Regulated exocytosis in astrocytic signal integration

Neurochemistry International

Volumn 57, Issue 4, 2010, Pages 451-459

  Parpura, Vladimir ^a   Baker, Brandi J ^a   Jeras, Matjaž ^b,c,d   Zorec, Robert ^b,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c Celica Biomedical Sciences Center   (Slovenia)

^d BLOOD TRANSFUSION CENTRE OF SLOVENIA   (Slovenia)

Author keywords

Astrocytes; ATP; Atrial natriuretic peptide; Brain derived neurotrophic factor; D Serine; Exocytosis; Glutamate; Integrator

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; ATRIAL NATRIURETIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; DEXTRO SERINE; GLUTAMIC ACID; NUCLEOTIDE; PEPTIDE;

ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CELL COMMUNICATION; EXOCYTOSIS; HUMAN; INTRACELLULAR TRANSPORT; MEMBRANE FUSION; NEUROCHEMISTRY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; AMINO ACIDS; ANIMALS; ASTROCYTES; CELL MEMBRANE; EXOCYTOSIS; HUMANS; NEUROPEPTIDES; SIGNAL TRANSDUCTION;

EID: 77956227264     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2010.02.007     Document Type: Article

References (118)

1. Anderson C.M., Nedergaard M. Astrocyte-mediated control of cerebral microcirculation. Trends Neurosci. 2003, 26:340-344. author reply 344-345.
2. Anlauf E., Derouiche A. Astrocytic exocytosis vesicles and glutamate: a high-resolution immunofluorescence study. Glia 2005, 49:96-106.
3. Araque A., Sanzgiri R.P., Parpura V., Haydon P.G. Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J. Neurosci. 1998, 18:6822-6829.
4. Araque A., Parpura V., Sanzgiri R.P., Haydon P.G. Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 1998, 10:2129-2142.
5. Araque A., Parpura V., Sanzgiri R.P., Haydon P.G. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 1999, 22:208-215.
6. Araque A., Li N., Doyle R.T., Haydon P.G. SNARE protein-dependent glutamate release from astrocytes. J. Neurosci. 2000, 20:666-673.
7. Baertschi A.J., Monnier D., Schmidt U., Levitan E.S., Fakan S., Roatti A. Acid prohormone sequence determines size, shape, and docking of secretory vesicles in atrial myocytes. Circ. Res. 2001, 89:E23-E29.
8. Baker B.J., Akhtar L.N., Benveniste E.N. SOCS1 and SOCS3 in the control of CNS immunity. Trends Immunol. 2009, 30:392-400.
9. Bal-Price A., Moneer Z., Brown G.C. Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia 2002, 40:312-323.
10. Banisadr G., Fontanges P., Haour F., Kitabgi P., Rostene W., Melik Parsadaniantz S. Neuroanatomical distribution of CXCR4 in adult rat brain and its localization in cholinergic and dopaminergic neurons. Eur. J. Neurosci. 2002, 16:1661-1671.
11. Beattie E.C., Stellwagen D., Morishita W., Bresnahan J.C., Ha B.K., Von Zastrow M., Beattie M.S., Malenka R.C. Control of synaptic strength by glial TNFalpha. Science 2002, 295:2282-2285.
12. Beck A., Nieden R.Z., Schneider H.P., Deitmer J.W. Calcium release from intracellular stores in rodent astrocytes and neurons in situ. Cell Calcium 2004, 35:47-58.
13. Bergami M., Santi S., Formaggio E., Cagnoli C., Verderio C., Blum R., Berninger B., Matteoli M., Canossa M. Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J. Cell Biol. 2008, 183:213-221.
14. Bergersen L.H., Gundersen V. Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 2009, 158:260-265.
15. Bezzi P., Gundersen V., Galbete J.L., 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.
