Genome editing in <italic>Drosophila melanogaster</italic>: from basic genome engineering to the multipurpose CRISPR-Cas9 system

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SCIENCE CHINA Life Sciences, Volume 60, Issue 5: 476-489(2017) https://doi.org/10.1007/s11427-017-9029-9

Genome editing in Drosophila melanogaster: from basic genome engineering to the multipurpose CRISPR-Cas9 system

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  • ReceivedJan 20, 2017
  • AcceptedMar 5, 2017
  • PublishedMay 1, 2017

Abstract

Nowadays, genome editing tools are indispensable for studying gene function in order to increase our knowledge of biochemical processes and disease mechanisms. The extensive availability of mutagenesis and transgenesis tools make Drosophila melanogaster an excellent model organism for geneticists. Early mutagenesis tools relied on chemical or physical methods, ethyl methane sulfonate (EMS) and X-rays respectively, to randomly alter DNA at a nucleotide or chromosomal level. Since the discovery of transposable elements and the availability of the complete fly genome, specific genome editing tools, such as P-elements, zinc-finger nucleases (ZFNs) and transcription activator-like effector nucleases (TALENs), have undergone rapid development. Currently, one of the leading and most effective contemporary tools is the CRISPR-cas9 system made popular because of its low cost, effectiveness, specificity and simplicity of use. This review briefly addresses the most commonly used mutagenesis and transgenesis tools in Drosophila, followed by an in-depth review of the multipurpose CRISPR-Cas9 system and its current applications.


Funded by

National Basic Research Program(2013CB35102)

National Key Technology Research and Development Program of the Ministry of Science and Technology of the People’s Republic of China(2015BAI09B03)

National Natural Science Foundation of China(31371496)


Acknowledgment

We thank members of the Ni lab for their critical comments on the manuscript. This work was supported by the National Key Technology Research and Development Program of the Ministry of Science and Technology of the People’s Republic of China (2015BAI09B03, 2016YFE0113700), the National Natural Science Foundation of China (31371496, 31571320), the National Basic Research Program (2013CB35102).


Interest statement

The author(s) declare that they have no conflict of interest.


References

[1] Adams M.D., Celniker S.E., Holt R.A., Evans C.A., Gocayne J.D., Amanatides P.G., Scherer S.E., Li P.W., Hoskins R.A., Galle R.F., George R.A., Lewis S.E., Richards S., Ashburner M., Henderson S.N., Sutton G.G., Wortman J.R., Yandell M.D., Zhang Q., Chen L.X., Brandon R.C., Rogers Y.H., Blazej R.G., Champe M., Pfeiffer B.D., Wan K.H., Doyle C., Baxter E.G., Helt G., Nelson C.R., Gabor G.L., Abril J.F., Agbayani A., An H.J., Andrews-Pfannkoch C., Baldwin D., Ballew R.M., Basu A., Baxendale J., Bayraktaroglu L., Beasley E.M., Beeson K.Y., Benos P.V., Berman B.P., Bhandari D., Bolshakov S., Borkova D., Botchan M.R., Bouck J., Brokstein P., Brottier P., Burtis K.C., Busam D.A., Butler H., Cadieu E., Center A., Chandra I., Cherry J.M., Cawley S., Dahlke C., Davenport L.B., Davies P., de P.B., Delcher A., Deng Z., Mays A.D., Dew I., Dietz S.M., Dodson K., Doup L.E., Downes M., Dugan-Rocha S., Dunkov B.C., Dunn P., Durbin K.J., Evangelista C.C., Ferraz C., Ferriera S., Fleischmann W., Fosler C., Gabrielian A.E., Garg N.S., Gelbart W.M., Glasser K., Glodek A., Gong F., Gorrell J.H., Gu Z., Guan P., Harris M., Harris N.L., Harvey D., Heiman T.J., Hernandez J.R., Houck J., Hostin D., Houston K.A., Howland T.J., Wei M.H., Ibegwam C., Jalali M., Kalush F., Karpen G.H., Ke Z., Kennison J.A., Ketchum K.A., Kimmel B.E., Kodira C.D., Kraft C., Kravitz S., Kulp D., Lai Z., Lasko P., Lei Y., Levitsky A.A., Li J., Li Z., Liang Y., Lin X., Liu X., Mattei B., McIntosh T.C., McLeod M.P., McPherson D., Merkulov G., Milshina N.V., Mobarry C., Morris J., Moshrefi A., Mount S.M., Moy M., Murphy B., Murphy L., Muzny D.M., Nelson D.L., Nelson D.R., Nelson K.A., Nixon K., Nusskern D.R., Pacleb J.M., Palazzolo M., Pittman G.S., Pan S., Pollard J., Puri V., Reese M.G., Reinert K., Remington K., Saunders R.D., Scheeler F., Shen H., Shue B.C., Siden-Kiamos I., Simpson M., Skupski M.P., Smith T., Spier E., Spradling A.C., Stapleton M., Strong R., Sun E., Svirskas R., Tector C., Turner R., Venter E., Wang A.H., Wang X., Wang Z.Y., Wassarman D.A., Weinstock G.M., Weissenbach J., Williams S.M., Woodage T., Worley K.C., Wu D., Yang S., Yao Q.A., Ye J., Yeh R.F., Zaveri J.S., Zhan M., Zhang G., Zhao Q., Zheng L., Zheng X.H., Zhong F.N., Zhong W., Zhou X., Zhu S., Zhu X., Smith H.O., Gibbs R.A., Myers E.W., Rubin G.M., Venter J.C.. The genome sequence of Drosophila melanogaster. Science, 2000, 287: 2185-2195 CrossRef ADS Google Scholar

