Review on the role of AMPA receptor nano-organization and dynamic in the properties of synaptic transmission

Compans, Benjamin; Choquet, Daniel; Hosy, Eric

doi:10.1117/1.nph.3.4.041811

Cited by 35 publications

(59 citation statements)

References 155 publications

(232 reference statements)

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“…The full recovery of the AMPA response points to an unexpected increase in sensitivity of the postsynaptic compartment to glutamate. By association with different auxiliary proteins and other scaffold-related mechanisms, the density and open probability of postsynaptic glutamate receptors can quickly change (24,25). In hippocampal slice cultures, post-tetanic potentiation is well established and requires the activity of protein kinase C (26).…”

Section: Discussionmentioning

confidence: 99%

“…iGluSnFR and variant plasmids were electroporated into 2-3 CA3 pyramidal cells at 40 ng/µL (iGluSnFR) or 50 ng/µL (iGluf, iGluu) together with tdimer2 (20 ng/µL), a cytoplasmic red fluorescent protein (29). 2 -4 days after electroporation (at DIV [14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30], slice cultures were placed in the recording chamber of a two-photon microscope and superfused with artificial cerebrospinal fluid (ACSF) containing (in mM) 25 NaHCO3, 1.25 NaH2PO4, 127 NaCl, 25 D-glucose, 2.5 KCl, 2 CaCl2, 1 MgCl2. Whole-cell recordings from a transfected CA3 pyramidal cell were made with a Multiclamp 700B amplifier (Molecular Devices).…”

Section: Synaptic Measurementsmentioning

confidence: 99%

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Ultrafast glutamate sensors resolve high-frequency release at Schaffer collateral synapses

Helassa

Dürst²,

Coates

et al. 2017

Preprint

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Glutamatergic synapses display a rich repertoire of plasticity mechanisms on many different time scales, involving dynamic changes in the efficacy of transmitter release as well as changes in the number and function of postsynaptic glutamate receptors. The genetically encoded glutamate sensor iGluSnFR enables visualization of glutamate release from presynaptic terminals at frequencies up to ~10 Hz. However, to resolve glutamate dynamics during high frequency bursts, faster indicators are required. Here we report the development of fast (iGluf) and ultrafast (iGluu) variants with comparable brightness, but increased Kd for glutamate (137 M and 600 M, respectively). Compared to iGluSnFR, iGluu has a 6-fold faster dissociation rate in vitro and 5-fold faster kinetics in synapses. Fitting a three-state model to kinetic data, we identify the large conformational change after glutamate binding as the rate-limiting step. In rat hippocampal slice culture stimulated at 100 Hz, we find that iGluu is sufficiently fast to resolve individual glutamate release events, revealing that glutamate is rapidly cleared from the synaptic cleft. Depression of iGluu responses during 100 Hz trains correlates with depression of postsynaptic EPSPs, indicating that depression during high frequency stimulation is purely presynaptic in origin. At individual boutons, the recovery from depression could be predicted from the amount of glutamate released on the second pulse (paired pulse facilitation/depression), demonstrating differential frequency-dependent filtering of spike trains at Schaffer collateral boutons. Significance StatementExcitatory synapses convert presynaptic action potentials into chemical signals that are sensed by postsynaptic glutamate receptors. To eavesdrop on synaptic transmission, genetically encoded fluorescent sensors for glutamate have been developed. However, even the best available sensors lag behind the very fast glutamate dynamics in the synaptic cleft. Here we report the development of an ultrafast genetically encoded glutamate sensor, iGluu, which allowed us to image glutamate clearance and synaptic depression during 100 Hz spike trains. We found that only boutons showing paired-pulse facilitation were able to rapidly recover from depression. Thus, presynaptic boutons act as frequency-specific filters to transmit select features of the spike train to specific postsynaptic cells. INTRODUCTIONThe efficacy of synaptic transmission is not constant, but changes dynamically during high-frequency activity. In terms of information processing, different forms of short-term plasticity act as specific frequency filters: Facilitating synapses are most effective during high frequency bursts, while depressing synapses preferentially transmit isolated spikes preceded by silent periods (Markram et al., 1998). Mechanistically, a number of pre-and postsynaptic parameters change dynamically during high frequency activity, e.g. the number of readily releasable vesicles, presynaptic Ca 2+ dynamics, and the properties of po...

