The neurotransmitter glutamate and human T cells: Glutamate receptors and glutamate-induced direct and potent effects on normal human T cells, cancerous human leukemia and lymphoma T cells, and autoimmune human T cells

Journal of Neural Transmission

Volumn 121, Issue 8, 2014, Pages 983-1006

  Ganor, Yonatan ^a   Levite, Mia ^b  

^a INSTITUT COCHIN   (France)

^b ACADEMIC COLLEGE OF TEL AVIV YAFFO   (Israel)

Author keywords

Autoimmune human T cells; Cancer human T cells; Glutamate; Glutamate Receptor; Normal human T cells

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; GELATINASE B; GLUTAMATE RECEPTOR; GLUTAMIC ACID; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM CHANNEL KV1.3; POTASSIUM ION; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ADAPTIVE IMMUNITY; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL ADHESION; CELL DEATH; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CYTOKINE RELEASE; DENDRITIC CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; LEUKEMIA; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; T CELL LEUKEMIA; T CELL LYMPHOMA; T LYMPHOCYTE; T-CELL LEUKEMIA CELL LINE; ANIMAL; AUTOIMMUNITY; LYMPHOMA; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AUTOIMMUNITY; GLUTAMIC ACID; HUMANS; LEUKEMIA; LYMPHOMA; NEURONS; NEUROTRANSMITTER AGENTS; RECEPTORS, GLUTAMATE; T-LYMPHOCYTES;

EID: 84925736574     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-014-1167-5     Document Type: Article

References (107)

