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Advances and perspectives in the application of CRISPR/Cas9 in insects


Lei CHEN, Gui WANG, Ya-Nan ZHU, Hui XIANG, Wen WANG. Advances and perspectives in the application of CRISPR/Cas9 in insects. Zoological Research, 2016, 37(4): 220-228. doi: 10.13918/j.issn.2095-8137.2016.4.220
Citation: Lei CHEN, Gui WANG, Ya-Nan ZHU, Hui XIANG, Wen WANG. Advances and perspectives in the application of CRISPR/Cas9 in insects. Zoological Research, 2016, 37(4): 220-228. doi: 10.13918/j.issn.2095-8137.2016.4.220


doi: 10.13918/j.issn.2095-8137.2016.4.220

    Wen WANG

Advances and perspectives in the application of CRISPR/Cas9 in insects

Funds: This work was supported by a 973 program (2013CB835200) to Wen WANG; a key grant of West Light Foundation of the Chinese Academy of Sciences to Hui XIANG
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    Corresponding author: Wen WANG
  • 摘要: 昆虫的种类多样,组成了地球上一半以上的生物个体,在全球生态系统中具有不可或缺的重要作用,并且和人类具有复杂紧密的联系。因而昆虫的研究具有重要的生物学重要性和实用价值。但是,长期以来昆虫的遗传操作只能有限的在少数模式昆虫例如果蝇中实现。这样的情况严重制约了昆虫生物学研究的发展。近年来,随着越来越多的昆虫基因组数据发表和高效的遗传操作系统CRISPR/Cas9的发展,使在更广泛的昆虫物种中进行重要的功能研究成为了可能。这里,我们总结了CRISPR/Cas9在不同昆虫中的研究进展、探讨了提升CRISPR/Cas9效果的方法和在今后的昆虫研究中的应用。这篇综述对CRISPR/Cas9在昆虫研究中的应用提供了详尽的信息,并展示了在功能研究和病虫害控制的应用中提升CRISPR/Cas9效果的可能途径。
  • [1] Auer TO, Duroure K, Concordet JP, Del Bene F. 2014a. CRISPR/Cas9-mediated conversion of eGFP-into Gal4-transgenic lines in zebrafish. Nature Protocols, 9(12):2823-2840.
    [2] Auer TO, Duroure K, De Cian A, Concordet JP, Del Bene F. 2014b. Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Research, 24(1):142-153.
    [3] Awata H, Watanabe T, Hamanaka Y, Mito T, Noji S, Mizunami M. 2015. Knockout crickets for the study of learning and memory:Dopamine receptor Dop1 mediates aversive but not appetitive reinforcement in crickets. Scientific Reports, 5:15885.
    [4] Bassett AR, Tibbit C, Ponting CP, Liu JL. 2013. Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Reports, 4(1):220-228.
    [5] Basu S, Aryan A, Overcash JM, Samuel GH, Anderson MaE, Dahlem TJ, Myles KM, Adelman ZN. 2015. Silencing of end-joining repair for efficient site-specific gene insertion after TALEN/CRISPR mutagenesis in Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America, 112(13):4038-4043.
    [6] Bi HL, Xu J, Tan AJ, Huang YP. 2016. CRISPR/Cas9-mediated targeted gene mutagenesis in Spodoptera litura. Insect Science, 23(3):469-477.
    [7] Bibikova M, Beumer K, Trautman JK, Carroll D. 2003. Enhancing gene targeting with designed zinc finger nucleases. Science, 300(5620):764.
    [8] Bogdanove AJ, Voytas DF. 2011. TAL effectors:customizable proteins for DNA targeting. Science, 333(6051):1843-1846.
    [9] Chakraborty S, Newton AC. 2011. Climate change, plant diseases and food security:an overview. Plant Pathology, 60(1):2-14.
