NHEJ-Mediated Repair of CRISPR-Cas9-Induced DNA Breaks Efficiently Corrects Mutations in HSPCs from Patients with Fanconi Anemia

Cell Stem Cell. 2019 Nov 7;25(5):607-621.e7. doi: 10.1016/j.stem.2019.08.016. Epub 2019 Sep 19.

Abstract

Non-homologous end-joining (NHEJ) is the preferred mechanism used by hematopoietic stem cells (HSCs) to repair double-stranded DNA breaks and is particularly increased in cells deficient in the Fanconi anemia (FA) pathway. Here, we show feasible correction of compromised functional phenotypes in hematopoietic cells from multiple FA complementation groups, including FA-A, FA-C, FA-D1, and FA-D2. NHEJ-mediated repair of targeted CRISPR-Cas9-induced DNA breaks generated compensatory insertions and deletions that restore the coding frame of the mutated gene. NHEJ-mediated editing efficacy was initially verified in FA lymphoblastic cell lines and then in primary FA patient-derived CD34+ cells, which showed marked proliferative advantage and phenotypic correction both in vitro and after transplantation. Importantly, and in contrast to homologous directed repair, NHEJ efficiently targeted primitive human HSCs, indicating that NHEJ editing approaches may constitute a sound alternative for editing self-renewing human HSCs and consequently for treatment of FA and other monogenic diseases affecting the hematopoietic system.

Keywords: CRISPR/Cas9 system; Fanconi anemia; gene editing; hematopoietic stem and progenitor cells; indels; non-homologous end-joining.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Antigens, CD34 / metabolism
  • CRISPR-Cas Systems / genetics*
  • Cell Line
  • Cell Proliferation / genetics
  • DNA Breaks, Double-Stranded
  • DNA End-Joining Repair / genetics*
  • Fanconi Anemia / genetics
  • Fanconi Anemia / metabolism
  • Fanconi Anemia / therapy*
  • Fanconi Anemia Complementation Group A Protein / genetics*
  • Fanconi Anemia Complementation Group A Protein / metabolism
  • Gene Editing / methods*
  • Genetic Therapy / methods*
  • Hematopoietic Stem Cell Transplantation* / adverse effects
  • Hematopoietic Stem Cell Transplantation* / methods
  • Hematopoietic Stem Cells / cytology
  • Hematopoietic Stem Cells / metabolism
  • High-Throughput Nucleotide Sequencing
  • Humans
  • INDEL Mutation
  • Mice
  • Mice, Inbred NOD
  • Mice, Nude

Substances

  • Antigens, CD34
  • FANCA protein, human
  • Fanconi Anemia Complementation Group A Protein