Impaired glutamate recycling and GluN2B‐mediated neuronal calcium overload in mice lacking TGF‐β1 in the CNS
Abstract
Transforming growth factor β1 (TGF‐β1) is a pleiotropic cytokine expressed throughout the CNS. Previous studies demonstrated that TGF‐β1 contributes to maintain neuronal survival, but mechanistically this effect is not well understood. We generated a CNS‐specific TGF‐β1‐deficient mouse model to investigate the functional consequences of TGF‐β1‐deficiency in the adult mouse brain. We found that depletion of TGF‐β1 in the CNS resulted in a loss of the astrocyte glutamate transporter (GluT) proteins GLT‐1 (EAAT2) and GLAST (EAAT1) and decreased glutamate uptake in the mouse hippocampus. Treatment with TGF‐β1 induced the expression of GLAST and GLT‐1 in cultured astrocytes and enhanced astroglial glutamate uptake. Similar to GLT‐1‐deficient mice, CNS‐TGF‐β1‐deficient mice had reduced brain weight and neuronal loss in the CA1 hippocampal region. CNS‐TGF‐β1‐deficient mice showed GluN2B‐dependent aberrant synaptic plasticity in the CA1 area of the hippocampus similar to the glutamate transport inhibitor DL‐TBOA and these mice were highly sensitive to excitotoxic injury. In addition, hippocampal neurons from TGF‐β1‐deficient mice had elevated GluN2B‐mediated calcium signals in response to extrasynaptic glutamate receptor stimulation, whereas cells treated with TGF‐β1 exhibited reduced GluN2B‐mediated calcium signals. In summary, our study demonstrates a previously unrecognized function of TGF‐β1 in the CNS to control extracellular glutamate homeostasis and GluN2B‐mediated calcium responses in the mouse hippocampus.
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IL2TGF-β1-Tg-TGF-β1−/− mice did not express TGF-β1 in the brain or spinal cord and had no TGF-β1-producing T-cells in the CNS.
“we found that these animals did not express TGF-β1 in the brain or spinal cord and we found no TGF-β1-producing T-cells in the CNS of those animals33.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [33]
Apart from previously described physiologic changes, the only morphological changes in the brains of CNS-TGFβ1−/− mice were loss of microglia.
“Thus, apart from the physiologic changes described previously33, the only morphological changes in the brains of CNS-TGFβ1−/− mice were loss of microglia.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [33]
CNS-TGFβ1−/− mice have defects in extracellular glutamate homeostasis and synaptic plasticity.
“These animals have defects in extracellular glutamate homeostasis and synaptic plasticity33”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [33]
These mice have defects related to glutamate recycling and synaptic plasticity.
“We have previously reported that these mice have defects related to glutamate recycling and synaptic plasticity33.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [33]
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Cites
Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways
Hardingham, G. E., Fukunaga, Y., & Bading, H. (2002) · Nature Neuroscience · doi:10.1038/nn835 · Cited by 1,686 · see citing works
Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders
Hardingham, G. E., & Bading, H. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2911 · Cited by 1,644 · cited 4× · see citing works
“The relative contribution of extrasynaptic NMDARs had been shown to be relevant for neuronal survival: whereas stimulation of synaptic NMDARs leads to the build-up of a neuroprotective ‘‘shield’’, stimulation of extrasynaptic NMDARs promotes cell death (Hardingham and Bading, 2010).”
BackgroundResultInfluentialShankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., & Sabatini, B. L. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4970-06.2007 · Cited by 1,592 · see citing works
Self-citationRegulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2
Tavazoie, S. F., Alvarez, V. A., Ridenour, D. A., Kwiatkowski, D. J., & Sabatini, B. L. (2005) · Nature Neuroscience · doi:10.1038/nn1566 · Cited by 497 · see citing works
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Research works printed but not linked: 87
- Abutbul S Shapiro J Szaingurten-Solodkin I Levy N Carmy Y Baron R Jung S Monsonego A 2012 TGF-beta signaling through SMAD2/3 induces the quiescent microglial phenotype within the CNS environment Glia 60 7 1160 71 22511296
- Ageta H Ikegami S Miura M Masuda M Migishima R Hino T Takashima N Murayama A Sugino H Setou M 2010 Activin plays a key role in the maintenance of long-term memory and late-LTP Learn Mem 17 4 176 85 20332189
- Arnth-Jensen N Jabaudon D Scanziani M 2002 Cooperation between independent hippocampal synapses is controlled by glutamate uptake Nat Neurosci 5 4 325 31 11896395
- Bannerman P Hahn A Soulika A Gallo V Pleasure D 2007 Astrogliosis in EAE spinal cord: derivation from radial glia, and relationships to oligodendroglia Glia 55 1 57 64 17009237
- Beart PM O’Shea RD 2007 Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement Br J Pharmacol 150 1 5 17 17088867 PMC2013845
- Bellesi M Melone M Gubbini A Battistacci S Conti F 2009 GLT-1 upregulation impairs prepulse inhibition of the startle reflex in adult rats Glia 57 7 703 13 18985735
- Ben-Ari Y Cossart R 2000 Kainate, a double agent that generates seizures: two decades of progress Trends Neurosci 23 11 580 7 11074268
- Boche D Cunningham C Gauldie J Perry VH 2003 Transforming growth factor-beta 1-mediated neuroprotection against excitotoxic injury in vivo J Cereb Blood Flow Metab 23 10 1174 82 14526228
- Brigman JL Wright T Talani G Prasad-Mulcare S Jinde S Seabold GK Mathur P Davis MI Bock R Gustin RM 2010 Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning J Neurosci 30 13 4590 600 20357110 PMC2869199
- Brionne TC Tesseur I Masliah E Wyss-Coray T 2003 Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain Neuron 40 6 1133 45 14687548
- Carmona MA Murai KK Wang L Roberts AJ Pasquale EB 2009 Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport Proc Natl Acad Sci U S A 106 30 12524 9 19592509 PMC2718351
- Carrier Y Yuan J Kuchroo VK Weiner HL 2007 Th3 cells in peripheral tolerance. I. Induction of Foxp3-positive regulatory T cells by Th3 cells derived from TGF-beta T cell-transgenic mice J Immunol 178 1 179 85 17182553
- Chaudhry FA Lehre KP van Lookeren Campagne M Ottersen OP Danbolt NC Storm-Mathisen J 1995 Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry Neuron 15 3 711 20 7546749
- Citri A Malenka RC 2008 Synaptic plasticity: multiple forms, functions, and mechanisms Neuropsychopharmacology 33 1 18 41 17728696
- Condorelli DF Dell’Albani P Corsaro M Giuffrida R Caruso A Trovato Salinaro A Spinella F Nicoletti F Albanese V Giuffrida Stella AM 1997 Metabotropic glutamate receptor expression in cultured rat astrocytes and human gliomas Neurochem Res 22 9 1127 33 9251103
- Coulter DA Eid T 2012 Astrocytic regulation of glutamate homeostasis in epilepsy Glia 60 8 1215 26 22592998 PMC3375386
- Cull-Candy SG Leszkiewicz DN 2004 Role of distinct NMDA receptor subtypes at central synapses Sci STKE 2004 255 re16 15494561
- Danbolt NC 2001 Glutamate uptake Prog Neurobiol 65 1 1 105 11369436
- Dingledine R Borges K Bowie D Traynelis SF 1999 The glutamate receptor ion channels Pharmacol Rev 51 1 7 61 10049997
- Flanders KC Ludecke G Engels S Cissel DS Roberts AB Kondaiah P Lafyatis R Sporn MB Unsicker K 1991 Localization and actions of transforming growth factor-beta s in the embryonic nervous system Development 113 1 183 91 1764993
- Flanders KC Ren RF Lippa CF 1998 Transforming growth factor-betas in neurodegenerative disease Prog Neurobiol 54 1 71 85 9460794
- Fuller L Dailey ME 2007 Preparation of rodent hippocampal slice cultures CSH Protoc pdb prot4848 21356949
