Effects of pharmacological and genetic disruption of CXCR4 chemokine receptor function in B-cell acute lymphoblastic leukaemia

Br J Haematol. 2016 Aug;174(3):425-36. doi: 10.1111/bjh.14075. Epub 2016 Apr 12.

Abstract

B cell acute lymphoblastic leukaemia (B-ALL) cells express high levels of CXCR4 chemokine receptors for homing and retention within the marrow microenvironment. Bone marrow stromal cells (BMSC) secrete CXCL12, the ligand for CXCR4, and protect B-ALL cells from cytotoxic drugs. Therefore, the therapeutic use of CXCR4 antagonists has been proposed to disrupt cross talk between B-ALL cells and the protective stroma. Because CXCR4 antagonists can have activating agonistic function, we compared the genetic and pharmacological deletion of CXCR4 in B-ALL cells, using CRISPR-Cas9 gene editing and CXCR4 antagonists that are in clinical use (plerixafor, BKT140). Both genetic and pharmacological CXCR4 inhibition significantly reduced B-ALL cell migration to CXCL12 gradients and beneath BMSC, and restored drug sensitivity to dexamethasone, vincristine and cyclophosphamide. NOD/SCID/IL-2rγnull mice injected with CXCR4 gene-deleted B-ALL cells had significant delay in disease progression and superior survival when compared to control mice injected with CXCR4 wild-type B-ALL cells. These findings indicate that anti-leukaemia activity of CXCR4 antagonists is primarily due to CXCR4 inhibition, rather than agonistic activity, and corroborate that CXCR4 is an important target to overcome stroma-mediated drug resistance in B-ALL.

Keywords: B-acute lymphoblastic leukaemia; CRISPR-Cas9; CXCL12; CXCR4; bone marrow microenvironment.

MeSH terms

  • Animals
  • Cell Line
  • Cell Movement / drug effects
  • Chemokine CXCL12 / metabolism
  • Drug Resistance / drug effects
  • Gene Editing
  • Humans
  • Leukemia, B-Cell / metabolism
  • Leukemia, B-Cell / pathology
  • Mice
  • Mice, Inbred Strains
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / metabolism
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology*
  • Receptor Cross-Talk / drug effects
  • Receptors, CXCR4 / antagonists & inhibitors*
  • Receptors, CXCR4 / genetics
  • Stromal Cells / metabolism
  • Tumor Cells, Cultured

Substances

  • CXCL12 protein, human
  • CXCR4 protein, human
  • Chemokine CXCL12
  • Receptors, CXCR4