Differential positioning of adherens junctions is associated with initiation of epithelial folding.

TitleDifferential positioning of adherens junctions is associated with initiation of epithelial folding.
Publication TypeJournal Articles
Year of Publication2012
AuthorsWang Y-C, Khan Z, Kaschube M, Wieschaus EF
JournalNature
Volume484
Issue7394
Pagination390-3
Date Published2012 Apr 19
ISSN1476-4687
KeywordsAdherens Junctions, Animals, Cell Polarity, Cell Shape, Choristoma, Drosophila melanogaster, Drosophila Proteins, Epithelial Cells, Epithelium, Gastrula, Gastrulation, Glycogen Synthase Kinase 3, Intracellular Signaling Peptides and Proteins, Protein-Serine-Threonine Kinases
Abstract

During tissue morphogenesis, simple epithelial sheets undergo folding to form complex structures. The prevailing model underlying epithelial folding involves cell shape changes driven by myosin-dependent apical constriction. Here we describe an alternative mechanism that requires differential positioning of adherens junctions controlled by modulation of epithelial apical-basal polarity. Using live embryo imaging, we show that before the initiation of dorsal transverse folds during Drosophila gastrulation, adherens junctions shift basally in the initiating cells, but maintain their original subapical positioning in the neighbouring cells. Junctional positioning in the dorsal epithelium depends on the polarity proteins Bazooka and Par-1. In particular, the basal shift that occurs in the initiating cells is associated with a progressive decrease in Par-1 levels. We show that uniform reduction of the activity of Bazooka or Par-1 results in uniform apical or lateral positioning of junctions and in each case dorsal fold initiation is abolished. In addition, an increase in the Bazooka/Par-1 ratio causes formation of ectopic dorsal folds. The basal shift of junctions not only alters the apical shape of the initiating cells, but also forces the lateral membrane of the adjacent cells to bend towards the initiating cells, thereby facilitating tissue deformation. Our data thus establish a direct link between modification of epithelial polarity and initiation of epithelial folding.

DOI10.1038/nature10938
Alternate JournalNature
PubMed ID22456706
PubMed Central IDPMC3597240
Grant List5R37HD15587 / HD / NICHD NIH HHS / United States
P50 GM071508 / GM / NIGMS NIH HHS / United States
R37 HD015587 / HD / NICHD NIH HHS / United States
/ / Howard Hughes Medical Institute / United States