XB-ART-52094
Elife
2016 May 03;5. doi: 10.7554/eLife.12190.
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A novel synaptic plasticity rule explains homeostasis of neuromuscular transmission.
Ouanounou G
,
Baux G
,
Bal T
.
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Excitability differs among muscle fibers and undergoes continuous changes during development and growth, yet the neuromuscular synapse maintains a remarkable fidelity of execution. Here we show in two evolutionarily distant vertebrates (Xenopus laevis cell culture and mouse nerve-muscle ex-vivo) that the skeletal muscle cell constantly senses, through two identified calcium signals, synaptic events and their efficacy in eliciting spikes. These sensors trigger retrograde signal(s) that control presynaptic neurotransmitter release, resulting in synaptic potentiation or depression. In the absence of spikes, synaptic events trigger potentiation. Once the synapse is sufficiently strong to initiate spiking, the occurrence of these spikes activates a negative retrograde feedback. These opposing signals dynamically balance the synapse in order to continuously adjust neurotransmitter release to a level matching current muscle cell excitability.
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Species referenced: Xenopus laevis
Genes referenced: dtl sh2b2
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References [+] :
Almers,
Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization.
1981, Pubmed
Almers, Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization. 1981, Pubmed
Barria, Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. 1997, Pubmed
Beattie, Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. 2000, Pubmed
Cash, Postsynaptic elevation of calcium induces persistent depression of developing neuromuscular synapses. 1996, Pubmed , Xenbase
Catterall, Excitation-contraction coupling in vertebrate skeletal muscle: a tale of two calcium channels. 1991, Pubmed
Changeux, Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. , Pubmed
Cruz, Conus geographus toxins that discriminate between neuronal and muscle sodium channels. 1985, Pubmed
Cull-Candy, On the release of transmitter at normal, myasthenia gravis and myasthenic syndrome affected human end-plates. 1980, Pubmed
Cull-Candy, End-plate currents and acetylcholine noise at normal and myasthenic human end-plates. 1979, Pubmed
Dan, Plasticity of developing neuromuscular synapses. 1995, Pubmed , Xenbase
Davis, Homeostatic control of presynaptic neurotransmitter release. 2015, Pubmed
Davis, Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. 1998, Pubmed
DiAntonio, Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. 1999, Pubmed
Frank, Homeostatic plasticity at the Drosophila neuromuscular junction. 2014, Pubmed
Frank, Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. 2006, Pubmed
Franzini-Armstrong, Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. 1997, Pubmed
Fu, ATP potentiates spontaneous transmitter release at developing neuromuscular synapses. 1991, Pubmed , Xenbase
Fucile, The human adult subtype ACh receptor channel has high Ca2+ permeability and predisposes to endplate Ca2+ overloading. 2006, Pubmed
Funakoshi, Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. 1995, Pubmed
Gautam, Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. 1995, Pubmed
Gautam, Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. 1996, Pubmed
Gaviño, Homeostatic synaptic depression is achieved through a regulated decrease in presynaptic calcium channel abundance. 2015, Pubmed
Goda, Mechanisms of synapse assembly and disassembly. 2003, Pubmed
Goldman, POTENTIAL, IMPEDANCE, AND RECTIFICATION IN MEMBRANES. 1943, Pubmed
Gorassini, Activity of hindlimb motor units during locomotion in the conscious rat. 2000, Pubmed
Gouzé, Selective stabilization of muscle innervation during development: a mathematical model. 1983, Pubmed
Guido, Refinement of the retinogeniculate pathway. 2008, Pubmed
HODGKIN, The effect of sodium ions on the electrical activity of giant axon of the squid. 1949, Pubmed
Haghighi, Retrograde control of synaptic transmission by postsynaptic CaMKII at the Drosophila neuromuscular junction. 2003, Pubmed
Hall, Synaptic structure and development: the neuromuscular junction. 1993, Pubmed
Henderson, Neurotrophins promote motor neuron survival and are present in embryonic limb bud. 1993, Pubmed
Hines, The NEURON simulation environment. 1997, Pubmed
Hong, Spatial and temporal expression patterns of two sodium channel genes in Drosophila. 1994, Pubmed
Koliatsos, Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. 1993, Pubmed
