Developmental and activity-dependent modulation of coupling distance between release site and Ca2+ channel

Midorikawa, Mitsuharu (2022) Developmental and activity-dependent modulation of coupling distance between release site and Ca2+ channel. Frontiers in Cellular Neuroscience, 16. ISSN 1662-5102

[thumbnail of pubmed-zip/versions/1/package-entries/fncel-16-1037721/fncel-16-1037721.pdf] Text
pubmed-zip/versions/1/package-entries/fncel-16-1037721/fncel-16-1037721.pdf - Published Version

Download (703kB)

Abstract

Developmental and activity-dependent modulation of coupling distance between release site and Ca2+ channel Mitsuharu Midorikawa

Synapses are junctions between a presynaptic neuron and a postsynaptic cell specialized for fast and precise information transfer. The presynaptic terminal secretes neurotransmitters via exocytosis of synaptic vesicles. Exocytosis is a tightly regulated reaction that occurs within a millisecond of the arrival of an action potential. One crucial parameter in determining the characteristics of the transmitter release kinetics is the coupling distance between the release site and the Ca 2+ channel. Still, the technical limitations have hindered detailed analysis from addressing how the coupling distance is regulated depending on the development or activity of the synapse. However, recent technical advances in electrophysiology and imaging are unveiling their different configurations in different conditions. Here, I will summarize developmental- and activity-dependent changes in the coupling distances revealed by recent studies.
10 26 2022 1037721 10.3389/fncel.2022.1037721 1 10.3389/crossmark-policy frontiersin.org true Japan Society for the Promotion of Science http://dx.doi.org/10.13039/501100001691 22K19367 Japan Society for the Promotion of Science http://dx.doi.org/10.13039/501100001691 21H02583 Japan Society for the Promotion of Science http://dx.doi.org/10.13039/501100001691 19H03343 Japan Society for the Promotion of Science http://dx.doi.org/10.13039/501100001691 20H05916 Brain Science Foundation http://dx.doi.org/10.13039/100012131 Takeda Science Foundation http://dx.doi.org/10.13039/100007449 https://creativecommons.org/licenses/by/4.0/ 10.3389/fncel.2022.1037721 https://www.frontiersin.org/articles/10.3389/fncel.2022.1037721/full https://www.frontiersin.org/articles/10.3389/fncel.2022.1037721/full Nature Abbott 431 796 2004 Synaptic computation. 10.1038/nature03010 Neuron Acuna 87 1234 2015 RIM-BPs mediate tight coupling of action potentials to Ca(2+)-triggered neurotransmitter release. 10.1016/j.neuron.2015.08.027 J. Neurosci. Adler 11 1496 1991 Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. 10.1523/jneurosci.11-06-01496.1991 J Physiol. Augustine 431 343 1990 Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current. 10.1113/jphysiol.1990.sp018333 Neuron Bacaj 80 947 2013 Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release. 10.1016/j.neuron.2013.10.026 Nat. Neurosci. Böhme 19 1311 2016 Active zone scaffolds differentially accumulate Unc13 isoforms to tune Ca(2+) channel-vesicle coupling. 10.1038/nn.4364 Science Bolshakov 269 1730 1995 Regulation of hippocampal transmitter release during development and long-term potentiation. 10.1126/science.7569903 Nature Borst 383 431 1996 Calcium influx and transmitter release in a fast CNS synapse. 10.1038/383431a0 Philos Trans R Soc Lond B Biol Sci. Borst 354 347 1999 Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem. 10.1098/rstb.1999.0386 Neuron Bucurenciu 57 536 2008 Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. 10.1016/j.neuron.2007.12.026 J. Neurosci. Budisantoso 32 2357 2012 Mechanisms underlying signal filtering at a multisynapse contact. 