Targeted Mutagenesis in the Malaria Mosquito Using TALE Nucleases

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Smidler, Andrea L ^a,b,c   Terenzi, Olivier ^a,b   Soichot, Julien ^a,b   Levashina, Elena A ^a,b,d   Marois, Eric ^a,b  

^a INSERM   (France)

^b CNRS   (France)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEASE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; ENDONUCLEASE; INSECT PROTEIN; MUTANT PROTEIN; TEP1 PROTEIN, ANOPHELES GAMBIAE; TRANSACTIVATOR PROTEIN;

ANIMAL TISSUE; ANOPHELES GAMBIAE; ARTICLE; BIOTECHNOLOGY; CONTROLLED STUDY; GENE; GENE DISRUPTION; GENE EXPRESSION; GENE ISOLATION; GENETIC ANALYSIS; GENETIC MANIPULATION; INFECTION SENSITIVITY; MALARIA CONTROL; MUTAGENESIS; MUTANT; NONHUMAN; PLASMODIUM BERGHEI; PROTEIN SYNTHESIS INHIBITION; REVERSE GENETICS; RNA INTERFERENCE; TEP1 GENE; TRANSGENE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENE TARGETING; GENETICS; HUMAN; MALARIA; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; BASE SEQUENCE; ENDONUCLEASES; GENE TARGETING; GENES, INSECT; HUMANS; INSECT PROTEINS; MALARIA; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTANT PROTEINS; MUTATION; PLASMODIUM BERGHEI; TRANS-ACTIVATORS;

EID: 84881574119     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074511     Document Type: Article

References (45)