[2] Anders C., Niewoehner O., Duerst A., Jinek M.. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature, 2014, 513: 569-573 CrossRef PubMed ADS Google Scholar

[3] Antosh M., Fox D., Hasselbacher T., Lanou R., Neretti N., Cooper L.N.. Drosophila Melanogaster show a threshold effect in response to radiation. Dose Response, 2014, 12: dose-response.1 CrossRef PubMed Google Scholar

[4] Ashburner, M. (1989). Drosophila: A Laboratory Handbook. (New York: Cold Spring Harbor Laboratory Press). Google Scholar

[5] B?kel, C. (2008). EMS screens: from mutagenesis to screening and mapping. Drosophila: Methods and Protocols, 119–138. Google Scholar

[6] Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P.. CRISPR provides acquired resistance against viruses in prokaryotes. Science, 2007, 315: 1709-1712 CrossRef PubMed ADS Google Scholar

[7] Bassett A.R., Tibbit C., Ponting C.P., Liu J.L.. Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep, 2013, 4: 220-228 CrossRef PubMed Google Scholar

[8] Bellen H.J., Levis R.W., He Y., Carlson J.W., Evans-Holm M., Bae E., Kim J., Metaxakis A., Savakis C., Schulze K.L., Hoskins R.A., Spradling A.C.. The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genets, 2011, 188: 731-743 CrossRef PubMed Google Scholar

[9] Berger J., Suzuki T., Senti K.A., Stubbs J., Schaffner G., Dickson B.J.. Genetic mapping with SNP markers in Drosophila. Nat Genet, 2001, 29: 475-481 CrossRef PubMed Google Scholar

[10] Berghammer A.J., Klingler M., A.~Wimmer E.. Genetic techniques: a universal marker for transgenic insects. Nature, 1999, 402: 370-371 CrossRef PubMed ADS Google Scholar

[11] Beumer K.J., Trautman J.K., Bozas A., Liu J.L., Rutter J., Gall J.G., Carroll D.. Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases. Proc Natl Acad Sci USA, 2008, 105: 19821-19826 CrossRef PubMed ADS Google Scholar

[12] Beumer K.J., Trautman J.K., Christian M., Dahlem T.J., Lake C.M., Hawley R.S., Grunwald D.J., Voytas D.F., Carroll D.. Comparing zinc finger nucleases and transcription activator-like effector nucleases for gene targeting in Drosophila. G3, 2013, 3: 1717-1725 CrossRef PubMed Google Scholar

[13] Bhakta M.S., Henry I.M., Ousterout D.G., Das K.T., Lockwood S.H., Meckler J.F., Wallen M.C., Zykovich A., Yu Y., Leo H., Xu L., Gersbach C.A., Segal D.J.. Highly active zinc-finger nucleases by extended modular assembly. Genome Res, 2013, 23: 530-538 CrossRef PubMed Google Scholar

[14] Bibikova M., Beumer K., Trautman J.K., Carroll D.. Enhancing gene targeting with designed zinc finger nucleases. Science, 2003, 300: 764-764 CrossRef PubMed Google Scholar

[15] Bibikova, M., Golic, M., Golic, K.G., and Carroll, D. (2002). Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169–1175. Google Scholar

[16] Bitinaite J., Wah D.A., Aggarwal A.K., Schildkraut I.. Fok I dimerization is required for DNA cleavage. Proc Natl Acad Sci USA, 1998, 95: 10570-10575 CrossRef Google Scholar

[17] Boch J., Bonas U.. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol, 2010, 48: 419-436 CrossRef PubMed Google Scholar

[18] Boch J., Scholze H., Schornack S., Landgraf A., Hahn S., Kay S., Lahaye T., Nickstadt A., Bonas U.. Breaking the code of DNA binding specificity of TAL-type III effectors. Science, 2009, 326: 1509-1512 CrossRef PubMed ADS Google Scholar

