Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular Junction

Neurexins and neuroligins are common synaptic adhesion molecules that are associated with autism and interact with each other in the synaptic cleft. The Drosophila neuromuscular junction (NMJ) bouton is a well-known model system in neuroscience, and ghost and satellite boutons, respectively, indicat...

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Main Authors: Gan Guangming, Geng Junhua, Zhang Chenchen, Mou Yang, Xie Wei
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnana.2020.00019/full
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author Gan Guangming
Gan Guangming
Geng Junhua
Zhang Chenchen
Zhang Chenchen
Mou Yang
Xie Wei
Xie Wei
author_facet Gan Guangming
Gan Guangming
Geng Junhua
Zhang Chenchen
Zhang Chenchen
Mou Yang
Xie Wei
Xie Wei
author_sort Gan Guangming
collection DOAJ
description Neurexins and neuroligins are common synaptic adhesion molecules that are associated with autism and interact with each other in the synaptic cleft. The Drosophila neuromuscular junction (NMJ) bouton is a well-known model system in neuroscience, and ghost and satellite boutons, respectively, indicate the poor development and overgrowth of the NMJ boutons. However, the Drosophila neurexin (DNrx) and Drosophila neuroligins (DNlgs) are mainly observed in type Ib boutons, indicating the ultrastructural and developmental phenotypes of the Drosophila NMJ. Here, we identified the ultrastructural and developmental features of ghost and satellite boutons by utilizing dneurexin (dnrx) and dneuroligins (dnlgs) fly mutants and other associated fly strains. Ghost boutons contain synaptic vesicles with multiple diameters but very rarely contain T-bar structures and swollen or thin subsynaptic reticulum (SSR) membranes. The muscle cell membrane is invaginated at different sites, stretches to the ghost bouton from different directions, forms several layers that enwrap the ghost bouton, and then branches into the complex SSR. Satellite boutons share a common SSR membrane and present either a typical profile in which a main bouton is encircled by small boutons or two atypical profiles in which the small boutons are grouped together or distributed in beads without a main bouton. Electron and confocal microscopy data showed that dnrx, dnlg1, dnlg2, dnlg3, and dnlg4 mutations led to ghost boutons; the overexpression of dnrx, dnlg1, dnlg2, dnlg3, and dnlg4 led to satellite boutons; and the dnlg2;dnlg3 double mutation also led to satellite boutons. These results suggested that DNrx and DNlgs jointly maintain the development and function of NMJ boutons by regulating the balance of ghost and satellite boutons in Drosophila.
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spelling doaj.art-2ee8ab7c8f3a473e88b1e2361210a9f62022-12-21T18:38:00ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292020-06-011410.3389/fnana.2020.00019519494Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular JunctionGan Guangming0Gan Guangming1Geng Junhua2Zhang Chenchen3Zhang Chenchen4Mou Yang5Xie Wei6Xie Wei7School of Medicine, Southeast University, Nanjing, ChinaThe Key Laboratory of Developmental Genes and Human Disease, Institute of Life Sciences, Southeast University, Nanjing, ChinaThe Key Laboratory of Developmental Genes and Human Disease, Institute of Life Sciences, Southeast University, Nanjing, ChinaSchool of Medicine, Southeast University, Nanjing, ChinaThe Key Laboratory of Developmental Genes and Human Disease, Institute of Life Sciences, Southeast University, Nanjing, ChinaSchool of Medicine, Southeast University, Nanjing, ChinaThe Key Laboratory of Developmental Genes and Human Disease, Institute of Life Sciences, Southeast University, Nanjing, ChinaInstitute of Life Sciences, The Collaborative Innovation Center for Brain Science, Southeast University, Nanjing, ChinaNeurexins and neuroligins are common synaptic adhesion molecules that are associated with autism and interact with each other in the synaptic cleft. The Drosophila neuromuscular junction (NMJ) bouton is a well-known model system in neuroscience, and ghost and satellite boutons, respectively, indicate the poor development and overgrowth of the NMJ boutons. However, the Drosophila neurexin (DNrx) and Drosophila neuroligins (DNlgs) are mainly observed in type Ib boutons, indicating the ultrastructural and developmental phenotypes of the Drosophila NMJ. Here, we identified the ultrastructural and developmental features of ghost and satellite boutons by utilizing dneurexin (dnrx) and dneuroligins (dnlgs) fly mutants and other associated fly strains. Ghost boutons contain synaptic vesicles with multiple diameters but very rarely contain T-bar structures and swollen or thin subsynaptic reticulum (SSR) membranes. The muscle cell membrane is invaginated at different sites, stretches to the ghost bouton from different directions, forms several layers that enwrap the ghost bouton, and then branches into the complex SSR. Satellite boutons share a common SSR membrane and present either a typical profile in which a main bouton is encircled by small boutons or two atypical profiles in which the small boutons are grouped together or distributed in beads without a main bouton. Electron and confocal microscopy data showed that dnrx, dnlg1, dnlg2, dnlg3, and dnlg4 mutations led to ghost boutons; the overexpression of dnrx, dnlg1, dnlg2, dnlg3, and dnlg4 led to satellite boutons; and the dnlg2;dnlg3 double mutation also led to satellite boutons. These results suggested that DNrx and DNlgs jointly maintain the development and function of NMJ boutons by regulating the balance of ghost and satellite boutons in Drosophila.https://www.frontiersin.org/article/10.3389/fnana.2020.00019/fullneurexinneuroliginsDrosophilaneuromuscular junctionghost boutonsatellite boutons
spellingShingle Gan Guangming
Gan Guangming
Geng Junhua
Zhang Chenchen
Zhang Chenchen
Mou Yang
Xie Wei
Xie Wei
Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular Junction
Frontiers in Neuroanatomy
neurexin
neuroligins
Drosophila
neuromuscular junction
ghost bouton
satellite boutons
title Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular Junction
title_full Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular Junction
title_fullStr Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular Junction
title_full_unstemmed Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular Junction
title_short Neurexin and Neuroligins Maintain the Balance of Ghost and Satellite Boutons at the Drosophila Neuromuscular Junction
title_sort neurexin and neuroligins maintain the balance of ghost and satellite boutons at the drosophila neuromuscular junction
topic neurexin
neuroligins
Drosophila
neuromuscular junction
ghost bouton
satellite boutons
url https://www.frontiersin.org/article/10.3389/fnana.2020.00019/full
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