Tools for anopheles gambiae transgenesis

G3: Genes, Genomes, Genetics

Volumn 5, Issue 6, 2015, Pages 1151-1163

  Volohonsky, Gloria ^a   Terenzi, Olivier ^a   Soichot, Julien ^a   Naujoks, Daniel A ^b   Nolan, Tony ^b   Windbichler, Nikolai ^b   Kapps, Delphine ^a   Smidler, Andrea L ^a   Vittu, Anaïs ^a   Costa, Giulia ^c   Steinert, Stefanie ^a   Levashina, Elena A ^c   Blandin, Stéphanie A ^a   Marois, Eric ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

Circumsporozoite protein; Codon usage; Cre recombinase; Phage C31 attP docking sites; Puromycin; Transgenesis vectors

Indexed keywords

CRE RECOMBINASE; CODON; INTEGRASE; TRANSPOSASE; TRANSPOSON;

AGRICULTURAL PEST; ANOPHELES GAMBIAE; ARTICLE; CODON; CONTROLLED STUDY; DISEASE CARRIER; FEMALE; GENETIC MANIPULATION; GENOTYPE; MALARIA; MALE; MARKER GENE; MUTAGENESIS; NONHUMAN; PLASMID; PROMOTER REGION; TRANSGENICS; TRANSPOSON; ANIMAL; FLOW CYTOMETRY; GENE; GENE TRANSFER; GENE VECTOR; GENETICS; LARVA; METABOLISM; MICROINJECTION; MOLECULAR CLONING; MOSAICISM; NONMAMMALIAN EMBRYO; OVUM; REPORTER GENE; TRANSGENE; TRANSGENIC ANIMAL;

ANOPHELES GAMBIAE; HEXAPODA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOPHELES GAMBIAE; CLONING, MOLECULAR; CODON; DNA TRANSPOSABLE ELEMENTS; EMBRYO, NONMAMMALIAN; FLOW CYTOMETRY; GENE TRANSFER TECHNIQUES; GENES, INSECT; GENES, REPORTER; GENETIC VECTORS; INTEGRASES; LARVA; MICROINJECTIONS; MOSAICISM; OVUM; PLASMIDS; PROMOTER REGIONS, GENETIC; TRANSGENES; TRANSPOSASES;

EID: 84930846906     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.016808     Document Type: Article

References (57)

