Protogenin facilitates trunk-to-tail HOX code transition via modulating GDF11/SMAD2 signaling in mammalian embryos

Commun Biol. 2024 Dec 19;7(1):1669. doi: 10.1038/s42003-024-07342-8.

Abstract

During embryogenesis, vertebral axial patterning is intricately regulated by multiple signaling networks. This study elucidates the role of protogenin (Prtg), an immunoglobulin superfamily member, in vertebral patterning control. Prtg knockout (Prtg-/-) mice manifest anterior homeotic transformations in their vertebral columns and significant alterations in homeobox (Hox) gene expression. Transcriptomic profiling of Prtg-/- mouse embryos highlights Prtg-regulated genes involved in axial development, particularly within the transforming growth factor beta (TGFβ) signaling pathway. Reduced TGFβ signaling in Prtg-/- mouse embryos is evidenced by decreased phosphorylated Smad2 (pSmad2) levels and its downstream target genes in the developing tail. We further show that Prtg interacts with growth differentiation factor 11 (GDF11) to enhance GDF11/pSmad2 signaling activity. Using human-induced pluripotent stem cell-derived presomitic mesoderm-like (hiPSC-PSM) cells, we demonstrate delayed posterior HOX gene expression upon PRTG knockout, which is rescued by GDF11 supplementation. These findings provide compelling evidence that PRTG regulates HOX genes through the GDF11/SMAD2 signaling pathway.

MeSH terms

  • Animals
  • Body Patterning / genetics
  • Bone Morphogenetic Proteins* / genetics
  • Bone Morphogenetic Proteins* / metabolism
  • Embryo, Mammalian / metabolism
  • Embryonic Development / genetics
  • Epidermal Growth Factor
  • Gene Expression Regulation, Developmental*
  • Growth Differentiation Factors* / genetics
  • Growth Differentiation Factors* / metabolism
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Membrane Glycoproteins
  • Mice
  • Mice, Knockout*
  • Neoplasm Proteins
  • Signal Transduction*
  • Smad2 Protein* / genetics
  • Smad2 Protein* / metabolism

Substances

  • Smad2 Protein
  • Bone Morphogenetic Proteins
  • Gdf11 protein, mouse
  • Growth Differentiation Factors
  • Smad2 protein, mouse
  • Homeodomain Proteins
  • Tdgf1 protein, mouse
  • Epidermal Growth Factor
  • Membrane Glycoproteins
  • Neoplasm Proteins