Optogenetic and chemogenetic modulation of astroglial secretory phenotype
-
Alla B. Salmina
Abstract
Astrocytes play a major role in brain function and alterations in astrocyte function that contribute to the pathogenesis of many brain disorders. The astrocytes are attractive cellular targets for neuroprotection and brain tissue regeneration. Development of novel approaches to monitor and to control astroglial function is of great importance for further progress in basic neurobiology and in clinical neurology, as well as psychiatry. Recently developed advanced optogenetic and chemogenetic techniques enable precise stimulation of astrocytes in vitro and in vivo, which can be achieved by the expression of light-sensitive channels and receptors, or by expression of receptors exclusively activated by designer drugs. Optogenetic stimulation of astrocytes leads to dramatic changes in intracellular calcium concentrations and causes the release of gliotransmitters. Optogenetic and chemogenetic protocols for astrocyte activation aid in extracting novel information regarding the function of brain’s neurovascular unit. This review summarizes current data obtained by this approach and discusses a potential mechanistic connection between astrocyte stimulation and changes in brain physiology.
Funding source: Russian Science Foundation
Award Identifier / Grant number: 20-65-46004
Acknowledgement
The authors thank A. Olsen for English language editing.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: The work is supported by a grant from the Russian Science Foundation 20-65-46004 (to A.B.S., Y.V.G., A.I.E., P.M.B., I.B.B., O.L.V.).
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Abbink, M.R., van Deijk, A.-L.F., Heine, V.M., Verheijen, M.H., and Korosi, A. (2019). The involvement of astrocytes in early-life adversity induced programming of the brain. Glia 67: 1637–1653.10.1002/glia.23625Search in Google Scholar PubMed PubMed Central
Acosta-Ruiz, A., Gutzeit, V.A., Skelly, M.J., Meadows, S., Lee, J., Parekh, P., Orr, A.G., Liston, C., Pleil, K.E., Broichhagen, J., et al.. (2020). Branched photoswitchable tethered ligands enable ultra-efficient optical control and detection of G protein-coupled receptors in vivo. Neuron 105: 446–463, e413.10.1016/j.neuron.2019.10.036Search in Google Scholar PubMed PubMed Central
Adamsky, A. and Goshen, I. (2018). Astrocytes in memory function: pioneering findings and future directions. Neuroscience 370: 14–26.10.1016/j.neuroscience.2017.05.033Search in Google Scholar PubMed
Adamsky, A., Kol, A., Kreisel, T., Doron, A., Ozeri-Engelhard, N., Melcer, T., Refaeli, R., Horn, H., Regev, L., Groysman, M., et al.. (2018b). Astrocytic activation generates de novo neuronal potentiation and memory enhancement. Cell 174: 59–71, e14.10.1016/j.cell.2018.05.002Search in Google Scholar PubMed
Allen, N.J. and Eroglu, C. (2017). Cell biology of astrocyte-synapse interactions. Neuron 96: 697–708.10.1016/j.neuron.2017.09.056Search in Google Scholar PubMed PubMed Central
Araque, A., Li, N., Doyle, R.T., and Haydon, P.G. (2000). SNARE protein-dependent glutamate release from astrocytes. J. Neurosci. 20: 666–673.10.1523/JNEUROSCI.20-02-00666.2000Search in Google Scholar
Asano, T., Igarashi, H., Ishizuka, T., and Yawo, H. (2018). Organelle optogenetics: direct manipulation of intracellular Ca2+ dynamics by light. Front. Neurosci. 12.10.3389/fnins.2018.00561Search in Google Scholar PubMed PubMed Central
Bang, J., Kim, H.Y., and Lee, H. (2016). Optogenetic and chemogenetic approaches for studying astrocytes and gliotransmitters. Exp. Neurobiol. 25: 205–221.10.5607/en.2016.25.5.205Search in Google Scholar PubMed PubMed Central
Barros, L.F. and Weber, B. (2018). CrossTalk proposal: an important astrocyte-to-neuron lactate shuttle couples neuronal activity to glucose utilisation in the brain. J. Physiol. 596: 347–350.10.1113/JP274944Search in Google Scholar PubMed PubMed Central
Beck, S., Yu-Strzelczyk, J., Pauls, D., Constantin, O.M., Gee, C.E., Ehmann, N., Kittel, R.J., Nagel, G., and Gao, S. (2018). Synthetic light-activated ion channels for optogenetic activation and inhibition. Front. Neurosci. 12.10.3389/fnins.2018.00643Search in Google Scholar PubMed PubMed Central
Bélanger, M., Allaman, I., and Magistretti, P.J. (2011). Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14: 724–738.10.1016/j.cmet.2011.08.016Search in Google Scholar PubMed
Bellot-Saez, A., Kékesi, O., Morley, J.W., and Buskila, Y. (2017). Astrocytic modulation of neuronal excitability through K+ spatial buffering. Neurosci. Biobehav. Rev. 77: 87–97.10.1016/j.neubiorev.2017.03.002Search in Google Scholar PubMed
Boitsova, E.B., Morgun, A.V., Osipova, E.D., Pozhilenkova, E.A., Martinova, G.P., Frolova, O.V., Olovannikova, R.Y., Tohidpour, A., Gorina, Y.V., Panina, Y.A., et al.. (2018). The inhibitory effect of LPS on the expression of GPR81 lactate receptor in blood-brain barrier model in vitro. J. Neuroinflammation 15: 196.10.1186/s12974-018-1233-2Search in Google Scholar PubMed PubMed Central
Brambilla, L., Martorana, F., and Rossi, D. (2013). Astrocyte signaling and neurodegeneration: new insights into CNS disorders. Prion 7: 28–36.10.4161/pri.22512Search in Google Scholar PubMed PubMed Central
Breslin, K., Wade, J.J., Wong-Lin, K., Harkin, J., Flanagan, B., Van Zalinge, H., Hall, S., Walker, M., Verkhratsky, A., and McDaid, L. (2018). Potassium and sodium microdomains in thin astroglial processes: a computational model study. PLoS Comput. Biol. 14: e1006151.10.1371/journal.pcbi.1006151Search in Google Scholar PubMed PubMed Central
Brockett, A.T., Kane, G.A., Monari, P.K., Briones, B.A., Vigneron, P.-A., Barber, G.A., Bermudez, A., Dieffenbach, U., Kloth, A.D., Buschman, T.J., et al.. (2018). Evidence supporting a role for astrocytes in the regulation of cognitive flexibility and neuronal oscillations through the Ca2+ binding protein S100β. PLoS One 13: e0195726.10.1371/journal.pone.0195726Search in Google Scholar PubMed PubMed Central
Bronzuoli, M.R., Facchinetti, R., Steardo, L.Jr., Romano, A., Stecca, C., Passarella, S., Steardo, L., Cassano, T., and Scuderi, C. (2018). Palmitoylethanolamide dampens reactive astrogliosis and improves neuronal trophic support in a triple transgenic model of Alzheimer’s disease: in vitro and in vivo evidence. Oxid. Med. Cell Longev.: 4720532.10.1155/2018/4720532Search in Google Scholar PubMed PubMed Central
Bull, C., Freitas, K.C.C., Zou, S., Poland, R.S., Syed, W.A., Urban, D.J., Minter, S.C., Shelton, K.L., Hauser, K.F., Negus, S.S., et al.. (2014). Rat nucleus accumbens core astrocytes modulate reward and the motivation to self-administer ethanol after abstinence. Neuropsychopharmacology 39: 2835–2845.10.1038/npp.2014.135Search in Google Scholar PubMed PubMed Central
