CCDC6-RET fusion protein regulates Ras/MAPK signaling through the fusion- GRB2-SHC1 signal niche

Proc Natl Acad Sci U S A. 2024 Jun 4;121(23):e2322359121. doi: 10.1073/pnas.2322359121. Epub 2024 May 28.

Abstract

Rearranged during transfection (RET) rearrangement oncoprotein-mediated Ras/MAPK signaling cascade is constitutively activated in cancers. Here, we demonstrate a unique signal niche. The niche is a ternary complex based on the chimeric RET liquid-liquid phase separation. The complex comprises the rearranged kinase (RET fusion); the adaptor (GRB2), and the effector (SHC1). Together, they orchestrate the Ras/MAPK signal cascade, which is dependent on tyrosine kinase. CCDC6-RET fusion undergoes LLPS requiring its kinase domain and its fusion partner. The CCDC6-RET fusion LLPS promotes the autophosphorylation of RET fusion, with enhanced kinase activity, which is necessary for the formation of the signaling niche. Within the signal niche, the interactions among the constituent components are reinforced, and the signal transduction efficiency is amplified. The specific RET fusion-related signal niche elucidates the mechanism of the constitutive activation of the Ras/MAPK signaling pathway. Beyond just focusing on RET fusion itself, exploration of the ternary complex potentially unveils a promising avenue for devising therapeutic strategies aimed at treating RET fusion-driven diseases.

Keywords: CCDC6-RET; fusion protein; kinase; liquid–liquid phase separation; signal niche.

MeSH terms

  • GRB2 Adaptor Protein* / genetics
  • GRB2 Adaptor Protein* / metabolism
  • HEK293 Cells
  • Humans
  • MAP Kinase Signaling System*
  • Oncogene Proteins, Fusion* / genetics
  • Oncogene Proteins, Fusion* / metabolism
  • Phosphorylation
  • Proto-Oncogene Proteins c-ret* / genetics
  • Proto-Oncogene Proteins c-ret* / metabolism
  • Signal Transduction
  • Src Homology 2 Domain-Containing, Transforming Protein 1* / genetics
  • Src Homology 2 Domain-Containing, Transforming Protein 1* / metabolism
  • ras Proteins* / genetics
  • ras Proteins* / metabolism

Substances

  • GRB2 Adaptor Protein
  • GRB2 protein, human
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Proteins c-ret
  • ras Proteins
  • RET protein, human
  • SHC1 protein, human
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • CCDC6 protein, human