Optogenetic countering of glial acidosis suppresses glial glutamate release and ischemic brain damage

Neuron

Volumn 81, Issue 2, 2014, Pages 314-320

  Beppu, Kaoru ^a   Sasaki, Takuya ^a   Tanaka, Kenji F ^b   Yamanaka, Akihiro ^c   Fukazawa, Yugo ^d   Shigemoto, Ryuichi ^a,e   Matsui, Ko ^a,f  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^f TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAERHODOPSIN; CHANNELRHODOPSIN 2; GLUCOSE; GLUTAMIC ACID; OXYGEN; RHODOPSIN; UNCLASSIFIED DRUG;

ACIDIFICATION; ACIDOSIS; ALKALINIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; EXCITOTOXICITY; GLIAL ACIDOSIS; IN VIVO STUDY; MOUSE; NERVE CELL LESION; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; OPTOGENETICS; PH; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACIDOSIS; ANIMALS; ANIMALS, NEWBORN; ANOXIA; ARCHAEAL PROTEINS; CEREBELLUM; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; GLUCOSE; GLUTAMIC ACID; HYPOXIA-ISCHEMIA, BRAIN; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, IMMUNOELECTRON; NEUROGLIA; OPTOGENETICS; RHODOPSIN; SODIUM CHANNEL BLOCKERS; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 84892745179     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.11.011     Document Type: Article

References (40)

