated by glycosylation. J Immunol 166 (3):1433-1438
30. Ganor Y, Besser M, Ben-Zakay N, Unger T, Levite M (2003) Human T cells express a functional ionotropic glutamate receptor GluR3, and glutamate by itself triggers integrin-mediated adhesion to laminin and fibronectin and chemotactic migration. J Immunol 170(8):4362-4372
31. Ganor Y, Goldberg-Stern H, Amrom D, Lerman-Sagie T, Teichberg VI, Pelled D, Futerman AH, Zeev BB, Freilinger M, Verheulpen D, Van Bogaert P, Levite M (2004) Autoimmune epilepsy: some epilepsy patients harbor autoantibodies to glutamate receptors and dsDNA on both sides of the blood-brain barrier, which may kill neurons and decrease in brain fluids after hemispherotomy. Clin Dev Immunol 11(3-4):241-252
32. Ganor Y, Goldberg-Stern H, Lerman-Sagie T, Teichberg VI, Levite M (2005a) Autoimmune epilepsy: distinct subpopulations of epilepsy patients harbor serum autoantibodies to either glutamate/AMPA receptor GluR3, glutamate/NMDA receptor subunit NR2A or doublestranded DNA. Epilepsy Res 65(1-2):11-22
33. Ganor Y, Gottlieb M, Eilam R, Otmy H, Teichberg VI, Levite M (2005b) Immunization with the glutamate receptor-derived peptide GluR3B induces neuronal death and reactive gliosis, but confers partial protection from pentylenetetrazole-induced seizures. Exp Neurol 195(1):92-102
34. Ganor Y, Teichberg VI, Levite M (2007) TCR activation eliminates glutamate receptor GluR3 from the cell surface of normal human T cells, via an autocrine/paracrine granzyme B-mediated proteolytic cleavage. J Immunol 178(2):683-692
35. Ganor Y, Grinberg I, Reis A, Cooper I, Goldstein RS, Levite M (2009) Human T-leukemia and T-lymphoma express glutamate receptor AMPA GluR3, and the neurotransmitter glutamate elevates the cancer-related matrix-metalloproteinases inducer CD147/EMMPRIN, MMP-9 secretion and engraftment of T-leukemia in vivo. Leuk Lymphoma 50(6):985-997
36. Gill SS, Pulido OM (2001) Glutamate receptors in peripheral tissues: current knowledge, future research, and implications for toxicology. Toxicol Pathol 29(2):208-223
37. Graham TE, Sgro V, Friars D, Gibala MJ (2000) Glutamate ingestion: the plasma and muscle free amino acid pools of resting humans. Am J Physiol Endocrinol Metab 278(1):E83-89
38. Green DR, Droin N, Pinkoski M (2003) Activation-induced cell death in T cells. Immunol Rev 193:70-81
39. 2+ signaling in T-lymphocytes. Crit Rev Immunol 18(5):419-448
40. Hawkins LM, Chazot PL, Stephenson FA (1999) Biochemical evidence for the co-association of three N-methyl-D-aspartate (NMDA) R2 subunits in recombinant NMDA receptors. J Biol Chem 274(38):27211-27218
41. Hemmer B, Cepok S, Nessler S, Sommer N (2002) Pathogenesis of multiple sclerosis: an update on immunology. Curr Opin Neurol 15(3):227-231
42. Hinoi E, Yoneda Y (2011) Possible involvement of glutamatergic signaling machineries in pathophysiology of rheumatoid arthritis. J Pharmacol Sci 116(3):248-256
43. Hinoi E, Ogita K, Takeuchi Y, Ohashi H, Maruyama T, Yoneda Y (2001) Characterization with [3H]quisqualate of group I metabotropic glutamate receptor subtype in rat central and peripheral excitable tissues. Neurochem Int 38(3):277-285
44. Hinoi E, Takarada T, Ueshima T, Tsuchihashi Y, Yoneda Y (2004) Glutamate signaling in peripheral tissues. Eur J Biochem 271(1):1-13
45. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108 Hollmann M, O’Shea-Greenfield A, Rogers SW, Heinemann S (1989) Cloning by functional expression of a member of the glutamate receptor family. Nature 342(6250):643-648
