BDNF regulates the expression and distribution of vesicular glutamate transporters in cultured hippocampal neurons

Melo, CV; Mele, M; Curcio, M; Comprido, D; Gomes Da Silva, Carla; Duarte, CB

doi:10.1371/journal.pone.0053793

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BDNF regulates the expression and distribution of vesicular glutamate transporters in cultured hippocampal neurons

Melo, CV; Mele, M; Curcio, M et al.

2013 • In PLoS ONE

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https://hdl.handle.net/2268/182546

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10.1371/journal.pone.0053793

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Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Melo, CV; Center for Neuroscience of Coimbra > 2013

Mele, M; Center for Neuroscience of Coimbra > 2013

Curcio, M; Center for Neuroscience of Coimbra > 2013

Comprido, D; Center for Neuroscience of Coimbra > 2013

Gomes Da Silva, Carla ; Center for Neuroscience of Coimbra > 2013

Duarte, CB; Center for Neuroscience of Coimbra > 2013

Language :

English

Title :

BDNF regulates the expression and distribution of vesicular glutamate transporters in cultured hippocampal neurons

Publication date :

January 2013

Journal title :

PLoS ONE

eISSN :

1932-6203

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Public Library of Science, San Franscisco, United States - California

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 06 June 2015

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Poo MM, (2001) Neurotrophins as synaptic modulators. Nat Rev Neurosci 2: 24-32.
Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S, (2010) Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70: 271-288.
Almeida RD, Manadas BJ, Melo CV, Gomes JR, Mendes CS, et al. (2005) Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ 12: 1329-1343.
Murray PS, Holmes PV, (2011) An overview of brain-derived neurotrophic factor and implications for excitotoxic vulnerability in the hippocampus. Int J Pept 2011: 654085.
Wang GX, Poo MM, (2005) Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434: 898-904.
Li Y, Jia YC, Cui K, Li N, Zheng ZY, et al. (2005) Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434: 894-898.
Ji Y, Pang PT, Feng L, Lu B, (2005) Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat Neurosci 8: 164-172.
An JJ, Gharami K, Liao GY, Woo NH, Lau AG, et al. (2008) Distinct role of long 3′ UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134: 175-187.
Kwon M, Fernandez JR, Zegarek GF, Lo SB, Firestein BL, (2011) BDNF-promoted increases in proximal dendrites occur via CREB-dependent transcriptional regulation of cypin. J Neurosci 31: 9735-9745.
Linnarsson S, Bjorklund A, Ernfors P, (1997) Learning deficit in BDNF mutant mice. Eur J Neurosci 9: 2581-2587.
Minichiello L, Korte M, Wolfer D, Kuhn R, Unsicker K, et al. (1999) Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24: 401-414.
Liu IY, Lyons WE, Mamounas LA, Thompson RF, (2004) Brain-derived neurotrophic factor plays a critical role in contextual fear conditioning. J Neurosci 24: 7958-7963.
Bekinschtein P, Cammarota M, Katche C, Slipczuk L, Rossato JI, et al. (2008) BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A 105: 2711-2716.
Korte M, Carroll P, Wolf E, Brem G, Thoenen H, et al. (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92: 8856-8860.
Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, et al. (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16: 1137-1145.
Chen G, Kolbeck R, Barde YA, Bonhoeffer T, Kossel A, (1999) Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation. J Neurosci 19: 7983-7990.
Xu B, Gottschalk W, Chow A, Wilson RI, Schnell E, et al. (2000) The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J Neurosci 20: 6888-6897.
Minichiello L, Calella AM, Medina DL, Bonhoeffer T, Klein R, et al. (2002) Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36: 121-137.
Rodriguez-Tebar A, Dechant G, Barde YA, (1990) Binding of brain-derived neurotrophic factor to the nerve growth factor receptor. Neuron 4: 487-492.
Huang EJ, Reichardt LF, (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642.
Ouyang Y, Kantor D, Harris KM, Schuman EM, Kennedy MB, (1997) Visualization of the distribution of autophosphorylated calcium/calmodulin-dependent protein kinase II after tetanic stimulation in the CA1 area of the hippocampus. J Neurosci 17: 5416-5427.
Gartner A, Polnau DG, Staiger V, Sciarretta C, Minichiello L, et al. (2006) Hippocampal long-term potentiation is supported by presynaptic and postsynaptic tyrosine receptor kinase B-mediated phospholipase Cgamma signaling. J Neurosci 26: 3496-3504.
