Exocytosis in Astrocytes
Abstract
:1. Introduction
1.1. Synaptic-like Microvesicles (SLMVs)
1.2. Dense-Core Vesicles (DCV)
1.3. Secretory Lysosomes (SL)
2. The Exocytosis Machinery in Astrocytes
3. Spatial Organisation of Exocytosis
4. The Ca2+ Sensor for Regulated Exocytosis in Astrocytes
5. Exocytosis in Pathological Conditions
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Oberheim, N.A.; Takano, T.; Han, X.; He, W.; Lin, J.H.C.; Wang, F.; Xu, Q.; Wyatt, J.D.; Pilcher, W.; Ojemann, J.; et al. Uniquely Hominid Features of Adult Human Astrocytes. J. Neurosci. 2009, 29, 3276–3287. [Google Scholar] [CrossRef] [PubMed]
- Giaume, C.; Naus, C.C. Connexins, gap junctions, and glia. Wiley Interdiscip. Rev. Membr. Transp. Signal. 2013, 2, 133–142. [Google Scholar] [CrossRef]
- Edallérac, G.; Echever, O.; Erouach, N. How do astrocytes shape synaptic transmission? Insights from electrophysiology. Front. Cell. Neurosci. 2013, 7, 159. [Google Scholar] [CrossRef] [Green Version]
- Cornell-Bell, A.H.; Finkbeiner, S.M.; Cooper, M.S.; Smith, S.J. Glutamate induces calcium waves in cultured astrocytes: Long-range glial signaling. Science 1990, 247, 470–473. [Google Scholar] [CrossRef]
- Agulhon, C.; Petravicz, J.; McMullen, A.B.; Sweger, E.J.; Minton, S.K.; Taves, S.; Casper, K.B.; Fiacco, T.A.; McCarthy, K.D. What Is the Role of Astrocyte Calcium in Neurophysiology? Neuron 2008, 59, 932–946. [Google Scholar] [CrossRef] [Green Version]
- Araque, A.; Carmignoto, G.; Haydon, P.G.; Oliet, S.H.; Robitaille, R.; Volterra, A. Gliotransmitters Travel in Time and Space. Neuron 2014, 81, 728–739. [Google Scholar] [CrossRef] [Green Version]
- Bazargani, N.; Attwell, D. Astrocyte calcium signaling: The third wave. Nat. Neurosci. 2016, 19, 182–189. [Google Scholar] [CrossRef]
- Bekar, L.K.; He, W.; Nedergaard, M. Locus Coeruleus α-Adrenergic–Mediated Activation of Cortical Astrocytes In Vivo. Cereb. Cortex 2008, 18, 2789–2795. [Google Scholar] [CrossRef] [Green Version]
- Hirase, H.; Qian, L.; Barthó, P.; Buzsaki, G. Calcium Dynamics of Cortical Astrocytic Networks In Vivo. PLoS Biol. 2004, 2, e96. [Google Scholar] [CrossRef] [Green Version]
- Nedergaard, M. Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 1994, 263, 1768–1771. [Google Scholar] [CrossRef]
- Parpura, V.; Basarsky, T.A.; Liu, F.; Jeftinija, K.; Jeftinija, S.; Haydon, P.G. Glutamate-mediated astrocyte–neuron signalling. Nat. Cell Biol. 1994, 369, 744–747. [Google Scholar] [CrossRef]
- Perea, G.; Navarrete, M.; Araque, A. Tripartite synapses: Astrocytes process and control synaptic information. Trends Neurosci. 2009, 32, 421–431. [Google Scholar] [CrossRef]
- Volterra, A.; Liaudet, N.; Savtchouk, I. Astrocyte Ca2+ signalling: An unexpected complexity. Nat. Rev. Neurosci. 2014, 15, 327–335. [Google Scholar] [CrossRef] [Green Version]
- Hamilton-Whitaker, N.; Attwell, D. Do astrocytes really exocytose neurotransmitters? Nat. Rev. Neurosci. 2010, 11, 227–238. [Google Scholar] [CrossRef] [PubMed]
- Angulo, M.C.; Kozlov, A.S.; Charpak, S.; Audinat, E. Glutamate Released from Glial Cells Synchronizes Neuronal Activity in the Hippocampus. J. Neurosci. 2004, 24, 6920–6927. [Google Scholar] [CrossRef] [Green Version]
- Henneberger, C.; Papouin, T.; Oliet, S.H.R.; Rusakov, D.A. Long-term potentiation depends on release of d-serine from astrocytes. Nature 2010, 463, 232–236. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Serrano, A.; Haddjeri, N.; Lacaille, J.-C.; Robitaille, R. GABAergic Network Activation of Glial Cells Underlies Hippocampal Heterosynaptic Depression. J. Neurosci. 2006, 26, 5370–5382. [Google Scholar] [CrossRef]
- Fiacco, T.A.; McCarthy, K.D. Multiple Lines of Evidence Indicate That Gliotransmission Does Not Occur under Physiological Conditions. J. Neurosci. 2018, 38, 3–13. [Google Scholar] [CrossRef]
- Savtchouk, I.; Volterra, A. Gliotransmission: Beyond Black-and-White. J. Neurosci. 2018, 38, 14–25. [Google Scholar] [CrossRef] [PubMed]
- Sugita, S. Mechanisms of exocytosis. Acta Physiol. 2007, 192, 185–193. [Google Scholar] [CrossRef]
- Thorn, P.; Zorec, R.; Rettig, J.; Keating, D.J. Exocytosis in non-neuronal cells. J. Neurochem. 2016, 137, 849–859. [Google Scholar] [CrossRef] [Green Version]
- Südhof, T.C.; Rizo, J. Synaptic Vesicle Exocytosis. Cold Spring Harb. Perspect. Biol. 2011, 3, a005637. [Google Scholar] [CrossRef]
- Chanaday, N.L.; Cousin, M.A.; Milosevic, I.; Watanabe, S.; Morgan, J.R. The Synaptic Vesicle Cycle Revisited: New Insights into the Modes and Mechanisms. J. Neurosci. 2019, 39, 8209–8216. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bezzi, P.; Gundersen, V.; Galbete, J.L.; Seifert, G.; Steinhäuser, C.; Pilati, E.; Volterra, A. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat. Neurosci. 2004, 7, 613–620. [Google Scholar] [CrossRef]
- Jourdain, P.; Bergersen, L.H.; 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. [Google Scholar] [CrossRef]
