Advances in engineering the fly genome with the CRISPR-Cas system

Genetics

Volumn 208, Issue 1, 2018, Pages 1-18

  Bier, Ethan ^a   Harrison, Melissa M ^b   O’connor Giles, Kate M ^c   Wildonger, Jill ^c  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

CRISPR Cas; Drosophila; FlyBook; Gene drive; Gene editing; Genome engineering

Indexed keywords

CAS9 PROTEIN; CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; CRISPR ASSOCIATED PROTEIN; DNA; GENOMIC RNA; NUCLEAR PROTEIN; PROTEIN; RNA; UNCLASSIFIED DRUG; GUIDE RNA;

ARTICLE; BACTERIAL IMMUNITY; CELL CULTURE; CELL REGENERATION; CRISPR CAS SYSTEM; DNA END JOINING REPAIR; DNA MODIFICATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DROSOPHILA; GENE EDITING; GENE EXPRESSION; GENE TARGETING; GENETIC ANALYSIS; GENETIC ENGINEERING; GERM LINE; GERMLINE MUTATION; INSECT GENOME; MOSQUITO VECTOR; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SITE DIRECTED MUTAGENESIS; TRANSGENICS; ANIMAL; BACTERIUM; GENETICS; GENOME; GENOMICS; IMMUNOLOGY; PROCEDURES;

ANIMALS; BACTERIA; CRISPR-CAS SYSTEMS; DNA REPAIR; DROSOPHILA; GENE EDITING; GENE TARGETING; GENETIC ENGINEERING; GENOME; GENOMICS; RNA, GUIDE;

EID: 85040129921     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.117.1113     Document Type: Article

References (128)