Gruart A, Sciarretta C, Valenzuela-Harrington M, Delgado-Garcia JM, Minichiello L, (2007) Mutation at the TrkB PLC{gamma}-docking site affects hippocampal LTP and associative learning in conscious mice. Learn Mem 14: 54-62.
Du JL, Poo MM, (2004) Rapid BDNF-induced retrograde synaptic modification in a developing retinotectal system. Nature 429: 878-883.
Amaral MD, Pozzo-Miller L, (2007) TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J Neurosci 27: 5179-5189.
Reichardt LF, (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361: 1545-1564.
Grewal SS, York RD, Stork PJ, (1999) Extracellular-signal-regulated kinase signalling in neurons. Curr Opin Neurobiol 9: 544-553.
Barnabe-Heider F, Miller FD, (2003) Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J Neurosci 23: 5149-5160.
Datta R, Kojima H, Yoshida K, Kufe D, (1997) Caspase-3-mediated cleavage of protein kinase C theta in induction of apoptosis. J Biol Chem 272: 20317-20320.
Bonni A, Brunet A, West AE, Datta SR, Takasu MA, et al. (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and-independent mechanisms. Science 286: 1358-1362.
Kelleher RJ, 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116: 467-479.
Brunet A, Datta SR, Greenberg ME, (2001) Transcription-dependent and-independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11: 297-305.
Yoshii A, Constantine-Paton M, (2007) BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat Neurosci 10: 702-711.
Takei N, Inamura N, Kawamura M, Namba H, Hara K, et al. (2004) Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24: 9760-9769.
Cunha C, Brambilla R, Thomas KL, (2010) A simple role for BDNF in learning and memory? Front Mol Neurosci 3: 1.
Manadas B, Santos AR, Szabadfi K, Gomes JR, Garbis SD, et al. (2009) BDNF-induced changes in the expression of the translation machinery in hippocampal neurons: protein levels and dendritic mRNA. J Proteome Res 8: 4536-4552.
Caldeira MV, Melo CV, Pereira DB, Carvalho R, Correia SS, et al. (2007) Brain-derived neurotrophic factor regulates the expression and synaptic delivery of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons. J Biol Chem 282: 12619-12628.
Caldeira MV, Melo CV, Pereira DB, Carvalho RF, Carvalho AL, et al. (2007) BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol Cell Neurosci 35: 208-219.
Jovanovic JN, Czernik AJ, Fienberg AA, Greengard P, Sihra TS, (2000) Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat Neurosci 3: 323-329.
Bamji SX, Rico B, Kimes N, Reichardt LF, (2006) BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions. J Cell Biol 174: 289-299.
Tyler WJ, Pozzo-Miller LD, (2001) BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J Neurosci 21: 4249-4258.
Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, et al. (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304: 1815-1819.
Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, et al. (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci U S A 101: 7158-7163.
Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, et al. (2005) Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci 25: 6221-6234.
Santos MS, Li H, Voglmaier SM, (2009) Synaptic vesicle protein trafficking at the glutamate synapse. Neuroscience 158: 189-203.
Balschun D, Moechars D, Callaerts-Vegh Z, Vermaercke B, Van Acker N, et al. (2010) Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 20: 684-693.
Tordera RM, Totterdell S, Wojcik SM, Brose N, Elizalde N, et al. (2007) Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1). Eur J Neurosci 25: 281-290.
Miyazaki T, Fukaya M, Shimizu H, Watanabe M, (2003) Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur J Neurosci 17: 2563-2572.
Dal Bo G, Berube-Carriere N, Mendez JA, Leo D, Riad M, et al. (2008) Enhanced glutamatergic phenotype of mesencephalic dopamine neurons after neonatal 6-hydroxydopamine lesion. Neuroscience 156: 59-70.
Butts BD, Hudson HR, Linseman DA, Le SS, Ryan KR, et al. (2005) Proteasome inhibition elicits a biphasic effect on neuronal apoptosis via differential regulation of pro-survival and pro-apoptotic transcription factors. Mol Cell Neurosci 30: 279-289.
Messaoudi E, Ying SW, Kanhema T, Croll SD, Bramham CR, (2002) Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci 22: 7453-7461.
Takei N, Kawamura M, Hara K, Yonezawa K, Nawa H, (2001) Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: comparison with the effects of insulin. J Biol Chem 276: 42818-42825.
