Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors

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• 作者：Hyungju Park (1)
  Kyung-Seok Han (1) (2)
  Jinsoo Seo (3)
  Jaekwang Lee (1)
  Shashank M Dravid (4)
  Junsung Woo (1) (2)
  Heejung Chun (1)
  Sukhee Cho (3)
  Jin Young Bae (5)
  Heeyoung An (1) (6)
  Woohyun Koh (1) (2)
  Bo-Eun Yoon (1) (7)
  Rolando Berlinguer-Palmini (8)
  Guido Mannaioni (9)
  Stephen F Traynelis (10)
  Yong Chul Bae (5)
  Se-Young Choi (3)
  C Justin Lee (1) (2) (6)
  
  1. Center for Neural Science ; Korea Institute of Science and Technology (KIST) ; Seoul ; Korea
  2. Neuroscience Program ; University of Science and Technology (UST) ; Daejeon ; Korea
  3. Department of Physiology and Dental Research Institute ; Seoul National University School of Dentistry ; Seoul ; Korea
  4. Department of Pharmacology ; Creighton University ; Omaha ; NE ; USA
  5. Department of Oral Anatomy and Neurobiology ; School of Dentistry ; Kyungpook National University ; Daegu ; Korea
  6. KU-KIST Graduate School of Converging Science and Technology ; Seoul ; Korea
  7. Department of Nanobiomedical Science ; Dankook University ; Cheonan ; Korea
  8. School of Electrical and Electronic Engineering ; Institute of Neuroscience ; Newcastle University ; Newcastle upon Tyne ; UK
  9. Department of Pharmacology ; University of Florence ; Florence ; Italy
  10. Department of Pharmacology ; Emory University ; Atlanta ; GA ; USA
  
