4.4 Article

Developmental regulation of epithelial cell cuboidal-to-squamous transition in Drosophila follicle cells

Journal

DEVELOPMENTAL BIOLOGY
Volume 491, Issue -, Pages 113-125

Publisher

ACADEMIC PRESS INC ELSEVIER SCIENCE
DOI: 10.1016/j.ydbio.2022.09.001

Keywords

Ecdysone; JAK; STAT; Notch; Broad; Follicle cells; Egg chamber; Stretched cells; Squamous cells

Funding

  1. TRiP at Harvard Medical School (NIH/NIGMS) [R01-GM084947]
  2. Florida State University
  3. Faculty Research Committee (FRC)
  4. COSM Research Grant Award from Georgia Southern University
  5. McNair Scholarship
  6. Undergraduate Student Research Assistantship from Georgia Southern University
  7. National Institute of Health [R01GM072562]
  8. National Science Foundation [IOS-1052333]
  9. Chandler Scholarship

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Epithelial cell shape transition between cuboidal and squamous shapes in Drosophila egg chamber is regulated by Notch signaling, ecdysone signaling, and JAK/STAT signaling. Ecdysone signaling is essential for cell stretching, while JAK/STAT signaling regulates cell clustering. This study reveals the inhibitory role of ecdysone signaling in suppressing the zinc-finger transcription factor Broad (Br) and highlights gene expression changes as Br is suppressed and cells become flattened using single-cell RNA sequencing data.
Epithelial cells form continuous membranous structures for organ formation, and these cells are classified into three major morphological categories: cuboidal, columnar, and squamous. It is crucial that cells transition be-tween these shapes during the morphogenetic events of organogenesis, yet this process remains poorly under-stood. All three epithelial cell shapes can be found in the follicular epithelium of Drosophila egg chamber during oogenesis. Squamous cells (SCs) are initially restricted to the anterior terminus in cuboidal shape. They then rapidly become flattened to assume squamous shape by stretching and expansion in 12 h during midoogenesis. Previously, we reported that Notch signaling activated a zinc -finger transcription factor Broad (Br) at the end of early oogenesis. Here we report that ecdysone and JAK/STAT pathways subsequently converge on Br to serve as an important spatiotemporal regulator of this dramatic morphological change of SCs. The early uniform pattern of Br in the follicular epithelium is directly established by Notch signaling at stage 5 of oogenesis. Later, ecdysone and JAK/STAT signaling activities synergize to suppress Br in SCs from stage 8 to 10a, contributing to proper SC squamous shape. During this process, ecdysone signaling is essential for SC stretching, while JAK/STAT regulates SC clustering and cell fate determination. This study reveals an inhibitory role of ecdysone signaling in sup-pressing Br in epithelial cell remodeling. In this study we also used single-cell RNA sequencing data to highlight the shift in gene expression which occurs as Br is suppressed and cells become flattened.

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