- Gegelashvili G Danbolt NC Schousboe A 1997 Neuronal soluble factors differentially regulate the expression of the GLT1 and GLAST glutamate transporters in cultured astroglia J Neurochem 69 6 2612 5 9375696
- Gegelashvili G Dehnes Y Danbolt NC Schousboe A 2000 The high-affinity glutamate transporters GLT1, GLAST, and EAAT4 are regulated via different signalling mechanisms Neurochem Int 37 2–3 163 70 10812201
- Gorelik L Constant S Flavell RA 2002 Mechanism of transforming growth factor beta-induced inhibition of T helper type 1 differentiation J Exp Med 195 11 1499 505 12045248 PMC2193549
- Gouix E Leveille F Nicole O Melon C Had-Aissouni L Buisson A 2009 Reverse glial glutamate uptake triggers neuronal cell death through extrasynaptic NMDA receptor activation Mol Cell Neurosci 40 4 463 73 19340933
- Hamby ME Hewett JA Hewett SJ 2010 Smad3-dependent signaling underlies the TGF-beta1-mediated enhancement in astrocytic iNOS expression Glia 58 11 1282 91 20607716 PMC4451602
- Hardingham GE 2009 Coupling of the NMDA receptor to neuroprotective and neurodestructive events Biochem Soc Trans 37 Pt 6 1147 60 19909238 PMC2837198
- Hendricson AW Miao CL Lippmann MJ Morrisett RA 2002 Ifenprodil and ethanol enhance NMDA receptor-dependent long-term depression J Pharmacol Exp Ther 301 3 938 44 12023522
- Henrich-Noack P Prehn JH Krieglstein J 1996 TGF-beta 1 protects hippocampal neurons against degeneration caused by transient global ischemia. Dose-response relationship and potential neuroprotective mechanisms Stroke 27 9 1609 14 discussion 1615 8784137
- Hrabetova S Sacktor TC 1997 Long-term potentiation and long-term depression are induced through pharmacologically distinct NMDA receptors Neurosci Lett 226 2 107 10 9159501
- Hrabetova S Serrano P Blace N Tse HW Skifter DA Jane DE Monaghan DT Sacktor TC 2000 Distinct NMDA receptor subpopulations contribute to long-term potentiation and long-term depression induction J Neurosci 20 12 RC81 10827202 PMC6772441
- Hu NW Klyubin I Anwy R Rowan MJ 2009 GluN2B subunit-containing NMDA receptor antagonists prevent Abeta-mediated synaptic plasticity disruption in vivo Proc Natl Acad Sci U S A 106 48 20504 9 19918059 PMC2787128
- Huang YH Sinha SR Tanaka K Rothstein JD Bergles DE 2004 Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons J Neurosci 24 19 4551 9 15140926 PMC6729403
- Katagiri H Tanaka K Manabe T 2001 Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction Eur J Neurosci 14 3 547 53 11553304
- Kawahara K Hosoya R Sato H Tanaka M Nakajima T Iwabuchi S 2002 Selective blockade of astrocytic glutamate transporter GLT-1 with dihydrokainate prevents neuronal death during ouabain treatment of astrocyte/neuron cocultures Glia 40 3 337 49 12420313
- Kiryk A Aida T Tanaka K Banerjee P Wilczynski GM Meyza K Knapska E Filipkowski RK Kaczmarek L Danysz W 2008 Behavioral characterization of GLT1 (+/−) mice as a model of mild glutamatergic hyperfunction Neurotox Res 13 1 19 30 18367437
- Klempt ND Sirimanne E Gunn AJ Klempt M Singh K Williams C Gluckman PD 1992 Hypoxia-ischemia induces transforming growth factor beta 1 mRNA in the infant rat brain Brain Res Mol Brain Res 13 1–2 93 101 1315921
- Konig HG Kogel D Rami A Prehn JH 2005 TGF-{beta}1 activates two distinct type I receptors in neurons: implications for neuronal NF-{kappa}B signaling J Cell Biol 168 7 1077 86 15781474 PMC2171851
- Krieglstein K Strelau J Schober A Sullivan A Unsicker K 2002 TGF-beta and the regulation of neuron survival and death J Physiol Paris 96 1–2 25 30 11755780
- Kulkarni AB Huh CG Becker D Geiser A Lyght M Flanders KC Roberts AB Sporn MB Ward JM Karlsson S 1993 Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death Proc Natl Acad Sci U S A 90 2 770 4 8421714 PMC45747
- Kutsuwada T Sakimura K Manabe T Takayama C Katakura N Kushiya E Natsume R Watanabe M Inoue Y Yagi T 1996 Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice Neuron 16 2 333 44 8789948
- Lau A Tymianski M Glutamate receptors, neurotoxicity and neurodegeneration Pflugers Arch 20229265
- Levenson J Weeber E Selcher JC Kategaya LS Sweatt JD Eskin A 2002 Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake Nat Neurosci 5 2 155 61 11788834
- Li MO Flavell RA 2008 TGF-beta: a master of all T cell trades Cell 134 3 392 404 18692464 PMC3677783
