Targeted, homology-driven gene insertion in stem cells by ZFN-loaded ‘all-in-one’ lentiviral vectors

eLife

Volumn 5, Issue JUN2016, 2016, Pages

  Cai, Yujia ^a   Laustsen, Anders ^a   Zhou, Yan ^a   Sun, Chenglong ^a   Anderson, Mads Valdemar ^a,b   Li, Shengting ^a,c   Uldbjerg, Niels ^a   Luo, Yonglun ^a   Jakobsen, Martin R ^a   Mikkelsen, Jacob Giehm ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c BGI SHENZHEN   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LENTIVIRUS VECTOR; ZINC FINGER NUCLEASE; DEOXYRIBONUCLEASE; DNA LIGASE;

ARTICLE; CD34 SELECTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA END JOINING REPAIR; FLOW CYTOMETRY; GENE EXPRESSION; GENE INSERTION; GENETIC TRANSFECTION; HEK293 CELL LINE; HEMATOPOIETIC STEM CELL; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; KARYOTYPE; LUCIFERASE ASSAY; NEXT GENERATION SEQUENCING; PLASMID; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; STEM CELL CULTURE; STEM CELL TRANSPLANTATION; VIRAL GENE THERAPY; CELL CULTURE; GENE EXPRESSION REGULATION; GENE TARGETING; GENE THERAPY; GENE VECTOR; GENETICS; LENTIVIRINAE; METABOLISM; PHYSIOLOGY; PROCEDURES; STEM CELL;

CELLS, CULTURED; DEOXYRIBONUCLEASES; DNA REPAIR ENZYMES; GENE TARGETING; GENETIC THERAPY; GENETIC VECTORS; HOMOLOGOUS RECOMBINATION; HUMANS; LENTIVIRUS; MUTAGENESIS, INSERTIONAL; STEM CELLS;

EID: 84975275047     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12213     Document Type: Article

References (35)

