Neurobiology of local and intercellular BDNF signaling

Brain-derived neurotrophic factor (BDNF) is a member of the neurotrophin family of secreted proteins. Signaling cascades induced by BDNF and its receptor, the receptor tyrosine kinase TrkB, link neuronal growth and differentiation with synaptic plasticity. For this reason, interference with BDNF signaling has emerged as a promising strategy for potential treatments in psychiatric and neurological disorders. In many brain circuits, synaptically released BDNF is essential for structural and functional long-term potentiation, two prototypical cellular models of learning and memory formation. Recent studies have revealed an unexpected complexity in the synaptic communication of mature BDNF and its precursor proBDNF, not only between local pre- and postsynaptic neuronal targets but also with participation of glial cells. Here, we consider recent findings on local actions of the BDNF family of ligands at the synapse and discuss converging lines of evidence which emerge from per se conflicting results.

[1]  M. Chao,et al.  Neurotrophins and their receptors: A convergence point for many signalling pathways , 2003, Nature Reviews Neuroscience.

[2]  C. Bramham,et al.  BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis , 2005, Progress in Neurobiology.

[3]  Ted Abel,et al.  Recombinant BDNF Rescues Deficits in Basal Synaptic Transmission and Hippocampal LTP in BDNF Knockout Mice , 1996, Neuron.

[4]  Q. Gu,et al.  Identification of a novel truncated isoform of trkB in the kitten primary visual cortex , 2001, Journal of Molecular Neuroscience.

[5]  S. Beggs,et al.  P2X4-Receptor-Mediated Synthesis and Release of Brain-Derived Neurotrophic Factor in Microglia Is Dependent on Calcium and p38-Mitogen-Activated Protein Kinase Activation , 2009, The Journal of Neuroscience.

[6]  Bin Xu,et al.  The BDNF Val66Met variant affects gene expression through miR-146b , 2015, Neurobiology of Disease.

[7]  T. Bonhoeffer,et al.  The involvement of brain-derived neurotrophic factor in hippocampal long-term potentiation revealed by gene targeting experiments , 1996, Journal of Physiology-Paris.

[8]  Elke Edelmann,et al.  Pre- and postsynaptic twists in BDNF secretion and action in synaptic plasticity , 2014, Neuropharmacology.

[9]  G. Buzsáki,et al.  Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells , 2002, Nature.

[10]  Stephen Maren,et al.  Seeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory , 2011, Neuron.

[11]  D. Paré,et al.  Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. , 2010, Physiological reviews.

[12]  M. Chao,et al.  A role for Fyn in Trk receptor transactivation by G-protein-coupled receptor signaling , 2006, Molecular and Cellular Neuroscience.

[13]  H. Thoenen,et al.  Are there differences between the secretion characteristics of NGF and BDNF? Implications for the modulatory role of neurotrophins in activity‐dependent neuronal plasticity , 1999, Microscopy research and technique.

[14]  M. Bergami,et al.  Hippocampal neurons recycle BDNF for activity‐dependent secretion and LTP maintenance , 2006, The EMBO journal.

[15]  Steven A. Siegelbaum,et al.  Visualization of changes in presynaptic function during long-term synaptic plasticity , 2001, Nature Neuroscience.

[16]  B. Lu,et al.  Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus , 1996, Nature.

[17]  Haruo Kasai,et al.  Protein Synthesis and Neurotrophin-Dependent Structural Plasticity of Single Dendritic Spines , 2008, Science.

[18]  F. Lee,et al.  Activation of Trk neurotrophin receptors in the absence of neurotrophins , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Elke Edelmann,et al.  Theta Burst Firing Recruits BDNF Release and Signaling in Postsynaptic CA1 Neurons in Spike-Timing-Dependent LTP , 2015, Neuron.

[20]  J. Gaiarsa,et al.  NMDA-dependent switch of proBDNF actions on developing GABAergic synapses. , 2013, Cerebral cortex.

[21]  H. Thoenen,et al.  Purification of a new neurotrophic factor from mammalian brain. , 1982, The EMBO journal.

[22]  S. Mineka,et al.  The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders. , 2008, Acta psychologica.

