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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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Autores principales: Loganathan, Rajprasad, Levings, Daniel C., Kim, Ji Hoon, Wells, Michael B., Chiu, Hannah, Wu, Yifan, Slattery, Matthew, Andrew, Deborah J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9237840/
https://www.ncbi.nlm.nih.gov/pubmed/35195669
http://dx.doi.org/10.1083/jcb.202110073
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author Loganathan, Rajprasad
Levings, Daniel C.
Kim, Ji Hoon
Wells, Michael B.
Chiu, Hannah
Wu, Yifan
Slattery, Matthew
Andrew, Deborah J.
author_facet Loganathan, Rajprasad
Levings, Daniel C.
Kim, Ji Hoon
Wells, Michael B.
Chiu, Hannah
Wu, Yifan
Slattery, Matthew
Andrew, Deborah J.
author_sort Loganathan, Rajprasad
collection PubMed
description 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.
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spelling pubmed-92378402022-10-04 Ribbon boosts ribosomal protein gene expression to coordinate organ form and function Loganathan, Rajprasad Levings, Daniel C. Kim, Ji Hoon Wells, Michael B. Chiu, Hannah Wu, Yifan Slattery, Matthew Andrew, Deborah J. J Cell Biol Article 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. Rockefeller University Press 2022-02-23 /pmc/articles/PMC9237840/ /pubmed/35195669 http://dx.doi.org/10.1083/jcb.202110073 Text en © 2022 Loganathan et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/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/).
spellingShingle Article
Loganathan, Rajprasad
Levings, Daniel C.
Kim, Ji Hoon
Wells, Michael B.
Chiu, Hannah
Wu, Yifan
Slattery, Matthew
Andrew, Deborah J.
Ribbon boosts ribosomal protein gene expression to coordinate organ form and function
title Ribbon boosts ribosomal protein gene expression to coordinate organ form and function
title_full Ribbon boosts ribosomal protein gene expression to coordinate organ form and function
title_fullStr Ribbon boosts ribosomal protein gene expression to coordinate organ form and function
title_full_unstemmed Ribbon boosts ribosomal protein gene expression to coordinate organ form and function
title_short Ribbon boosts ribosomal protein gene expression to coordinate organ form and function
title_sort ribbon boosts ribosomal protein gene expression to coordinate organ form and function
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9237840/
https://www.ncbi.nlm.nih.gov/pubmed/35195669
http://dx.doi.org/10.1083/jcb.202110073
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