Actin maintains synaptic transmission by restraining vesicle release probability

Summary: Despite decades of pharmacological studies, how the ubiquitous cytoskeletal actin regulates synaptic transmission remains poorly understood. We addressed this issue with a tissue-specific knockout of actin β-isoform or γ-isoform, combined with recordings of postsynaptic EPSCs, presynaptic c...

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Main Authors: Xin-Sheng Wu, Zhen Zhang, Yinghui Jin, Afreen Mushtaheed, Ling-Gang Wu
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225002603
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author Xin-Sheng Wu
Zhen Zhang
Yinghui Jin
Afreen Mushtaheed
Ling-Gang Wu
author_facet Xin-Sheng Wu
Zhen Zhang
Yinghui Jin
Afreen Mushtaheed
Ling-Gang Wu
author_sort Xin-Sheng Wu
collection DOAJ
description Summary: Despite decades of pharmacological studies, how the ubiquitous cytoskeletal actin regulates synaptic transmission remains poorly understood. We addressed this issue with a tissue-specific knockout of actin β-isoform or γ-isoform, combined with recordings of postsynaptic EPSCs, presynaptic capacitance jumps or fluorescent synaptophysin-pHluorin changes, and electron microscopy in large calyx-type and small conventional hippocampal synapses. We found that actin restrains basal synaptic transmission during single action potential firings by lowering the readily releasable vesicle’s release probability. Such an inhibition of basal synaptic transmission is turned into facilitation during repetitive firings by slowing down depletion of the readily releasable vesicle pool and, thus, short-term synaptic depression, leading to more effective synaptic transmission for a longer time. These mechanisms, together with the previous finding that actin promotes vesicle replenishment to the readily releasable pool, may control synaptic transmission and short-term synaptic plasticity at many synapses, contributing to neurological disorders caused by actin cytoskeleton impairment.
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spelling doaj-art-a0ff62c04aa247d6ba08130cd2238e702025-08-20T02:11:09ZengElsevieriScience2589-00422025-03-0128311200010.1016/j.isci.2025.112000Actin maintains synaptic transmission by restraining vesicle release probabilityXin-Sheng Wu0Zhen Zhang1Yinghui Jin2Afreen Mushtaheed3Ling-Gang Wu4National Institute of Neurological Disorders and Stroke, 35 Convent Dr., Bethesda, MD 20892, USANational Institute of Neurological Disorders and Stroke, 35 Convent Dr., Bethesda, MD 20892, USA; Office of Genetic Drugs, Center for Drug Evaluation and Research, Food and Drug Administration, 10903 New Hampshire Avenue, Silver Spring, MD 20993, USANational Institute of Neurological Disorders and Stroke, 35 Convent Dr., Bethesda, MD 20892, USANational Institute of Neurological Disorders and Stroke, 35 Convent Dr., Bethesda, MD 20892, USANational Institute of Neurological Disorders and Stroke, 35 Convent Dr., Bethesda, MD 20892, USA; Corresponding authorSummary: Despite decades of pharmacological studies, how the ubiquitous cytoskeletal actin regulates synaptic transmission remains poorly understood. We addressed this issue with a tissue-specific knockout of actin β-isoform or γ-isoform, combined with recordings of postsynaptic EPSCs, presynaptic capacitance jumps or fluorescent synaptophysin-pHluorin changes, and electron microscopy in large calyx-type and small conventional hippocampal synapses. We found that actin restrains basal synaptic transmission during single action potential firings by lowering the readily releasable vesicle’s release probability. Such an inhibition of basal synaptic transmission is turned into facilitation during repetitive firings by slowing down depletion of the readily releasable vesicle pool and, thus, short-term synaptic depression, leading to more effective synaptic transmission for a longer time. These mechanisms, together with the previous finding that actin promotes vesicle replenishment to the readily releasable pool, may control synaptic transmission and short-term synaptic plasticity at many synapses, contributing to neurological disorders caused by actin cytoskeleton impairment.http://www.sciencedirect.com/science/article/pii/S2589004225002603Biological sciencesNeuroscienceCell biologySpecialized functions of cells
spellingShingle Xin-Sheng Wu
Zhen Zhang
Yinghui Jin
Afreen Mushtaheed
Ling-Gang Wu
Actin maintains synaptic transmission by restraining vesicle release probability
iScience
Biological sciences
Neuroscience
Cell biology
Specialized functions of cells
title Actin maintains synaptic transmission by restraining vesicle release probability
title_full Actin maintains synaptic transmission by restraining vesicle release probability
title_fullStr Actin maintains synaptic transmission by restraining vesicle release probability
title_full_unstemmed Actin maintains synaptic transmission by restraining vesicle release probability
title_short Actin maintains synaptic transmission by restraining vesicle release probability
title_sort actin maintains synaptic transmission by restraining vesicle release probability
topic Biological sciences
Neuroscience
Cell biology
Specialized functions of cells
url http://www.sciencedirect.com/science/article/pii/S2589004225002603
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AT yinghuijin actinmaintainssynaptictransmissionbyrestrainingvesiclereleaseprobability
AT afreenmushtaheed actinmaintainssynaptictransmissionbyrestrainingvesiclereleaseprobability
AT linggangwu actinmaintainssynaptictransmissionbyrestrainingvesiclereleaseprobability