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Completion of the epithelial to mesenchymal transition in zebrafish mesoderm requires Spadetail

Richard H. Row, Jean-Léon Maîtreb, c, Benjamin L. Martina, Petra Stockingerb, c, Carl-Philipp Heisenbergc,David Kimelmana,

a Department of Biochemistry, University of Washington, Seattle, WA, USA
b Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
c Institute of Science and Technology Austria, A-3400 Klosterneuburg, Austria

Received 7 December 2010; revised 25 March 2011; Accepted 25 March 2011. Available online 2 April 2011.

Abstract

The process of gastrulation is highly conserved across vertebrates on both the genetic and morphological levels, despite great variety in embryonic shape and speed of development. This mechanism spatially separates the germ layers and establishes the organizational foundation for future development. Mesodermal identity is specified in a superficial layer of cells, the epiblast, where cells maintain an epithelioid morphology. These cells involute to join the deeper hypoblast layer where they adopt a migratory, mesenchymal morphology. Expression of a cascade of related transcription factors orchestrates the parallel genetic transition from primitive to mature mesoderm. Although the early and late stages of this process are increasingly well understood, the transition between them has remained largely mysterious. We present here the first high resolution in vivo observations of the blebby transitional morphology of involuting mesodermal cells in a vertebrate embryo. We further demonstrate that the zebrafish spadetail mutation creates a reversible block in the maturation program, stalling cells in the transition state. This mutation creates an ideal system for dissecting the specific properties of cells undergoing the morphological transition of maturing mesoderm, as we demonstrate with a direct measurement of cell–cell adhesion.

Graphical Abstract

Research highlights

► We visualize mesodermal cells undergoing the epithelial–mesenchymal transition. ► We show that cells undergoing the transition are in a highly blebbing state. ► We show that spadetail mutant mesoderm is trapped in the transition state. ► We describe a novel system for examining transition state cells. ► We show that transition state cells are more adhesive than mature mesoderm.

Keywords: Mesoderm; Gastrulation; Involution; Adhesion; Bleb; spadetail; Cadherin; Myosin

 

Source:

Developmental Biology
Volume 354, Issue 1, 1 June 2011, Pages 102-110