Astrocytes as secretory cells of the central nervous system: Idiosyncrasies of vesicular secretion

EMBO Journal

Volumn 35, Issue 3, 2016, Pages 239-257

  Verkhratsky, Alexei ^a,b,c,d,e,f   Matteoli, Michela ^g,h   Parpura, Vladimir ⁱ   Mothet, Jean Pierre ^j   Zorec, Robert ^e,f  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b BASQUE FOUNDATION FOR SCIENCE   (Spain)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d LOBACHEVSKY STATE UNIVERSITY OF NIZHNY NOVGOROD   (Russian Federation)

^e UNIVERSITY OF LJUBLJANA   (Slovenia)

^f Celica Biomedical Sciences Center   (Slovenia)

^g CNR   (Italy)

^h HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

ⁱ University of Alabama at Birmingham   (United States)

^j AIX MARSEILLE UNIVERSITY   (France)

more..

Author keywords

astrocytes; exocytosis; secretion; secretory vesicles; SNARE proteins

Indexed keywords

AMINO ACID; AQUAPORIN 4; EXCITATORY AMINO ACID TRANSPORTER; G PROTEIN COUPLED RECEPTOR; GLUTAMATE TRANSPORTER; IONOTROPIC RECEPTOR; SIGNAL PEPTIDE;

ANTIGEN PRESENTATION; ASTROCYTE; BIOGENESIS; CELL FUNCTION; CELL MEMBRANE; CELL ORGANELLE; CENTRAL NERVOUS SYSTEM; COCAINE DEPENDENCE; EXOCYTOSIS; EXOSOME; MEMBRANE MICROPARTICLE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; SECRETORY CELL; SECRETORY VESICLE; ANIMAL; CELL COMMUNICATION; CYTOLOGY; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SECRETION (PROCESS); SECRETORY PATHWAY;

ANIMALS; ASTROCYTES; CELL COMMUNICATION; CENTRAL NERVOUS SYSTEM; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN TRANSPORT; SECRETORY PATHWAY; SECRETORY VESICLES;

EID: 84957432057     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592705     Document Type: Review

References (249)

