The Drosophila Actin Regulator ENABLED Regulates Cell Shape and Orientation During Gonad Morphogenesis

PLoS One. 2012;7(12):e52649. doi: 10.1371/journal.pone.0052649. Epub 2012 Dec 26.

Abstract

Organs develop distinctive morphologies to fulfill their unique functions. We used Drosophila embryonic gonads as a model to study how two different cell lineages, primordial germ cells (PGCs) and somatic gonadal precursors (SGPs), combine to form one organ. We developed a membrane GFP marker to image SGP behaviors live. These studies show that a combination of SGP cell shape changes and inward movement of anterior and posterior SGPs leads to the compaction of the spherical gonad. This process is disrupted in mutants of the actin regulator, enabled (ena). We show that Ena coordinates these cell shape changes and the inward movement of the SGPs, and Ena affects the intracellular localization of DE-cadherin (DE-cad). Mathematical simulation based on these observations suggests that changes in DE-cad localization can generate the forces needed to compact an elongated structure into a sphere. We propose that Ena regulates force balance in the SGPs by sequestering DE-cad, leading to the morphogenetic movement required for gonad compaction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cadherins / metabolism
  • Cell Shape
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • DNA-Binding Proteins / physiology
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / embryology*
  • Female
  • Germ Cells / physiology
  • Gonads / cytology
  • Gonads / embryology*
  • Models, Biological
  • Morphogenesis
  • Organogenesis*
  • Protein Transport
  • Stem Cells / physiology
  • Time-Lapse Imaging

Substances

  • Cadherins
  • DNA-Binding Proteins
  • Drosophila Proteins
  • ENA-VASP proteins
  • shg protein, Drosophila