Near-perfect precise on-target editing of human hematopoietic stem and progenitor cells

Authors:
Cloarec-Ung FM, Beaulieu J, Suthananthan A, Lehnertz B, Sauvageau G, Sheppard HM, Knapp DJHF
In:
Source: eLife
Publication Date: (2024)
Issue: 12: RP91288
Research Area:
Cancer Research/Cell Biology
Immunotherapy / Hematology
Stem Cells
Gene Expression
Basic Research
Molecular Biology
Regenerative medicine
Drug Discovery
Cells used in publication:
CD34+ cell, human
Species: human
Tissue Origin: blood
Platform:
4D-Nucleofector® X-Unit
Experiment

CD34+ cell editing
After 48 hr of pre-stimulation, viable cells were counted by hemocytometer. Prior to nucleofection, cells were washed once with PBS, spun down for 5 min at 300 g, and re-suspended in buffer 1M (Chicaybam et al., 2016) (5 mM KCl; 15 mM MgCl2; 120 mM Na2HPO4/NaH2PO4 pH7.2; 50 mM Manitol) such that each well of the Nucleocuvette strip would contain 20,000–100,000 cells. Assembled RNP, p53 siRNA (20 fmol, Thermo id s605), electroporation enhancer (IDT), and any ssODN donors (IDT) (as specified in each experiment). Overall RNP and other additives were kept at or below 10% of the total 20 µL volume per well. Handling time between wash and nucleofection was kept within a 10 min window. Cells were nucleofected using the Lonza 4D nucleofector device with nucleocuvette strips, Primary P3, and DZ-100 program. Following nucleofection, cells were allowed to rest for 5 min and then added to pre-warmed wells of a 24-well plate containing media (as specified in CD34 + cell culture) supplemented with small molecules as indicated for specific experiments (AZD7648, RS-1, Cayman Chemicals; M-3814, Toronto Research Chemicals). Where AAV donor was used, it was added to the well within 15 min of nucleofection (Charlesworth et al., 2018). 

Abstract

Precision gene editing in primary hematopoietic stem and progenitor cells (HSPCs) would facilitate both curative treatments for monogenic disorders as well as disease modelling. Precise efficiencies even with the CRISPR/Cas system, however, remain limited. Through an optimization of guide RNA delivery, donor design, and additives, we have now obtained mean precise editing efficiencies >90% on primary cord blood HSCPs with minimal toxicity and without observed off-target editing. The main protocol modifications needed to achieve such high efficiencies were the addition of the DNA-PK inhibitor AZD7648, and the inclusion of spacer-breaking silent mutations in the donor in addition to mutations disrupting the PAM sequence. Critically, editing was even across the progenitor hierarchy, did not substantially distort the hierarchy or affect lineage outputs in colony-forming cell assays or the frequency of high self-renewal potential long-term culture initiating cells. As modelling of many diseases requires heterozygosity, we also demonstrated that the overall editing and zygosity can be tuned by adding in defined mixtures of mutant and wild-type donors. With these optimizations, editing at near-perfect efficiency can now be accomplished directly in human HSPCs. This will open new avenues in both therapeutic strategies and disease modelling.