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Section: Discussionmentioning

confidence: 99%

Section: Synaptic Measurementsmentioning

confidence: 99%

Ultrafast glutamate sensors resolve high-frequency release at Schaffer collateral synapses

Helassa

Dürst²,

Coates

et al. 2017

Preprint

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“…This is achieved via a network of molecular interactions with the membrane skeleton and associated transmembrane proteins (Sheng and Sala, 2001;Garner et al, 2000). For instance, singleparticle tracking in living cells and super-resolution imaging in fixed cells have revealed that the nanoscale localization and lateral mobility of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors can greatly influence synaptic transmission (Compans et al, 2016). In the case of AMPA receptors, the interactions with the cytoskeleton have been shown to be mediated by stargazin (also known as TARP γ2), an auxiliary subunit of the AMPA receptor, which, in turn, interacts with the postsynaptic density protein 95 (PSD95).…”

Section: The Importance Of the Cytoskeletonmentioning

confidence: 99%

The subcellular dynamics of GPCR signaling

Calebiro

Köszegi

2019

Molecular and Cellular Endocrinology

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“…The metabotropic glutamate receptors are G protein coupled receptors. Glutamate binding to ionotropic Amino-Methyl Propionic Acid (AMPA)-type and N-Methyl-D-Aspartate (NMDA)-type receptors leads to excitatory synaptic transmission [5]. The Gamma Amino Butyric Acid (GABA) receptors provide major route for inhibitory transmission.…”

Section: Synapse Physiology and Disruptionmentioning

confidence: 99%

“…This provides Long Term Potentiation (LTP) of synapse strength. The weaker, prolonged NMDA receptor activation causes removal of the AMPA receptors which results in Long Term Depression (LTD) [5]. The trafficking of synaptic AMPA receptors is thus, carefully controlled to modify synaptic strength during plasticity.…”

Section: Synapse Physiology and Disruptionmentioning

confidence: 99%

Disruption of Neurosynaptic Physiology and Neuron Network Dysfunction in Brain Disorders: An Environmental and Occupational Health Perspective

Pandey¹

2017

AND

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Networks of signaling cascades regulate synaptic transmission and morphology. Signaling molecules and their dynamics are subject to impact of environmental insults as well as genes predisposing to disease risks. Pollutants may impact brain through cellular, molecular and inflammatory pathways, causing direct damage or predisposing to damage by other insults, leading to diseases. Disruptions in structure and function of neurotransmission elements and protein networks contribute to pathogenesis of neuropsychiatric diseases. Different affected brain regions and/or synaptic connections between excitatory and inhibitory neurons charecterise specific clinical states. Functional identification of synaptic signaling networks and specific neuronal pathways would facilitate understanding of specific pathomechanisms relevant to preventive and corrective interventions. Physiology of neural networks and pathogenesis, therapeutics and prevention of diseases arising of their disruption, specially with environmental afflictions, deserve holistic and not fragmentary understanding. Present article attempts to present such diverse information with possible coherence to emphasize necessary address in contemporary medical teaching and continuing education for young researchers. The mounting challenge of prevention and management of pollution inflicted disruption of neurophysiology associated with brain dysfunction and diseases in contemporary world may be better addressed by integrated interdisciplinary understanding of the problems.

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Review on the role of AMPA receptor nano-organization and dynamic in the properties of synaptic transmission

Cited by 35 publications

References 155 publications

Ultrafast glutamate sensors resolve high-frequency release at Schaffer collateral synapses

Ultrafast glutamate sensors resolve high-frequency release at Schaffer collateral synapses

The subcellular dynamics of GPCR signaling

Disruption of Neurosynaptic Physiology and Neuron Network Dysfunction in Brain Disorders: An Environmental and Occupational Health Perspective

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