1. Alphey, L., 2014 Genetic control of mosquitoes. Annu. Rev. Entomol. 59: 205-224.
2. Alphey, L., M. Koukidou, and N. I. Morrison, 2014 Conditional dominant lethals - RIDL, pp. 101-111 in Transgenic Insects Techniques and Applications, edited by M. Q. Benedict. CABI, Wallingford, UK and Boston, MA.
3. Anderson, M. A., T. L. Gross, K. M. Myles, and Z. N. Adelman, 2010 Validation of novel promoter sequences derived from two endogenous ubiquitin genes in transgenic Aedes aegypti. Insect Mol. Biol. 19: 441-449.
4. Atella, G. C., M. A. Silva-Neto, D. M. Golodne, S. Arefin, and M. Shahabuddin, 2006 Anopheles gambiae lipophorin: characterization and role in lipid transport to developing oocyte. Insect Biochem. Mol. Biol. 36: 375-386.
5. Baena-Lopez, L. A., C. Alexandre, A. Mitchell, L. Pasakarnis, and J. P. Vincent, 2013 Accelerated homologous recombination and subsequent genome modification in Drosophila. Development 140: 4818-4825.
6. Benedict, M. Q., L. M. McNitt, A. J. Cornel, and F. H. Collins, 1999 A new marker, black, a useful recombination suppressor, In(2)2, and a balanced lethal for chromosome 2 of the mosquito Anopheles gambiae. Am. J. Trop. Med. Hyg. 61: 618-624.
7. Berghammer, A. J., M. Klingler, and E. A. Wimmer, 1999 A universal marker for transgenic insects. Nature 402: 370-371.
8. Bernardini, F., R. Galizi, M. Menichelli, P. A. Papathanos, V. Dritsou et al., 2014 Site-specific genetic engineering of the Anopheles gambiae Y chromosome. Proc. Natl. Acad. Sci. USA 111: 7600-7605.
9. 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.
10. Bordier, C., 1981 Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256: 1604-1607.
11. Catteruccia, F., T. Nolan, T. G. Loukeris, C. Blass, C. Savakis et al., 2000 Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405: 959-962.
12. Dimarcq, J. L., J. L. Imler, R. Lanot, R. A. Ezekowitz, J. A. Hoffmann et al., 1997 Treatment of l(2)mbn Drosophila tumorous blood cells with the steroid hormone ecdysone amplifies the inducibility of antimicrobial peptide gene expression. Insect Biochem. Mol. Biol. 27: 877-886.
13. Dong, Y., S. Das, C. Cirimotich, J. A. Souza-Neto, K. J. Mclean et al., 2011 Engineered anopheles immunity to Plasmodium infection. PLoS Pathog. 7: e1002458.
14. Dyck, V. A., J. Hendrichs, and A. S. Robinson (Editors), 2005 Sterile Insect Technique: Principles and Practice in Area-wide Integrated Pest Management, Springer, Dordrecht, The Netherlands.
15. Engler, C., and S. Marillonnet, 2013 Combinatorial DNA assembly using Golden Gate Cloning. Methods Mol. Biol. 1073: 141-156.
16. Fang, J., J. J. Qian, S. Yi, T. C. Harding, G. H. Tu et al., 2005 Stable antibody expression at therapeutic levels using the 2A peptide. Nat. Biotechnol. 23: 584-590.
17. Feil, R., 2007 Conditional somatic mutagenesis in the mouse using sitespecific recombinases. pp. 3-28 in Handb Exp Pharmacol: vol. 178. Edited by W. Rosenthal, Springer.
18. Fish, M. P., A. C. Groth, M. P. Calos, and R. Nusse, 2007 Creating transgenic Drosophila by microinjecting the site-specific phiC31 integrase mRNA and a transgene-containing donor plasmid. Nat. Protoc. 2: 2325-2331.
19. Franz, A. W., N. Jasinskiene, I. Sanchez-Vargas, A. T. Isaacs, M. R. Smith et al., 2011 Comparison of transgene expression in Aedes aegypti generated by mariner Mos1 transposition and PhiC31 site-directed recombination. Insect Mol. Biol. 20: 587-598.
20. Fu, G., R. S. Lees, D. Nimmo, D. Aw, L. Jin et al., 2010 Female-specific flightless phenotype for mosquito control. Proc. Natl. Acad. Sci. USA 107: 4550-4554.
21. Fuchs, S., T. Nolan, and A. Crisanti, 2013 Mosquito transgenic technologies to reduce Plasmodium transmission. Methods Mol. Biol. 923: 601-622.
22. Geissler, R., H. Scholze, S. Hahn, J. Streubel, U. Bonas et al., 2011 Transcriptional activators of human genes with programmable DNA-specificity. PLoS ONE 6: e19509.
23. Goedhart, J., D. Von Stetten, M. Noirclerc-Savoye, M. Lelimousin, L. Joosen et al., 2012 Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat. Commun. 3: 751.
24. Grossman, G. L., C. S. Rafferty, J. R. Clayton, T. K. Stevens, O. Mukabayire et al., 2001 Germline transformation of the malaria vector, Anopheles gambiae, with the piggyBac transposable element. Insect Mol. Biol. 10: 597-604.
25. Groth, A. C., M. Fish, R. Nusse, and M. P. Calos, 2004 Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775-1782.
26. James, A. A., B. T. Beerntsen, L. Capurro Mde, C. J. Coates, J. Coleman et al., 1999 Controlling malaria transmission with genetically-engineered, Plasmodium-resistant mosquitoes: milestones in a model system. Parassitologia 41: 461-471.
27. Kanegae, Y., G. Lee, Y. Sato, M. Tanaka, M. Nakai et al., 1995 Efficient gene activation in mammalian cells by using recombinant adenovirus expressing site-specific Cre recombinase. Nucleic Acids Res. 23: 3816-3821.
28. Kokoza, V., A. Ahmed, E. A. Wimmer, and A. S. Raikhel, 2001 Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac. [3xP3-EGFP afm] Insect Biochem. Mol. Biol. 31: 1137-1143.
29. Kokoza, V. A., and A. S. Raikhel, 2011 Targeted gene expression in the transgenic Aedes aegypti using the binary Gal4-UAS system. Insect Biochem. Mol. Biol. 41: 637-644.
