Scalloped and Yorkie are required for cell cycle re-entry of quiescent cells after tissue damage

Development. 2015 Aug 15;142(16):2740-51. doi: 10.1242/dev.119339. Epub 2015 Jul 9.

Abstract

Regeneration of damaged tissues typically requires a population of active stem cells. How damaged tissue is regenerated in quiescent tissues lacking a stem cell population is less well understood. We used a genetic screen in the developing Drosophila melanogaster eye to investigate the mechanisms that trigger quiescent cells to re-enter the cell cycle and proliferate in response to tissue damage. We discovered that Hippo signaling regulates compensatory proliferation after extensive cell death in the developing eye. Scalloped and Yorkie, transcriptional effectors of the Hippo pathway, drive Cyclin E expression to induce cell cycle re-entry in cells that normally remain quiescent in the absence of damage. Ajuba, an upstream regulator of Hippo signaling that functions as a sensor of epithelial integrity, is also required for cell cycle re-entry. Thus, in addition to its well-established role in modulating proliferation during periods of tissue growth, Hippo signaling maintains homeostasis by regulating quiescent cell populations affected by tissue damage.

Keywords: Apoptosis; Cell cycle; Compensatory proliferation; Drosophila; Hippo signaling; Quiescence; Regeneration.

Publication types

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

MeSH terms

  • Animals
  • Cell Cycle / physiology*
  • Cyclin E
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / physiology*
  • Eye / embryology*
  • Female
  • Image Processing, Computer-Assisted
  • In Situ Hybridization, Fluorescence
  • Indoles
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Microscopy, Fluorescence
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Protein Serine-Threonine Kinases / metabolism
  • RNA Interference
  • Regeneration / genetics
  • Regeneration / physiology*
  • Signal Transduction / physiology*
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • YAP-Signaling Proteins
  • beta-Galactosidase

Substances

  • Cyclin E
  • Drosophila Proteins
  • Indoles
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • Trans-Activators
  • Transcription Factors
  • YAP-Signaling Proteins
  • Yki protein, Drosophila
  • sd protein, Drosophila
  • DAPI
  • Protein Serine-Threonine Kinases
  • hpo protein, Drosophila
  • beta-Galactosidase