1. Abudayyeh, O. O., J. S. Gootenberg, S. Konermann, J. Joung, I. M. Slaymaker et al., 2016 C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353: aaf5573.
2. Akbari, O. S., H. J. Bellen, E. Bier, S. L. Bullock, A. Burt et al., 2015 Safeguarding gene drive experiments in the laboratory. Science 349: 927-929
3. Anand, R. P., S. T. Lovett, and J. E. Haber, 2013 Break-induced DNA replication. Cold Spring Harb. Perspect. Biol. 5: a010397.
4. Banga, S. S., and J. B. Boyd, 1992 Oligonucleotide-directed sitespecific mutagenesis in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 89: 1735-1739
5. Barrangou, R., C. Fremaux, H. Deveau, M. Richards, P. Boyaval et al., 2007 CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712
6. Bassett, A., and J. L. Liu, 2014 CRISPR/Cas9 mediated genome engineering in Drosophila. Methods 69: 128-136
7. Bassett, A. R., C. Tibbit, C. P. Ponting, and J. L. Liu, 2013 Highly efficient targeted mutagenesis of Drosophila with the CRISPR/ Cas9 system. Cell Rep. 4: 220-228
8. Bassett, A. R., L. Kong, and J. L. Liu, 2015 A genome-wide CRISPR library for high-throughput genetic screening in Drosophila cells. J. Genet. Genomics 42: 301-309
9. Baudat, F., Y. Imai, and B. de Massy, 2013 Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet. 14: 794-806
10. Beumer, K. J., J. K. Trautman, K. Mukherjee, and D. Carroll, 2013 Donor DNA utilization during gene targeting with zincfinger nucleases. G3 (Bethesda) 3: 657-664
11. Beumer, K. J., J. K. Trautman, A. Bozas, J. L. Liu, J. Rutter et al., 2008 Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases. Proc. Natl. Acad. Sci. USA 105: 19821-19826
12. Bibikova, M., M. Golic, K. G. Golic, and D. Carroll, 2002 Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161: 1169-1175
13. Bischof, J., R. K. Maeda, M. Hediger, F. Karch, and K. Basler, 2007 An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104: 3312-3317
14. Bottcher, R., M. Hollmann, K. Merk, V. Nitschko, C. Obermaier et al., 2014 Efficient chromosomal gene modification with CRISPR/cas9 and PCR-based homologous recombination donors in cultured Drosophila cells. Nucleic Acids Res. 42: e89.
15. Bozas, A., K. J. Beumer, J. K. Trautman, and D. Carroll, 2009 Genetic analysis of zinc-finger nuclease-induced gene targeting in Drosophila. Genetics 182: 641-651
16. Burt, A., 2003 Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. Biol. Sci. 270: 921-928
17. Burt, A., 2014 Heritable strategies for controlling insect vectors of disease. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369: 20130432.
18. Chapman, J. R., M. R. Taylor, and S. J. Boulton, 2012 Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47: 497-510
19. Chavez, A., J. Scheiman, S. Vora, B. W. Pruitt, M. Tuttle et al., 2015 Highly efficient Cas9-mediated transcriptional programming. Nat. Methods 12: 326-328
20. Chen, B., L. A. Gilbert, B. A. Cimini, J. Schnitzbauer, W. Zhang et al., 2013 Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155: 1479-1491
21. Chen, B., J. Hu, R. Almeida, H. Liu, S. Balakrishnan et al., 2016 Expanding the CRISPR imaging toolset with Staphylococcus aureus Cas9 for simultaneous imaging of multiple genomic loci. Nucleic Acids Res. 44: e75.
22. Cheng, A. W., N. Jillette, P. Lee, D. Plaskon, Y. Fujiwara et al., 2016 Casilio: a versatile CRISPR-Cas9-Pumilio hybrid for gene regulation and genomic labeling. Cell Res. 26: 254-257
23. Cho, S. W., S. Kim, Y. Kim, J. Kweon, H. S. Kim et al., 2014 Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 24: 132-141
24. Cong, L., F. A. Ran, D. Cox, S. Lin, R. Barretto et al., 2013 Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823
25. Curtis, C. F., 1968 Possible use of translocations to fix desirable genes in insect pest populations. Nature 218: 368-369
26. Deredec, A., A. Burt, and H. C. Godfray, 2008 The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179: 2013-2026
