Targeted gene editing and near-universal cDNA insertion of CYBA and CYBB as a treatment for chronic granulomatous disease

Authors:
Wolff JH, Skov TW, Haslund D, Dorset SR, Revenfeld ALS, Aussel C, Jørgensen SE, Holm M, Thomsen MK, Ammann S, Cathomen T, Mogensen TH, Møller BK, Bak RO, Mikkelsen JG
In:
Source: Nat Commun.
Publication Date: (2025)
Issue: 16(1): 7475
Research Area:
Cancer Research/Cell Biology
Immunotherapy / Hematology
Gene Expression
Basic Research
Regenerative medicine
Drug Discovery
Cells used in publication:
K-562
Species: human
Tissue Origin: blood
CD34+ cell, human
Species: human
Tissue Origin: blood
Platform:
4D-Nucleofector® X-Unit
Experiment

Gene editing of cell lines and human CD34+ HSPCs
For gene editing experiments, cells were nucleofected with 6 µg Cas9 (Alt-R™ S.p. Cas9 Nuclease V3 or Alt-R™ S.p. HiFi Cas9 Nuclease V3, IDT) and 3.2 µg synthetic sgRNA (Synthego) using a Lonza 4D Nucleofector X (Lonza). Cells were washed in Gibco Opti-MEM Reduced Serum Medium (K562 cells, Thermo Fischer Scientific) or PBS (CD34+ HSPCs) and resuspended in 18-20 µL 1M buffer (50mMDMannitol, 5mM KCL, 120mM Na2HPO4, 15mM MgCl2) prior to nucleofection. When applicable, 100 pmol ssODNs (IDT) were included in the nucleofection. K562 cells were nucleofected using the CM-138 program and the Primary Cell P3 setting. CD34+ HSPCs were nucleofected using the DZ-100 program and the Primary Cell P3 settings. When i53, GSE56, and/or Ad5-E4orf6/7 mRNAs were used, 3 µg of each was included in the nucleofection. Mock nucleofections were carried out the same way, but without adding sgRNA, Cas9, or mRNA. Following nucleofection, cells were seeded at 5×10^5 cells mL-1 and transduced with viral vectors carrying HDR repair templates within 15 min. 

Abstract

Chronic granulomatous disease (CGD) is a severe inborn error of immunity caused by NADPH oxidase defects. Here, we develop CRISPR/Cas9-based gene editing strategies for correction of variants in the CYBA and CYBB genes causing CGD. For X-linked CGD, we also develop a near-universal gene editing strategy by targeted integration of a truncated CYBB cDNA in CD34+ hematopoietic stem and progenitor cells (HSPCs). Throughout, off-target editing and chromosomal translocations are evident, which negatively impact the ability of gene-edited HSPCs to engraft in immunodeficient mice. However, by employing a high-fidelity Cas9 to minimize off-target editing, we demonstrate restoration of the multilineage engraftment potential of gene-edited HSPCs. Moreover, to further improve safety, we develop a D10A Cas9n editing approach with no detectable off-target activity or chromosomal translocations. Collectively, through risk assessments of different gene editing approaches, we present a D10A Cas9n-based strategy with improved safety, offering a potentially curative treatment for CGD patients.