Astrocyte and Microglial Control of Glutamatergic Signalling: A Primer on Understanding the Disruptive Role of Chronic Stress

Journal of Neuroendocrinology

Volumn 27, Issue 6, 2015, Pages 498-506

  Mayhew, J ^a,b,c   Beart, P M ^d   Walker, F R ^a,b,c  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

^c HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Astrocyte; Chronic stress; Depression; Glutamate; Microglia; Stress

Indexed keywords

AMPA RECEPTOR; CORTICOSTERONE; GLUCOCORTICOID; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ACUTE STRESS; ASTROCYTE; BRAIN NERVE CELL; CELL INTERACTION; CELLULAR STRESS RESPONSE; CHRONIC STRESS; GLUTAMATERGIC SYNAPSE; HIPPOCAMPUS; HUMAN; MICROGLIA; NEUROBIOLOGY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHRONIC DISEASE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; ASTROCYTES; CHRONIC DISEASE; GLUTAMIC ACID; HUMANS; MICROGLIA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84929741420     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12273     Document Type: Review

References (113)

1. Siegrist J. Chronic psychosocial stress at work and risk of depression: evidence from prospective studies. Eur Arch Psychiatry Clin Neurosci 2008; 258(Suppl 5): 115-119.
2. Bagley J, Moghaddam B. Temporal dynamics of glutamate efflux in the prefrontal cortex and in the hippocampus following repeated stress: effects of pretreatment with saline or diazepam. Neuroscience 1997; 77: 65-73.
3. Moghaddam B. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 1993; 60: 1650-1657.
4. Moghaddam B, Bolinao ML, Stein-Behrens B, Sapolsky R. Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res 1994; 655: 251-254.
5. Venero C, Borrell J. Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. Eur J Neurosci 1999; 11: 2465-2473.
6. Abraham I, Juhasz G, Kekesi KA, Kovacs KJ. Effect of intrahippocampal dexamethasone on the levels of amino acid transmitters and neuronal excitability. Brain Res 1996; 733: 56-63.
7. Hascup ER, Hascup KN, Stephens M, Pomerleau F, Huettl P, Gratton A, Gerhardt GA. Rapid microelectrode measurements and the origin and regulation of extracellular glutamate in rat prefrontal cortex. J Neurochem 2010; 115: 1608-1620.
8. Wang CC, Wang SJ. Modulation of presynaptic glucocorticoid receptors on glutamate release from rat hippocampal nerve terminals. Synapse 2009; 63: 745-751.
9. Yuen EY, Wei J, Liu W, Zhong P, Li X, Yan Z. Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron 2012; 73: 962-977.
10. Bartanusz V, Aubry JM, Pagliusi S, Jezova D, Baffi J, Kiss JZ. Stress-induced changes in messenger RNA levels of N-methyl-d-aspartate and AMPA receptor subunits in selected regions of the rat hippocampus and hypothalamus. Neuroscience 1995; 66: 247-252.
11. 2+-permeable AMPA receptors to facilitate long-term potentiation in the hippocampus. Brain 2013; 136: 3753-3765.
12. McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999; 22: 105-122.
13. Joels M, Karst H, Krugers HJ, Lucassen PJ. Chronic stress: implications for neuronal morphology, function and neurogenesis. Front Neuroendocrinol 2007; 28: 72-96.
14. McEwen BS, Eiland L, Hunter RG, Miller MM. Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 2012; 62: 3-12.
15. Liu RJ, Aghajanian GK. Stress blunts serotonin- and hypocretin-evoked EPSCs in prefrontal cortex: role of corticosterone-mediated apical dendritic atrophy. Proc Natl Acad Sci U S A. 2008; 105: 359-64.
16. Karst H, Berger S, Turiault M, Tronche F, Schutz G, Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA 2005; 102: 19204-19207.
17. Karst H, Joels M. Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J Neurophysiol 2005; 94: 3479-3486.
18. Chaouloff F, Hemar A, Manzoni O. Acute stress facilitates hippocampal CA1 metabotropic glutamate receptor-dependent long-term depression. J Neurosci 2007; 27: 7130-7135.
19. Foy MR, Stanton ME, Levine S, Thompson RF. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol 1987; 48: 138-149.
20. Alfarez DN, Joels M, Krugers HJ. Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci 2003; 17: 1928-1934.
21. Pavlides C, Nivon LG, McEwen BS. Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 2002; 12: 245-257.
22. Shors TJ, Seib TB, Levine S, Thompson RF. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 1989; 244: 224-226.
23. Xu L, Anwyl R, Rowan MJ. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 1997; 387: 497-500.
24. Wong TP, Howland JG, Robillard JM, Ge Y, Yu W, Titterness AK, Brebner K, Liu L, Weinberg J, Christie BR, Phillips AG, Wang YT. Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment. Proc Natl Acad Sci USA 2007; 104: 11471-11476.