16. Bezzi P., Carmignoto G., Pasti L., Vesce S., Rossi D., Rizzini B.L., Pozzan T., Volterra A. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 1998, 391:281-285.
17. Bezzi P., Domercq M., Brambilla L., Galli R., Schols D., De Clercq E., Vescovi A., Bagetta G., Kollias G., Meldolesi J., Volterra A. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 2001, 4:702-710.
18. Bianco F., Pravettoni E., Colombo A., Schenk U., Moller T., Matteoli M., Verderio C. Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J. Immunol. 2005, 174:7268-7277.
19. Bowser D.N., Khakh B.S. Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:4212-4217.
20. Calegari F., Coco S., Taverna E., Bassetti M., Verderio C., Corradi N., Matteoli M., Rosa P. A regulated secretory pathway in cultured hippocampal astrocytes. J. Biol. Chem. 1999, 274:22539-22547.
21. Cali C., Marchaland J., Regazzi R., Bezzi P. SDF 1-alpha (CXCL12) triggers glutamate exocytosis from astrocytes on a millisecond time scale: imaging analysis at the single-vesicle level with TIRF microscopy. J. Neuroimmunol. 2008, 198:82-91.
22. Chen X., Wang L., Zhou Y., Zheng L.H., Zhou Z. " Kiss-and-run" glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J. Neurosci. 2005, 25:9236-9243.
23. Coco S., Calegari F., Pravettoni E., Pozzi D., Taverna E., Rosa P., Matteoli M., Verderio C. Storage and release of ATP from astrocytes in culture. J. Biol. Chem. 2003, 278:1354-1362.
24. Constantinescu C.S., Tani M., Ransohoff R.M., Wysocka M., Hilliard B., Fujioka T., Murphy S., Tighe P.J., Das Sarma J., Trinchieri G., Rostami A. Astrocytes as antigen-presenting cells: expression of IL-12/IL-23. J. Neurochem. 2005, 95:331-340.
25. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., Kang J., Naus C.C., Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:15735-15740.
26. Crippa D., Schenk U., Francolini M., Rosa P., Verderio C., Zonta M., Pozzan T., Matteoli M., Carmignoto G. Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis. J. Physiol. 2006, 570:567-582.
27. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65:1-105.
28. Dannies P.S. Protein hormone storage in secretory granules: mechanisms for concentration and sorting. Endocr. Rev. 1999, 20:3-21.
29. Davalos D., Grutzendler J., Yang G., Kim J.V., Zuo Y., Jung S., Littman D.R., Dustin M.L., Gan W.B. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 2005, 8:752-758.
30. Del Castillo J., Katz B. Quantal components of the end-plate potential. J. Physiol. 1954, 124:560-573.
31. Domercq M., Brambilla L., Pilati E., Marchaland J., Volterra A., Bezzi P. P2Y1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-alpha and prostaglandins. J. Biol. Chem. 2006, 281:30684-30696.
32. Duan S., Anderson C.M., Keung E.C., Chen Y., Chen Y., Swanson R.A. P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J. Neurosci. 2003, 23:1320-1328.
33. Fields R.D., Burnstock G. Purinergic signalling in neuron-glia interactions. Nat. Rev. Neurosci. 2006, 7:423-436.
34. Fontana A., Fierz W., Wekerle H. Astrocytes present myelin basic protein to encephalitogenic T-cell lines. Nature 1984, 307:273-276.
35. Fremeau R.T., Burman J., Qureshi T., Tran C.H., Proctor J., Johnson J., Zhang H., Sulzer D., Copenhagen D.R., Storm-Mathisen J., Reimer R.J., Chaudhry F.A., Edwards R.H. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14488-14493.
36. Girvin A.M., Gordon K.B., Welsh C.J., Clipstone N.A., Miller S.D. Differential abilities of central nervous system resident endothelial cells and astrocytes to serve as inducible antigen-presenting cells. Blood 2002, 99:3692-3701.
