Fasciclin 2 functions as an expression-level switch on EGFR to control organ shape and size in Drosophila

PLoS One. 2024 Dec 20;19(12):e0309891. doi: 10.1371/journal.pone.0309891. eCollection 2024.

Abstract

Fasciclin 2 (Drosophila NCAM) is a homophilic Cell Adhesion Molecule expressed at moderate levels in the proliferating epithelial cells of imaginal discs, where it engages EGFR in a cell autonomous auto-stimulatory loop that promotes growth along larval development. In addition, Fasciclin 2 is expressed at high levels in the pre-differentiating cells of imaginal discs. Gain-of-function genetic analysis shows that Fasciclin 2 acts as a non-cell autonomous repressor of EGFR when high expression levels are induced during imaginal disc growth. Loss-of-function genetic analysis shows that this Fasciclin 2 functional facet is required at the end of larval development and it is mediated by interaction with IgCAMs CG15630 (Fipi) and CG33543 (Elff). Thus, Fasciclin 2 bears two complementary functional roles which correspond with different levels of expression. The combined results from loss- and gain-of-function analyses suggest a scenario where the Fasciclin 2/EGFR cell autonomous auto-stimulatory loop promotes cell proliferation until reaching a Fasciclin 2 expression threshold where its non-cell autonomous function stops growth. Thus, cellular integration of Fasciclin 2 autonomous and non-cell autonomous signaling from neighbor cells may be a key regulator component to orchestrate the rate of intercalary cell proliferation and the final size and shape of an organ.

MeSH terms

  • Animals
  • Cell Adhesion Molecules, Neuronal / genetics
  • Cell Adhesion Molecules, Neuronal / metabolism
  • Cell Proliferation
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • ErbB Receptors* / genetics
  • ErbB Receptors* / metabolism
  • Gene Expression Regulation, Developmental
  • Imaginal Discs / growth & development
  • Imaginal Discs / metabolism
  • Larva / genetics
  • Larva / growth & development
  • Larva / metabolism
  • Neural Cell Adhesion Molecules / genetics
  • Neural Cell Adhesion Molecules / metabolism
  • Organ Size
  • Receptors, Invertebrate Peptide / genetics
  • Receptors, Invertebrate Peptide / metabolism

Substances

  • ErbB Receptors
  • Drosophila Proteins
  • fasciclin II
  • Egfr protein, Drosophila
  • Receptors, Invertebrate Peptide
  • Cell Adhesion Molecules, Neuronal
  • Neural Cell Adhesion Molecules

Grants and funding

This work was supported by PID2021-123407OB-I00, CEX2021-001165-S and BFU2016-76295-R from MCIN/AEI/10.13039/501100011033 and by “ERDF a way of making Europe”; PROMETEU 2021-027 from Generalitat Valenciana, and SAF2004-06593 from MCYT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.