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

Rajprasad Loganathan, Daniel C. Levings, Jihoon Kim, Michael B. Wells, Hannah Chiu, Yifan Wu, Matthew Slattery, Deborah J. Andrew

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish (US)
Article numbere202110073
JournalJournal of Cell Biology
Volume221
Issue number4
DOIs
StatePublished - Apr 4 2022

Bibliographical note

Funding Information:
This work was supported by National Institutes of Health grants R01DE013899 and R56DE029450 (D.J. Andrew) and R35GM119553 (M. Slattery). The authors declare no competing financial interests.

Publisher Copyright:
© 2022 Loganathan et al. publication date (see http.

Keywords

  • Animals
  • Cytoskeletal Proteins/metabolism
  • Drosophila Proteins/genetics
  • Drosophila melanogaster/metabolism
  • Promoter Regions, Genetic
  • Ribosomal Proteins/genetics
  • Salivary Glands/metabolism
  • Transcription Initiation Site

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural

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