Homology-driven genome editing in hematopoietic stem and progenitor cells using ZFN mRNA and AAV6 donors

Nature Biotechnology

Volumn 33, Issue 12, 2015, Pages 1256-1263

  Wang, Jianbin ^a   Exline, Colin M ^b   Declercq, Joshua J ^a   Llewellyn, G Nicholas ^b   Hayward, Samuel B ^a   Li, Patrick Wai Lun ^a   Shivak, David A ^a   Surosky, Richard T ^a   Gregory, Philip D ^a   Holmes, Michael C ^a   Cannon, Paula M ^b  

^a SANGAMO BIOSCIENCES INC   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; CELLS; CYTOLOGY; GENES; NUCLEIC ACIDS; VIRUSES;

ADENO-ASSOCIATED VIRUS; CELL POPULATIONS; EDITING TECHNOLOGY; HEMATOPOIETIC STEM CELLS; MINOR COMPONENTS; PERIPHERAL BLOOD; ROBUST APPLICATION; ZINC FINGER NUCLEASE;

STEM CELLS;

CD34 ANTIGEN; MESSENGER RNA; ZINC FINGER NUCLEASE;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 6; ARTICLE; BURST FORMING UNIT E; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL DIFFERENTIATION; CELL POPULATION; COLONY FORMATION; ELECTROPORATION; EX VIVO STUDY; FETUS LIVER; FLOW CYTOMETRY; GENE EXPRESSION; GENOME; GRANULOCYTE; HEMATOPOIETIC STEM CELL; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REPORTER GENE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; STEM CELL;

EID: 84949814888     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.3408     Document Type: Article

References (67)