- Martineau, M.; Shi, T.; Puyal, J.; Knolhoff, A.; Dulong, J.; Gasnier, B.; Klingauf, J.; Sweedler, J.V.; Jahn, R.; Mothet, J.-P. Storage and uptake of d-serine into astrocytic synaptic-like vesicles specify gliotransmission. J. Neurosci. 2013, 33, 3413–3423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bergersen, L.; Gundersen, V. Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 2009, 158, 260–265. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Prada, I.; Marchaland, J.; Podini, P.; Magrassi, L.; D’Alessandro, R.; Bezzi, P.; Meldolesi, J. REST/NRSF governs the expression of dense-core vesicle gliosecretion in astrocytes. J. Cell Biol. 2011, 193, 537–549. [Google Scholar] [CrossRef]
- Hur, Y.S.; Kim, K.D.; Paek, S.H.; Yoo, S.H. Evidence for the Existence of Secretory Granule (Dense-Core Vesicle)-Based Inositol 1,4,5-Trisphosphate-Dependent Ca2+ Signaling System in Astrocytes. PLoS ONE 2010, 5, e11973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, T.; Sun, L.; Xiong, Y.; Shang, S.; Guo, N.; Teng, S.; Wang, Y.; Liu, B.; Wang, C.; Wang, L.; et al. Calcium Triggers Exocytosis from Two Types of Organelles in a Single Astrocyte. J. Neurosci. 2011, 31, 10593–10601. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef]
- Li, D.; Ropert, N.; Koulakoff, A.; Giaume, C.; Oheim, M. Lysosomes Are the Major Vesicular Compartment Undergoing Ca2+-Regulated Exocytosis from Cortical Astrocytes. J. Neurosci. 2008, 28, 7648–7658. [Google Scholar] [CrossRef] [PubMed]
- Vardjan, N.; Parpura, V.; Verkhratsky, A.; Zorec, R. Gliocrine System: Astroglia as Secretory Cells of the CNS. In Advances in Experimental Medicine and Biology; Springer Science and Business Media LLC: Berlin, Germany, 2019; Volume 1175, pp. 93–115. [Google Scholar]
- Verkhratsky, A.; Matteoli, M.; Parpura, V.; Mothet, J.; Zorec, R. Astrocytes as secretory cells of the central nervous system: Idiosyncrasies of vesicular secretion. EMBO J. 2016, 35, 239–257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bergersen, L.; Morland, C.; Ormel, L.; Rinholm, J.; Larsson, M.; Wold, J.; Røe, Å.T.; Stranna, A.; Santello, M.; Bouvier, D.; et al. Immunogold Detection of l-glutamate and d-serine in Small Synaptic-Like Microvesicles in Adult Hippocampal Astrocytes. Cereb. Cortex 2012, 22, 1690–1697. [Google Scholar] [CrossRef] [Green Version]
- Ormel, L.; Stensrud, M.J.; Bergersen, L.H.; Gundersen, V. VGLUT1 is localized in astrocytic processes in several brain regions. Glia 2012, 60, 229–238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patrushev, I.; Gavrilov, N.; Turlapov, V.; Semyanov, A. Subcellular location of astrocytic calcium stores favors extrasynaptic neuron–astrocyte communication. Cell Calcium 2013, 54, 343–349. [Google Scholar] [CrossRef]
- Stenovec, M.; Kreft, M.; Grilc, S.; Potokar, M.; Kreft, M.E.; Pangršič, T.; Zorec, R. Ca2+-dependent mobility of vesicles capturing anti-VGLUT1 antibodies. Exp. Cell Res. 2007, 313, 3809–3818. [Google Scholar] [CrossRef]
- Hiasa, M.; Miyaji, T.; Haruna, Y.; Takeuchi, T.; Harada, Y.; Moriyama, S.; Yamamoto, A.; Omote, H.; Moriyama, Y. Identification of a mammalian vesicular polyamine transporter. Sci. Rep. 2015, 4, 6836. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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. [Google Scholar] [CrossRef]
- Domercq, M.; Brambilla, L.; Pilati, E.; Marchaland, J.; Volterra, A.; Bezzi, P. P2Y1 Receptor-evoked Glutamate Exocytosis from Astrocytes. J. Biol. Chem. 2006, 281, 30684–30696. [Google Scholar] [CrossRef] [Green Version]
- Montana, V.; Ni, Y.; Sunjara, V.; Hua, X.; Parpura, V. Vesicular Glutamate Transporter-Dependent Glutamate Release from Astrocytes. J. Neurosci. 2004, 24, 2633–2642. [Google Scholar] [CrossRef]
- Zhang, Q.; Pangršič, T.; Kreft, M.; Kržan, 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. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kasymov, V.; Larina, O.; Castaldo, C.; Marina, N.; Patrushev, M.; Kasparov, S.; Gourine, A.V. Differential Sensitivity of Brainstem versus Cortical Astrocytes to Changes in pH Reveals Functional Regional Specialization of Astroglia. J. Neurosci. 2013, 33, 435–441. [Google Scholar] [CrossRef] [Green Version]
- Höltje, M.; Hofmann, F.; Lux, R.; Veh, R.W.; Just, I.; Ahnert-Hilger, G. Glutamate Uptake and Release by Astrocytes Are Enhanced by Clostridium botulinum C3 Protein. J. Biol. Chem. 2008, 283, 9289–9299. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bowser, D.; Khakh, B.S. Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc. Natl. Acad. Sci. USA 2007, 104, 4212–4217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fremeau, R.T.; Burman, J.; Qureshi, T.; Tran, C.H.; Proctor, J.; Johnson, J.; Zhang, H.; Sulzer, D.; Copenhagen, D.R.; Storm-Mathisen, J.; et al. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl. Acad. Sci. USA 2002, 99, 14488–14493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ormel, L.; Stensrud, M.J.; Chaudhry, F.A.; Gundersen, V. A distinct set of synaptic-like microvesicles in atroglial cells contain VGLUT3. Glia 2012, 60, 1289–1300. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Chen, K.; Sloan, S.A.; Bennett, M.L.; Scholze, A.R.; O’Keeffe, S.; Phatnani, H.P.; Guarnieri, P.; Caneda, C.; Ruderisch, N.; et al. An RNA-Sequencing Transcriptome and Splicing Database of Glia, Neurons, and Vascular Cells of the Cerebral Cortex. J. Neurosci. 2014, 34, 11929–11947. [Google Scholar] [CrossRef] [PubMed]