• 关键词：Astrocytes ; Bestrophin 1 ; Ca2+ ; activated anion channel ; Synaptic plasticity ; Glutamate ; NMDA receptor ; LTP ; PAR1
• 刊名：Molecular Brain
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：8
• 期：1
• 全文大小：1,903 KB
• 参考文献：1. Halassa MM, Fellin T, Haydon PG. The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med. 2007;13(2):54鈥?3. CrossRef
  2. Haydon PG, Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev. 2006;86(3):1009鈥?1. CrossRef
  3. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, et al. Glial cells in (patho)physiology. J Neurochem. 2012;121(1):4鈥?7. CrossRef
  4. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, et al. Astrocytic purinergic signaling coordinates synaptic networks. Science. 2005;310(5745):113鈥?. CrossRef
  5. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, et al. Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci. 2007;10(3):331鈥?. CrossRef
  6. Perea G, Araque A. Astrocytes potentiate transmitter release at single hippocampal synapses. Science. 2007;317(5841):1083鈥?. CrossRef
  7. Takano T, Kang J, Jaiswal JK, Simon SM, Lin JH, Yu Y, et al. Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proc Natl Acad Sci U S A. 2005;102(45):16466鈥?1. CrossRef
  8. Park H, Oh SJ, Han KS, Woo DH, Mannaioni G, Traynelis SF, et al. Bestrophin-1 encodes for the Ca2鈥?鈥夆垝activated anion channel in hippocampal astrocytes. J Neurosci. 2009;29(41):13063鈥?3. CrossRef
  9. Li D, Herault K, Isacoff EY, Oheim M, Ropert N. Optogenetic activation of LiGluR-expressing astrocytes evokes anion channel-mediated glutamate release. J Physiol. 2012;590(Pt 4):855鈥?3. CrossRef
  10. Woo DH, Han KS, Shim JW, Yoon BE, Kim E, Bae JY, et al. TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell. 2012;151(1):25鈥?0. CrossRef
  11. Park H, Han KS, Oh SJ, Jo S, Woo J, Yoon BE, et al. High glutamate permeability and distal localization of Best1 channel in CA1 hippocampal astrocyte. Mol Brain. 2013;6:54. CrossRef
  12. Fiacco TA, McCarthy KD. Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J Neurosci. 2004;24(3):722鈥?2. CrossRef
  13. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron. 2004;43(5):729鈥?3. CrossRef
  14. Shigetomi E, Bowser DN, Sofroniew MV, Khakh BS. Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J Neurosci. 2008;28(26):6659鈥?3. CrossRef
  15. Agulhon C, Fiacco TA, McCarthy KD. Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science. 2010;327(5970):1250鈥?. CrossRef
  16. Agulhon C, Petravicz J, McMullen AB, Sweger EJ, Minton SK, Taves SR, et al. What is the role of astrocyte calcium in neurophysiology? Neuron. 2008;59(6):932鈥?6. CrossRef
  17. Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, Dong X, et al. Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron. 2007;54(4):611鈥?6. CrossRef
  18. Wang F, Smith NA, Xu Q, Goldman S, Peng W, Huang JH, et al. Photolysis of caged Ca2+ but not receptor-mediated Ca2+ signaling triggers astrocytic glutamate release. J Neurosci. 2013;33(44):17404鈥?2. CrossRef
  19. Hollenberg MD, Saifeddine M, al-Ani B, Kawabata A. Proteinase-activated receptors: structural requirements for activity, receptor cross-reactivity, and receptor selectivity of receptor-activating peptides. Can J Physiol Pharmacol. 1997;75(7):832鈥?1. CrossRef
  20. Lee CJ, Mannaioni G, Yuan H, Woo DH, Gingrich MB, Traynelis SF. Astrocytic control of synaptic NMDA receptors. J Physiol. 2007;581(Pt 3):1057鈥?1. CrossRef
  21. Hamilton NB, Attwell D. Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci. 2010;11(4):227鈥?8. CrossRef
  22. Junge CE, Lee CJ, Hubbard KB, Zhang Z, Olson JJ, Hepler JR, et al. Protease-activated receptor-1 in human brain: localization and functional expression in astrocytes. Exp Neurol. 2004;188(1):94鈥?03. CrossRef
  23. Gingrich MB, Junge CE, Lyuboslavsky P, Traynelis SF. Potentiation of NMDA receptor function by the serine protease thrombin. J Neurosci. 2000;20(12):4582鈥?5.
  24. Mannaioni G, Orr AG, Hamill CE, Yuan H, Pedone KH, McCoy KL, et al. Plasmin potentiates synaptic N-methyl-D-aspartate receptor function in hippocampal neurons through activation of protease-activated receptor-1. J Biol Chem. 2008;283(29):20600鈥?1. CrossRef
  25. Han KS, Woo J, Park H, Yoon BJ, Choi S, Lee CJ. Channel-mediated astrocytic glutamate release via Bestrophin-1 targets synaptic NMDARs. Mol Brain. 2013;6:4. CrossRef
  26. Oh SJ, Han KS, Park H, Woo DH, Kim HY, Traynelis SF, et al. 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. CrossRef
  27. Almonte AG, Qadri LH, Sultan FA, Watson JA, Mount DJ, Rumbaugh G, et al. Protease-activated receptor-1 modulates hippocampal memory formation and synaptic plasticity. J Neurochem. 2013;124(1):109鈥?2. CrossRef
