Engineering HIV-resistant human CD4+ T cells with CXCR4-specific zinc-finger nucleases
Open accessAbstract
HIV-1 entry requires the cell surface expression of CD4 and either the CCR5 or CXCR4 coreceptors on host cells. Individuals homozygous for the ccr5Δ32 polymorphism do not express CCR5 and are protected from infection by CCR5-tropic (R5) virus strains. As an approach to inactivating CCR5, we introduced CCR5-specific zinc-finger nucleases into human CD4+ T cells prior to adoptive transfer, but the need to protect cells from virus strains that use CXCR4 (X4) in place of or in addition to CCR5 (R5X4) remains. Here we describe engineering a pair of zinc finger nucleases that, when introduced into human T cells, efficiently disrupt cxcr4 by cleavage and error-prone non-homologous DNA end-joining. The resulting cells proliferated normally and were resistant to infection by X4-tropic HIV-1 strains. CXCR4 could also be inactivated in ccr5Δ32 CD4+ T cells, and we show that such cells were resistant to all strains of HIV-1 tested. Loss of CXCR4 also provided protection from X4 HIV-1 in a humanized mouse model, though this protection was lost over time due to the emergence of R5-tropic viral mutants. These data suggest that CXCR4-specific ZFNs may prove useful in establishing resistance to CXCR4-tropic HIV for autologous transplant in HIV-infected individuals.
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Many studies have successfully disrupted CCR5 in various cell lines, primary T cells and hematopoietic stem cells, as well as in humanized mice.
“Since then, many studies have successfully disrupted CCR5 in various cell lines, primary T cells and hematopoietic stem cells (HSCs), as well as in humanized mice [30,31,32,38,39,40].”
From Newer Gene Editing Technologies toward HIV Gene Therapy (2013) · cites this paper as [31]
Three studies have demonstrated that targeting CXCR4 can promote HIV-1 resistance.
“To date, three studies have demonstrated that targeting CXCR4 can promote HIV-1 resistance.”
From Newer Gene Editing Technologies toward HIV Gene Therapy (2013) · cites this paper as [31]
An adenoviral vector delivered ZFNs to activated CD4+ T cells in vitro, reaching a gene-disruption efficiency as high as 54% for CCR5 and 30%-34% for CXCR4.
“As a proof-of-concept delivery method, an adenoviral vector was used to deliver ZFNs to activated CD4+T cells in vitro, reaching a gene-disruption efficiency as high as 54% for CCR5 [30] and 30%–34% for CXCR4 [31,32].”
From Newer Gene Editing Technologies toward HIV Gene Therapy (2013) · cites this paper as [31]
After expansion in vitro, adenovirus-ZFN transduced CD4+ T cells infused into humanized mice were able to establish resistance to HIV-1 infection.
“After expansion in vitro, the adenovirus-ZFN transduced CD4+ T cells were infused into humanized mice where they were able to establish resistance to HIV-1 infection.”
From Newer Gene Editing Technologies toward HIV Gene Therapy (2013) · cites this paper as [31]
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- Authors
- Wilen, C. B., Wang, J., Tilton, J. C., Miller, J. C., Kim, K. A., Rebar, E. J., Sherrill-Mix, S. A., Patro, S. C., Secreto, A. J., Jordan, A. P. O., Lee, G., Kahn, J., Aye, P. P., Bunnell, B. A., Lackner, A. A., Hoxie, J. A., Danet-Desnoyers, G. A., Bushman, F. D., Riley, J. L., Gregory, P. D., June, C. H., Holmes, M. C., & Doms, R. W.
- Affiliations
- University of Pennsylvania (US)
- Sangamo BioSciences (United States) (US)
- Tulane University (US)
- Corresponding author
- Doms, Robert W.
- ORCID
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-04-14
- Volume
- 7
- Issue
- 4
- Pages
- e1002020
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC3077364
- OpenAlex
- W2007764764
- Cited by
- 142
- References
- 63
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 2 · 2022: 5 · 2021: 7 · 2020: 2 · 2019: 2 · 2018: 7 · 2017: 17 · 2016: 13 · 2015: 21 · 2014: 19 · 2013: 13 · 2012: 25
- FWCI
- 7.46
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Pennsylvania Department of Health
- University of Pennsylvania
- National Institutes of Health (RR000164)
- Center for AIDS Research, University of Washington
- National Institute of Allergy and Infectious Diseases (P01AI090935, T32 AI000632, R01AI040880, F32AI077370, F32 1F32AI077370, U19AI082628)
- National Center for Research Resources (P51RR000164)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Keywords
- HIV-1, CXCR4, zinc finger nucleases, CD4+ T cells, HIV drug resistance, CCR5, CCR5Δ32, HIV co-receptor, genome editing, adoptive cell transfer, humanized mice, CCR5-tropic HIV
- MeSH terms
- Animals, Deoxyribonucleases, Disease Models, Animal, Genetic Engineering, Humans, Macaca mulatta, Transplantation, Autologous, Transplantation, Heterologous, CD4-Positive T-Lymphocytes, HIV-1, HIV Infections, Receptors, CCR5, Receptors, CXCR4, Cell Proliferation, Mice, Virus Internalization
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