- Li S Hong S Shepardson NE Walsh DM Shankar GM Selkoe D 2009 Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake Neuron 62 6 788 801 19555648 PMC2702854
- Lipton SA 2006 Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond Nat Rev Drug Discov 5 2 160 70 16424917
- Liu L Wong TP Pozza MF Lingenhoehl K Wang Y Sheng M Auberson YP Wang YT 2004 Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity Science 304 5673 1021 4 15143284
- Maragakis NJ Rothstein JD 2004 Glutamate transporters: animal models to neurologic disease Neurobiol Dis 15 3 461 73 15056453
- Massague J Blain SW Lo RS 2000 TGFbeta signaling in growth control, cancer, and heritable disorders Cell 103 2 295 309 11057902
- Massey PV Johnson BE Moult PR Auberson YP Brown MW Molnar E Collingridge GL Bashir ZI 2004 Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression J Neurosci 24 36 7821 8 15356193 PMC6729941
- Momiyama A 2000 Distinct synaptic and extrasynaptic NMDA receptors identified in dorsal horn neurones of the adult rat spinal cord J Physiol 523 Pt 3 621 8 10718742 PMC2269820
- Morishita W Lu W Smith GB Nicoll RA Bear MF Malenka RC 2007 Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression Neuropharmacology 52 1 71 6 16899258
- Nie H Weng HR 2010 Impaired glial glutamate uptake induces extrasynaptic glutamate spillover in the spinal sensory synapses of neuropathic rats J Neurophysiol 103 5 2570 80 20220084 PMC2867569
- Okamoto S Pouladi MA Talantova M Yao D Xia P Ehrnhoefer DE Zaidi R Clemente A Kaul M Graham RK 2009 Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin Nat Med 15 12 1407 13 19915593 PMC2789858
- Potier B Billard JM Riviere S Sinet PM Denis I Champeil-Potokar G Grintal B Jouvenceau A Kollen M Dutar P 2010 Reduction in glutamate uptake is associated with extrasynaptic NMDA and metabotropic glutamate receptor activation at the hippocampal CA1 synapse of aged rats Aging Cell 9 5 722 35 20569241
- Prehn JH Backhauss C Krieglstein J 1993a Transforming growth factor-beta 1 prevents glutamate neurotoxicity in rat neocortical cultures and protects mouse neocortex from ischemic injury in vivo J Cereb Blood Flow Metab 13 3 521 5 8097519
- Prehn JH Bindokas VP Marcuccilli CJ Krajewski S Reed JC Miller RJ 1994 Regulation of neuronal Bcl2 protein expression and calcium homeostasis by transforming growth factor type beta confers wide-ranging protection on rat hippocampal neurons Proc Natl Acad Sci U S A 91 26 12599 603 7809085 PMC45486
- Prehn JH Miller RJ 1996 Opposite effects of TGF-beta 1 on rapidly- and slowly-triggered excitotoxic injury Neuropharmacology 35 3 249 56 8783198
- Prehn JH Peruche B Unsicker K Krieglstein J 1993b Isoform-specific effects of transforming growth factors-beta on degeneration of primary neuronal cultures induced by cytotoxic hypoxia or glutamate J Neurochem 60 5 1665 72 8097233
- Reilly JF Maher PA Kumari VG 1998 Regulation of astrocyte GFAP expression by TGF-beta1 and FGF-2 Glia 22 2 202 10 9537840
- Rogawski MA Wenk GL 2003 The neuropharmacological basis for the use of memantine in the treatment of Alzheimer’s disease CNS Drug Rev 9 3 275 308 14530799 PMC6741669
- Sakimura K Kutsuwada T Ito I Manabe T Takayama C Kushiya E Yagi T Aizawa S Inoue Y Sugiyama H 1995 Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit Nature 373 6510 151 5 7816096
- Schmierer B Hill CS 2007 TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility Nat Rev Mol Cell Biol 8 12 970 82 18000526
- Schulz R Vogel T Mashima T Tsuruo T Krieglstein K 2009 Involvement of Fractin in TGF-beta-induced apoptosis in oligodendroglial progenitor cells Glia 57 15 1619 29 19330858
- Scimemi A Fine A Kullmann DM Rusakov DA 2004 NR2B-containing receptors mediate cross talk among hippocampal synapses J Neurosci 24 20 4767 77 15152037 PMC3379686
- Shull MM Ormsby I Kier AB Pawlowski S Diebold RJ Yin M Allen R Sidman C Proetzel G Calvin D 1992 Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease Nature 359 6397 693 9 1436033 PMC3889166
- Sjostrom PJ Turrigiano GG Nelson SB 2003 Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors Neuron 39 4 641 54 12925278