27. Diao, F., H. Ironfield, H. Luan, W. C. Shropshire, J. Ewer et al., 2015 Plug-and-play genetic access to drosophila cell types using exchangeable exon cassettes. Cell Rep. 10: 1410-1421
28. DiCarlo, J. E., A. Chavez, S. L. Dietz, K. M. Esvelt, and G. M. Church, 2015 RNA-guided gene drives can efficiently bias inheritance in wild yeast. bioRxiv, doi: https://doi.org/10.1101/013896.
29. Do, A. T., J. T. Brooks, M. K. Le Neveu, and J. R. LaRocque, 2014 Double-strand break repair assays determine pathway choice and structure of gene conversion events in Drosophila melanogaster. G3 4: 425-432
30. Doench, J. G., N. Fusi, M. Sullender, M. Hegde, E. W. Vaimberg et al., 2016 Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat. Biotechnol. 34: 184-191
31. Dominguez, A. A., W. A. Lim, and L. S. Qi, 2016 Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation. Nat. Rev. Mol. Cell Biol. 17: 5-15
32. Drury, D. W., A. L. Dapper, D. J. Siniard, G. E. Zentner, and M. J. Wade, 2017 CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Sci. Adv. 3: e1601910.
33. Esvelt, K. M., P. Mali, J. L. Braff, M. Moosburner, S. J. Yaung et al., 2013 Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat. Methods 10: 1116-1121
34. Farboud, B., and B. J. Meyer, 2015 Dramatic enhancement of genome editing by CRISPR/Cas9 through improved guide RNA design. Genetics 199: 959-971
35. Fu, Y., P. P. Rocha, V. M. Luo, R. Raviram, Y. Deng et al., 2016 CRISPR-dCas9 and sgRNA scaffolds enable dual-colour live imaging of satellite sequences and repeat-enriched individual loci. Nat. Commun. 7: 11707.
36. Gantz, V. M., and E. Bier, 2015 The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science 348: 442-444
37. Gantz, V. M., and E. Bier, 2016 The dawn of active genetics. Bioessays 38: 50-63
38. Gantz, V. M., N. Jasinskiene, O. Tatarenkova, A. Fazekas, V. M. Macias et al., 2015 Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc. Natl. Acad. Sci. USA 112: E6736-E6743.
39. Gao, Y., and Y. Zhao, 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
40. Gasiunas, G., R. Barrangou, P. Horvath, and V. Siksnys, 2012 Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. USA 109: E2579-E2586.
41. Ge, D. T., C. Tipping, M. H. Brodsky, and P. D. Zamore, 2016 Rapid screening for CRISPR-directed editing of the Drosophila genome using white coconversion. G3 (Bethesda) 6: 3197-3206
42. Ghosh, S., C. Tibbit, and J. L. Liu, 2016 Effective knockdown of Drosophila long non-coding RNAs by CRISPR interference. Nucleic Acids Res. 44: e84.
43. Gloor, G. B., N. A. Nassif, D. M. Johnson-Schlitz, C. R. Preston, and W. R. Engels, 1991 Targeted gene replacement in Drosophila via P element-induced gap repair. Science 253: 1110-1117
44. Gong, W. J., and K. G. Golic, 2003 Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl. Acad. Sci. USA 100: 2556-2561.
45. Gratz, S. J., A. M. Cummings, J. N. Nguyen, D. C. Hamm, L. K. Donohue et al., 2013 Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194: 1029-1035
46. Gratz, S. J., F. P. Ukken, C. D. Rubinstein, G. Thiede, L. K. Donohue et al., 2014 Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 196: 961-971
47. Gratz, S. J., M. M. Harrison, J. Wildonger, and K. M. O’Connor-Giles, 2015a Precise genome editing of Drosophila with CRISPR RNA-guided Cas9. Methods Mol. Biol. 1311: 335-348
48. Gratz, S. J., C. D. Rubinstein, M. M. Harrison, J. Wildonger, and K. M. O’Connor-Giles, 2015b CRISPR-Cas9 genome editing in Drosophila. Curr. Protoc. Mol. Biol. 111: 31. 2. 1-31. 2. 20.
49. Haber, J. E., 2015 TOPping off meiosis. Mol. Cell 57: 577-581
50. Haeussler, M., K. Schonig, H. Eckert, A. Eschstruth, J. Mianne et al., 2016 Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biol. 17: 148.
51. Hammond, A., R. Galizi, K. Kyrou, A. Simoni, C. Siniscalchi et al., 2016 A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat. Biotechnol. 34: 78-83
52. Harrison, M. M., B. V. Jenkins, K. M. O’Connor-Giles, and J. Wildonger, 2014 A CRISPR view of development. Genes Dev. 28: 1859-1872
