CRISPR genome engineering and viral gene delivery: A case of mutual attraction

Biotechnology Journal

Volumn 10, Issue 2, 2015, Pages 258-272

  Schmidt, Florian ^a   Grimm, Dirk ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

AAV (Adeno associated virus); CRISPR; Gene editing; Genome engineering; Viral vectors

Indexed keywords

CELL ENGINEERING; GENE TRANSFER; GENES; MACHINERY; MAMMALS; ONCOGENIC VIRUSES; SAFETY ENGINEERING;

ADENO-ASSOCIATED VIRUS; BASIC AND APPLIED RESEARCH; BIOLOGY AND MEDICINE; CRISPR; ENGINEERING MACHINERY; GENOME ENGINEERING; THERAPEUTIC STRATEGY; VIRAL VECTORS;

VECTORS;

ADENOVIRUS VECTOR; DNA; GUIDE RNA; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR; RETROVIRUS VECTOR; VIRUS VECTOR;

CAS9 GENE; CELL CULTURE; CHROMOSOME REARRANGEMENT; CRISPR GENE; DISEASE MODEL; GENE; GENE EXPRESSION; GENE LIBRARY; GENE TARGETING; GENETIC ENGINEERING; GENOME; HUMAN; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SAFETY; VIRAL GENE DELIVERY SYSTEM; VIRUS CAPSID; VIRUS GENOME; ADENOVIRIDAE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DEPENDOPARVOVIRUS; GENE TRANSFER; GENE VECTOR; GENETICS; LENTIVIRINAE; PROCEDURES; RETROVIRIDAE; VIRUS GENE;

ADENO-ASSOCIATED VIRUS; ANIMALIA; BACTERIA (MICROORGANISMS); MAMMALIA;

ADENOVIRIDAE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; DEPENDOVIRUS; GENE TRANSFER TECHNIQUES; GENES, VIRAL; GENETIC ENGINEERING; GENETIC VECTORS; LENTIVIRUS; RETROVIRIDAE;

EID: 84922720418     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400529     Document Type: Review

References (77)

