Characterization of Subcellular Organelles in Cortical Perisynaptic Astrocytes
Perisynaptic astrocytic processes (PAPs) carry out several different functions, from metabolite clearing to control of neuronal excitability and synaptic plasticity. All these functions are likely orchestrated by complex cellular machinery that resides within the PAPs and relies on a fine interplay...
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Frontiers Media S.A.
2021-01-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncel.2020.573944/full |
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| author | Amina Aboufares El Alaoui Amina Aboufares El Alaoui Molly Jackson Mara Fabri Luisa de Vivo Michele Bellesi |
| author_facet | Amina Aboufares El Alaoui Amina Aboufares El Alaoui Molly Jackson Mara Fabri Luisa de Vivo Michele Bellesi |
| author_sort | Amina Aboufares El Alaoui |
| collection | DOAJ |
| description | Perisynaptic astrocytic processes (PAPs) carry out several different functions, from metabolite clearing to control of neuronal excitability and synaptic plasticity. All these functions are likely orchestrated by complex cellular machinery that resides within the PAPs and relies on a fine interplay between multiple subcellular components. However, traditional transmission electron microscopy (EM) studies have found that PAPs are remarkably poor of intracellular organelles, failing to explain how such a variety of PAP functions are achieved in the absence of a proportional complex network of intracellular structures. Here, we use serial block-face scanning EM to reconstruct and describe in three dimensions PAPs and their intracellular organelles in two different mouse cortical regions. We described five distinct organelles, which included empty and full endosomes, phagosomes, mitochondria, and endoplasmic reticulum (ER) cisternae, distributed within three PAPs categories (branches, branchlets, and leaflets). The majority of PAPs belonged to the leaflets category (~60%), with branchlets representing a minority (~37%). Branches were rarely in contact with synapses (<3%). Branches had a higher density of mitochondria and ER cisternae than branchlets and leaflets. Also, branches and branchlets displayed organelles more frequently than leaflets. Endosomes and phagosomes, which accounted for more than 60% of all the organelles detected, were often associated with the same PAP. Likewise, mitochondria and ER cisternae, representing ~40% of all organelles were usually associated. No differences were noted between the organelle distribution of the somatosensory and the anterior cingulate cortex. Finally, the organelle distribution in PAPs did not largely depend on the presence of a spine apparatus or a pre-synaptic mitochondrion in the synapse that PAPs were enwrapping, with some exceptions regarding the presence of phagosomes and ER cisternae, which were slightly more represented around synapses lacking a spine apparatus and a presynaptic mitochondrion, respectively. Thus, PAPs contain several subcellular organelles that could underlie the diverse astrocytic functions carried out at central synapses. |
| first_indexed | 2024-12-16T17:05:36Z |
| format | Article |
| id | doaj.art-ba7dcfbf3b924a7ca3efa5cd0f6db565 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-12-16T17:05:36Z |
| publishDate | 2021-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-ba7dcfbf3b924a7ca3efa5cd0f6db5652022-12-21T22:23:35ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022021-01-011410.3389/fncel.2020.573944573944Characterization of Subcellular Organelles in Cortical Perisynaptic AstrocytesAmina Aboufares El Alaoui0Amina Aboufares El Alaoui1Molly Jackson2Mara Fabri3Luisa de Vivo4Michele Bellesi5Department of Experimental and Clinical Medicine, Marche Polytechnic University, Ancona, ItalySchool of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol, United KingdomSchool of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol, United KingdomDepartment of Experimental and Clinical Medicine, Marche Polytechnic University, Ancona, ItalySchool of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol, United KingdomSchool of Physiology, Pharmacology, and Neuroscience, University of Bristol, Bristol, United KingdomPerisynaptic astrocytic processes (PAPs) carry out several different functions, from metabolite clearing to control of neuronal excitability and synaptic plasticity. All these functions are likely orchestrated by complex cellular machinery that resides within the PAPs and relies on a fine interplay between multiple subcellular components. However, traditional transmission electron microscopy (EM) studies have found that PAPs are remarkably poor of intracellular organelles, failing to explain how such a variety of PAP functions are achieved in the absence of a proportional complex network of intracellular structures. Here, we use serial block-face scanning EM to reconstruct and describe in three dimensions PAPs and their intracellular organelles in two different mouse cortical regions. We described five distinct organelles, which included empty and full endosomes, phagosomes, mitochondria, and endoplasmic reticulum (ER) cisternae, distributed within three PAPs categories (branches, branchlets, and leaflets). The majority of PAPs belonged to the leaflets category (~60%), with branchlets representing a minority (~37%). Branches were rarely in contact with synapses (<3%). Branches had a higher density of mitochondria and ER cisternae than branchlets and leaflets. Also, branches and branchlets displayed organelles more frequently than leaflets. Endosomes and phagosomes, which accounted for more than 60% of all the organelles detected, were often associated with the same PAP. Likewise, mitochondria and ER cisternae, representing ~40% of all organelles were usually associated. No differences were noted between the organelle distribution of the somatosensory and the anterior cingulate cortex. Finally, the organelle distribution in PAPs did not largely depend on the presence of a spine apparatus or a pre-synaptic mitochondrion in the synapse that PAPs were enwrapping, with some exceptions regarding the presence of phagosomes and ER cisternae, which were slightly more represented around synapses lacking a spine apparatus and a presynaptic mitochondrion, respectively. Thus, PAPs contain several subcellular organelles that could underlie the diverse astrocytic functions carried out at central synapses.https://www.frontiersin.org/articles/10.3389/fncel.2020.573944/fullastrocytesynapseperisynaptic astrocytic processeselectron microscopymouse |
| spellingShingle | Amina Aboufares El Alaoui Amina Aboufares El Alaoui Molly Jackson Mara Fabri Luisa de Vivo Michele Bellesi Characterization of Subcellular Organelles in Cortical Perisynaptic Astrocytes Frontiers in Cellular Neuroscience astrocyte synapse perisynaptic astrocytic processes electron microscopy mouse |
| title | Characterization of Subcellular Organelles in Cortical Perisynaptic Astrocytes |
| title_full | Characterization of Subcellular Organelles in Cortical Perisynaptic Astrocytes |
| title_fullStr | Characterization of Subcellular Organelles in Cortical Perisynaptic Astrocytes |
| title_full_unstemmed | Characterization of Subcellular Organelles in Cortical Perisynaptic Astrocytes |
| title_short | Characterization of Subcellular Organelles in Cortical Perisynaptic Astrocytes |
| title_sort | characterization of subcellular organelles in cortical perisynaptic astrocytes |
| topic | astrocyte synapse perisynaptic astrocytic processes electron microscopy mouse |
| url | https://www.frontiersin.org/articles/10.3389/fncel.2020.573944/full |
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