BACKGROUND: High-risk neuroblastomas (NBL) display substantial clinical and molecular heterogeneity. Despite progress understanding NBL genetics, little progress has been made in procuring personalized treatments. Here we sought to determine effector molecular mechanisms downstream of genetic alterations sustaining different tumor subtypes1.
METHODS: We first defined molecular subtypes from the TARGET and NRC Consortium gene expression datasets by consensus clustering and identified specific master regulators (MRs) of transcriptional programs using VIPER/ssMARINA algorithm2 available as a bioconductor R package. We performed in vitro and in vivo validation of MRs by RNAi screening followed by experimental and computational assays to elucidate the interdependencies between top MRs and their biological role. Finally, we studied tissue microarrays (TMA) and applied multivariate Cox regression to understand the clinical relevance of our findings.
RESULTS: We identified MRs from three distinct molecular subtypes of high-risk NBL, conserved across cohorts. siRNA and shRNA screens identified a TEAD4-MYCN positive feed forward loop as a key NBL state maintenance of MYCN dysregulated tumors. RNA-seq upon MYCN and TEAD4 knockdown showed that MYCN controls cell growth and represses differentiation and that TEAD4 is essential for G1 to S transition and DNA repair. Specifically, TEAD4 transactivates AURKA, CDKs, Cyclin D, E2Fs, DNA replication factors, checkpoint kinases and ubiquitin ligases. Consistently, TEAD4 inhibition induced critical loss of NBL cell viability, both in vitro and in vivo. TMA staining shows increased TEAD4 protein levels in high risk tumors (P = 0.021); expression/activity is an independent predictor of survival in multivariable analysis (P = 0.0084 corrected for age, stage and MYCN status).
CONCLUSION: TEAD4 plays a critical role in maintaining the high proliferative state of undifferentiated NBLs with sustained growth promoted by MYCN dysregulation. The critical effect of disrupting TEAD4-MYCN module on cell viability and its clinical relevance brings forward TEAD4 as an excellent candidate target for therapeutic intervention.