    [10] Chavez A, Tuttle M, Pruitt BW, Ewen-Campen B, Chari R, Ter-Ovanesyan D, Haque SJ, Cecchi RJ, Kowal EJK, Buchthal J, Housden BE, Perrimon N, Collins JJ, Church G. 2016. Comparison of Cas9 activators in multiple species. Nature Methods, 13(7):563-567.
    [11] Chavez A, Scheiman J, Vora S, Pruitt BW, Tuttle M, P R Iyer E, Lin S, Kiani S, Guzman CD, Wiegand DJ, Ter-Ovanesyan D, Braff JL, Davidsohn N, Housden BE, Perrimon N, Weiss R, Aach J, Collins JJ, Church GM. 2015. Highly efficient Cas9-mediated transcriptional programming. Nature Methods, 12(4):326-328.
    [12] Chen BH, Hu J, Almeida R, Liu H, Balakrishnan S, Covill-Cooke C, Lim WA, Huang B. 2016. Expanding the CRISPR imaging toolset with Staphylococcus aureus Cas9 for simultaneous imaging of multiple genomic loci. Nucleic Acids Research, 44(8):e75.
    [13] Chen BH, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, Park J, Blackburn EH, Weissman JS, Qi LS, Huang B. 2013. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 155(7):1479-1491.
    [14] Chen L, Tang LY, Xiang H, Jin LJ, Li QY, Dong Y, Wang W, Zhang GJ. 2014. Advances in genome editing technology and its promising application in evolutionary and ecological studies. GigaScience, 3:24.
    [15] Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, Kim JS. 2014. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Research, 24(1):132-141.
    [16] Dong SZ, Lin JY, Held NL, Clem RJ, Passarelli AL, Franz AWE. 2015. Heritable CRISPR/Cas9-mediated genome editing in the yellow fever mosquito, Aedes aegypti. PLoS One, 10(3):e0122353.
    [17] Fu Y, Rocha PP, Luo VM, Raviram R, Deng Y, Mazzoni EO, Skok JA. 2016. CRISPR-dCas9 and sgRNA scaffolds enable dual-colour live imaging of satellite sequences and repeat-enriched individual loci. Nature Communications, 7:11707.
    [18] Fu YF, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nature Biotechnology, 32(3):279-284.
    [19] Fu YF, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nature Biotechnology, 31(9):822-826.
    [20] Gaj T, Gersbach CA, Barbas CF. 2013. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnology, 31(7):397-405.
    [21] Gantz VM, Bier E. 2015. The mutagenic chain reaction:A method for converting heterozygous to homozygous mutations. Science, 348(6233):442-444.
    [22] Gantz VM, Jasinskiene N, Tatarenkova O, Fazekas A, Macias VM, Bier E, James AA. 2015. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proceedings of the National Academy of Sciences of the United States of America, 112(49):E6736-E6743.
    [23] Gasiunas G, Barrangou R, Horvath P, Siksnys V. 2012. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proceedings of the National Academy of Sciences of the United States of America, 109(39):E2579-E2586.
    [24] Ghosh S, Tibbit C, Liu JL. 2016. Effective knockdown of Drosophila long non-coding RNAs by CRISPR interference. Nucleic Acids Research, 44(9):e84.
    [25] Gilbert LA, Larson MH, Morsut L, Liu ZR, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154(2):442-451.
    [26] Gilles AF, Schinko JB, Averof M. 2015. Efficient CRISPR-mediated gene targeting and transgene replacement in the beetle Tribolium castaneum. Development, 142(16):2832-2839.
    [27] Gokcezade J, Sienski G, Duchek P. 2014. Efficient CRISPR/Cas9 plasmids for rapid and versatile genome editing in Drosophila. G3:Genes Genomes Genetics, 4(11):2279-2282.
    [28] Gratz SJ, Ukken FP, Rubinstein CD, Thiede G, Donohue LK, Cummings AM, O'connor-Giles KM. 2014. Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics, 196(4):961-971.