[23]  P. Séguéla,et al.  proBDNF and p75NTR Control Excitability and Persistent Firing of Cortical Pyramidal Neurons , 2015, The Journal of Neuroscience.

[24]  C. Siao,et al.  Genetic Variant BDNF (Val66Met) Polymorphism Alters Anxiety-Related Behavior , 2006, Science.

[25]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

[26]  Y. Barde,et al.  Brain‐Derived Neurotrophic Factor Levels in the Nervous System of Wild‐Type and Neurotrophin Gene Mutant Mice , 1999, Journal of neurochemistry.

[27]  V. Lessmann,et al.  Differential Vesicular Targeting and Time Course of Synaptic Secretion of the Mammalian Neurotrophins , 2005, The Journal of Neuroscience.

[28]  Girstaute Dagyte,et al.  Sustained Arc/Arg3.1 Synthesis Controls Long-Term Potentiation Consolidation through Regulation of Local Actin Polymerization in the Dentate Gyrus In Vivo , 2007, The Journal of Neuroscience.

[29]  S. Wiese,et al.  Adenosine receptor A2A-R contributes to motoneuron survival by transactivating the tyrosine kinase receptor TrkB , 2007, Proceedings of the National Academy of Sciences.

[30]  Lauren C Harte-Hargrove,et al.  proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus. , 2014, Cell reports.

[31]  C. Bramham,et al.  BDNF mechanisms in late LTP formation: A synthesis and breakdown , 2014, Neuropharmacology.

[32]  Arthur Konnerth,et al.  Postsynaptic Induction of BDNF-Mediated Long-Term Potentiation , 2002, Science.

[33]  J. Delgado-García,et al.  TrkB Modulates Fear Learning and Amygdalar Synaptic Plasticity by Specific Docking Sites , 2009, The Journal of Neuroscience.

[34]  Joseph A. Gogos,et al.  Genetic Modulation of BDNF Signaling Affects the Outcome of Axonal Competition In Vivo , 2007, Current Biology.

[35]  N. Woo,et al.  Ama“Zinc” Link between TrkB Transactivation and Synaptic Plasticity , 2008, Neuron.

[36]  A. Konnerth,et al.  Neurotrophin-evoked rapid excitation through TrkB receptors , 1999, Nature.

[37]  H. Thoenen Neurotrophins and Neuronal Plasticity , 1995, Science.

[38]  Paresh D Patel,et al.  Variant Brain-Derived Neurotrophic Factor (BDNF) (Met66) Alters the Intracellular Trafficking and Activity-Dependent Secretion of Wild-Type BDNF in Neurosecretory Cells and Cortical Neurons , 2004, The Journal of Neuroscience.

[39]  E. Kandel,et al.  Presynaptic BDNF Required for a Presynaptic but Not Postsynaptic Component of LTP at Hippocampal CA1-CA3 Synapses , 2003, Neuron.

[40]  L. Monteggia,et al.  Brain-Derived Neurotrophic Factor and Neuropsychiatric Disorders , 2012, Pharmacological Reviews.

[41]  E. Masliah,et al.  Glutamatergic axon-derived BDNF controls GABAergic synaptic differentiation in the cerebellum , 2016, Scientific Reports.

[42]  Pradeep J. Nathan,et al.  BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases , 2013, Nature Reviews Neuroscience.

[43]  Rudolf Jaenisch,et al.  Mice lacking brain-derived neurotrophic factor develop with sensory deficits , 1994, Nature.

[44]  H. Thoenen,et al.  Localization of Cellular Storage Compartments and Sites of Constitutive and Activity-Dependent Release of Nerve Growth Factor (NGF) in Primary Cultures of Hippocampal Neurons , 1996, Molecular and Cellular Neuroscience.

[45]  M. Tuszynski,et al.  Potential therapeutic uses of BDNF in neurological and psychiatric disorders , 2011, Nature Reviews Drug Discovery.

[46]  J. McNamara,et al.  Autocrine BDNF–TrkB signalling within a single dendritic spine , 2016, Nature.