53. Hartenian, E., and J. G. Doench, 2015 Genetic screens and functional genomics using CRISPR/Cas9 technology. FEBS J. 282: 1383-1393
54. Hemphill, J., E. K. Borchardt, K. Brown, A. Asokan, and A. Deiters, 2015 Optical control of CRISPR/Cas9 gene editing. J. Am. Chem. Soc. 137: 5642-5645
55. Hou, Z., Y. Zhang, N. E. Propson, S. E. Howden, L. F. Chu et al., 2013 Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 110: 15644-15649
56. Housden, B. E., and N. Perrimon, 2016a Cas9-mediated genome engineering in Drosophila melanogaster. Cold Spring Harb. Protoc. 2016: pdb. top086843.
57. Housden, B. E., and N. Perrimon, 2016b Comparing CRISPR and RNAi-based screening technologies. Nat. Biotechnol. 34: 621-623
58. Housden, B. E., and N. Perrimon, 2016c Design and generation of donor constructs for genome engineering in Drosophila. Cold Spring Harb. Protoc. 2016: pdb. prot090787.
59. Housden, B. E., and N. Perrimon, 2016d Detection of indel mutations in Drosophila by high-resolution melt analysis (HRMA). Cold Spring Harb. Protoc. 2016: pdb. prot090795.
60. Housden, B. E., S. Lin, and N. Perrimon, 2014 Cas9-based genome editing in Drosophila. Methods Enzymol. 546: 415-439
61. Housden, B. E., A. J. Valvezan, C. Kelley, R. Sopko, Y. Hu et al., 2015 Identification of potential drug targets for tuberous sclerosis complex by synthetic screens combining CRISPR-based knockouts with RNAi. Sci. Signal. 8: rs9.
62. Housden, B. E., Y. Hu, and N. Perrimon, 2016 Design and generation of Drosophila single guide RNA expression constructs. Cold Spring Harb. Protoc. 2016: pdb. prot090779.
63. Huang, J., W. Zhou, A. M. Watson, Y. N. Jan, and Y. Hong, 2008 Efficient ends-out gene targeting in Drosophila. Genetics 180: 703-707
64. Huang, J., W. Zhou, W. Dong, A. M. Watson, and Y. Hong, 2009 From the cover: directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc. Natl. Acad. Sci. USA 106: 8284-8289
65. Isaacs, A. T., N. Jasinskiene, M. Tretiakov, I. Thiery, A. Zettor et al., 2012 Transgenic Anopheles stephensi coexpressing singlechain antibodies resist Plasmodium falciparum development. Proc. Natl. Acad. Sci. USA 109: E1922-E1930.
66. Ishino, Y., H. Shinagawa, K. Makino, M. Amemura, and A. Nakata, 1987 Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169: 5429-5433.
67. James, A. A., 2005 Gene drive systems in mosquitoes: rules of the road. Trends Parasitol. 21: 64-67
68. Jinek, M., K. Chylinski, I. Fonfara, M. Hauer, J. A. Doudna et al., 2012 A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821
69. Jinek, M., A. East, A. Cheng, S. Lin, E. Ma et al., 2013 RNAprogrammed genome editing in human cells. Elife 2: e00471.
70. Joyce, E. F., A. Paul, K. E. Chen, N. Tanneti, and K. S. McKim, 2012 Multiple barriers to nonhomologous DNA end joining during meiosis in Drosophila. Genetics 191: 739-746
71. Kamiyama, D., S. Sekine, B. Barsi-Rhyne, J. Hu, B. Chen et al., 2016 Versatile protein tagging in cells with split fluorescent protein. Nat. Commun. 7: 11046.
72. Keeney, S., J. Lange, and N. Mohibullah, 2014 Self-organization of meiotic recombination initiation: general principles and molecular pathways. Annu. Rev. Genet. 48: 187-214
73. Kleinstiver, B. P., M. S. Prew, S. Q. Tsai, V. V. Topkar, N. T. Nguyen et al., 2015 Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523: 481-485
74. Kleinstiver, B. P., S. Q. Tsai, M. S. Prew, N. T. Nguyen, M. M. Welch et al., 2016 Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat. Biotechnol. 34: 869-874
75. Koike-Yusa, H., Y. Li, E. P. Tan, C. Velasco-Herrera Mdel, and K. Yusa, 2014 Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat. Biotechnol. 32: 267-273
76. Komor, A. C., Y. B. Kim, M. S. Packer, J. A. Zuris, and D. R. Liu, 2016 Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533: 420-424
