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

Volumn 112, Issue 13, 2015, Pages 4038-4043

  Basu, Sanjay ^a   Aryan, Azadeh ^a   Overcash, Justin M ^a   Samuel, Glady Hazitha ^a   Anderson, Michelle A E ^a   Dahlem, Timothy J ^b   Myles, Kevin M ^a   Adelman, Zach N ^a  

^a Fralin Life Science Institute   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Aedes; CRISPR; Recombination; TALEN; Transgenic

Indexed keywords

DOUBLE STRANDED RNA; GUIDE RNA; KU ANTIGEN; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE;

AEDES AEGYPTI; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA END JOINING REPAIR; GENE INSERTION; GENE MUTATION; GENE SILENCING; MICROINJECTION; MUTAGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; AEDES; ANIMAL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DIMERIZATION; DNA REPAIR; EXON; GENE EXPRESSION REGULATION; GENE VECTOR; GENETIC RECOMBINATION; GENETICS; GENOME; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION; RNA EDITING; TEMPERATURE; TRANSGENE;

AEDES AEGYPTI;

AEDES; ANIMALS; BASE SEQUENCE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; DIMERIZATION; DNA REPAIR; EXONS; GENE SILENCING; GENETIC VECTORS; GENOME; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; PLASMIDS; POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; RNA EDITING; RNA, DOUBLE-STRANDED; TEMPERATURE; TRANSGENES;

EID: 84926051661     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1502370112     Document Type: Article

References (49)