1. Kim, D. H., Rossi, J. J., Strategies for silencing human disease using RNA interference. Nat. Rev. Genet. 2007, 8, 173-184.
2. Grimm, D., Kay, M. A., Therapeutic application of RNAi: Is mRNA targeting finally ready for prime time? J. Clin. Invest. 2007, 117, 3633-3641.
3. Grimm, D., Streetz, K. L., Jopling, C. L., Storm, T. A. et al., Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 2006, 441, 537-541.
4. Grimm, D., The dose can make the poison: Lessons learned from adverse in vivo toxicities caused by RNAi overexpression. Silence 2011, 2, 8.
5. Mussolino, C., Cathomen, T., TALE nucleases: Tailored genome engineering made easy. Curr. Opin. Biotechnol. 2012, 23, 644-650.
6. Joung, J. K., Sander, J. D., TALENs: A widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell. Biol. 2013, 14, 49-55.
7. Wirt, S. E., Porteus, M. H., Development of nuclease-mediated site-specific genome modification. Curr. Opin. Immunol. 2012, 24, 609-616.
8. Carroll, D., Genome engineering with targetable nucleases. Annu. Rev. Biochem. 2014, 83, 409-439.
9. Pennisi, E., The CRISPR craze. Science 2013, 341, 833-836.
10. Hsu, P. D., Lander, E. S., Zhang, F., Development and applications of CRISPR-Cas9 for genome engineering. Cell 2014, 157, 1262-1278.
11. Doudna, J. A., Charpentier, E., Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 2014, 346, 1258096.
12. Sander, J. D., Joung, J. K., CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 2014, 32, 347-355.
13. Sheridan, C., Gene therapy finds its niche. Nat. Biotechnol. 2011, 29, 121-128.
14. Thomas, C. E., Ehrhardt, A., Kay, M. A., Progress and problems with the use of viral vectors for gene therapy. Nat. Rev. Genet. 2003, 4, 346-358.
15. Waehler, R., Russell, S. J., Curiel, D. T., Engineering targeted viral vectors for gene therapy. Nat. Rev. Genet. 2007, 8, 573-587.
16. Wu, Z., Yang, H., Colosi, P., Effect of genome size on AAV vector packaging. Mol. Ther. 2010, 18, 80-86.
17. Grimm, D., Kay, M. A., From virus evolution to vector revolution: Use of naturally occurring serotypes of adeno-associated virus (AAV) as novel vectors for human gene therapy. Curr. Gene Ther. 2003, 3, 281-304.
18. Senis, E., Fatouros, C., Grosse, S., Wiedtke, E. et al., CRISPR/Cas9-mediated genome engineering: An adeno-associated viral (AAV) vector toolbox. Biotechnol. J. 2014, 9, 1402-1412.
19. Swiech, L., Heidenreich, M., Banerjee, A., Habib, N. et al., In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat. Biotechnol. 2014, 33, 102-106.
20. Gray, S. J., Foti, S. B., Schwartz, J. W., Bachaboina, L. et al., Optimizing promoters for recombinant adeno-associated virus-mediated gene expression in the peripheral and central nervous system using self-complementary vectors. Hum. Gene Ther. 2011, 22, 1143-1153.
21. McCarty, D. M., Monahan, P. E., Samulski, R. J., Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 2001, 8, 1248-1254.
22. Platt, R. J., Chen, S., Zhou, Y., Yim, M. J. et al., CRISPR-Cas9 Knockin Mice for Genome Editing and Cancer Modeling. Cell 2014, 159, 440-455.
23. Bouard, D., Alazard-Dany, D., Cosset, F. L., Viral vectors: From virology to transgene expression. Br. J. Pharmacol. 2009, 157, 153-165.
24. Candolfi, M., Curtin, J. F., Xiong, W. D., Kroeger, K. M. et al., Effective high-capacity gutless adenoviral vectors mediate transgene expression in human glioma cells. Mol. Ther. 2006, 14, 371-381.
25. Shalem, O., Sanjana, N. E., Hartenian, E., Shi, X. et al., Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014, 343, 84-87.
26. Cheng, R., Peng, J., Yan, Y., Cao, P. et al., Efficient gene editing in adult mouse livers via adenoviral delivery of CRISPR/Cas9. FEBS Lett. 2014, 588, 3954-3958.
27. Malina, A., Mills, J. R., Cencic, R., Yan, Y. et al., Repurposing CRISPR/Cas9 for in situ functional assays. Genes Dev. 2013, 27, 2602-2614.
28. Kabadi, A. M., Ousterout, D. G., Hilton, I. B., Gersbach, C. A., Multiplex CRISPR/Cas9-based genome engineering from a single lentiviral vector. Nucleic Acids Res. 2014, 42, e147.