- Chai, H.; Diaz-Castro, B.; Shigetomi, E.; Monte, E.; Octeau, J.C.; Yu, X.; Cohn, W.; Rajendran, P.S.; Vondriska, T.M.; Whitelegge, J.P.; et al. Neural Circuit-Specialized Astrocytes: Transcriptomic, Proteomic, Morphological, and Functional Evidence. Neuron 2017, 95, 531–549.e9. [Google Scholar] [CrossRef] [PubMed]
- Cahoy, J.D.; Emery, B.; Kaushal, A.; Foo, L.C.; Zamanian, J.; Christopherson, K.S.; Xing, Y.; Lubischer, J.; Krieg, P.A.; Krupenko, S.A.; et al. A Transcriptome Database for Astrocytes, Neurons, and Oligodendrocytes: A New Resource for Understanding Brain Development and Function. J. Neurosci. 2008, 28, 264–278. [Google Scholar] [CrossRef] [Green Version]
- Li, D.; Hérault, K.; Silm, K.; Evrard, A.; Wojcik, S.; Oheim, M.; Herzog, E.; Ropert, N. Lack of Evidence for Vesicular Glutamate Transporter Expression in Mouse Astrocytes. J. Neurosci. 2013, 33, 4434–4455. [Google Scholar] [CrossRef] [Green Version]
- Guček, A.; Vardjan, N.; Zorec, R. Exocytosis in Astrocytes: Transmitter Release and Membrane Signal Regulation. Neurochem. Res. 2012, 37, 2351–2363. [Google Scholar] [CrossRef]
- Vardjan, N.; Kreft, M.; Zorec, R. Regulated Exocytosis in Astrocytes is as Slow as the Metabolic Availability of Gliotransmitters: Focus on Glutamate and ATP. Adv. Neurobiol. 2014, 11, 81–101. [Google Scholar]
- El Mestikawy, S.; Mackenzie, Å.; Fortin, G.M.; Descarries, L.; Trudeau, L.-E. From glutamate co-release to vesicular synergy: Vesicular glutamate transporters. Nat. Rev. Neurosci. 2011, 12, 204–216. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. USA 2005, 102, 5606–5611. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolosker, H.; Balu, D.T.; Coyle, J.T. The Rise and Fall of the d -Serine-Mediated Gliotransmission Hypothesis. Trends Neurosci. 2016, 39, 712–721. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Papouin, T.; Henneberger, C.; Rusakov, D.A.; Oliet, S.H. Astroglial versus Neuronal d-Serine: Fact Checking. Trends Neurosci. 2017, 40, 517–520. [Google Scholar] [CrossRef] [Green Version]
- Neame, S.; Safory, H.; Radzishevsky, I.; Touitou, A.; Marchesani, F.; Marchetti, M.; Kellner, S.; Berlin, S.; Foltyn, V.N.; Engelender, S.; et al. The NMDA receptor activation by d-serine and glycine is controlled by an astrocytic Phgdh-dependent serine shuttle. Proc. Natl. Acad. Sci. USA 2019, 116, 20736–20742. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perez, E.J.; Tapanes, S.A.; Loris, Z.B.; Balu, D.; Sick, T.J.; Coyle, J.T.; Liebl, D.J. Enhanced astrocytic d-serine underlies synaptic damage after traumatic brain injury. J. Clin. Investig. 2017, 127, 3114–3125. [Google Scholar] [CrossRef] [PubMed]
- Potokar, M.; Stenovec, M.; Kreft, M.; Kreft, M.E.; Zorec, R. Stimulation inhibits the mobility of recycling peptidergic vesicles in astrocytes. Glia 2007, 56, 135–144. [Google Scholar] [CrossRef] [PubMed]
- Paco, S.; Margelí, M.A.; Olkkonen, V.M.; Imai, A.; Blasi, J.; Aguado, F.; Fischer-Colbrie, R. Regulation of exocytotic protein expression and Ca2+-dependent peptide secretion in astrocytes. J. Neurochem. 2009, 110, 143–156. [Google Scholar] [CrossRef]
- Fischer-Colbrie, R.; Kirchmair, R.; Schobert, A.; Olenik, C.; Meyer, D.K.; Winkler, H. Secretogranin II Is Synthesized and Secreted in Astrocyte Cultures. J. Neurochem. 1993, 60, 2312–2314. [Google Scholar] [CrossRef] [PubMed]
- Paco, S.; Pozas, E.; Aguado, F. Secretogranin III Is an Astrocyte Granin That Is Overexpressed in Reactive Glia. Cereb. Cortex 2009, 20, 1386–1397. [Google Scholar] [CrossRef] [Green Version]
- Zhan, X.; Wen, G.; Jiang, E.; Li, F.; Wu, X.; Pang, H. Secretogranin III upregulation is involved in parkinsonian toxin-mediated astroglia activation. J. Toxicol. Sci. 2020, 45, 271–280. [Google Scholar] [CrossRef]
- Kreft, M.; Stenovec, M.; Rupnik, M.S.; Grilc, S.; Kržan, M.; Potokar, M.; Pangršič, T.; Haydon, P.G.; Zorec, R. Properties of Ca2+-dependent exocytosis in cultured astrocytes. Glia 2004, 46, 437–445. [Google Scholar] [CrossRef]
- Chatterjee, S.; Sikdar, S.K. Corticosterone treatment results in enhanced release of peptidergic vesicles in astrocytes via cytoskeletal rearrangements. Glia 2013, 61, 2050–2062. [Google Scholar] [CrossRef]
- Ramamoorthy, P.; Whim, M.D. Trafficking and Fusion of Neuropeptide Y-Containing Dense-Core Granules in Astrocytes. J. Neurosci. 2008, 28, 13815–13827. [Google Scholar] [CrossRef] [PubMed]
- Guček, A.; Jorgačevski, J.; Singh, P.; Geisler, C.; Lisjak, M.; Vardjan, N.; Kreft, M.; Egner, A.; Zorec, R. Dominant negative SNARE peptides stabilize the fusion pore in a narrow, release-unproductive state. Cell. Mol. Life Sci. 2016, 73, 3719–3731. [Google Scholar] [CrossRef] [PubMed]
- Hong, Y.; Zhao, T.; Li, X.-J.; Li, S. Mutant Huntingtin Impairs BDNF Release from Astrocytes by Disrupting Conversion of Rab3a-GTP into Rab3a-GDP. J. Neurosci. 2016, 36, 8790–8801. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Pangršič, 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. [Google Scholar] [CrossRef] [Green Version]
- Potokar, M.; Kreft, M.; Pangršič, T.; Zorec, R. Vesicle mobility studied in cultured astrocytes. Biochem. Biophys. Res. Commun. 2005, 329, 678–683. [Google Scholar] [CrossRef]
- Potokar, M.; Vardjan, N.; Stenovec, M.; Gabrijel, M.; Trkov, S.; Jorgačevski, J.; Kreft, M.; Zorec, R. Astrocytic Vesicle Mobility in Health and Disease. Int. J. Mol. Sci. 2013, 14, 11238–11258. [Google Scholar] [CrossRef] [Green Version]
