A Huluwa phosphorylation switch regulates embryonic axis induction

Nat Commun. 2024 Nov 19;15(1):10028. doi: 10.1038/s41467-024-54450-4.

Abstract

Embryonic axis formation is essential for patterning and morphogenesis in vertebrates and is tightly regulated by the dorsal organizer. Previously, we demonstrated that maternally derived Huluwa (Hwa) acts as a dorsal determinant, dictating axis formation by activating β-catenin signaling in zebrafish and Xenopus. However, the mechanism of activation and fine regulation of the Hwa protein remains unclear. Through candidate screening we identified a mutation at Ser168 in the PPNSP motif of Hwa that dramatically abolishes its axis-inducing activity. Mechanistically, mutating the Ser168 residue reduced its binding affinity to Tankyrase 1/2 and the degradation of the Axin protein, weakening β-catenin signaling activation. We confirmed that Ser168 is phosphorylated and that phosphorylation increases Hwa activity in β-catenin signaling and axis induction. Several kinases including Cdk16, Cdk2, and GSK3β, were found to enhance Ser168 phosphorylation in vitro and in vivo. Both dominant-negative Cdk16 expression and pHwa (Ser168) antibody treatment reduce Hwa function. Lastly, a knock-in allele mutating Ser168 to alanine resulted in embryos lacking body axes, demonstrating that Ser168 is essential to axis formation. In summary, Ser168 acts as a phosphorylation switch in Hwa/β-catenin signaling for embryonic axis induction, regulated by multiple kinases.

MeSH terms

  • Animals
  • Axin Protein / genetics
  • Axin Protein / metabolism
  • Body Patterning / genetics
  • Cyclin-Dependent Kinases / genetics
  • Cyclin-Dependent Kinases / metabolism
  • Embryo, Nonmammalian / metabolism
  • Gene Expression Regulation, Developmental
  • Mutation
  • Phosphorylation
  • Signal Transduction
  • Tankyrases / genetics
  • Tankyrases / metabolism
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism
  • Zebrafish Proteins* / genetics
  • Zebrafish Proteins* / metabolism
  • Zebrafish* / embryology
  • Zebrafish* / genetics
  • Zebrafish* / metabolism
  • beta Catenin* / genetics
  • beta Catenin* / metabolism

Substances

  • Zebrafish Proteins
  • beta Catenin
  • Xenopus Proteins
  • Axin Protein
  • Cyclin-Dependent Kinases
  • Tankyrases