37. Golovina V.A. Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J. Physiol. 2005, 564:737-749.
38. Gomes I., Grushko J.S., Golebiewska U., Hoogendoorn S., Gupta A., Heimann A.S., Ferro E.S., Scarlata S., Fricker L.D., Devi L.A. Novel endogenous peptide agonists of cannabinoid receptors. FASEB J. 2009, April 20 On-Line.
39. Grimaldi M., Maratos M., Verma A. Transient receptor potential channel activation causes a novel form of [Ca2+]I oscillations and is not involved in capacitative Ca2+ entry in glial cells. J. Neurosci. 2003, 23:4737-4745.
40. Halassa M.M., Fellin T., Haydon P.G. Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology 2009, 57:343-346.
41. Hertz L., Gibbs M.E. What learning in day-old chickens can teach a neurochemist: focus on astrocyte metabolism. J. Neurochem. 2009, 109(Suppl 1):10-16.
42. Hertz L., Dringen R., Schousboe A., Robinson S.R. Astrocytes: glutamate producers for neurons. J. Neurosci. Res. 1999, 57:417-428.
43. Hua X., Malarkey E.B., Sunjara V., Rosenwald S.E., Li W.H., Parpura V. Ca2+-dependent glutamate release involves two classes of endoplasmic reticulum Ca2+ stores in astrocytes. J. Neurosci. Res. 2004, 76:86-97.
44. Iglesias R., Dahl G., Qiu F., Spray D.C., Scemes E. Pannexin 1: the molecular substrate of astrocyte " hemichannels" J. Neurosci. 2009, 29:7092-7097.
45. Innocenti B., Parpura V., Haydon P.G. Imaging extracellular waves of glutamate during calcium signaling in cultured astrocytes. J. Neurosci. 2000, 20:1800-1808.
46. Jeremic A., Jeftinija K., Stevanovic J., Glavaski A., Jeftinija S. ATP stimulates calcium-dependent glutamate release from cultured astrocytes. J. Neurochem. 2001, 77:664-675.
47. Kang N., Xu J., Xu Q., Nedergaard M., Kang J. Astrocytic glutamate release-induced transient depolarization and epileptiform discharges in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 2005, 94:4121-4130.
48. Koizumi S., Fujishita K., Inoue K. Regulation of cell-to-cell communication mediated by astrocytic ATP in the CNS. Purinergic Signal 2005, 1:211-217.
49. Kreft M., Stenovec M., Rupnik M., Grilc S., Krzan M., Potokar M., Pangrsic T., Haydon P.G., Zorec R. Properties of Ca2+-dependent exocytosis in cultured astrocytes. Glia 2004, 46:437-445.
50. Krzan M., Stenovec M., Kreft M., Pangrsic T., Grilc S., Haydon P.G., Zorec R. Calcium-dependent exocytosis of atrial natriuretic peptide from astrocytes. J. Neurosci. 2003, 23:1580-1583.
51. Leterrier C., Bonnard D., Carrel D., Rossier J., Lenkei Z. Constitutive endocytic cycle of the CB1 cannabinoid receptor. J. Biol. Chem. 2004, 279:36013-36021.
52. Maienschein V., Marxen M., Volknandt W., Zimmermann H. A plethora of presynaptic proteins associated with ATP-storing organelles in cultured astrocytes. Glia 1999, 26:233-244.
53. Malarkey E.B., Ni Y., Parpura V. Ca2+ entry through TRPC1 channels contributes to intracellular Ca2+ dynamics and consequent glutamate release from rat astrocytes. Glia 2008.
54. Marchaland J., Cali C., Voglmaier S.M., Li H., Regazzi R., Edwards R.H., Bezzi P. Fast subplasma membrane Ca2+ transients control exo-endocytosis of synaptic-like microvesicles in astrocytes. J. Neurosci. 2008, 28:9122-9132.
55. Martineau M., Galli T., Baux G., Mothet J.P. Confocal imaging and tracking of the exocytotic routes for d-serine-mediated gliotransmission. Glia 2008, 56:1271-1284.
