The Snakeskin-Mesh Complex of Smooth Septate Junction Restricts Yorkie to Regulate Intestinal Homeostasis in Drosophila

Stem Cell Reports. 2020 May 12;14(5):828-844. doi: 10.1016/j.stemcr.2020.03.021. Epub 2020 Apr 23.

Abstract

Tight junctions in mammals and septate junctions in insects are essential for epithelial integrity. We show here that, in the Drosophila intestine, smooth septate junction proteins provide barrier and signaling functions. During an RNAi screen for genes that regulate adult midgut tissue growth, we found that loss of two smooth septate junction components, Snakeskin and Mesh, caused a hyperproliferation phenotype. By examining epitope-tagged endogenous Snakeskin and Mesh, we demonstrate that the two proteins are present in the cytoplasm of differentiating enteroblasts and in cytoplasm and septate junctions of mature enterocytes. In both enteroblasts and enterocytes, loss of Snakeskin and Mesh causes Yorkie-dependent expression of the JAK-STAT pathway ligand Upd3, which in turn promotes proliferation of intestinal stem cells. Snakeskin and Mesh form a complex with each other, with other septate junction proteins and with Yorkie. Therefore, the Snakeskin-Mesh complex has both barrier and signaling function to maintain stem cell-mediated tissue homeostasis.

Keywords: Drosophila; Mesh; Snakeskin; Upd3; Yorkie; barrier; intestine; septate junction; signaling; stem cells.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation
  • Cell Self Renewal
  • Cytoplasm / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster
  • Enterocytes / cytology
  • Enterocytes / metabolism*
  • Gap Junctions / metabolism*
  • Homeostasis
  • Janus Kinases / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • STAT Transcription Factors / metabolism
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*
  • YAP-Signaling Proteins

Substances

  • Drosophila Proteins
  • Membrane Proteins
  • Mesh protein, Drosophila
  • Nuclear Proteins
  • STAT Transcription Factors
  • Ssk protein, Drosophila
  • Trans-Activators
  • Upd3 protein, Drosophila
  • YAP-Signaling Proteins
  • Yki protein, Drosophila
  • Janus Kinases