Inhibitory Synaptic Transmission Tuned by Ca and Glutamate Through the Control of GABA R Lateral Diffusion Dynamics

Overview

Journal Dev Growth Differ

Specialties Biology
Reproductive Medicine

Date 2020 Apr 25

PMID 32329058

Citations 4

Authors

Hiroko Bannai

Fumihiro Niwa

Shigeo Sakuragi

Katsuhiko Mikoshiba

Affiliations

Soon will be listed here.

Abstract

The GABAergic synapses, a primary inhibitory synapse in the mammalian brain, is important for the normal development of brain circuits, and for the regulation of the excitation-inhibition balance critical for brain function from the developmental stage throughout life. However, the molecular mechanism underlying the formation, maintenance, and modulation of GABAergic synapses is less understood compared to that of excitatory synapses. Quantum dot-single particle tracking (QD-SPT), a super-resolution imaging technique that enables the analysis of membrane molecule dynamics at single-molecule resolution, is a powerful tool to analyze the behavior of proteins and lipids on the plasma membrane. In this review, we summarize the recent application of QD-SPT in understanding of GABAergic synaptic transmission. Here we introduce QD-SPT experiments that provide further insights into the molecular mechanism supporting GABAergic synapses. QD-SPT studies revealed that glutamate and Ca signaling is involved in (a) the maintenance of GABAergic synapses, (b) GABAergic long-term depression, and GABAergic long-term potentiation, by specifically activating signaling pathways unique to each phenomenon. We also introduce a novel Ca imaging technique to describe the diversity of Ca signals that may activate the downstream signaling pathways that induce specific biological output.

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Inhibitory synaptic transmission tuned by Ca and glutamate through the control of GABA R lateral diffusion dynamics.

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References

Michalet X, Pinaud F, Bentolila L, Tsay J, Doose S, Li J . Quantum dots for live cells, in vivo imaging, and diagnostics. Science. 2005; 307(5709):538-44. PMC: 1201471. DOI: 10.1126/science.1104274. View

Swift J, Cramb D . Nanoparticles as fluorescence labels: is size all that matters?. Biophys J. 2008; 95(2):865-76. PMC: 2440474. DOI: 10.1529/biophysj.107.127688. View

Yan D, Tomita S . Defined criteria for auxiliary subunits of glutamate receptors. J Physiol. 2011; 590(1):21-31. PMC: 3300042. DOI: 10.1113/jphysiol.2011.213868. View

Groc L, Lafourcade M, Heine M, Renner M, Racine V, Sibarita J . Surface trafficking of neurotransmitter receptor: comparison between single-molecule/quantum dot strategies. J Neurosci. 2007; 27(46):12433-7. PMC: 6673310. DOI: 10.1523/JNEUROSCI.3349-07.2007. View

Smith K, Davenport E, Wei J, Li X, Pathania M, Vaccaro V . GIT1 and βPIX are essential for GABA(A) receptor synaptic stability and inhibitory neurotransmission. Cell Rep. 2014; 9(1):298-310. PMC: 4536293. DOI: 10.1016/j.celrep.2014.08.061. View

Bannai H, Levi S, Schweizer C, Dahan M, Triller A . Imaging the lateral diffusion of membrane molecules with quantum dots. Nat Protoc. 2007; 1(6):2628-34. DOI: 10.1038/nprot.2006.429. View

Wen X, Van Hook M, Grassmeyer J, Wiesman A, Rich G, Cork K . Endocytosis sustains release at photoreceptor ribbon synapses by restoring fusion competence. J Gen Physiol. 2018; 150(4):591-611. PMC: 5881445. DOI: 10.1085/jgp.201711919. View

Fricke S, Metzdorf K, Ohm M, Haak S, Heine M, Korte M . Fast Regulation of GABAR Diffusion Dynamics by Nogo-A Signaling. Cell Rep. 2019; 29(3):671-684.e6. DOI: 10.1016/j.celrep.2019.09.015. View

Marsden K, Shemesh A, Bayer K, Carroll R . Selective translocation of Ca2+/calmodulin protein kinase IIalpha (CaMKIIalpha) to inhibitory synapses. Proc Natl Acad Sci U S A. 2010; 107(47):20559-64. PMC: 2996683. DOI: 10.1073/pnas.1010346107. View

10.

Liu S, Zhang Z, Tian Z, Zhao H, Liu H, Sun E . Effectively and efficiently dissecting the infection of influenza virus by quantum-dot-based single-particle tracking. ACS Nano. 2011; 6(1):141-50. DOI: 10.1021/nn2031353. View

11.

Bannai H, Niwa F, Sherwood M, Shrivastava A, Arizono M, Miyamoto A . Bidirectional Control of Synaptic GABAAR Clustering by Glutamate and Calcium. Cell Rep. 2015; 13(12):2768-80. PMC: 4700050. DOI: 10.1016/j.celrep.2015.12.002. View

12.

Kasugai Y, Swinny J, Roberts J, Dalezios Y, Fukazawa Y, Sieghart W . Quantitative localisation of synaptic and extrasynaptic GABAA receptor subunits on hippocampal pyramidal cells by freeze-fracture replica immunolabelling. Eur J Neurosci. 2010; 32(11):1868-88. PMC: 4487817. DOI: 10.1111/j.1460-9568.2010.07473.x. View

13.

Bogdanov Y, Michels G, Armstrong-Gold C, Haydon P, Lindstrom J, Pangalos M . Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J. 2006; 25(18):4381-9. PMC: 1570424. DOI: 10.1038/sj.emboj.7601309. View

14.

Bannai H, Levi S, Schweizer C, Inoue T, Launey T, Racine V . Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron. 2009; 62(5):670-82. DOI: 10.1016/j.neuron.2009.04.023. View

15.

Awabdh S, Gupta-Agarwal S, Sheehan D, Muir J, Norkett R, Twelvetrees A . Neuronal activity mediated regulation of glutamate transporter GLT-1 surface diffusion in rat astrocytes in dissociated and slice cultures. Glia. 2016; 64(7):1252-64. PMC: 4915597. DOI: 10.1002/glia.22997. View

16.

Hausrat T, Muhia M, Gerrow K, Thomas P, Hirdes W, Tsukita S . Radixin regulates synaptic GABAA receptor density and is essential for reversal learning and short-term memory. Nat Commun. 2015; 6:6872. PMC: 4411296. DOI: 10.1038/ncomms7872. View

17.

Shigetomi E, Kracun S, Sofroniew M, Khakh B . A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nat Neurosci. 2010; 13(6):759-66. PMC: 2920135. DOI: 10.1038/nn.2557. View

18.

Muir J, Arancibia-Carcamo I, MacAskill A, Smith K, Griffin L, Kittler J . NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the γ2 subunit. Proc Natl Acad Sci U S A. 2010; 107(38):16679-84. PMC: 2944765. DOI: 10.1073/pnas.1000589107. View

19.

Varela J, Dupuis J, Etchepare L, Espana A, Cognet L, Groc L . Targeting neurotransmitter receptors with nanoparticles in vivo allows single-molecule tracking in acute brain slices. Nat Commun. 2016; 7:10947. PMC: 4793083. DOI: 10.1038/ncomms10947. View

20.

Heine M, Groc L, Frischknecht R, Beique J, Lounis B, Rumbaugh G . Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science. 2008; 320(5873):201-5. PMC: 2715948. DOI: 10.1126/science.1152089. View