- Bowser, D.; Khakh, B.S. Vesicular ATP Is the Predominant Cause of Intercellular Calcium Waves in Astrocytes. J. Gen. Physiol. 2007, 129, 485–491. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hines, D.J.; Haydon, P.G. Astrocytic adenosine: From synapses to psychiatric disorders. Philos. Trans. R. Soc. B Biol. Sci. 2014, 369, 20130594. [Google Scholar] [CrossRef] [Green Version]
- 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. USA 2008, 105, 5683–5686. [Google Scholar] [CrossRef] [Green Version]
- Imura, Y.; Morizawa, Y.; Komatsu, R.; Shibata, K.; Shinozaki, Y.; Kasai, H.; Moriishi, K.; Moriyama, Y.; Koizumi, S. Microglia release ATP by exocytosis. Glia 2013, 61, 1320–1330. [Google Scholar] [CrossRef]
- Oya, M.; Kitaguchi, T.; Yanagihara, Y.; Numano, R.; Kakeyama, M.; Ikematsu, K.; Tsuboi, T. Vesicular nucleotide transporter is involved in ATP storage of secretory lysosomes in astrocytes. Biochem. Biophys. Res. Commun. 2013, 438, 145–151. [Google Scholar] [CrossRef]
- Angelova, P.R.; Iversen, K.Z.; Teschemacher, A.G.; Kasparov, S.; Gourine, A.V.; Abramov, A.Y. Signal transduction in astrocytes: Localization and release of inorganic polyphosphate. Glia 2018, 66, 2126–2136. [Google Scholar] [CrossRef] [Green Version]
- Beckel, J.M.; Gómez, N.M.; Lu, W.; Campagno, K.; Nabet, B.; AlBalawi, F.; Lim, J.C.; Boesze-Battaglia, K.; Mitchell, C.H. Stimulation of TLR3 triggers release of lysosomal ATP in astrocytes and epithelial cells that requires TRPML1 channels. Sci. Rep. 2018, 8, 1–14. [Google Scholar] [CrossRef]
- Lalo, U.; Palygin, O.; Rasooli-Nejad, S.; Andrew, J.; Haydon, P.G.; Pankratov, Y. Exocytosis of ATP From Astrocytes Modulates Phasic and Tonic Inhibition in the Neocortex. PLoS Biol. 2014, 12, e1001747. [Google Scholar] [CrossRef] [PubMed]
- Kinoshita, M.; Hirayama, Y.; Fujishita, K.; Shibata, K.; Shinozaki, Y.; Shigetomi, E.; Takeda, A.; Le, H.P.N.; Hayashi, H.; Hiasa, M.; et al. Anti-Depressant Fluoxetine Reveals its Therapeutic Effect Via Astrocytes. EBioMedicine 2018, 32, 72–83. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Jaiswal, J.K.; Fix, M.; Takano, T.; Nedergaard, M.; Simon, S.M. Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes. Proc. Natl. Acad. Sci. USA 2007, 104, 14151–14156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, L.; Lundkvist, A.; Andersson, D.; Wilhelmsson, U.; Nagai, N.; Pardo, A.; Nodin, C.; Ståhlberg, A.; Aprico, K.; Larsson, K.; et al. Protective Role of Reactive Astrocytes in Brain Ischemia. Br. J. Pharmacol. 2007, 28, 468–481. [Google Scholar] [CrossRef] [Green Version]
- Verderio, C.; Cagnoli, C.; Bergami, M.; Francolini, M.; Schenk, U.; Colombo, A.; Riganti, L.; Frassoni, C.; Zuccaro, E.; Danglot, L.; et al. TI-VAMP/VAMP7 is the SNARE of secretory lysosomes contributing to ATP secretion from astrocytes. Biol. Cell 2012, 104, 213–228. [Google Scholar] [CrossRef]
- Vardjan, N.; Gabrijel, M.; Potokar, M.; Švajger, U.; Kreft, M.; Jeras, M.; de Pablo, Y.; Faiz, M.; Pekny, M.; Zorec, R. IFN-γ-induced increase in the mobility of MHC class II compartments in astrocytes depends on intermediate filaments. J. Neuroinflam. 2012, 9, 144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jaiswal, J.; Andrews, N.; Simon, S.M. Membrane proximal lysosomes are the major vesicles responsible for calcium-dependent exocytosis in nonsecretory cells. J. Cell Biol. 2002, 159, 625–635. [Google Scholar] [CrossRef] [Green Version]
- Soerensen, C.; Novak, I. Visualization of ATP Release in Pancreatic Acini in Response to Cholinergic Stimulus. J. Biol. Chem. 2001, 276, 32925–32932. [Google Scholar] [CrossRef] [Green Version]
- Li, D.; Herault, K.; Oheim, M.; Ropert, N. FM dyes enter via a store-operated calcium channel and modify calcium signaling of cultured astrocytes. Proc. Natl. Acad. Sci. USA 2009, 106, 21960–21965. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Božić, M.; Verkhratsky, A.; Zorec, R.; Stenovec, M. Exocytosis of large-diameter lysosomes mediates interferon γ-induced relocation of MHC class II molecules toward the surface of astrocytes. Cell. Mol. Life Sci. 2019, 77, 3245–3264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Söllner, T.; Bennett, M.K.; Whiteheart, S.; Scheller, R.H.; Rothman, J.E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 1993, 75, 409–418. [Google Scholar] [CrossRef]
- Südhof, T.C. Neurotransmitter release: The last millisecond in the life of a synaptic vesicle. Neuron 2013, 80, 675–690. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aslamy, A.; Thurmond, D.C. Exocytosis proteins as novel targets for diabetes prevention and/or remediation? Am. J. Physiol. Integr. Comp. Physiol. 2017, 312, R739–R752. [Google Scholar] [CrossRef] [Green Version]
- Anlauf, E.; Derouiche, A. Astrocytic exocytosis vesicles and glutamate: A high-resolution immunofluorescence study. Glia 2004, 49, 96–106. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Singh, P.; Jorgačevski, J.; Kreft, M.; Grubišić, V.; Stout, R.; Potokar, M.; Parpura, V.; Zorec, R. Single-vesicle architecture of synaptobrevin2 in astrocytes. Nat. Commun. 2014, 5, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, J.-H.; Kim, J.-H.; Cho, Y.-E.; Baek, M.-C.; Jung, J.-Y.; Lee, M.-G.; Jang, I.-S.; Lee, H.-W.; Suk, K. Chronic Sleep Deprivation-Induced Proteome Changes in Astrocytes of the Rat Hypothalamus. J. Proteome Res. 2014, 13, 4047–4061. [Google Scholar] [CrossRef] [PubMed]