1. Hoffmann AA, et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476(7361):454-457.
2. Alphey L (2014) Genetic control of mosquitoes. Annu Rev Entomol 59:205-224.
3. Windbichler N, et al. (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473(7346):212-215.
4. Oye KA, et al. (2014) Biotechnology. Regulating gene drives. Science 345(6197): 626-628.
5. Esvelt KM, Smidler AL, Catteruccia F, Church GM (2014) Concerning RNA-guided gene drives for the alteration of wild populations [published online ahead of print July 17,2014]. eLife, 10.7554/eLife.03401.
6. Terns MP, Terns RM (2011) CRISPR-based adaptive immune systems. Curr Opin Microbiol 14(3):321-327.
7. Bassett AR, Tibbit C, Ponting CP, Liu J-L (2013) Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Reports 4(1):220-228.
8. Aryan A, Anderson MA, Myles KM, Adelman ZN (2013) TALEN-based gene disruption in the dengue vector Aedes aegypti. PLoS ONE 8(3):e60082.
9. Smidler AL, Terenzi O, Soichot J, Levashina EA, Marois E (2013) Targeted mutagenesis in the malaria mosquito using TALE nucleases. PLoS ONE 8(8):e74511.
10. Cermak T, et al. (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39(12):e82.
11. Miller JC, et al. (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25(7):778-785.
12. Söllü C, et al. (2010) Autonomous zinc-finger nuclease pairs for targeted chromosomal deletion. Nucleic Acids Res 38(22):8269-8276.
13. Szczepek M, et al. (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25(7):786-793.
14. Doyon Y, et al. (2011) Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Methods 8(1):74-79.
15. Miller LH, et al. (1987) Stable integration and expression of a bacterial gene in the mosquito Anopheles gambiae. Science 237(4816):779-781.
16. McGrane V, Carlson JO, Miller BR, Beaty BJ (1988) Microinjection of DNA into Aedes triseriatus ova and detection of integration. Am J Trop Med Hyg 39(5):502-510.
17. Morris AC, Eggleston P, Crampton JM (1989) Genetic transformation of the mosquito Aedes aegypti by micro-injection of DNA. Med Vet Entomol 3(1):1-7.
18. Coates CJ, Jasinskiene N, Miyashiro L, James AA (1998) Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 95(7):3748-3751.
19. Jasinskiene N, et al. (1998) Stable transformation of the yellow fever mosquito, Aedes aegypti, with the Hermes element from the housefly. Proc Natl Acad Sci USA 95(7): 3743-3747.
20. Corby-Harris V, et al. (2010) Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathog 6(7):e1001003.
21. Kokoza V, et al. (2010) Blocking of Plasmodium transmission by cooperative action of Cecropin A and Defensin A in transgenic Aedes aegypti mosquitoes. Proc Natl Acad Sci USA 107(18):8111-8116.
22. Meredith JM, et al. (2011) Site-specific integration and expression of an anti-malarial gene in transgenic Anopheles gambiae significantly reduces Plasmodium infections. PLoS ONE 6(1):e14587.
23. Thomas DD, Donnelly CA, Wood RJ, Alphey LS (2000) Insect population control using a dominant, repressible, lethal genetic system. Science 287(5462):2474-2476.
24. Phuc HK, et al. (2007) Late-acting dominant lethal genetic systems and mosquito control. BMC Biol 5:11.
25. Fu G, et al. (2010) Female-specific flightless phenotype for mosquito control. Proc Natl Acad Sci USA 107(10):4550-4554.
26. Galizi R, et al. (2014) A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nat Commun 5:3977.
27. Liesch J, Bellani LL, Vosshall LB (2013) Functional and genetic characterization of neuropeptide Y-like receptors in Aedes aegypti. PLoS Negl Trop Dis 7(10):e2486.
28. McMeniman CJ, Corfas RA, Matthews BJ, Ritchie SA, Vosshall LB (2014) Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156(5):1060-1071.
29. Bernardini F, et al. (2014) Site-specific genetic engineering of the Anopheles gambiae Y chromosome. Proc Natl Acad Sci USA 111(21):7600-7605.
30. Lieber MR (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79:181-211.
31. Williams GJ, et al. (2014) Structural insights into NHEJ: Building up an integrated picture of the dynamic DSB repair super complex, one component and interaction at a time. DNA Repair (Amst) 17(0):110-120.
32. Beumer KJ, et al. (2008) Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases. Proc Natl Acad Sci USA 105(50):19821-19826.
33. Ma S, et al. (2014) CRISPR/Cas9 mediated multiplex genome editing and heritable mutagenesis of BmKu70 in Bombyx mori. Sci Rep 4:4489.
34. Aryan A, Anderson MAE, Myles KM, Adelman ZN (2013) Germline excision of transgenes in Aedes aegypti by homing endonucleases. Sci Rep 3:1603.
35. Dahlem TJ, et al. (2012) Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet 8(8):e1002861.
36. Beumer KJ, et al. (2013) Comparing zinc finger nucleases and transcription activatorlike effector nucleases for gene targeting in Drosophila. G3 3(10):1717-1725.
37. Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346(6213):1258096.
38. Wang T, Wei JJ, Sabatini DM, Lander ES (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science 343(6166):80-84.
39. Gratz SJ, et al. (2014) Highly specific and efficient CRISPR/Cas9-catalyzed homologydirected repair in Drosophila. Genetics 196(4):961-971.
40. Amenya DA, et al. (2010) Comparative fitness assessment of Anopheles stephensi transgenic lines receptive to site-specific integration. Insect Mol Biol 19(2):263-269.
41. Paton D, Underhill A, Meredith J, Eggleston P, Tripet F (2013) Contrasted Fitness Costs of Docking and Antibacterial Constructs in the EE and EVida3 Strains Validates Two-Phase Anopheles gambiae Genetic Transformation System. PLoS ONE 8(6):e67364.
42. Isaacs AT, et al. (2012) Transgenic Anopheles stephensi coexpressing single-chain antibodies resist Plasmodium falciparum development. Proc Natl Acad Sci USA 109(28):E1922-E1930.
43. Nimmo DD, Alphey L, Meredith JM, Eggleston P (2006) High efficiency site-specific genetic engineering of the mosquito genome. Insect Mol Biol 15(2):129-136.
44. Labbé GM, Nimmo DD, Alphey L (2010) piggybac- and PhiC31-mediated genetic transformation of the Asian tiger mosquito, Aedes albopictus (Skuse). PLoS Negl Trop Dis 4(8):e788.
45. Aryan A, Myles KM, Adelman ZN (2014) Targeted genome editing in Aedes aegypti using TALENs. Methods 69(1):38-45.
46. Hu R, Wallace J, Dahlem TJ, Grunwald DJ, O'Connell RM (2013) Targeting human microRNA genes using engineered Tal-effector nucleases (TALENs). PLoS ONE 8(5): e63074.
47. Doyle EL, et al. (2012) TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: Tools for TAL effector design and target prediction. Nucleic Acids Res 40(web server issue):W117-W122.
48. Anderson MA, Gross TL, Myles KM, Adelman ZN (2010) Validation of novel promoter sequences derived from two endogenous ubiquitin genes in transgenic Aedes aegypti . Insect Mol Biol 19(4):441-449.
49. Hill JT, et al. (2014) Poly peak parser: Method and software for identification of unknown indels using sanger sequencing of polymerase chain reaction products. Dev Dyn 243(12):1632-1636.