Santos AR, Comprido D, Duarte CB, (2010) Regulation of local translation at the synapse by BDNF. Prog Neurobiol 92: 505-516.
Nye SH, Squinto SP, Glass DJ, Stitt TN, Hantzopoulos P, et al. (1992) K-252a and staurosporine selectively block autophosphorylation of neurotrophin receptors and neurotrophin-mediated responses. Mol Biol Cell 3: 677-686.
Ip NY, Li Y, Yancopoulos GD, Lindsay RM, (1993) Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J Neurosci 13: 3394-3405.
Lamballe F, Klein R, Barbacid M, (1991) trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66: 967-979.
Dorsey SG, Bambrick LL, Balice-Gordon RJ, Krueger BK, (2002) Failure of brain-derived neurotrophic factor-dependent neuron survival in mouse trisomy 16. J Neurosci 22: 2571-2578.
Zheng WH, Quirion R, (2004) Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival. J Neurochem 89: 844-852.
Nelson TJ, Sun MK, Hongpaisan J, Alkon DL, (2008) Insulin, PKC signaling pathways and synaptic remodeling during memory storage and neuronal repair. Eur J Pharmacol 585: 76-87.
Katsuki H, Itsukaichi Y, Matsuki N, (2000) Distinct signaling pathways involved in multiple effects of basic fibroblast growth factor on cultured rat hippocampal neurons. Brain Res 885: 240-250.
Hong J, Yoshida K, Rosner MR, (2002) Characterization of a cysteine proteinase inhibitor induced during neuronal cell differentiation. J Neurochem 81: 922-934.
McCusker RH, McCrea K, Zunich S, Dantzer R, Broussard SR, et al. (2006) Insulin-like growth factor-I enhances the biological activity of brain-derived neurotrophic factor on cerebrocortical neurons. J Neuroimmunol 179: 186-190.
Kwon YK, (1997) Expression of brain-derived neurotrophic factor mRNA stimulated by basic fibroblast growth factor and platelet-derived growth factor in rat hippocampal cell line. Mol Cells 7: 320-325.
Pereira DB, Rebola N, Rodrigues RJ, Cunha RA, Carvalho AP, et al. (2006) Trkb receptors modulation of glutamate release is limited to a subset of nerve terminals in the adult rat hippocampus. J Neurosci Res 83: 832-844.
Amaral MD, Pozzo-Miller L, (2012) Intracellular Ca2+ stores and Ca2+ influx are both required for BDNF to rapidly increase quantal vesicular transmitter release. Neural Plast 2012: 203536.
Tartaglia N, Du J, Tyler WJ, Neale E, Pozzo-Miller L, et al. (2001) Protein synthesis-dependent and-independent regulation of hippocampal synapses by brain-derived neurotrophic factor. J Biol Chem 276: 37585-37593.
Giralt A, Carreton O, Lao-Peregrin C, Martin ED, Alberch J, (2011) Conditional BDNF release under pathological conditions improves Huntington's disease pathology by delaying neuronal dysfunction. Mol Neurodegener 6: 71.
Ni B, Rosteck PR Jr, Nadi NS, Paul SM, (1994) Cloning and expression of a cDNA encoding a brain-specific Na(+)-dependent inorganic phosphate cotransporter. Proc Natl Acad Sci U S A 91: 5607-5611.
Aihara Y, Mashima H, Onda H, Hisano S, Kasuya H, et al. (2000) Molecular cloning of a novel brain-type Na(+)-dependent inorganic phosphate cotransporter. J Neurochem 74: 2622-2625.
Takamori S, Rhee JS, Rosenmund C, Jahn R, (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407: 189-194.
Zhang GR, Geller AI, (2010) A helper virus-free HSV-1 vector containing the vesicular glutamate transporter-1 promoter supports expression preferentially in VGLUT1-containing glutamatergic neurons. Brain Res 1331: 12-19.
Zhang GR, Li X, Cao H, Zhao H, Geller AI, (2011) The vesicular glutamate transporter-1 upstream promoter and first intron each support glutamatergic-specific expression in rat postrhinal cortex. Brain Res 1377: 1-12.
Li T, Bai L, Li J, Igarashi S, Ghishan FK, (2008) Sp1 is required for glucose-induced transcriptional regulation of mouse vesicular glutamate transporter 2 gene. Gastroenterology 134: 1994-2003.
Yelamanchili SV, Pendyala G, Brunk I, Darna M, Albrecht U, et al. (2006) Differential sorting of the vesicular glutamate transporter 1 into a defined vesicular pool is regulated by light signaling involving the clock gene Period2. J Biol Chem 281: 15671-15679.
Ko GY, Ko ML, Dryer SE, (2001) Circadian regulation of cGMP-gated cationic channels of chick retinal cones. Erk MAP Kinase and Ca2+/calmodulin-dependent protein kinase II. Neuron 29: 255-266.
Yokota S, Yamamoto M, Moriya T, Akiyama M, Fukunaga K, et al. (2001) Involvement of calcium-calmodulin protein kinase but not mitogen-activated protein kinase in light-induced phase delays and Per gene expression in the suprachiasmatic nucleus of the hamster. J Neurochem 77: 618-627.
