A role for the extraembryonic yolk syncytial layer in patterning the zebrafish embryo suggested by properties of the hex gene

Abstract

Recent studies in mouse suggest that the extraembryonic endoderm has an important role in early embryonic patterning [1]. To analyze whether similar mechanisms operate in other vertebrates, we cloned the zebrafish homologue of Hex, a homeobox gene that is expressed asymmetrically in the mouse visceral endoderm [2]. Early expression of zebrafish hex is restricted to the dorsal portion of the yolk syncytial layer (YSL), an extraembryonic tissue. By the onset of gastrulation, hex is expressed in the entire dorsal half of the YSL, which directly underlies the cells fated to form the neural plate. We show that hex expression is initially regulated by the maternal Wnt pathway and later by a Bmp-mediated pathway. Overexpression experiments of wild-type and chimeric Hex constructs indicate that Hex functions as a transcriptional repressor and its overexpression led to the downregulation of bmp2b and wnt8 expression and the expansion of chordin expression. These findings provide further evidence that the zebrafish YSL is the functional equivalent of the mouse visceral endoderm and that extraembryonic structures may regulate early embryonic patterning in many vertebrates.

Zebrafish hhex regulates liver development and digestive organ chirality

“…Table 1B). Furthermore, a significant effect on chirality was also seen with selective knock-down hhex activity in the YSL (Table 1C), an extraembryonic tissue (Ho et al, 1999;Kimmel et al, 1985). In contrast, knock-down of YSL hhex activity had no effect on liver development (not shown).…”

“…Roles for hhex in embryonic and forebrain patterning (Brickman et al, 2000;Martinez Barbera et al, 2000), and thyroid (Martinez Barbera et al, 2000), and hematopoietic (Keng et al, 2000) development have been described. hhex appears to function as a transcriptional repressor in early development (Brickman et al, 2000;Ho et al, 1999;Tanaka et al, 1999), although recent data suggest it also functions as a transcriptional activator (Denson et al, 2000). Zebrafish hhex is first expressed in the yolk syncytial layer (YSL), an extraembryonic tissue that forms before the onset of gastrulation (Chin et al, 2000;Ho et al, 1999).…”

“…hhex appears to function as a transcriptional repressor in early development (Brickman et al, 2000;Ho et al, 1999;Tanaka et al, 1999), although recent data suggest it also functions as a transcriptional activator (Denson et al, 2000). Zebrafish hhex is first expressed in the yolk syncytial layer (YSL), an extraembryonic tissue that forms before the onset of gastrulation (Chin et al, 2000;Ho et al, 1999). hhex activity in the YSL has been proposed to play a role in dorsoventral patterning by regulating bmp expression (Ho et al, 1999).…”

“…Zebrafish hhex is first expressed in the yolk syncytial layer (YSL), an extraembryonic tissue that forms before the onset of gastrulation (Chin et al, 2000;Ho et al, 1999). hhex activity in the YSL has been proposed to play a role in dorsoventral patterning by regulating bmp expression (Ho et al, 1999). Zebrafish hhex is also expressed in blood and endothelial precursors, and hhex activity has been shown to be sufficient for hematopoietic and endothelial gene expression (Liao et al, 2000).…”

Molecular and developmental biology of the hemangioblast

“…This indicates that endodermal induction in the extraembryonic region takes place in a very short time window, probably just before gastrulation. The extraembryonic yolk syncytial layer (YSL) in zebrafish is believed to be equivalent to mouse visceral endoderm (Ho et al, 1999) and is reported to have important roles in germ layer patterning in zebrafish and is required for the formation of ventrolateral mesendoderm and induction of the nodal-related genes in the ventrolateral marginal blastomeres (Chen and Kimelman, 2000). While the casanova gene is strongly reduced in the embryo proper, it is normally expressed or up-regulated in the extraembryonic YSL in zebrafish endodermal mutants casanova, bonnie and clyde, and faust (Kikuchi et al, 2001).…”