10.1523/jneurosci.5243-11.2012 J. Neurosci. Butola 41 7742 2021 RIM-binding protein 2 organizes Ca2+ channel topography and regulates release probability and vesicle replenishment at a fast central synapse. 10.1523/jneurosci.0586-21.2021 Elife Calloway 4 728 2015 The active-zone protein munc13 controls the use-dependence of presynaptic voltage-gated calcium channels. 10.7554/eLife.07728 J. Neurosci. Chen 33 8336 2013 The Munc13 proteins differentially regulate readily releasable pool dynamics and calcium-dependent recovery at a central synapse. 10.1523/jneurosci.5128-12.2013 Annu. Rev. Physiol. Davis 77 251 2015 Homeostatic control of presynaptic neurotransmitter release. 10.1146/annurev-physiol-021014-071740 Cell Rep. Dong 24 284 2018 CAST/ELKS proteins control voltage-gated Ca2+ channel density and synaptic release probability at a mammalian central synapse. 10.1016/j.celrep.2018.06.024 Nat. Rev. Neurosci. Eggermann 13 7 2011 Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. 10.1038/nrn3125 Front Cell Neurosci. Eshra 13 289 2019 Enriched environment shortens the duration of action potentials in cerebellar granule cells. 10.3389/fncel.2019.00289 J. Neurosci. Fedchyshyn 25 4131 2005 Developmental transformation of the release modality at the calyx of held synapse. 10.1523/JNEUROSCI.0350-05.2005 Proc. Natl. Acad. Sci. U.S.A. Fukaya 118 e2016754118 2021 Rapid Ca2+ channel accumulation contributes to cAMP-mediated increase in transmission at hippocampal mossy fiber synapses. 10.1073/pnas.2016754118 Neuron Geiger 28 927 2000 Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons. 10.1016/s0896-6273(00)00164-1 Proc. Natl. Acad. Sci. U.S.A. Grauel 113 11615 2016 RIM-binding protein 2 regulates release probability by fine-tuning calcium channel localization at murine hippocampal synapses. 10.1073/pnas.1605256113 Proc Natl. Acad. Sci. U.S.A. Hallermann 100 8975 2003 A large pool of releasable vesicles in a cortical glutamatergic synapse. 10.1073/pnas.1432836100 J. Neurophysiol. Han 113 255 2015 RIM1 and RIM2 redundantly determine Ca2+ channel density and readily releasable pool size at a large hindbrain synapse. 10.1152/jn.00488.2014 Neuron Held 107 667 2020 Synapse and active zone assembly in the absence of presynaptic Ca2+ channels and Ca2+ entry. 10.1016/j.neuron.2020.05.032 Neuron Hooks 106 21 2020 Circuitry underlying experience-dependent plasticity in the mouse visual system. 10.1016/j.neuron.2020.01.031 Cell Huang 79 69 1994 cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. 10.1016/0092-8674(94)90401-4 Nature Jackman 529 88 2016 The calcium sensor synaptotagmin 7 is required for synaptic facilitation. 10.1038/nature16507 J. Neurosci. Joselevitch 40 7390 2020 Direct observation of vesicle transport on the synaptic ribbon provides evidence that vesicles are mobilized and prepared rapidly for release. 10.1523/JNEUROSCI.0605-20.2020 Cell Kaeser 144 282 2011 RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. 10.1016/j.cell.2010.12.029 F1000Res Kano 8 18903 2019 Developmental synapse remodeling in the cerebellum and visual thalamus. 10.12688/f1000research.18903.1 Neuron Kawaguchi 85 1273 2015 Control of inhibitory synaptic outputs by low excitability of axon terminals revealed by direct recording. 10.1016/j.neuron.2015.02.013 Cell Rep. Kawaguchi 21 3338 2017 Fast Ca2+ buffer-dependent reliable but plastic transmission at small CNS synapses revealed by direct bouton recording. 10.1016/j.celrep.2017.11.072 Nat. Neurosci. Kiyonaka 10 691 2007 RIM1 confers sustained activity and neurotransmitter vesicle anchoring to presynaptic Ca2+ channels. 10.1038/nn1904 J Physiol. Kochubey 587 3009 2009 Developmental regulation of the intracellular Ca2+ sensitivity of vesicle fusion and Ca2+-secretion coupling at the rat calyx of Held. 10.1113/jphysiol.2009.172387 Cell Rep. Kusch 22 1965 2018 Munc13-3 is required for the developmental localization of Ca2+ channels to active zones and the nanopositioning of Cav2.1 near release sensors. 