Tordera RM, Pei Q, Sharp T, (2005) Evidence for increased expression of the vesicular glutamate transporter, VGLUT1, by a course of antidepressant treatment. J Neurochem 94: 875-883.
Mark KA, Quinton MS, Russek SJ, Yamamoto BK, (2007) Dynamic changes in vesicular glutamate transporter 1 function and expression related to methamphetamine-induced glutamate release. J Neurosci 27: 6823-6831.
Kawasaki A, Shutoh F, Nogami H, Hisano S, (2006) VGLUT2 expression is up-regulated in neurohypophysial vasopressin neurons of the rat after osmotic stimulation. Neurosci Res 56: 124-127.
Smith RE, Haroutunian V, Davis KL, Meador-Woodruff JH, (2001) Vesicular glutamate transporter transcript expression in the thalamus in schizophrenia. Neuroreport 12: 2885-2887.
Gomes RA, Hampton C, El-Sabeawy F, Sabo SL, McAllister AK, (2006) The dynamic distribution of TrkB receptors before, during, and after synapse formation between cortical neurons. J Neurosci 26: 11487-11500.
Numakawa T, Yamagishi S, Adachi N, Matsumoto T, Yokomaku D, et al. (2002) Brain-derived neurotrophic factor-induced potentiation of Ca(2+) oscillations in developing cortical neurons. J Biol Chem 277: 6520-6529.
Matsumoto T, Numakawa T, Yokomaku D, Adachi N, Yamagishi S, et al. (2006) Brain-derived neurotrophic factor-induced potentiation of glutamate and GABA release: different dependency on signaling pathways and neuronal activity. Mol Cell Neurosci 31: 70-84.
Numakawa T, Kumamaru E, Adachi N, Yagasaki Y, Izumi A, et al. (2009) Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-gamma signaling for glutamate release via a glutamate transporter. Proc Natl Acad Sci U S A 106: 647-652.
Li YX, Xu Y, Ju D, Lester HA, Davidson N, et al. (1998) Expression of a dominant negative TrkB receptor, T1, reveals a requirement for presynaptic signaling in BDNF-induced synaptic potentiation in cultured hippocampal neurons. Proc Natl Acad Sci U S A 95: 10884-10889.
Monteggia LM, Barrot M, Powell CM, Berton O, Galanis V, et al. (2004) Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc Natl Acad Sci U S A 101: 10827-10832.
Heldt SA, Stanek L, Chhatwal JP, Ressler KJ, (2007) Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12: 656-670.
Weston MC, Nehring RB, Wojcik SM, Rosenmund C, (2011) Interplay between VGLUT isoforms and endophilin A1 regulates neurotransmitter release and short-term plasticity. Neuron 69: 1147-1159.
Lessmann V, Gottmann K, Heumann R, (1994) BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport 6: 21-25.
Schinder AF, Berninger B, Poo M, (2000) Postsynaptic target specificity of neurotrophin-induced presynaptic potentiation. Neuron 25: 151-163.
Crozier RA, Black IB, Plummer MR, (1999) Blockade of NR2B-containing NMDA receptors prevents BDNF enhancement of glutamatergic transmission in hippocampal neurons. Learn Mem 6: 257-266.
Lan JY, Skeberdis VA, Jover T, Grooms SY, Lin Y, et al. (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci 4: 382-390.
Buck CR, Martinez HJ, Chao MV, Black IB, (1988) Differential expression of the nerve growth factor receptor gene in multiple brain areas. Brain Res Dev Brain Res 44: 259-268.
Lu B, Buck CR, Dreyfus CF, Black IB, (1989) Expression of NGF and NGF receptor mRNAs in the developing brain: evidence for local delivery and action of NGF. Exp Neurol 104: 191-199.
Ferrer I, Bernet E, Soriano E, del Rio T, Fonseca M, (1990) Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience 39: 451-458.
Gould E, Woolley CS, McEwen BS, (1991) Naturally occurring cell death in the developing dentate gyrus of the rat. J Comp Neurol 304: 408-418.
Fryer RH, Kaplan DR, Feinstein SC, Radeke MJ, Grayson DR, et al. (1996) Developmental and mature expression of full-length and truncated TrkB receptors in the rat forebrain. J Comp Neurol 374: 21-40.
Wallen-Mackenzie A, Gezelius H, Thoby-Brisson M, Nygard A, Enjin A, et al. (2006) Vesicular glutamate transporter 2 is required for central respiratory rhythm generation but not for locomotor central pattern generation. J Neurosci 26: 12294-12307.
He H, Mahnke AH, Doyle S, Fan N, Wang C-C, et al. (2012) Neurodevelopmental role for VGLUT2 in pyramidal neuron plasticity, dendritic refinement, and in spatial learning. J Neurosci 32: 15886-15901.
Daniels RW, Collins CA, Chen K, Gelfand MV, Featherstone DE, et al. (2006) A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron 49: 11-16.
Edwards RH, (2007) The neurotransmitter cycle and quantal size. Neuron 55: 835-858.
Moechars D, Weston MC, Leo S, Callaerts-Vegh Z, Goris I, et al. (2006) Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J Neurosci 26: 12055-12066.