Capecchi, P.L., Pasini, F.L., Quartarolo, E., and Perri, T.D. (1997). Carnitines increase plasma levels of adenosine and ATP in humans. Vasc. Med. 2: 77–81.10.1177/1358863X9700200201Search in Google Scholar PubMed
Cardozo, T., Shmelkov, E., Felsovalyi, K., Swetnam, J., Butler, T., Malaspina, D., and Shmelkov, S.V. (2017). Chemistry-based molecular signature underlying the atypia of clozapine. Transl. Psychiatry 7: e1036.10.1038/tp.2017.6Search in Google Scholar PubMed PubMed Central
Cavaccini, A., Durkee, C., Kofuji, P., Tonini, R., and Araque, A. (2020). Astrocyte signaling gates long-term depression at corticostriatal synapses of the direct pathway. J. Neurosci JN-RM-2369-2319.10.1523/JNEUROSCI.2369-19.2020Search in Google Scholar PubMed PubMed Central
Cheli, V.T., Santiago González, D.A., Smith, J., Spreuer, V., Murphy, G.G., and Paez, P.M. (2016). L-type voltage-operated calcium channels contribute to astrocyte activation in vitro. Glia 64: 1396–1415.10.1002/glia.23013Search in Google Scholar PubMed PubMed Central
Chen, L.-F., Lin, Y.T., Gallegos, D.A., Hazlett, M.F., Gómez-Schiavon, M., Yang, M.G., Kalmeta, B., Zhou, A.S., Holtzman, L., Gersbach, C.A., et al.. (2019). Enhancer histone acetylation modulates transcriptional bursting dynamics of neuronal activity-inducible genes. Cell Rep. 26: 1174–1188, e1175.10.1016/j.celrep.2019.01.032Search in Google Scholar PubMed PubMed Central
Chen, X.-S., Huang, N., Michael, N., and Xiao, L. (2015). Advancements in the underlying pathogenesis of schizophrenia: implications of DNA methylation in glial cells. Front. Cell. Neurosci. 9: 451.10.3389/fncel.2015.00451Search in Google Scholar PubMed PubMed Central
Chiechio, S., Canonico, P.L., and Grilli, M. (2017). l-Acetylcarnitine: a mechanistically distinctive and potentially rapid-acting antidepressant drug. Int. J. Mol. Sci. 19: 11.10.3390/ijms19010011Search in Google Scholar PubMed PubMed Central
Chisolm, D.A. and Weinmann, A.S. (2018). Connections between metabolism and epigenetics in programming cellular differentiation. Annu. Rev. Immunol. 36: 221–246.10.1146/annurev-immunol-042617-053127Search in Google Scholar PubMed
Cho, W.-H., Barcelon, E., and Lee, S.J. (2016). Optogenetic glia manipulation: possibilities and future prospects. Exp. Neurobiol. 25: 197–204.10.5607/en.2016.25.5.197Search in Google Scholar PubMed PubMed Central
Choi, S.S., Lee, H.J., Lim, I., Satoh, J.-I., and Kim, S.U. (2014). Human astrocytes: secretome profiles of cytokines and chemokines. PLoS One 9: e92325.10.1371/journal.pone.0092325Search in Google Scholar PubMed PubMed Central
Corkrum, M., Covelo, A., Lines, J., Bellocchio, L., Pisansky, M., Loke, K., Quintana, R., Rothwell, P.E., Lujan, R., Marsicano, G., et al.. (2020). Dopamine-evoked synaptic regulation in the nucleus accumbens requires astrocyte activity. Neuron 105: 1036–1047, e1035.10.1016/j.neuron.2019.12.026Search in Google Scholar PubMed PubMed Central
Cosentino, C., Alberio, L., Gazzarrini, S., Aquila, M., Romano, E., Cermenati, S., Zuccolini, P., Petersen, J., Beltrame, M., Van Etten, J.L., et al.. (2015). Optogenetics. Engineering of a light-gated potassium channel. Science 348: 707–710.10.1126/science.aaa2787Search in Google Scholar PubMed
Davila, D., Thibault, K., Fiacco, T.A., and Agulhon, C. (2013). Recent molecular approaches to understanding astrocyte function in vivo. Front. Cell. Neurosci. 7: 272.10.3389/fncel.2013.00272Search in Google Scholar PubMed PubMed Central
De Bock, M., Decrock, E., Wang, N., Bol, M., Vinken, M., Bultynck, G., and Leybaert, L. (2014). The dual face of connexin-based astroglial Ca2+ communication: a key player in brain physiology and a prime target in pathology. Biochim. Biophys. Acta Mol. Cell Res. 1843: 2211–2232.10.1016/j.bbamcr.2014.04.016Search in Google Scholar PubMed
de Castro Abrantes, H., Briquet, M., Schmuziger, C., Restivo, L., Puyal, J., Rosenberg, N., Rocher, A.-B., Offermanns, S., and Chatton, J.-Y. (2019). The lactate receptor HCAR1 modulates neuronal network activity through the activation of Gα and Gβγ subunits. J. Neurosci. 39: 4422–4433.10.1523/JNEUROSCI.2092-18.2019Search in Google Scholar PubMed PubMed Central
Deemyad, T., Lüthi, J., and Spruston, N. (2018). Astrocytes integrate and drive action potential firing in inhibitory subnetworks. Nat. Commun. 9: 4336.10.1038/s41467-018-06338-3Search in Google Scholar PubMed PubMed Central
Denizot, A., Arizono, M., Nägerl, U.V., Soula, H., and Berry, H. (2019). Simulation of calcium signaling in fine astrocytic processes: effect of spatial properties on spontaneous activity. PLoS Comput. Biol. 15: e1006795.10.1371/journal.pcbi.1006795Search in Google Scholar PubMed PubMed Central
Descalzi, G., Gao, V., Steinman, M.Q., Suzuki, A., and Alberini, C.M. (2019). Lactate from astrocytes fuels learning-induced mRNA translation in excitatory and inhibitory neurons. Commun. Biol. 2: 247.10.1038/s42003-019-0495-2Search in Google Scholar PubMed PubMed Central
Dhitavat, S., Ortiz, D., Shea, T.B., and Rivera, E.R. (2002). Acetyl-l-carnitine protects against amyloid-β neurotoxicity: roles of oxidative buffering and ATP levels. Neurochem. Res. 27: 501–505.10.1023/A:1019800703683Search in Google Scholar
Díaz-García, C.M., Mongeon, R., Lahmann, C., Koveal, D., Zucker, H., and Yellen, G. (2017). Neuronal stimulation triggers neuronal glycolysis and not lactate uptake. Cell Metab. 26: 361–374, e364.10.1016/j.cmet.2017.06.021Search in Google Scholar PubMed PubMed Central
Divakaruni, A.S., Wallace, M., Buren, C., Martyniuk, K., Andreyev, A.Y., Li, E., Fields, J.A., Cordes, T., Reynolds, I.J., Bloodgood, B.L., et al.. (2017). Inhibition of the mitochondrial pyruvate carrier protects from excitotoxic neuronal death. J. Cell Biol. 216: 1091–1105.10.1083/jcb.201612067Search in Google Scholar PubMed PubMed Central
Dolgikh, D.A., Malyshev, A.Y., Roshchin, M.V., Smirnova, G.R., Nekrasova, O.V., Petrovskaya, L.E., Feldman, T.B., Balaban, P.M., Kirpichnikov, M.P., and Ostrovsky, M.A. (2016). Comparative characteristics of two anion-channel rhodopsins and prospects of their use in optogenetics. Dokl. Biochem. Biophys. 471: 440–442.10.1134/S160767291606017XSearch in Google Scholar PubMed
Dombeck, D.A., Khabbaz, A.N., Collman, F., Adelman, T.L., and Tank, D.W. (2007). Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56: 43–57.10.1016/j.neuron.2007.08.003Search in Google Scholar PubMed PubMed Central
