BETP degradation simultaneously targets acute myelogenous leukemia stem cells and the microenvironment

J Clin Invest. 2019 Feb 21;129(5):1878-1894. doi: 10.1172/JCI120654. Print 2019 May 1.

Abstract

Anti-leukemic effect of BET/BRD4 (BETP) protein inhibition has been largely attributed to transcriptional downregulation of cellular anabolic/anti-apoptotic processes but its effect on bone marrow microenvironment, a sanctuary favoring persistence of leukemia stem/progenitor cells, is unexplored. Sustained degradation of BETP with small-molecule BET proteolysis-targeting chimera (PROTAC), ARV-825, resulted in marked downregulation of surface CXCR4 and CD44, key proteins in leukemia-microenvironment interaction, in AML cells. Abrogation of surface CXCR4 expression impaired SDF-1α directed migration and was mediated through transcriptional down-regulation of PIM1 kinase that in turn phosphorylates CXCR4 and facilitates its surface localization. Down-regulation of CD44/CD44v8-10 impaired cystine uptake, lowered intracellular reduced glutathione and increased oxidative stress. More importantly, BETP degradation markedly decreased CD34+CD38-CD90-CD45RA+ leukemic stem cell population and alone or in combination with Cytarabine, prolonged survival in mouse model of human leukemia including AML-PDX. Gene expression profiling and single cell proteomics confirmed down regulation of the gene signatures associated with 'stemness' in AML and Wnt/β-catenin, Myc pathways. Hence, BETP degradation by ARV-825 simultaneously targets cell intrinsic signaling, stromal interactions and metabolism in AML.

Keywords: Cancer; Cell Biology; Epigenetics; Oncology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP-ribosyl Cyclase 1 / metabolism
  • Animals
  • Antigens, CD34 / metabolism
  • Azepines / pharmacology
  • Bone Marrow / metabolism
  • Cell Cycle Proteins / antagonists & inhibitors*
  • Cell Line, Tumor
  • Cell Movement
  • Chemokine CXCL12 / metabolism
  • Cysteine / chemistry
  • Gene Expression Profiling
  • Glutathione / chemistry
  • HL-60 Cells
  • Humans
  • Hyaluronan Receptors / metabolism
  • Leukemia, Myeloid, Acute / metabolism*
  • Leukocyte Common Antigens / metabolism
  • Male
  • Membrane Glycoproteins / metabolism
  • Mice
  • Neoplasm Transplantation
  • Neoplastic Stem Cells / metabolism*
  • Nuclear Proteins / metabolism*
  • Oxidative Stress
  • Phosphorylation
  • Receptors, CXCR4 / metabolism
  • THP-1 Cells
  • Thalidomide / analogs & derivatives
  • Thalidomide / pharmacology
  • Thy-1 Antigens / metabolism
  • Transcription Factors / antagonists & inhibitors*
  • U937 Cells

Substances

  • ARV-825
  • Antigens, CD34
  • Azepines
  • BRD4 protein, human
  • CD44 protein, human
  • CXCR4 protein, human
  • Cell Cycle Proteins
  • Chemokine CXCL12
  • Hyaluronan Receptors
  • Membrane Glycoproteins
  • Nuclear Proteins
  • Receptors, CXCR4
  • Thy-1 Antigens
  • Transcription Factors
  • Thalidomide
  • Leukocyte Common Antigens
  • CD38 protein, human
  • ADP-ribosyl Cyclase 1
  • Glutathione
  • Cysteine