    [29] Gratz SJ, Cummings AM, Nguyen JN, Hamm DC, Donohue LK, Harrison MM, Wildonger J, O'connor-Giles KM. 2013. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics, 194(4):1029-1035.
    [30] Guilinger JP, Thompson DB, Liu DR. 2014. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nature Biotechnology, 32(6):577-582.
    [31] Hall AB, Basu S, Jiang XF, Qi YM, Timoshevskiy VA, Biedler JK, Sharakhova MV, Elahi R, Anderson MaE, Chen XG, Sharakhov IV, Adelman ZN, Tu ZJ. 2015. A male-determining factor in the mosquito Aedes aegypti. Science, 348(6240):1268-1270.
    [32] 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. 2016. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nature Biotechnology, 34(1):78-83.
    [33] Hsu PD, Lander ES, Zhang F. 2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell, 157(6):1262-1278.
    [34] Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li YQ, Fine EJ, Wu XB, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F. 2013. DNA targeting specificity of RNA-guided Cas9 nucleases. Nature Biotechnology, 31(9):827-832.
    [35] Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096):816-821.
    [36] Kistler KE, Vosshall LB, Matthews BJ. 2015. Genome engineering with CRISPR-Cas9 in the mosquito Aedes aegypti. Cell Reports, 11(1):51-60.
    [37] Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng ZL, Joung JK. 2016. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature, 529(7587):490-495.
    [38] Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng ZL, Gonzales APW, Li ZY, Peterson RT, Yeh JRJ, Aryee MJ, Joung JK. 2015. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature, 523(7561):481-485.
    [39] Kondo S, Ueda R. 2013. Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genetics, 195(3):715-721.
    [40] Li XY, Fan DD, Zhang W, Liu GC, Zhang L, Zhao L, Fang XD, Chen L, Dong Y, Chen Y, Ding Y, Zhao RP, Feng MJ, Zhu YB, Feng Y, Jiang XT, Zhu DY, Xiang H, Feng XK, Li SC, Wang J, Zhang GJ, Kronforst MR, Wang W. 2015a. Outbred genome sequencing and CRISPR/Cas9 gene editing in butterflies. Nature Communications, 6:8212.
    [41] Li ZQ, You L, Zeng BS, Ling L, Xu J, Chen X, Zhang ZJ, Palli SR, Huang YP, Tan AJ. 2015b. Ectopic expression of ecdysone oxidase impairs tissue degeneration in Bombyx mori. Proceedings of the Royal Society of London B:Biological Sciences, 282(1809):20150513.
    [42] Ling L, Ge X, Li ZQ, Zeng BS, Xu J, Chen X, Shang P, James AA, Huang YP, Tan AJ. 2015. MiR-2 family targets awd and fng to regulate wing morphogenesis in Bombyx mori. RNA Biology, 12(7):742-748.
    [43] Liu YY, Ma SY, Wang XG, Chang JS, Gao J, Shi R, Zhang JD, Lu W, Liu Y, Zhao P, Xia QY. 2014. Highly efficient multiplex targeted mutagenesis and genomic structure variation in Bombyx mori cells using CRISPR/Cas9. Insect Biochemistry and Molecular Biology, 49:35-42.
    [44] Ma HH, Naseri A, Reyes-Gutierrez P, Wolfe SA, Zhang SJ, Pederson T. 2015. Multicolor CRISPR labeling of chromosomal loci in human cells. Proceedings of the National Academy of Sciences of the United States of America, 112(10):3002-3007.
    [45] Ma SY, Chang JS, Wang XG, Liu YY, Zhang JD, Lu W, Gao J, Shi R, Zhao P, Xia QY. 2014. CRISPR/Cas9 mediated multiplex genome editing and heritable mutagenesis of BmKu70 in Bombyx mori. Scientific Reports, 4:4489.
    [46] Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, Yang L, Church GM. 2013. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nature Biotechnology, 31(9):833-838.