Durkee, C.A., Covelo, A., Lines, J., Kofuji, P., Aguilar, J., and Araque, A. (2019). Gi/o protein-coupled receptors inhibit neurons but activate astrocytes and stimulate gliotransmission. Glia 67: 1076–1093.10.1002/glia.23589Search in Google Scholar PubMed PubMed Central
Durnin, L., Dai, Y., Aiba, I., Shuttleworth, C.W., Yamboliev, I.A., and Mutafova-Yambolieva, V.N. (2012). Release, neuronal effects and removal of extracellular β-nicotinamide adenine dinucleotide (β-NAD⁺) in the rat brain. Eur. J. Neurosci. 35: 423–435.10.1111/j.1460-9568.2011.07957.xSearch in Google Scholar PubMed PubMed Central
Edling, Y., Ingelman-Sundberg, M., and Simi, A. (2007). Glutamate activates c-fos in glial cells via a novel mechanism involving the glutamate receptor subtype mGlu5 and the transcriptional repressor DREAM. Glia 55: 328–340.10.1002/glia.20464Search in Google Scholar PubMed
Erlichman, J.S., Hewitt, A., Damon, T.L., Hart, M., Kurascz, J., Li, A., and Leiter, J.C. (2008). Inhibition of monocarboxylate transporter 2 in the retrotrapezoid nucleus in rats: a test of the astrocyte-neuron lactate-shuttle hypothesis. J. Neurosci. 28: 4888–4896.10.1523/JNEUROSCI.5430-07.2008Search in Google Scholar PubMed PubMed Central
Ermakova, Y.G., Lanin, A.A., Fedotov, I.V., Roshchin, M., Kelmanson, I.V., Kulik, D., Bogdanova, Y.A., Shokhina, A.G., Bilan, D.S., Staroverov, D.B., et al.. (2017). Thermogenetic neurostimulation with single-cell resolution. Nat. Commun. 8: 15362.10.1038/ncomms15362Search in Google Scholar PubMed PubMed Central
Erofeev, A.I., Matveev, M.V., Terekhin, S.G., Zakharova, O.A., Plotnikova, P.V., and Vlasova, O.L. (2015). The new method for studying neuronal activity: optogenetics. Petersburg Polytechnical Univ. J. Phys. Math. 1: 256–263.10.1016/j.spjpm.2015.12.001Search in Google Scholar
Fellin, T., Pozzan, T., and Carmignoto, G. (2006). Purinergic receptors mediate two distinct glutamate release pathways in hippocampal astrocytes. J. Biol. Chem. 281: 4274–4284.10.1074/jbc.M510679200Search in Google Scholar PubMed
Fernández-Moncada, I., Ruminot, I., Robles-Maldonado, D., Alegría, K., Deitmer, J.W., and Barros, L.F. (2018). Neuronal control of astrocytic respiration through a variant of the Crabtree effect. Proc. Natl. Acad. Sci. U. S. A. 115: 1623–1628.10.1073/pnas.1716469115Search in Google Scholar PubMed PubMed Central
Ferreira, G.C. and McKenna, M.C. (2017). L-carnitine and acetyl-L-carnitine roles and neuroprotection in developing brain. Neurochem. Res. 42: 1661–1675.10.1007/s11064-017-2288-7Search in Google Scholar PubMed PubMed Central
Ferrer, I. (2017). Diversity of astroglial responses across human neurodegenerative disorders and brain aging. Brain Pathol. 27: 645–674.10.1111/bpa.12538Search in Google Scholar PubMed PubMed Central
Figueiredo, M., Lane, S., Stout, R.F., Liu, B., Parpura, V., Teschemacher, A.G., and Kasparov, S. (2014). Comparative analysis of optogenetic actuators in cultured astrocytes. Cell Calcium 56: 208–214.10.1016/j.ceca.2014.07.007Search in Google Scholar PubMed PubMed Central
Figueiredo, M., Lane, S., Tang, F., Liu, B.H., Hewinson, J., Marina, N., Kasymov, V., Souslova, E.A., Chudakov, D.M., Gourine, A.V., et al.. (2011). Optogenetic experimentation on astrocytes. Exp. Physiol. 96: 40–50.10.1113/expphysiol.2010.052597Search in Google Scholar PubMed
Gomez, J.L., Bonaventura, J., Lesniak, W., Mathews, W.B., Sysa-Shah, P., Rodriguez, L.A., Ellis, R.J., Richie, C.T., Harvey, B.K., Dannals, R.F., et al.. (2017). Chemogenetics revealed: DREADD occupancy and activation via converted clozapine. Science 357: 503–507.10.1126/science.aan2475Search in Google Scholar PubMed PubMed Central
Gomez-Ramirez, M., More, A.I., Friedman, N.G., Hochgeschwender, U., and Moore, C.I. (2020). The BioLuminescent-OptoGenetic in vivo response to coelenterazine is proportional, sensitive, and specific in neocortex. J. Neurosci. Res. 98: 471–480.10.1002/jnr.24498Search in Google Scholar PubMed PubMed Central
Gonçalves, C.-A., Rodrigues, L., Bobermin, L.D., Zanotto, C., Vizuete, A., Quincozes-Santos, A., Souza, D.O., and Leite, M.C. (2019). Glycolysis-derived compounds from astrocytes that modulate synaptic communication. Front. Neurosci. 12.10.3389/fnins.2018.01035Search in Google Scholar PubMed PubMed Central
Gordon, G.R.J., Choi, H.B., Rungta, R.L., Ellis-Davies, G.C.R., and MacVicar, B.A. (2008). Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456: 745–749.10.1038/nature07525Search in Google Scholar PubMed PubMed Central
Gourine, A.V., Kasymov, V., Marina, N., Tang, F., Figueiredo, M.F., Lane, S., Teschemacher, A.G., Spyer, K.M., Deisseroth, K., and Kasparov, S. (2010). Astrocytes control breathing through pH-dependent release of ATP. Science 329: 571–575.10.1126/science.1190721Search in Google Scholar PubMed PubMed Central
Grimm, C., Silapetere, A., Vogt, A., Bernal Sierra, Y.A., and Hegemann, P. (2018). Electrical properties, substrate specificity and optogenetic potential of the engineered light-driven sodium pump eKR2. Sci. Rep. 8: 9316.10.1038/s41598-018-27690-wSearch in Google Scholar PubMed PubMed Central
Guerra-Gomes, S., Sousa, N., Pinto, L., and Oliveira, J.F. (2018). Functional roles of astrocyte calcium elevations: from synapses to behavior. Front. Cell. Neurosci. 11.10.3389/fncel.2017.00427Search in Google Scholar PubMed PubMed Central
Halim, N.D., McFate, T., Mohyeldin, A., Okagaki, P., Korotchkina, L.G., Patel, M.S., Jeoung, N.H., Harris, R.A., Schell, M.J., and Verma, A. (2010). Phosphorylation status of pyruvate dehydrogenase distinguishes metabolic phenotypes of cultured rat brain astrocytes and neurons. Glia 58: 1168–1176.10.1002/glia.20996Search in Google Scholar PubMed PubMed Central
Harada, K., Kamiya, T., and Tsuboi, T. (2016). Gliotransmitter Release from astrocytes: functional, developmental, and pathological implications in the brain. Front. Neurosci. 9: 499.10.3389/fnins.2015.00499Search in Google Scholar PubMed PubMed Central
Hasel, P., Dando, O., Jiwaji, Z., Baxter, P., Todd, A.C., Heron, S., Márkus, N.M., McQueen, J., Hampton, D.W., Torvell, M., et al.. (2017). Neurons and neuronal activity control gene expression in astrocytes to regulate their development and metabolism. Nat. Commun. 8: 15132.10.1038/ncomms15132Search in Google Scholar PubMed PubMed Central
Higashida, H., Salmina, A.B., Olovyannikova, R.Y., Hashii, M., Yokoyama, S., Koizumi, K., Jin, D., Liu, H.X., Lopatina, O., Amina, S., et al.. (2007). Cyclic ADP-ribose as a universal calcium signal molecule in the nervous system. Neurochem. Int. 51: 192–199.10.1016/j.neuint.2007.06.023Search in Google Scholar PubMed
Hirase, H., Qian, L., Barthó, P., and Buzsáki, G. (2004). Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol. 2: e96.10.1371/journal.pbio.0020096Search in Google Scholar PubMed PubMed Central
