Targeted genome editing in human repopulating haematopoietic stem cells

Authors:
Genovese P, Schiroli G, Escobar G, Di Tomaso T1, Firrito C, Calabria A, Moi D, Mazzieri R, Bonini C, Holmes MC, Gregory PD, van der Burg M, Gentner B, Montini E, Lombardo A, Naldini L.
In:
Source: Nature
Publication Date: (2014)
Issue: 510: 235-40
Research Area:
Cancer Research/Cell Biology
Immunotherapy / Hematology
Stem Cells
Basic Research
Molecular Biology
Cells used in publication:
CD34+ cell, human
Species: human
Tissue Origin: blood
Platform:
Nucleofector® I/II/2b
4D-Nucleofector® X-Unit
Experiment

Donor IDLV for HDR were generated as described. ZFNs targeting intron 1 of PPP1R12C or exon 5 of IL2RG were expressed by mRNA electroporation. CD34+ cells from human umbilical cord blood or bone marrow were used on approval by the San Raffaele Hospital Bioethical Committee, stimulated in serum-free medium with early acting cytokines, infected with IDLVs at a multiplicity of infection (MOI) 100–500, and then electroporated with 175 mg/ml ZFNs encoding mRNAs (P3 Primary Cell 4D-Nucleofector X Kit, program EO-100; Lonza). Targeted integration was assessed by PCR and Southern blot while ZFN activity was determined by Cel1 assay and deep sequencing of genomic target sites. The treated CD34+ cells at day 4 of culture were infused intravenously into sublethally irradiated 8–11-week-old NOD-SCID-Il2rg-/- (NSG) mice. To expand human T and NK cells, 4 million MDA3-MB231 tumour cells expressing human IL-7, IL-15 and GM-CSF were implanted orthotopically in the mammary fat pad of NSG mice 14 weeks after CD34+ cells transplantation. Functional assays on IL2RG-edited T cells collected from transplanted mice were carried out after stimulation with beads conjugated to anti-human CD3 and CD28 antibodies and sorting for GFP expression. Summary (Lonza): The authors optimized a protocol that allows gene repair in repopulating human haematopoietic stem cells (HSCs), key target cells for treating blood inherited disorders. Genovese et al. achieved efficient integration of a GFP sequence into the genome of human HSCs at chosen sites, including a protein-coding region (exon 5) of the IL2RG gene that is mutated in patients with X-linked severe combined immunodeficiency (SCID-X1). HSCs were pre-stimulated with cytokines, delivered with the recombination template, and followed by a transfection with Zn-finger nuclease mRNA using the 4D-Nucleofector. Cells were prevented from differentiation using dmPGE2 and SR1 factors. A portion of the cells was modified with success, then transferred into immunodeficient mice. Edited functional cells could be detected for up to 18 weeks and further transferred into a second recipient. The authors were also able to correct HSC derived from a patient carrying Il2rg-/- SCID-X1 syndrome. Using this approach, the authors opened new avenues for treating SCID-X1 disease and other genetic diseases using genome editing tools.

Abstract

Targeted genome editing by artificial nucleases has brought the goal of site-specific transgene integration and gene correction within the reach of gene therapy. However, its application to long-term repopulating haematopoietic stem cells (HSCs) has remained elusive. Here we show that poor permissiveness to gene transfer and limited proficiency of the homology-directed DNA repair pathway constrain gene targeting in human HSCs. By tailoring delivery platforms and culture conditions we overcame these barriers and provide stringent evidence of targeted integration in human HSCs by long-term multilineage repopulation of transplanted mice. We demonstrate the therapeutic potential of our strategy by targeting a corrective complementary DNA into the IL2RG gene of HSCs from healthy donors and a subject with X-linked severe combined immunodeficiency (SCID-X1). Gene-edited HSCs sustained normal haematopoiesis and gave rise to functional lymphoid cells that possess a selective growth advantage over those carrying disruptive IL2RG mutations. These results open up new avenues for treating SCID-X1 and other diseases.