ASXL1 mutation correction by CRISPR/Cas9 restores gene function in leukemia cells and increases survival in mouse xenografts

Oncotarget. 2015 Dec 29;6(42):44061-71. doi: 10.18632/oncotarget.6392.

Abstract

Recurrent somatic mutations of the epigenetic modifier and tumor suppressor ASXL1 are common in myeloid malignancies, including chronic myeloid leukemia (CML), and are associated with poor clinical outcome. CRISPR/Cas9 has recently emerged as a powerful and versatile genome editing tool for genome engineering in various species. We have used the CRISPR/Cas9 system to correct the ASXL1 homozygous nonsense mutation present in the CML cell line KBM5, which lacks ASXL1 protein expression. CRISPR/Cas9-mediated ASXL1 homozygous correction resulted in protein re-expression with restored normal function, including down-regulation of Polycomb repressive complex 2 target genes. Significantly reduced cell growth and increased myeloid differentiation were observed in ASXL1 mutation-corrected cells, providing new insights into the role of ASXL1 in human myeloid cell differentiation. Mice xenografted with mutation-corrected KBM5 cells showed significantly longer survival than uncorrected xenografts. These results show that the sole correction of a driver mutation in leukemia cells increases survival in vivo in mice. This study provides proof-of-concept for driver gene mutation correction via CRISPR/Cas9 technology in human leukemia cells and presents a strategy to illuminate the impact of oncogenic mutations on cellular function and survival.

Keywords: ASXL1; CRISPR; chronic myeloid leukemia; mutation correction; tumor suppressor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • CRISPR-Associated Proteins / genetics*
  • CRISPR-Associated Proteins / metabolism
  • CRISPR-Cas Systems*
  • Cell Differentiation
  • Cell Line, Tumor
  • Cell Proliferation
  • Clustered Regularly Interspaced Short Palindromic Repeats*
  • Codon, Nonsense*
  • Gene Expression Regulation, Leukemic
  • Genetic Predisposition to Disease
  • Heterografts
  • Homozygote
  • Humans
  • Interleukin Receptor Common gamma Subunit / deficiency
  • Interleukin Receptor Common gamma Subunit / genetics
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / genetics*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology
  • Mice, Inbred NOD
  • Mice, Knockout
  • Mice, SCID
  • Molecular Sequence Data
  • Neoplasm Transplantation
  • Phenotype
  • Polycomb Repressive Complex 2 / genetics
  • Polycomb Repressive Complex 2 / metabolism
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism
  • Time Factors
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism
  • Ubiquitin Thiolesterase / genetics
  • Ubiquitin Thiolesterase / metabolism

Substances

  • ASXL1 protein, human
  • BAP1 protein, human
  • CRISPR-Associated Proteins
  • Codon, Nonsense
  • Il2rg protein, mouse
  • Interleukin Receptor Common gamma Subunit
  • Repressor Proteins
  • Tumor Suppressor Proteins
  • Polycomb Repressive Complex 2
  • Ubiquitin Thiolesterase