25. McNally L, Bhagwagar Z, Hannestad J. Inflammation, glutamate, and glia in depression: a literature review. CNS Spectr 2008; 13: 501-510.
26. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008; 9: 46-56.
27. Shigeri Y, Seal RP, Shimamoto K. Molecular pharmacology of glutamate transporters, EAATs and VGLUTs. Brain Res Brain Res Rev 2004; 45: 250-265.
28. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996; 16: 675-686.
29. Dani JW, Chernjavsky A, Smith SJ. Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 1992; 8: 429-440.
30. Bowser DN, Khakh BS. Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J Gen Physiol 2007; 129: 485-491.
31. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG. Glutamate-mediated astrocyte-neuron signalling. Nature 1994; 369: 744-747.
32. 2+ waves trigger responses in microglial cells in brain slices. FASEB J 2002; 16: 255-257.
33. Verderio C, Matteoli M. ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN-gamma. J Immunol 2001; 166: 6383-6391.
34. Montana V, Ni Y, Sunjara V, Hua X, Parpura V. Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 2004; 24: 2633-2642.
35. 2+ waves transmit brain-damage signals to microglia. Dev Cell 2012; 22: 1138-1148.
36. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 2004; 7: 613-620.
37. Araque A, Li N, Doyle RT, Haydon PG. SNARE protein-dependent glutamate release from astrocytes. J Neurosci 2000; 20: 666-673.
38. Zhang Q, Pangrsic T, Kreft M, Krzan M, Li N, Sul JY, Halassa M, Van Bockstaele E, Zorec R, Haydon PG. Fusion-related release of glutamate from astrocytes. J Biol Chem 2004; 279: 12724-12733.
39. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, Matute C, Tonello F, Gundersen V, Volterra A. Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 2007; 10: 331-339.
40. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 2004; 43: 729-743.
41. Angulo MC, Kozlov AS, Charpak S, Audinat E. Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci 2004; 24: 6920-6927.
42. Fiacco TA, McCarthy KD. Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J Neurosci 2004; 24: 722-732.
43. Perea G, Araque A. Astrocytes potentiate transmitter release at single hippocampal synapses. Science 2007; 317: 1083-1086.
44. Perea G, Araque A. Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 2005; 25: 2192-2203.
45. Navarrete M, Araque A. Endocannabinoids mediate neuron-astrocyte communication. Neuron 2008; 57: 883-893.
46. Popoli M, Yan Z, McEwen BS, Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 2012; 13: 22-37.
47. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 2009; 29: 3974-3980.
48. Tremblay ME, Lowery RL, Majewska AK. Microglial interactions with synapses are modulated by visual experience. PLoS Biol 2010; 8: e1000527.
49. Chretien F, Le Pavec G, Vallat-Decouvelaere AV, Delisle MB, Uro-Coste E, Ironside JW, Gambetti P, Parchi P, Creminon C, Dormont D, Mikol J, Gray F, Gras G. Expression of excitatory amino acid transporter-1 (EAAT-1) in brain macrophages and microglia of patients with prion diseases. J Neuropathol Exp Neurol 2004; 63: 1058-1071.
50. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR 3rd, Lafaille JJ, Hempstead BL, Littman DR, Gan WB. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 2013; 155: 1596-1609.
51. Choi DW, Rothman SM. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 1990; 13: 171-182.
52. Tomasello E, Desmoulins PO, Chemin K, Guia S, Cremer H, Ortaldo J, Love P, Kaiserlian D, Vivier E. Combined natural killer cell and dendritic cell functional deficiency in KARAP/DAP12 loss-of-function mutant mice. Immunity 2000; 13: 355-364.
53. Roumier A, Pascual O, Bechade C, Wakselman S, Poncer JC, Real E, Triller A, Bessis A. Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function. PLoS ONE 2008; 3: e2595.
54. Roumier A, Bechade C, Poncer JC, Smalla KH, Tomasello E, Vivier E, Gundelfinger ED, Triller A, Bessis A. Impaired synaptic function in the microglial KARAP/DAP12-deficient mouse. J Neurosci 2004; 24: 11421-11428.
55. Murugan M, Ling EA, Kaur C. Glutamate receptors in microglia. CNS Neurol Disord Drug Targets 2013; 12: 773-784.
56. Fontainhas AM, Wang M, Liang KJ, Chen S, Mettu P, Damani M, Fariss RN, Li W, Wong WT. Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS ONE 2011; 6: e15973.