- Bezzi, P.; Carmignoto, P.; Pasti, L.; Vesce, S.; Rossi, D.M.; Rizzini, B.L.; Pozzan, T.; Volterra, A. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nat. Cell Biol. 1998, 391, 281–285. [Google Scholar] [CrossRef]
- Bezzi, P.; Domercq, M.; Brambilla, L.; Galli, R.; Schols, D.; De Clercq, E.; Vescovi, A.; Bagetta, G.; Kollias, G.; Meldolesi, J.; et al. CXCR4-activated astrocyte glutamate release via TNFα: Amplification by microglia triggers neurotoxicity. Nat. Neurosci. 2001, 4, 702–710. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Perea, G.; Araque, A. Astrocytes Potentiate Transmitter Release at Single Hippocampal Synapses. Science 2007, 317, 1083–1086. [Google Scholar] [CrossRef]
- Halassa, M.M.; Florian, C.; Fellin, T.; Munoz, J.R.; Lee, S.-Y.; Abel, T.; Haydon, P.G.; Frank, M.G. Astrocytic Modulation of Sleep Homeostasis and Cognitive Consequences of Sleep Loss. Neuron 2009, 61, 213–219. [Google Scholar] [CrossRef] [Green Version]
- Hines, D.; Haydon, P.G. Inhibition of a SNARE-sensitive pathway in astrocytes attenuates damage following stroke. J. Neurosci. 2013, 33, 4234–4240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sultan, S.; Li, L.; Moss, J.; Petrelli, F.; Cassé, F.; Gebara, E.; Lopatar, J.; Pfrieger, F.; Bezzi, P.; Bischofberger, J.; et al. Synaptic Integration of Adult-Born Hippocampal Neurons Is Locally Controlled by Astrocytes. Neuron 2015, 88, 957–972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sardinha, V.M.; Guerra-Gomes, S.; Caetano, I.; Tavares, G.; Martins, M.; Reis, J.S.; Correia, J.S.; Teixeira-Castro, A.; Pinto, L.; Sousa, N.; et al. Astrocytic signaling supports hippocampal-prefrontal theta synchronization and cognitive function. Glia 2017, 65, 1944–1960. [Google Scholar] [CrossRef] [PubMed]
- Nadjar, A.; Blutstein, T.; Aubert, A.; Laye, S.; Haydon, P.G. Astrocyte-derived adenosine modulates increased sleep pressure during inflammatory response. Glia 2013, 61, 724–731. [Google Scholar] [CrossRef] [PubMed]
- Turner, J.R.; Ecke, L.E.; Briand, L.A.; Haydon, P.G.; Blendy, J.A.; Haydon, P. Cocaine-related behaviors in mice with deficient gliotransmission. Psychopharmacology 2013, 226, 167–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fujita, T.; Chen, M.J.; Li, B.; Smith, N.; Peng, W.; Sun, W.; Toner, M.J.; Kress, B.T.; Wang, L.; Benraiss, A.; et al. Neuronal transgene expression in dominant-negative SNARE mice. J. Neurosci. 2014, 34, 16594–16604. [Google Scholar] [CrossRef] [Green Version]
- Sloan, S.A.; Barres, B.A. Looks Can Be Deceiving: Reconsidering the Evidence for Gliotransmission. Neuron 2014, 84, 1112–1115. [Google Scholar] [CrossRef] [Green Version]
- Petrelli, F.; Bezzi, P. Novel insights into gliotransmitters. Curr. Opin. Pharmacol. 2016, 26, 138–145. [Google Scholar] [CrossRef]
- Ślęzak, M.; Grosche, A.; Niemiec, A.; Tanimoto, N.; Pannicke, T.; Münch, T.; Crocker, B.; Isope, P.; Härtig, W.; Beck, S.C.; et al. Relevance of Exocytotic Glutamate Release from Retinal Glia. Neuron 2012, 74, 504–516. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Jeftinija, S.D.; Jeftinija, K.V.; Stefanović, G. Cultured astrocytes express proteins involved in vesicular glutamate release. Brain Res. 1997, 750, 41–47. [Google Scholar] [CrossRef]
- Schubert, V.; Bouvier, D.; Volterra, A. SNARE protein expression in synaptic terminals and astrocytes in the adult hippocampus: A comparative analysis. Glia 2011, 59, 1472–1488. [Google Scholar] [CrossRef]
- Tao-Cheng, J.-H.; Pham, A.; Yang, Y.; Winters, C.; Gallant, P.; Reese, T. Syntaxin 4 is concentrated on plasma membrane of astrocytes. Neuroscience 2015, 286, 264–271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hepp, R.; Perraut, M.; Chasserot-Golaz, S.; Galli, T.; Aunis, D.; Langley, K.; Grant, N.J. Cultured glial cells express the SNAP-25 analogue SNAP-23. Glia 1999, 27, 181–187. [Google Scholar] [CrossRef]
- Malarkey, E.B.; Parpura, V. Temporal characteristics of vesicular fusion in astrocytes: Examination of synaptobrevin 2-laden vesicles at single vesicle resolution. J. Physiol. 2011, 589, 4271–4300. [Google Scholar] [CrossRef] [Green Version]
- Smithers, N.P.; Hodgkinson, C.P.; Cuttle, M.; Sale, G.J. Insulin-triggered repositioning of munc18c on syntaxin-4 in GLUT4 signalling. Biochem. J. 2008, 410, 255–260. [Google Scholar] [CrossRef]
- Predescu, S.; Predescu, D.N.; Shimizu, K.; Klein, I.K.; Malik, A.B. Cholesterol-dependent Syntaxin-4 and SNAP-23 Clustering Regulates Caveolar Fusion with the Endothelial Plasma Membrane. J. Biol. Chem. 2005, 280, 37130–37138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brandie, F.M.; Aran, V.; Verma, A.; McNew, J.A.; Bryant, N.J.; Gould, G. Negative Regulation of Syntaxin4/SNAP-23/VAMP2-Mediated Membrane Fusion by Munc18c In Vitro. PLoS ONE 2008, 3, e4074. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Voets, T.; Toonen, R.F.; Brian, E.C.; de Wit, H.; Moser, T.; Rettig, J.; Südhof, T.C.; Neher, E.; Verhage, M. Munc18-1 Promotes Large Dense-Core Vesicle Docking. Neuron 2001, 31, 581–592. [Google Scholar] [CrossRef] [Green Version]
