NSD3 protein methylation and stabilization transforms human ES cells into variant state

Life Sci Alliance. 2024 Dec 31;8(3):e202402871. doi: 10.26508/lsa.202402871. Print 2025 Mar.

Abstract

Cultured human embryonic stem cells (hESCs) can develop genetic anomalies that increase their susceptibility to transformation. In this study, we characterized a variant hESC (vhESC) line and investigated the molecular mechanisms leading to the drift towards a transformed state. Our findings revealed that vhESCs up-regulate EMT-specific markers, accelerate wound healing, exhibit compromised lineage differentiation, and retain pluripotency gene expression in teratomas. Furthermore, we discovered an altered epigenomic landscape and overexpression of the lysine methyltransferases EHMT1, EHMT2, and NSD group of proteins in vhESCs. Remarkably, depleting NSD3 oncogene reversed the molecular and phenotypic changes in vhESCs. We identified a detailed mechanism where EHMT2 interacts and methylates NSD3 at lysine 477, stabilizing its protein levels in vhESCs. In addition, we showed that NSD3 levels are regulated by protein degradation in hESCs, and its stabilization leads to the emergence of the variant state. Overall, our study identify that misregulation of NSD3 in pluripotent stem cells, through methylation-mediated abrogation of its protein degradation, drives hESCs towards oncogenic transformation.

MeSH terms

  • Cell Differentiation* / genetics
  • Cell Line
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / metabolism
  • Epigenesis, Genetic
  • Epithelial-Mesenchymal Transition / genetics
  • Histone-Lysine N-Methyltransferase* / genetics
  • Histone-Lysine N-Methyltransferase* / metabolism
  • Human Embryonic Stem Cells* / cytology
  • Human Embryonic Stem Cells* / metabolism
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Methylation
  • Nuclear Proteins
  • Pluripotent Stem Cells / cytology
  • Pluripotent Stem Cells / metabolism
  • Protein Stability
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism

Substances

  • Histone-Lysine N-Methyltransferase
  • NSD3 protein, human
  • Intracellular Signaling Peptides and Proteins
  • Repressor Proteins
  • Nuclear Proteins