10.1016/j.celrep.2018.02.010 J. Comput. Neurol. LeVay 191 1 1980 The development of ocular dominance columns in normal and visually deprived monkeys. 10.1002/cne.901910102 Science Liu 334 1565 2011 RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. 10.1126/science.1212991 Neuron Lübbert 101 260 2019 CaV2.1 α1 subunit expression regulates presynaptic CaV2.1 abundance and synaptic strength at a central synapse. 10.1016/j.neuron.2018.11.028 Neuron Luo 94 826 2017 Synaptotagmin-7-mediated asynchronous release boosts high-fidelity synchronous transmission at a central synapse. 10.1016/j.neuron.2017.04.020 EMBO J. Luo 39 e103208 2020 Neurexins cluster Ca2+ channels within the presynaptic active zone. 10.15252/embj.2019103208 Nature Malinow 346 177 1990 Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. 10.1038/346177a0 J. Neurosci. Meinrenken 22 1648 2002 Calcium secretion coupling at calyx of held governed by nonuniform channel-vesicle topography. 10.1523/jneurosci.22-05-01648.2002 Neurosci. Res. Midorikawa 181 1 2022 Pathway-specific maturation of presynaptic functions of the somatosensory thalamus. 10.1016/j.neures.2022.04.008 Proc. Natl. Acad. Sci. U.S.A. Midorikawa 2021 118 2021 Distinct functional developments of surviving and eliminated presynaptic terminals. 10.1073/pnas.2022423118 Neuron Midorikawa 88 492 2015 Imaging exocytosis of single synaptic vesicles at a fast CNS presynaptic terminal. 10.1016/j.neuron.2015.09.047 Neuron Midorikawa 96 1033 2017 Kinetics of releasable synaptic vesicles and their plastic changes at hippocampal mossy fiber synapses. 10.1016/j.neuron.2017.10.016 Nat. Neurosci. Midorikawa 10 1268 2007 Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells. 10.1038/nn1963 Nature Missler 423 939 2003 Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. 10.1038/nature01755 Neuron Nakamura 85 145 2015 Nanoscale distribution of presynaptic Ca(2+) channels and its impact on vesicular release during development. 10.1016/j.neuron.2014.11.019 J. Neurosci. Nakamura 38 3971 2018 Variations in Ca2+ influx can alter chelator-based estimates of Ca2+ channel-synaptic vesicle coupling distance. 10.1523/JNEUROSCI.2061-17.2018 Proc. Natl. Acad. Sci. U.S.A. Ngodup 112 6479 2015 Activity-dependent, homeostatic regulation of neurotransmitter release from auditory nerve fibers. 10.1073/pnas.1420885112 Nat. Rev. Neurosci. Nicoll 6 863 2005 Synaptic plasticity at hippocampal mossy fibre synapses. 10.1038/nrn1786 J. Physiol. Ohana 513 135 1998 Transmitter release modulation in nerve terminals of rat neocortical pyramidal cells by intracellular calcium buffers. 10.1111/j.1469-7793.1998.135by.x J. Physiol. Oleskevich 560 709 2004 Presynaptic plasticity at two giant auditory synapses in normal and deaf mice. 10.1113/jphysiol.2004.066662 J. Neurosci. Pouzat 17 9104 1997 Developmental regulation of basket/stellate cell–>Purkinje cell synapses in the cerebellum. 10.1523/jneurosci.17-23-09104.1997 Neuron Rebola 104 693 2019 Distinct nanoscale calcium channel and synaptic vesicle topographies contribute to the diversity of synaptic function. 10.1016/j.neuron.2019.08.014 Neuron Reddy-Alla 95 1350 2017 Stable positioning of Unc13 restricts synaptic vesicle fusion to defined release sites to promote synchronous neurotransmission. 10.1016/j.neuron.2017.08.016 Cold Spring Harb Perspect Biol. Regehr 4 a005702 2012 Short-term presynaptic plasticity. 10.1101/cshperspect.a005702 J. Physiol. Rozov 531 807 2001 Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. 10.1111/j.1469-7793.2001.0807h.x Proc. JPN Acad. Ser. B Phys. Biol. Sci. Sakaba 94 139 2018 Kinetics of transmitter release at the calyx of Held synapse. 