Cargando…

Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe

Glial phagocytic activity refines connectivity, though molecular mechanisms regulating this exquisitely sensitive process are incompletely defined. We developed the Drosophila antennal lobe as a model for identifying molecular mechanisms underlying glial refinement of neural circuits in the absence...

Descripción completa

Detalles Bibliográficos
Autores principales: Jindal, Darren A., Leier, Hans C., Salazar, Gabriela, Foden, Alexander J., Seitz, Elizabeth A., Wilkov, Abigail J., Coutinho-Budd, Jaeda C., Broihier, Heather T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272751/
https://www.ncbi.nlm.nih.gov/pubmed/37333889
http://dx.doi.org/10.3389/fncel.2023.1166199
_version_ 1785059566277361664
author Jindal, Darren A.
Leier, Hans C.
Salazar, Gabriela
Foden, Alexander J.
Seitz, Elizabeth A.
Wilkov, Abigail J.
Coutinho-Budd, Jaeda C.
Broihier, Heather T.
author_facet Jindal, Darren A.
Leier, Hans C.
Salazar, Gabriela
Foden, Alexander J.
Seitz, Elizabeth A.
Wilkov, Abigail J.
Coutinho-Budd, Jaeda C.
Broihier, Heather T.
author_sort Jindal, Darren A.
collection PubMed
description Glial phagocytic activity refines connectivity, though molecular mechanisms regulating this exquisitely sensitive process are incompletely defined. We developed the Drosophila antennal lobe as a model for identifying molecular mechanisms underlying glial refinement of neural circuits in the absence of injury. Antennal lobe organization is stereotyped and characterized by individual glomeruli comprised of unique olfactory receptor neuronal (ORN) populations. The antennal lobe interacts extensively with two glial subtypes: ensheathing glia wrap individual glomeruli, while astrocytes ramify considerably within them. Phagocytic roles for glia in the uninjured antennal lobe are largely unknown. Thus, we tested whether Draper regulates ORN terminal arbor size, shape, or presynaptic content in two representative glomeruli: VC1 and VM7. We find that glial Draper limits the size of individual glomeruli and restrains their presynaptic content. Moreover, glial refinement is apparent in young adults, a period of rapid terminal arbor and synapse growth, indicating that synapse addition and elimination occur simultaneously. Draper has been shown to be expressed in ensheathing glia; unexpectedly, we find it expressed at high levels in late pupal antennal lobe astrocytes. Surprisingly, Draper plays differential roles in ensheathing glia and astrocytes in VC1 and VM7. In VC1, ensheathing glial Draper plays a more significant role in shaping glomerular size and presynaptic content; while in VM7, astrocytic Draper plays the larger role. Together, these data indicate that astrocytes and ensheathing glia employ Draper to refine circuitry in the antennal lobe before the terminal arbors reach their mature form and argue for local heterogeneity of neuron-glia interactions.
format Online
Article
Text
id pubmed-10272751
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-102727512023-06-17 Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe Jindal, Darren A. Leier, Hans C. Salazar, Gabriela Foden, Alexander J. Seitz, Elizabeth A. Wilkov, Abigail J. Coutinho-Budd, Jaeda C. Broihier, Heather T. Front Cell Neurosci Neuroscience Glial phagocytic activity refines connectivity, though molecular mechanisms regulating this exquisitely sensitive process are incompletely defined. We developed the Drosophila antennal lobe as a model for identifying molecular mechanisms underlying glial refinement of neural circuits in the absence of injury. Antennal lobe organization is stereotyped and characterized by individual glomeruli comprised of unique olfactory receptor neuronal (ORN) populations. The antennal lobe interacts extensively with two glial subtypes: ensheathing glia wrap individual glomeruli, while astrocytes ramify considerably within them. Phagocytic roles for glia in the uninjured antennal lobe are largely unknown. Thus, we tested whether Draper regulates ORN terminal arbor size, shape, or presynaptic content in two representative glomeruli: VC1 and VM7. We find that glial Draper limits the size of individual glomeruli and restrains their presynaptic content. Moreover, glial refinement is apparent in young adults, a period of rapid terminal arbor and synapse growth, indicating that synapse addition and elimination occur simultaneously. Draper has been shown to be expressed in ensheathing glia; unexpectedly, we find it expressed at high levels in late pupal antennal lobe astrocytes. Surprisingly, Draper plays differential roles in ensheathing glia and astrocytes in VC1 and VM7. In VC1, ensheathing glial Draper plays a more significant role in shaping glomerular size and presynaptic content; while in VM7, astrocytic Draper plays the larger role. Together, these data indicate that astrocytes and ensheathing glia employ Draper to refine circuitry in the antennal lobe before the terminal arbors reach their mature form and argue for local heterogeneity of neuron-glia interactions. Frontiers Media S.A. 2023-06-02 /pmc/articles/PMC10272751/ /pubmed/37333889 http://dx.doi.org/10.3389/fncel.2023.1166199 Text en Copyright © 2023 Jindal, Leier, Salazar, Foden, Seitz, Wilkov, Coutinho-Budd and Broihier. 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 Neuroscience
Jindal, Darren A.
Leier, Hans C.
Salazar, Gabriela
Foden, Alexander J.
Seitz, Elizabeth A.
Wilkov, Abigail J.
Coutinho-Budd, Jaeda C.
Broihier, Heather T.
Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe
title Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe
title_full Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe
title_fullStr Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe
title_full_unstemmed Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe
title_short Early Draper-mediated glial refinement of neuropil architecture and synapse number in the Drosophila antennal lobe
title_sort early draper-mediated glial refinement of neuropil architecture and synapse number in the drosophila antennal lobe
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272751/
https://www.ncbi.nlm.nih.gov/pubmed/37333889
http://dx.doi.org/10.3389/fncel.2023.1166199
work_keys_str_mv AT jindaldarrena earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe
AT leierhansc earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe
AT salazargabriela earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe
AT fodenalexanderj earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe
AT seitzelizabetha earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe
AT wilkovabigailj earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe
AT coutinhobuddjaedac earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe
AT broihierheathert earlydrapermediatedglialrefinementofneuropilarchitectureandsynapsenumberinthedrosophilaantennallobe