77. Kunzelmann, S., R. Bottcher, I. Schmidts, and K. Forstemann, 2016 A comprehensive toolbox for genome editing in cultured Drosophila melanogaster cells. G3 6: 1777-1785
78. Lamb, A. M., E. A. Walker, and P. J. Wittkopp, 2017 Tools and strategies for scarless allele replacement in Drosophila using CRISPR/Cas9. Fly (Austin) 11: 53-64
79. Lee, H., C. J. McManus, D. Y. Cho, M. Eaton, F. Renda et al., 2014 DNA copy number evolution in Drosophila cell lines. Genome Biol. 15: R70.
80. Lin, C. C., and C. J. Potter, 2016a Editing transgenic DNA components by inducible gene replacement in Drosophila melanogaster. Genetics 203: 1613-1628
81. Lin, C. C., and C. J. Potter, 2016b Non-Mendelian dominant maternal effects caused by CRISPR/Cas9 transgenic components in Drosophila melanogaster. G3 6: 3685-3691
82. Lin, S., B. Ewen-Campen, X. Ni, B. E. Housden, and N. Perrimon, 2015 In vivo transcriptional activation using CRISPR/Cas9 in Drosophila. Genetics 201: 433-442
83. Liu, J., C. Li, Z. Yu, P. Huang, H. Wu et al., 2012 Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy. J. Genet. Genomics 39: 209-215
84. Ma, H., A. Naseri, P. Reyes-Gutierrez, S. A. Wolfe, S. Zhang et al., 2015 Multicolor CRISPR labeling of chromosomal loci in human cells. Proc. Natl. Acad. Sci. USA 112: 3002-3007
85. Ma, H., L. C. Tu, A. Naseri, M. Huisman, S. Zhang et al., 2016a CRISPRCas9 nuclear dynamics and target recognition in living cells. J. Cell Biol. 214: 529-537
86. Ma, H., L. C. Tu, A. Naseri, M. Huisman, S. Zhang et al., 2016b Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow. Nat. Biotechnol. 34: 528-530
87. Makarova, K. S., D. H. Haft, R. Barrangou, S. J. Brouns, E. Charpentier et al., 2011 Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9: 467-477
88. Makarova, K. S., Y. I. Wolf, O. S. Alkhnbashi, F. Costa, S. A. Shah et al., 2015 An updated evolutionary classification of CRISPRCas systems. Nat. Rev. Microbiol. 13: 722-736
89. Mali, P., J. Aach, P. B. Stranges, K. M. Esvelt, M. Moosburner et al., 2013a CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31: 833-838
90. Mali, P., L. Yang, K. M. Esvelt, J. Aach, M. Guell et al., 2013b RNA-guided human genome engineering via Cas9. Science 339: 823-826
91. Malina, A., C. J. Cameron, F. Robert, M. Blanchette, J. Dostie et al., 2015 PAM multiplicity marks genomic target sites as inhibitory to CRISPR-Cas9 editing. Nat. Commun. 6: 10124.
92. McKenna, A., G. M. Findlay, J. A. Gagnon, M. S. Horwitz, A. F. Schier et al., 2016 Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science 353: aaf7907.
93. Moreno-Mateos, M. A., C. E. Vejnar, J. D. Beaudoin, J. P. Fernandez, E. K. Mis et al., 2015 CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo. Nat. Methods 12: 982-988
94. Nelles, D. A., M. Y. Fang, S. Aigner, and G. W. Yeo, 2015 Applications of Cas9 as an RNA-programmed RNA-binding protein. Bioessays 37: 732-739
95. Nelles, D. A., M. Y. Fang, M. R. O’Connell, J. L. Xu, S. J. Markmiller et al., 2016 Programmable RNA tracking in live cells with CRISPR/Cas9. Cell 165: 488-496
96. Nihongaki, Y., F. Kawano, T. Nakajima, and M. Sato, 2015 Photoactivatable CRISPR-Cas9 for optogenetic genome editing. Nat. Biotechnol. 33: 755-760
97. Noma, K., and Y. Jin, 2015 Optogenetic mutagenesis in Caenorhabditis elegans. Nat. Commun. 6: 8868.
98. North, A., A. Burt, H. C. Godfray, and Y. Buckley, 2013 Modelling the spatial spread of a homing endonuclease gene in a mosquito population. J. Appl. Ecol. 50: 1216-1225
99. O’Connell, M. R., B. L. Oakes, S. H. Sternberg, A. East-Seletsky, M. Kaplan et al., 2014 Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516: 263-266
100. Polstein, L. R., and C. A. Gersbach, 2015 A light-inducible CRISPR-Cas9 system for control of endogenous gene activation. Nat. Chem. Biol. 11: 198-200
101. Port, F., and S. L. Bullock, 2016a Augmenting CRISPR applications in Drosophila with tRNA-flanked sgRNAs. Nat. Methods 13: 852-854
102. Port, F., and S. L. Bullock, 2016b Creating heritable mutations in Drosophila with CRISPR-Cas9. Methods Mol. Biol. 1478: 145-160.