46. Huerta PT, Kowal C, DeGiorgio LA, Volpe BT, Diamond B (2006) Immunity and behavior: antibodies alter emotion. Proc Natl Acad Sci USA 103(3):678-683
47. Huettner JE (2003) Kainate receptors and synaptic transmission. Prog Neurobiol 70(5):387-407
48. Hughes EG, Peng X, Gleichman AJ, Lai M, Zhou L, Tsou R, Parsons TD, Lynch DR, Dalmau J, Balice-Gordon RJ (2011) Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J Neurosci 30(17):5866-5875
49. Irani SR, Vincent A (2011) NMDA receptor antibody encephalitis. Curr Neurol Neurosci Rep 11 (3):298-304
50. Ishiuchi S, Tsuzuki K, Yoshida Y, Yamada N, Hagimura N, Okado H, Miwa A, Kurihara H, Nakazato Y, Tamura M, Sasaki T, Ozawa S (2002) Blockage of Ca(2+)-permeable AMPA receptors suppresses migration and induces apoptosis in human glioblastoma cells. Nat Med 8(9):971-978
51. Kalariti N, Pissimissis N, Koutsilieris M (2005) The glutamatergic system outside the CNS and in cancer biology. Expert Opin Investig Drugs 14(12):1487-1496
52. Kaul M, Zheng J, Okamoto S, Gendelman HE, Lipton SA (2005) HIV-1 infection and AIDS: consequences for the central nervous system. Cell Death Differ 12(Suppl 1):878-892
53. Keinanen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249(4968):556-560
54. Kew JN, Kemp JA (2005) Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology (Berl) 179(1):4-29
55. Komuro H, Rakic P (1993) Modulation of neuronal migration by NMDA receptors. Science 260(5104):95-97
56. Kostanyan IA, Merkulova MI, Navolotskaya EV, Nurieva RI (1997) Study of interaction between L-glutamate and human blood lymphocytes. Immunol Lett 58(3):177-180
57. Kowal C, DeGiorgio LA, Nakaoka T, Hetherington H, Huerta PT, Diamond B, Volpe BT (2004) Cognition and immunity; antibody impairs memory. Immunity 21(2):179-188
58. Lerma J (2006) Kainate receptor physiology. Curr Opin Pharmacol 6(1):89-97
59. Levite M (2002) Autoimmune epilepsy. Nat Immunol 3(6):500
60. Levite M (2008) Neurotransmitters activate T-cells and elicit crucial functions via neurotransmitter receptors. Curr Opin Pharmacol 8(4):460-471
61. Levite M, Ganor Y (2008) Autoantibodies to glutamate receptors can damage the brain in epilepsy, systemic lupus erythematosus and encephalitis. Expert Rev Neurother 8(7):1141-1160
62. Levite M, Hermelin A (1999) Autoimmunity to the glutamate receptor in mice-a model for Rasmussen’s encephalitis? J Autoimmun 13(1):73-82
63. Levite M, Fleidervish IA, Schwarz A, Pelled D, Futerman AH (1999) Autoantibodies to the glutamate receptor kill neurons via activation of the receptor ion channel. J Autoimmun 13 (1):61-72
64. Levite M, Cahalon L, Peretz A, Hershkoviz R, Sobko A, Ariel A, Desai R, Attali B, Lider O (2000) Extracellular K(+) and opening of voltage-gated potassium channels activate T cell integrin function: physical and functional association between Kv1.3 channels and beta1 integrins. J Exp Med 191(7):1167-1176
65. Li F, Tsien JZ (2009) Memory and the NMDA receptors. N Engl J Med 361(3):302-303
66. Lin CS, Boltz RC, Blake JT, Nguyen M, Talento A, Fischer PA, Springer MS, Sigal NH, Slaughter RS, Garcia ML et al (1993) Voltage-gated potassium channels regulate calcium-dependent pathways involved in human T lymphocyte activation. J Exp Med 177(3):637-645