1. Bushman FD, Miller MD. 1997. Tethering human immunodeficiency virus type 1 preintegration complexes to target DNA promotes integration at nearby sites. Journal of Virology 71: 458-464.
2. Cai Y, Bak RO, Mikkelsen JG. 2014a. Targeted genome editing by lentiviral protein transduction of zinc-finger and tal-effector nucleases. eLife 3: e01911. doi: 10.7554/eLife.01911
3. Cai Y, Bak RO, Krogh LB, Staunstrup NH, Moldt B, Corydon TJ, Schrøder LD, Mikkelsen JG. 2014b. DNA transposition by protein transduction of the piggybac transposase from lentiviral gag precursors. Nucleic Acids Research 42: e28. doi: 10.1093/nar/gkt1163
4. Chu VT, Weber T, Wefers B, Wurst W, Sander S, Rajewsky K, Kühn R. 2015. Increasing the efficiency of homology-directed repair for crispr-cas9-induced precise gene editing in mammalian cells. Nature Biotechnology 33: 543-548. doi: 10.1038/nbt.3198
5. Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC. 2011. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nature Methods 8: 74-79. doi: 10.1038/nmeth.1539
6. Gaj T, Guo J, Kato Y, Sirk SJ, Barbas CF. 2012. Targeted gene knockout by direct delivery of zinc-finger nuclease proteins. Nature Methods 9: 805-807. doi: 10.1038/nmeth.2030
7. Genovese P, Schiroli G, Escobar G, Di Tomaso T, 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. 2014. Targeted genome editing in human repopulating haematopoietic stem cells. Nature 510: 235-240. doi: 10.1038/nature13420
8. Gijsbers R, Ronen K, Vets S, Malani N, De Rijck J, McNeely M, Bushman FD, Debyser Z. 2010. LEDGF hybrids efficiently retarget lentiviral integration into heterochromatin. Molecular Therapy 18: 552-560. doi: 10.1038/mt.2010.36
9. Hendel A, Bak RO, Clark JT, Kennedy AB, Ryan DE, Roy S, Steinfeld I, Lunstad BD, Kaiser RJ, Wilkens AB, Bacchetta R, Tsalenko A, Dellinger D, Bruhn L, Porteus MH. 2015. Chemically modified guide rnas enhance crispr-cas genome editing in human primary cells. Nature Biotechnology 33. doi: 10.1038/nbt.3290
10. Hoban MD, Cost GJ, Mendel MC, Romero Z, Kaufman ML, Joglekar AV, Ho M, Lumaquin D, Gray D, Lill GR, Cooper AR, Urbinati F, Senadheera S, Zhu A, Liu PQ, Paschon DE, Zhang L, Rebar EJ, Wilber A, Wang X, et al. 2015. Correction of the sickle cell disease mutation in human hematopoietic stem/progenitor cells. Blood 125: 2597-2604. doi: 10.1182/blood-2014-12-615948
11. Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, DeKelver RC, Katibah GE, Amora R, Boydston EA, Zeitler B, Meng X, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R. 2009. Efficient targeting of expressed and silent genes in human escs and ipscs using zinc-finger nucleases. Nature Biotechnology 27: 851-857. doi: 10.1038/nbt.1562
12. Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, Zeitler B, Cherone JM, Meng X, Hinkley SJ, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R. 2011. Genetic engineering of human pluripotent cells using TALE nucleases. Nature Biotechnology 29: 731-734. doi: 10.1038/nbt.1927
13. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F. 2013. DNA targeting specificity of rna-guided cas9 nucleases. Nature Biotechnology 31: 827-832. doi: 10.1038/nbt.2647
14. Joshi N, Fass J. Sickle: A sliding-window, adaptive, quality-based trimming tool for fastq files. Version 1.33 https://github.com/najoshi/sickle. 2011
15. Kang R, Zhou Y, Tan S, Zhou G, Aagaard L, Xie L, Bünger C, Bolund L, Luo Y. 2015. Mesenchymal stem cells derived from human induced pluripotent stem cells retain adequate osteogenicity and chondrogenicity but less adipogenicity. Stem Cell Research & Therapy 6. doi: 10.1186/s13287-015-0137-7
16. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Ségéral E, Yatim A, Emiliani S, Schwartz O, Benkirane M. 2011. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by vpx. Nature 474: 654-657. doi: 10.1038/nature10117
17. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with bowtie 2. Nature Methods 9: 357-359. doi: 10.1038/nmeth.1923
18. Lei Y, Lee CL, Joo KI, Zarzar J, Liu Y, Dai B, Fox V, Wang P. 2011. Gene editing of human embryonic stem cells via an engineered baculoviral vector carrying zinc-finger nucleases. Molecular Therapy 19: 942-950. doi: 10.1038/mt.2011.12
19. Marniemi J, Parkki MG, Lin S, Staahl BT, Alla RK, Doudna JA. 1975. Radiochemical assay of glutathione s-epoxide transferase and its enhancement by phenobarbital in rat liver in vivo. Biochemical Pharmacology 24. doi: 10.1016/0006-2952(75)90080-5