57. Eyo UB, Peng J, Swiatkowski P, Mukherjee A, Bispo A, Wu LJ. Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J Neurosci 2014; 34: 10528-10540.
58. Wollmer MA, Lucius R, Wilms H, Held-Feindt J, Sievers J, Mentlein R. ATP and adenosine induce ramification of microglia in vitro. J Neuroimmunol 2001; 115: 19-27.
59. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 2001; 21: 1975-1982.
60. Ohsawa K, Irino Y, Nakamura Y, Akazawa C, Inoue K, Kohsaka S. Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 2007; 55: 604-616.
61. Ohsawa K, Irino Y, Sanagi T, Nakamura Y, Suzuki E, Inoue K, Kohsaka S. P2Y12 receptor-mediated integrin-beta1 activation regulates microglial process extension induced by ATP. Glia 2010; 58: 790-801.
62. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 2005; 8: 752-758.
63. Beschorner R, Dietz K, Schauer N, Mittelbronn M, Schluesener HJ, Trautmann K, Meyermann R, Simon P. Expression of EAAT1 reflects a possible neuroprotective function of reactive astrocytes and activated microglia following human traumatic brain injury. Histol Histopathol 2007; 22: 515-526.
64. Beschorner R, Simon P, Schauer N, Mittelbronn M, Schluesener HJ, Trautmann K, Dietz K, Meyermann R. Reactive astrocytes and activated microglial cells express EAAT1, but not EAAT2, reflecting a neuroprotective potential following ischaemia. Histopathology 2007; 50: 897-910.
65. Dai SS, Zhou YG, Li W, An JH, Li P, Yang N, Chen XY, Xiong RP, Liu P, Zhao Y, Shen HY, Zhu PF, Chen JF. Local glutamate level dictates adenosine A2A receptor regulation of neuroinflammation and traumatic brain injury. J Neurosci 2010; 30: 5802-5810.
66. Chretien F, Vallat-Decouvelaere AV, Bossuet C, Rimaniol AC, Le Grand R, Le Pavec G, Creminon C, Dormont D, Gray F, Gras G. Expression of excitatory amino acid transporter-2 (EAAT-2) and glutamine synthetase (GS) in brain macrophages and microglia of SIVmac251-infected macaques. Neuropathol Appl Neurobiol 2002; 28: 410-417.
67. Vallat-Decouvelaere AV, Chretien F, Gras G, Le Pavec G, Dormont D, Gray F. Expression of excitatory amino acid transporter-1 in brain macrophages and microglia of HIV-infected patients. A neuroprotective role for activated microglia? J Neuropathol Exp Neurol 2003; 62: 475-485.
68. Brown DR, Mohn CM. Astrocytic glutamate uptake and prion protein expression. Glia 1999; 25: 282-292.
69. Wang Z, Pekarskaya O, Bencheikh M, Chao W, Gelbard HA, Ghorpade A, Rothstein JD, Volsky DJ. Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 2003; 312: 60-73.
70. Vesce S, Bezzi P, Rossi D, Meldolesi J, Volterra A. HIV-1 gp120 glycoprotein affects the astrocyte control of extracellular glutamate by both inhibiting the uptake and stimulating the release of the amino acid. FEBS Lett 1997; 411: 107-109.
71. Nakajima K, Tohyama Y, Kohsaka S, Kurihara T. Ability of rat microglia to uptake extracellular glutamate. Neurosci Lett 2001; 307: 171-174.
72. Persson M, Brantefjord M, Hansson E, Ronnback L. Lipopolysaccharide increases microglial GLT-1 expression and glutamate uptake capacity in vitro by a mechanism dependent on TNF-alpha. Glia 2005; 51: 111-120.
73. Jacobsson J, Persson M, Hansson E, Ronnback L. Corticosterone inhibits expression of the microglial glutamate transporter GLT-1 in vitro. Neuroscience 2006; 139: 475-483.
74. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci USA 2012; 109: E197-E205.
75. Gosselin RD, Gibney S, O'Malley D, Dinan TG, Cryan JF. Region specific decrease in glial fibrillary acidic protein immunoreactivity in the brain of a rat model of depression. Neuroscience 2009; 159: 915-925.
76. Tynan RJ, Beynon SB, Hinwood M, Johnson SJ, Nilsson M, Woods JJ, Walker FR. Chronic stress-induced disruption of the astrocyte network is driven by structural atrophy and not loss of astrocytes. Acta Neuropathol 2013; 126: 75-91.