1. Aiuti, A. et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 296, 2410-2413 (2002).
2. Cartier, N. et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326, 818-823 (2009).
3. Biffi, A. et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 341, 1233158 (2013).
4. Aiuti, A. et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 341, 1233151 (2013).
5. Cavazza, A., Moiani, A., Mavilio, F. Mechanisms of retroviral integration and mutagenesis. Hum. Gene Ther. 24, 119-131 (2013).
6. Braun, C.J. et al. Gene therapy for Wiskott-Aldrich syndrome-long-term efficacy and genotoxicity. Sci. Transl. Med. 6, 227-33 (2014).
7. HaceinBeyAbina, S. et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118, 3132-3142 (2008).
8. Gaj, T., Gersbach, C.A., Barbas, C.F. III. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31, 397-405 (2013).
9. Sung, P., Klein, H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7, 739-750 (2006).
10. Wyman, C., Kanaar, R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40, 363-383 (2006).
11. Brugmans, L., Kanaar, R., Essers, J. Analysis of DNA double-strand break repair pathways in mice. Mutat. Res. 614, 95-108 (2007).
12. Kowalczykowski, S.C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25, 156-165 (2000).
13. Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S., Gregory, P.D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646 (2010).
14. Tebas, P. et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N. Engl. J. Med. 370, 901-910 (2014).
15. Xu, J. et al. Corepressor-dependent silencing of fetal hemoglobin expression by BCL11A. Proc. Natl. Acad. Sci. USA 110, 6518-6523 (2013).
16. Lombardo, A. et al. Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nat. Methods 8, 861-869 (2011).
17. Coluccio, A. et al. Targeted gene addition in human epithelial stem cells by zinc-finger nuclease-mediated homologous recombination. Mol. Ther. 21, 1695-1704 (2013).
18. Meyer, M., de Angelis, M.H., Wurst, W., Kühn, R. Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases. Proc. Natl. Acad. Sci. USA 107, 15022-15026 (2010).
19. Pei, Y. et al. A platform for rapid generation of single and multiplexed reporters in human iPSC lines. Sci. Rep. 5, 9205 (2015).
20. Lombardo, A. et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat. Biotechnol. 25, 1298-1306 (2007).
21. Genovese, P. et al. Targeted genome editing in human repopulating haematopoietic stem cells. Nature 510, 235-240 (2014).
22. Baum, C.M., Weissman, I.L., Tsukamoto, A.S., Buckle, A.M., Peault, B. Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl. Acad. Sci. USA 89, 2804-2808 (1992).
23. Doulatov, S., Notta, F., Laurenti, E., Dick, J.E. Hematopoiesis: a human perspective. Cell Stem Cell 10, 120-136 (2012).
24. Hoban, M.D. et al. Correction of the sickle cell disease mutation in human hematopoietic stem/progenitor cells. Blood 125, 2597-2604 (2015).
25. Song, L. et al. Optimizing the transduction efficiency of capsid-modified AAV6 serotype vectors in primary human hematopoietic stem cells in vitro and in a xenograft mouse model in vivo. Cytotherapy 15, 986-998 (2013).
26. Song, L. et al. High-efficiency transduction of primary human hematopoietic stem cells and erythroid lineage-restricted expression by optimized AAV6 serotype vectors in vitro and in a murine xenograft model in vivo. PLoS One 8, e58757 (2013).
27. Veldwijk, M.R. et al. Pseudotyped recombinant adeno-associated viral vectors mediate efficient gene transfer into primary human CD34(+) peripheral blood progenitor cells. Cytotherapy 12, 107-112 (2010).
28. Perez, E.E. et al. Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat. Biotechnol. 26, 808-816 (2008).
29. Moehle, E.A. et al. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc. Natl. Acad. Sci. USA 104, 3055-3060 (2007).
30. Chen, F. et al. High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases. Nat. Methods 8, 753-755 (2011).
31. Kim, H., Kim, J.-S. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 15, 321-334 (2014).
32. Miller, J.C. et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 25, 778-785 (2007).
33. Miller, J.C. et al. Improved specificity of TALE-based genome editing using an expanded RVD repertoire. Nat. Methods 12, 465-471 (2015).
34. Ran, F.A. et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013).
35. Gabriel, R. et al. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat. Biotechnol. 29, 816-823 (2011).
36. Li, L. et al. Genomic editing of the HIV-1 coreceptor CCR5 in adult hematopoietic stem and progenitor cells using zinc finger nucleases. Mol. Ther. 21, 1259-1269 (2013).
37. Cheung, A.K., Hoggan, M.D., Hauswirth, W.W., Berns, K.I. Integration of the adeno-associated virus genome into cellular DNA in latently infected human Detroit 6 cells. J. Virol. 33, 739-748 (1980).
38. Smith, J.R. et al. Robust, persistent transgene expression in human embryonic stem cells is achieved with AAVS1-targeted integration. Stem Cells 26, 496-504 (2008).
39. Miller, D.G., Petek, L.M., Russell, D.W. Adeno-associated virus vectors integrate at chromosome breakage sites. Nat. Genet. 36, 767-773 (2004).
40. Lin, Y., Waldman, A.S. Promiscuous patching of broken chromosomes in mammalian cells with extrachromosomal DNA. Nucleic Acids Res. 29, 3975-3981 (2001).
41. Lin, Y., Waldman, A.S. Capture of DNA sequences at double-strand breaks in mammalian chromosomes. Genetics 158, 1665-1674 (2001).
42. Murray, L. et al. Enrichment of human hematopoietic stem cell activity in the CD34+Thy-1+Lin-subpopulation from mobilized peripheral blood. Blood 85, 368-378 (1995).
43. Majeti, R., Park, C.Y., Weissman, I.L. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 1, 635-645 (2007).
44. Negrin, R.S. et al. Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with metastatic breast cancer. Biol. Blood Marrow Transplant. 6, 262-271 (2000).
45. Vose, J.M. et al. Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with recurrent indolent non-Hodgkin's lymphoma. Biol. Blood Marrow Transplant. 7, 680-687 (2001).
46. Dick, J.E., Bhatia, M., Gan, O., Kapp, U., Wang, J.C.Y. Assay of human stem cells by repopulation of NOD/SCID mice. Stem Cells 15(suppl. 1), 199-203, discussion 204-207 (1997).
47. Holt, N. et al. Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat. Biotechnol. 28, 839-847 (2010).
48. Hogan, C.J., Shpall, E.J., Keller, G. Differential long-term and multilineage engraftment potential from subfractions of human CD34+ cord blood cells transplanted into NOD/SCID mice. Proc. Natl. Acad. Sci. USA 99, 413-418 (2002).
49. Dick, J.E., Guenechea, G., Gan, O.I., Dorrell, C. In vivo dynamics of human stem cell repopulation in NOD/SCID mice. Ann. NY Acad. Sci. 938, 184-190 (2001).
50. McKenzie, J.L., Gan, O.I., Doedens, M., Wang, J.C.Y., Dick, J.E. Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment. Nat. Immunol. 7, 1225-1233 (2006).
51. Gu, A. et al. Engraftment and lineage potential of adult hematopoietic stem and progenitor cells is compromised following short-term culture in the presence of an aryl hydrocarbon receptor antagonist. Hum. Gene Ther. Methods 25, 221-231 (2014).
52. Hofer, U. et al. Pre-clinical modeling of CCR5 knockout in human hematopoietic stem cells by zinc finger nucleases using humanized mice. J. Infect. Dis. 208 (suppl. 2), S160-S164 (2013).
53. Branzei, D., Foiani, M. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9, 297-308 (2008).
54. Notta, F. et al. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 333, 218-221 (2011).
55. Hirata, R., Chamberlain, J., Dong, R., Russell, D.W. Targeted transgene insertion into human chromosomes by adeno-associated virus vectors. Nat. Biotechnol. 20, 735-738 (2002).
56. Miller, D.G. et al. Gene targeting in vivo by adeno-associated virus vectors. Nat. Biotechnol. 24, 1022-1026 (2006).
57. Russell, D.W., Hirata, R.K. Human gene targeting by viral vectors. Nat. Genet. 18, 325-330 (1998).
58. Rogers, C.S. et al. Production of CFTR-null and CFTR-DeltaF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer. J. Clin. Invest. 118, 1571-1577 (2008).
59. Hirsch, M.L. Adeno-associated virus inverted terminal repeats stimulate gene editing. Gene Ther. 22, 190-195 (2015).
60. Barzel, A. et al. Promoterless gene targeting without nucleases ameliorates haemophilia B in mice. Nature 517, 360-364 (2015).
61. DeKelver, R.C. et al. Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome. Genome Res. 20, 1133-1142 (2010).
62. Doyon, Y. et al. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat. Methods 8, 74-79 (2011).
63. Boczkowski, D., Nair, S.K., Nam, J.-H., Lyerly, H.K., Gilboa, E. Induction of tumor immunity and cytotoxic T lymphocyte responses using dendritic cells transfected with messenger RNA amplified from tumor cells. Cancer Res. 60, 1028-1034 (2000).
64. Wang, J. et al. Targeted gene addition to a predetermined site in the human genome using a ZFN-based nicking enzyme. Genome Res. 22, 1316-1326 (2012).
65. Xiao, X., Li, J., Samulski, R.J. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 72, 2224-2232 (1998).
66. Langmead, B., Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
67. Guilinger, J.P. et al. Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity. Nat. Methods 11, 429-435 (2014).