Engineering of potent CAR NK cells using non-viral Sleeping Beauty transposition from minimalistic DNA vectors

Authors:
Bexte T, Botezatu L, Miskey C, Gierschek F, Moter A, Wendel P, Reindl LM, Campe J, Villena-Ossa JF, Gebel V, Stein K, Cathomen T, Cremer A, Wels WS, Hudecek M, Ivics Z, Ullrich E.
In:
Source: Mol Ther
Publication Date: (2024)
Issue: S1525-0016: 00320-4
Research Area:
Cancer Research/Cell Biology
Immunotherapy / Hematology
Gene Expression
Molecular Biology
Regenerative medicine
Cells used in publication:
Natural killer Cells (NK), human
Species: human
Tissue Origin: blood
Platform:
4D-Nucleofector® X-Unit
Experiment

Generation and nucleofection of primary CD19-CAR NK cells
 NK cells were isolated from the peripheral blood of healthy donors and nucleofected with either pmaxGFP alone or SB transposons vectorized as MCs, which encode either a Venus fluorescent protein or a CD19-CAR in combination with a hyperactive SB100X transposase. The transposon MC vectors carrying CD19-CAR were flanked by ITRs and provided in the form of SNIM mRNA SB100X. Per sample, 1 × 10^6 NK cells were nucleofected with 2.5 µg of SB  transposase and 1 µg MC DNA using the 4D Nucleofector (Lonza), P3 Primary Cell 4D Nucleofector X Kit S and L, and the DO-100 nucleofection program. After nucleofection, the cells were transferred to cultivation medium. Production of viral vectors and following transduction have been performed as previously described. The utilized transfer plasmid was provided by M. Hudecek.Transduction of IL-15 stimulated primary NK cells was performed by spinfection at 800 × g for 1 ½ h at 32 °C in presence of Vectofusin-1 (Miltenyi Biotec, 10µg/mL) as described previously.

Abstract

Natural Killer (NK) cells have high intrinsic cytotoxic capacity, and clinical trials have demonstrated their safety and efficacy for adoptive cancer therapy. Expression of chimeric antigen receptors (CARs) enhances NK cell target-specificity, with these cells applicable as 'off-the-shelf' products generated from allogeneic donors. Here, we present for the first time an innovative approach for CAR NK cell engineering employing a non-viral Sleeping Beauty (SB) transposon/transposase-based system and minimized DNA vectors termed minicircles. SB-modified peripheral blood-derived primary NK cells displayed high and stable CAR expression and more frequent vector integration into 'genomic safe harbors' than lentiviral vectors. Importantly, SB-generated CAR NK cells demonstrated enhanced cytotoxicity compared to non-transfected NK cells. A strong antileukemic potential was confirmed using established acute lymphocytic leukemia (ALL) cells and patient-derived primary B-ALL samples as targets in vitro and in vivo in a xenograft leukemia mouse model. Our data suggest that the SB-transposon system is an efficient, safe and cost-effective approach to non-viral engineering of highly functional CAR NK cells, which may be suitable for cancer immunotherapy of leukemia as well as many other malignancies.