67. Lombardi G, Dianzani C, Miglio G, Canonico PL, Fantozzi R (2001) Characterization of ionotropic glutamate receptors in human lymphocytes. Br J Pharmacol 133(6):936-944
68. Lombardi G, Miglio G, Canonico PL, Naldi P, Comi C, Monaco F (2003) Abnormal response to glutamate of T lymphocytes from multiple sclerosis patients. Neurosci Lett 340(1):5-8
69. Lombardi G, Miglio G, Dianzani C, Mesturini R, Varsaldi F, Chiocchetti A, Dianzani U, Fantozzi R (2004) Glutamate modulation of human lymphocyte growth: in vitro studies. Biochem Biophys Res Commun 318(2):496-502
70. Mantegazza R, Bernasconi P, Baggi F, Spreafico R, Ragona F, Antozzi C, Bernardi G, Granata T (2002) Antibodies against GluR3 peptides are not specific for Rasmussen’s encephalitis but are also present in epilepsy patients with severe, early onset disease and intractable seizures. J Neuroimmunol 131(1-2):179-185
71. Manto M, Dalmau J, Didelot A, Rogemond V, Honnorat J (2011) In vivo effects of antibodies from patients with anti-NMDA receptor encephalitis: further evidence of synaptic glutamatergic dysfunction. Orphanet J Rare Dis 5:31
72. Mashkina AP, Tyulina OV, Solovyova TI, Kovalenko EI, Kanevski LM, Johnson P, Boldyrev AA (2007) The excitotoxic effect of NMDA on human lymphocyte immune function. Neurochem Int 51(6-7):356-360
73. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349(6312):760-765
74. Mayer ML (2005a) Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity. Neuron 45(4):539-552
75. Mayer ML (2005b) Glutamate receptor ion channels. Curr Opin Neurobiol 15(3):282-288
76. Mayer ML, Westbrook GL (1987) The physiology of excitatory amino acids in the vertebrate central nervous system. Prog Neurobiol 28(3):197-276
77. Meldrum BS (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130(4S Suppl):1007S-1015S
78. Merrill JE, Benveniste EN (1996) Cytokines in inflammatory brain lesions: helpful and harmful.Trends Neurosci 19(8):331-338
79. Miglio G, Varsaldi F, Dianzani C, Fantozzi R, Lombardi G (2005a) Stimulation of group I metabotropic glutamate receptors evokes calcium signals and c-jun and c-fos gene expression in human T cells. Biochem Pharmacol 70(2):189-199
80. Miglio G, Varsaldi F, Lombardi G (2005b) Human T lymphocytes express N-methyl-D-aspartate receptors functionally active in controlling T cell activation. Biochem Biophys Res Commun 338(4):1875-1883
81. Miglio G, Dianzani C, Fallarini S, Fantozzi R, Lombardi G (2007) Stimulation ofN-methyl-D-aspartate receptors modulates Jurkat T cell growth and adhesion to fibronectin. Biochem Biophys Res Commun 361(2):404-409
82. Monaghan DT, Bridges RJ, Cotman CW (1989) The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol 29:365-402
83. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354(6348):31-37
84. Moscato EH, Jain A, Peng X, Hughes EG, Dalmau J, Balice-Gordon RJ (2011) Mechanisms underlying autoimmune synaptic encephalitis leading to disorders of memory, behavior and cognition: insights from molecular, cellular and synaptic studies. Eur J Neurosci 32(2):298-309
85. Nakayama T, Yamashita M (2010) The TCR-mediated signaling pathways that control the direction of helper T cell differentiation. Semin Immunol 22(5):303-309
86. Nedergaard M, Takano T, Hansen AJ (2002) Beyond the role of glutamate as a neurotransmitter.Nat Rev Neurosci 3(9):748-755
87. Nicoletti F, Arcella A, Iacovelli L, Battaglia G, Giangaspero F, Melchiorri D (2007) Metabotropic glutamate receptors: new targets for the control of tumor growth? Trends Pharmacol Sci 28(5):206-213