Hohnholt, M.C., Andersen, V.H., Andersen, J.V., Christensen, S.K., Karaca, M., Maechler, P., and Waagepetersen, H.S. (2018). Glutamate dehydrogenase is essential to sustain neuronal oxidative energy metabolism during stimulation. J. Cerebr. Blood Flow Metabol. 38: 1754–1768.10.1177/0271678X17714680Search in Google Scholar PubMed PubMed Central
Hollnagel, J.-O., Cesetti, T., Schneider, J., Vazetdinova, A., Valiullina-Rakhmatullina, F., Lewen, A., Rozov, A., and Kann, O. (2020). Lactate attenuates synaptic transmission and affects brain rhythms featuring high energy expenditure. iScience 23: 101316.10.1016/j.isci.2020.101316Search in Google Scholar PubMed PubMed Central
Horenstein, A.L., Bracci, C., Morandi, F., and Malavasi, F. (2019). CD38 in adenosinergic pathways and metabolic re-programming in human multiple myeloma cells: in-tandem insights from basic science to therapy. Front. Immunol. 10.10.3389/fimmu.2019.00760Search in Google Scholar PubMed PubMed Central
Horenstein, A.L., Chillemi, A., Zaccarello, G., Bruzzone, S., Quarona, V., Zito, A., Serra, S., and Malavasi, F. (2013). A CD38/CD203a/CD73 ectoenzymatic pathway independent of CD39 drives a novel adenosinergic loop in human T lymphocytes. OncoImmunology 2: e26246.10.4161/onci.26246Search in Google Scholar PubMed PubMed Central
Huang, T., Zhou, X., Mao, X., Yu, C., Zhang, Z., Yang, J., Zhang, Y., Su, T., Chen, C., Cao, Y., et al.. (2020). Lactate-fueled oxidative metabolism drives DNA methyltransferase 1-mediated transcriptional co-activator with PDZ binding domain protein activation. Cancer Sci. 111: 186–199.10.1111/cas.14246Search in Google Scholar PubMed PubMed Central
Inazu, M., Takeda, H., Maehara, K., Miyashita, K., Tomoda, A., and Matsumiya, T. (2006). Functional expression of the organic cation/carnitine transporter 2 in rat astrocytes. J. Neurochem. 97: 424–434.10.1111/j.1471-4159.2006.03757.xSearch in Google Scholar PubMed
Inoue, K., Ono, H., Abe-Yoshizumi, R., Yoshizawa, S., Ito, H., Kogure, K., and Kandori, H. (2013). A light-driven sodium ion pump in marine bacteria. Nat. Commun. 4: 1678.10.1038/ncomms2689Search in Google Scholar PubMed
Ioannou, M.S., Jackson, J., Sheu, S.-H., Chang, C.-L., Weigel, A.V., Liu, H., Pasolli, H.A., Xu, C.S., Pang, S., Matthies, D., et al.. (2019). Neuron-astrocyte metabolic coupling protects against activity-induced fatty acid toxicity. Cell 177: 1522–1535, e1514.10.1016/j.cell.2019.04.001Search in Google Scholar PubMed
Jessen, N.A., Munk, A.S.F., Lundgaard, I., and Nedergaard, M. (2015). The glymphatic system: a beginner’s guide. Neurochem. Res. 40: 2583–2599.10.1007/s11064-015-1581-6Search in Google Scholar PubMed PubMed Central
Jha, M.K., Jeon, S., and Suk, K. (2012). Pyruvate dehydrogenase kinases in the nervous system: their principal functions in neuronal-glial metabolic interaction and neuro-metabolic disorders. Curr. Neuropharmacol. 10: 393–403.10.2174/157015912804499528Search in Google Scholar
Ji, Z.-g. and Wang, H. (2014). Optogenetic control of astrocytes: is it possible to treat astrocyte-related epilepsy? Brain Res. Bull. 110.10.1016/j.brainresbull.2014.10.013Search in Google Scholar PubMed
Kang, S., Hong, S.-I., Lee, J., Peyton, L., Baker, M., Choi, S., Kim, H., Chang, S.-Y., and Choi, D.-S. (2020). Activation of astrocytes in the dorsomedial striatum facilitates transition from habitual to goal-directed reward-seeking behavior. Biol. Psychiatr.10.1016/j.biopsych.2020.04.023Search in Google Scholar PubMed PubMed Central
Kanski, R., Sneeboer, M.A., van Bodegraven, E.J., Sluijs, J.A., Kropff, W., Vermunt, M.W., Creyghton, M.P., De Filippis, L., Vescovi, A., Aronica, E., et al.. (2014). Histone acetylation in astrocytes suppresses GFAP and stimulates a reorganization of the intermediate filament network. J. Cell Sci. 127: 4368–4380.10.1242/dev.118489Search in Google Scholar
Kery, R., Chen, A., and Kirschen, G. (2020). Genetic targeting of astrocytes to combat neurodegenerative disease. Neural. Regen. Res. 15: 199–211.10.4103/1673-5374.265541Search in Google Scholar PubMed PubMed Central
Kim, S., Kyung, T., Chung, J.-H., Kim, N., Keum, S., Lee, J., Park, H., Kim, H.M., Lee, S., Shin, H.-S., et al.. (2020). Non-invasive optical control of endogenous Ca2+ channels in awake mice. Nat. Commun. 11: 210.10.1038/s41467-019-14005-4Search in Google Scholar PubMed PubMed Central
Kol, A., Adamsky, A., Groysman, M., Kreisel, T., London, M., and Goshen, I. (2020). Astrocytes contribute to remote memory formation by modulating hippocampal–cortical communication during learning. Nat. Neurosci.10.1038/s41593-020-0679-6Search in Google Scholar PubMed PubMed Central
Kovalev, K., Polovinkin, V., Gushchin, I., Alekseev, A., Shevchenko, V., Borshchevskiy, V., Astashkin, R., Balandin, T., Bratanov, D., Vaganova, S., et al.. (2019). Structure and mechanisms of sodium-pumping KR2 rhodopsin. Sci. Adv. 5: eaav2671.10.1126/sciadv.aav2671Search in Google Scholar PubMed PubMed Central
Kozai, T.D. and Vazquez, A.L. (2015). Photoelectric artefact from optogenetics and imaging on microelectrodes and bioelectronics: new challenges and opportunities. J. Mater. Chem. B 3: 4965–4978.10.1039/C5TB00108KSearch in Google Scholar PubMed PubMed Central
Kulijewicz-Nawrot, M., Verkhratsky, A., Chvátal, A., Syková, E., and Rodríguez, J.J. (2012). Astrocytic cytoskeletal atrophy in the medial prefrontal cortex of a triple transgenic mouse model of Alzheimer’s disease. J. Anat. 221: 252–262.10.1111/j.1469-7580.2012.01536.xSearch in Google Scholar PubMed PubMed Central
Langer, J. and Rose, C.R. (2009). Synaptically induced sodium signals in hippocampal astrocytes in situ. J. Physiol. 587: 5859–5877.10.1113/jphysiol.2009.182279Search in Google Scholar PubMed PubMed Central
Larsen, B.R. and MacAulay, N. (2014). Kir4.1-mediated spatial buffering of K+: experimental challenges in determination of its temporal and quantitative contribution to K+ clearance in the brain. Channels 8: 544–550.10.4161/19336950.2014.970448Search in Google Scholar PubMed PubMed Central
Latham, T., Mackay, L., Sproul, D., Karim, M., Culley, J., Harrison, D.J., Hayward, L., Langridge-Smith, P., Gilbert, N., and Ramsahoye, B.H. (2012). Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression. Nucleic Acids Res. 40: 4794–4803.10.1093/nar/gks066Search in Google Scholar PubMed PubMed Central
Liddelow, S., Guttenplan, K.A., Clarke, L., Bennett, F.C., Bohlen, C.J., Schirmer, L., Bennett, M., Munch, A., Chung, W.-S., Peterson, T., et al.. (2017). Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541: 481–487.10.1038/nature21029Search in Google Scholar PubMed PubMed Central
