Aberrant regulation of proteomic networks is implicated in cancer development and progression and the understanding of these processes opens new opportunities for therapeutic interventions. In this study, we performed phosphoproteomic analysis and ex-vivo drug testing on a cohort of ten metastatic colorectal cancer (mCRC) tissues and matched patient-derived organoids (PDO) to identify new potential druggable biomarkers. Besides the upregulation of well-known tumor-sustaining pathways, such as MYC and mTORC1 signaling, our data highlighted increased casein kinase II (CKII) activity, an important regulator of cell cycle progression.
Ex-vivo drug treatment on mCRC PDOs demonstrated that silmitasertib-mediated CKII inhibition exerted anti-tumoral activity and induced PARP cleavage and DNA damage. On the other hand, no cytotoxic effects were noticed on PDOs derived from normal colon tissues. Our phosphoproteomics dataset also revealed that the heterogeneous sensitivity of PDOs to clinically relevant concentrations of silmitasertib was correlated with increased EGFR and mTORC1 signaling activities. Accordingly, molecular analysis confirmed that failure to reduce CKII activity and PDO viability correlated with sustained ERK1/2 and S6 signaling, suggesting potential resistance mechanisms.
Complementing CKII blockade with targeted MAPK or mTORC1 signaling inhibition, we observed additive/synergistic interactions that resulted in an enhanced antitumor activity. In particular, the combination between silmitasertib and trametinib, a selective inhibitor of MEK1/2, induced a simultaneous reduction of mTORC1, MAPK and CKII signaling compared to either drug alone. KRAS-mutant PDOs showed the greatest benefit from the combinatorial treatment. Importantly, no major cytotoxic effects were observed in normal colon PDOs. Additionally, the dual therapy significantly reduced active β-catenin levels and decreased the pool of CD44/CD133 double-positive cancer stem cells, which are critical in therapy resistance.
Taken together, our findings highlight the potential of phosphoproteomic analysis to strategically inform and advance cancer therapy and propose a promising new therapeutic opportunity for mCRC patients, warranting further preclinical and clinical investigations.