1. Andrews NW, Chakrabarti S, (2005) There's more to life than neurotransmission: the regulation of exocytosis by synaptotagmin VII. Trends Cell Biol 15: 626-631
2. Arcienega II, Brunet JF, Bloch J, Badaut J, (2010) Cell locations for AQP1, AQP4 and 9 in the non-human primate brain. Neuroscience 167: 1103-1114
3. Arima H, Yamamoto N, Sobue K, Umenishi F, Tada T, Katsuya H, Asai K, (2003) Hyperosmolar mannitol simulates expression of aquaporins 4 and 9 through a p38 mitogen-activated protein kinase-dependent pathway in rat astrocytes. J Biol Chem 278: 44525-44534
4. Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G, (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14: 677-685
5. 2+ channels in insulin-secreting mouse pancreatic β cells. Biophys J 81: 3308-3323
6. Barnea A, Aguila-Mansilla N, Bigio EH, Worby C, Roberts J, (1998) Evidence for regulated expression of neuropeptide Y gene by rat and human cultured astrocytes. Regul Pept 75-76: 293-300
7. Barnea A, Roberts J, Keller P, Word RA, (2001) Interleukin-1beta induces expression of neuropeptide Y in primary astrocyte cultures in a cytokine-specific manner: induction in human but not rat astrocytes. Brain Res 896: 137-145
8. Barois N, Forquet F, Davoust J, (1998) Actin microfilaments control the MHC class II antigen presentation pathway in B cells. J Cell Sci 111: 1791-1800
9. Basheer R, Strecker RE, Thakkar MM, McCarley RW, (2004) Adenosine and sleep-wake regulation. Prog Neurobiol 73: 379-396
10. Batter DK, Vilijn MH, Kessler J, (1991) Cultured astrocytes release proenkephalin. Brain Res 563: 28-32
11. Bergami M, Santi S, Formaggio E, Cagnoli C, Verderio C, Blum R, Berninger B, Matteoli M, Canossa M, (2008) Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J Cell Biol 183: 213-221
12. Bergersen LH, Gundersen V, (2009) Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 158: 260-265
13. Bergersen LH, Morland C, Ormel L, Rinholm JE, Larsson M, Wold JF, Roe AT, Stranna A, Santello M, Bouvier D, Ottersen OP, Volterra A, Gundersen V, (2012) Immunogold detection of L-glutamate and D-serine in small synaptic-like microvesicles in adult hippocampal astrocytes. Cereb Cortex 22: 1690-1697
14. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A, (2001) CXCR4-activated astrocyte glutamate release via TNFα: amplification by microglia triggers neurotoxicity. Nat Neurosci 4: 702-710
15. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A, (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7: 613-620
16. Bianco F, Perrotta C, Novellino L, Francolini M, Riganti L, Menna E, Saglietti L, Schuchman EH, Furlan R, Clementi E, Matteoli M, Verderio C, (2009) Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 28: 1043-1054
17. Bianco F, Pravettoni E, Colombo A, Schenk U, Moller T, Matteoli M, Verderio C, (2005) Astrocyte-derived ATP induces vesicle shedding and IL-1 β release from microglia. J Immunol 174: 7268-7277
18. Blackburn RE, Samson WK, Fulton RJ, Stricker EM, Verbalis JG, (1995) Central oxytocin and ANP receptors mediate osmotic inhibition of salt appetite in rats. Am J Physiol 269: R245-R251
19. Blakely RD, Edwards RH, (2012) Vesicular and plasma membrane transporters for neurotransmitters. Cold Spring Harb Perspect Biol 4: a005595
20. Bollmann JH, Sakmann B, Borst JG, (2000) Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289: 953-957
21. Bowser DN, Khakh BS, (2007) Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc Natl Acad Sci USA 104: 4212-4217
22. Brignone MS, Lanciotti A, Camerini S, De Nuccio C, Petrucci TC, Visentin S, Ambrosini E, (2015) MLC1 protein: a likely link between leukodystrophies and brain channelopathies. Front Cell Neurosci 9: 66
23. Burda JE, Sofroniew MV, (2014) Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81: 229-248
24. Burgoyne RD, Morgan A, (2003) Secretory granule exocytosis. Physiol Rev 83: 581-632
25. Calegari F, Coco S, Taverna E, Bassetti M, Verderio C, Corradi N, Matteoli M, Rosa P, (1999) A regulated secretory pathway in cultured hippocampal astrocytes. J Biol Chem 274: 22539-22547
26. Cali C, Marchaland J, Regazzi R, Bezzi P, (2008) SDF 1-α (CXCL12) triggers glutamate exocytosis from astrocytes on a millisecond time scale: imaging analysis at the single-vesicle level with TIRF microscopy. J Neuroimmunol 198: 82-91
27. Ceruti S, Colombo L, Magni G, Vigano F, Boccazzi M, Deli MA, Sperlagh B, Abbracchio MP, Kittel A, (2011) Oxygen-glucose deprivation increases the enzymatic activity and the microvesicle-mediated release of ectonucleotidases in the cells composing the blood-brain barrier. Neurochem Int 59: 259-271
28. Chaineau M, Danglot L, Galli T, (2009) Multiple roles of the vesicular-SNARE TI-VAMP in post-Golgi and endosomal trafficking. FEBS Lett 583: 3817-3826
29. Chaudhry FA, Boulland JL, Jenstad M, Bredahl MK, Edwards RH, (2008) Pharmacology of neurotransmitter transport into secretory vesicles. Handb Exp Pharmacol 184: 77-106
30. Chen X, Wang L, Zhou Y, Zheng LH, Zhou Z, (2005) "Kiss-and-run" glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J Neurosci 25: 9236-9243
31. Chevallier J, Chamoun Z, Jiang G, Prestwich G, Sakai N, Matile S, Parton RG, Gruenberg J, (2008) Lysobisphosphatidic acid controls endosomal cholesterol levels. J Biol Chem 283: 27871-27880
32. Choi SS, Lee HJ, Lim I, Satoh J, Kim SU, (2014) Human astrocytes: secretome profiles of cytokines and chemokines. PLoS ONE 9: e92325
33. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C, (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278: 1354-1362
34. Cocucci E, Meldolesi J, (2015) Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol 25: 364-372
35. Coorssen JR, Zorec R, (2012) Regulated exocytosis per partes. Cell Calcium 52: 191-195
36. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ, (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247: 470-473
37. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M, (1998) Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 95: 15735-15740
38. Crippa D, Schenk U, Francolini M, Rosa P, Verderio C, Zonta M, Pozzan T, Matteoli M, Carmignoto G, (2006) Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis. J Physiol 570: 567-582
39. Curcio L, Podda MV, Leone L, Piacentini R, Mastrodonato A, Cappelletti P, Sacchi S, Pollegioni L, Grassi C, D'Ascenzo M, (2013) Reduced D-serine levels in the nucleus accumbens of cocaine-treated rats hinder the induction of NMDA receptor-dependent synaptic plasticity. Brain 136: 1216-1230
40. Danbolt NC, (2001) Glutamate uptake. Prog Neurobiol 65: 1-105
41. De Keyser J, Zeinstra E, Mostert J, Wilczak N, (2004) β2-adrenoceptor involvement in inflammatory demyelination and axonal degeneration in multiple sclerosis. Trends Pharmacol Sci 25: 67-71
42. Di Malta C, Fryer JD, Settembre C, Ballabio A, (2012) Astrocyte dysfunction triggers neurodegeneration in a lysosomal storage disorder. Proc Natl Acad Sci USA 109: E2334-E2342
43. 1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-alpha and prostaglandins. J Biol Chem 281: 30684-30696
44. 2+ channels and sensors of exocytosis at fast mammalian synapses. Nat Rev Neurosci 13: 7-21
45. Ehrenreich H, Kehrl JH, Anderson RW, Rieckmann P, Vitkovic L, Coligan JE, Fauci AS, (1991) A vasoactive peptide, endothelin-3, is produced by and specifically binds to primary astrocytes. Brain Res 538: 54-58
46. Erta M, Giralt M, Esposito FL, Fernandez-Gayol O, Hidalgo J, (2015) Astrocytic IL-6 mediates locomotor activity, exploration, anxiety, learning and social behavior. Horm Behav 73: 64-74
47. Eulenburg V, Gomeza J, (2010) Neurotransmitter transporters expressed in glial cells as regulators of synapse function. Brain Res Rev 63: 103-112
48. Falchi AM, Sogos V, Saba F, Piras M, Congiu T, Piludu M, (2013) Astrocytes shed large membrane vesicles that contain mitochondria, lipid droplets and ATP. Histochem Cell Biol 139: 221-231
49. Fasshauer D, Sutton RB, Brunger AT, Jahn R, (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci USA 95: 15781-15786
50. Fellin T, Halassa MM, Terunuma M, Succol F, Takano H, Frank M, Moss SJ, Haydon PG, (2009) Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci USA 106: 15037-15042
51. Fontana A, Fierz W, Wekerle H, (1984) Astrocytes present myelin basic protein to encephalitogenic T-cell lines. Nature 307: 273-276
52. Fremeau RT Jr, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH, (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99: 14488-14493
53. Frohman EM, Vayuvegula B, Gupta S, van den Noort S, (1988) Norepinephrine inhibits gamma-interferon-induced major histocompatibility class II (Ia) antigen expression on cultured astrocytes via beta-2-adrenergic signal transduction mechanisms. Proc Natl Acad Sci USA 85: 1292-1296
54. Fujita T, Chen MJ, Li B, Smith NA, Peng W, Sun W, Toner MJ, Kress BT, Wang L, Benraiss A, Takano T, Wang S, Nedergaard M, (2014) Neuronal transgene expression in dominant-negative SNARE mice. J Neurosci 34: 16594-16604
55. Geloso MC, Corvino V, Di Maria V, Marchese E, Michetti F, (2015) Cellular targets for neuropeptide Y-mediated control of adult neurogenesis. Front Cell Neurosci 9: 85
56. Glees P, (1955) Neuroglia morphology and function. Oxford: Blackwell
57. Gucek A, Vardjan N, Zorec R, (2012) Exocytosis in astrocytes: transmitter release and membrane signal regulation. Neurochem Res 37: 2351-2363
58. Guescini M, Genedani S, Stocchi V, Agnati LF, (2010) Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J Neural Transm 117: 1-4
59. Gunnarson E, Zelenina M, Axehult G, Song Y, Bondar A, Krieger P, Brismar H, Zelenin S, Aperia A, (2008) Identification of a molecular target for glutamate regulation of astrocyte water permeability. Glia 56: 587-596
60. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Haydon PG, Frank MG, (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61: 213-219
61. Hamilton NB, Attwell D, (2010) Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11: 227-238
62. Hansel DE, Eipper BA, Ronnett GV, (2001) Neuropeptide Y functions as a neuroproliferative factor. Nature 410: 940-944
63. Heidelberger R, Heinemann C, Neher E, Matthews G, (1994) Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371: 513-515
64. Heja L, Barabas P, Nyitrai G, Kekesi KA, Lasztoczi B, Toke O, Tarkanyi G, Madsen K, Schousboe A, Dobolyi A, Palkovits M, Kardos J, (2009) Glutamate uptake triggers transporter-mediated GABA release from astrocytes. PLoS ONE 4: e7153
65. Held H, (1909) Über die Neuroglia marginalis der menschlichen Grosshirnrinde. Monatschr f Psychol u Neurol 26 Rdg.-Heft: 360-416
66. Henneberger C, Papouin T, Oliet SH, Rusakov DA, (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463: 232-236
67. Hepp R, Perraut M, Chasserot-Golaz S, Galli T, Aunis D, Langley K, Grant NJ, (1999) Cultured glial cells express the SNAP-25 analogue SNAP-23. Glia 27: 181-187
68. Hertz L, (2013) The Glutamate-Glutamine (GABA) Cycle: importance of Late Postnatal Development and Potential Reciprocal Interactions between Biosynthesis and Degradation. Front Endocrinol (Lausanne) 4: 59
69. Hines DJ, Haydon PG, (2013) Inhibition of a SNARE-sensitive pathway in astrocytes attenuates damage following stroke. J Neurosci 33: 4234-4240
70. Hirt B, Gleiser C, Eckhard A, Mack AF, Muller M, Wolburg H, Lowenheim H, (2011) All functional aquaporin-4 isoforms are expressed in the rat cochlea and contribute to the formation of orthogonal arrays of particles. Neuroscience 189: 79-92