56. McDonald N.A., Henstridge C.M., Connolly C.N., Irving A.J. An essential role for constitutive endocytosis, but not activity, in the axonal targeting of the CB1 cannabinoid receptor. Mol. Pharmacol. 2007, 71:976-984.
57. McKenzie J.C., Juan Y.W., Thomas C.R., Berman N.E., Klein R.M. Atrial natriuretic peptide-like immunoreactivity in neurons and astrocytes of human cerebellum and inferior olivary complex. J. Histochem. Cytochem. 2001, 49:1453-1467.
58. Mennerick S., Zorumski C.F. Glial contributions to excitatory neurotransmission in cultured hippocampal cells. Nature 1994, 368:59-62.
59. Miyata H., Silverman H.S., Sollott S.J., Lakatta E.G., Stern M.D., Hansford R.G. Measurement of mitochondrial free Ca2+ concentration in living single rat cardiac myocytes. Am. J. Physiol. 1991, 261:H1123-H1134.
60. Montana V., Ni Y., Sunjara V., Hua X., Parpura V. Vesicular glutamate transporter-dependent glutamate release from astrocytes. J. Neurosci. 2004, 24:2633-2642.
61. Montana V., Malarkey E.B., Verderio C., Matteoli M., Parpura V. Vesicular transmitter release from astrocytes. Glia 2006, 54:700-715.
62. Montgomery D.L. Astrocytes: form, functions, and roles in disease. Vet. Pathol. 1994, 31:145-167.
63. Mothet J.P., Pollegioni L., Ouanounou G., Martineau M., Fossier P., Baux G. Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter d-serine. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5606-5611.
64. Nakamura Y., Iga K., Shibata T., Shudo M., Kataoka K. Glial plasmalemmal vesicles: a subcellular fraction from rat hippocampal homogenate distinct from synaptosomes. Glia 1993, 9:48-56.
65. Navarrete M., Araque A. Endocannabinoids mediate neuron-astrocyte communication. Neuron 2008, 57:883-893.
66. Nedergaard M., Ransom B., Goldman S.A. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 2003, 26:523-530.
67. Newman E.A. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 2003, 26:536-542.
68. Ni Y., Parpura V. Dual regulation of Ca2+-dependent glutamate release from astrocytes: vesicular glutamate transporters and cytosolic glutamate levels. Glia 2009, 57:1296-1305.
69. Ni Y., Malarkey E.B., Parpura V. Vesicular release of glutamate mediates bidirectional signaling between astrocytes and neurons. J. Neurochem. 2007, 103:1273-1284.
70. Oliet S.H., Mothet J.P. Regulation of N-methyl-d-aspartate receptors by astrocytic d-serine. Neuroscience 2009, 158:275-283.
71. Osborne K.D., Lee W., Malarkey E.B., Irving A.J., Parpura V. Dynamic imaging of cannabinoid receptor 1 vesicular trafficking in cultured astrocytes. ASN Neuro. 2009.
72. Paco S., Margeli M.A., Olkkonen V.M., Imai A., Blasi J., Fischer-Colbrie R., Aguado F. Regulation of exocytotic protein expression and Ca2+-dependent peptide secretion in astrocytes. J. Neurochem. 2009, 110:143-156.
73. Pangrsic T., Potokar M., Stenovec M., Kreft M., Fabbretti E., Nistri A., Pryazhnikov E., Khiroug L., Giniatullin R., Zorec R. Exocytotic release of ATP from cultured astrocytes. J. Biol. Chem. 2007, 282:28749-28758.
74. Parpura V., Haydon P.G. Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8629-8634.
75. Parpura V., Fang Y., Basarsky T., Jahn R., Haydon P.G. Expression of synaptobrevin II, cellubrevin and syntaxin but not SNAP-25 in cultured astrocytes. FEBS Lett. 1995, 377:489-492.
76. Parpura V., Basarsky T.A., Liu F., Jeftinija K., Jeftinija S., Haydon P.G. Glutamate-mediated astrocyte-neuron signalling. Nature 1994, 369:744-747.
77. 2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat. Neurosci. 2001, 4:803-812.
