Combined HAT/EZH2 modulation leads to cancer-selective cell death

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Petraglia Francesca, Singh Abhishek A., Carafa Vincenzo, Nebbioso Angela, Conte Mariarosaria, Scisciola Lucia, Valente Sergio, Baldi Alfonso, Mandoli Amit, Petrizzi Valeria Belsito, Ingenito Concetta, De Falco Sandro, Cicatiello Valeria, Apicella Ivana, Janssen-Megens Eva M., Kim Bowon, Yi Guoqiang, Logie Colin, Heath Simon, Ruvo Menotti, Wierenga Albertus T. J., Flicek Paul, Yaspo Marie Laure, Della Valle Veronique, Bernard Olivier, Tomassi Stefano, Novellino Ettore, Feoli Alessandra, Sbardella Gianluca, Gut Ivo, Vellenga Edo, Stunnenberg Hendrik G., Mai Antonello, Martens Joost H. A., Altucci Lucia
ISSN: 1949-2553

Epigenetic alterations have been associated with both pathogenesis and progression of cancer. By screening of library compounds, we identified a novel hybrid epi-drug MC2884, a HAT/EZH2 inhibitor, able to induce bona fide cancer-selective cell death in both solid and hematological cancers in vitro, ex vivo and in vivo xenograft models. Anticancer action was due to an epigenome modulation by H3K27me3, H3K27ac, H3K9/14ac decrease, and to caspase-dependent apoptosis induction. MC2884 triggered mitochondrial pathway apoptosis by up-regulation of cleaved-BID, and strong down-regulation of BCL2. Even aggressive models of cancer, such as p53-/-or TET2-/-cells, responded to MC2884, suggesting MC2884 therapeutic potential also for the therapy of TP53 or TET2-deficient human cancers. MC2884 induced massive apoptosis in ex vivo human primary leukemia blasts with poor prognosis in vivo, by targeting BCL2 expression. MC2884-treatment reduced acetylation of the BCL2 promoter at higher level than combined p300 and EZH2 inhibition. This suggests a key role for BCL-2 reduction in potentiating responsiveness, also in combination therapy with BCL2 inhibitors. Finally, we identified both the mechanism of MC2884 action as well as a potential therapeutic scheme of its use. Altogether, this provides proof of concept for the use of epi-drugs coupled with epigenome analyses to 'personalize' precision medicine.

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