The syncytial mammalian muscle fiber contains a heterogeneous population of (myo)nuclei. At the neuromuscular junction (NMJ), myonuclei have specialized positioning and gene expression. However, it remains unclear how myonuclei are recruited and what regulates myonuclear output at the NMJ. Here, we identify specific properties of myonuclei located near the Drosophila larval NMJ. These synaptic myonuclei have increased size in relation to their surrounding cytoplasmic domain (size scaling), increased DNA content (ploidy), and increased levels of transcription factor pMad, a readout for BMP signaling activity. Our genetic manipulations show that local BMP signaling affects muscle size, nuclear size, ploidy, and NMJ size and function. In support, RNA sequencing analysis reveals that pMad regulates genes involved in muscle growth, ploidy (i.e., E2f1), and neurotransmission. Our data suggest that muscle BMP signaling instructs synaptic myonuclear output that positively shapes the NMJ synapse. This study deepens our understanding of how myonuclear heterogeneity supports local signaling demands to fine tune cellular function and NMJ activity.
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October 30 2024
Postsynaptic BMP signaling regulates myonuclear properties in Drosophila larval muscles
Victoria E. von Saucken
,
Victoria E. von Saucken
(Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing - original draft, Writing - review & editing)
1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
, New York, NY, USA
2
Weill Cornell-Rockefeller-Sloan Kettering Tri-Institutional MD-PhD Program
, New York, NY, USA
3
Biochemistry, Cell and Developmental Biology, and Molecular Biology (BCMB) Program, Weill Cornell Graduate School of Medical Sciences
, New York, NY, USA
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Stefanie E. Windner
,
Stefanie E. Windner
(Methodology, Writing - review & editing)
1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
, New York, NY, USA
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Giovanna Armetta
,
Giovanna Armetta
(Formal analysis, Writing - review & editing)
1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
, New York, NY, USA
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Mary K. Baylies
(Data curation, Funding acquisition, Project administration, Resources, Supervision, Validation, Visualization, Writing - review & editing)
1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
, New York, NY, USA
Correspondence to Mary K. Baylies: [email protected]
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Victoria E. von Saucken
Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing - original draft, Writing - review & editing
1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
, New York, NY, USA
2
Weill Cornell-Rockefeller-Sloan Kettering Tri-Institutional MD-PhD Program
, New York, NY, USA
3
Biochemistry, Cell and Developmental Biology, and Molecular Biology (BCMB) Program, Weill Cornell Graduate School of Medical Sciences
, New York, NY, USA
Stefanie E. Windner
Methodology, Writing - review & editing
1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
, New York, NY, USA
Giovanna Armetta
Formal analysis, Writing - review & editing
1
Developmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
, New York, NY, USA
Correspondence to Mary K. Baylies: [email protected]
Disclosures: The authors declare no competing interests exist.
Received:
April 10 2024
Revision Received:
September 13 2024
Accepted:
October 13 2024
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funder(s):
National Institutes of Health
- Award Id(s): R35GM141877,R01AR068128
Funder(s):
National Cancer Institute
- Award Id(s): P30 CA 008748
Funder(s):
National Institute of General Medical Sciences
- Award Id(s): T32GM007739,T32GM152349
© 2024 von Saucken et al.
2024
von Saucken 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/).
J Cell Biol (2025) 224 (1): e202404052.
Article history
Received:
April 10 2024
Revision Received:
September 13 2024
Accepted:
October 13 2024
Citation
Victoria E. von Saucken, Stefanie E. Windner, Giovanna Armetta, Mary K. Baylies; Postsynaptic BMP signaling regulates myonuclear properties in Drosophila larval muscles. J Cell Biol 6 January 2025; 224 (1): e202404052. doi: https://doi.org/10.1083/jcb.202404052
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