Live analysis of endodermal layer formation identifies random walk as a novel gastrulation movement.
During gastrulation, dramatic movements rearrange cells into three germ layers expanded over the entire embryo [1-3]. In fish, both endoderm and mesoderm are specified as a belt at the embryo margin. Mesodermal layer expansion is achieved through the combination of two directed migrations. The outer ring of precursors moves toward the vegetal pole and continuously seeds mesodermal cells inside the embryo, which then reverse their movement in the direction of the animal pole [3-6]. Unlike mesoderm, endodermal cells internalize at once and must therefore adopt a different strategy to expand over the embryo [7, 8]. With live imaging of YFP-expressing zebrafish endodermal cells, we demonstrate that in contrast to mesoderm, internalized endodermal cells display a nonoriented/noncoordinated movement fit by a random walk that rapidly disperses them over the yolk surface. Transplantation experiments reveal that this behaviour is largely cell autonomous, induced by TGF-beta/Nodal, and dependent on the downstream effector Casanova. At midgastrulation, endodermal cells switch to a convergence movement. We demonstrate that this switch is triggered by environmental cues. These results uncover random walk as a novel Nodal-induced gastrulation movement and as an efficient strategy to transform a localized cell group into a layer expanded over the embryo.
Pézeron
Guillaume
G
INSERM U784, F-75005 Paris, France.
Mourrain
Philippe
P
Courty
Sébastien
S
Ghislain
Julien
J
Becker
Thomas S
TS
Rosa
Frédéric M
FM
David
Nicolas B
NB
D000818:Animals; D030801:Animals, Genetically Modified / Q000196:embryology / Q000502:physiology; D002465:Cell Movement / Q000502:physiology*; D004627:Embryonic Induction / Q000502:physiology; D004707:Endoderm / Q000166:cytology* / Q000502:physiology; D054262:Gastrulation / Q000502:physiology*; D006609:High Mobility Group Proteins / Q000378:metabolism; D055457:Nodal Protein; D055747:SOX Transcription Factors; D014157:Transcription Factors / Q000378:metabolism; D016212:Transforming Growth Factor beta / Q000378:metabolism; D015027:Zebrafish / Q000196:embryology* / Q000502:physiology; D029961:Zebrafish Proteins / Q000378:metabolism
D006609:High Mobility Group Proteins; D055457:Nodal Protein; D055747:SOX Transcription Factors; D014157:Transcription Factors; D016212:Transforming Growth Factor beta; D029961:Zebrafish Proteins; C438614:sox32 protein, zebrafish