30. Labbe, G. M., D. D. Nimmo, and L. Alphey, 2010 piggybac- and PhiC31-mediated genetic transformation of the Asian tiger mosquito, Aedes albopictus (Skuse). PLoS Negl. Trop. Dis. 4: e788.
31. Lynd, A., and G. J. Lycett, 2012 Development of the bi-partite Gal4-UAS system in the African malaria mosquito, Anopheles gambiae. PLoS ONE 7: e31552.
32. Marinotti, O., L. Capurro Mde, X. Nirmala, E. Calvo, and A. A. James, 2006 Structure and expression of the lipophorin-encoding gene of the malaria vector, Anopheles gambiae. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 144: 101-109.
33. Marinotti, O., N. Jasinskiene, A. Fazekas, S. Scaife, G. Fu et al., 2013 Development of a population suppression strain of the human malaria vector mosquito, Anopheles stephensi. Malar. J. 12: 142.
34. Marois, E., C. Scali, J. Soichot, C. Kappler, E. A. Levashina et al., 2012 High-throughput sorting of mosquito larvae for laboratory studies and for future vector control interventions. Malar. J. 11: 302.
35. Meredith, J. M., S. Basu, D. D. Nimmo, I. Larget-Thiery, E. L. Warr 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.
36. Meredith, J. M., A. Underhill, C. C. McArthur, and P. Eggleston, 2013 Next-generation site-directed transgenesis in the malaria vector mosquito Anopheles gambiae: self-docking strains expressing germline-specific phiC31 integrase. PLoS ONE 8: e59264.
37. Mindrinos, M., F. Katagiri, G. L. Yu, and F. M. Ausubel, 1994 The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089-1099.
38. Nimmo, D. D., L. Alphey, J. M. Meredith, and P. Eggleston, 2006 High efficiency site-specific genetic engineering of the mosquito genome. Insect Mol. Biol. 15: 129-136.
39. Nolan, T., E. Petris, H.M. Muller, A. Cronin, F. Catteruccia et al., 2011 Analysis of two novel midgut-specific promoters driving transgene expression in Anopheles stephensi mosquitoes. PLoS ONE 6: e16471.
40. Panáková, D., H. Sprong, E. Marois, C. Thiele, and S. Eaton, 2005 Lipoprotein particles are required for Hedgehog and Wingless signalling. Nature 435: 58-65.
41. Papathanos, P. A., N. Windbichler, M. Menichelli, A. Burt, and A. Crisanti, 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.
42. Pfeiffer, B. D., T. T. Ngo, K. L. Hibbard, C. Murphy, A. Jenett et al., 2010 Refinement of tools for targeted gene expression in Drosophila. Genetics 186: 735-755.
43. Pondeville, E., N. Puchot, J. M. Meredith, A. Lynd, K. D. Vernick et al., 2014 Efficient PhiC31 integrase-mediated site-specific germline transformation of Anopheles gambiae. Nat. Protoc. 9: 1698-1712.
44. Redemann, S., S. Schloissnig, S. Ernst, A. Pozniakowsky, S. Ayloo et al., 2011 Codon adaptation-based control of protein expression in C. elegans. Nat. Methods 8: 250-252.
45. Rong, Y. S., and K. G. Golic, 2000 Gene targeting by homologous recombination in Drosophila. Science 288: 2013-2018.
46. Rono, M. K., M. M. Whitten, M. Oulad-Abdelghani, E. A. Levashina, and E. Marois, 2010 The major yolk protein vitellogenin interferes with the anti-plasmodium response in the malaria mosquito Anopheles gambiae. PLoS Biol. 8: e1000434.
47. Sambrook, J., E. F. Fritsch, and T. Maniatis, 1989 "Molecular Cloning." A Laboratory Manual, CSH Laboratory Press, Cold Spring Harbor, NY.
48. Scali, C., T. Nolan, I. Sharakhov, M. Sharakhova, A. Crisanti et al., 2007 Post-integration behavior of a Minos transposon in the malaria mosquito Anopheles stephensi. Mol. Genet. Genomics 278: 575-584.
49. Scott, M. J., N. I. Morrison, and G. S. Simmons, 2014 Transgenic approaches for sterile insect control of Dipteran livestock pests and Lepidopteran crop pests, pp. 152-167 in Transgenic Insects Techniques and Applications, edited by M. Q. Benedict CABI, Wallingford, UK and Boston, MA.
50. Sethuraman, N., M. J. Fraser, Jr, P. Eggleston, and D. A. O'Brochta, 2007 Post-integration stability of piggyBac in Aedes aegypti. Insect Biochem. Mol. Biol. 37: 941-951.
51. Smidler, A. L., O. Terenzi, J. Soichot, E. A. Levashina, and E. Marois, 2013 Targeted mutagenesis in the malaria mosquito using TALE nucleases. PLoS ONE 8: e74511.
52. Sprong, H., M. Suchanek, S. M. Van Dijk, A. Van Remoortere, J. Klumperman et al., 2006 Aberrant receptor-mediated endocytosis of Schistosoma mansoni glycoproteins on host lipoproteins. PLoS Med. 3: e253.
53. St. Johnston, D., 2013 Using mutants, knockdowns, and transgenesis to investigate gene function in Drosophila. Wiley Interdiscip Rev Dev Biol. 2: 587-613.
54. Thorpe, H. M., and M. C. Smith, 1998 In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc. Natl. Acad. Sci. USA 95: 5505-5510.
55. Wang, S., and M. Jacobs-Lorena, 2013 Genetic approaches to interfere with malaria transmission by vector mosquitoes. Trends Biotechnol. 31: 185-193.
56. Yan, J., X. Yang, M. A. Mortin, and M. Shahabuddin, 2009 Malaria sporozoite antigen-directed genome-wide response in transgenic Drosophila. Genesis 47: 196-203.
57. Yoshida, N., R. S. Nussenzweig, P. Potocnjak, V. Nussenzweig, and M. Aikawa, 1980 Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207: 71-73.