Ribbon boosts ribosomal protein gene expression to coordinate organ form and function

Cell growth is well defined for late (postembryonic) stages of development, but evidence for early (embryonic) cell growth during postmitotic morphogenesis is limited. Here, we report early cell growth as a key characteristic of tubulogenesis in the Drosophila embryonic salivary gland (SG) and trach...

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Published in:The Journal of cell biology 2022-04, Vol.221 (4), p.1
Main Authors: Loganathan, Rajprasad, Levings, Daniel C, Kim, Ji Hoon, Wells, Michael B, Chiu, Hannah, Wu, Yifan, Slattery, Matthew, Andrew, Deborah J
Format: Article
Language:English
Subjects:
Animals
Cell growth
Cytoskeletal Proteins - metabolism
Development
Developmental stages
Drosophila melanogaster - metabolism
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Embryogenesis
Gene expression
Morphogenesis
Promoter Regions, Genetic
Protein Homeostasis
Proteins
Ribosomal Proteins - genetics
Salivary gland
Salivary glands
Salivary Glands - metabolism
Trachea
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Summary:Cell growth is well defined for late (postembryonic) stages of development, but evidence for early (embryonic) cell growth during postmitotic morphogenesis is limited. Here, we report early cell growth as a key characteristic of tubulogenesis in the Drosophila embryonic salivary gland (SG) and trachea. A BTB/POZ domain nuclear factor, Ribbon (Rib), mediates this early cell growth. Rib binds the transcription start site of nearly every SG-expressed ribosomal protein gene (RPG) and is required for full expression of all RPGs tested. Rib binding to RPG promoters in vitro is weak and not sequence specific, suggesting that specificity is achieved through cofactor interactions. Accordingly, we demonstrate Rib's ability to physically interact with each of the three known regulators of RPG transcription. Surprisingly, Rib-dependent early cell growth in another tubular organ, the embryonic trachea, is not mediated by direct RPG transcription. These findings support a model of early cell growth customized by transcriptional regulatory networks to coordinate organ form and function.
ISSN:0021-9525
1540-8140
DOI:10.1083/jcb.202110073