78. Pasantes Morales H., Schousboe A. Volume regulation in astrocytes: a role for taurine as an osmoeffector. J. Neurosci. Res. 1988, 20:503-509.
79. Pascual O., Casper K.B., Kubera C., Zhang J., Revilla-Sanchez R., Sul J.Y., Takano H., Moss S.J., McCarthy K., Haydon P.G. Astrocytic purinergic signaling coordinates synaptic networks. Science 2005, 310:113-116.
80. Pasti L., Zonta M., Pozzan T., Vicini S., Carmignoto G. Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. J. Neurosci. 2001, 21:477-484.
81. Pfrieger F.W., Barres B.A. Synaptic efficacy enhanced by glial cells in vitro. Science 1997, 277:1684-1687.
82. Pizzo P., Burgo A., Pozzan T., Fasolato C. Role of capacitative calcium entry on glutamate-induced calcium influx in type-I rat cortical astrocytes. J. Neurochem. 2001, 79:98-109.
83. Potokar M., Kreft M., Pangrsic T., Zorec R. Vesicle mobility studied in cultured astrocytes. Biochem. Biophys. Res. Commun. 2005, 329:678-683.
84. Potokar M., Stenovec M., Kreft M., Kreft M.E., Zorec R. Stimulation inhibits the mobility of recycling peptidergic vesicles in astrocytes. Glia 2008, 56:135-144.
85. Potokar M., Kreft M., Lee S.Y., Takano H., Haydon P.G., Zorec R. Trafficking of astrocytic vesicles in hippocampal slices. Biochem. Biophys. Res. Commun. 2009.
86. Potokar M., Kreft M., Li L., Daniel Andersson J., Pangrsic T., Chowdhury H.H., Pekny M., Zorec R. Cytoskeleton and vesicle mobility in astrocytes. Traffic 2007, 8:12-20.
87. Pryazhnikov E., Khiroug L. Sub-micromolar increase in [Ca2+]i triggers delayed exocytosis of ATP in cultured astrocytes. Glia 2008, 56:38-49.
88. Ramamoorthy P., Whim M.D. Trafficking and fusion of neuropeptide Y-containing dense-core granules in astrocytes. J. Neurosci. 2008, 28:13815-13827.
89. Reyes R.C., Parpura V. Mitochondria modulate Ca2+-dependent glutamate release from rat cortical astrocytes. J. Neurosci. 2008, 28:9682-9691.
90. Robinson M.B. Regulated trafficking of neurotransmitter transporters: common notes but different melodies. J. Neurochem. 2002, 80:1-11.
91. Rodriguez J.J., Mackie K., Pickel V.M. Ultrastructural localization of the CB1 cannabinoid receptor in mu-opioid receptor patches of the rat Caudate putamen nucleus. J. Neurosci. 2001, 21:823-833.
92. Rose C., Kresse W., Kettenmann H. Acute insult of ammonia leads to calcium-dependent glutamate release from cultured astrocytes, an effect of pH. J. Biol. Chem. 2005, 280:20937-20944.
93. Rosenberg P.A., Knowles R., Knowles K.P., Li Y. Beta-adrenergic receptor-mediated regulation of extracellular adenosine in cerebral cortex in culture. J. Neurosci. 1994, 14:2953-2965.
94. Sabatini B.L., Regehr W.G. Timing of synaptic transmission. Annu. Rev. Physiol. 1999, 61:521-542.
95. Sawada K., Echigo N., Juge N., Miyaji T., Otsuka M., Omote H., Yamamoto A., Moriyama Y. Identification of a vesicular nucleotide transporter. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5683-5686.
96. Schell M.J., Molliver M.E., Snyder S.H. d-Serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:3948-3952.
97. Simpson P.B., Russell J.T. Role of mitochondrial Ca2+ regulation in neuronal and glial cell signalling. Brain Res. Brain Res. Rev. 1998, 26:72-81.
98. Sorensen J.B., Nagy G., Varoqueaux F., Nehring R.B., Brose N., Wilson M.C., Neher E. Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell 2003, 114:75-86.
99. Stenovec M., Kreft M., Poberaj I., Betz W.J., Zorec R. Slow spontaneous secretion from single large dense-core vesicles monitored in neuroendocrine cells. FASEB J. 2004, 18:1270-1272.