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. 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
3. 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
4. Boettger MK, Weber K, Gajda M, Brauer R, Schaible HG (2010) Spinally applied ketamine or morphine attenuate peripheral inflammation and hyperalgesia in acute and chronic phases of experimental arthritis. Brain Behav Immun 24(3):474-485
5. 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
6. Braun S, Gaza N, Werdehausen R, Hermanns H, Bauer I, Durieux ME, Hollmann MW, Stevens MF (2010) Ketamine induces apoptosis via the mitochondrial pathway in human lymphocytes and neuronal cells. Br J Anaesth 105(3):347-354
7. 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
8. Carvalheiro H, da Silva JA, Souto-Carneiro MM (2013) Potential roles for CD8(?) T cells in rheumatoid arthritis. Autoimmun Rev 12(3):401-409
9. 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
10. 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 activationinduced cell death of human T lymphocytes. Br J Pharmacol 148(6):760-768
11. Chu Z, Hablitz JJ (2000) Quisqualate induces an inward current via mGluR activation in neocortical pyramidal neurons. Brain Res 879(1-2):88-92
12. 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
13. Collingridge GL, Singer W (1990) Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci 11(7):290-296
14. Collingridge GL, Olsen RW, Peters J, Spedding M (2009) A nomenclature for ligand-gated ion channels. Neuropharmacology 56(1):2-5
15. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65(1):1-105
16. 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
17. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51(1):7-61
18. DivinoFilho 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
19. 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. Ganor Y, Levite M (2012) Glutamate in the immune system: glutamate receptors in immune cells, potent effects, endogenous production and involvement in disease. In: Levite M (ed) Nervedriven immunity: neurotransmitters and neuropeptides in the immune system. Springer, Vienna, pp 121-161
28. 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
29. 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
30. 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
31. Garg SK, Banerjee R, Kipnis J (2008) Neuroprotective immunity: T cell-derived glutamate endows astrocytes with a neuroprotective phenotype. J Immunol 180(6):3866-3873
32. Gill SS, Pulido OM (2001) Glutamate receptors in peripheral tissues: current knowledge, future research, and implications for toxicology. Toxicol Pathol 29(2):208-223
33. 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-E89
34. Green DR, Droin N, Pinkoski M (2003) Activation-induced cell death in T cells. Immunol Rev 193:70-81
35. Guse AH (1998) Ca2? signaling in T-lymphocytes. Crit Rev Immunol 18(5):419-448
36. Hinoi E, Yoneda Y (2011) Possible involvement of glutamatergic signaling machineries in pathophysiology of rheumatoid arthritis. J Pharmacol Sci 116(3):248-256
37. 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
38. Hinoi E, Takarada T, Ueshima T, Tsuchihashi Y, Yoneda Y (2004) Glutamate signaling in peripheral tissues. Eur J Biochem 271(1):1-13
39. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108
40. 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
41. Huettner JE (2003) Kainate receptors and synaptic transmission. Prog Neurobiol 70(5):387-407
42. 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
43. 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
44. 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
45. Keinanen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPAselective glutamate receptors. Science 249(4968):556-560
46. Kew JN, Kemp JA (2005) Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology 179(1):4-29
47. Komuro H, Rakic P (1993) Modulation of neuronal migration by NMDA receptors. Science 260(5104):95-97
48. 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
49. LaCava A (2009) Lupus and T cells. Lupus 18(3):196-201
50. Lerma J (2006) Kainate receptor physiology. Curr Opin Pharmacol 6(1):89-97
51. Levite M (2008) Neurotransmitters activate T-cells and elicit crucial functions via neurotransmitter receptors. Curr Opin Pharmacol 8(4):460-471
52. Levite M (2012) Nerve-driven immunity: neurotransmitters and neuropeptides in the immune system, First edition edn edn. Springer, Berlin
53. 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
54. 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
55. Li F, Tsien JZ (2009) Memory and the NMDA receptors. N Engl J Med 361(3):302-303
56. 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
57. Lindblad SS, Mydel P, Hellvard A, Jonsson IM, Bokarewa MI (2011) The N-methyl-D-aspartic acid receptor antagonist memantine ameliorates and delays the development of arthritis by enhancing regulatory T cells. Neurosignals 20(2):61-71
58. 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
59. 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
60. 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
61. Maddur MS, Miossec P, Kaveri SV, Bayry J (2012) Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol 181(1):8-18
62. 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
63. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349(6312):760-765
64. Mayer ML (2005) Glutamate receptor ion channels. Curr Opin Neurobiol 15(3):282-288
65. Mayer ML, Westbrook GL (1987) The physiology of excitatory amino acids in the vertebrate central nervous system. Prog Neurobiol 28(3):197-276
66. Meldrum BS (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130(4S Suppl): 1007S-1015S
67. Melzer N, Hicking G, Bittner S, Bobak N, Gobel K, Herrmann AM, Wiendl H, Meuth SG (2013) Excitotoxic neuronal cell death during an oligodendrocyte-directed CD8? T cell attack in the CNS gray matter. J Neuroinflammation 10:121
68. Midgett CR, Gill A, Madden DR (2012) Domain architecture of a calcium-permeable AMPA receptor in a ligand-free conformation. Front Mol Neurosci 4:56
69. 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
70. 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
71. Miglio G, Dianzani C, Fallarini S, Fantozzi R, Lombardi G (2007) Stimulation of N-methyl-D-aspartate receptors modulates Jurkat T cell growth and adhesion to fibronectin. Biochem Biophys Res Commun 361(2):404-409
72. Miossec P, Kolls JK (2012) Targeting IL-17 and TH17 cells in chronic inflammation. Nat Rev Drug Discov 11(10):763-776
73. 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
74. 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
75. 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
76. Nedergaard M, Takano T, Hansen AJ (2002) Beyond the role of glutamate as a neurotransmitter. Nat Rev Neurosci 3(9):748-755
77. 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
78. 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
79. 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
80. 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
81. 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
82. Pacheco R, Gallart T, Lluis C, Franco R (2007) Role of glutamate on T-cell mediated immunity. J Neuroimmunol 185(1-2):9-19
83. 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
84. 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
85. Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34(1):1-26
86. Pitt D, Werner P, Raine CS (2000) Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6(1):67-70
87. Platt SR (2007) The role of glutamate in central nervous system health and disease-a review. Vet J 173(2):278-286
88. Poulopoulou C, Davaki P, Koliaraki V, Kolovou D, Markakis I, Vassilopoulos D (2005a) Reduced expression of metabotropic glutamate receptor 2mRNA in T cells of ALS patients. Ann Neurol 58(6):946-949
89. 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
90. 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 voltagegated potassium Kv1.3 channel in patients with systemic lupus erythematosus. Arthritis Rheum 58(5):1445-1450
91. Puchert M, Engele J (2014) The peculiarities of the SDF-1/CXCL12 system: in some cells, CXCR4 and CXCR7 sing solos, in others, they sing duets. Cell Tissue Res 355(2):239-253
92. 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
93. Rosenmund C, Stern-Bach Y, Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280(5369): 1596-1599
94. Rzeski W, Turski L, Ikonomidou C (2001) Glutamate antagonists limit tumor growth. Proc Natl Acad Sci USA 98(11):6372-6377
95. 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
96. Sattler R, Tymianski M (2001) Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 24(1-3):107-129
97. 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
98. Smith T, Groom A, Zhu B, Turski L (2000) Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat Med 6(1):62-66
99. 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 signalregulated kinase pathway and suppresses cancer growth. Proc Natl Acad Sci USA 102(43):15605-15610
100. 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
101. 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
102. Tanabe Y,MasuM,IshiiT,Shigemoto R, Nakanishi S (1992)Afamily of metabotropic glutamate receptors. Neuron 8(1):169-179
103. 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 phytohemagglutininstimulated lymphocytes. Exp Hematol 24(2):277-284
104. Weyand CM, Bryl E, Goronzy JJ (2000) The role of T cells in rheumatoid arthritis. Arch Immunol Ther Exp (Warsz) 48(5):429-435
105. Wollmuth LP, Sobolevsky AI (2004) Structure and gating of the glutamate receptor ion channel. Trends Neurosci 27(6):321-328
106. Zhou L, Chong MM, Littman DR (2009) Plasticity of CD4? T cell lineage differentiation. Immunity 30(5):646-655
107. Zlotnik A, Tsesis S, Gruenbaum BF, Ohayon S, Gruenbaum SE, Boyko M, Sheiner E, Brotfain E, Shapira Y, Teichberg VI (2012) Relationship between glutamate, GOT and GPT levels in maternal and fetal blood: a potential mechanism for fetal neuroprotection. Early Hum Dev 88(9):773-778