88. Ohashi H, Maruyama T, Higashi-Matsumoto H, Nomoto T, Nishimura S, Takeuchi Y (2002) A novel binding assay for metabotropic glutamate receptors using [3H] L-quisqualic acid and recombinant receptors. Z Naturforsch C 57(3-4):348-355
89. Ollenschlager G, Karner J, Karner-Hanusch J, Jansen S, Schindler J, Roth E (1989) Plasma glutamate-a prognostic marker of cancer and of other immunodeficiency syndromes? Scand J Clin Lab Invest 49(8):773-777
90. Pacheco R, Ciruela F, Casado V, Mallol J, Gallart T, Lluis C, Franco R (2004) Group I metabotropic glutamate receptors mediate a dual role of glutamate in T cell activation. J Biol Chem 279(32):33352-33358
91. Pacheco R, Oliva H, Martinez-Navio JM, Climent N, Ciruela F, Gatell JM, Gallart T, Mallol J, Lluis C, Franco R (2006) Glutamate released by dendritic cells as a novel modulator of T cell activation. J Immunol 177(10):6695-6704
92. Pacheco R, Gallart T, Lluis C, Franco R (2007) Role of glutamate on T-cell mediated immunity.J Neuroimmunol 185(1-2):9-19
93. Piani D, Frei K, Do KQ, Cuenod M, Fontana A (1991) Murine brain macrophages induced NMDA receptor mediated neurotoxicity in vitro by secreting glutamate. Neurosci Lett 133(2):159-162
94. Piani D, Spranger M, Frei K, Schaffner A, Fontana A (1992) Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur J Immunol 22(9):2429-2436
95. Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34(1):1-26
96. Pitt D, Werner P, Raine CS (2000) Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6(1):67-70
97. Platt SR (2007) The role of glutamate in central nervous system health and disease-a review. Vet J 173(2):278-286
98. Poulopoulou C, Davaki P, Koliaraki V, Kolovou D, Markakis I, Vassilopoulos D (2005a) Reduced expression of metabotropic glutamate receptor 2 mRNA in T cells of ALS patients. Ann Neurol 58(6):946-949
99. Poulopoulou C, Markakis I, Davaki P, Nikolaou C, Poulopoulos A, Raptis E, Vassilopoulos D (2005b) Modulation of voltage-gated potassium channels in human T lymphocytes by extracellular glutamate. Mol Pharmacol 67(3):856-867
100. Poulopoulou C, Papadopoulou-Daifoti Z, Hatzimanolis A, Fragiadaki K, Polissidis A, Anderzanova E, Davaki P, Katsiari CG, Sfikakis PP (2008) Glutamate levels and activity of the T cell voltage-gated potassium Kv1.3 channel in patients with systemic lupus erythematosus. Arthritis Rheum 58(5):1445-1450
101. Reynolds JD, Amory DW, Grocott HP, White WD, Newman MF (2002) Change in plasma glutamate concentration during cardiac surgery is a poor predictor of cognitive outcome. J Cardiothorac Vasc Anesth 16(4):431-436
102. Rezzani R, Corsetti G, Rodella L, Angoscini P, Lonati C, Bianchi R (2003) Cyclosporine-A treatment inhibits the expression of metabotropic glutamate receptors in rat thymus. Acta Histochem 105(1):81-87
103. Rogers SW, Andrews PI, Gahring LC, Whisenand T, Cauley K, Crain B, Hughes TE, Heinemann SF, Mc Namara JO (1994) Autoantibodies to glutamate receptor GluR3 in Rasmussen’s encephalitis. Science 265(5172):648-651
104. Rosenmund C, Stern-Bach Y, Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280(5369):1596-1599
105. Rzeski W, Turski L, Ikonomidou C (2001) Glutamate antagonists limit tumor growth. Proc Natl Acad Sci USA 98(11):6372-6377