Lin, J.Y. (2011). A user’s guide to channelrhodopsin variants: features, limitations and future developments. Exp. Physiol. 96: 19–25.10.1113/expphysiol.2009.051961Search in Google Scholar PubMed PubMed Central
Liu, X., Cooper, D.E., Cluntun, A.A., Warmoes, M.O., Zhao, S., Reid, M.A., Liu, J., Lund, P.J., Lopes, M., Garcia, B.A., et al.. (2018). Acetate production from glucose and coupling to mitochondrial metabolism in mammals. Cell 175: 502–513, e513.10.1016/j.cell.2018.08.040Search in Google Scholar PubMed PubMed Central
Liu, X., Lu, Y., Iseri, E., Shi, Y., and Kuzum, D. (2018b). A compact closed-loop optogenetics system based on artifact-free transparent graphene electrodes. Front. Neurosci. 12: 132.10.3389/fnins.2018.00132Search in Google Scholar PubMed PubMed Central
Losi, G., Mariotti, L., Sessolo, M., and Carmignoto, G. (2017). New tools to study astrocyte Ca2+ signal dynamics in brain networks in vivo. Front. Cell. Neurosci. 11.10.3389/fncel.2017.00134Search in Google Scholar PubMed PubMed Central
MacDonald, A.J., Holmes, F.E., Beall, C., Pickering, A.E., and Ellacott, K.L.J. (2020). Regulation of food intake by astrocytes in the brainstem dorsal vagal complex. Glia 68: 1241–1254.10.1002/glia.23774Search in Google Scholar PubMed PubMed Central
MacVicar, B.A., Crichton, S.A., Burnard, D.M., and Tse, F.W.Y. (1987). Membrane conductance oscillations in astrocytes induced by phorbol ester. Nature 329: 242–243.10.1038/329242a0Search in Google Scholar PubMed
Malarkey, E.B. and Parpura, V. (2008). Mechanisms of glutamate release from astrocytes. Neurochem. Int. 52: 142–154.10.1016/j.neuint.2007.06.005Search in Google Scholar PubMed PubMed Central
Mangia, S., Simpson, I.A., Vannucci, S.J., and Carruthers, A. (2009). The in vivo neuron-to-astrocyte lactate shuttle in human brain: evidence from modeling of measured lactate levels during visual stimulation. J. Neurochem. 109(Suppl. 1): 55–62.10.1111/j.1471-4159.2009.06003.xSearch in Google Scholar PubMed PubMed Central
Marcelino, H., Nogueira, V.C., Santos, C.R.A., Quelhas, P., Carvalho, T.M.A., Fonseca-Gomes, J., Tomás, J., Diógenes, M.J., Sebastião, A.M., and Cascalheira, J.F. (2020). Adenosine inhibits human astrocyte proliferation independently of adenosine receptor activation. J. Neurochem. 153: 455–467.10.1111/jnc.14937Search in Google Scholar PubMed
Margineanu, M.B., Mahmood, H., Fiumelli, H., and Magistretti, P.J. (2018). L-lactate regulates the expression of synaptic plasticity and neuroprotection genes in cortical neurons: a transcriptome analysis. Front. Mol. Neurosci. 11: 375.10.3389/fnmol.2018.00375Search in Google Scholar PubMed PubMed Central
Martin-Fernandez, M., Jamison, S., Robin, L.M., Zhao, Z., Martin, E.D., Aguilar, J., Benneyworth, M.A., Marsicano, G., and Araque, A. (2017). Synapse-specific astrocyte gating of amygdala-related behavior. Nat. Neurosci. 20: 1540–1548.10.1038/nn.4649Search in Google Scholar PubMed PubMed Central
Masamoto, K., Unekawa, M., Watanabe, T., Toriumi, H., Takuwa, H., Kawaguchi, H., Kanno, I., Matsui, K., Tanaka, K.F., Tomita, Y., et al.. (2015). Unveiling astrocytic control of cerebral blood flow with optogenetics. Sci. Rep. 5: 11455.10.1038/srep11455Search in Google Scholar PubMed PubMed Central
Mayorquin, L.C., Rodriguez, A.V., Sutachan, J.-J., and Albarracín, S.L. (2018). Connexin-mediated functional and metabolic coupling between astrocytes and neurons. Front. Mol. Neurosci. 11.10.3389/fnmol.2018.00118Search in Google Scholar PubMed PubMed Central
Mederos, S., González-Arias, C., and Perea, G. (2018). Astrocyte–neuron networks: a multilane highway of signaling for homeostatic brain function. Front. Synaptic Neurosci. 10.10.3389/fnsyn.2018.00045Search in Google Scholar PubMed PubMed Central
Mederos, S., Hernández-Vivanco, A., Ramírez-Franco, J., Martín-Fernández, M., Navarrete, M., Yang, A., Boyden, E.S., and Perea, G. (2019). Melanopsin for precise optogenetic activation of astrocyte-neuron networks. Glia 67: 915–934.10.1002/glia.23580Search in Google Scholar PubMed
Mishima, T., Sakatani, S., and Hirase, H. (2007). Intracellular labeling of single cortical astrocytes in vivo. J. Neurosci. Methods 166: 32–40.10.1016/j.jneumeth.2007.06.021Search in Google Scholar PubMed
Montana, V., Malarkey, E.B., Verderio, C., Matteoli, M., and Parpura, V. (2006). Vesicular transmitter release from astrocytes. Glia 54: 700–715.10.1002/glia.20367Search in Google Scholar PubMed
Mu, Y., Bennett, D.V., Rubinov, M., Narayan, S., Yang, C.-T., Tanimoto, M., Mensh, B.D., Looger, L.L., and Ahrens, M.B. (2019). Glia accumulate evidence that actions are futile and suppress unsuccessful behavior. Cell 178: 27–43, e19.10.1016/j.cell.2019.05.050Search in Google Scholar PubMed
Muir, J., Lopez, J., and Bagot, R.C. (2019). Wiring the depressed brain: optogenetic and chemogenetic circuit interrogation in animal models of depression. Neuropsychopharmacology 44: 1013–1026.10.1038/s41386-018-0291-6Search in Google Scholar PubMed PubMed Central
Nagai, J., Rajbhandari, A.K., Gangwani, M.R., Hachisuka, A., Coppola, G., Masmanidis, S.C., Fanselow, M.S., and Khakh, B.S. (2019). Hyperactivity with disrupted attention by activation of an astrocyte synaptogenic cue. Cell 177: 1280–1292, e1220.10.1016/j.cell.2019.03.019Search in Google Scholar PubMed PubMed Central
Nagel, G., Brauner, M., Liewald, J.F., Adeishvili, N., Bamberg, E., and Gottschalk, A. (2005). Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15: 2279–2284.10.1016/j.cub.2005.11.032Search in Google Scholar PubMed
Nakamichi, N. and Kato, Y. (2017). Physiological roles of carnitine/organic cation transporter OCTN1/SLC22A4 in neural cells. Biol. Pharm. Bull. 40: 1146–1152.10.1248/bpb.b17-00099Search in Google Scholar PubMed
Nam, M.-H., Han, K.-S., Lee, J., Won, W., Koh, W., Bae, J.Y., Woo, J., Kim, J., Kwong, E., Choi, T.-Y., et al.. (2019). Activation of astrocytic μ-opioid receptor causes conditioned place preference. Cell Rep. 28: 1154–1166, e1155.10.1016/j.celrep.2019.06.071Search in Google Scholar PubMed
Nasca, C., Xenos, D., Barone, Y., Caruso, A., Scaccianoce, S., Matrisciano, F., Battaglia, G., Mathé, A.A., Pittaluga, A., Lionetto, L., et al.. (2013). L-acetylcarnitine causes rapid antidepressant effects through the epigenetic induction of mGlu2 receptors. Proc. Natl. Acad. Sci. U. S. A. 110: 4804–4809.10.1073/pnas.1216100110Search in Google Scholar PubMed PubMed Central
Neal, M. and Richardson, J.R. (2018). Epigenetic regulation of astrocyte function in neuroinflammation and neurodegeneration. Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 1864: 432–443.10.1016/j.bbadis.2017.11.004Search in Google Scholar PubMed PubMed Central
