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Bmp inhibition is necessary for post-gastrulation patterning and morphogenesis of the zebrafish tailbud.

ABSTRACT: Intricate interactions between the Wnt and Bmp signaling pathways pattern the gastrulating vertebrate embryo using a network of secreted protein ligands and inhibitors. While many of these proteins are expressed post-gastrula, their later roles have typically remained unclear, obscured by the effects of early perturbation. We find that Bmp signaling continues during somitogenesis in zebrafish embryos, with high activity in a small region of the mesodermal progenitor zone at the posterior end of the embryo. To test the hypothesis that Bmp inhibitors expressed just anterior to the tailbud are important to restrain Bmp signaling we produced a new zebrafish transgenic line, allowing temporal cell-autonomous activation of Bmp signaling and thereby bypassing the effects of the Bmp inhibitors. Ectopic activation of Bmp signaling during somitogenesis results in severe defects in the tailbud, including altered morphogenesis and gene expression. We show that these defects are due to non-autonomous effects on the tailbud, and present evidence that the tailbud defects are caused by alterations in Wnt signaling. We present a model in which the posteriorly expressed Bmp inhibitors function during somitogenesis to constrain Bmp signaling in the tailbud in order to allow normal expression of Wnt inhibitors in the presomitic mesoderm, which in turn constrain the levels of canonical and non-canonical Wnt signaling in the tailbud.

SUBMITTER: Row RH

PROVIDER: S-EPMC2670352 | biostudies-literature | 2009 May

REPOSITORIES: biostudies-literature

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Bmp inhibition is necessary for post-gastrulation patterning and morphogenesis of the zebrafish tailbud.

Row Richard H RH Kimelman David D

Developmental biology 20090221 1

Intricate interactions between the Wnt and Bmp signaling pathways pattern the gastrulating vertebrate embryo using a network of secreted protein ligands and inhibitors. While many of these proteins are expressed post-gastrula, their later roles have typically remained unclear, obscured by the effects of early perturbation. We find that Bmp signaling continues during somitogenesis in zebrafish embryos, with high activity in a small region of the mesodermal progenitor zone at the posterior end of ...[more]

PMID: 19236859

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Project description:The tailbud is a population of stem cells in the posterior embryonic tail. During zebrafish development, these stem cells give rise to the main structures of the embryo's posterior body, including the tail somites. Progenitor cells reside in the tailbud for variable amounts of time before they exit and begin to differentiate. There must be a careful balance between cells that leave the tailbud and cells that are held back in order to give rise to later somites. However, this meticulous process is not well understood. A gene that has shed some light on this area is the t-box transcription factor spadetail (spt). When spt is mutated, embryos develop an enlarged tailbud and are only able to form roughly half of their somites. This phenotype is due to the fact that some of the somitic precursors are not able to leave the tailbud or differentiate. Another factor involved in tail morphogenesis is the Bone Morphogenetic Protein (BMP) pathway. BMPs are important for many processes during early development, including cell migration. Chordino (chd) is a secreted protein that inhibits BMP signaling. BMPs are upregulated in chd mutants, however, these mutants are able to form organized somites. In embryos where chd and spt are mutated, somites are completely absent. These double mutants also develop a large tailbud due to the accumulation of progenitor cells that are never able to leave or differentiate. To study the dynamics of cells in the tailbud and their role in somite formation, we have analyzed the genetic factors and pathway interactions involved, conducted transplant experiments to look at behavior of mutant cells in different genetic backgrounds, and used time lapse microscopy to characterize cell movements and behavior in wild type and mutant tailbuds. These data suggest that spt expression and BMP inhibition are both required for somitic precursors to exit the tailbud. They also elucidate that chd;spt tailbud mesodermal progenitor cells (MPC) behave autonomously and their dynamics within the tailbud are drastically different than WT MPCs.

Dataset Information

Bmp inhibition is necessary for post-gastrulation patterning and morphogenesis of the zebrafish tailbud.

Publications

Bmp inhibition is necessary for post-gastrulation patterning and morphogenesis of the zebrafish tailbud.

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