106. Sarchielli P, Di Filippo M, Candeliere A, Chiasserini D, Mattioni A, Tenaglia S, Bonucci M, Calabresi P (2007) Expression of ionotropic glutamate receptor GLUR3 and effects of glutamate on MBP-and MOG-specific lymphocyte activation and chemotactic migration in multiple sclerosis patients. J Neuroimmunol 188(1-2):146-158
107. Sattler R, Tymianski M (2001) Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 24(1-3):107-129
108. Schmitz D, Mellor J, Nicoll RA (2001) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291(5510):1972-1976
109. Sixt M, Engelhardt B, Pausch F, Hallmann R, Wendler O, Sorokin LM (2001) Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J Cell Biol 153(5):933-946
110. Sladeczek F, Momiyama A, Takahashi T (1993) Presynaptic inhibitory action of a metabotropic glutamate receptor agonist on excitatory transmission in visual cortical neurons. Proc Biol Sci 253(1338):297-303
111. Smith T, Groom A, Zhu B, Turski L (2000) Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat Med 6(1):62-66
112. Song I, Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25(11):578-588
113. Stepulak A, Sifringer M, Rzeski W, Endesfelder S, Gratopp A, Pohl EE, Bittigau P, Felderhoff-Mueser U, Kaindl AM, Buhrer C, Hansen HH, Stryjecka-Zimmer M, Turski L, Ikonomidou C (2005) NMDA antagonist inhibits the extracellular signal-regulated kinase pathway and suppresses cancer growth. Proc Natl Acad Sci USA 102(43):15605-15610
114. Stepulak A, Luksch H, Gebhardt C, Uckermann O, Marzahn J, Sifringer M, Rzeski W, Staufner C, Brocke KS, Turski L, Ikonomidou C (2009) Expression of glutamate receptor subunits in human cancers. Histochem Cell Biol 132(4):435-445
115. Storto M, de Grazia U, Battaglia G, Felli MP, Maroder M, Gulino A, Ragona G, Nicoletti F, Screpanti I, Frati L, Calogero A (2000) Expression of metabotropic glutamate receptors in murine thymocytes and thymic stromal cells. J Neuroimmunol 109(2):112-120
116. Sturgill JL, Mathews J, Scherle P, Conrad DH (2011) Glutamate signaling through the kainate receptor enhances human immunoglobulin production. J Neuroimmunol 233(1-2):80-89
117. Takano T, Lin JH, Arcuino G, Gao Q, Yang J, Nedergaard M (2001) Glutamate release promotes growth of malignant gliomas. Nat Med 7(9):1010-1015
118. Tanabe Y, Masu M, Ishii T, Shigemoto R, Nakanishi S (1992) A family of metabotropic glutamate receptors. Neuron 8(1):169-179
119. Tay DL, Hoffbrand AV, Wickremasinghe GR (1996) Expression of c-fos and c-jun proteins and AP-1 binding activity during cell cycle progression of HL60 cells and phytohemagglutinin-stimulated lymphocytes. Exp Hematol 24(2):277-284
120. Twyman RE, Gahring LC, Spiess J, Rogers SW (1995) Glutamate receptor antibodies activate a subset of receptors and reveal an agonist binding site. Neuron 14(4):755-762
121. Tziperman B, Garty BZ, Schoenfeld N, Hoffer V, Watemberg N, Lev D, Ganor Y, Levite M, Lerman-Sagie T (2007) Acute intermittent porphyria, Rasmussen encephalitis, or both? J Child Neurol 22(1):99-105
122. Vincent A, Bien CG, Irani SR, Waters P (2011) Autoantibodies associated with diseases of the CNS: new developments and future challenges. Lancet Neurol 10(8):759-772
123. Wiendl H, Bien CG, Bernasconi P, Fleckenstein B, Elger CE, Dichgans J, Mantegazza R, Melms A (2001) GluR3 antibodies: prevalence in focal epilepsy but no specificity for Rasmussen’s encephalitis. Neurology 57(8):1511-1514
124. Zhou L, Chong MM, Littman DR (2009) Plasticity of CD4+ T cell lineage differentiation. Immunity 30(5):646-655