Developmental neuronal remodeling is extensive and mechanistically diverse across the nervous system. We sought to identify Drosophila pupal neurons that underwent mechanistically new types of neuronal remodeling and describe remodeling Beat-VaM and Beat-VaL neurons. We show that Beat-VaM neurons produce highly branched neurites in the CNS during larval stages that undergo extensive local pruning. Surprisingly, although the ecdysone receptor (EcR) is essential for pruning in all other cell types studied, Beat-VaM neurons remodel their branches extensively despite cell autonomous blockade EcR or caspase signaling. Proper execution of local remodeling in Beat-VaM neurons instead depends on extrinsic signaling from astrocytes converging with intrinsic and less dominant EcR-regulated mechanisms. In contrast, Beat-VaL neurons undergo steroid hormone–dependent, apoptotic cell death, which we show relies on the segment-specific expression of the Hox gene Abd-B. Our work provides new cell types in which to study neuronal remodeling, highlights an important role for astrocytes in activating local pruning in Drosophila independent of steroid signaling, and defines a Hox gene-mediated mechanism for segment-specific cell elimination.
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6 January 2025
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December 09 2024
Astrocyte-dependent local neurite pruning in Beat-Va neurons
Katherine S. Lehmann
,
Katherine S. Lehmann
(Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Validation, Visualization, Writing - original draft, Writing - review & editing)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
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Madison T. Hupp
,
Madison T. Hupp
(Data curation, Investigation, Visualization, Writing - review & editing)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
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Leire Abalde-Atristain
,
Leire Abalde-Atristain
(Data curation, Formal analysis, Investigation, Validation, Writing - review & editing)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
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Amanda Jefferson
,
Amanda Jefferson
(Data curation, Investigation, Validation, Writing - review & editing)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
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Ya-Chen Cheng
,
Ya-Chen Cheng
(Resources)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
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Amy E. Sheehan
,
Amy E. Sheehan
(Investigation, Resources)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
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Yunsik Kang
,
(Conceptualization, Data curation, Investigation, Methodology, Project administration, Supervision, Validation, Visualization, Writing - review & editing)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
2Department of Cell and Developmental Biology,
University of Colorado School of Medicine
, Aurora, CO, USA
Correspondence to Yunsik Kang: [email protected]
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Marc R. Freeman
(Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing - original draft, Writing - review & editing)
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
Marc R. Freeman: [email protected]
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Katherine S. Lehmann
Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Validation, Visualization, Writing - original draft, Writing - review & editing
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
Madison T. Hupp
Data curation, Investigation, Visualization, Writing - review & editing
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
Leire Abalde-Atristain
Data curation, Formal analysis, Investigation, Validation, Writing - review & editing
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
Amanda Jefferson
Data curation, Investigation, Validation, Writing - review & editing
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
Ya-Chen Cheng
Resources
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
Amy E. Sheehan
Investigation, Resources
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
Yunsik Kang
Conceptualization, Data curation, Investigation, Methodology, Project administration, Supervision, Validation, Visualization, Writing - review & editing
1
Vollum Institute, Oregon Health & Science University
, Portland, OR, USA
2Department of Cell and Developmental Biology,
University of Colorado School of Medicine
, Aurora, CO, USA
Correspondence to Yunsik Kang: [email protected]
Marc R. Freeman: [email protected]
Disclosures: The authors declare no competing interests exist.
Received:
December 07 2023
Revision Received:
July 01 2024
Accepted:
September 05 2024
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funder(s):
National Science Foundation
- Award Id(s): DGE-1448072
Funder(s):
Damon Runyon Fellowship
- Award Id(s): DRG 2329-18
Funder(s):
National Institutes of Health
- Award Id(s): K99 NS126642-01
Funder(s):
National Institute of Neurological Disorders and Stroke
- Award Id(s): RO1s R37NS053538,R01NS124146
© 2024 Lehmann et al.
2024
Lehmann et al.
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
This work is licensed under a
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License
.
J Cell Biol (2025) 224 (1): e202312043.
Article history
Received:
December 07 2023
Revision Received:
July 01 2024
Accepted:
September 05 2024
Citation
Katherine S. Lehmann, Madison T. Hupp, Leire Abalde-Atristain, Amanda Jefferson, Ya-Chen Cheng, Amy E. Sheehan, Yunsik Kang, Marc R. Freeman; Astrocyte-dependent local neurite pruning in Beat-Va neurons. J Cell Biol 6 January 2025; 224 (1): e202312043. doi: https://doi.org/10.1083/jcb.202312043
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