[47]  E. Huang,et al.  Trk receptors: roles in neuronal signal transduction. , 2003, Annual review of biochemistry.

[48]  Michael Sendtner,et al.  Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches , 2002, Nature Neuroscience.

[49]  E. Rolls,et al.  A computational theory of hippocampal function, and tests of the theory: New developments , 2015, Neuroscience & Biobehavioral Reviews.

[50]  Yves-Alain Barde,et al.  The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. , 2002, Nature neuroscience.

[51]  C. Siao,et al.  Neuronal release of proBDNF , 2009, Nature Neuroscience.

[52]  M. Poo,et al.  Self-amplifying autocrine actions of BDNF in axon development , 2011, Proceedings of the National Academy of Sciences.

[53]  J. Os,et al.  The size and burden of mental disorders and other disorders of the brain in Europe 2010 , 2011, European Neuropsychopharmacology.

[54]  L. Minichiello TrkB signalling pathways in LTP and learning , 2009, Nature Reviews Neuroscience.

[55]  J. Schlessinger Cell Signaling by Receptor Tyrosine Kinases , 2000, Cell.

[56]  Sadegh Nabavi,et al.  Engineering a memory with LTD and LTP , 2014, Nature.

[57]  L. C. Katz,et al.  BDNF release from single cells elicits local dendritic growth in nearby neurons , 2002, Nature Neuroscience.

[58]  T. Tsumoto,et al.  Activity-Dependent Transfer of Brain-Derived Neurotrophic Factor to Postsynaptic Neurons , 2001, Science.

[59]  M. Poo,et al.  Essential Role of Presynaptic NMDA Receptors in Activity-Dependent BDNF Secretion and Corticostriatal LTP , 2014, Neuron.

[60]  T. Goldberg,et al.  BNDF modulates normal human hippocampal ageing , 2010, Molecular Psychiatry.

[61]  H. Thoenen,et al.  Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non‐NMDA glutamate receptors. , 1990, The EMBO journal.

[62]  M. Poo,et al.  Autocrine Action of BDNF on Dendrite Development of Adult-Born Hippocampal Neurons , 2015, The Journal of Neuroscience.

[63]  R. Huganir,et al.  Role of pro-brain-derived neurotrophic factor (proBDNF) to mature BDNF conversion in activity-dependent competition at developing neuromuscular synapses , 2012, Proceedings of the National Academy of Sciences.

[64]  M. Götz,et al.  Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior , 2008, Proceedings of the National Academy of Sciences.

[65]  Fabrice P Cordelières,et al.  Huntingtin Controls Neurotrophic Support and Survival of Neurons by Enhancing BDNF Vesicular Transport along Microtubules , 2004, Cell.

[66]  Amanda L. Loshbaugh,et al.  Labelling and optical erasure of synaptic memory traces in the motor cortex , 2015, Nature.

[67]  G. Glover,et al.  A Genetic Variant BDNF Polymorphism Alters Extinction Learning in Both Mouse and Human , 2010, Science.

[68]  T. Bonhoeffer,et al.  The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[69]  J. McNamara,et al.  Vesicular Zinc Promotes Presynaptic and Inhibits Postsynaptic Long-Term Potentiation of Mossy Fiber-CA3 Synapse , 2011, Neuron.

[70]  W. Yung,et al.  TrkB phosphorylation by Cdk5 is required for activity-dependent structural plasticity and spatial memory , 2012, Nature Neuroscience.

[71]  E. Schreiter,et al.  Axonal Endoplasmic Reticulum Ca2+ Content Controls Release Probability in CNS Nerve Terminals , 2017, Neuron.

[72]  C. Grillon,et al.  Phasic vs Sustained Fear in Rats and Humans: Role of the Extended Amygdala in Fear vs Anxiety , 2010, Neuropsychopharmacology.

[73]  T. Bonhoeffer,et al.  Mechanism of TrkB-Mediated Hippocampal Long-Term Potentiation , 2002, Neuron.

[74]  M. Barbacid,et al.  A human oncogene formed by the fusion of truncated tropomyosin and protein tyrosine kinase sequences , 1986, Nature.

[75]  A. Konnerth,et al.  Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. , 2005, Physiology.

