SS18-SSX-Dependent YAP/TAZ Signaling in Synovial Sarcoma

Clin Cancer Res. 2019 Jun 15;25(12):3718-3731. doi: 10.1158/1078-0432.CCR-17-3553. Epub 2019 Feb 27.

Abstract

Purpose: Synovial sarcoma is a soft tissue malignancy characterized by a reciprocal t(X;18) translocation. The chimeric SS18-SSX fusion protein acts as a transcriptional dysregulator representing the major driver of the disease; however, the signaling pathways activated by SS18-SSX remain to be elucidated to define innovative therapeutic strategies.

Experimental design: Immunohistochemical evaluation of the Hippo signaling pathway effectors YAP/TAZ was performed in a large cohort of synovial sarcoma tissue specimens. SS18-SSX dependency and biological function of the YAP/TAZ Hippo signaling cascade were analyzed in five synovial sarcoma cell lines and a mesenchymal stem cell model in vitro. YAP/TAZ-TEAD-mediated transcriptional activity was modulated by RNAi-mediated knockdown and the small-molecule inhibitor verteporfin. The effects of verteporfin were finally tested in vivo in synovial sarcoma cell line-based avian chorioallantoic membrane and murine xenograft models as well as a patient-derived xenograft.

Results: A significant subset of synovial sarcoma showed nuclear positivity for YAP/TAZ and their transcriptional targets FOXM1 and PLK1. In synovial sarcoma cells, RNAi-mediated knockdown of SS18-SSX led to significant reduction of YAP/TAZ-TEAD transcriptional activity. Conversely, SS18-SSX overexpression in SCP-1 cells induced aberrant YAP/TAZ-dependent signals, mechanistically mediated by an IGF-II/IGF-IR signaling loop leading to dysregulation of the Hippo effectors LATS1 and MOB1. Modulation of YAP/TAZ-TEAD-mediated transcriptional activity by RNAi or verteporfin treatment resulted in significant growth inhibitory effects in vitro and in vivo.

Conclusions: Our preclinical study identifies an elementary role of SS18-SSX-driven YAP/TAZ signals, highlights the complex network of oncogenic signaling pathways in synovial sarcoma pathogenesis, and provides evidence for innovative therapeutic approaches.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acyltransferases
  • Adolescent
  • Adult
  • Aged
  • Animals
  • Cell Cycle Proteins / metabolism*
  • Cell Line, Tumor
  • Child
  • Cohort Studies
  • Female
  • Humans
  • Male
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Middle Aged
  • Oncogene Proteins, Fusion / metabolism*
  • Photosensitizing Agents / pharmacology
  • Sarcoma, Synovial / drug therapy
  • Sarcoma, Synovial / genetics
  • Sarcoma, Synovial / metabolism*
  • Signal Transduction
  • Transcription Factors / metabolism*
  • Verteporfin / pharmacology*
  • Xenograft Model Antitumor Assays
  • Young Adult

Substances

  • Cell Cycle Proteins
  • Oncogene Proteins, Fusion
  • Photosensitizing Agents
  • SS18-SSX1 fusion protein
  • Transcription Factors
  • YY1AP1 protein, human
  • Verteporfin
  • Acyltransferases
  • TAFAZZIN protein, human