Tbx2 mediates dorsal patterning and germ layer suppression through inhibition of BMP/GDF and Activin/Nodal signaling

BMC Mol Cell Biol. 2020 May 28;21(1):39. doi: 10.1186/s12860-020-00282-1.

Abstract

Background: Members of the T-box family of DNA-binding proteins play a prominent role in the differentiation of the three primary germ layers. VegT, Brachyury, and Eomesodermin function as transcriptional activators and, in addition to directly activating the transcription of endoderm- and mesoderm-specific genes, serve as regulators of growth factor signaling during induction of these germ layers. In contrast, the T-box gene, tbx2, is expressed in the embryonic ectoderm, where Tbx2 functions as a transcriptional repressor and inhibits mesendodermal differentiation by the TGFβ ligand Activin. Tbx2 misexpression also promotes dorsal ectodermal fate via inhibition of the BMP branch of the TGFβ signaling network.

Results: Here, we report a physical association between Tbx2 and both Smad1 and Smad2, mediators of BMP and Activin/Nodal signaling, respectively. We perform structure/function analysis of Tbx2 to elucidate the roles of both Tbx2-Smad interaction and Tbx2 DNA-binding in germ layer suppression.

Conclusion: Our studies demonstrate that Tbx2 associates with intracellular mediators of the Activin/Nodal and BMP/GDF pathways. We identify a novel repressor domain within Tbx2, and have determined that Tbx2 DNA-binding activity is required for repression of TGFβ signaling. Finally, our data also point to overlapping yet distinct mechanisms for Tbx2-mediated repression of Activin/Nodal and BMP/GDF signaling.

Keywords: Development; Ectoderm; Gastrulation; Gene regulation; Smads; Tbx2; Xenopus.

MeSH terms

  • Activins / pharmacology*
  • Animals
  • Body Patterning
  • Bone Morphogenetic Proteins / metabolism
  • Ectoderm / metabolism*
  • Gene Expression Regulation, Developmental / genetics
  • Germ Layers / metabolism*
  • Growth Differentiation Factors / metabolism
  • Phosphorylation
  • Protein Domains / genetics
  • Signal Transduction / genetics
  • Smad1 Protein / genetics
  • Smad1 Protein / metabolism*
  • Smad2 Protein / genetics
  • Smad2 Protein / metabolism*
  • T-Box Domain Proteins / chemistry
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism*
  • Transforming Growth Factor beta / metabolism
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism*
  • Xenopus laevis

Substances

  • Bone Morphogenetic Proteins
  • Growth Differentiation Factors
  • NODAL protein, Xenopus
  • SMAD1 protein, Xenopus
  • Smad1 Protein
  • Smad2 Protein
  • Smad2 protein, Xenopus
  • T-Box Domain Protein 2
  • T-Box Domain Proteins
  • Transforming Growth Factor beta
  • Xenopus Proteins
  • Activins