Concurrent transposon engineering and CRISPR/Cas9 genome editing of primary CLL-1 chimeric antigen receptor-natural killer cells

Cytotherapy. 2022 Nov;24(11):1087-1094. doi: 10.1016/j.jcyt.2022.07.008. Epub 2022 Aug 29.

Abstract

Background: Natural killer (NK) cell genome editing promises to enhance the innate and alloreactive anti-tumor potential of NK cell adoptive transfer. DNA transposons are versatile non-viral gene vectors now being adapted to primary NK cells, representing important tools for research and clinical product development.

Aims and methods: We set out to generate donor-derived, primary chimeric antigen receptor (CAR)-NK cells by combining the TcBuster transposon system with Epstein-Barr virus-transformed lymphoblastoid feeder cell-mediated activation and expansion.

Results: This approach allowed for clinically relevant NK-cell expansion capability and CAR expression, which was further enhanced by immunomagnetic selection based on binding to the CAR target protein.The resulting CAR-NK cells targeting the myeloid associated antigen CLL-1 efficiently targeted CLL-1-positive AML cell lines and primary AML populations, including a population enriched for leukemia stem cells. Subsequently, concurrent delivery of CRISPR/Cas9 cargo was applied to knockout the NK cell cytokine checkpoint cytokine-inducible SH2-containing protein (CIS, product of the CISH gene), resulting in enhanced cytotoxicity and an altered NK cell phenotype.

Conclusions: This report contributes a promising application of transposon engineering to donor-derived NK cells and emphasizes the importance of feeder mediated NK cell activation and expansion to current protocols.

Keywords: CAR-NK cells; CRISPR/Cas9; DNA transposon; Genome editing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CRISPR-Cas Systems / genetics
  • Cell Line, Tumor
  • Cytokines / metabolism
  • Cytotoxicity, Immunologic
  • DNA Transposable Elements / genetics
  • Epstein-Barr Virus Infections*
  • Gene Editing
  • Herpesvirus 4, Human / genetics
  • Humans
  • Immunotherapy, Adoptive / methods
  • Killer Cells, Natural
  • Leukemia, Lymphocytic, Chronic, B-Cell* / genetics
  • Leukemia, Lymphocytic, Chronic, B-Cell* / therapy
  • Leukemia, Myeloid, Acute*
  • Receptors, Chimeric Antigen* / genetics
  • Receptors, Chimeric Antigen* / metabolism

Substances

  • Cytokines
  • DNA Transposable Elements
  • Receptors, Chimeric Antigen