[19] Bolotin A., Quinquis B., Sorokin A., Ehrlich S.D.. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology, 2005, 151: 2551-2561 CrossRef PubMed Google Scholar

[20] B?ttcher R., Hollmann M., Merk K., Nitschko V., Obermaier C., Philippou-Massier J., Wieland I., Gaul U., F?rstemann K.. Efficient chromosomal gene modification with CRISPR/cas9 and PCR-based homologous recombination donors in cultured Drosophila cells. Nucleic Acids Res, 2014, 42: e89-e89 CrossRef PubMed Google Scholar

[21] Brand A.H., Dormand E.L.. The GAL4 system as a tool for unravelling the mysteries of the Drosophila nervous system. Curr Opin Neurobiol, 1995, 5: 572-578 CrossRef Google Scholar

[22] Brouns S.J.J., Jore M.M., Lundgren M., Westra E.R., Slijkhuis R.J.H., Snijders A.P.L., Dickman M.J., Makarova K.S., Koonin E.V., van der Oost J.. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 2008, 321: 960-964 CrossRef PubMed ADS Google Scholar

[23] Capecchi M.R.. Essay: gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century. Nat Rev Genet, 2005, 6: 507-512 CrossRef PubMed Google Scholar

[24] Chavez A., Scheiman J., Vora S., Pruitt B.W., Tuttle M., P R Iyer E., Lin S., Kiani S., Guzman C.D., Wiegand D.J., Ter-Ovanesyan D., Braff J.L., Davidsohn N., Housden B.E., Perrimon N., Weiss R., Aach J., Collins J.J., Church G.M.. Highly efficient Cas9-mediated transcriptional programming. Nat Meth, 2015, 12: 326-328 CrossRef PubMed Google Scholar

[25] Chen K., Gao C.. TALENs: customizable molecular DNA scissors for genome engineering of plants. J Genet Genomics, 2013, 40: 271-279 CrossRef PubMed Google Scholar

[26] Chen Y., Wang Z., Ni H., Xu Y., Chen Q., Jiang L.. CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. Sci China Life Sci, 2017, : in press doi: 10.1007/s11427-017-9021-5 CrossRef PubMed Google Scholar

[27] Choi C.M., Vilain S., Langen M., Van Kelst S., De Geest N., Yan J., Verstreken P., Hassan B.A.. Conditional mutagenesis in Drosophila. Science, 2009, 324: 54-54 CrossRef PubMed ADS Google Scholar

[28] Chylinski K., Makarova K.S., Charpentier E., Koonin E.V.. Classification and evolution of type II CRISPR-Cas systems. Nucleic Acids Res, 2014, 42: 6091-6105 CrossRef PubMed Google Scholar

[29] Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., Zhang F.. Multiplex genome engineering using CRISPR/Cas systems. Science, 2013, 339: 819-823 CrossRef PubMed ADS Google Scholar

[30] Cooley L., Berg C., Spradling A.. Controlling P element insertional mutagenesis. Trends Genets, 1988, 4: 254-258 CrossRef Google Scholar

[31] Dahlem T.J., Hoshijima K., Jurynec M.J., Gunther D., Starker C.G., Locke A.S., Weis A.M., Voytas D.F., Grunwald D.J.. Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet, 2012, 8: e1002861 CrossRef PubMed Google Scholar

[32] Dever D.P., Bak R.O., Reinisch A., Camarena J., Washington G., Nicolas C.E., Pavel-Dinu M., Saxena N., Wilkens A.B., Mantri S., Uchida N., Hendel A., Narla A., Majeti R., Weinberg K.I., Porteus M.H.. CRISPR/Cas9 β-globin gene targeting in human haematopoietic stem cells. Nature, 2016, 539: 384-389 CrossRef PubMed ADS Google Scholar

[33] Dodson M.W., Leung L.K., Lone M., Lizzio M.A., Guo M.. Novel ethyl methanesulfonate (EMS)-induced null alleles of the Drosophila homolog of LRRK2 reveal a crucial role in endolysosomal functions and autophagy in vivo. Dis Model Mech, 2014, 7: 1351-1363 CrossRef PubMed Google Scholar

[34] Doyon Y., Vo T.D., Mendel M.C., Greenberg S.G., Wang J., Xia D.F., Miller J.C., Urnov F.D., Gregory P.D., Holmes M.C.. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Meth, 2011, 8: 74-79 CrossRef PubMed Google Scholar

[35] Eeken J., Dejong A., Loos M., Vreeken C., Romeyn R., Pastink A., Lohman P.. The nature of X-ray-induced mutations in mature sperm and spermatogonial cells of Drosophila melanogaster. Mutat Res, 1994, 307: 201-212 CrossRef Google Scholar

