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

J Cell Biol. 2022 Apr 4;221(4):e202110073. doi: 10.1083/jcb.202110073. Epub 2022 Feb 23.

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.

Publication types

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

MeSH terms

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

Substances

  • Cytoskeletal Proteins
  • Drosophila Proteins
  • Ribosomal Proteins
  • rib protein, Drosophila