10.2183/pjab.94.010 Nat. Neurosci. Sakamoto 21 41 2018 Synaptic weight set by Munc13-1 supramolecular assemblies 10.1038/s41593-017-0041-9 Neuron Sando 94 312 2017 Assembly of excitatory synapses in the absence of glutamatergic neurotransmission. 10.1016/j.neuron.2017.03.047 Curr. Biol. Schmidt 23 244 2013 Nanodomain coupling at an excitatory cortical synapse. 10.1016/j.cub.2012.12.007 Neuron Schneider 86 672 2015 Mobility of calcium channels in the presynaptic membrane. 10.1016/j.neuron.2015.03.050 Neuron Senn 81 428 2014 Long-range connectivity defines behavioral specificity of amygdala neurons. 10.1016/j.neuron.2013.11.006 Neuron Sigler 94 304 2017 Formation and Maintenance of Functional Spines in the Absence of Presynaptic Glutamate Release. 10.1016/j.neuron.2017.03.029 Neuron Südhof 80 675 2013 Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. 10.1016/j.neuron.2013.10.022 Cell Südhof 171 745 2017 Synaptic neurexin complexes: a molecular code for the logic of neural circuits. 10.1016/j.cell.2017.10.024 Proc. JPN Acad. Ser. B Phys. Biol. Sci. Takahashi 91 305 2015 Strength and precision of neurotransmission at mammalian presynaptic terminals. 10.2183/pjab.91.305 J. Neurosci. Taschenberger 20 9162 2000 Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, epsc kinetics, and synaptic plasticity. 10.1523/jneurosci.20-24-09162.2000 Neuron Taschenberger 36 1127 2002 Optimizing synaptic architecture and efficiency for high-frequency transmission. 10.1016/s0896-6273(02)01137-6 Nature Turecek 551 503 2017 Synaptotagmin 7 confers frequency invariance onto specialized depressing synapses. 10.1038/nature24474 J. Neurosci. Uesaka 27 5215 2007 Interplay between laminar specificity and activity-dependent mechanisms of thalamocortical axon branching. 10.1523/jneurosci.4685-06.2007 J. Neurosci. Uesaka 25 1 2005 Activity dependence of cortical axon branch formation: a morphological and electrophysiological study using organotypic slice cultures. 10.1523/jneurosci.3855-04.2005 Science Verhage 287 864 2000 Synaptic assembly of the brain in the absence of neurotransmitter secretion. 10.1126/science.287.5454.864 Science Vyleta 343 665 2014 Loose coupling between Ca2+ channels and release sensors at a plastic hippocampal synapse. 10.1126/science.1244811 Neuron Wadel 53 563 2007 The coupling between synaptic vesicles and Ca2+ channels determines fast neurotransmitter release. 10.1016/j.neuron.2007.01.021 Nature Weisskopf 376 256 1995 Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses. 10.1038/376256a0 Science Weisskopf 265 1878 1994 Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. 10.1126/science.7916482 Nat Commun. Wentzel 9 267 2018 Dysbindin links presynaptic proteasome function to homeostatic recruitment of low release probability vesicles. 10.1038/s41467-017-02494-0 Front. Synaptic Neurosci. Yang 5 8 2013 Presynaptic long-term plasticity. 10.3389/fnsyn.2013.00008 Science Zalutsky 248 1619 1990 Comparison of two forms of long-term potentiation in single hippocampal neurons. 10.1126/science.2114039 Proc. Natl. Acad. Sci. U.S.A. Zenisek 105 4922 2008 Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. 10.1073/pnas.0709067105 J. Neurosci. Zhuang 37 323 2017 Changes in properties of auditory nerve synapses following conductive hearing loss. 10.1523/jneurosci.0523-16.2016 J. Neurosci. Zhuang 40 6896 2020 Mechanisms and functional consequences of presynaptic homeostatic plasticity at auditory nerve synapses. 10.1523/jneurosci.1175-19.2020 Annu. Rev. Physiol. Zucker 64 355 2002 Short-term synaptic plasticity. 10.1146/annurev.physiol.64.092501.1145s47

Item Type: Article
Subjects: Academic Digital Library > Medical Science
Depositing User: Unnamed user with email info@academicdigitallibrary.org
Date Deposited: 25 Mar 2023 12:57
Last Modified: 18 May 2024 07:15
URI: http://publications.article4sub.com/id/eprint/1045

Actions (login required)

View Item
View Item