- Oh, E.; Kalwat, M.; Kim, M.-J.; Verhage, M.; Thurmond, D.C. Munc18-1 Regulates First-phase Insulin Release by Promoting Granule Docking to Multiple Syntaxin Isoforms. J. Biol. Chem. 2012, 287, 25821–25833. [Google Scholar] [CrossRef] [Green Version]
- Motoike, T.; Sano, K.; Nakamura, H.; Takai, Y. Expression of smg p25A/rab 3A guanine nucleotide dissociation inhibitor (GDI) in neurons and glial cells from rat brain. Neurosci. Lett. 1993, 156, 87–90. [Google Scholar] [CrossRef]
- Madison, D.; Krüger, W.; Kim, T.; Pfeiffer, S. Differential expression of rab3 isoforms in oligodendrocytes and astrocytes. J. Neurosci. Res. 1996, 45, 258–268. [Google Scholar] [CrossRef]
- Bonet-Ponce, L.; Beilina, A.; Williamson, C.D.; Lindberg, E.; Kluss, J.H.; Saez-Atienzar, S.; Landeck, N.; Kumaran, R.; Mamais, A.; Bleck, C.K.E.; et al. LRRK2 mediates tubulation and vesicle sorting from lysosomes. Sci. Adv. 2020, 6, eabb2454. [Google Scholar] [CrossRef]
- Südhof, T.C. The Presynaptic Active Zone. Neuron 2012, 75, 11–25. [Google Scholar] [CrossRef] [Green Version]
- Mungenast, A.E. Diacylglycerol Signaling Underlies Astrocytic ATP Release. Neural Plast. 2011, 2011. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bohmbach, K.; Schwarz, M.K.; Schoch, S.; Henneberger, C. The structural and functional evidence for vesicular release from astrocytes in situ. Brain Res. Bull. 2018, 136, 65–75. [Google Scholar] [CrossRef]
- Buscemi, L.; Ginet, V.; Lopatar, J.; Montana, V.; Pucci, L.; Spagnuolo, P.; Zehnder, T.; Grubišić, V.; Truttman, A.; Sala, C.; et al. Homer1 Scaffold Proteins Govern Ca2+ Dynamics in Normal and Reactive Astrocytes. Cereb. Cortex 2017, 27, 2365–2384. [Google Scholar] [CrossRef] [Green Version]
- Paquet, M.; Ribeiro, F.M.; Guadagno, J.; Esseltine, J.L.; Ferguson, S.S.; Cregan, S.P. Role of metabotropic glutamate receptor 5 signaling and homer in oxygen glucose deprivation-mediated astrocyte apoptosis. Mol. Brain 2013, 6, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foa, L.; Gasperini, R. Developmental roles for Homer: More than just a pretty scaffold. J. Neurochem. 2009, 108. [Google Scholar] [CrossRef]
- Kennedy, M.J.; Ehlers, M.D. Mechanisms and Function of Dendritic Exocytosis. Neuron 2011, 69, 856–875. [Google Scholar] [CrossRef] [Green Version]
- Perin, M.S.; Fried, V.A.; Mignery, G.A.; Jahn, R.; Südhof, T.C. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nat. Cell Biol. 1990, 345, 260–263. [Google Scholar] [CrossRef] [PubMed]
- Südhof, T.C. Calcium Control of Neurotransmitter Release. Cold Spring Harb. Perspect. Biol. 2011, 4, a011353. [Google Scholar] [CrossRef]
- Mittelsteadt, T.; Seifert, G.; Alvárez-Barón, E.; Steinhäuser, C.; Becker, A.J.; Schoch, S. Differential mRNA expression patterns of the synaptotagmin gene family in the rodent brain. J. Comp. Neurol. 2009, 512, 514–528. [Google Scholar] [CrossRef]
- Zhang, Q.; Fukuda, M.; Van Bockstaele, E.; Pascual, O.; Haydon, P.G. Synaptotagmin IV regulates glial glutamate release. Proc. Natl. Acad. Sci. USA 2004, 101, 9441–9446. [Google Scholar] [CrossRef] [Green Version]
- Schonn, J.-S.; Maximov, A.; Lao, Y.; Sudhof, T.C.; Sorensen, J.B. Synaptotagmin-1 and -7 are functionally overlapping Ca2+ sensors for exocytosis in adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA 2008, 105, 3998–4003. [Google Scholar] [CrossRef] [Green Version]
- Gustavsson, N.; Lao, Y.; Maximov, A.; Chuang, J.-C.; Kostromina, E.; Repa, J.; Li, C.; Radda, G.K.; Südhof, T.C.; Han, W. Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc. Natl. Acad. Sci. USA 2008, 105, 3992–3997. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gustavsson, N.; Wei, S.-H.; Hoang, D.N.; Lao, Y.; Zhang, Q.; Radda, G.K.; Rorsman, P.; Südhof, T.C.; Han, W. Synaptotagmin-7 is a principal Ca2+sensor for Ca2+-induced glucagon exocytosis in pancreas. J. Physiol. 2009, 587, 1169–1178. [Google Scholar] [CrossRef]
- Martinez, I.; Chakrabarti, S.; Hellevik, T.; Morehead, J.; Fowler, K.; Andrews, N.W. Synaptotagmin VII Regulates Ca2+-Dependent Exocytosis of Lysosomes in Fibroblasts. J. Cell Biol. 2000, 148, 1141–1150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, F.; Bacaj, T.; Südhof, T.C. Synaptotagmin-7 Is Essential for Ca2+-Triggered Delayed Asynchronous Release But Not for Ca2+-Dependent Vesicle Priming in Retinal Ribbon Synapses. J. Neurosci. 2015, 35, 11024–11033. [Google Scholar] [CrossRef]
- Sreetama, S.C.; Takano, T.; Nedergaard, M.; Simon, S.; Jaiswal, J.K. Injured astrocytes are repaired by Synaptotagmin XI-regulated lysosome exocytosis. Cell Death Differ. 2015, 23, 596–607. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oh, S.-J.; Han, K.-S.; Park, H.; Woo, D.H.; Kim, H.Y.; Traynelis, S.F.; Lee, C.J. Protease activated receptor 1-induced glutamate release in cultured astrocytes is mediated by Bestrophin-1 channel but not by vesicular exocytosis. Mol. Brain 2012, 5, 38. [Google Scholar] [CrossRef] [Green Version]
- Stenovec, M.; Lasič, E.; Božić, M.; Bobnar, S.T.; Stout, R.F.; Grubišić, V.; Parpura, V.; Zorec, R. Ketamine Inhibits ATP-Evoked Exocytotic Release of Brain-Derived Neurotrophic Factor from Vesicles in Cultured Rat Astrocytes. Mol. Neurobiol. 2016, 53, 6882–6896. [Google Scholar] [CrossRef]