103. Port, F., H. M. Chen, T. Lee, and S. L. Bullock, 2014 Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc. Natl. Acad. Sci. USA 111: E2967-E2976.
104. Qi, L. S., M. H. Larson, L. A. Gilbert, J. A. Doudna, J. S. Weissman et al., 2013 Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152: 1173-1183
105. Ran, F. A., P. D. Hsu, C. Y. Lin, J. S. Gootenberg, S. Konermann et al., 2013 Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389
106. Ran, F. A., L. Cong, W. X. Yan, D. A. Scott, J. S. Gootenberg et al., 2015 In vivo genome editing using Staphylococcus aureus Cas9. Nature 520: 186-191
107. Ren, X., Z. Yang, D. Mao, Z. Chang, H. H. Qiao et al., 2014 Performance of the Cas9 nickase system in Drosophila melanogaster. G3 4: 1955-1962.
108. Ren, X., J. Sun, B. E. Housden, Y. Hu, C. Roesel et al., 2013 Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9. Proc. Natl. Acad. Sci. USA 110: 19012-19017
109. Richardson, K. M., M. Schiffer, P. C. Griffin, S. F. Lee, and A. A. Hoffmann, 2016 Tropical Drosophila pandora carry Wolbachia infections causing cytoplasmic incompatibility or male killing. Evolution 70: 1791-1802
110. Rong, Y. S., and K. G. Golic, 2000 Gene targeting by homologous recombination in Drosophila. Science 288: 2013-2018
111. Sekelsky, J., 2017 DNA repair in Drosophila: mutagens, models, and missing genes. Genetics 205: 471-490
112. Shalem, O., N. E. Sanjana, E. Hartenian, X. Shi, D. A. Scott et al., 2014 Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343: 84-87
113. Shalem, O., N. E. Sanjana, and F. Zhang, 2015 High-throughput functional genomics using CRISPR-Cas9. Nat. Rev. Genet. 16: 299-311
114. Shechner, D. M., E. Hacisuleyman, S. T. Younger, and J. L. Rinn, 2015 Multiplexable, locus-specific targeting of long RNAs with CRISPR-Display. Nat. Methods 12: 664-670
115. Shmakov, S., O. O. Abudayyeh, K. S. Makarova, Y. I. Wolf, J. S. Gootenberg et al., 2015 Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol. Cell 60: 385-397
116. Sternberg, S. H., S. Redding, M. Jinek, E. C. Greene, and J. A. Doudna, 2014 DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507: 62-67
117. Tanenbaum, M. E., L. A. Gilbert, L. S. Qi, J. S. Weissman, and R. D. Vale, 2014 A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159: 635-646.
118. Unckless, R. L., A. G. Clark, and P. W. Messer, 2017 Evolution of resistance against CRISPR/Cas9 gene drive. Genetics 205: 827-841.
119. van der Oost, J., M. M. Jore, E. R. Westra, M. Lundgren, and S. J. Brouns, 2009 CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci. 34: 401-407
120. Wang, S., J. H. Su, F. Zhang, and X. Zhuang, 2016 An RNAaptamer-based two-color CRISPR labeling system. Sci. Rep. 6: 26857.
121. Wang, T., J. J. Wei, D. M. Sabatini, and E. S. Lander, 2014 Genetic screens in human cells using the CRISPR-Cas9 system. Science 343: 80-84
122. Ward, J. D., 2015 Rapid and precise engineering of the Caenorhabditis elegans genome with lethal mutation co-conversion and inactivation of NHEJ repair. Genetics 199: 363-377
123. Xie, K., B. Minkenberg, and Y. Yang, 2015 Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. USA 112: 3570-3575
124. Xue, Z., M. Ren, M. Wu, J. Dai, Y. S. Rong et al., 2014 Efficient gene knock-out and knock-in with transgenic Cas9 in Drosophila. G3 4: 925-929
125. Zalatan, J. G., M. E. Lee, R. Almeida, L. A. Gilbert, E. H. Whitehead et al., 2015 Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell 160: 339-350
126. Zetsche, B., J. S. Gootenberg, O. O. Abudayyeh, I. M. Slaymaker, K. S. Makarova et al., 2015a Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163: 759-771
127. Zetsche, B., S. E. Volz, and F. Zhang, 2015b A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat. Biotechnol. 33: 139-142
128. Zhou, Y., S. Zhu, C. Cai, P. Yuan, C. Li et al., 2014 High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature 509: 487-491