Empower multiplex cell and tissue-specific CRISPR-mediated gene manipulation with self-cleaving ribozymes and tRNA

Nucleic Acids Research

Volumn 45, Issue 5, 2017, Pages

  Xu, Li ^a   Zhao, Lixia ^a   Gao, Yandi ^a   Xu, Jing ^a   Han, Renzhi ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; FOLLISTATIN; MYOSIN; RIBOZYME; TRANSFER RNA; DNA DIRECTED DNA POLYMERASE ALPHA; GUIDE RNA; HYBRID PROTEIN; SMALL NUCLEAR RNA; U6 SMALL NUCLEAR RNA;

ANIMAL CELL; ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DMD GENE; DNA DETERMINATION; DNA EXTRACTION; ELECTROPORATION; GASTROCNEMIUS MUSCLE; GENE; GENE EDITING; GENETIC MANIPULATION; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; MYBPC3 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL LINE; CRISPR CAS SYSTEM; CYTOLOGY; CYTOMEGALOVIRUS; GENETICS; HEK293 CELL LINE; HUMAN; LIVER; MACROPHAGE; METABOLISM; MYOBLAST; PROMOTER REGION; SKELETAL MUSCLE; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ANIMALS; CELL LINE; CRISPR-CAS SYSTEMS; CYTOMEGALOVIRUS; DNA POLYMERASE II; DYSTROPHIN; FOLLISTATIN; GENE EDITING; HEK293 CELLS; HUMANS; LIVER; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; MYOBLASTS; MYOSINS; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; RNA, CATALYTIC; RNA, GUIDE; RNA, SMALL NUCLEAR; RNA, TRANSFER; TRANSCRIPTIONAL ACTIVATION;

EID: 85018274309     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw1048     Document Type: Article

References (59)

1. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A. and Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
2. Mali, P., Yang, L.H., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E. and Church, G.M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
3. Cong, L., Ran, F.A., Cox, D., Lin, S.L., Barretto, R., Habib, N., Hsu, P.D., Wu, X.B., Jiang, W.Y., Marraffini, L.A. et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
4. Konermann, S., Brigham, M.D., Trevino, A.E., Hsu, P.D., Heidenreich, M., Cong, L., Platt, R.J., Scott, D.A., Church, G.M. and Zhang, F. (2013) Optical control of mammalian endogenous transcription and epigenetic states. Nature, 500, 472-476.
5. Maeder, M.L., Linder, S.J., Cascio, V.M., Fu, Y.F., Ho, Q.H. and Joung, J.K. (2013) CRISPR RNA-guided activation of endogenous human genes. Nat. Methods, 10, 977-979.
6. Perez-Pinera, P., Kocak, D.D., Vockley, C.M., Adler, A.F., Kabadi, A.M., Polstein, L.R., Thakore, P.I., Glass, K.A., Ousterout, D.G., Leong, K.W. et al. (2013) RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat. Methods, 10, 973-976.
7. Cheng, A.W., Wang, H.Y., Yang, H., Shi, L.Y., Katz, Y., Theunissen, T.W., Rangarajan, S., Shivalila, C.S., Dadon, D.B. and Jaenisch, R. (2013) Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res., 23, 1163-1171.
8. Qi, L.S., Larson, M.H., Gilbert, L.A., Doudna, J.A., Weissman, J.S., Arkin, A.P. and Lim, W.A. (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152, 1173-1183.
9. Larson, M.H., Gilbert, L.A., Wang, X.W., Lim, W.A., Weissman, J.S. and Qi, L.S. (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc., 8, 2180-2196.
10. Gilbert, L.A., Larson, M.H., Morsut, L., Liu, Z.R., Brar, G.A., Torres, S.E., Stern-Ginossar, N., Brandman, O., Whitehead, E.H., Doudna, J.A. et al. (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154, 442-451.
11. Bikard, D., Jiang, W.Y., Samai, P., Hochschild, A., Zhang, F. and Marraffini, L.A. (2013) Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res., 41, 7429-7437.
12. Zalatan, J.G., Lee, M.E., Almeida, R., Gilbert, L.A., Whitehead, E.H., La Russa, M., Tsai, J.C., Weissman, J.S., Dueber, J.E., Qi, L.S. et al. (2015) Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell, 160, 339-350.
13. Konermann, S., Brigham, M.D., Trevino, A.E., Joung, J., Abudayyeh, O.O., Barcena, C., Hsu, P.D., Habib, N., Gootenberg, J.S., Nishimasu, H. et al. (2015) Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature, 517, 583-588.
14. Wang, H., Yang, H., Shivalila, C.S., Dawlaty, M.M., Cheng, A.W., Zhang, F. and Jaenisch, R. (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 153, 910-918.
15. Jinek, M., East, A., Cheng, A., Lin, S., Ma, E. and Doudna, J. (2013) RNA-programmed genome editing in human cells. Elife, 2, e00471.
16. Li, J.F., Norville, J.E., Aach, J., McCormack, M., Zhang, D.D., Bush, J., Church, G.M. and Sheen, J. (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol., 31, 688-691.
17. Zhou, H.B., Liu, B., Weeks, D.P., Spalding, M.H. and Yang, B. (2014) Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res., 42, 10903-10914.
18. Shan, Q.W., Wang, Y.P., Li, J., Zhang, Y., Chen, K.L., Liang, Z., Zhang, K., Liu, J.X., Xi, J.J., Qiu, J.L. et al. (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol., 31, 686-688.
19. Nissim, L., Perli, S.D., Fridkin, A., Perez-Pinera, P. and Lu, T.K. (2014) Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol. Cell, 54, 698-710.
20. Tsai, S.Q., Wyvekens, N., Khayter, C., Foden, J.A., Thapar, V., Reyon, D., Goodwin, M.J., Aryee, M.J. and Joung, J.K. (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol., 32, 569-576.
21. Carter, C.W. Jr and Wolfenden, R. (2015) tRNA acceptor stem and anticodon bases form independent codes related to protein folding. Proc. Natl. Acad. Sci. U.S.A., 112, 7489-7494.
22. Port, F. and Bullock, S.L. (2016) Augmenting CRISPR applications in Drosophila with tRNA-flanked sgRNAs. Nat. Methods, 13, 852-854.
23. Qi, W.W., Zhu, T., Tian, Z.R., Li, C.B., Zhang, W. and Song, R.T. (2016) High-efficiency CRISPR/Cas9 multiplex gene editing using the glycine tRNA-processing system-based strategy in maize. BMC Biotechnol., 16, 58.
24. Mefferd, A.L., Kornepati, A.V.R., Bogerd, H.P., Kennedy, E.M. and Cullen, B.R. (2015) Expression of CRISPR/Cas single guide RNAs using small tRNA promoters. RNA, 21, 1683-1689.
25. Port, F. and Bullock, S.L. (2016) Expansion of the CRISPR toolbox in an animal with tRNA-flanked Cas9 and Cpf1 gRNAs. Bioarxiv, doi: 10.1101/046417.
26. Kruger, K., Grabowski, P.J., Zaug, A.J., Sands, J., Gottschling, D.E. and Cech, T.R. (1982) Self-splicing RNA: Autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell, 31, 147-157.
27. Gao, Y. and Zhao, Y. (2014) Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J. Integr. Plant Biol., 56, 343-349.
28. Zhang, W.W. and Matlashewski, G. (2015) CRISPR-Cas9-mediated genome editing in Leishmania donovani. Mbio, 6, e00861.
29. Yoshioka, S., Fujii, W., Ogawa, T., Sugiura, K. and Naito, K. (2015) Development of a mono-promoter-driven CRISPR/Cas9 system in mammalian cells. Sci. Rep.-UK, 5, 18341.
30. Xu, L., Park, K.H., Zhao, L., Xu, J., El Refaey, M., Gao, Y., Zhu, H., Ma, J. and Han, R. (2015) CRISPR-mediated genome editing restores dystrophin expression and function in mdx mice. Mol. Ther., 24, 564-569.
31. Nelson, C.E., Hakim, C.H., Ousterout, D.G., Thakore, P.I., Moreb, E.A., Castellanos Rivera, R.M., Madhavan, S., Pan, X., Ran, F.A., Yan, W.X. et al. (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science, 351, 403-407.