- Dai, H.; Shin, O.-H.; Machius, M.; Tomchick, D.; Südhof, T.C.; Rizo, J. Structural basis for the evolutionary inactivation of Ca2+ binding to synaptotagmin 4. Nat. Struct. Mol. Biol. 2004, 11, 844–849. [Google Scholar] [CrossRef]
- Rusakov, D. Disentangling calcium-driven astrocyte physiology. Nat. Rev. Neurosci. 2015, 16, 226–233. [Google Scholar] [CrossRef] [PubMed]
- Hazell, A.S.; Wang, N. Identification of complexin II in astrocytes: A possible regulator of glutamate release in these cells. Biochem. Biophys. Res. Commun. 2011, 404, 228–232. [Google Scholar] [CrossRef]
- Wang, Z.; Wei, X.; Liu, K.; Zhang, X.; Yang, F.; Zhang, H.; He, Y.; Zhu, T.; Li, F.; Shi, W.; et al. NOX2 deficiency ameliorates cerebral injury through reduction of complexin II-mediated glutamate excitotoxicity in experimental stroke. Free. Radic. Biol. Med. 2013, 65, 942–951. [Google Scholar] [CrossRef] [PubMed]
- Burgoyne, R.D.; Handel, S.E. Activation of exocytosis by GTP analogues in adrenal chromaffin cells revealed by patch-clamp capacitance measurement. FEBS Lett. 1994, 344, 139–142. [Google Scholar] [CrossRef] [Green Version]
- Fernandez, J.M.; Neher, E.; Gomperts, B.D. Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nat. Cell Biol. 1984, 312, 453–455. [Google Scholar] [CrossRef]
- Regazzi, R.; Li, G.; Ullrich, S.; Jaggi, C.; Wollheim, C.B. Different requirements for protein kinase C activation and Ca2+-independent insulin secretion in response to guanine nucleotides. J. Biol. Chem. 1989, 264, 9939–9944. [Google Scholar] [CrossRef]
- Li, G.; Han, L.; Chou, T.-C.; Fujita, Y.; Arunachalam, L.; Xu, A.; Wong, A.; Chiew, S.-K.; Wan, Q.; Wang, L.; et al. RalA and RalB Function as the Critical GTP Sensors for GTP-Dependent Exocytosis. J. Neurosci. 2007, 27, 190–202. [Google Scholar] [CrossRef] [Green Version]
- Wu, B.; Guo, W. The Exocyst at a Glance. J. Cell Sci. 2015, 128, 2957–2964. [Google Scholar] [CrossRef] [Green Version]
- Rivera-Molina, F.; Toomre, D. Live-cell imaging of exocyst links its spatiotemporal dynamics to various stages of vesicle fusion. J. Cell Biol. 2013, 201, 673–680. [Google Scholar] [CrossRef] [Green Version]
- Zorec, R.; Verkhratsky, A.; Rodríguez, J.; Parpura, V. Astrocytic vesicles and gliotransmitters: Slowness of vesicular release and synaptobrevin2-laden vesicle nanoarchitecture. Neuroscience 2016, 323, 67–75. [Google Scholar] [CrossRef]
- Lepore, D.; Martínez-Núñez, L.; Munson, M. Exposing the Elusive Exocyst Structure. Trends Biochem. Sci. 2018, 43, 714–725. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Zuo, X.; Yue, P.; Guo, W. Phosphatidylinositol 4,5-Bisphosphate Mediates the Targeting of the Exocyst to the Plasma Membrane for Exocytosis in Mammalian Cells. Mol. Biol. Cell 2007, 18, 4483–4492. [Google Scholar] [CrossRef] [Green Version]
- Morgera, F.; Sallah, M.R.; Dubuke, M.L.; Gandhi, P.; Brewer, D.N.; Carr, C.M.; Munson, M. Regulation of exocytosis by the exocyst subunit Sec6 and the SM protein Sec1. Mol. Biol. Cell 2012, 23, 337–346. [Google Scholar] [CrossRef] [PubMed]
- Moulson, A.J.; Squair, J.W.; Franklin, R.J.M.; Tetzlaff, W.; Assinck, P. Diversity of Reactive Astrogliosis in CNS Pathology: Heterogeneity or Plasticity? Front. Cell. Neurosci. 2021. [Google Scholar] [CrossRef] [PubMed]
- Nosi, D.; Lana, D.; Giovannini, M.; Delfino, G.; Zecchi-Orlandini, S. Neuroinflammation: Integrated Nervous Tissue Response through Intercellular Interactions at the “Whole System” Scale. Cells 2021, 10, 1195. [Google Scholar] [CrossRef]
- Escartin, C.; Galea, E.; Lakatos, A.; O’Callaghan, J.P.; Petzold, G.C.; Serrano-Pozo, A.; Steinhäuser, C.; Volterra, A.; Carmignoto, G.; Agarwal, A.; et al. Reactive astrocyte nomenclature, definitions, and future directions. Nat. Neurosci. 2021, 24, 312–325. [Google Scholar] [CrossRef]
- Liddelow, S.A.; Guttenplan, K.A.; Clarke, L.E.; Bennett, F.C.; Bohlen, C.J.; Schirmer, L.; Bennett, M.L.; Münch, A.E.; Chung, W.S.; Petersong, T.C.; et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 2017, 541, 481–487. [Google Scholar] [CrossRef] [PubMed]
- Liddelow, S.A.; Barres, B.A. Reactive Astrocytes: Production, Function, and Therapeutic Potential. Immunity 2017, 46, 957–967. [Google Scholar] [CrossRef] [Green Version]
- Peng, H.; Erdmann, N.; Whitney, N.; Dou, H.; Gorantla, S.; Gendelman, H.E.; Ghorpade, A.; Zheng, J. HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1β. Glia 2006, 54, 619–629. [Google Scholar] [CrossRef] [Green Version]
- Zheng, J.C.; Huang, Y.; Tang, K.; Cui, M.; Niemann, D.; Lopez, A.; Morgello, S.; Chen, S. HIV-1-infected and/or immune-activated macrophages regulate astrocyte CXCL8 production through IL-1β and TNF-α: Involvement of mitogen-activated protein kinases and protein kinase R. J. Neuroimmunol. 2008, 200, 100–110. [Google Scholar] [CrossRef] [Green Version]
- Álvarez, S.; Blanco, A.; Fresno, M.; Muñoz-Fernández, M. Ángeles Nuclear factor-κB activation regulates cyclooxygenase-2 induction in human astrocytes in response to CXCL12: Role in neuronal toxicity. J. Neurochem. 2010, 113, 772–783. [Google Scholar] [CrossRef]
