Activating mutations of the ALK receptor occur in 8% of neuroblastoma tumors at diagnosis. The RET gene has been previously identified as a target of activated ALK at the mRNA level in both human neuroblastoma cell lines and primary tumors as well as in murine tumors driven by mutated Alk and MYCN. We also reported that the Ret inhibitor vandetanib inhibited tumor growth in these murine neuroblastoma models.
In the present work, we sought to: (1) determine the mechanism of RET upregulation by activated ALK; (2) demonstrate the contribution of RET to ALK mutated dependent neuroblastoma oncogenesis by a genetic approach; (3) evaluate the therapeutic potential of a combination of vandetanib with the ALK inhibitor crizotinib.
Transcriptomic data of murine MYCN/Alkmut tumors first identified Etv5 as a candidate transcription factor regulating Ret expression. We then showed that ETV5 is regulated both at the protein and mRNA levels upon ALK modulation in neuroblastoma cell lines and that ETV5 regulation precedes RET modulation. We further demonstrate that ETV5 and RET are regulated by ALK through the MEK/ERK pathway and show that RNA interference-mediated inhibition of ETV5 decreases RET expression. Then, to further determine the contribution of RET to ALK mutated dependent neuroblastoma oncogenesis in vivo, we bred knock-in RetM919T mice with TH-MYCN mice. We document an oncogenic cooperation between activated Ret and MYCN overexpression in neuroblastoma formation and show that MYCN/RetM919T tumors present with histological features and expression profiles close to MYCN/Alkmut tumors. We finally demonstrate that the combination of vandetanib and crizotinib more efficiently reduces tumor growth than each single agent in our murine neuroblastoma models.
Altogether, these results define the ERK-ETV5-RET pathway as a critical axis driving neuroblastoma oncogenesis downstream of activated ALK and identify the crizotinib/vandetanib combination as an interesting approach for patients presenting with neuroblastoma harbouring ALK activation.