[36] Engels W.R.. The origin of P elements in Drosophila melanogaster. Bioessays, 1992, 14: 681-686 CrossRef PubMed Google Scholar

[37] Engels, W.R. (1996). P elements in Drosophila. Curr Top Microbiol Immunol 204, 103–123. Google Scholar

[38] Fonfara I., Le Rhun A., Chylinski K., Makarova K.S., Lécrivain A.L., Bzdrenga J., Koonin E.V., Charpentier E.. Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res, 2014, 42: 2577-2590 CrossRef PubMed Google Scholar

[39] Friedland A.E., Tzur Y.B., Esvelt K.M., Colaiácovo M.P., Church G.M., Calarco J.A.. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Meth, 2013, 10: 741-743 CrossRef PubMed Google Scholar

[40] Gasiunas G., Barrangou R., Horvath P., Siksnys V.. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci USA, 2012, 109: E2579-E2586 CrossRef PubMed ADS Google Scholar

[41] Gebler C., Lohoff T., Paszkowski-Rogacz M., Mircetic J., Chakraborty D., Camgoz A., Hamann M.V., Theis M., Thiede C., Buchholz F.. Inactivation of cancer mutations utilizing CRISPR/Cas9. J Natl Cancer Inst, 2017, 109: djw183 CrossRef PubMed Google Scholar

[42] Gloor G.B., Nassif N.A., Johnson-Schlitz D.M., Preston C.R., Engels W.R.. Targeted gene replacement in Drosophila via P element-induced gap repair. Science, 1991, 253: 1110-1117 CrossRef ADS Google Scholar

[43] Gokcezade J., Sienski G., Duchek P.. Efficient CRISPR/Cas9 plasmids for rapid and versatile genome editing in Drosophila. G3, 2014, 4: 2279-2282 CrossRef PubMed Google Scholar

[44] Golic K.G.. Site-specific recombination between homologous chromosomes in Drosophila. Science, 1991, 252: 958-961 CrossRef ADS Google Scholar

[45] Golic K.G., Lindquist S.. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell, 1989, 59: 499-509 CrossRef Google Scholar

[46] Golic M.M., Rong Y.S., Petersen R.B., Lindquist S.L., Golic K.G.. FLP-mediated DNA mobilization to specific target sites in Drosophila chromosomes. Nucleic Acids Res, 1997, 25: 3665-3671 CrossRef Google Scholar

[47] Gorski, M.M., Eeken, J.C., de Jong, A.W., Klink, I., Loos, M., Romeijn, R.J., van Veen, B.L., Mullenders, L.H., Ferro, W., and Pastink, A. (2003). The Drosophila melanogaster DNA Ligase IV gene plays a crucial role in the repair of radiation-induced DNA double-strand breaks and acts synergistically with Rad54. Genetics 165, 1929–1941. Google Scholar

[48] Gratz S.J., Cummings A.M., Nguyen J.N., Hamm D.C., Donohue L.K., Harrison M.M., Wildonger J., O’Connor-Giles K.M.. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genets, 2013, 194: 1029-1035 CrossRef PubMed Google Scholar

[49] Gratz S.J., Ukken F.P., Rubinstein C.D., Thiede G., Donohue L.K., Cummings A.M., O’Connor-Giles K.M.. Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genets, 2014, 196: 961-971 CrossRef PubMed Google Scholar

[50] Gray, Y.H., Tanaka, M.M., and Sved, J.A. (1996). P-element-induced recombination in Drosophila melanogaster: hybrid element insertion. Genetics 144, 1601–1610. Google Scholar

[51] Greenspan, R.J. (2004). Fly Pushing: the Theory and Practice of Drosophila Genetics. (New York: Cold Spring Harbor Laboratory Press). Google Scholar

[52] Gupta A., Christensen R.G., Rayla A.L., Lakshmanan A., Stormo G.D., Wolfe S.A.. An optimized two-finger archive for ZFN-mediated gene targeting. Nat Meth, 2012, 9: 588-590 CrossRef PubMed Google Scholar

[53] Hacker U., Nystedt S., Barmchi M.P., Horn C., Wimmer E.A.. piggyBac-based insertional mutagenesis in the presence of stably integrated P elements in Drosophila. Proc Natl Acad Sci USA, 2003, 100: 7720-7725 CrossRef PubMed ADS Google Scholar

[54] Hammond A., Galizi R., Kyrou K., Simoni A., Siniscalchi C., Katsanos D., Gribble M., Baker D., Marois E., Russell S., Burt A., Windbichler N., Crisanti A., Nolan T.. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat Biotechnol, 2016, 34: 78-83 CrossRef PubMed Google Scholar