[76]  J. McNamara,et al.  Localization of Brain-Derived Neurotrophic Factor to Distinct Terminals of Mossy Fiber Axons Implies Regulation of Both Excitation and Feedforward Inhibition of CA3 Pyramidal Cells , 2004, The Journal of Neuroscience.

[77]  J. McNamara,et al.  Rho GTPase complementation underlies BDNF-dependent homo- and heterosynaptic plasticity , 2016, Nature.

[78]  T. Bonhoeffer,et al.  The p75 Neurotrophin Receptor Negatively Modulates Dendrite Complexity and Spine Density in Hippocampal Neurons , 2005, The Journal of Neuroscience.

[79]  H. Blau,et al.  Structural and Mechanistic Insights into Nerve Growth Factor Interactions with the TrkA and p75 Receptors , 2007, Neuron.

[80]  V. Lessmann,et al.  Acute and chronic interference with BDNF/TrkB-signaling impair LTP selectively at mossy fiber synapses in the CA3 region of mouse hippocampus , 2013, Neuropharmacology.

[81]  Petti T. Pang,et al.  The yin and yang of neurotrophin action , 2005, Nature Reviews Neuroscience.

[82]  Barbara L. Hempstead,et al.  Regulation of Cell Survival by Secreted Proneurotrophins , 2001, Science.

[83]  C. Montell,et al.  Activation of a TRPC3-Dependent Cation Current through the Neurotrophin BDNF , 1999, Neuron.

[84]  J. Conner,et al.  Anterograde transport of brain-derived neurotrophic factor and its role in the brain , 1997, Nature.

[85]  A. Lüthi,et al.  Neuronal circuits for fear and anxiety , 2015, Nature Reviews Neuroscience.

[86]  I. Sora,et al.  Dopamine D1 Receptor-induced Signaling through TrkB Receptors in Striatal Neurons* , 2008, Journal of Biological Chemistry.

[87]  S. Oliet,et al.  Gliotransmitters Travel in Time and Space , 2014, Neuron.

[88]  G Buzsáki,et al.  GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus , 1998, The Journal of Neuroscience.

[89]  C. Bramham,et al.  Two-stage translational control of dentate gyrus LTP consolidation is mediated by sustained BDNF-TrkB signaling to MNK. , 2014, Cell reports.

[90]  T. Bonhoeffer,et al.  A caged Ab reveals an immediate/instructive effect of BDNF during hippocampal synaptic potentiation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[91]  T. Bonhoeffer,et al.  Hippocampal Long-Term Potentiation Is Supported by Presynaptic and Postsynaptic Tyrosine Receptor Kinase B-Mediated Phospholipase Cγ Signaling , 2006, The Journal of Neuroscience.

[92]  E. Schuman,et al.  Neurotrophins and Time: Different Roles for TrkB Signaling in Hippocampal Long-Term Potentiation , 1997, Neuron.

[93]  R. Blum,et al.  Direct imaging of ER calcium with targeted-esterase induced dye loading (TED). , 2013, Journal of visualized experiments : JoVE.

[94]  P. Pauli,et al.  The BDNF Val66Met Polymorphism Modulates the Generalization of Cued Fear Responses to a Novel Context , 2014, Neuropsychopharmacology.

[95]  B. Hempstead Brain-Derived Neurotrophic Factor: Three Ligands, Many Actions. , 2015, Transactions of the American Clinical and Climatological Association.

[96]  J. Gaiarsa,et al.  Backpropagating Action Potentials Trigger Dendritic Release of BDNF during Spontaneous Network Activity , 2008, The Journal of Neuroscience.

[97]  H. Thoenen,et al.  Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section , 1992, Nature.

[98]  J. Yates,et al.  Microglia Promote Learning-Dependent Synapse Formation through Brain-Derived Neurotrophic Factor , 2013, Cell.

[99]  Y. Barde,et al.  Binding characteristics of brain-derived neurotrophic factor to its receptors on neurons from the chick embryo , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[100]  L. C. Katz,et al.  Destabilization of Cortical Dendrites and Spines by BDNF , 1999, Neuron.

