The Snail repressor is required for PMC ingression in the sea urchin embryo.
In metazoans, the epithelial-mesenchymal transition (EMT) is a crucial process for placing the mesoderm beneath the ectoderm. Primary mesenchyme cells (PMCs) at the vegetal pole of the sea urchin embryo ingress into the floor of the blastocoele from the blastula epithelium and later become the skeletogenic mesenchyme. This ingression movement is a classic EMT during which the PMCs penetrate the basal lamina, lose adherens junctions and migrate into the blastocoele. Later, secondary mesenchyme cells (SMCs) also enter the blastocoele via an EMT, but they accompany the invagination of the archenteron initially, in much the same way vertebrate mesenchyme enters the embryo along with endoderm. Here we identify a sea urchin ortholog of the Snail transcription factor, and focus on its roles regulating EMT during PMC ingression. Functional knockdown analyses of Snail in whole embryos and chimeras demonstrate that Snail is required in micromeres for PMC ingression. Snail represses the transcription of cadherin, a repression that appears evolutionarily conserved throughout the animal kingdom. Furthermore, Snail expression is required for endocytosis of cadherin, a cellular activity that accompanies PMC ingression. Perturbation studies position Snail in the sea urchin micromere-PMC gene regulatory network (GRN), downstream of Pmar1 and Alx1, and upstream of several PMC-expressed proteins. Taken together, our findings indicate that Snail plays an essential role in PMCs to control the EMT process, in part through its repression of cadherin expression during PMC ingression, and in part through its role in the endocytosis that helps convert an epithelial cell to a mesenchyme cell.
Wu
Shu-Yu
SY
DCMB group, Biology Department, Duke University, Durham, NC 27708, USA.
McClay
David R
DR
D000595:Amino Acid Sequence; D000818:Animals; D015820:Cadherins / Q000235:genetics / Q000378:metabolism; D015536:Down-Regulation; D004625:Embryo, Nonmammalian / Q000737:chemistry / Q000378:metabolism; D047108:Embryonic Development / Q000235:genetics*; D004705:Endocytosis / Q000235:genetics; D005775:Gastrula / Q000737:chemistry / Q000166:cytology / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental; D047331:Lytechinus / Q000166:cytology / Q000196:embryology* / Q000235:genetics; D008648:Mesoderm / Q000166:cytology / Q000378:metabolism / Q000502:physiology*; D008969:Molecular Sequence Data; D010802:Phylogeny; D012333:RNA, Messenger / Q000032:analysis / Q000378:metabolism; D012097:Repressor Proteins / Q000235:genetics / Q000502:physiology*; D000071250:Snail Family Transcription Factors; D014157:Transcription Factors / Q000145:classification / Q000235:genetics / Q000502:physiology*
D015820:Cadherins; D012333:RNA, Messenger; D012097:Repressor Proteins; D000071250:Snail Family Transcription Factors; D014157:Transcription Factors