[55] Heigwer F., Kerr G., Boutros M.. E-CRISP: fast CRISPR target site identification. Nat Meth, 2014, 11: 122-123 CrossRef PubMed Google Scholar

[56] Horn C., Wimmer E.A.. A versatile vector set for animal transgenesis. Dev Genes Evol, 2000, 210: 630-637 CrossRef Google Scholar

[57] Hruscha A., Krawitz P., Rechenberg A., Heinrich V., Hecht J., Haass C., Schmid B.. Efficient CRISPR/Cas9 genome editing with low off-target effects in zebrafish. Development, 2013, 140: 4982-4987 CrossRef PubMed Google Scholar

[58] 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., Cradick T.J., Marraffini L.A., Bao G., Zhang F.. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol, 2013, 31: 827-832 CrossRef PubMed Google Scholar

[59] Ishino Y., Shinagawa H., Makino K., Amemura M., Nakata A.. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol, 1987, 169: 5429-5433 CrossRef Google Scholar

[60] Jansen R., Embden J.D.A., Gaastra W., Schouls L.M.. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol, 2002, 43: 1565-1575 CrossRef Google Scholar

[61] Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E.. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 2012, 337: 816-821 CrossRef PubMed ADS Google Scholar

[62] Jinek M., Jiang F., Taylor D.W., Sternberg S.H., Kaya E., Ma E., Anders C., Hauer M., Zhou K., Lin S., Kaplan M., Iavarone A.T., Charpentier E., Nogales E., Doudna J.A.. Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science, 2014, 343: 1247997-1247997 CrossRef PubMed Google Scholar

[63] Josephs E.A., Kocak D.D., Fitzgibbon C.J., McMenemy J., Gersbach C.A., Marszalek P.E.. Structure and specificity of the RNA-guided endonuclease Cas9 during DNA interrogation, target binding and cleavage. Nucleic Acids Res, 2015, 43: 8924-8941 CrossRef PubMed Google Scholar

[64] Kaminski R., Chen Y., Salkind J., Bella R., Young W.B., Ferrante P., Karn J., Malcolm T., Hu W., Khalili K.. Negative feedback regulation of HIV-1 by gene editing strategy. Sci Rep, 2016, 6: 31527 CrossRef PubMed ADS Google Scholar

[65] Katsuyama T., Akmammedov A., Seimiya M., Hess S.C., Sievers C., Paro R.. An efficient strategy for TALEN-mediated genome engineering in Drosophila. Nucleic Acids Res, 2013, 41: e163-e163 CrossRef PubMed Google Scholar

[66] Kim Y.G., Cha J., Chandrasegaran S.. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA, 1996, 93: 1156-1160 CrossRef Google Scholar

[67] Kleinstiver B.P., Prew M.S., Tsai S.Q., Nguyen N.T., Topkar V.V., Zheng Z., Joung J.K.. Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat Biotechnol, 2015a, 33: 1293-1298 CrossRef PubMed Google Scholar

[68] Kleinstiver B.P., Prew M.S., Tsai S.Q., Topkar V.V., Nguyen N.T., Zheng Z., Gonzales A.P.W., Li Z., Peterson R.T., Yeh J.R.J., Aryee M.J., Joung J.K.. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature, 2015b, 523: 481-485 CrossRef PubMed ADS Google Scholar

[69] Koana T., Okada M.O., Ogura K., Tsujimura H., Sakai K.. Reduction of background mutations by low-dose X irradiation of Drosophila spermatocytes at a low dose rate. Radiat Res, 2007, 167: 217-221 CrossRef Google Scholar

[70] Kondo S., Ueda R.. Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genets, 2013, 195: 715-721 CrossRef PubMed Google Scholar

[71] 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., Nureki O., Zhang F.. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature, 2015, 517: 583-588 CrossRef PubMed ADS Google Scholar

[72] Lewis, E., and Bacher, F. (1968). Method of feeding ethyl methane sulfonate (EMS) to Drosophila males. Dros Inf Serv 43, 193. Google Scholar

[73] Li L., Wu L.P., Chandrasegaran S.. Functional domains in Fok I restriction endonuclease. Proc Natl Acad Sci USA, 1992, 89: 4275-4279 CrossRef ADS Google Scholar

[74] Lieber M.R., Ma Y., Pannicke U., Schwarz K.. Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol, 2003, 4: 712-720 CrossRef PubMed Google Scholar

[75] Lin S., Ewen-Campen B., Ni X., Housden B.E., Perrimon N.. In vivo transcriptional activation using CRISPR/Cas9 in Drosophila. Genets, 2015, 201: 433-442 CrossRef PubMed Google Scholar

[76] Liu, J., Guo, Y., Li, C., Chen, Y., and Jiao, R. (2016). Methods for TALEN-mediated genomic manipulations in Drosophila. Methods Mol Biol 1338, 179–190. Google Scholar