    [47] Marcus JM, Ramos DM, Monteiro A. 2004. Germline transformation of the butterfly Bicyclus anynana. Proceedings of the Royal Society of London B:Biological Sciences, 271(Suppl 5):S263-S265.
    [48] Markert MJ, Zhang Y, Enuameh MS, Reppert SM, Wolfe SA, Merlin C. 2016. Genomic access to monarch migration using TALEN and CRISPR/Cas9-mediated targeted mutagenesis. G3:Genes Genomes Genetics, 6(4):905-915.
    [49] Martins S, Naish N, Walker AS, Morrison NI, Scaife S, Fu G, Dafa'alla T, Alphey L. 2012. Germline transformation of the diamondback moth, Plutella xylostella L., using the piggyBac transposable element. Insect Molecular Biology, 21(4):414-421.
    [50] Nakade S, Tsubota T, Sakane Y, Kume S, Sakamoto N, Obara M, Daimon T, Sezutsu H, Yamamoto T, Sakuma T, Suzuki KT. 2014. Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nature Communications, 5:5560.
    [51] Nelles DA, Fang MY, O'Connell MR, Xu JL, Markmiller SJ, Doudna JA, Yeo GW. 2016. Programmable RNA tracking in live cells with CRISPR/Cas9. Cell, 165(2):488-496.
    [52] Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI, Dohmae N, Ishitani R, Zhang F, Nureki O. 2014. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell, 156(5):935-949.
    [53] O'Connell MR, Oakes BL, Sternberg SH, East-Seletsky A, Kaplan M, Doudna JA. 2014. Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature, 516(7530):263-266.
    [54] Peters JM, Colavin A, Shi HD, Czarny TL, Larson MH, Wong S, Hawkins JS, Lu CHS, Koo BM, Marta E, Shiver AL, Whitehead EH, Weissman JS, Brown ED, Qi LS, Huang KC, Gross CA. 2016. A comprehensive, CRISPR-based functional analysis of essential genes in bacteria. Cell, 165(6):1493-1506.
    [55] Port F, Chen HM, Lee T, Bullock SL. 2014. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 111(29):E2967-E2976.
    [56] Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152(5):1173-1183.
    [57] Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell, 154(6):1380-1389.
    [58] Ren XJ, Sun J, Housden BE, Hu YH, Roesel C, Lin SL, Liu LP, Yang ZH, Mao DC, Sun LZ, Wu QJ, Ji JY, Xi JZ, Mohr SE, Xu J, Perrimon N, Ni JQ. 2013. Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9. Proceedings of the National Academy of Sciences of the United States of America, 110(47):19012-19017.
    [59] Ren XJ, Yang ZH, Mao DC, Chang Z, Qiao HH, Wang X, Sun J, Hu Q, Cui Y, Liu LP, Ji JY, Xu J, Ni JQ. 2014. Performance of the Cas9 nickase system in Drosophila melanogaster. G3:Genes Genomes Genetics, 4(10):1955-1962.
    [60] Richardson CD, Ray GJ, Dewitt MA, Curie GL, Corn JE. 2016. Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nature Biotechnology, 34(3):339-344.
    [61] Rio DC, Rubin GM. 1988. Identification and purification of a Drosophila protein that binds to the terminal 31-base-pair inverted repeats of the P transposable element. Proceedings of the National Academy of Sciences of the United States of America, 85(23):8929-8933.
    [62] Rubin GM, Spradling AC. 1982. Genetic transformation of Drosophila with transposable element vectors. Science, 218(4570):348-353.
    [63] Sebo ZL, Lee HB, Peng Y, Guo Y. 2014. A simplified and efficient germline-specific CRISPR/Cas9 system for Drosophila genomic engineering. Fly, 8(1):52-57.
    [64] Shalem O, Sanjana NE, Zhang F. 2015. High-throughput functional genomics using CRISPR-Cas9. Nature Reviews Genetics, 16(5):299-311.