[101]  H. Pape,et al.  Cannabinoid CB1 receptors in distinct circuits of the extended amygdala determine fear responsiveness to unpredictable threat , 2017, Molecular Psychiatry.

[102]  Mu-ming Poo,et al.  Neurotrophin regulation of neural circuit development and function , 2012, Nature Reviews Neuroscience.

[103]  T. Hunter,et al.  trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors , 1991, Molecular and cellular biology.

[104]  E. Schuman,et al.  Deep Sequencing and High-Resolution Imaging Reveal Compartment-Specific Localization of Bdnf mRNA in Hippocampal Neurons , 2013, Science Signaling.

[105]  M. Canossa,et al.  Glioactive ATP controls BDNF recycling in cortical astrocytes , 2017, Communicative & integrative biology.

[106]  M. Bergami,et al.  Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes , 2008, The Journal of cell biology.

[107]  K. Luan Phan,et al.  The contextual brain: implications for fear conditioning, extinction and psychopathology , 2013, Nature Reviews Neuroscience.

[108]  K. Suzuki,et al.  Sequential cis/trans autophosphorylation in TrkB tyrosine kinase. , 1997, Biochemistry.

[109]  J. McNamara,et al.  Brain‐derived neurotrophic factor but not vesicular zinc promotes TrkB activation within mossy fibers of mouse hippocampus in vivo , 2014, The Journal of comparative neurology.

[110]  Wei Li,et al.  Activity-dependent BDNF release and TRPC signaling is impaired in hippocampal neurons of Mecp2 mutant mice , 2012, Proceedings of the National Academy of Sciences.

[111]  Spartaco Santi,et al.  Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[112]  D. Katz,et al.  Cellular Mechanisms Regulating Activity-Dependent Release of Native Brain-Derived Neurotrophic Factor from Hippocampal Neurons , 2002, The Journal of Neuroscience.

[113]  Mark J. Schnitzer,et al.  Impermanence of dendritic spines in live adult CA1 hippocampus , 2015, Nature.

[114]  J. Rubenstein,et al.  Conditional ablation of brain-derived neurotrophic factor-TrkB signaling impairs striatal neuron development , 2012, Proceedings of the National Academy of Sciences of the United States of America.

[115]  V. Lessmann,et al.  Mechanisms, locations, and kinetics of synaptic BDNF secretion: An update , 2009, Neuroscience Research.

[116]  Sarah Aufmkolk,et al.  High abundance of BDNF within glutamatergic presynapses of cultured hippocampal neurons , 2014, Front. Cell. Neurosci..

[117]  Y. Barde,et al.  Global Deprivation of Brain-Derived Neurotrophic Factor in the CNS Reveals an Area-Specific Requirement for Dendritic Growth , 2010, The Journal of Neuroscience.

[118]  N. Berardi,et al.  Peri-Synaptic Glia Recycles Brain-Derived Neurotrophic Factor for LTP Stabilization and Memory Retention , 2016, Neuron.

[119]  Christian Lohmann,et al.  Spontaneous Activity Drives Local Synaptic Plasticity In Vivo , 2015, Neuron.

[120]  M. Egan,et al.  The BDNF val66met Polymorphism Affects Activity-Dependent Secretion of BDNF and Human Memory and Hippocampal Function , 2003, Cell.

[121]  V. Lessmann,et al.  Postsynaptic BDNF signalling regulates long‐term potentiation at thalamo‐amygdala afferents , 2012, The Journal of physiology.

[122]  S. Cichon,et al.  GLRB allelic variation associated with agoraphobic cognitions, increased startle response and fear network activation: a potential neurogenetic pathway to panic disorder , 2017, Molecular Psychiatry.

[123]  R. Levi‐montalcini,et al.  The nerve growth factor 35 years later. , 1987, Science.

[124]  H. Thoenen,et al.  Molecular cloning and expression of brain-derived neurotrophic factor , 1989, Nature.

[125]  Tobias Bonhoeffer,et al.  Essential Role for TrkB Receptors in Hippocampus-Mediated Learning , 1999, Neuron.