[77] Liu J., Li C., Yu Z., Huang P., Wu H., Wei C., Zhu N., Shen Y., Chen Y., Zhang B., Deng W.M., Jiao R.. Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy. J Genet Genomics, 2012, 39: 209-215 CrossRef PubMed Google Scholar

[78] Mahmoud J., Fossett N.G., Arbour-Reily P., McDaniel M., Tucker A., Chang S.H., Lee W.R., Aaron C.S.. DNA sequence analysis of X-ray inducedAdh null mutations in Drosophila melanogaster. Environ Mol Mutagen, 1991, 18: 157-160 CrossRef Google Scholar

[79] Mali P., Aach J., Stranges P.B., Esvelt K.M., Moosburner M., Kosuri S., Yang L., Church G.M.. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol, 2013a, 31: 833-838 CrossRef PubMed Google Scholar

[80] Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M.. RNA-guided human genome engineering via Cas9. Science, 2013b, 339: 823-826 CrossRef PubMed ADS Google Scholar

[81] Martin, S.G., Dobi, K.C., and St Johnston, D. (2001). A rapid method to map mutations in Drosophila. Genome Biol 2, RESEARCH0036. Google Scholar

[82] McClintock B.. The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA, 1950, 36: 344-355 CrossRef ADS Google Scholar

[83] McVey M., Radut D., Sekelsky J.J.. End-joining repair of double-strand breaks in Drosophila melanogaster is largely DNA ligase IV independent. Genets, 2004, 168: 2067-2076 CrossRef PubMed Google Scholar

[84] Metaxakis A., Oehler S., Klinakis A., Savakis C.. Minos as a genetic and genomic tool in Drosophila melanogaster. Genets, 2005, 171: 571-581 CrossRef PubMed Google Scholar

[85] Mglinets, V.A. (1973). Cytological investigation of crossovers induced by irradiation in males of Drosophila melanogaster. Sov Genet 7, 1036–1041. Google Scholar

[86] Miller J.C., Holmes M.C., Wang J., Guschin D.Y., Lee Y.L., Rupniewski I., Beausejour C.M., Waite A.J., Wang N.S., Kim K.A., Gregory P.D., Pabo C.O., Rebar E.J.. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol, 2007, 25: 778-785 CrossRef PubMed Google Scholar

[87] Miller J.C., Tan S., Qiao G., Barlow K.A., Wang J., Xia D.F., Meng X., Paschon D.E., Leung E., Hinkley S.J., Dulay G.P., Hua K.L., Ankoudinova I., Cost G.J., Urnov F.D., Zhang H.S., Holmes M.C., Zhang L., Gregory P.D., Rebar E.J.. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol, 2011, 29: 143-148 CrossRef PubMed Google Scholar

[88] Mohr, S.E., and Gelbart, W.M. (2002). Using the P{wHy} hybrid transposable element to disrupt genes in region 54D-55B in Drosophila melanogaster. Genetics 162, 165–176. Google Scholar

[89] Mojica F.J.M., Díez-Villase?or C., García-Martínez J., Soria E.. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol, 2005, 60: 174-182 CrossRef PubMed Google Scholar

[90] Mojica F.J.M., Diez-Villasenor C., Soria E., Juez G.. Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol, 2000, 36: 244-246 CrossRef Google Scholar

[91] Moscou M.J., Bogdanove A.J.. A simple cipher governs DNA recognition by TAL effectors. Science, 2009, 326: 1501-1501 CrossRef PubMed ADS Google Scholar

[92] Muller H.J.. Artificial transmutation of the gene. Science, 1927, 66: 84-87 CrossRef PubMed ADS Google Scholar

[93] Nairz K., Zipperlen P., Dearolf C., Basler K., Hafen E.. A reverse genetic screen in Drosophila using a deletion-inducing mutagen. Genome Biol, 2004, 5: R83 CrossRef PubMed Google Scholar

[94] Ni J.Q., Zhou R., Czech B., Liu L.P., Holderbaum L., Yang-Zhou D., Shim H.S., Tao R., Handler D., Karpowicz P., Binari R., Booker M., Brennecke J., Perkins L.A., Hannon G.J., Perrimon N.. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Meth, 2011, 8: 405-407 CrossRef PubMed Google Scholar

[95] Nishimasu H., Ran F.A., Hsu P.D., Konermann S., Shehata S.I., Dohmae N., Ishitani R., Zhang F., Nureki O.. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell, 2014, 156: 935-949 CrossRef PubMed Google Scholar

[96] Patton J.S., Gomes X.V., Geyer P.K.. Position-independent germline transformation in Drosophila using a cuticle pigmentation gene as a selectable marker. Nucl Acids Res, 1992, 20: 5859-5860 CrossRef Google Scholar