Nguyen, N.T., Ma, G., Lin, E., D’Souza, B., Jing, J., He, L., Huang, Y., and Zhou, Y. (2018). CRAC channel-based optogenetics. Cell Calcium 75: 79–88.10.1016/j.ceca.2018.08.007Search in Google Scholar PubMed PubMed Central
Nizar, K., Uhlirova, H., Tian, P., Saisan, P.A., Cheng, Q., Reznichenko, L., Weldy, K.L., Steed, T.C., Sridhar, V.B., MacDonald, C.L., et al.. (2013). In vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase. J. Neurosci. 33: 8411–8422.10.1523/JNEUROSCI.3285-12.2013Search in Google Scholar PubMed PubMed Central
Noguchi, H., Murao, N., Kimura, A., Matsuda, T., Namihira, M., and Nakashima, K. (2016). DNA methyltransferase 1 is indispensable for development of the hippocampal dentate gyrus. J. Neurosci. 36: 6050–6068.10.1523/JNEUROSCI.0512-16.2016Search in Google Scholar PubMed PubMed Central
Octeau, J.C., Gangwani, M.R., Allam, S.L., Tran, D., Huang, S., Hoang-Trong, T.M., Golshani, P., Rumbell, T.H., Kozloski, J.R., and Khakh, B.S. (2019). Transient, consequential increases in extracellular potassium ions accompany channelrhodopsin2 excitation. Cell Rep. 27: 2249–2261, e2247.10.1016/j.celrep.2019.04.078Search in Google Scholar PubMed PubMed Central
Oheim, M., Schmidt, E., and Hirrlinger, J. (2018). Local energy on demand: are ‘spontaneous’ astrocytic Ca2+-microdomains the regulatory unit for astrocyte-neuron metabolic cooperation? Brain Res. Bull. 136: 54–64.10.1016/j.brainresbull.2017.04.011Search in Google Scholar PubMed
Orkand, R.K., Nicholls, J.G., and Kuffler, S.W. (1966). Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29: 788–806.10.1152/jn.1966.29.4.788Search in Google Scholar PubMed
Osipova, E.D., Semyachkina-Glushkovskaya, O.V., Morgun, A.V., Pisareva, N.V., Malinovskaya, N.A., Boitsova, E.B., Pozhilenkova, E.A., Belova, O.A., Salmin, V.V., Taranushenko, T.E., et al.. (2018). Gliotransmitters and cytokines in the control of blood-brain barrier permeability. Rev. Neurosci.10.1515/revneuro-2017-0092Search in Google Scholar PubMed
Pannasch, U. and Rouach, N. (2013). Emerging role for astroglial networks in information processing: from synapse to behavior. Trends Neurosci. 36: 405–417.10.1016/j.tins.2013.04.004Search in Google Scholar PubMed
Park, K. and Lee, S.J. (2020). Deciphering the star codings: astrocyte manipulation alters mouse behavior. Exp. Mol. Med.10.1038/s12276-020-0468-zSearch in Google Scholar PubMed PubMed Central
Parpura, V., Grubišić, V., and Verkhratsky, A. (2011). Ca2+ sources for the exocytotic release of glutamate from astrocytes. Biochim. Biophys. Acta Mol. Cell Res. 1813: 984–991.10.1016/j.bbamcr.2010.11.006Search in Google Scholar PubMed
Peedicayil, J. (2018). l-Acetylcarnitine as a histone acetylation modulator in psychiatric disorders. Psychopharmacology 235: 3361–3362.10.1007/s00213-018-5043-0Search in Google Scholar PubMed
Pellerin, L. and Magistretti, P.J. (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. U. S. A. 91: 10625, 10629.10.1073/pnas.91.22.10625Search in Google Scholar PubMed PubMed Central
Pelluru, D., Konadhode, R.R., Bhat, N.R., and Shiromani, P.J. (2016). Optogenetic stimulation of astrocytes in the posterior hypothalamus increases sleep at night in C57BL/6J mice. Eur. J. Neurosci. 43: 1298–1306.10.1111/ejn.13074Search in Google Scholar PubMed PubMed Central
Perea, G. and Araque, A. (2010). GLIA modulates synaptic transmission. Brain Res. Rev. 63: 93–102.10.1016/j.brainresrev.2009.10.005Search in Google Scholar PubMed
Perea, G., Yang, A., Boyden, E.S., and Sur, M. (2014). Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat. Commun. 5: 3262.10.1038/ncomms4262Search in Google Scholar PubMed PubMed Central
Petravicz, J., Boyt, K.M., and McCarthy, K.D. (2014). Astrocyte IP3R2-dependent Ca2+ signaling is not a major modulator of neuronal pathways governing behavior. Front. Behav. Neurosci. 8: 384.10.3389/fnbeh.2014.00384Search in Google Scholar PubMed PubMed Central
Pettegrew, J.W., Levine, J., and McClure, R.J. (2000). Acetyl-L-carnitine physical-chemical, metabolic, and therapeutic properties: relevance for its mode of action in Alzheimer’s disease and geriatric depression. Mol. Psychiatr. 5: 616–632.10.1038/sj.mp.4000805Search in Google Scholar PubMed
Petzold, G.C. and Murthy, V.N. (2011). Role of astrocytes in neurovascular coupling. Neuron 71: 782–797.10.1016/j.neuron.2011.08.009Search in Google Scholar PubMed
Philtjens, S., Turnbull, M.T., Thedy, B.P., Moon, Y., and Kim, J. (2020). Chemogenetic activation of astrocytes in the hippocampus and cortex changes the transcriptome of microglia and other cell types. bioRxiv, https://doi.org/10.1101/2020.04.27.064881.Search in Google Scholar
Popugaeva, E., Vlasova, O.L., and Bezprozvanny, I. (2015). Restoring calcium homeostasis to treat Alzheimer’s disease: a future perspective. Neurodegener. Dis. Manag. 5: 395–398.10.2217/nmt.15.36Search in Google Scholar PubMed PubMed Central
Poskanzer, K.E. and Yuste, R. (2016). Astrocytes regulate cortical state switching in vivo. Proc. Natl. Acad. Sci. U. S. A. 113: E2675–2684.10.1073/pnas.1520759113Search in Google Scholar PubMed PubMed Central
Rein, M.L. and Deussing, J.M. (2012). The optogenetic (r)evolution. Mol. Genet. Genom. 287: 95–109.10.1007/s00438-011-0663-7Search in Google Scholar PubMed PubMed Central
Reyes, R.C. and Parpura, V. (2008). Models of astrocytic Ca dynamics and epilepsy. Drug Discov. Today Dis. Model. 5: 13–18.10.1016/j.ddmod.2008.07.002Search in Google Scholar PubMed PubMed Central
Robertson, J.M. (2018). The gliocentric brain. Int. J. Mol. Sci. 19: 3033.10.3390/ijms19103033Search in Google Scholar PubMed PubMed Central
Roth, B.L. (2016). DREADDs for neuroscientists. Neuron 89: 683–694.10.1016/j.neuron.2016.01.040Search in Google Scholar PubMed PubMed Central
Rowlands, B.D., Klugmann, M., and Rae, C.D. (2017). Acetate metabolism does not reflect astrocytic activity, contributes directly to GABA synthesis, and is increased by silent information regulator 1 activation. J. Neurochem. 140: 903–918.10.1111/jnc.13916Search in Google Scholar PubMed
Rungta, R.L., Osmanski, B.-F., Boido, D., Tanter, M., and Charpak, S. (2017). Light controls cerebral blood flow in naive animals. Nat. Commun. 8: 14191.10.1038/ncomms14191Search in Google Scholar PubMed PubMed Central
Ruzaeva, V.A., Morgun, A.V., Khilazheva, E.D., Kuvacheva, N.V., Pozhilenkova, E.A., Boitsova, E.B., Martynova, G.P., Taranushenko, T.E., and Salmina, A.B. (2016). [Development of blood-brain barrier under the modulation of HIF activity in astroglialand neuronal cells in vitro]. Biomed Khim 62: 664–669.10.18097/PBMC20166206664Search in Google Scholar PubMed