71. Holers VM, (2014) Complement and its receptors: new insights into human disease. Annu Rev Immunol 32: 433-459
72. Holopainen I, Kontro P, (1989) Uptake and release of glycine in cerebellar granule cells and astrocytes in primary culture: potassium-stimulated release from granule cells is calcium-dependent. J Neurosci Res 24: 374-383
73. Hsu C, Morohashi Y, Yoshimura S, Manrique-Hoyos N, Jung S, Lauterbach MA, Bakhti M, Gronborg M, Mobius W, Rhee J, Barr FA, Simons M, (2010) Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 189: 223-232
74. Hu G, Yao H, Chaudhuri AD, Duan M, Yelamanchili SV, Wen H, Cheney PD, Fox HS, Buch S, (2012) Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death Dis 3: e381
75. Huang YH, Bergles DE, (2004) Glutamate transporters bring competition to the synapse. Curr Opin Neurobiol 14: 346-352
76. 2+ signaling system in astrocytes. PLoS ONE 5: e11973
77. Jahn HM, Scheller A, Kirchhoff F, (2015) Genetic control of astrocyte function in neural circuits. Front Cell Neurosci 9: 310
78. Jahn R, Scheller RH, (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643
79. Jaiswal JK, Andrews NW, Simon SM, (2002) Membrane proximal lysosomes are the major vesicles responsible for calcium-dependent exocytosis in nonsecretory cells. J Cell Biol 159: 625-635
80. Jaiswal JK, Fix M, Takano T, Nedergaard M, Simon SM, (2007) Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes. Proc Natl Acad Sci USA 104: 14151-14156
81. Jayakumar AR, Tong XY, Curtis KM, Ruiz-Cordero R, Shamaladevi N, Abuzamel M, Johnstone J, Gaidosh G, Rama Rao KV, Norenberg MD, (2014) Decreased astrocytic thrombospondin-1 secretion after chronic ammonia treatment reduces the level of synaptic proteins: in vitro and in vivo studies. J Neurochem 131: 333-347
82. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, Matute C, Tonello F, Gundersen V, Volterra A, (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 10: 331-339
83. 2-adrenergic receptors. Neurochem Int 52: 297-306
84. Kang N, Peng H, Yu Y, Stanton PK, Guilarte TR, Kang J, (2013) Astrocytes release D-serine by a large vesicle. Neuroscience 240: 243-257
85. Kasai H, Takahashi N, Tokumaru H, (2012) Distinct initial SNARE configurations underlying the diversity of exocytosis. Physiol Rev 92: 1915-1964
86. Ke C, Poon WS, Ng HK, Pang JC, Chan Y, (2001) Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci Lett 301: 21-24
87. Kimelberg HK, Goderie SK, Higman S, Pang S, Waniewski RA, (1990) Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. J Neurosci 10: 1583-1591
88. Kirischuk S, Kirchhoff F, Matyash V, Kettenmann H, Verkhratsky A, (1999) Glutamate-triggered calcium signalling in mouse bergmann glial cells in situ: role of inositol-1,4,5-trisphosphate-mediated intracellular calcium release. Neuroscience 92: 1051-1059
89. Klyachko VA, Jackson MB, (2002) Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418: 89-92
90. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J, (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392: 193-197
91. Kreft M, Krizaj D, Grilc S, Zorec R, (2003) Properties of exocytotic response in vertebrate photoreceptors. J Neurophysiol 90: 218-225
92. 2+-dependent exocytosis in cultured astrocytes. Glia 46: 437-445
93. Krzan M, Stenovec M, Kreft M, Pangrsic T, Grilc S, Haydon PG, Zorec R, (2003) Calcium-dependent exocytosis of atrial natriuretic peptide from astrocytes. J Neurosci 23: 1580-1583
94. Lafon-Cazal M, Adjali O, Galeotti N, Poncet J, Jouin P, Homburger V, Bockaert J, Marin P, (2003) Proteomic analysis of astrocytic secretion in the mouse. Comparison with the cerebrospinal fluid proteome. J Biol Chem 278: 24438-24448
95. Lalo U, Palygin O, Rasooli-Nejad S, Andrew J, Haydon PG, Pankratov Y, (2014) Exocytosis of ATP from astrocytes modulates phasic and tonic inhibition in the neocortex. PLoS Biol 12: e1001747
96. Lane DJ, Lawen A, (2013) The glutamate aspartate transporter (GLAST) mediates L-glutamate-stimulated ascorbate-release via swelling-activated anion channels in cultured neonatal rodent astrocytes. Cell Biochem Biophys 65: 107-119
97. Lee M, McGeer EG, McGeer PL, (2011) Mechanisms of GABA release from human astrocytes. Glia 59: 1600-1611
98. von Lenhossék M, (1895) Der feinere Bau des Nervensystems im Lichte neuester Forschung, 2nd edn. Berlin: Fischer's Medicinische Buchhandlung H. Kornfield
99. Li D, Herault K, Silm K, Evrard A, Wojcik S, Oheim M, Herzog E, Ropert N, (2013) Lack of evidence for vesicular glutamate transporter expression in mouse astrocytes. J Neurosci 33: 4434-4455
100. 2+ -independent cycling and modulate glutamate transporter trafficking. J Physiol 593: 2807-2832
101. 2+-regulated exocytosis from cortical astrocytes. J Neurosci 28: 7648-7658
102. Lian H, Yang L, Cole A, Sun L, Chiang AC, Fowler SW, Shim DJ, Rodriguez-Rivera J, Taglialatela G, Jankowsky JL, Lu HC, Zheng H, (2015) NFkappaB-activated astroglial release of complement C3 compromises neuronal morphology and function associated with Alzheimer's disease. Neuron 85: 101-115
103. Liu T, Sun L, Xiong Y, Shang S, Guo N, Teng S, Wang Y, Liu B, Wang C, Wang L, Zheng L, Zhang CX, Han W, Zhou Z, (2011) Calcium triggers exocytosis from two types of organelles in a single astrocyte. J Neurosci 31: 10593-10601
104. Lu B, Pang PT, Woo NH, (2005) The yin and yang of neurotrophin action. Nat Rev Neurosci 6: 603-614
105. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Waldman SA, (2000) Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 52: 375-414
106. Maienschein V, Marxen M, Volknandt W, Zimmermann H, (1999) A plethora of presynaptic proteins associated with ATP-storing organelles in cultured astrocytes. Glia 26: 233-244