20. Lombardo A, Cesana D, Genovese P, Di Stefano B, Provasi E, Colombo DF, Neri M, Magnani Z, Cantore A, Lo Riso P, Damo M, Pello OM, Holmes MC, Gregory PD, Gritti A, Broccoli V, Bonini C, Naldini L. 2011. Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nature Methods 8: 861-869. doi: 10.1038/nmeth.1674
21. Lump E, Castellano LM, Meier C, Seeliger J, Erwin N, Sperlich B, Stürzel CM, Usmani S, Hammond RM, von Einem J, Gerold G, Kreppel F, Bravo-Rodriguez K, Pietschmann T, Holmes VM, Palesch D, Zirafi O, Weissman D, Sowislok A, Wettig B, et al. 2015. A molecular tweezer antagonizes seminal amyloids and HIV infection. eLife 4. doi: 10.7554/eLife.05397
22. Magoč T, Salzberg SL. 2011. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963. doi: 10.1093/bioinformatics/btr507
23. Merling RK, Sweeney CL, Chu J, Bodansky A, Choi U, Priel DL, Kuhns DB, Wang H, Vasilevsky S, De Ravin SS, Winkler T, Dunbar CE, Zou J, Zarember KA, Gallin JI, Holland SM, Malech HL. 2015. An aavs1-targeted minigene platform for correction of ipscs from all five types of chronic granulomatous disease. Molecular Therapy 23: 147-157. doi: 10.1038/mt.2014.195
24. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC, Ecker JR, Bushman FD. 2004. Retroviral DNA integration: Aslv, HIV, and MLV show distinct target site preferences. PLoS Biology 2: E234. doi: 10.1371/journal.pbio.0020234
25. Modlich U, Navarro S, Zychlinski D, Maetzig T, Knoess S, Brugman MH, Schambach A, Charrier S, Galy A, Thrasher AJ, Bueren J, Baum C. 2009. Insertional transformation of hematopoietic cells by self-inactivating lentiviral and gammaretroviral vectors. Molecular Therapy 17: 1919-1928. doi: 10.1038/mt.2009.179
26. Moldt B, Miskey C, Staunstrup NH, Gogol-Döring A, Bak RO, Sharma N, Mátés L, Izsvák Z, Chen W, Ivics Z, Mikkelsen JG. 2011. Comparative genomic integration profiling of sleeping beauty transposons mobilized with high efficacy from integrase-defective lentiviral vectors in primary human cells. Molecular Therapy 19: 1499-1510. doi: 10.1038/mt.2011.47
27. Perez EE, Wang J, Miller JC, Jouvenot Y, Kim KA, Liu O, Wang N, Lee G, Bartsevich VV, Lee YL, Guschin DY, Rupniewski I, Waite AJ, Carpenito C, Carroll RG, Orange JS, Urnov FD, Rebar EJ, Ando D, Gregory PD, et al. 2008. Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nature Biotechnology 26: 808-816. doi: 10.1038/nbt1410
28. Pinello L. 2015. Crispresso: Sequencing analysis toolbox for crispr-cas9 genome editing. bioRxiv.
29. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics : TIG 16: 276-277. doi: 10.1016/S0168-9525(00)02024-2
30. Schröder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F. 2002. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110: 521-529. doi: 10.1016/S0092-8674(02)00864-4
31. Staunstrup NH, Moldt B, Mátés L, Villesen P, Jakobsen M, Ivics Z, Izsvák Z, Mikkelsen JG. 2009. Hybrid lentivirus-transposon vectors with a random integration profile in human cells. Molecular Therapy 17: 1205-1214. doi: 10.1038/mt.2009.10
32. Tay FC, Tan WK, Goh SL, Ramachandra CJ, Lau CH, Zhu H, Chen C, Du S, Phang RZ, Shahbazi M, Fan W, Wang S. 2013. Targeted transgene insertion into the AAVS1 locus driven by baculoviral vector-mediated zinc finger nuclease expression in human-induced pluripotent stem cells. The Journal of Gene Medicine 15: 384-395. doi: 10.1002/jgm.2745
33. Tiyaboonchai A, Mac H, Shamsedeen R, Mills JA, Kishore S, French DL, Gadue P. 2014. Utilization of the AAVS1 safe harbor locus for hematopoietic specific transgene expression and gene knockdown in human ES cells. Stem Cell Research 12: 630-637. doi: 10.1016/j.scr.2014.02.004
34. Vink CA, Gaspar HB, Gabriel R, Schmidt M, McIvor RS, Thrasher AJ, Qasim W. 2009. Sleeping beauty transposition from nonintegrating lentivirus. Molecular Therapy 17: 1197-1204. doi: 10.1038/mt.2009.94
35. Yolamanova M, Meier C, Shaytan AK, Vas V, Bertoncini CW, Arnold F, Zirafi O, Usmani SM, Müller JA, Sauter D, Goffinet C, Palesch D, Walther P, Roan NR, Geiger H, Lunov O, Simmet T, Bohne J, Schrezenmeier H, Schwarz K, et al. 2013. Peptide nanofibrils boost retroviral gene transfer and provide a rapid means for concentrating viruses. Nature Nanotechnology 8: 130-136. doi: 10.1038/nnano.2012.248