A Novel Notch-YAP Circuit Drives Stemness and Tumorigenesis in Embryonal Rhabdomyosarcoma

Mol Cancer Res. 2017 Dec;15(12):1777-1791. doi: 10.1158/1541-7786.MCR-17-0004. Epub 2017 Sep 18.

Abstract

Rhabdomyosarcoma (RMS), a cancer characterized by skeletal muscle features, is the most common soft-tissue sarcoma of childhood. While low- and intermediate-risk groups have seen improved outcomes, high-risk patients still face a 5-year survival rate of <30%, a statistic that has not changed in over 40 years. Understanding the biologic underpinnings of RMS is critical. The developmental pathways of Notch and YAP have been identified as potent but independent oncogenic signals that support the embryonal variant of RMS (eRMS). Here, the cross-talk between these pathways and the impact on eRMS tumorigenesis is reported. Using human eRMS cells grown as three-dimensional (3D) rhabdospheres, which enriches in stem cells, it was found that Notch signaling transcriptionally upregulates YAP1 gene expression and YAP activity. Reciprocally, YAP transcriptionally upregulates the Notch ligand genes JAG1 and DLL1 and the core Notch transcription factor RBPJ This bidirectional circuit boosts expression of key stem cell genes, including SOX2, which is functionally required for eRMS spheres. Silencing this circuit for therapeutic purposes may be challenging, because the inhibition of one node (e.g., pharmacologic Notch blockade) can be rescued by upregulation of another (constitutive YAP expression). Instead, dual inhibition of Notch and YAP is necessary. Finally, supporting the existence of this circuit beyond a model system, nuclear Notch and YAP protein expression are correlated in human eRMS tumors, and YAP suppression in vivo decreases Notch signaling and SOX2 expression.Implications: This study identifies a novel oncogenic signaling circuit driving eRMS stemness and tumorigenesis, and provides evidence and rationale for combination therapies co-targeting Notch and YAP. Mol Cancer Res; 15(12); 1777-91. ©2017 AACR.

MeSH terms

  • Calcium-Binding Proteins
  • Carcinogenesis / genetics*
  • Cell Cycle Proteins
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / genetics
  • Intercellular Signaling Peptides and Proteins / genetics
  • Jagged-1 Protein / genetics
  • Membrane Proteins / genetics
  • Neoplastic Stem Cells / pathology
  • Nuclear Proteins / genetics*
  • Receptors, Notch / genetics*
  • Rhabdomyosarcoma, Embryonal / drug therapy
  • Rhabdomyosarcoma, Embryonal / genetics*
  • Rhabdomyosarcoma, Embryonal / pathology
  • SOXB1 Transcription Factors / genetics
  • Signal Transduction / genetics
  • Transcription Factors / genetics*

Substances

  • Calcium-Binding Proteins
  • Cell Cycle Proteins
  • DLK1 protein, human
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein
  • Intercellular Signaling Peptides and Proteins
  • JAG1 protein, human
  • Jagged-1 Protein
  • Membrane Proteins
  • Nuclear Proteins
  • RBPJ protein, human
  • Receptors, Notch
  • SOX2 protein, human
  • SOXB1 Transcription Factors
  • Transcription Factors
  • YY1AP1 protein, human