107. Malarkey EB, Parpura V, (2008) Mechanisms of glutamate release from astrocytes. Neurochem Int 52: 142-154
108. Malarkey EB, Parpura V, (2011) Temporal characteristics of vesicular fusion in astrocytes: examination of synaptobrevin 2-laden vesicles at single vesicle resolution. J Physiol 589: 4271-4300
109. 2+ transients control exo-endocytosis of synaptic-like microvesicles in astrocytes. J Neurosci 28: 9122-9132
110. Martineau M, Galli T, Baux G, Mothet JP, (2008) Confocal imaging and tracking of the exocytotic routes for D-serine-mediated gliotransmission. Glia 56: 1271-1284
111. Martineau M, Parpura V, Mothet JP, (2014) Cell-type specific mechanisms of D-serine uptake and release in the brain. Front Synaptic Neurosci 6: 12
112. Martineau M, Shi T, Puyal J, Knolhoff AM, Dulong J, Gasnier B, Klingauf J, Sweedler JV, Jahn R, Mothet JP, (2013) Storage and uptake of D-serine into astrocytic synaptic-like vesicles specify gliotransmission. J Neurosci 33: 3413-3423
113. Mathivanan S, Ji H, Simpson RJ, (2010) Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73: 1907-1920
114. Mause SF, Weber C, (2010) Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res 107: 1047-1057
115. Mazzanti M, Sul JY, Haydon PG, (2001) Glutamate on demand: astrocytes as a ready source. Neuroscientist 7: 396-405
116. McKenna MC, (2007) The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain. J Neurosci Res 85: 3347-3358
117. McKenzie JC, Juan YW, Thomas CR, Berman NE, Klein RM, (2001) Atrial natriuretic peptide-like immunoreactivity in neurons and astrocytes of human cerebellum and inferior olivary complex. J Histochem Cytochem 49: 1453-1467
118. Minich T, Riemer J, Schulz JB, Wielinga P, Wijnholds J, Dringen R, (2006) The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J Neurochem 97: 373-384
119. Mittelsteadt T, Seifert G, Alvarez-Baron E, Steinhauser C, Becker AJ, Schoch S, (2009) Differential mRNA expression patterns of the synaptotagmin gene family in the rodent brain. J Comp Neurol 512: 514-528
120. Montana V, Liu W, Mohideen U, Parpura V, (2009) Single molecule measurements of mechanical interactions within ternary SNARE complexes and dynamics of their disassembly: SNAP25 vs. SNAP23. J Physiol 587: 1943-1960
121. Montana V, Malarkey EB, Verderio C, Matteoli M, Parpura V, (2006) Vesicular transmitter release from astrocytes. Glia 54: 700-715
122. Montana V, Ni Y, Sunjara V, Hua X, Parpura V, (2004) Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 24: 2633-2642
123. Morte B, Bernal J, (2014) Thyroid hormone action: astrocyte-neuron communication. Front Endocrinol (Lausanne) 5: 82
124. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P, Baux G, (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci USA 102: 5606-5611
125. Muhic M, Vardjan N, Chowdhury HH, Zorec R, Kreft M, (2015) Insulin and Insulin-like Growth Factor 1 (IGF-1) Modulate Cytoplasmic Glucose and Glycogen Levels but Not Glucose Transport across the Membrane in Astrocytes. J Biol Chem 290: 11167-11176
126. Murphy S, Pearce B, Jeremy J, Dandona P, (1988) Astrocytes as eicosanoid-producing cells. Glia 1: 241-245
127. Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q, (2012) Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci USA 109: 4146-4151
128. Nadjar A, Blutstein T, Aubert A, Laye S, Haydon PG, (2013) Astrocyte-derived adenosine modulates increased sleep pressure during inflammatory response. Glia 61: 724-731
129. Nagelhus EA, Ottersen OP, (2013) Physiological roles of aquaporin-4 in brain. Physiol Rev 93: 1543-1562
130. Nagelhus EA, Veruki ML, Torp R, Haug FM, Laake JH, Nielsen S, Agre P, Ottersen OP, (1998) Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Muller cells and fibrous astrocytes. J Neurosci 18: 2506-2519
131. Nageotte J, (1910) Phenomenes de secretion dans le protoplasma des cellules nevrogliques de la substance grise. C R Soc Biol (Paris) 68: 1068-1069
132. Nakamura Y, Iga K, Shibata T, Shudo M, Kataoka K, (1993) Glial plasmalemmal vesicles: a subcellular fraction from rat hippocampal homogenate distinct from synaptosomes. Glia 9: 48-56
133. Navarrete M, Araque A, (2008) Endocannabinoids mediate neuron-astrocyte communication. Neuron 57: 883-893
134. Neher E, (2012) Introduction: regulated exocytosis. Cell Calcium 52: 196-198
135. Nicchia GP, Ficarella R, Rossi A, Giangreco I, Nicolotti O, Carotti A, Pisani F, Estivill X, Gasparini P, Svelto M, Frigeri A, (2011) D184E mutation in aquaporin-4 gene impairs water permeability and links to deafness. Neuroscience 197: 80-88
136. van Niel G, Porto-Carreiro I, Simoes S, Raposo G, (2006) Exosomes: a common pathway for a specialized function. J Biochem 140: 13-21
137. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP, (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17: 171-180
138. Nogami M, Shiga J, Takatsu A, Endo N, Ishiyama I, (2001) Immunohistochemistry of atrial natriuretic peptide in brain infarction. Histochem J 33: 87-90
139. Ormel L, Stensrud MJ, Chaudhry FA, Gundersen V, (2012) A distinct set of synaptic-like microvesicles in atroglial cells contain VGLUT3. Glia 60: 1289-1300
140. Osborne KD, Lee W, Malarkey EB, Irving AJ, Parpura V, (2009) Dynamic imaging of cannabinoid receptor 1 vesicular trafficking in cultured astrocytes. ASN Neuro 1: e00022
141. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C, (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19-30; sup pp 11-13
142. Oya M, Kitaguchi T, Yanagihara Y, Numano R, Kakeyama M, Ikematsu K, Tsuboi T, (2013) Vesicular nucleotide transporter is involved in ATP storage of secretory lysosomes in astrocytes. Biochem Biophys Res Commun 438: 145-151
143. 2+-dependent peptide secretion in astrocytes. J Neurochem 110: 143-156
