Dev. Dyn. 2015 Oct;
Tissue thinning and spreading, a morphogenetic movement termed epiboly, is used widely during animal development. In zebrafish, epiboly is a prominent cell movement during gastrulation, whereby a squamous epithelium (the enveloping layer), a multi-layer of loosely packed cells (the deep cells), and a yolk nuclear syncytium (the yolk syncytial layer) undergo coordinated expansion to engulf the yolk and close the blastopore. Elucidating the mechanisms that underlie epiboly is important not only for understanding animal development in general, but also for providing insights into fundamental cell behaviors including cell intercalation, cell adhesion, cell signaling and epithelial morphogenesis. Here, recent work is reviewed with a focus on findings that advance our understanding of (1) the role of actomyosin motors in the yolk cell to drive epiboly, (2) the mechanisms that underlie the spreading of the epithelial enveloping layer, and (3) the regulation of deep cell movements by E-cadherin based adhesion. A discussion of how these new insights add to the current view of epiboly and future prospects is also presented. Overall, the study of zebrafish epiboly can provide general and broadly applicable insights into the genetic, molecular and cellular control of morphogenesis. This article is protected by copyright. All rights reserved.
Luu O, Damm EW, Parent SE, Barua D, Smith TH, Wen JW, Lepage SE, Nagel M, Ibrahim-Gawel H, Huang Y, Bruce AE, Winklbauer R
J. Cell Biol. 2015 Mar;208(6):839-856
Cleft-like boundaries represent a type of cell sorting boundary characterized by the presence of a physical gap between tissues. We studied the cleft-like ectoderm-mesoderm boundary in Xenopus laevis and zebrafish gastrulae. We identified the transcription factor Snail1 as being essential for tissue separation, showed that its expression in the mesoderm depends on noncanonical Wnt signaling, and demonstrated that it enables paraxial protocadherin (PAPC) to promote tissue separation through two novel functions. First, PAPC attenuates planar cell polarity signaling at the ectoderm-mesoderm boundary to lower cell adhesion and facilitate cleft formation. Second, PAPC controls formation of a distinct type of adhesive contact between mesoderm and ectoderm cells that shows properties of a cleft-like boundary at the single-cell level. It consists of short stretches of adherens junction-like contacts inserted between intermediate-sized contacts and large intercellular gaps. These roles of PAPC constitute a self/non-self-recognition mechanism that determines the site of boundary formation at the interface between PAPC-expressing and -nonexpressing cells.
Du S, Draper BW, Mione M, Moens CB, Bruce A
Dev. Biol. 2012 Feb;362(1):11-23
The T-box transcription factor Eomesodermin (Eomes) has been implicated in patterning and morphogenesis in frog, fish and mouse. In zebrafish, one of the two Eomes homologs, Eomesa, has been implicated in dorsal-ventral patterning, epiboly and endoderm specification in experiments employing over-expression, dominant-negative constructs and antisense morpholino oligonucleotides. Here we report for the first time the identification and characterization of an Eomesa mutant generated by TILLING. We find that Eomesa has a strictly maternal role in the initiation of epiboly, which involves doming of the yolk cell up into the overlying blastoderm. By contrast, epiboly progression is normal, demonstrating for the first time that epiboly initiation is genetically separable from progression. The yolk cell microtubules, which are required for epiboly, are defective in maternal-zygotic eomesa mutant embryos. In addition, the deep cells of the blastoderm are more tightly packed and exhibit more bleb-like protrusions than cells in control embryos. We postulate that the doming delay may be the consequence both of overly stabilized yolk cell microtubules and defects in the adhesive properties or motility of deep cells. We also show that Eomesa is required for normal expression of the endoderm markers sox32, bon and og9x; however it is not essential for endoderm formation.