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Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans

Sexually dimorphic differentiation of sex-shared behaviors is observed across the animal world, but the underlying neurobiological mechanisms are not fully understood. Here we report sexual dimorphism in neurotransmitter release at the neuromuscular junctions (NMJs) of adult Caenorhabditis elegans....

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Autores principales: Yan, Zhenzhen, Cheng, Xinran, Li, Yuansong, Su, Zexiong, Zhou, Yiwei, Liu, Jie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8841764/
https://www.ncbi.nlm.nih.gov/pubmed/35173578
http://dx.doi.org/10.3389/fnmol.2021.780396
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author Yan, Zhenzhen
Cheng, Xinran
Li, Yuansong
Su, Zexiong
Zhou, Yiwei
Liu, Jie
author_facet Yan, Zhenzhen
Cheng, Xinran
Li, Yuansong
Su, Zexiong
Zhou, Yiwei
Liu, Jie
author_sort Yan, Zhenzhen
collection PubMed
description Sexually dimorphic differentiation of sex-shared behaviors is observed across the animal world, but the underlying neurobiological mechanisms are not fully understood. Here we report sexual dimorphism in neurotransmitter release at the neuromuscular junctions (NMJs) of adult Caenorhabditis elegans. Studying worm locomotion confirms sex differences in spontaneous locomotion of adult animals, and quantitative fluorescence analysis shows that excitatory cholinergic synapses, but not inhibitory GABAergic synapses exhibit the adult-specific difference in synaptic vesicles between males and hermaphrodites. Electrophysiological recording from the NMJ of C. elegans not only reveals an enhanced neurotransmitter release but also demonstrates increased sensitivity of synaptic exocytosis to extracellular calcium concentration in adult males. Furthermore, the cholinergic synapses in adult males are characterized with weaker synaptic depression but faster vesicle replenishment than that in hermaphrodites. Interestingly, T-type calcium channels/CCA-1 play a male-specific role in acetylcholine release at the NMJs in adult animals. Taken together, our results demonstrate sexually dimorphic differentiation of synaptic mechanisms at the C. elegans NMJs, and thus provide a new mechanistic insight into how biological sex shapes animal behaviors through sex-shared neurons and circuits.
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spelling pubmed-88417642022-02-15 Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans Yan, Zhenzhen Cheng, Xinran Li, Yuansong Su, Zexiong Zhou, Yiwei Liu, Jie Front Mol Neurosci Molecular Neuroscience Sexually dimorphic differentiation of sex-shared behaviors is observed across the animal world, but the underlying neurobiological mechanisms are not fully understood. Here we report sexual dimorphism in neurotransmitter release at the neuromuscular junctions (NMJs) of adult Caenorhabditis elegans. Studying worm locomotion confirms sex differences in spontaneous locomotion of adult animals, and quantitative fluorescence analysis shows that excitatory cholinergic synapses, but not inhibitory GABAergic synapses exhibit the adult-specific difference in synaptic vesicles between males and hermaphrodites. Electrophysiological recording from the NMJ of C. elegans not only reveals an enhanced neurotransmitter release but also demonstrates increased sensitivity of synaptic exocytosis to extracellular calcium concentration in adult males. Furthermore, the cholinergic synapses in adult males are characterized with weaker synaptic depression but faster vesicle replenishment than that in hermaphrodites. Interestingly, T-type calcium channels/CCA-1 play a male-specific role in acetylcholine release at the NMJs in adult animals. Taken together, our results demonstrate sexually dimorphic differentiation of synaptic mechanisms at the C. elegans NMJs, and thus provide a new mechanistic insight into how biological sex shapes animal behaviors through sex-shared neurons and circuits. Frontiers Media S.A. 2022-01-31 /pmc/articles/PMC8841764/ /pubmed/35173578 http://dx.doi.org/10.3389/fnmol.2021.780396 Text en Copyright © 2022 Yan, Cheng, Li, Su, Zhou and Liu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Neuroscience
Yan, Zhenzhen
Cheng, Xinran
Li, Yuansong
Su, Zexiong
Zhou, Yiwei
Liu, Jie
Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans
title Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans
title_full Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans
title_fullStr Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans
title_full_unstemmed Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans
title_short Sexually Dimorphic Neurotransmitter Release at the Neuromuscular Junction in Adult Caenorhabditis elegans
title_sort sexually dimorphic neurotransmitter release at the neuromuscular junction in adult caenorhabditis elegans
topic Molecular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8841764/
https://www.ncbi.nlm.nih.gov/pubmed/35173578
http://dx.doi.org/10.3389/fnmol.2021.780396
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