GemC1 governs multiciliogenesis through direct interaction with and transcriptional regulation of p73

J Cell Sci. 2019 Jun 3;132(11):jcs228684. doi: 10.1242/jcs.228684.

Abstract

A distinct combination of transcription factors elicits the acquisition of a specific fate and the initiation of a differentiation program. Multiciliated cells (MCCs) are a specialized type of epithelial cells that possess dozens of motile cilia on their apical surface. Defects in cilia function have been associated with ciliopathies that affect many organs, including brain and airway epithelium. Here we show that the geminin coiled-coil domain-containing protein 1 GemC1 (also known as Lynkeas) regulates the transcriptional activation of p73, a transcription factor central to multiciliogenesis. Moreover, we show that GemC1 acts in a trimeric complex with transcription factor E2F5 and tumor protein p73 (officially known as TP73), and that this complex is important for the activation of the p73 promoter. We also provide in vivo evidence that GemC1 is necessary for p73 expression in different multiciliated epithelia. We further show that GemC1 regulates multiciliogenesis through the control of chromatin organization, and the epigenetic marks/tags of p73 and Foxj1. Our results highlight novel signaling cues involved in the commitment program of MCCs across species and tissues.This article has an associated First Person interview with the first author of the paper.

Keywords: Epigenetic regulation; GMNC; GemC1; Lynkeas; Multiciliated cells; Multiciliogenesis; Transcriptional regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Differentiation
  • Cell Line
  • Chromatin / metabolism
  • Cilia / metabolism*
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism*
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Regulation / genetics*
  • HEK293 Cells
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nuclear Proteins / metabolism
  • Promoter Regions, Genetic / genetics
  • Signal Transduction
  • Transcriptional Activation / genetics
  • Tumor Protein p73 / genetics
  • Tumor Protein p73 / metabolism*

Substances

  • Cell Cycle Proteins
  • Chromatin
  • FOXJ1 protein, mouse
  • Forkhead Transcription Factors
  • Gmnc protein, mouse
  • Nuclear Proteins
  • Trp73 protein, mouse
  • Tumor Protein p73