77. Banasr M, Chowdhury GM, Terwilliger R, Newton SS, Duman RS, Behar KL, Sanacora G. Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol Psychiatry 2010; 15: 501-511.
78. Czeh B, Simon M, Schmelting B, Hiemke C, Fuchs E. Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology 2006; 31: 1616-1626.
79. Webster MJ, Knable MB, Johnston-Wilson N, Nagata K, Inagaki M, Yolken RH. Immunohistochemical localization of phosphorylated glial fibrillary acidic protein in the prefrontal cortex and hippocampus from patients with schizophrenia, bipolar disorder, and depression. Brain Behav Immun 2001; 15: 388-400.
80. Rajkowska G, Miguel-Hidalgo JJ, Wei J, Dilley G, Pittman SD, Meltzer HY, Overholser JC, Roth BL, Stockmeier CA. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999; 45: 1085-1098.
81. Ye Y, Wang G, Wang H, Wang X. Brain-derived neurotrophic factor (BDNF) infusion restored astrocytic plasticity in the hippocampus of a rat model of depression. Neurosci Lett 2011; 503: 15-19.
82. Domin H, Szewczyk B, Wozniak M, Wawrzak-Wlecial A, Smialowska M. Antidepressant-like effect of the mGluR5 antagonist MTEP in an astroglial degeneration model of depression. Behav Brain Res 2014; 273: 23-33.
83. Banasr M, Duman RS. Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol Psychiatry 2008; 64: 863-870.
84. Sullivan SM, Lee A, Bjorkman ST, Miller SM, Sullivan RK, Poronnik P, Colditz PB, Pow DV. Cytoskeletal anchoring of GLAST determines susceptibility to brain damage: an identified role for GFAP. J Biol Chem 2007; 282: 29414-29423.
85. Lau CL, Beart PM, O'Shea RD. Transportable and non-transportable inhibitors of l-glutamate uptake produce astrocytic stellation and increase EAAT2 cell surface expression. Neurochem Res 2010; 35: 735-742.
86. Hughes EG, Maguire JL, McMinn MT, Scholz RE, Sutherland ML. Loss of glial fibrillary acidic protein results in decreased glutamate transport and inhibition of PKA-induced EAAT2 cell surface trafficking. Brain Res Mol Brain Res 2004; 124: 114-123.
87. Kong H, Zeng XN, Fan Y, Yuan ST, Ge S, Xie WP, Wang H, Hu G. Aquaporin-4 knockout exacerbates corticosterone-induced depression by inhibiting astrocyte function and hippocampal neurogenesis. CNS Neurosci Ther 2014; 20: 391-402.
88. Zschocke J, Bayatti N, Clement AM, Witan H, Figiel M, Engele J, Behl C. Differential promotion of glutamate transporter expression and function by glucocorticoids in astrocytes from various brain regions. J Biol Chem 2005; 280: 34924-34932.
89. Gilad GM, Gilad VH, Wyatt RJ, Tizabi Y. Region-selective stress-induced increase of glutamate uptake and release in rat forebrain. Brain Res 1990; 525: 335-338.
90. Yang CH, Huang CC, Hsu KS. Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake. J Neurosci 2005; 25: 4288-4293.
91. Zink M, Vollmayr B, Gebicke-Haerter PJ, Henn FA. Reduced expression of glutamate transporters vGluT1, EAAT2 and EAAT4 in learned helpless rats, an animal model of depression. Neuropharmacology 2010; 58: 465-473.
92. Olivenza R, Moro MA, Lizasoain I, Lorenzo P, Fernandez AP, Rodrigo J, Bosca L, Leza JC. Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex. J Neurochem 2000; 74: 785-791.
93. Fontella FU, Vendite DA, Tabajara AS, Porciuncula LO, da Silva Torres IL, Jardim FM, Martini L, Souza DO, Netto CA, Dalmaz C. Repeated restraint stress alters hippocampal glutamate uptake and release in the rat. Neurochem Res 2004; 29: 1703-1709.
94. Reagan LP, Rosell DR, Wood GE, Spedding M, Munoz C, Rothstein J, McEwen BS. Chronic restraint stress up-regulates GLT-1 mRNA and protein expression in the rat hippocampus: reversal by tianeptine. Proc Natl Acad Sci USA 2004; 101: 2179-2184.
95. Bechtholt-Gompf AJ, Walther HV, Adams MA, Carlezon WA Jr, Ongur D, Cohen BM. Blockade of astrocytic glutamate uptake in rats induces signs of anhedonia and impaired spatial memory. Neuropsychopharmacology 2010; 35: 2049-2059.