29. ter Brake, O., t Hooft, K., Liu, Y. P., Centlivre, M. et al., Lentiviral vector design for multiple shRNA expression and durable HIV-1 inhibition. Mol. Ther. 2008, 16, 557-564.
30. Grimm, D., Production methods for gene transfer vectors based on adeno-associated virus serotypes. Methods 2002, 28, 146-157.
31. Dull, T., Zufferey, R., Kelly, M., Mandel, R. J. et al., A third-generation lentivirus vector with a conditional packaging system. J. Virol. 1998, 72, 8463-8471.
32. Trono, D., Lentiviral vectors: Turning a deadly foe into a therapeutic agent. Gene Ther. 2000, 7, 20-23.
33. Somia, N., Verma, I. M., Gene therapy: Trials and tribulations. Nat. Rev. Genet. 2000, 1, 91-99.
34. Cesana, D., Ranzani, M., Volpin, M., Bartholomae, C. et al., Uncovering and dissecting the genotoxicity of self-inactivating lentiviral vectors in vivo. Mol. Ther. 2014, 22, 774-785.
35. Biasco, L., Baricordi, C., Aiuti, A., Retroviral integrations in gene therapy trials. Mol. Ther. 2012, 20, 709-716.
36. High, K. H., Nathwani, A., Spencer, T., Lillicrap, D., Current status of haemophilia gene therapy. Haemophilia 2014, 20, 4, 43-49.
37. Niemeyer, G. P., Herzog, R. W., Mount, J., Arruda, V. R. et al., Long-term correction of inhibitor-prone hemophilia B dogs treated with liver-directed AAV2-mediated factor IX gene therapy. Blood 2009, 113, 797-806.
38. Heigwer, F., Kerr, G., Boutros, M., E-CRISP: Fast CRISPR target site identification. Nat. Methods 2014, 11, 122-123.
39. Doench, J. G., Hartenian, E., Graham, D. B., Tothova, Z. et al., Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol. 2014, 32, 1262-1267.
40. Gao, G., Vandenberghe, L. H., Wilson, J. M., New recombinant serotypes of AAV vectors. Curr. Gene Ther. 2005, 5, 285-297.
41. Kotterman, M. A., Schaffer, D. V., Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet. 2014, 15, 445-451.
42. Grimm, D., Lee, J. S., Wang, L., Desai, T. et al., In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 2008, 82, 5887-5911.
43. Koerber, J. T., Jang, J. H., Schaffer, D. V., DNA shuffling of adeno-associated virus yields functionally diverse viral progeny. Mol. Ther. 2008, 16, 1703-1709.
44. Li, W., Asokan, A., Wu, Z., Van Dyke, T. et al., Engineering and selection of shuffled AAV genomes: A new strategy for producing targeted biological nanoparticles. Mol. Ther. 2008, 16, 1252-1260.
45. Gray, S. J., Blake, B. L., Criswell, H. E., Nicolson, S. C. et al., Directed evolution of a novel adeno-associated virus (AAV) vector that crosses the seizure-compromised blood-brain barrier (BBB). Mol. Ther. 2010, 18, 570-578.
46. Kienle, E., Senis, E., Borner, K., Niopek, D. et al., Engineering and evolution of synthetic adeno-associated virus (AAV) gene therapy vectors via DNA family shuffling. J. Vis. Exp. 2012, 3819.
47. Muller, O. J., Kaul, F., Weitzman, M. D., Pasqualini, R. et al., Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat. Biotechnol. 2003, 21, 1040-1046.
48. Huttner, N. A., Girod, A., Perabo, L., Edbauer, D. et al., Genetic modifications of the adeno-associated virus type 2 capsid reduce the affinity and the neutralizing effects of human serum antibodies. Gene Ther. 2003, 10, 2139-2147.
49. Chiriaco, M., Farinelli, G., Capo, V., Zonari, E. et al., Dual-regulated lentiviral vector for gene therapy of X-linked chronic granulomatosis. Mol. Ther. 2014, 22, 1472-1483.
50. Qiao, C., Yuan, Z., Li, J., He, B. et al., Liver-specific microRNA-122 target sequences incorporated in AAV vectors efficiently inhibits transgene expression in the liver. Gene Ther. 2011, 18, 403-410.
51. Brown, B. D., Naldini, L., Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat. Rev. Genet. 2009, 10, 578-585.
52. Nissim, L., Perli, S. D., Fridkin, A., Perez-Pinera, P., Lu, T. K., Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol. Cell 2014, 54, 698-710.
53. Maggio, I., Holkers, M., Liu, J., Janssen, J. M. et al., Adenoviral vector delivery of RNA-guided CRISPR/Cas9 nuclease complexes induces targeted mutagenesis in a diverse array of human cells. Sci. Rep. 2014, 4, 5105.