    [65] Slaymaker IM, Gao LY, Zetsche B, Scott DA, Yan WX, Zhang F. 2016. Rationally engineered Cas9 nucleases with improved specificity. Science, 351(6268):84-88.
    [66] Tamura T, Thibert C, Royer C, Kanda T, Abraham E, Kamba M, Komoto N, Thomas JL, Mauchamp B, Chavancy G, Shirk P, Fraser M, Prudhomme JC, Couble P. 2000. Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nature Biotechnology, 18(1):81-84.
    [67] Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ, Joung JK. 2014. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nature Biotechnology, 32(6):569-576.
    [68] Venken KJT, Bellen HJ. 2007. Transgenesis upgrades for Drosophila melanogaster. Development, 134(20):3571-3584.
    [69] Wang YQ, Li ZQ, Xu J, Zeng BS, Ling L, You L, Chen YZ, Huang YP, Tan AJ. 2013. The CRISPR/Cas system mediates efficient genome engineering in Bombyx mori. Cell Research, 23(12):1414-1416.
    [70] Wei W, Xin HH, Roy B, Dai JB, Miao YG, Gao GJ. 2014. Heritable genome editing with CRISPR/Cas9 in the silkworm, Bombyx mori. PLoS One, 9(7):e101210.
    [71] World Health Organization. 2014. World Malaria Report 2014.
    [72] Xin HH, Zhang DP, Chen RT, Cai ZZ, Lu Y, Liang S, Miao YG. 2015. Transcription factor bmsage plays a crucial role in silk gland generation in silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology, 90(2):59-69.
    [73] Xue ZY, Ren MD, Wu MH, Dai JB, Rong YS, Gao GJ. 2014. Efficient gene knock-out and knock-in with transgenic Cas9 in Drosophila. G3:Genes Genomes Genetics, 4(5):925-929.
    [74] Yoshimi K, Kunihiro Y, Kaneko T, Nagahora H, Voigt B, Mashimo T. 2016. ssODN-mediated knock-in with CRISPR-Cas for large genomic regions in zygotes. Nature Communications, 7:10431.
    [75] Yu ZS, Ren MD, Wang ZX, Zhang B, Rong YS, Jiao RJ, Gao GJ. 2013. Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genetics, 195(1):289-291.
    [76] Zalatan JG, Lee ME, Almeida R, Gilbert LA, Whitehead EH, La Russa M, Tsai JC, Weissman JS, Dueber JE, Qi LS, Lim WA. 2015. Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell, 160(1-2):339-350.
    [77] Zeng BS, Zhan S, Wang YQ, Huang YP, Xu J, Liu Q, Li ZQ, Huang YP, Tan AJ. 2016. Expansion of CRISPR targeting sites in Bombyx mori. Insect Biochemistry and Molecular Biology, 72:31-40.
    [78] Zhang X, Koolhaas WH, Schnorrer F. 2014. A versatile two-step CRISPR-and RMCE-based strategy for efficient genome engineering in Drosophila. G3:Genes Genomes Genetics, 4(12):2409-2418.
    [79] Zhang ZJ, Aslam AFM, Liu XJ, Li MW, Huang YP, Tan AJ. 2015. Functional analysis of Bombyx Wnt1 during embryogenesis using the CRISPR/Cas9 system. Journal of Insect Physiology, 79:73-79.
    [80] Zhu GH, Xu J, Cui Z, Dong XT, Ye ZF, Niu DJ, Huang YP, Dong SL. 2016. Functional characterization of SlitPBP3 in Spodoptera litura by CRISPR/Cas9 mediated genome editing. Insect Biochemistry and Molecular Biology, 75:1-9.
    [81] Zhu L, Mon H, Xu J, Lee JM, Kusakabe T. 2015. CRISPR/Cas9-mediated knockout of factors in non-homologous end joining pathway enhances gene targeting in silkworm cells. Scientific Reports, 5:18103.
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  • 收稿日期:  2016-07-01
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