96. John CS, Smith KL, Van't Veer A, Gompf HS, Carlezon WA Jr, Cohen BM, Ongur D, Bechtholt-Gompf AJ Blockade of astrocytic glutamate uptake in the prefrontal cortex induces anhedonia. Neuropsychopharmacology 2012; 37: 2467-2475.
97. Gourley SL, Espitia JW, Sanacora G, Taylor JR. Antidepressant-like properties of oral riluzole and utility of incentive disengagement models of depression in mice. Psychopharmacology 2012; 219: 805-814.
98. Rodrigues RJ, Almeida T, Richardson PJ, Oliveira CR, Cunha RA. Dual presynaptic control by ATP of glutamate release via facilitatory P2X1, P2X2/3, and P2X3 and inhibitory P2Y1, P2Y2, and/or P2Y4 receptors in the rat hippocampus. J Neurosci 2005; 25: 6286-6295.
99. Cao X, Li LP, Wang Q, Wu Q, Hu HH, Zhang M, Fang YY, Zhang J, Li SJ, Xiong WC, Yan HC, Gao YB, Liu JH, Li XW, Sun LR, Zeng YN, Zhu XH, Gao TM. Astrocyte-derived ATP modulates depressive-like behaviors. Nat Med 2013; 19: 773-777.
100. Ando RD, Sperlagh B. The role of glutamate release mediated by extrasynaptic P2X7 receptors in animal models of neuropathic pain. Brain Res Bull 2013; 93: 80-85.
101. Cervetto C, Alloisio S, Frattaroli D, Mazzotta MC, Milanese M, Gavazzo P, Passalacqua M, Nobile M, Maura G, Marcoli M. The P2X7 receptor as a route for non-exocytotic glutamate release: dependence on the carboxyl tail. J Neurochem 2013; 124: 821-831.
102. Marcoli M, Cervetto C, Paluzzi P, Guarnieri S, Alloisio S, Thellung S, Nobile M, Maura G. P2X7 pre-synaptic receptors in adult rat cerebrocortical nerve terminals: a role in ATP-induced glutamate release. J Neurochem 2008; 105: 2330-2342.
103. Marin-Garcia P, Sanchez-Nogueiro J, Gomez-Villafuertes R, Leon D, Miras-Portugal MT. Synaptic terminals from mice midbrain exhibit functional P2X7 receptor. Neuroscience 2008; 151: 361-373.
104. Sperlagh B, Kofalvi A, Deuchars J, Atkinson L, Milligan CJ, Buckley NJ, Vizi ES. Involvement of P2X7 receptors in the regulation of neurotransmitter release in the rat hippocampus. J Neurochem 2002; 81: 1196-1211.
105. Sanacora G, Treccani G, Popoli M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 2012; 62: 63-77.
106. Sanacora G, Zarate CA, Krystal JH, Manji HK. Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 2008; 7: 426-437.
107. Miguel-Hidalgo JJ, Baucom C, Dilley G, Overholser JC, Meltzer HY, Stockmeier CA, Rajkowska G. Glial fibrillary acidic protein immunoreactivity in the prefrontal cortex distinguishes younger from older adults in major depressive disorder. Biol Psychiatry 2000; 48: 861-873.
108. Bowley MP, Drevets WC, Ongur D, Price JL Low glial numbers in the amygdala in major depressive disorder. Biol Psychiatry 2002; 52: 404-412.
109. Si X, Miguel-Hidalgo JJ, O'Dwyer G, Stockmeier CA, Rajkowska G. Age-dependent reductions in the level of glial fibrillary acidic protein in the prefrontal cortex in major depression. Neuropsychopharmacology 2004; 29: 2088-2096.
110. Davis S, Thomas A, Perry R, Oakley A, Kalaria RN, O'Brien JT. Glial fibrillary acidic protein in late life major depressive disorder: an immunocytochemical study. J Neurol Neurosurg Psychiatry 2002; 73: 556-560.
111. Cotter D, Mackay D, Landau S, Kerwin R, Everall I. Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 2001; 58: 545-553.
112. Cotter DR, Pariante CM, Everall IP. Glial cell abnormalities in major psychiatric disorders: the evidence and implications. Brain Res Bull 2001; 55: 585-595.
113. Fatemi SH, Laurence JA, Araghi-Niknam M, Stary JM, Schulz SC, Lee S, Gottesman II. Glial fibrillary acidic protein is reduced in cerebellum of subjects with major depression, but not schizophrenia. Schizophr Res 2004; 69: 317-323.