144. Paco S, Pozas E, Aguado F, (2010) Secretogranin III is an astrocyte granin that is overexpressed in reactive glia. Cereb Cortex 20: 1386-1397
145. Pangrsic T, Potokar M, Stenovec M, Kreft M, Fabbretti E, Nistri A, Pryazhnikov E, Khiroug L, Giniatullin R, Zorec R, (2007) Exocytotic release of ATP from cultured astrocytes. J Biol Chem 282: 28749-28758
146. Papadopoulos MC, Manley GT, Krishna S, Verkman AS, (2004) Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 18: 1291-1293
147. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG, (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369: 744-747
148. Parpura V, Fang Y, Basarsky T, Jahn R, Haydon PG, (1995) Expression of synaptobrevin II, cellubrevin and syntaxin but not SNAP-25 in cultured astrocytes. FEBS Lett 377: 489-492
149. Parpura V, Zorec R, (2010) Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63: 83-92
150. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG, (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310: 113-116
151. Passafaro M, Piech V, Sheng M, (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4: 917-926
152. Pekny M, Wilhelmsson U, Pekna M, (2014) The dual role of astrocyte activation and reactive gliosis. Neurosci Lett 565: 30-38
153. Pellerin L, Magistretti PJ, (2012) Sweet sixteen for ANLS. J Cereb Blood Flow Metab 32: 1152-1166
154. Penfield W, (1932) Neuroglia, normal and pathological. In Cytology and Cellular pathology of the Nervous system, Penfield W, (ed.), Vol. 2, pp 421-479. New York: Paul B. Hoeber, Inc.
155. Perea G, Araque A, (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317: 1083-1086
156. Pershing ML, Bortz DM, Pocivavsek A, Fredericks PJ, Jorgensen CV, Vunck SA, Leuner B, Schwarcz R, Bruno JP, (2015) Elevated levels of kynurenic acid during gestation produce neurochemical, morphological, and cognitive deficits in adulthood: implications for schizophrenia. Neuropharmacology 90: 33-41
157. van der Pol E, Boing AN, Harrison P, Sturk A, Nieuwland R, (2012) Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 64: 676-705
158. Poo MM, (2001) Neurotrophins as synaptic modulators. Nat Rev Neurosci 2: 24-32
159. Potokar M, Kreft M, Pangrsic T, Zorec R, (2005) Vesicle mobility studied in cultured astrocytes. Biochem Biophys Res Commun 329: 678-683
160. Potokar M, Stenovec M, Gabrijel M, Li L, Kreft M, Grilc S, Pekny M, Zorec R, (2010) Intermediate filaments attenuate stimulation-dependent mobility of endosomes/lysosomes in astrocytes. Glia 58: 1208-1219
161. Potokar M, Stenovec M, Jorgacevski J, Holen T, Kreft M, Ottersen OP, Zorec R, (2013a) Regulation of AQP4 surface expression via vesicle mobility in astrocytes. Glia 61: 917-928
162. Potokar M, Stenovec M, Kreft M, Kreft ME, Zorec R, (2008) Stimulation inhibits the mobility of recycling peptidergic vesicles in astrocytes. Glia 56: 135-144
163. Potokar M, Vardjan N, Stenovec M, Gabrijel M, Trkov S, Jorgacevski J, Kreft M, Zorec R, (2013b) Astrocytic vesicle mobility in health and disease. Int J Mol Sci 14: 11238-11258
164. Potter LR, Abbey-Hosch S, Dickey DM, (2006) Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 27: 47-72
165. Prada I, Marchaland J, Podini P, Magrassi L, D'Alessandro R, Bezzi P, Meldolesi J, (2011) REST/NRSF governs the expression of dense-core vesicle gliosecretion in astrocytes. J Cell Biol 193: 537-549
166. Prebil M, Vardjan N, Jensen J, Zorec R, Kreft M, (2011) Dynamic monitoring of cytosolic glucose in single astrocytes. Glia 59: 903-913
167. Proia P, Schiera G, Mineo M, Ingrassia AM, Santoro G, Savettieri G, Di Liegro I, (2008) Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor. Int J Mol Med 21: 63-67
168. i triggers delayed exocytosis of ATP in cultured astrocytes. Glia 56: 38-49
169. 7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol 179: 1913-1925
170. Queiroz G, Gebicke-Haerter PJ, Schobert A, Starke K, von Kugelgen I, (1997) Release of ATP from cultured rat astrocytes elicited by glutamate receptor activation. Neuroscience 78: 1203-1208
171. Ramamoorthy P, Whim MD, (2008) Trafficking and fusion of neuropeptide Y-containing dense-core granules in astrocytes. J Neurosci 28: 13815-13827
172. Rana S, Dringen R, (2007) Gap junction hemichannel-mediated release of glutathione from cultured rat astrocytes. Neurosci Lett 415: 45-48
173. Robinson MB, (2002) Regulated trafficking of neurotransmitter transporters: common notes but different melodies. J Neurochem 80: 1-11
174. Rose RA, Giles WR, (2008) Natriuretic peptide C receptor signalling in the heart and vasculature. J Physiol 586: 353-366
175. Rossi D, (2015) Astrocyte physiopathology: at the crossroads of intercellular networking, inflammation and cell death. Prog Neurobiol 130: 86-120
176. Rupnik M, Kreft M, Sikdar SK, Grilc S, Romih R, Zupancic G, Martin TF, Zorec R, (2000) Rapid regulated dense-core vesicle exocytosis requires the CAPS protein. Proc Natl Acad Sci USA 97: 5627-5632
177. Sahlender DA, Savtchouk I, Volterra A, (2014) What do we know about gliotransmitter release from astrocytes? Philos Trans R Soc Lond B Biol Sci 369: 20130592
178. 2+-dependent steps controlling synaptic vesicle fusion and replenishment at the cerebellar basket cell terminal. Neuron 57: 406-419
179. Santello M, Bezzi P, Volterra A, (2011) TNFalpha controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69: 988-1001
180. Sarkar A, Mitra S, Mehta S, Raices R, Wewers MD, (2009) Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS ONE 4: e7140
181. Sato K, Malchinkhuu E, Horiuchi Y, Mogi C, Tomura H, Tosaka M, Yoshimoto Y, Kuwabara A, Okajima F, (2007) Critical role of ABCA1 transporter in sphingosine 1-phosphate release from astrocytes. J Neurochem 103: 2610-2619
182. Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M, Omote H, Yamamoto A, Moriyama Y, (2008) Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 105: 5683-5686
183. Sbai O, Ould-Yahoui A, Ferhat L, Gueye Y, Bernard A, Charrat E, Mehanna A, Risso JJ, Chauvin JP, Fenouillet E, Rivera S, Khrestchatisky M, (2010) Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes. Glia 58: 344-366
184. Schell MJ, Molliver ME, Snyder SH, (1995) D-serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc Natl Acad Sci USA 92: 3948-3952
185. Schneggenburger R, Neher E, (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406: 889-893
186. Schubert V, Bouvier D, Volterra A, (2011) SNARE protein expression in synaptic terminals and astrocytes in the adult hippocampus: a comparative analysis. Glia 59: 1472-1488
187. Scofield MD, Boger HA, Smith RJ, Li H, Haydon PG, Kalivas PW, (2015) Gq-DREADD selectively initiates glial glutamate release and inhibits cue-induced cocaine seeking. Biol Psychiatry 78: 441-451
188. Shigetomi E, Jackson-Weaver O, Huckstepp RT, O'Dell TJ, Khakh BS, (2013) TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J Neurosci 33: 10143-10153
189. Shinjyo N, Stahlberg A, Dragunow M, Pekny M, Pekna M, (2009) Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells. Stem Cells 27: 2824-2832
190. Shrikant P, Benveniste EN, (1996) The central nervous system as an immunocompetent organ: role of glial cells in antigen presentation. J Immunol 157: 1819-1822
191. Sild M, Van Horn MR, (2013) Astrocytes use a novel transporter to fill gliotransmitter vesicles with D-serine: evidence for vesicular synergy. J Neurosci 33: 10193-10194
192. Singh P, Jorgacevski J, Kreft M, Grubisic V, Stout RF Jr, Potokar M, Parpura V, Zorec R, (2014) Single-vesicle architecture of synaptobrevin2 in astrocytes. Nat Commun 5: 3780
193. Slezak M, Grosche A, Niemiec A, Tanimoto N, Pannicke T, Munch TA, Crocker B, Isope P, Hartig W, Beck SC, Huber G, Ferracci G, Perraut M, Reber M, Miehe M, Demais V, Leveque C, Metzger D, Szklarczyk K, Przewlocki R, et al, (2012) Relevance of exocytotic glutamate release from retinal glia. Neuron 74: 504-516
194. Sloan SA, Barres BA, (2014) Looks can be deceiving: reconsidering the evidence for gliotransmission. Neuron 84: 1112-1115
195. Sofroniew MV, (2015) Astrocyte barriers to neurotoxic inflammation. Nat Rev Neurosci 16: 249-263
196. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE, (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362: 318-324
197. Soos JM, Morrow J, Ashley TA, Szente BE, Bikoff EK, Zamvil SS, (1998) Astrocytes express elements of the class II endocytic pathway and process central nervous system autoantigen for presentation to encephalitogenic T cells. J Immunol 161: 5959-5966
198. +-stimulated astrocytes. J Neurosci 35: 4168-4178
199. Spang A, Saw JH, Jorgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJ, (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521: 173-179
200. 2+-regulated exocytosis. Mol Membr Biol 25: 203-215
201. 2+-dependent mobility of vesicles capturing anti-VGLUT1 antibodies. Exp Cell Res 313: 3809-3818
202. Stenovec M, Lasic E, Bozic M, Bobnar ST, Stout RF Jr, Grubisic V, Parpura V, Zorec R, (2015) Ketamine inhibits ATP-evoked exocytotic release of brain-derived neurotrophic factor from vesicles in cultured rat astrocytes. Mol Neurobiol doi: 10.1007/s12035-015-9562-y
203. Stenovec M, Trkov S, Lasic E, Terzieva S, Kreft M, Rodriguez Arellano JJ, Parpura V, Verkhratsky A, Zorec R, (2016) Expression of familial Alzheimer disease presenilin 1 gene attenuates vesicle traffic and reduces peptide secretion in cultured astrocytes devoid of pathologic tissue environment. Glia 64: 317-329
204. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA, (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131: 1164-1178
205. Stigliani S, Zappettini S, Raiteri L, Passalacqua M, Melloni E, Venturi C, Tacchetti C, Diaspro A, Usai C, Bonanno G, (2006) Glia re-sealed particles freshly prepared from adult rat brain are competent for exocytotic release of glutamate. J Neurochem 96: 656-668
206. 2+ signaling. J Neurosci 26: 1378-1385
207. Suadicani SO, Iglesias R, Wang J, Dahl G, Spray DC, Scemes E, (2012) ATP signaling is deficient in cultured Pannexin1-null mouse astrocytes. Glia 60: 1106-1116
208. Sudhof TC, (2012) Calcium control of neurotransmitter release. Cold Spring Harb Perspect Biol 4: a011353
209. Sultan S, Li L, Moss J, Petrelli F, Casse F, Gebara E, Lopatar J, Pfrieger FW, Bezzi P, Bischofberger J, Toni N, (2015) Synaptic integration of adult-born hippocampal neurons is locally controlled by astrocytes. Neuron 88: 957-972
210. Sutton RB, Fasshauer D, Jahn R, Brunger AT, (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395: 347-353
211. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J, et al, (2006) Molecular anatomy of a trafficking organelle. Cell 127: 831-846
212. Tang F, Lane S, Korsak A, Paton JF, Gourine AV, Kasparov S, Teschemacher AG, (2014) Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat Commun 5: 3284
213. Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M, Milligan CE, (2007) Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases. Dev Neurobiol 67: 1815-1829
214. Thery C, Ostrowski M, Segura E, (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593
215. 2+ receptor controls the final steps in peptide secretion from pituitary melanotrophs. Neuron 11: 93-104
216. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42: 595-605
217. Thrane AS, Rangroo Thrane V, Nedergaard M, (2014) Drowning stars: reassessing the role of astrocytes in brain edema. Trends Neurosci 37: 620-628