Ryoo, K. and Park, J.Y. (2016). Two-pore domain potassium channels in astrocytes. Exp. Neurobiol. 25: 222–232.10.5607/en.2016.25.5.222Search in Google Scholar PubMed PubMed Central
Sahlender, D.A., Savtchouk, I., and Volterra, A. (2014). What do we know about gliotransmitter release from astrocytes? Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 369: 20130592.10.1098/rstb.2013.0592Search in Google Scholar PubMed PubMed Central
Salmina, A.B., Kuvacheva, N.V., Morgun, A.V., Komleva, Y.K., Pozhilenkova, E.A., Lopatina, O.L., Gorina, Y.V., Taranushenko, T.E., and Petrova, L.L. (2015). Glycolysis-mediated control of blood-brain barrier development and function. Int. J. Biochem. Cell Biol. 64: 174–184.10.1016/j.biocel.2015.04.005Search in Google Scholar PubMed
Salmina, A.B., Malinovskaya, N.A., Okuneva, O.S., Taranushenko, T.E., Fursov, A.A., Mikhutkina, S.V., Morgun, A.V., Prokopenko, S.V., and Zykova, L.D. (2008). Perinatal hypoxic and ischemic damage to the central nervous system causes changes in the expression of connexin 43 and CD38 and ADP-ribosyl cyclase activity in brain cells. Bull. Exp. Biol. Med. 146: 733–736.10.1007/s10517-009-0385-6Search in Google Scholar PubMed
Salmina, A.B., Olovyannikova, R.Ya., Noda, M., and Higashida, H. (2006). ADR-ribosyl cyclase as a therapeutic target for central nervous system diseases. Cent. Nerv. Syst. Agents Med. Chem. 6: 193–210.10.2174/187152406778226699Search in Google Scholar
Santello, M., Bezzi, P., and Volterra, A. (2011). TNFα controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69: 988–1001.10.1016/j.neuron.2011.02.003Search in Google Scholar PubMed
Sasaki, T., Beppu, K., Tanaka, K.F., Fukazawa, Y., Shigemoto, R., and Matsui, K. (2012). Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation. Proc. Natl. Acad. Sci. U. S. A. 109: 20720–20725.10.1073/pnas.1213458109Search in Google Scholar PubMed PubMed Central
Schummers, J., Yu, H., and Sur, M. (2008). Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320: 1638–1643.10.1126/science.1156120Search in Google Scholar PubMed
Scofield, M.D. (2018). Exploring the role of astroglial glutamate release and association with synapses in neuronal function and behavior. Biol. Psychiatr. 84: 778–786.10.1016/j.biopsych.2017.10.029Search in Google Scholar PubMed PubMed Central
Scofield, M.D., Boger, H.A., Smith, R.J., Li, H., Haydon, P.G., and Kalivas, P.W. (2015). Gq-DREADD selectively initiates glial glutamate release and inhibits cue-induced cocaine seeking. Biol. Psychiatr. 78: 441–451.10.1016/j.biopsych.2015.02.016Search in Google Scholar PubMed PubMed Central
Shen, W., Nikolic, L., Meunier, C., Pfrieger, F., and Audinat, E. (2017). An autocrine purinergic signaling controls astrocyte-induced neuronal excitation. Sci. Rep. 7: 11280.10.1038/s41598-017-11793-xSearch in Google Scholar PubMed PubMed Central
Shigetomi, E., Hirayama, Y.J., Ikenaka, K., Tanaka, K.F., and Koizumi, S. (2018). Role of purinergic receptor P2Y1 in spatiotemporal Ca2+ dynamics in astrocytes. J. Neurosci. 38: 1383–1395.10.1523/JNEUROSCI.2625-17.2017Search in Google Scholar PubMed PubMed Central
Shigetomi, E., Jackson-Weaver, O., Huckstepp, R.T., O’Dell, T.J., and Khakh, B.S. (2013). TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J. Neurosci. 33: 10143–10153.10.1523/JNEUROSCI.5779-12.2013Search in Google Scholar PubMed PubMed Central
Siuda, E.R., McCall, J.G., Al-Hasani, R., Shin, G., Il Park, S., Schmidt, M.J., Anderson, S.L., Planer, W.J., Rogers, J.A., and Bruchas, M.R. (2015). Optodynamic simulation of β-adrenergic receptor signalling. Nat. Commun. 6: 8480.10.1038/ncomms9480Search in Google Scholar PubMed PubMed Central
Sotelo-Hitschfeld, T., Niemeyer, M.I., Mächler, P., Ruminot, I., Lerchundi, R., Wyss, M.T., Stobart, J., Fernández-Moncada, I., Valdebenito, R., Garrido-Gerter, P., et al.. (2015). Channel-mediated lactate release by K⁺-stimulated astrocytes. J. Neurosci. 35: 4168–4178.10.1523/JNEUROSCI.5036-14.2015Search in Google Scholar PubMed PubMed Central
Sun, L., Shay, J., McLoed, M., Roodhouse, K., Chung, S.H., Clark, C.M., Pirri, J.K., Alkema, M.J., and Gabel, C.V. (2014). Neuronal regeneration in C. elegans requires subcellular calcium release by ryanodine receptor channels and can be enhanced by optogenetic stimulation. J. Neurosci. 34: 15947–15956.10.1523/JNEUROSCI.4238-13.2014Search in Google Scholar PubMed PubMed Central
Takata, N., Nagai, T., Ozawa, K., Oe, Y., Mikoshiba, K., and Hirase, H. (2013). Cerebral blood flow modulation by basal forebrain or whisker stimulation can occur independently of large cytosolic Ca2+ signaling in astrocytes. PLoS One 8: e66525.10.1371/journal.pone.0066525Search in Google Scholar PubMed PubMed Central
Takata, N., Sugiura, Y., Yoshida, K., Koizumi, M., Hiroshi, N., Honda, K., Yano, R., Komaki, Y., Matsui, K., Suematsu, M., et al.. (2018). Optogenetic astrocyte activation evokes BOLD fMRI response with oxygen consumption without neuronal activity modulation. Glia 66: 2013–2023.10.1002/glia.23454Search in Google Scholar PubMed
Tang, F., Lane, S., Korsak, A., Paton, J.F.R., Gourine, A.V., Kasparov, S., and Teschemacher, A.G. (2014). Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat. Commun. 5: 3284.10.1038/ncomms4284Search in Google Scholar PubMed PubMed Central
Teschemacher, A.G., Gourine, A.V., and Kasparov, S. (2015). A role for astrocytes in sensing the brain microenvironment and neuro-metabolic integration. Neurochem. Res. 40: 2386–2393.10.1007/s11064-015-1562-9Search in Google Scholar PubMed
Tochitsky, I., Banghart, M.R., Mourot, A., Yao, J.Z., Gaub, B., Kramer, R.H., and Trauner, D. (2012). Optochemical control of genetically engineered neuronal nicotinic acetylcholine receptors. Nat. Chem. 4: 105–111.10.1038/nchem.1234Search in Google Scholar PubMed PubMed Central
Toth, A.B., Hori, K., Novakovic, M.M., Bernstein, N.G., Lambot, L., and Prakriya, M. (2019). CRAC channels regulate astrocyte Ca2+ signaling and gliotransmitter release to modulate hippocampal GABAergic transmission. Sci. Signal. 12.10.1126/scisignal.aaw5450Search in Google Scholar
Traina, G. (2016). The neurobiology of acetyl-L-carnitine. Front. Biosci. 21: 1314–1329.10.2741/4459Search in Google Scholar PubMed
Tran, C.H.T., Peringod, G., and Gordon, G.R. (2018). Astrocytes integrate behavioral state and vascular signals during functional hyperemia. Neuron 100: 1133–1148, e1133.10.1016/j.neuron.2018.09.045Search in Google Scholar PubMed
Vardjan, N., Chowdhury, H.H., Horvat, A., Velebit, J., Malnar, M., Muhič, M., Kreft, M., Krivec, Š.G., Bobnar, S.T., Miš, K., et al.. (2018). Enhancement of astroglial aerobic glycolysis by extracellular lactate-mediated increase in cAMP. Front. Mol. Neurosci. 11: 148.10.3389/fnmol.2018.00148Search in Google Scholar PubMed PubMed Central
