Germline soma communication mediated by gap junction proteins regulates epithelial morphogenesis

PLoS Genet. 2021 Aug 3;17(8):e1009685. doi: 10.1371/journal.pgen.1009685. eCollection 2021 Aug.

Abstract

Gap junction (GJ) proteins, the primary constituents of GJ channels, are conserved determinants of patterning. Canonically, a GJ channel, made up of two hemi-channels contributed by the neighboring cells, facilitates transport of metabolites/ions. Here we demonstrate the involvement of GJ proteins during cuboidal to squamous epithelial transition displayed by the anterior follicle cells (AFCs) from Drosophila ovaries. Somatically derived AFCs stretch and flatten when the adjacent germline cells start increasing in size. GJ proteins, Innexin2 (Inx2) and Innexin4 (Inx4), functioning in the AFCs and germline respectively, promote the shape transformation by modulating calcium levels in the AFCs. Our observations suggest that alterations in calcium flux potentiate STAT activity to influence actomyosin-based cytoskeleton, possibly resulting in disassembly of adherens junctions. Our data have uncovered sequential molecular events underlying the cuboidal to squamous shape transition and offer unique insight into how GJ proteins expressed in the neighboring cells contribute to morphogenetic processes.

Publication types

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

MeSH terms

  • Actomyosin / metabolism
  • Animals
  • Body Patterning
  • Calcium Signaling
  • Connexins / genetics
  • Connexins / metabolism*
  • Cytoskeleton / metabolism
  • Drosophila / growth & development*
  • Drosophila / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Epithelial Cells / metabolism
  • Epithelial Cells / physiology*
  • Female
  • Morphogenesis
  • Ovarian Follicle / metabolism
  • Ovarian Follicle / physiology*

Substances

  • Connexins
  • Drosophila Proteins
  • Zpg protein, Drosophila
  • inx2 protein, Drosophila
  • Actomyosin

Grants and funding

A. S. and S. K. were supported by Junior and Senior Research Fellowships respectively from Indian Council of Medical Research (Govt. of India), S. H. by Junior Research Fellowship from University Grants Commission (Govt. of India). S. A. and P. D. by Junior Research Fellowship from Innovation in Science Pursuit for Inspired Research, Department of Science and Technology (Govt. of India). G. G. was supported by Indian Institute of Science Education and Research Kolkata. G. D. was supported by National of Institutes of Health (USA) Grant (HD093913). This work was supported by the Grant (BT/HRD/35/02/2006) from Department of Biotechnology, Ministry of Science and Technology, Govt. of India to M. P. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.