BCR-ABL1 mediated miR-150 downregulation through MYC contributed to myeloid differentiation block and drug resistance in chronic myeloid leukemia
Klara Srutova,
Nikola Curik,
Pavel Burda,
Filipp Savvulidi,
Giovannino Silvestri,
Rossana Trotta,
Hana Klamova,
Pavla Pecherkova,
Zofie Sovova,
Jitka Koblihova,
Tomas Stopka,
Danilo Perrotti,
Katerina Machova Polakova
Affiliations
Klara Srutova
Institute of Hematology and Blood Transfusion, Prague, Czech Republic
Nikola Curik
Institute of Hematology and Blood Transfusion, Prague, Czech Republic;Institute of Pathological Physiology, First Medical Faculty, Charles University, Prague, Czech Republic
Pavel Burda
Institute of Hematology and Blood Transfusion, Prague, Czech Republic;Institute of Pathological Physiology, First Medical Faculty, Charles University, Prague, Czech Republic
Filipp Savvulidi
Institute of Pathological Physiology, First Medical Faculty, Charles University, Prague, Czech Republic
Giovannino Silvestri
Department of Medicine, Marlene and Stewart Greenebaum Comprehensive Cancer Center, University of Maryland Baltimore, MD, USA
Rossana Trotta
Department of Microbiology and Immunology, Marlene and Stewart Greenebaum Comprehensive Cancer Center, University of Maryland Baltimore, MD, USA
Hana Klamova
Institute of Hematology and Blood Transfusion, Prague, Czech Republic;Institute of Clinical and Experimental Hematology, First Medical Faculty, Charles University, Prague, Czech Republic
Pavla Pecherkova
Institute of Hematology and Blood Transfusion, Prague, Czech Republic
Zofie Sovova
Institute of Hematology and Blood Transfusion, Prague, Czech Republic
Jitka Koblihova
Institute of Hematology and Blood Transfusion, Prague, Czech Republic
Tomas Stopka
BIOCEV, First Medical Faculty, Charles University, Vestec, Czech Republic
Danilo Perrotti
Department of Medicine, Marlene and Stewart Greenebaum Comprehensive Cancer Center, University of Maryland Baltimore, MD, USA
Katerina Machova Polakova
Institute of Hematology and Blood Transfusion, Prague, Czech Republic;Institute of Clinical and Experimental Hematology, First Medical Faculty, Charles University, Prague, Czech Republic
The fusion oncoprotein BCR-ABL1 exhibits aberrant tyrosine kinase activity and it has been proposed that it deregulates signaling networks involving both transcription factors and non-coding microRNAs that result in chronic myeloid leukemia (CML). Previously, microRNA expression profiling showed deregulated expression of miR-150 and miR-155 in CML. In this study, we placed these findings into the broader context of the MYC/miR-150/MYB/miR-155/PU.1 oncogenic network. We propose that up-regulated MYC and miR-155 in CD34+ leukemic stem and progenitor cells, in concert with BCR-ABL1, impair the molecular mechanisms of myeloid differentiation associated with low miR-150 and PU.1 levels. We revealed that MYC directly occupied the −11.7 kb and −0.35 kb regulatory regions in the MIR150 gene. MYC occupancy was markedly increased through BCR-ABL1 activity, causing inhibition of MIR150 gene expression in CML CD34+ and CD34− cells. Furthermore, we found an association between reduced miR-150 levels in CML blast cells and their resistance to tyrosine kinase inhibitors (TKIs). Although TKIs successfully disrupted BCR-ABL1 kinase activity in proliferating CML cells, this treatment did not efficiently target quiescent leukemic stem cells. The study presents new evidence regarding the MYC/miR-150/MYB/miR-155/PU.1 leukemic network established by aberrant BCR-ABL1 activity. The key connecting nodes of this network may serve as potential druggable targets to overcome resistance of CML stem and progenitor cells.