Verderio, C., Bruzzone, S., Zocchi, E., Fedele, E., Schenk, U., De Flora, A., and Matteoli, M. (2001). Evidence of a role for cyclic ADP-ribose in calcium signalling and neurotransmitter release in cultured astrocytes. J. Neurochem. 78: 646–657.10.1046/j.1471-4159.2001.00455.xSearch in Google Scholar PubMed
Verkhratsky, A., Steardo, L., Parpura, V., and Montana, V. (2016). Translational potential of astrocytes in brain disorders. Prog. Neurobiol. 144: 188–205.10.1016/j.pneurobio.2015.09.003Search in Google Scholar PubMed PubMed Central
Wang, F., Smith, N.A., Xu, Q., Fujita, T., Baba, A., Matsuda, T., Takano, T., Bekar, L., and Nedergaard, M. (2012). Astrocytes modulate neural network activity by Ca2+-dependent uptake of extracellular K+. Sci. Signal. 5: ra26.10.1126/scisignal.2002334Search in Google Scholar
Wang, J., Tu, J., Cao, B., Mu, L., Yang, X., Cong, M., Ramkrishnan, A.S., Chan, R.H.M., Wang, L., and Li, Y. (2017). Astrocytic L-lactate signaling facilitates amygdala-anterior cingulate cortex synchrony and decision making in rats. Cell Rep. 21: 2407–2418.10.1016/j.celrep.2017.11.012Search in Google Scholar PubMed
Wei, L., Sheng, H., Chen, L., Hao, B., Shi, X., and Chen, Y. (2016). Effect of pannexin-1 on the release of glutamate and cytokines in astrocytes. J. Clin. Neurosci. 23: 135–141.10.1016/j.jocn.2015.05.043Search in Google Scholar PubMed
Winkler, U., Seim, P., Enzbrenner, Y., Köhler, S., Sicker, M., and Hirrlinger, J. (2017). Activity-dependent modulation of intracellular ATP in cultured cortical astrocytes. J. Neurosci. Res. 95: 2172–2181.10.1002/jnr.24020Search in Google Scholar PubMed
Witthoft, A., Filosa, J.A., and Karniadakis, G.E. (2013). Potassium buffering in the neurovascular unit: models and sensitivity analysis. Biophys. J. 105: 2046–2054.10.1016/j.bpj.2013.09.012Search in Google Scholar PubMed PubMed Central
Xie, A.X., Madayag, A., Minton, S.K., McCarthy, K.D., and Malykhina, A.P. (2020a). Sensory satellite glial Gq-GPCR activation alleviates inflammatory pain via peripheral adenosine 1 receptor activation. Sci. Rep. 10: 14181.10.1038/s41598-020-71073-zSearch in Google Scholar PubMed PubMed Central
Xie, A.X., Petravicz, J., and McCarthy, K.D. (2015). Molecular approaches for manipulating astrocytic signaling in vivo. Front. Cell. Neurosci. 9: 144.10.3389/fncel.2015.00144Search in Google Scholar PubMed PubMed Central
Xie, Z., Yang, Q., Song, D., Quan, Z., and Qing, H. (2020b). Optogenetic manipulation of astrocytes from synapses to neuronal networks: a potential therapeutic strategy for neurodegenerative diseases. Glia 68: 215–226.10.1002/glia.23693Search in Google Scholar PubMed
Yang, L., Qi, Y., and Yang, Y. (2015). Astrocytes control food intake by inhibiting AGRP neuron activity via adenosine A1 receptors. Cell Rep. 11: 798–807.10.1016/j.celrep.2015.04.002Search in Google Scholar PubMed
Yang, Y., Pacia, C.P., Ye, D., Zhu, L., Baek, H., Yue, Y., Yuan, J., Miller, M.J., Cui, J., Culver, J.P., et al.. (2020). Sonogenetics for noninvasive and cellular-level neuromodulation in rodent brain. bioRxiv.10.1101/2020.01.28.919910Search in Google Scholar
Yoichi, S., Shibata, K., Yoshida, K., Shigetomi, E., Gachet, C., Ikenaka, K., Tanaka, K., and Koizumi, S. (2017). Transformation of astrocytes to a neuroprotective phenotype by microglia via P2Y 1 receptor downregulation. Cell Rep. 19: 1151–1164.10.1016/j.celrep.2017.04.047Search in Google Scholar PubMed
Zamora, N.N., Cheli, V.T., Santiago González, D.A., Wan, R., and Paez, P.M. (2020). Deletion of voltage-gated calcium channels in astrocytes during demyelination reduces brain inflammation and promotes myelin regeneration in mice. J. Neurosci. 40: 3332–3347.10.1523/JNEUROSCI.1644-19.2020Search in Google Scholar PubMed PubMed Central
Zanelli, S.A., Solenski, N.J., Rosenthal, R.E., and Fiskum, G. (2005). Mechanisms of ischemic neuroprotection by acetyl-L-carnitine. Ann. N. Y. Acad. Sci. 1053: 153–161.10.1196/annals.1344.013Search in Google Scholar PubMed PubMed Central
Zdzisińska, B., Żurek, A., and Kandefer-Szerszeń, M. (2017). Alpha-Ketoglutarate as a molecule with pleiotropic activity: well-known and novel possibilities of therapeutic use. Arch. Immunol. Ther. Exp. 65: 21–36.10.1007/s00005-016-0406-xSearch in Google Scholar PubMed PubMed Central
Zhang, D., Tang, Z., Huang, H., Zhou, G., Cui, C., Weng, Y., Liu, W., Kim, S., Lee, S., Perez-Neut, M., et al.. (2019). Metabolic regulation of gene expression by histone lactylation. Nature 574: 575–580.10.1038/s41586-019-1678-1Search in Google Scholar
Zhang, J.M., Wang, H.K., Ye, C.Q., Ge, W., Chen, Y., Jiang, Z.L., Wu, C.P., Poo, M.M., and Duan, S. (2003). ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40: 971–982.10.1016/S0896-6273(03)00717-7Search in Google Scholar
Zorec, R., Araque, A., Carmignoto, G., Haydon, P.G., Verkhratsky, A., and Parpura, V. (2012). Astroglial excitability and gliotransmission: an appraisal of Ca2+ as a signalling route. ASN Neuro 4.10.1042/AN20110061Search in Google Scholar PubMed PubMed Central
Zuend, M., Saab, A.S., Wyss, M.T., Ferrari, K.D., Hösli, L., Looser, Z.J., Stobart, J.L., Duran, J., Guinovart, J.J., Barros, L.F., et al.. (2020). Arousal-induced cortical activity triggers lactate release from astrocytes. Nat. Metab. 2: 179–191.10.1038/s42255-020-0170-4Search in Google Scholar PubMed
© 2021 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Optogenetic and chemogenetic modulation of astroglial secretory phenotype
- The role of PKMζ in the maintenance of long-term memory: a review
- Advances in imaging acute ischemic stroke: evaluation before thrombectomy
- Current updates on various treatment approaches in the early management of acute spinal cord injury
- The long-term prognosis of Transient Global Amnesia: a systematic review
- The cellular mechanism by which the rostral ventromedial medulla acts on the spinal cord during chronic pain
- Psychedelic drugs and perception: a narrative review of the first era of research
Articles in the same Issue
- Frontmatter
- Optogenetic and chemogenetic modulation of astroglial secretory phenotype
- The role of PKMζ in the maintenance of long-term memory: a review
- Advances in imaging acute ischemic stroke: evaluation before thrombectomy
- Current updates on various treatment approaches in the early management of acute spinal cord injury
- The long-term prognosis of Transient Global Amnesia: a systematic review
- The cellular mechanism by which the rostral ventromedial medulla acts on the spinal cord during chronic pain
- Psychedelic drugs and perception: a narrative review of the first era of research