  28. Hires SA, Zhu Y, Tsien RY. Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters. Proc Natl Acad Sci U S A. 2008;105(11):4411鈥?. CrossRef
  29. Ventura A, Meissner A, Dillon CP, McManus M, Sharp PA, Van Parijs L, et al. Cre-lox-regulated conditional RNA interference from transgenes. Proc Natl Acad Sci U S A. 2004;101(28):10380鈥?. CrossRef
  30. Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, Anderson DJ, et al. Subregion- and cell type-restricted gene knockout in mouse brain. Cell. 1996;87(7):1317鈥?6. CrossRef
  31. Barbour B, Keller BU, Llano I, Marty A. Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells. Neuron. 1994;12(6):1331鈥?3. CrossRef
  32. Mennerick S, Zorumski CF. Presynaptic influence on the time course of fast excitatory synaptic currents in cultured hippocampal cells. J Neurosci. 1995;15(4):3178鈥?2.
  33. Diamond JS, Jahr CE. Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron. 1995;15(5):1097鈥?07. CrossRef
  34. Paoletti P, Ascher P, Neyton J. High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J Neurosci. 1997;17(15):5711鈥?5.
  35. Papouin T, Ladepeche L, Ruel J, Sacchi S, Labasque M, Hanini M, et al. Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell. 2012;150(3):633鈥?6. CrossRef
  36. Malenka RC, Nicoll RA. Long-term potentiation鈥揳 decade of progress? Science. 1999;285(5435):1870鈥?. CrossRef
  37. Cull-Candy SG, Leszkiewicz DN. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE. 2004;2004(255):re16.
  38. Volterra A, Liaudet N, Savtchouk I. Astrocyte Ca(2+) signalling: an unexpected complexity. Nat Rev Neurosci. 2014;15(5):327鈥?5. CrossRef
  39. Maggio N, Shavit E, Chapman J, Segal M. Thrombin induces long-term potentiation of reactivity to afferent stimulation and facilitates epileptic seizures in rat hippocampal slices: toward understanding the functional consequences of cerebrovascular insults. J Neurosci. 2008;28(3):732鈥?. CrossRef
  40. Gualandris A, Jones TE, Strickland S, Tsirka SE. Membrane depolarization induces calcium-dependent secretion of tissue plasminogen activator. J Neurosci. 1996;16(7):2220鈥?.
  41. Lochner JE, Honigman LS, Grant WF, Gessford SK, Hansen AB, Silverman MA, et al. Activity-dependent release of tissue plasminogen activator from the dendritic spines of hippocampal neurons revealed by live-cell imaging. J Neurobiol. 2006;66(6):564鈥?7. CrossRef
  42. Baranes D, Lederfein D, Huang YY, Chen M, Bailey CH, Kandel ER. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron. 1998;21(4):813鈥?5. CrossRef
  43. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, et al. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science. 2004;306(5695):487鈥?1. CrossRef
  44. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron. 2001;29(1):243鈥?4. CrossRef
  45. Kessels HW, Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron. 2009;61(3):340鈥?0. CrossRef
  46. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, et al. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell. 2006;125(4):775鈥?4. CrossRef
  47. Henneberger C, Papouin T, Oliet SH, Rusakov DA. Long-term potentiation depends on release of D-serine from astrocytes. Nature. 2010;463(7278):232鈥?. CrossRef
  48. Cetin A, Komai S, Eliava M, Seeburg PH, Osten P. Stereotaxic gene delivery in the rodent brain. Nat Protoc. 2006;1(6):3166鈥?3. CrossRef
  49. Seo J, Kim K, Jang S, Han S, Choi SY, Kim E. Regulation of hippocampal long-term potentiation and long-term depression by diacylglycerol kinase zeta. Hippocampus. 2012;22(5):1018鈥?6. CrossRef
  
• 刊物主题：Neurosciences; Neurology;
• 出版者：BioMed Central
• ISSN：1756-6606

文摘

Background Activation of G protein coupled receptor (GPCR) in astrocytes leads to Ca2+-dependent glutamate release via Bestrophin 1 (Best1) channel. Whether receptor-mediated glutamate release from astrocytes can regulate synaptic plasticity remains to be fully understood. Results We show here that Best1-mediated astrocytic glutamate activates the synaptic N-methyl-D-aspartate receptor (NMDAR) and modulates NMDAR-dependent synaptic plasticity. Our data show that activation of the protease-activated receptor 1 (PAR1) in hippocampal CA1 astrocytes elevates the glutamate concentration at Schaffer collateral-CA1 (SC-CA1) synapses, resulting in activation of GluN2A-containing NMDARs and NMDAR-dependent potentiation of synaptic responses. Furthermore, the threshold for inducing NMDAR-dependent long-term potentiation (LTP) is lowered when astrocytic glutamate release accompanied LTP induction, suggesting that astrocytic glutamate is significant in modulating synaptic plasticity. Conclusions Our results provide direct evidence for the physiological importance of channel-mediated astrocytic glutamate in modulating neural circuit functions.