The Drosophila Hippo pathway transcription factor Scalloped and its co-factors alter each other's chromatin binding dynamics and transcription in vivo

Dev Cell. 2024 Jul 8;59(13):1640-1654.e5. doi: 10.1016/j.devcel.2024.04.006. Epub 2024 Apr 25.

Abstract

The Hippo pathway is an important regulator of organ growth and cell fate. The major mechanism by which Hippo is known to control transcription is by dictating the nucleo-cytoplasmic shuttling rate of Yorkie, a transcription co-activator, which promotes transcription with the DNA binding protein Scalloped. The nuclear biophysical behavior of Yorkie and Scalloped, and whether this is regulated by the Hippo pathway, remains unexplored. Using multiple live-imaging modalities on Drosophila tissues, we found that Scalloped interacts with DNA on a broad range of timescales, and enrichment of Scalloped at sites of active transcription is mediated by longer DNA dwell times. Further, Yorkie increased Scalloped's DNA dwell time, whereas the repressors Nervous fingers 1 (Nerfin-1) and Tondu-domain-containing growth inhibitor (Tgi) decreased it. Therefore, the Hippo pathway influences transcription not only by controlling nuclear abundance of Yorkie but also by modifying the DNA binding kinetics of the transcription factor Scalloped.

Keywords: Drosophila; Hippo signaling; biophysical behavior; live imaging; transcription; transcription factor.

MeSH terms

  • Animals
  • Cell Nucleus / metabolism
  • Chromatin* / metabolism
  • DNA / genetics
  • DNA / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster* / genetics
  • Drosophila melanogaster* / metabolism
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Protein Binding
  • Protein Serine-Threonine Kinases* / genetics
  • Protein Serine-Threonine Kinases* / metabolism
  • Signal Transduction*
  • Trans-Activators* / genetics
  • Trans-Activators* / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic*
  • YAP-Signaling Proteins* / metabolism

Substances

  • Drosophila Proteins
  • Chromatin
  • sd protein, Drosophila
  • Protein Serine-Threonine Kinases
  • YAP-Signaling Proteins
  • Trans-Activators
  • Yki protein, Drosophila
  • hpo protein, Drosophila
  • Transcription Factors
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • DNA-Binding Proteins
  • DNA