[97] Pavletich N.P., Pabo C.O.. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science, 1991, 252: 809-817 CrossRef ADS Google Scholar

[98] Peabody, D.S. (1993). The RNA binding site of bacteriophage MS2 coat protein. EMBO J 12, 595–600. Google Scholar

[99] Peterson B.A., Haak D.C., Nishimura M.T., Teixeira P.J.P.L., James S.R., Dangl J.L., Nimchuk Z.L.. Genome-wide assessment of efficiency and specificity in CRISPR/Cas9 mediated multiple site targeting in Arabidopsis. PLoS ONE, 2016, 11: e0162169 CrossRef PubMed ADS Google Scholar

[100] Pfeifer G.P., You Y.H., Besaratinia A.. Mutations induced by ultraviolet light. Mutat Res, 2005, 571: 19-31 CrossRef PubMed Google Scholar

[101] Pirrotta, V. (1988). Vectors for P-mediated transformation in Drosophila. Biotechnology 10, 437–456. Google Scholar

[102] Port F., Bullock S.L.. Augmenting CRISPR applications in Drosophila with tRNA-flanked sgRNAs. Nat Meth, 2016, 13: 852-854 CrossRef PubMed Google Scholar

[103] Port F., Chen H.M., Lee T., Bullock S.L.. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc Natl Acad Sci USA, 2014, 111: E2967-E2976 CrossRef PubMed ADS Google Scholar

[104] Pourcel C., Salvignol G., Vergnaud G.. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology, 2005, 151: 653-663 CrossRef PubMed Google Scholar

[105] Ren B., Yan F., Kuang Y., Li N., Zhang D., Lin H., Zhou H.. A CRISPR/Cas9 toolkit for efficient targeted base editing to induce genetic variations in rice. Sci China Life Sci, 2017, : in press doi: 10.1007/s11427-016-0406-x CrossRef PubMed Google Scholar

[106] Ren X., Sun J., Housden B.E., Hu Y., Roesel C., Lin S., Liu L.P., Yang Z., Mao D., Sun L., Wu Q., Ji J.Y., Xi J., Mohr S.E., Xu J., Perrimon N., Ni J.Q.. Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9. Proc Natl Acad Sci USA, 2013, 110: 19012-19017 CrossRef PubMed ADS Google Scholar

[107] Ren X., Yang Z., Mao D., Chang Z., Qiao H.H., Wang X., Sun J., Hu Q., Cui Y., Liu L.P., Ji J.Y., Xu J., Ni J.Q.. Performance of the Cas9 nickase system in Drosophila melanogaster. G3, 2014a, 4: 1955-1962 CrossRef PubMed Google Scholar

[108] Ren X., Yang Z., Xu J., Sun J., Mao D., Hu Y., Yang S.J., Qiao H.H., Wang X., Hu Q., Deng P., Liu L.P., Ji J.Y., Li J.B., Ni J.Q.. Enhanced specificity and efficiency of the CRISPR/Cas9 system with optimized sgRNA parameters in Drosophila. Cell Rep, 2014b, 9: 1151-1162 CrossRef PubMed Google Scholar

[109] Rio D.C.. Molecular mechanisms regulating Drosophila P element transposition. Annu Rev Genet, 1990, 24: 543-576 CrossRef Google Scholar

[110] Rio D.C., Laski F.A., Rubin G.M.. Identification and immunochemical analysis of biologically active Drosophila P element transposase. Cell, 1986, 44: 21-32 CrossRef Google Scholar

[111] Roberts D.B.. Necrotizing fasciffis of the vulva. Am J Obstetr Gynecol, 1987, 157: 568-571 CrossRef Google Scholar

[112] Robertson, H.M., Preston, C.R., Phillis, R.W., Johnson-Schlitz, D.M., Benz, W.K., and Engels, W.R. (1988). A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470. Google Scholar

[113] Rong Y.S., Golic K.G.. Gene targeting by homologous recombination in Drosophila. Science, 2000, 288: 2013-2018 CrossRef ADS Google Scholar

[114] Sander J.D., Dahlborg E.J., Goodwin M.J., Cade L., Zhang F., Cifuentes D., Curtin S.J., Blackburn J.S., Thibodeau-Beganny S., Qi Y., Pierick C.J., Hoffman E., Maeder M.L., Khayter C., Reyon D., Dobbs D., Langenau D.M., Stupar R.M., Giraldez A.J., Voytas D.F., Peterson R.T., Yeh J.R.J., Joung J.K.. Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat Meth, 2011, 8: 67-69 CrossRef PubMed Google Scholar

[115] Sebo Z.L., Lee H.B., Peng Y., Guo Y.. A simplified and efficient germline-specific CRISPR/Cas9 system for Drosophila genomic engineering. Fly, 2014, 8: 52-57 CrossRef PubMed Google Scholar

