CRISPR-Mediated Non-Viral Site-Specific Gene Integration and Expression in T Cells: Protocol and Application for T-Cell Therapy

Authors:
Zelda Odé , Jose Condori , Nicolas Peterson , Sheng Zhou , Giedre Krenciute 
In:
Source: Cancers
Publication Date: (2020)
Issue: 12(6): 1704
Research Area:
Cancer Research/Cell Biology
Immunotherapy / Hematology
Cells used in publication:
PBMC, human
Species: human
Tissue Origin: blood
CD4+, human
Species: human
Tissue Origin: blood
CD8+, human
Species: human
Tissue Origin: blood
Platform:
4D-Nucleofector® X-Unit
Experiment

Two days after T-cell activation, cells were electroporated to enable site-specific knock-in using
Cas9 RNPs. All electroporation experiments were performed on the 4D-NucleofectorTM System X Unit (Lonza, Basel, Switzerland) using the EH-115 program. RNPs were pre-complexed at a sgRNA:Cas9 ratio of 4.5:1, prepared by adding 3 µL of 60 µM sgRNA (Synthego Menlo Park, CA, USA) to 1 µL of 40 µM Cas 9 (QB3 Macrolab, University of California, Berkeley, CA, USA), and incubated for 10 min at room temperature (RT). Complexed RNPs were used right away or frozen fr later use. Sequences for all sgRNAs can be found in Table S2. T cells (0.6 x 106 or 1.0 x 106) were re-suspended in 17 µL P3 buffer including supplement 1 (Lonza). Subsequently, 4 µL of RNP complex was added together withthe  dsDNA template donor (2 µg/3 µL unless stated  otherwise) and incubated for 10 min at room temp. The RNP and dsDNA mix were added to the cell mixture and 23 µL was added to the transfection vessel and electroporated. After electroporation, 80 µL of recovery media (RPMI (GE Healthcare Life Sciences, Marlborough, MA, USA) including 20% FBS (GE Healthcare Life Sciences, Marlborough, MA, USA), 1% GlutaMAX-I (Invitrogen, Carlsbad, CA, USA), IL-7 at 10 ng/mL, and IL-15 at 5 ng/mL) was added to the electroporation vessel. The cells were rested for 30 min at 37 C and 5% CO2 before being transferred into a 48-well, tissue culture plate with 650 µL of recovery media. Two to three days after electroporation, the FBS concentration was reduced to 10% in the T-cell culture media with cytokines. T cell s were split every 3–4 days and fresh IL-7 and IL-15 cytokines were added.

Abstract

T cells engineered with chimeric antigen receptors (CARs) show great promise in the treatment of some cancers. Modifying T cells to express CARs generally relies on T-cell transduction using viral vectors carrying a transgene, resulting in semi-random DNA integration within the T-cell genome. While this approach has proven successful and is used in generating the Food and Drug Administration (FDA, USA) approved B-lymphocyte antigen CD19-specific CAR T cells, it is possible the transgene could integrate into a locus that would lead to malignant transformation of the engineered T cells. In addition, manufacturing viral vectors is time-consuming and expensive. One way to overcome these challenges is site-specific gene integration, which can be achieved through clustered regularly interspaced short palindromic repeat (CRISPR) mediated editing and non-viral DNA, which serves as a template for homology-directed repair (HDR). This non-viral gene editing approach provides a rapid, highly specific, and inexpensive way to engineer T cells. Here, we describe an optimized protocol for the site-specific knock-in of a large transgene in primary human T cells using non-viral double stranded DNA as a repair template. As proof-of-principle, we targeted the T-cell receptor alpha constant (TRAC) locus for insertion of a large transgene containing green fluorescence protein (GFP) and interleukin-15 (IL-15). To optimize the knock-in conditions we tested template DNA concentration, homology arm length, cell number, and knock-in efficiency over time. We then applied these established guidelines to target the TRAC or interleukin-13 (IL-13) locus for the knock-in of synthetic molecules, such as a CAR, bispecific T-cell engager (BiTE), and other transgenes. While integration efficiency depends on the targeted gene locus and selected transgene, this optimized protocol reliably generates the desired insertion at rates upwards of 20%. Thus, it should serve as a good starting point for investigators who are interested in knocking in transgenes into specific loci.