218. Toyomoto M, Ohta M, Okumura K, Yano H, Matsumoto K, Inoue S, Hayashi K, Ikeda K, (2004) Prostaglandins are powerful inducers of NGF and BDNF production in mouse astrocyte cultures. FEBS Lett 562: 211-215
219. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M, (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244-1247
220. Turner JR, Ecke LE, Briand LA, Haydon PG, Blendy JA, (2013) Cocaine-related behaviors in mice with deficient gliotransmission. Psychopharmacology 226: 167-176
221. Unichenko P, Dvorzhak A, Kirischuk S, (2013) Transporter-mediated replacement of extracellular glutamate for GABA in the developing murine neocortex. Eur J Neurosci 38: 3580-3588
222. + concentration influences short-term plasticity of glutamate transporter-mediated currents in neocortical astrocytes. Glia 60: 605-614
223. Vanlandingham PA, Ceresa BP, (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284: 12110-12124
224. Vardjan N, Gabrijel M, Potokar M, Svajger U, Kreft M, Jeras M, de Pablo Y, Faiz M, Pekny M, Zorec R, (2012) IFN-γ-induced increase in the mobility of MHC class II compartments in astrocytes depends on intermediate filaments. J Neuroinflammation 9: 144
225. Vardjan N, Kreft M, Zorec R, (2014a) Regulated Exocytosis in Astrocytes is as Slow as the Metabolic Availability of Gliotransmitters: Focus on Glutamate and ATP. Adv Neurobiol 11: 81-101
226. Vardjan N, Parpura V, Zorec R, (2015) Loose excitation-secretion coupling in astrocytes. Glia doi: 10.1002/glia.22920
227. Vardjan N, Potokar M, Stenovec M, Jorgačevski J, Saša T, Kreft M, Zorec R, (2014b) Pathophysiology of vesicle dynamics in astrocytes. In Pathological Potential of Neuroglia: Possible New Targets for Medical Intervention, Parpura V, Verkhratsky A, (eds), pp 33-60. Heidelberg: Springer
228. Vardjan N, Stenovec M, Jorgacevski J, Kreft M, Zorec R, (2010) Fusion pore: an evolutionary invention of nucleated cells. Eur Rev 18: 347-364
229. Vardjan N, Zorec R, (2015) Excitable astrocytes: Ca- and cAMP-regulated exocytosis. Neurochem Res 40: 2414-2424
230. Vascotto F, Lankar D, Faure-Andre G, Vargas P, Diaz J, Le Roux D, Yuseff MI, Sibarita JB, Boes M, Raposo G, Mougneau E, Glaichenhaus N, Bonnerot C, Manoury B, Lennon-Dumenil AM, (2007) The actin-based motor protein myosin II regulates MHC class II trafficking and BCR-driven antigen presentation. J Cell Biol 176: 1007-1019
231. Verderio C, Cagnoli C, Bergami M, Francolini M, Schenk U, Colombo A, Riganti L, Frassoni C, Zuccaro E, Danglot L, Wilhelm C, Galli T, Canossa M, Matteoli M, (2012) TI-VAMP/VAMP7 is the SNARE of secretory lysosomes contributing to ATP secretion from astrocytes. Biol Cell 104: 213-228
232. Verderio C, Coco S, Rossetto O, Montecucco C, Matteoli M, (1999) Internalization and proteolytic action of botulinum toxins in CNS neurons and astrocytes. J Neurochem 73: 372-379
233. 2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28: 537-545
234. Vyas JM, Kim YM, Artavanis-Tsakonas K, Love JC, Van der Veen AG, Ploegh HL, (2007) Tubulation of class II MHC compartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells. J Immunol 178: 7199-7210
235. 2+. J Gen Physiol 124: 653-662
236. Wang G, Dinkins M, He Q, Zhu G, Poirier C, Campbell A, Mayer-Proschel M, Bieberich E, (2012) Astrocytes secrete exosomes enriched with proapoptotic ceramide and prostate apoptosis response 4 (PAR-4): potential mechanism of apoptosis induction in Alzheimer disease (AD). J Biol Chem 287: 21384-21395
237. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Sollner TH, Rothman JE, (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92: 759-772
238. Wilhelm A, Volknandt W, Langer D, Nolte C, Kettenmann H, Zimmermann H, (2004) Localization of SNARE proteins and secretory organelle proteins in astrocytes in vitro and in situ. Neurosci Res 48: 249-257
239. Wilson JX, Jaworski EM, Dixon SJ, (1991) Evidence for electrogenic sodium-dependent ascorbate transport in rat astroglia. Neurochem Res 16: 73-78
240. Wu HQ, Pereira EF, Bruno JP, Pellicciari R, Albuquerque EX, Schwarcz R, (2010) The astrocyte-derived α7 nicotinic receptor antagonist kynurenic acid controls extracellular glutamate levels in the prefrontal cortex. J Mol Neurosci 40: 204-210
241. Wubbolts R, Fernandez-Borja M, Jordens I, Reits E, Dusseljee S, Echeverri C, Vallee RB, Neefjes J, (1999) Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J Cell Sci 112: 785-795
242. Xu J, Chalimoniuk M, Shu Y, Simonyi A, Sun AY, Gonzalez FA, Weisman GA, Wood WG, Sun GY, (2003a) Prostaglandin E2 production in astrocytes: regulation by cytokines, extracellular ATP, and oxidative agents. Prostaglandins Leukot Essent Fatty Acids 69: 437-448
243. 2. Free Radic Biol Med 34: 1531-1543
244. Yamamoto N, Yoneda K, Asai K, Sobue K, Tada T, Fujita Y, Katsuya H, Fujita M, Aihara N, Mase M, Yamada K, Miura Y, Kato T, (2001) Alterations in the expression of the AQP family in cultured rat astrocytes during hypoxia and reoxygenation. Brain Res Mol Brain Res 90: 26-38
245. Zhang Q, Fukuda M, Van Bockstaele E, Pascual O, Haydon PG, (2004a) Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci USA 101: 9441-9446
246. Zhang Q, Pangrsic T, Kreft M, Krzan M, Li N, Sul JY, Halassa M, Van Bockstaele E, Zorec R, Haydon PG, (2004b) Fusion-related release of glutamate from astrocytes. J Biol Chem 279: 12724-12733
247. Zhang Z, Chen G, Zhou W, Song A, Xu T, Luo Q, Wang W, Gu XS, Duan S, (2007) Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol 9: 945-953
248. Zhou Y, Danbolt NC, (2013) GABA and Glutamate Transporters in Brain. Front Endocrinol (Lausanne) 4: 165
249. Zukowska-Grojec Z, Pruszczyk P, Colton C, Yao J, Shen GH, Myers AK, Wahlestedt C, (1993) Mitogenic effect of neuropeptide Y in rat vascular smooth muscle cells. Peptides 14: 263-268