54. Holkers, M., Maggio, I., Henriques, S. F., Janssen, J. M. et al., Adenoviral vector DNA for accurate genome editing with engineered nucleases. Nat. Methods 2014, 11, 1051-1057.
55. Zhou, Y., Zhu, S., Cai, C., Yuan, P. et al., High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature 2014, 509, 487-491.
56. Wang, T., Wei, J. J., Sabatini, D. M., Lander, E. S., Genetic screens in human cells using the CRISPR-Cas9 system. Science 2014, 343, 80-84.
57. Koike-Yusa, H., Li, Y., Tan, E. P., Velasco-Herrera Mdel, C., Yusa, K., Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat. Biotechnol. 2014, 32, 267-273.
58. Yan, T., Berry, S. E., Desai, A. B., Kinsella, T. J., DNA mismatch repair (MMR) mediates 6-thioguanine genotoxicity by introducing single-strand breaks to signal a G2-M arrest in MMR-proficient RKO cells. Clin. Cancer Res. 2003, 9, 2327-2334.
59. Gilbert, L. A., Horlbeck, M. A., Adamson, B., Villalta, J. E. et al., Genome-Scale CRISPR-Mediated Control of Gene Repression and Activation. Cell 2014, 159, 647-661.
60. Ding, Q., Strong, A., Patel, K. M., Ng, S. L. et al., Permanent alteration of PCSK9 with in vivo CRISPR-Cas9 genome editing. Circ. Res. 2014, 115, 488-492.
61. Fu, Y., Foden, J. A., Khayter, C., Maeder, M. L. et al., High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 2013, 31, 822-826.
62. Brown, B. D., Cantore, A., Annoni, A., Sergi, L. S. et al., A microRNA-regulated lentiviral vector mediates stable correction of hemophilia B mice. Blood 2007, 110, 4144-4152.
63. Brown, B. D., Venneri, M. A., Zingale, A., Sergi Sergi, L., Naldini, L., Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat. Med. 2006, 12, 585-591.
64. Heckl, D., Kowalczyk, M. S., Yudovich, D., Belizaire, R. et al., Generation of mouse models of myeloid malignancy with combinatorial genetic lesions using CRISPR-Cas9 genome editing. Nat. Biotechnol. 2014, 32, 941-946.
65. Torres, R., Martin, M. C., Garcia, A., Cigudosa, J. C. et al., Engineering human tumour-associated chromosomal translocations with the RNA-guided CRISPR-Cas9 system. Nat. Commun. 2014, 5, 3964.
66. Choi, P. S., Meyerson, M., Targeted genomic rearrangements using CRISPR/Cas technology. Nat. Commun. 2014, 5, 3728.
67. Blasco, R. B., Karaca, E., Ambrogio, C., Cheong, T. C. et al., Simple and Rapid In Vivo Generation of Chromosomal Rearrangements using CRISPR/Cas9 Technology. Cell Rep. 2014, 9, 1219-1227.
68. Maddalo, D., Manchado, E., Concepcion, C. P., Bonetti, C. et al., In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 2014, 516, 423-427.
69. Park, C. Y., Kim, J., Kweon, J., Son, J. S. et al., Targeted inversion and reversion of the blood coagulation factor 8 gene in human iPS cells using TALENs. Proc. Natl. Acad. Sci. USA 2014, 111, 9253-9258.
70. Ebina, H., Misawa, N., Kanemura, Y., Koyanagi, Y., Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus. Sci. Rep. 2013, 3, 2510.
71. Adachi, K., Enoki, T., Kawano, Y., Veraz, M., Nakai, H., Drawing a high-resolution functional map of adeno-associated virus capsid by massively parallel sequencing. Nat. Commun. 2014, 5, 3075.
72. Hesse, A., Kosmides, D., Kontermann, R. E., Nettelbeck, D. M., Tropism modification of adenovirus vectors by peptide ligand insertion into various positions of the adenovirus serotype 41 short-fiber knob domain. J. Virol. 2007, 81, 2688-2699.
73. Fu, Y., Sander, J. D., Reyon, D., Cascio, V. M., Joung, J. K., Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 2014, 32, 279-284.
74. Chen, B., Gilbert, L. A., Cimini, B. A., Schnitzbauer, J. et al., Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 2013, 155, 1479-1491.
75. Shen, B., Zhang, W., Zhang, J., Zhou, J. et al., Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat. Methods 2014, 11, 399-402.
76. Niopek, D., Benzinger, D., Roensch, J., Draebing, T. et al., Engineering light-inducible nuclear localization signals for precise spatiotemporal control of protein dynamics in living cells. Nat. Commun. 2014, 5, 4404.
77. Stieger, K., Belbellaa, B., Le Guiner, C., Moullier, P., Rolling, F., In vivo gene regulation using tetracycline-regulatable systems. Adv. Drug. Deliv. Rev. 2009, 61, 527-541.