32. Long, C., Amoasii, L., Mireault, A.A., McAnally, J.R., Li, H., Sanchez-Ortiz, E., Bhattacharyya, S., Shelton, J.M., Bassel-Duby, R. and Olson, E.N. (2016) Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science, 351, 400-403.
33. Tabebordbar, M., Zhu, K., Cheng, J.K., Chew, W.L., Widrick, J.J., Yan, W.X., Maesner, C., Wu, E.Y., Xiao, R., Ran, F.A. et al. (2016) In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science, 351, 407-411.
34. Xu, L., Zhao, P., Mariano, A. and Han, R. (2013) Targeted myostatin gene editing in multiple mammalian species directed by a single pair of TALE nucleases. Mol. Ther. Nucleic Acids, 2, e112.
35. Xu, J., El Refaey, M., Xu, L., Zhao, L., Gao, Y., Floyd, K., Karaze, T., Janssen, P.M.L. and Han, R. (2015) Genetic disruption of Ano5 in mice does not recapitulate human ANO5-deficient muscular dystrophy. Skelet. Muscle, 5, 43.
36. Sweeney, J.A. and Hennessey, J.P. Jr (2002) Evaluation of accuracy and precision of adenovirus absorptivity at 260 nm under conditions of complete DNA disruption. Virology, 295, 284-288.
37. Scott, W.G., Murray, J.B., Arnold, J.R.P., Stoddard, B.L. and Klug, A. (1996) Capturing the structure of a catalytic RNA intermediate: The hammerhead ribozyme. Science, 274, 2065-2069.
38. Nakano, S., Chadalavada, D.M. and Bevilacqua, P.C. (2000) General acid-base catalysis in the mechanism of a hepatitis delta virus ribozyme. Science, 287, 1493-1497.
39. Xie, K., Minkenberg, B. and Yang, Y. (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. U.S.A., 112, 3570-3575.
40. Carrier, L., Bonne, G., Bahrend, E., Yu, B., Richard, P., Niel, F., Hainque, B., Cruaud, C., Gary, F., Labeit, S. et al. (1997) Organization and sequence of human cardiac myosin binding protein C gene (MYBPC3) and identification of mutations predicted to produce truncated proteins in familial hypertrophic cardiomyopathy. Circ. Res, 80, 427-434.
41. Nishimasu, H., Ran, F.A., Hsu, P.D., Konermann, S., Shehata, S.I., Dohmae, N., Ishitani, R., Zhang, F. and Nureki, O. (2014) Crystal structure of Cas9 in complex with guide RNA and Target DNA. Cell, 156, 935-949.
42. Lee, S.J. and McPherron, A.C. (2001) Regulation of myostatin activity and muscle growth. Proc. Natl. Acad. Sci. U.S.A., 98, 9306-9311.
43. Hilton, I.B., D'Ippolito, A.M., Vockley, C.M., Thakore, P.I., Crawford, G.E., Reddy, T.E. and Gersbach, C.A. (2015) Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol., 33, 510-517.
44. Yin, H., Xue, W., Chen, S., Bogorad, R.L., Benedetti, E., Grompe, M., Koteliansky, V., Sharp, P.A., Jacks, T. and Anderson, D.G. (2014) Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat. Biotechnol., 32, 551-553.
45. Young, C.S., Hicks, M.R., Ermolova, N.V., Nakano, H., Jan, M., Younesi, S., Karumbayaram, S., Kumagai-Cresse, C., Wang, D., Zack, J.A. et al. (2016) A single CRISPR-Cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells. Cell Stem Cell, 18, 533-540.
46. Iyombe-Engembe, J.P., Ouellet, D.L., Barbeau, X., Rousseau, J., Chapdelaine, P., Lague, P. and Tremblay, J.P. (2016) Efficient restoration of the dystrophin gene reading frame and protein structure in DMD myoblasts using the CinDel method. Mol. Ther. Nucleic Acids, 5, e283.
47. Lee, C.M., Cradick, T.J., Fine, E.J. and Bao, G. (2016) Nuclease target site selection for maximizing on-target activity and minimizing off-target effects in genome editing. Mol. Ther., 24, 475-487.
48. Paule, M.R. and White, R.J. (2000) Survey and summary: Transcription by RNA polymerases I and III. Nucleic Acids Res., 28, 1283-1298.
49. Nielsen, S., Yuzenkova, Y. and Zenkin, N. (2013) Mechanism of eukaryotic RNA polymerase III transcription termination. Science, 340, 1577-1580.
50. Chen, B., Hu, J., Almeida, R., Liu, H., Balakrishnan, S., Covill-Cooke, C., Lim, W.A. and Huang, B. (2016) Expanding the CRISPR imaging toolset with Staphylococcus aureus Cas9 for simultaneous imaging of multiple genomic loci. Nucleic Acids Res., 44, e75.
51. Chen, B., Gilbert, L.A., Cimini, B.A., Schnitzbauer, J., Zhang, W., Li, G.W., Park, J., Blackburn, E.H., Weissman, J.S., Qi, L.S. et al. (2013) Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 155, 1479-1491.
52. Dang, Y., Jia, G., Choi, J., Ma, H., Anaya, E., Ye, C., Shankar, P. and Wu, H. (2015) Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency. Genome Biol., 16, 280.
53. Hsu, P.D., Scott, D.A., Weinstein, J.A., Ran, F.A., Konermann, S., Agarwala, V., Li, Y., Fine, E.J., Wu, X., Shalem, O. et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol., 31, 827-832.
54. Medina, M.F. and Joshi, S. (1999) RNA-polymerase III-driven expression cassettes in human gene therapy. Curr. Opin. Mol. Ther., 1, 580-594.
55. White, R.J. (2011) Transcription by RNA polymerase III: More complex than we thought. Nat. Rev. Genet., 12, 459-463.
56. Dieci, G., Fiorino, G., Castelnuovo, M., Teichmann, M. and Pagano, A. (2007) The expanding RNA polymerase III transcriptome. Trends Genet.: TIG, 23, 614-622.
57. Salva, M.Z., Himeda, C.L., Tai, P.W., Nishiuchi, E., Gregorevic, P., Allen, J.M., Finn, E.E., Nguyen, Q.G., Blankinship, M.J., Meuse, L. et al. (2007) Design of tissue-specific regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol. Ther., 15, 320-329.
58. Eagle, M., Baudouin, S.V., Chandler, C., Giddings, D.R., Bullock, R. and Bushby, K. (2002) Survival in Duchenne muscular dystrophy: Improvements in life expectancy since 1967 and the impact of home nocturnal ventilation. Neuromuscul. Disord., 12, 926-929.
59. Nigro, G., Comi, L.I., Politano, L. and Bain, R.J. (1990) The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int. J. Cardiol., 26, 271-277.