- Lau, L.T.; Yu, A.C.-H. Astrocytes Produce and Release Interleukin-1, Interleukin-6, Tumor Necrosis Factor Alpha and Interferon-Gamma Following Traumatic and Metabolic Injury. J. Neurotrauma 2001, 18, 351–359. [Google Scholar] [CrossRef] [PubMed]
- Verhoog, Q.P.; Holtman, L.; Aronica, E.; Van Vliet, E.A. Astrocytes as Guardians of Neuronal Excitability: Mechanisms Underlying Epileptogenesis. Front. Neurol. 2020, 11, 11. [Google Scholar] [CrossRef] [PubMed]
- Agulhon, C.; Sun, M.-Y.; Murphy, T.; Myers, T.; Lauderdale, K.; Fiacco, T.A. Calcium Signaling and Gliotransmission in Normal vs. Reactive Astrocytes. Front. Pharmacol. 2012, 3, 139. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Santello, M.; Bezzi, P.; Volterra, A. TNFα Controls Glutamatergic Gliotransmission in the Hippocampal Dentate Gyrus. Neuron 2011, 69, 988–1001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takata-Tsuji, F.; Chounlamountri, N.; Do, L.; Philippot, C.; Ducassou, J.N.; Couté, Y.; Ben Achour, S.; Honnorat, J.; Place, C.; Pascual, O. Microglia modulate gliotransmission through the regulation of VAMP2 proteins in astrocytes. Glia 2021, 69, 61–72. [Google Scholar] [CrossRef]
- Calì, 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. [Google Scholar] [CrossRef]
- Canedo, T.; Portugal, C.C.; Socodato, R.; Almeida, T.O.; Terceiro, A.F.; Bravo, J.; Silva, A.I.; Magalhães, J.D.; Guerra-Gomes, S.; Oliveira, J.F.; et al. Astrocyte-derived TNF and glutamate critically modulate microglia activation by methamphetamine. Neuropsychopharmacology 2021. [Google Scholar] [CrossRef]
- Habbas, S.; Santello, M.; Becker, D.; Stubbe, H.; Zappia, G.; Liaudet, N.; Klaus, F.; Kollias, G.; Fontana, A.; Pryce, C.R.; et al. Neuroinflammatory TNFα Impairs Memory via Astrocyte Signaling. Cell 2015, 163, 1730–1741. [Google Scholar] [CrossRef] [Green Version]
- Gourine, A.V.; Kasymov, V.; Marina, N.; Tang, F.; Figueiredo, M.F.; Lane, S.; Teschemacher, A.G.; Spyer, K.M.; Deisseroth, K.; Kasparov, S. Astrocytes Control Breathing Through pH-Dependent Release of ATP. Science 2010, 329, 571–575. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Angelova, P.R.; Kasymov, V.; Christie, I.; Sheikhbahaei, S.; Turovsky, E.; Marina, N.; Korsak, A.; Zwicker, J.D.; Teschemacher, A.G.; Ackland, G.L.; et al. Functional Oxygen Sensitivity of Astrocytes. J. Neurosci. 2015, 35, 10460–10473. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marina, N.; Turovsky, E.; Christie, I.N.; Hosford, P.; Hadjihambi, A.; Korsak, A.; Ang, R.; Mastitskaya, S.; Sheikhbahaei, S.; Theparambil, S.M.; et al. Brain metabolic sensing and metabolic signaling at the level of an astrocyte. Glia 2018, 66, 1185–1199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Byts, N.; Sharma, S.; Laurila, J.; Paudel, P.; Miinalainen, I.; Ronkainen, V.-P.; Hinttala, R.; Törnquist, K.; Koivunen, P.; Myllyharju, J. Transmembrane Prolyl 4-Hydroxylase is a Novel Regulator of Calcium Signaling in Astrocytes. Eneuro 2021, 8, 1–23. [Google Scholar] [CrossRef] [PubMed]
- Gaidin, S.G.; Turovskaya, M.V.; Mal’Tseva, V.N.; Zinchenko, V.P.; Blinova, E.; Turovsky, E.A. A Complex Neuroprotective Effect of Alpha-2-Adrenergic Receptor Agonists in a Model of Cerebral Ischemia–Reoxygenation In Vitro. Biochem. (Moscow) Suppl. Ser. A Membr. Cell Biol. 2019, 13, 319–333. [Google Scholar] [CrossRef]
- Lian, H.; Yang, L.; Cole, A.; Sun, L.; Chiang, A.C.-A.; Fowler, S.W.; Shim, D.J.; Rodriguez-Rivera, J.; Taglialatela, G.; Jankowsky, J.L.; et al. NFκB-Activated Astroglial Release of Complement C3 Compromises Neuronal Morphology and Function Associated with Alzheimer’s Disease. Neuron 2015, 85, 101–115. [Google Scholar] [CrossRef] [Green Version]
- Stephan, A.H.; Barres, B.A.; Stevens, B. The Complement System: An Unexpected Role in Synaptic Pruning During Development and Disease. Annu. Rev. Neurosci. 2012, 35, 369–389. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stevens, B.; Allen, N.J.; Vazquez, L.E.; Howell, G.R.; Christopherson, K.S.; Nouri, N.; Micheva, K.; Mehalow, A.; Huberman, A.D.; Stafford, B.; et al. The Classical Complement Cascade Mediates CNS Synapse Elimination. Cell 2007, 131, 1164–1178. [Google Scholar] [CrossRef] [Green Version]
Secretory Organelle | Diameter | Cargo | Associated Proteins | |
---|---|---|---|---|
Protein Name | Gene Name | |||
Synaptic-Like Microvesicles (SLMVs) | 30–100 nm | Glutamate d-serine | VGluT1 VGlut2 VGlut3 VAMP2 (synaptobrevin 2) VAMP3 (cellubrevin) Rab3a V-ATPase | Slc17a7 Slc17a6 Slc17a8 Vamp2 Vamp3 Rab3a Atp6v0, Atp6v1 1 |
Dense-Core Vesicles (DCV) | 100–600 nm | ANP ATP BDNF Secretogranin II Secretogranin III Chromogranin NPY | VAMP2 (synaptobrevin 2) VAMP3 (cellubrevin) VNuT | Vamp2 Vamp3 Slc17a9 |
Secretory Lysosome (SL) | 300–500 nm | ATP Cathepsin B Cathepsin D Proteolytic enzymes | VAMP7 (TI-VAMP) Rab7 CD63 LAMP1 Sialin VNuT | Vamp7 Rab7a Cd63 Lamp1 Slc17a5 Slc17a9 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mielnicka, A.; Michaluk, P. Exocytosis in Astrocytes. Biomolecules 2021, 11, 1367. https://doi.org/10.3390/biom11091367
Mielnicka A, Michaluk P. Exocytosis in Astrocytes. Biomolecules. 2021; 11(9):1367. https://doi.org/10.3390/biom11091367
Chicago/Turabian StyleMielnicka, Aleksandra, and Piotr Michaluk. 2021. "Exocytosis in Astrocytes" Biomolecules 11, no. 9: 1367. https://doi.org/10.3390/biom11091367