[126]  G. Lynch,et al.  Behavioral / Systems / Cognitive Brain-Derived Neurotrophic Factor Promotes Long-Term Potentiation-Related Cytoskeletal Changes in Adult Hippocampus , 2007 .

[127]  M. Sendtner,et al.  EGF transactivation of Trk receptors regulates the migration of newborn cortical neurons , 2013, Nature Neuroscience.

[128]  C. Bramham,et al.  Brain-Derived Neurotrophic Factor Triggers Transcription-Dependent, Late Phase Long-Term Potentiation In Vivo , 2002, The Journal of Neuroscience.

[129]  Takafumi Inoue,et al.  Activity-dependent release of endogenous BDNF from mossy fibers evokes a TRPC3 current and Ca2+ elevations in CA3 pyramidal neurons. , 2010, Journal of neurophysiology.

[130]  J. McNamara,et al.  Zinc-Mediated Transactivation of TrkB Potentiates the Hippocampal Mossy Fiber-CA3 Pyramid Synapse , 2008, Neuron.

[131]  Dietmar Schmitz,et al.  Synaptic plasticity at hippocampal mossy fibre synapses , 2005, Nature Reviews Neuroscience.

[132]  T. Bonhoeffer,et al.  Endogenous Brain-Derived Neurotrophic Factor Triggers Fast Calcium Transients at Synapses in Developing Dendrites , 2007, The Journal of Neuroscience.

[133]  N. Woo,et al.  Distinct Role of Long 3′ UTR BDNF mRNA in Spine Morphology and Synaptic Plasticity in Hippocampal Neurons , 2008, Cell.

[134]  Y. Barde,et al.  Brain-derived Neurotrophic Factor in Megakaryocytes*♦ , 2016, The Journal of Biological Chemistry.

[135]  Tamara Aid,et al.  Dissecting the human BDNF locus: Bidirectional transcription, complex splicing, and multiple promoters☆ , 2007, Genomics.

[136]  P. Strata,et al.  Learning-related feedforward inhibitory connectivity growth required for memory precision , 2011, Nature.

[137]  Petti T. Pang,et al.  Cleavage of proBDNF by tPA/Plasmin Is Essential for Long-Term Hippocampal Plasticity , 2004, Science.

[138]  Yves-Alain Barde,et al.  Trophic factors and neuronal survival , 1989, Neuron.

[139]  B. Lu,et al.  Control of extracellular cleavage of ProBDNF by high frequency neuronal activity , 2009, Proceedings of the National Academy of Sciences.

[140]  J. Flint,et al.  No association between the BDNF Val66Met polymorphism and mood status in a non-clinical community sample of 7389 older adults. , 2007, Journal of psychiatric research.

[141]  M. Amaral,et al.  BDNF induces calcium elevations associated with IBDNF, a nonselective cationic current mediated by TRPC channels. , 2007, Journal of neurophysiology.

[142]  M. Poo,et al.  Activity-dependent BDNF release via endocytic pathways is regulated by synaptotagmin-6 and complexin , 2015, Proceedings of the National Academy of Sciences.

[143]  K M Harris,et al.  Three-Dimensional Organization of Smooth Endoplasmic Reticulum in Hippocampal CA1 Dendrites and Dendritic Spines of the Immature and Mature Rat , 1997, The Journal of Neuroscience.

[144]  W. Chiu,et al.  TRiC subunits enhance BDNF axonal transport and rescue striatal atrophy in Huntington’s disease , 2016, Proceedings of the National Academy of Sciences.

[145]  C. Alberini,et al.  A Positive Autoregulatory BDNF Feedback Loop via C/EBPβ Mediates Hippocampal Memory Consolidation , 2014, The Journal of Neuroscience.

[146]  R. Kalisch,et al.  A review on experimental and clinical genetic associations studies on fear conditioning, extinction and cognitive-behavioral treatment , 2011, Translational Psychiatry.

[147]  M. Korte,et al.  Neurotrophin receptors TrkB.T1 and p75NTR cooperate in modulating both functional and structural plasticity in mature hippocampal neurons , 2010, The European journal of neuroscience.

