Forces directing germ-band extension in Drosophila embryos

Abstract

Body axis elongation by convergent extension is a conserved developmental process found in all metazoans. Drosophila embryonic germ-band extension is an important morphogenetic process during embryogenesis, by which the length of the germ-band is more than doubled along the anterior-posterior axis. This lengthening is achieved by typical convergent extension, i.e. narrowing the lateral epidermis along the dorsal-ventral axis and simultaneous extension along the anterior-posterior axis. Germ-band extension is largely driven by cell intercalation, whose directionality is determined by the planar polarity of the tissue and ultimately by the anterior-posterior patterning system. In addition, extrinsic tensile forces originating from the invaginating endoderm induce cell shape changes, which transiently contribute to germ-band extension. Here, we review recent progress in understanding of the role of mechanical forces in germ-band extension.

The Drosophila Afadin and ZO-1 homologs Canoe and Polychaetoid act in parallel to maintain epithelial integrity when challenged by adherens junction remodeling

“…One place where unbalanced contractility is a necessary feature of normal cell rearrangements is during germband extension. Wildtype embryos rely on "regulated unbalanced contractility", resulting from the planar polarization of junctional and cytoskeletal proteins (reviewed in Kong et al, 2017)). Actin and myosin accumulate at elevated levels on anterior-posterior (AP) borders while adherens junction proteins and Baz are elevated at dorsal-ventral (DV) borders.…”

“…Baz/Par3 has an interesting and complex relationship with myosin. During germband extension Baz and myosin have opposing planar polarization (reviewed in Kong et al, 2017), with activation of Rho kinase and Abelson tyrosine kinase (Abl) on AP borders working together to simultaneously activate myosin and downregulate cortical localization of AJ proteins and Baz (Simoes Sde et al, 2010;Tamada et al, 2012). The tension generated by myosin contractility reinforces these opposing polarities Fernandez-Gonzalez and Zallen, 2009;Levayer et al, 2011).…”

Tissue tension and not interphase cell shape determines cell division orientation in the Drosophila follicular epithelium

“…In contrast, salivary gland tube formation and germband extension in Drosophila embryos are driven by cell shape changes and cell rearrangements, with the latter process also including an additional small contribution from oriented cell divisions (reviewed in Ref. Girdler & Röper, 2014;Kong et al, 2017).…”

Myosin II is not required for Drosophila tracheal branch elongation and cell intercalation

“…However, external forces acting on tissue boundaries have also been implicated in tissue elongation. For example, extrinsic pulling forces generated by posterior midgut invagination were linked to Drosophila GBE (Butler et al, 2009;Collinet et al, 2015;Kong et al, 2016;Lye et al, 2015), and also the Drosophila wing is shaped by extrinsic tensile forces (Etournay et al, 2015;Ray et al, 2015). Therefore, tissue elongation is a consequence of a combination of local and tissue-scale forces.…”