- Sprengel R Suchanek B Amico C Brusa R Burnashev N Rozov A Hvalby O Jensen V Paulsen O Andersen P 1998 Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo Cell 92 2 279 89 9458051
- Steigerwald F Schulz TW Schenker LT Kennedy MB Seeburg PH Kohr G 2000 C-Terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors J Neurosci 20 12 4573 81 10844027 PMC6772457
- Stipursky J Gomes FC 2007 TGF-beta1/SMAD signaling induces astrocyte fate commitment in vitro: implications for radial glia development Glia 55 10 1023 33 17549683
- Stocca G Vicini S 1998 Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons J Physiol 507 Pt 1 13 24 9490809 PMC2230772
- Sullivan R Rauen T Fischer F Wiessner M Grewer C Bicho A Pow DV 2004 Cloning, transport properties, and differential localization of two splice variants of GLT-1 in the rat CNS: implications for CNS glutamate homeostasis Glia 45 2 155 69 14730709
- Swanson RA Liu J Miller JW Rothstein JD Farrell K Stein BA Longuemare MC 1997 Neuronal regulation of glutamate transporter subtype expression in astrocytes J Neurosci 17 3 932 40 8994048 PMC6573161
- Takayasu Y Iino M Shimamoto K Tanaka K Ozawa S 2006 Glial glutamate transporters maintain one-to-one relationship at the climbing fiber-Purkinje cell synapse by preventing glutamate spillover J Neurosci 26 24 6563 72 16775144 PMC6674041
- Tanaka K Watase K Manabe T Yamada K Watanabe M Takahashi K Iwama H Nishikawa T Ichihara N Kikuchi T 1997 Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1 Science 276 5319 1699 702 9180080
- Tesseur I Wyss-Coray T 2006 A role for TGF-beta signaling in neurodegeneration: evidence from genetically engineered models Curr Alzheimer Res 3 5 505 13 17168649
- Tesseur I Zou K Esposito L Bard F Berber E Can JV Lin AH Crews L Tremblay P Mathews P 2006 Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer’s pathology J Clin Invest 116 11 3060 9 17080199 PMC1626127
- Tovar KR Westbrook GL 1999 The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro J Neurosci 19 10 4180 8 10234045 PMC6782704
- Tzingounis AV Wadiche JI 2007 Glutamate transporters: confining runaway excitation by shaping synaptic transmission Nat Rev Neurosci 8 12 935 47 17987031
- Unsicker K Flanders KC Cissel DS Lafyatis R Sporn MB 1991 Transforming growth factor beta isoforms in the adult rat central and peripheral nervous system Neuroscience 44 3 613 25 1754055
- Unsicker K Meier C Krieglstein K Sartor BM Flanders KC 1996 Expression, localization, and function of transforming growth factor-beta s in embryonic chick spinal cord, hindbrain, and dorsal root ganglia J Neurobiol 29 2 262 76 8821181
- Wang Q Yu S Simonyi A Sun GY Sun AY 2005 Kainic acid-mediated excitotoxicity as a model for neurodegeneration Mol Neurobiol 31 1–3 3 16 15953808
- Waxman EA Lynch DR 2005 N-methyl-D-aspartate receptor subtypes: multiple roles in excitotoxicity and neurological disease Neuroscientist 11 1 37 49 15632277
- Wiessner C Gehrmann J Lindholm D Topper R Kreutzberg GW Hossmann KA 1993 Expression of transforming growth factor-beta 1 and interleukin-1 beta mRNA in rat brain following transient forebrain ischemia Acta Neuropathol 86 5 439 46 8310794
- Xia P Chen HS Zhang D Lipton SA 2010 Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses J Neurosci 30 33 11246 50 20720132 PMC2932667
- Yoshimura Y Ohmura T Komatsu Y 2003 Two forms of synaptic plasticity with distinct dependence on age, experience, and NMDA receptor subtype in rat visual cortex J Neurosci 23 16 6557 66 12878697 PMC6740618
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- Authors
- Koeglsperger, T., Li, S., Brenneis, C., Saulnier, J. L., Mayo, L., Carrier, Y., Selkoe, D. J., & Weiner, H. L.
- Affiliations
- Department of Neurology Center for Neurologic Diseases Brigham and Women's Hospital Harvard Medical School Boston Massachusetts
- Department of Neurology F.M. Kirby Neurobiology Center Children's Hospital Boston Boston Massachusetts
- Department of Neurobiology Harvard Medical School Boston Massachusetts
- Venue
- Glia
- Publisher
- Wiley
- Published
- 2013-03-28
- Volume
- 61
- Issue
- 6
- Pages
- 985-1002
- ISSN
- 0894-1491
- 1098-1136
- PMC
- PMC3981075
- Cited by
- 67
- References
- 4
- Language
- en
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