Kullmann, Roles of distinct glutamate receptors in induction of anti-Hebbian long-term potentiation. 2008, Pubmed
Kunze, A mobile intracellular microelectrode designed to record from neurons in contracting tissue. 1998, Pubmed
Li, Molecular basis of isoform-specific micro-conotoxin block of cardiac, skeletal muscle, and brain Na+ channels. 2003, Pubmed
Lo, Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. 1991, Pubmed , Xenbase
Lo, Depression of developing neuromuscular synapses induced by repetitive postsynaptic depolarizations. 1994, Pubmed , Xenbase
Lo, Heterosynaptic suppression of developing neuromuscular synapses in culture. 1994, Pubmed , Xenbase
Lohof, Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. 1993, Pubmed , Xenbase
Lømo, What controls the position, number, size, and distribution of neuromuscular junctions on rat muscle fibers? 2003, Pubmed
Macleod, Synaptic homeostasis on the fast track. 2006, Pubmed
Malenka, An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. 1989, Pubmed
Malinow, Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. 1989, Pubmed
Mammen, Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. 1997, Pubmed
Marder, Variability, compensation and homeostasis in neuron and network function. 2006, Pubmed
McMahan, The agrin hypothesis. 1990, Pubmed
Melzer, The role of Ca2+ ions in excitation-contraction coupling of skeletal muscle fibres. 1995, Pubmed
Mulkey, An essential role for protein phosphatases in hippocampal long-term depression. 1993, Pubmed
Mulkey, Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. 1994, Pubmed
Munz, Rapid Hebbian axonal remodeling mediated by visual stimulation. 2014, Pubmed , Xenbase
Müller, RIM-binding protein links synaptic homeostasis to the stabilization and replenishment of high release probability vesicles. 2015, Pubmed
Müller, RIM controls homeostatic plasticity through modulation of the readily-releasable vesicle pool. 2012, Pubmed
Müller, Transsynaptic control of presynaptic Ca²⁺ influx achieves homeostatic potentiation of neurotransmitter release. 2012, Pubmed
Nelson, Strength through diversity. 2008, Pubmed
Paradis, Homeostatic control of presynaptic release is triggered by postsynaptic membrane depolarization. 2001, Pubmed
Penney, TOR is required for the retrograde regulation of synaptic homeostasis at the Drosophila neuromuscular junction. 2012, Pubmed
Peron, From action potential to contraction: neural control and excitation-contraction coupling in larval muscles of Drosophila. 2009, Pubmed
Petersen, Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. 1997, Pubmed
Plomp, Involvement of protein kinases in the upregulation of acetylcholine release at endplates of alpha-bungarotoxin-treated rats. 1996, Pubmed
Plomp, Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in alpha-bungarotoxin-treated rats. 1992, Pubmed
Poo, Neurotrophins as synaptic modulators. 2001, Pubmed
Prinz, The dynamic clamp comes of age. 2004, Pubmed
Rios, Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. , Pubmed
Roberts, Anti-hebbian spike-timing-dependent plasticity and adaptive sensory processing. 2010, Pubmed
Robinson, Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. 1993, Pubmed
Sandrock, Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. 1997, Pubmed
Sanes, Development of the vertebrate neuromuscular junction. 1999, Pubmed
Schinder, The neurotrophin hypothesis for synaptic plasticity. 2000, Pubmed
Sharp, Dynamic clamp: computer-generated conductances in real neurons. 1993, Pubmed
Turrigiano, Homeostatic signaling: the positive side of negative feedback. 2007, Pubmed
Turrigiano, Homeostatic plasticity in the developing nervous system. 2004, Pubmed
WOODBURY, Intracellular recording from moving tissues with a flexibly mounted ultramicroelectrode. 1956, Pubmed
Wan, Activity-induced potentiation of developing neuromuscular synapses. 1999, Pubmed , Xenbase
Wang, Endostatin is a trans-synaptic signal for homeostatic synaptic plasticity. 2014, Pubmed
Wang, Potentiation of developing synapses by postsynaptic release of neurotrophin-4. 1997, Pubmed , Xenbase
Witzemann, Development of the neuromuscular junction. 2006, Pubmed
Wong, The neurotrophins BDNF, NT-3 and NT-4/5, but not NGF, up-regulate the cholinergic phenotype of developing motor neurons. 1993, Pubmed
Wood, Safety factor at the neuromuscular junction. 2001, Pubmed
Wood, Action potential generation in rat slow- and fast-twitch muscles. 1995, Pubmed
Xie, Activity-dependent expression of NT-3 in muscle cells in culture: implications in the development of neuromuscular junctions. 1997, Pubmed , Xenbase
Yan, Influences of neurotrophins on mammalian motoneurons in vivo. 1993, Pubmed