100. Stenovec M., Kreft M., Grilc S., Pangrsic T., Zorec R. EAAT2 density at the astrocyte plasma membrane and Ca2+-regulated exocytosis. Mol. Membr. Biol. 2008, 25:203-215.
101. Stenovec M., Kreft M., Grilc S., Potokar M., Kreft M.E., Pangrsic T., Zorec R. Ca2+-dependent mobility of vesicles capturing anti-VGLUT1 antibodies. Exp. Cell Res. 2007, 313:3809-3818.
102. Stigliani S., Zappettini S., Raiteri L., Passalacqua M., Melloni E., Venturi C., Tacchetti C., Diaspro A., Usai C., Bonanno G. Glia re-sealed particles freshly prepared from adult rat brain are competent for exocytotic release of glutamate. J. Neurochem. 2006, 96:656-668.
103. Szatkowski M., Barbour B., Attwell D. Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 1990, 348:443-446.
104. Takemura H., Putney J.W. Capacitative calcium entry in parotid acinar cells. Biochem. J. 1989, 258:409-412.
105. Tran P.B., Banisadr G., Ren D., Chenn A., Miller R.J. Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. J. Comp. Neurol. 2007, 500:1007-1033.
106. Vardjan N., Stenovec M., Jorgacevski J., Kreft M., Zorec R. Subnanometer fusion pores in spontaneous exocytosis of peptidergic vesicles. J. Neurosci. 2007, 27:4737-4746.
107. Verkhratsky A. Neurotransmitter receptors in astrocytes. Astrocytes in (Patho)Physiology of the Nervous System 2009, 50-67. Springer, Boston, MA. V. Parpura, P.G. Haydon (Eds.).
108. Warr O., Takahashi M., Attwell D. Modulation of extracellular glutamate concentration in rat brain slices by cystine-glutamate exchange. J. Physiol. 1999, 514(Pt 3):783-793.
109. Westergaard N., Drejer J., Schousboe A., Sonnewald U. Evaluation of the importance of transamination versus deamination in astrocytic metabolism of [U-13C]glutamate. Glia 1996, 17:160-168.
110. Wilhelm A., Volknandt W., Langer D., Nolte C., Kettenmann H., Zimmermann H. Localization of SNARE proteins and secretory organelle proteins in astrocytes in vitro and in situ. Neurosci. Res. 2004, 48:249-257.
111. Winkler H., Fischer-Colbrie R. The chromogranins A and B: the first 25 years and future perspectives. Neuroscience 1992, 49:497-528.
112. Wolosker H., Sheth K.N., Takahashi M., Mothet J.P., Brady R.O., Ferris C.D., Snyder S.H. Purification of serine racemase: biosynthesis of the neuromodulator d-serine. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:721-725.
113. Xu J., Peng H., Kang N., Zhao Z., Lin J.H., Stanton P.K., Kang J. Glutamate-induced exocytosis of glutamate from astrocytes. J. Biol. Chem. 2007, 282:24185-24197.
114. Zhang J.M., Wang H.K., Ye C.Q., Ge W., Chen Y., Jiang Z.L., Wu C.P., Poo M.M., Duan S. ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 2003, 40:971-982.
115. Zhang Q., Fukuda M., Van Bockstaele E., Pascual O., Haydon P.G. Synaptotagmin IV regulates glial glutamate release. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9441-9446.
116. Zhang Q., Pangrsic T., Kreft M., Krzan M., Li N., Sul J.Y., Halassa M., Van Bockstaele E., Zorec R., Haydon P.G. Fusion-related release of glutamate from astrocytes. J. Biol. Chem. 2004, 279:12724-12733.
117. Zhang Z., Chen G., Zhou W., Song A., Xu T., Luo Q., Wang W., Gu X.S., Duan S. Regulated ATP release from astrocytes through lysosome exocytosis. Nat. Cell Biol. 2007, 9:945-953.
118. Zonta M., Angulo M.C., Gobbo S., Rosengarten B., Hossmann K.A., Pozzan T., Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci. 2003, 6:43-50.