[116] Sepp, K.J., and Auld, V.J. (1999). Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151, 1093–1101. Google Scholar

[117] Shen L., Hua Y., Fu Y., Li J., Liu Q., Jiao X., Xin G., Wang J., Wang X., Yan C., Wang K.. Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice. Sci China Life Sci, 2017, 309: in press doi: 10.1007/s11427-017-9008-8 CrossRef PubMed Google Scholar

[118] Slaymaker I.M., Gao L., Zetsche B., Scott D.A., Yan W.X., Zhang F.. Rationally engineered Cas9 nucleases with improved specificity. Science, 2016, 351: 84-88 CrossRef PubMed ADS Google Scholar

[119] Smith J., Bibikova M., Whitby F.G., Reddy A.R., Chandrasegaran S., Carroll D.. Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Res, 2000, 28: 3361-3369 CrossRef Google Scholar

[120] Spradling A.C., Bellen H.J., Hoskins R.A.. Drosophila P elements preferentially transpose to replication origins. Proc Natl Acad Sci USA, 2011, 108: 15948-15953 CrossRef PubMed ADS Google Scholar

[121] Spradling A.C., Rubin G.M.. Transposition of cloned P elements into Drosophila germ line chromosomes. Science, 1982, 218: 341-347 CrossRef ADS Google Scholar

[122] St Johnston D.. The art and design of genetic screens: Drosophila melanogaster. Nat Rev Genet, 2002, 3: 176-188 CrossRef PubMed Google Scholar

[123] Sternberg S.H., Redding S., Jinek M., Greene E.C., Doudna . DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, 2014, 507: 62-67 CrossRef PubMed ADS Google Scholar

[124] Szczepek M., Brondani V., Büchel J., Serrano L., Segal D.J., Cathomen T.. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol, 2007, 25: 786-793 CrossRef PubMed Google Scholar

[125] Szostak J.W., Orr-Weaver T.L., Rothstein R.J., Stahl F.W.. The double-strand-break repair model for recombination. Cell, 1983, 33: 25-35 CrossRef Google Scholar

[126] Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S.. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J, 1998, 17: 5497-5508 CrossRef Google Scholar

[127] Vazquez J., Belmont A.S., Sedat J.W.. The dynamics of homologous chromosome pairing during male Drosophila meiosis. Curr Biol, 2002, 12: 1473-1483 CrossRef Google Scholar

[128] Venken K.J.T., Bellen H.J.. Transgenesis upgrades for Drosophila melanogaster. Dev, 2007, 134: 3571-3584 CrossRef PubMed Google Scholar

[129] Wang H., Yang H., Shivalila C.S., Dawlaty M.M., Cheng A.W., Zhang F., Jaenisch R.. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 2013, 153: 910-918 CrossRef PubMed Google Scholar

[130] Wen K., Yang L., Xiong T., Di C., Ma D., Wu M., Xue Z., Zhang X., Long L., Zhang W., Zhang J., Bi X., Dai J., Zhang Q., Lu Z.J., Gao G.. Critical roles of long noncoding RNAs in Drosophila spermatogenesis. Genome Res, 2016, 26: 1233-1244 CrossRef PubMed Google Scholar

[131] Xu J., Ren X., Sun J., Wang X., Qiao H.H., Xu B.W., Liu L.P., Ni J.Q.. A toolkit of CRISPR-based genome editing systems in Drosophila. J Genet Genomics, 2015, 42: 141-149 CrossRef PubMed Google Scholar

[132] Xue Z., Wu M., Wen K., Ren M., Long L., Zhang X., Gao G.. CRISPR/Cas9 mediates efficient conditional mutagenesis in Drosophila. G3, 2014, 4: 2167-2173 CrossRef PubMed Google Scholar

[133] Yu Z., Chen H., Liu J., Zhang H., Yan Y., Zhu N., Guo Y., Yang B., Chang Y., Dai F., Liang X., Chen Y., Shen Y., Deng W.M., Chen J., Zhang B., Li C., Jiao R.. Various applications of TALEN- and CRISPR/Cas9-mediated homologous recombination to modify the Drosophila genome. Biol Open, 2014, 3: 271-280 CrossRef PubMed Google Scholar

[134] Yu Z., Ren M., Wang Z., Zhang B., Rong Y.S., Jiao R., Gao . Highly efficient genome modifications mediated by CRISPR/ Cas9 in Drosophila. Genets, 2013, 195: 289-291 CrossRef PubMed Google Scholar

[135] Zhang, P., and Spradling, A.C. (1993). Efficient and dispersed local P element transposition from Drosophila females. Genetics 133, 361–373. Google Scholar

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