Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation

Neurotrophins have been proposed to participate in activity-dependent modifications of neuronal connectivity and synaptic efficacy. Preferential strengthening of active inputs requires restriction of putative neurotrophin-mediated synaptic potentiation to active synapses. Here we report that potentiation of synaptic efficacy by brain-derived neurotrophic factor (BDNF) is greatly facilitated by presynaptic depolarization at developing neuromuscular synapses. Brief depolarization in the presence of low-level BDNF results in a marked potentiation of both evoked and spontaneous synaptic transmission, whereas exposure to either BDNF or depolarization alone is without effect. This potentiation depends on the relative timing of depolarization and reflects an enhancement of transmitter secretion from the presynaptic neuron. Thus synapses made by active inputs may be selectively strengthened by secreted neurotrophins as part of activity-dependent refinement of developing connections or of mature synapses.

[1]  D. Anderson,et al.  Membrane depolarization induces p140trk and NGF responsiveness, but not p75LNGFR, in MAH cells. , 1992, Science.

[2]  Mu-ming Poo,et al.  cAMP-induced switching in turning direction of nerve growth cones , 1997, Nature.

[3]  E. Villacres,et al.  Voltage-sensitive Adenylyl Cyclase Activity in Cultured Neurons. A CALCIUM-INDEPENDENT PHENOMENON (*) , 1995, The Journal of Biological Chemistry.

[4]  Mu-ming Poo,et al.  Fast actions of neurotrophic factors , 1996, Current Opinion in Neurobiology.

[5]  M. Poo,et al.  Synaptic Modulation by Neurotrophic Factors: Differential and Synergistic Effects of Brain-Derived Neurotrophic Factor and Ciliary Neurotrophic Factor , 1996, The Journal of Neuroscience.

[6]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[7]  Y. Barde,et al.  Physiology of the neurotrophins. , 1996, Annual review of neuroscience.

[8]  R. Heumann,et al.  BDNF, and NT‐4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones , 1994, Neuroreport.

[9]  Scott E. Fraser,et al.  Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo , 1995, Nature.

[10]  M. Hanson,et al.  Depolarization and cAMP Elevation Rapidly Recruit TrkB to the Plasma Membrane of CNS Neurons , 1998, Neuron.

[11]  Lawrence C. Katz,et al.  Neurotrophins regulate dendritic growth in developing visual cortex , 1995, Neuron.

[12]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

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

[14]  B. Lu,et al.  Presynaptic Modulation of Synaptic Transmission and Plasticity by Brain-Derived Neurotrophic Factor in the Developing Hippocampus , 1998, The Journal of Neuroscience.

[15]  D. Shelton,et al.  Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  D. Lo Neurotrophic factors and synaptic plasticity , 1995, Neuron.

[17]  C. Stevens,et al.  Presynaptic mechanism for long-term potentiation in the hippocampus , 1990, Nature.

[18]  Howard J. Federoff,et al.  Regulated Release and Polarized Localization of Brain-Derived Neurotrophic Factor in Hippocampal Neurons , 1996, Molecular and Cellular Neuroscience.

[19]  R. Zucker,et al.  Residual Ca2 + and short-term synaptic plasticity , 1994, Nature.

[20]  Nancy Y. Ip,et al.  Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF , 1993, Nature.

[21]  Dale Purves,et al.  Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system , 1988, Nature.

[22]  E. Schuman,et al.  Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus , 1995, Science.

[23]  H. G. Kim,et al.  Neurotrophin 3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in cortical neurons. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[24]  M. Poo,et al.  Expression of a Putative Vesicular Acetylcholine Transporter Facilitates Quantal Transmitter Packaging , 1997, Neuron.

[25]  C. Gall,et al.  Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. , 1989, Science.

[26]  I. Black,et al.  Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[27]  K. Anderson,et al.  BDNF down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. , 1996, The European journal of neuroscience.

[28]  T. Bonhoeffer Neurotrophins and activity-dependent development of the neocortex , 1996, Current Opinion in Neurobiology.

[29]  C. Shatz,et al.  Blockade of Endogenous Ligands of TrkB Inhibits Formation of Ocular Dominance Columns , 1997, Neuron.

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

[31]  W. Almers,et al.  Dihydropyridine receptors in muscle are voltage-dependent but most are not functional calcium channels , 1985, Nature.

[32]  Guo-li Ming,et al.  Acute Morphogenic and Chemotropic Effects of Neurotrophins on Cultured Embryonic Xenopus Spinal Neurons , 1997, The Journal of Neuroscience.

[33]  A. Meyer-Franke,et al.  Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture , 1995, Neuron.

[34]  L Maffei,et al.  Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Y. Barde,et al.  Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. , 1995, Development.

[36]  H. Thoenen,et al.  Physiology of nerve growth factor. , 1980, Physiological reviews.

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

[38]  C F Ibáñez,et al.  Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. , 1995, Science.

[39]  Mu-ming Poo,et al.  Potentiation of Developing Synapses by Postsynaptic Release of Neurotrophin-4 , 1997, Neuron.

[40]  H. Thoenen,et al.  Characterization of Nerve Growth Factor (NGF) Release from Hippocampal Neurons: Evidence for a Constitutive and an Unconventional Sodium‐dependent Regulated Pathway , 1995, The European journal of neuroscience.

[41]  Y. Barde,et al.  Differential Regulation of p21ras Activation in Neurons by Nerve Growth Factor and Brain-derived Neurotrophic Factor (*) , 1995, The Journal of Biological Chemistry.

[42]  Lawrence C Katz,et al.  Neurotrophin Regulation of Cortical Dendritic Growth Requires Activity , 1996, Neuron.

[43]  Bernard Katz,et al.  The Croonian Lecture - The transmission of impulses from nerve to muscle, and the subcellular unit of synaptic action , 1962, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[44]  T Bonhoeffer,et al.  Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[45]  L. Greene,et al.  Regulation of growth cone morphology by nerve growth factor: A comparative study by scanning electron microscopy , 1985, Journal of neuroscience research.

[46]  X Wang,et al.  Localized Synaptic Actions of Neurotrophin-4 , 1998, The Journal of Neuroscience.

[47]  I. Black,et al.  Depolarizing stimuli regulate nerve growth factor gene expression in cultured hippocampal neurons. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Poo,et al.  Erratum: CAMP-induced switching in turning direction of nerve growth cones (Nature (1997) 388 (275-279)) , 1997 .

[49]  G. Banker,et al.  Culturing nerve cells , 1998 .

[50]  Andrew Gloster,et al.  Synaptic Innervation Density Is Regulated by Neuron-Derived BDNF , 1997, Neuron.