1. WHO (2012) Malaria Report.
2. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129-149. doi:10.1126/science.1076181. PubMed: 12364791.
3. Catteruccia F, (2007) Malaria vector control in the third millennium: progress and perspectives of molecular approaches (in press). Pest Manag Sci.
4. 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 Genetic Transformation System. PLOS ONE 8: e67364. doi:10.1371/journal.pone.0067364. PubMed: 23840679.
5. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, et al. (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326: 1509-1512. doi:10.1126/science.1178811. PubMed: 19933107.
6. Moscou MJ, Bogdanove AJ, (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326: 1501. doi:10.1126/science.1178817. PubMed: 19933106.
7. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143-148. doi:10.1038/nbt.1755. PubMed: 21179091.
8. Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, et al. (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res, 39: e82-. PubMed: 21493687.
9. Geissler R, Scholze H, Hahn S, Streubel J, Bonas U, et al. (2011) Transcriptional activators of human genes with programmable DNA-specificity. PLOS ONE 6: e19509. doi:10.1371/journal.pone.0019509. PubMed: 21625585.
10. Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, et al. (2012) FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30: 460-465. doi:10.1038/nbt.2170. PubMed: 22484455.
11. Chen S, Oikonomou G, Chiu CN, Niles BJ, Liu J, et al. (2013) A large-scale in vivo analysis reveals that TALENs are significantly more mutagenic than ZFNs generated using context-dependent assembly. Nucleic Acids Res.
12. Move over ZFNs. Nat Biotechnol 29: 681-684. doi:10.1038/nbt.1935. PubMed: 21822235, (2011).
13. Huang P, Xiao A, Zhou M, Zhu Z, Lin S, et al. (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29: 699-700. doi:10.1038/nbt.1939. PubMed: 21822242.
14. Liu J, Li C, Yu Z, Huang P, Wu H, et al. (2012) Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy. J Genet Genomics 39: 209-215. doi:10.1016/j.jgg.2012.04.003. PubMed: 22624882.
15. Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C, et al. (2012) Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci U S A 109: 17382-17387. doi:10.1073/pnas.1211446109. PubMed: 23027955.
16. Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, et al. (2012) In vivo genome editing using a high-efficiency TALEN system. Nature 491: 114-118. doi:10.1038/nature11537. PubMed: 23000899.
17. Cade L, Reyon D, Hwang WY, Tsai SQ, Patel S, et al. (2012) Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Res 40: 8001-8010. doi:10.1093/nar/gks518. PubMed: 22684503.
18. Watanabe T, Ochiai H, Sakuma T, Horch HW, Hamaguchi N, et al. (2012) Non-transgenic genome modifications in a hemimetabolous insect using zinc-finger and TAL effector nucleases. Nat Commun 3: 1017. doi:10.1038/ncomms2020. PubMed: 22910363.
19. Sung YH, Baek IJ, Kim DH, Jeon J, Lee J, et al. (2013) Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol 31: 23-24. doi:10.1038/nbt.2477. PubMed: 23302927.
20. Aryan A, Anderson MA, Myles KM, Adelman ZN, (2013) TALEN-Based Gene Disruption in the Dengue Vector Aedes aegypti. PLOS ONE 8: e60082. doi:10.1371/journal.pone.0060082. PubMed: 23555893.
21. Li T, Liu B, Spalding MH, Weeks DP, Yang B, (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30: 390-392. doi:10.1038/nbt.2199. PubMed: 22565958.
22. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661-670. doi:10.1016/S0092-8674(04)00173-4. PubMed: 15006349.
23. Blandin SA, Wang-Sattler R, Lamacchia M, Gagneur J, Lycett G, et al. (2009) Dissecting the genetic basis of resistance to malaria parasites in Anopheles gambiae. Science 326: 147-150. doi:10.1126/science.1175241. PubMed: 19797663.
24. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLOS Pathog 2: e52. doi:10.1371/journal.ppat.0020052. PubMed: 16789837.
25. Molina-Cruz A, Garver LS, Alabaster A, Bangiolo L, Haile A, et al. (2013) The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340: 984-987. doi:10.1126/science.1235264. PubMed: 23661646.
26. Baxter RH, Chang CI, Chelliah Y, Blandin S, Levashina EA, et al. (2007) Structural basis for conserved complement factor-like function in the antimalarial protein TEP1. Proc Natl Acad Sci U S A 104: 11615-11620. doi:10.1073/pnas.0704967104. PubMed: 17606907.
27. Papathanos PA, Windbichler N, Menichelli M, Burt A, Crisanti A, (2009) The vasa regulatory region mediates germline expression and maternal transmission of proteins in the malaria mosquito Anopheles gambiae: a versatile tool for genetic control strategies. BMC Mol Biol 10: 65. doi:10.1186/1471-2199-10-65. PubMed: 19573226.
28. Marois E, Scali C, Soichot J, Kappler C, Levashina EA, et al. (2012) High-throughput sorting of mosquito larvae for laboratory studies and for future vector control interventions. Malar J 11: 302. doi:10.1186/1475-2875-11-302. PubMed: 22929810.
29. Horn C, Wimmer EA, (2000) A versatile vector set for animal transgenesis. Dev Genes Evol 210: 630-637. doi:10.1007/s004270000110. PubMed: 11151300.
30. Szczepek M, Brondani V, Büchel J, Serrano L, Segal DJ, et al. (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25: 786-793. doi:10.1038/nbt1317. PubMed: 17603476.
31. Gupta A, Meng X, Zhu LJ, Lawson ND, Wolfe SA, (2011) Zinc finger protein-dependent and-independent contributions to the in vivo off-target activity of zinc finger nucleases. Nucleic Acids Res 39: 381-392. doi:10.1093/nar/gkq787. PubMed: 20843781.
32. Le BV, Williams M, Logarajah S, Baxter RH, (2012) Molecular basis for genetic resistance of Anopheles gambiae to Plasmodium: structural analysis of TEP1 susceptible and resistant alleles. PLOS Pathog 8: e1002958. PubMed: 23055931.
33. Blandin S, Levashina EA, (2004) Thioester-containing proteins and insect immunity. Mol Immunol 40: 903-908. doi:10.1016/j.molimm.2003.10.010. PubMed: 14698229.
34. Catteruccia F, Levashina EA, (2009) RNAi in the malaria vector, Anopheles gambiae. Methods Mol Biol 555: 63-75. doi:10.1007/978-1-60327-295-7_5. PubMed: 19495688.
35. Nsango SE, Abate L, Thoma M, Pompon J, Fraiture M, et al. (2012) Genetic clonality of Plasmodium falciparum affects the outcome of infection in Anopheles gambiae. Int J Parasitol 42: 589-595. doi:10.1016/j.ijpara.2012.03.008. PubMed: 22554991.
36. Degennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, et al. (2013) orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature.
37. Ghosh AK, Devenport M, Jethwaney D, Kalume DE, Pandey A, et al. (2009) Malaria parasite invasion of the mosquito salivary gland requires interaction between the Plasmodium TRAP and the Anopheles saglin proteins. PLOS Pathog 5: e1000265. PubMed: 19148273.
38. Bhattacharyya MK, Kumar N, (2001) Effect of xanthurenic acid on infectivity of Plasmodium falciparum to Anopheles stephensi. Int J Parasitol 31: 1129-1133. doi:10.1016/S0020-7519(01)00222-3. PubMed: 11429178.
39. Volz J, Müller HM, Zdanowicz A, Kafatos FC, Osta MA, (2006) A genetic module regulates the melanization response of Anopheles to Plasmodium. Cell Microbiol 8: 1392-1405. doi:10.1111/j.1462-5822.2006.00718.x. PubMed: 16922859.
40. Thailayil J, Magnusson K, Godfray HC, Crisanti A, Catteruccia F, (2011) Spermless males elicit large-scale female responses to mating in the malaria mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 108: 13677-13681. doi:10.1073/pnas.1104738108. PubMed: 21825136.
41. Meredith JM, Basu S, Nimmo DD, Larget-Thiery I, Warr EL, et al. (2011) Site-specific integration and expression of an anti-malarial gene in transgenic Anopheles gambiae significantly reduces Plasmodium infections. PLOS ONE 6: e14587. doi:10.1371/journal.pone.0014587. PubMed: 21283619.
42. Rono MK, Whitten MM, Oulad-Abdelghani M, Levashina EA, Marois E, (2010) The major yolk protein vitellogenin interferes with the anti-plasmodium response in the malaria mosquito Anopheles gambiae. PLOS Biol 8: e1000434. PubMed: 20652016.
43. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular cloning A laboratory manual. Cold Spring Harbor: CSH Laboratory Press.
44. Fraiture M, Baxter RH, Steinert S, Chelliah Y, Frolet C, et al. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5: 273-284. doi:10.1016/j.chom.2009.01.005. PubMed: 19286136.
45. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, et al. (2001) Conserved Role of a Complement-like Protein in Phagocytosis Revealed by dsRNA Knockout in Cultured Cells of the Mosquito, Anopheles gambiae. Cell 104: 709-718. doi:10.1016/S0092-8674(01)00267-7. PubMed: 11257225.