[148]  Bai Lu,et al.  Activation of p75NTR by proBDNF facilitates hippocampal long-term depression , 2005, Nature Neuroscience.

[149]  Arthur Konnerth,et al.  Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells , 2003, Nature.

[150]  K. Bath,et al.  Endogenous Truncated TrkB.T1 Receptor Regulates Neuronal Complexity and TrkB Kinase Receptor Function In Vivo , 2009, The Journal of Neuroscience.

[151]  K. Domschke,et al.  Genetics of anxiety disorders - status quo and quo vadis. , 2012, Current pharmaceutical design.

[152]  G. Turrigiano,et al.  Experience‐dependent regulation of TrkB isoforms in rodent visual cortex , 2009, Developmental neurobiology.

[153]  T Bonhoeffer,et al.  Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[154]  A. Konnerth,et al.  Neurotrophin-evoked depolarization requires the sodium channel NaV1.9 , 2002, Nature.

[155]  R. Heumann,et al.  Synaptic secretion of BDNF after high‐frequency stimulation of glutamatergic synapses , 2001, The EMBO journal.

[156]  Yonatan Stelzer,et al.  Editing DNA Methylation in the Mammalian Genome , 2016, Cell.

[157]  C. Pariante,et al.  The human BDNF gene: peripheral gene expression and protein levels as biomarkers for psychiatric disorders , 2016, Translational psychiatry.

[158]  M. Frotscher,et al.  Jcb: Article , 2022 .

[159]  Y. Barde,et al.  Neurotrophin receptors TrkA and TrkC cause neuronal death whereas TrkB does not , 2010, Nature.

[160]  Joshua L. Plotkin,et al.  Impaired TrkB Receptor Signaling Underlies Corticostriatal Dysfunction in Huntington’s Disease , 2014, Neuron.

[161]  H. Thoenen,et al.  Regulated secretion of neurotrophins by metabotropic glutamate group I (mGluRI) and Trk receptor activation is mediated via phospholipase C signalling pathways , 2001, The EMBO journal.

[162]  J. Baraban,et al.  Dendritic trafficking of BDNF mRNA is mediated by translin and blocked by the G196A (Val66Met) mutation , 2009, Proceedings of the National Academy of Sciences.

[163]  F. Lee,et al.  Transactivation of Trk Neurotrophin Receptors by G-Protein-Coupled Receptor Ligands Occurs on Intracellular Membranes , 2004, The Journal of Neuroscience.

[164]  F. Lee,et al.  Val66Met Polymorphism of BDNF Alters Prodomain Structure to Induce Neuronal Growth Cone Retraction , 2013, Nature Communications.

[165]  A. Menini,et al.  TrkB Signaling Directs the Incorporation of Newly Generated Periglomerular Cells in the Adult Olfactory Bulb , 2013, The Journal of Neuroscience.

[166]  S. Duan,et al.  Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons , 2010, Nature Neuroscience.

[167]  Kaia Palm,et al.  Mouse and rat BDNF gene structure and expression revisited , 2006, Journal of neuroscience research.

[168]  J. Conner,et al.  Distribution of Brain-Derived Neurotrophic Factor (BDNF) Protein and mRNA in the Normal Adult Rat CNS: Evidence for Anterograde Axonal Transport , 1997, The Journal of Neuroscience.

[169]  Fang Liu,et al.  Glutamate-mediated astrocyte–neuron signalling , 1994, Nature.

[170]  M. Hayashi,et al.  Changes in BDNF-immunoreactive structures in the hippocampal formation of the aged macaque monkey , 2001, Brain Research.

[171]  Yves-Alain Barde,et al.  Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF , 2008, Nature Neuroscience.

[172]  T. Bonhoeffer,et al.  Relative Contribution of Endogenous Neurotrophins in Hippocampal Long-Term Potentiation , 1999, The Journal of Neuroscience.

[173]  K. Martinowich,et al.  TrkB as a Potential Synaptic and Behavioral Tag , 2011, The Journal of Neuroscience.

[174]  M. Bergami,et al.  Polarized expression of p75(NTR) specifies axons during development and adult neurogenesis. , 2014, Cell reports.