1. Agulhon C., Fiacco T.A., McCarthy K.D. Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science 2010, 327:1250-1254.
2. Bergles D.E., Dzubay J.A., Jahr C.E. Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate. Proc. Natl. Acad. Sci. USA 1997, 94:14821-14825.
3. Berndt A., Yizhar O., Gunaydin L.A., Hegemann P., Deisseroth K. Bi-stable neural state switches. Nat. Neurosci. 2009, 12:229-234.
4. Camacho A., Montiel T., Massieu L. The anion channel blocker, 4,4'-dinitrostilbene-2,2'-disulfonic acid prevents neuronal death and excitatory amino acid release during glycolysis inhibition in the hippocampus in vivo. Neuroscience 2006, 142:1005-1017.
5. Cataldo A.M., Broadwell R.D. Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions. II. Choroid plexus and ependymal epithelia, endothelia and pericytes. J. Neurocytol. 1986, 15:511-524.
6. Cavelier P., Attwell D. Tonic release of glutamate by a DIDS-sensitive mechanism in rat hippocampal slices. J. Physiol. 2005, 564:397-410.
7. Fields R.D., Ni Y. Nonsynaptic communication through ATP release from volume-activated anion channels in axons. Sci. Signal. 2010, 3:ra73.
8. Gebhardt C., Körner R., Heinemann U. Delayed anoxic depolarizations in hippocampal neurons of mice lacking the excitatory amino acid carrier 1. J. Cereb. Blood Flow Metab. 2002, 22:569-575.
9. 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.
10. Halassa M.M., Haydon P.G. Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 2010, 72:335-355.
11. Hamann M., Rossi D.J., Mohr C., Andrade A.L., Attwell D. The electrical response of cerebellar Purkinje neurons to simulated ischaemia. Brain 2005, 128:2408-2420.
12. Han X., Chow B.Y., Zhou H., Klapoetke N.C., Chuong A., Rajimehr R., Yang A., Baratta M.V., Winkle J., Desimone R., Boyden E.S. A high-light sensitivity optical neural silencer: development and application to optogenetic control of non-human primate cortex. Front. Syst. Neurosci. 2011, 5:18.
13. Hines D.J., Haydon P.G. Inhibition of a SNARE-sensitive pathway in astrocytes attenuates damage following stroke. J. Neurosci. 2013, 33:4234-4240.
14. 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.
15. 2+-permeable channelrhodopsin CatCh. Nat. Neurosci. 2011, 14:513-518.
16. Lambert S., Oberwinkler J. Characterization of a proton-activated, outwardly rectifying anion channel. J. Physiol. 2005, 567:191-213.
17. Lau A., Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010, 460:525-542.
18. Li D., Hérault K., Isacoff E.Y., Oheim M., Ropert N. Optogenetic activation of LiGluR-expressing astrocytes evokes anion channel-mediated glutamate release. J. Physiol. 2012, 590:855-873.
19. Liu H.T., Tashmukhamedov B.A., Inoue H., Okada Y., Sabirov R.Z. Roles of two types of anion channels in glutamate release from mouse astrocytes under ischemic or osmotic stress. Glia 2006, 54:343-357.
20. Mutch W.A., Hansen A.J. Extracellular pH changes during spreading depression and cerebral ischemia: mechanisms of brain pH regulation. J. Cereb. Blood Flow Metab. 1984, 4:17-27.
21. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 2003, 100:13940-13945.
22. Orlowski P., Chappell M., Park C.S., Grau V., Payne S. Modelling of pH dynamics in brain cells after stroke. Interface Focus 2011, 1:408-416.
23. Panatier A., Vallée J., Haber M., Murai K.K., Lacaille J.C., Robitaille R. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 2011, 146:785-798.
24. Parajuli L.K., Nakajima C., Kulik A., Matsui K., Schneider T., Shigemoto R., Fukazawa Y. Quantitative regional and ultrastructural localization of the Ca(v)2.3 subunit of R-type calcium channel in mouse brain. J. Neurosci. 2012, 32:13555-13567.
25. Phillis J.W., Ren J., O'Regan M.H. Transporter reversal as a mechanism of glutamate release from the ischemic rat cerebral cortex: studies with DL-threo-beta-benzyloxyaspartate. Brain Res. 2000, 868:105-112.
26. Rossi D.J., Brady J.D., Mohr C. Astrocyte metabolism and signaling during brain ischemia. Nat. Neurosci. 2007, 10:1377-1386.
27. Saab A.S., Neumeyer A., Jahn H.M., Cupido A., Šimek A.A., Boele H.J., Scheller A., Le Meur K., Götz M., Monyer H., et al. Bergmann glial AMPA receptors are required for fine motor coordination. Science 2012, 337:749-753.
28. Sakai K., Shimizu H., Koike T., Furuya S., Watanabe M. Neutral amino acid transporter ASCT1 is preferentially expressed in L-Ser-synthetic/storing glial cells in the mouse brain with transient expression in developing capillaries. J. Neurosci. 2003, 23:550-560.
29. Sasaki T., Beppu K., Tanaka K.F., Fukazawa Y., Shigemoto R., Matsui K. Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation. Proc. Natl. Acad. Sci. USA 2012, 109:20720-20725.
30. Schurr A., Payne R.S., Miller J.J., Rigor B.M. Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia. Brain Res. 1997, 774:221-224.
31. Seki Y., Feustel P.J., Keller R.W., Tranmer B.I., Kimelberg H.K. Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker. Stroke 1999, 30:433-440.
32. Sun W., McConnell E., Pare J.F., Xu Q., Chen M., Peng W., Lovatt D., Han X., Smith Y., Nedergaard M. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 2013, 339:197-200.
33. Tanaka K.F., Ahmari S.E., Leonardo E.D., Richardson-Jones J.W., Budreck E.C., Scheiffele P., Sugio S., Inamura N., Ikenaka K., Hen R. Flexible Accelerated STOP Tetracycline Operator-knockin (FAST): a versatile and efficient new gene modulating system. Biol. Psychiatry 2010, 67:770-773.
34. Tanaka K.F., Matsui K., Sasaki T., Sano H., Sugio S., Fan K., Hen R., Nakai J., Yanagawa Y., Hasuwa H., et al. Expanding the repertoire of optogenetically targeted cells with an enhanced gene expression system. Cell Rep 2012, 2:397-406.
35. Tsunematsu T., Tabuchi S., Tanaka K.F., Boyden E.S., Tominaga M., Yamanaka A. Long-lasting silencing of orexin/hypocretin neurons using archaerhodopsin induces slow-wave sleep in mice. Behav. Brain Res. 2013, 255:64-74.
36. Watson B.D., Dietrich W.D., Busto R., Wachtel M.S., Ginsberg M.D. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann. Neurol. 1985, 17:497-504.
37. Weiss M.D., Rossignol C., Sumners C., Anderson K.J. A pH-dependent increase in neuronal glutamate efflux in vitro: possible involvement of ASCT1. Brain Res. 2005, 1056:105-112.
38. Woo D.H., Han K.S., Shim J.W., Yoon B.E., Kim E., Bae J.Y., Oh S.J., Hwang E.M., Marmorstein A.D., Bae Y.C., et al. TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell 2012, 151:25-40.
39. Zhang Z., Nguyen K.T., Barrett E.F., David G. Vesicular ATPase inserted into the plasma membrane of motor terminals by exocytosis alkalinizes cytosolic pH and facilitates endocytosis. Neuron 2010, 68:1097-1108.
40. Zifarelli G., Murgia A.R., Soliani P., Pusch M. Intracellular proton regulation of ClC-0. J. Gen. Physiol. 2008, 132:185-198.