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Malaria pp 601-622 | Cite as

Mosquito Transgenic Technologies to Reduce Plasmodium Transmission

  • Silke Fuchs
  • Tony Nolan
  • Andrea CrisantiEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 923)

Abstract

The ability to introduce genetic constructs of choice into the genome of Anopheles mosquitoes provides a valuable tool to study the molecular interactions between the Plasmodium parasite and its insect host. In the long term, this technology could potentially offer new ways to control vector-borne diseases through the suppression of target mosquito populations or through the introgression of traits that preclude pathogen transmission. Here, we describe in detail protocols for the generation of transgenic Anopheles gambiae mosquitoes based on germ-line transformation using either modified transposable elements or the site-specific PhiC31 recombinase.

Key words

Genetic modification Mosquito Transposable element Transgenic Embryo injection piggyBac PhiC31 Plasmodium Effector gene 

References

  1. 1.
    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 95:3743–3747PubMedCrossRefGoogle Scholar
  2. 2.
    Coates CJ et al (1998) Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 95:3748–3751PubMedCrossRefGoogle Scholar
  3. 3.
    Catteruccia F et al (2000) Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405:959–962PubMedCrossRefGoogle Scholar
  4. 4.
    Kokoza V et al (2001) Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac[3xP3-EGFP afm]. Insect Biochem Mol Biol 31:1137–1143PubMedCrossRefGoogle Scholar
  5. 5.
    Nolan T et al (2002) piggyBac-mediated germline transformation of the malaria mosquito Anopheles stephensi using the red fluorescent protein dsRED as a selectable marker. J Biol Chem 277:8759–8762PubMedCrossRefGoogle Scholar
  6. 6.
    Allen ML et al (2001) Stable, germ-line transformation of Culex quinquefasciatus (Diptera: Culicidae). J Med Entomol 38:701–710PubMedCrossRefGoogle Scholar
  7. 7.
    Grossman GL et al (2001) Germline transformation of the malaria vector, Anopheles gambiae, with the piggyBac transposable element. Insect Mol Biol 10:597–604PubMedCrossRefGoogle Scholar
  8. 8.
    Perera OP et al (2002) Germ-line transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac/EGFP transposon vector is routine and highly efficient. Insect Mol Biol 11:291–297PubMedCrossRefGoogle Scholar
  9. 9.
    Handler AM (2001) A current perspective on insect gene transformation. Insect Biochem Mol Biol 31:111–128PubMedCrossRefGoogle Scholar
  10. 10.
    Tamura T et al (2000) Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat Biotechnol 18:81–84PubMedCrossRefGoogle Scholar
  11. 11.
    Nolan T et al (2011) Analysis of two novel midgut-specific promoters driving transgene expression in Anopheles stephensi mosquitoes. PLoS One 6:e16471PubMedCrossRefGoogle Scholar
  12. 12.
    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:e14587PubMedCrossRefGoogle Scholar
  13. 13.
    Thorpe HM et al (2000) Control of directionality in the site-specific recombination system of the Streptomyces phage phi C31. Mol Microbiol 38:232–241PubMedCrossRefGoogle Scholar
  14. 14.
    Chater KF et al (1981) Dispensable sequences and packaging constraints of DNA from the Streptomyces temperate phage phi C31. Gene 15:249–256PubMedCrossRefGoogle Scholar
  15. 15.
    Venken KJ et al (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314:1747–1751PubMedCrossRefGoogle Scholar
  16. 16.
    Geurts AM et al (2003) Gene transfer into genomes of human cells by the sleeping beauty transposon system. Mol Ther 8:108–117PubMedCrossRefGoogle Scholar
  17. 17.
    Moreira LA et al (2002) Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J Biol Chem 277:40839–40843PubMedCrossRefGoogle Scholar
  18. 18.
    Ito J et al (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417:452–455PubMedCrossRefGoogle Scholar
  19. 19.
    Adelman ZN et al (2002) Development and applications of transgenesis in the yellow fever mosquito, Aedes aegypti. Mol Biochem Parasitol 121:1–10PubMedCrossRefGoogle Scholar
  20. 20.
    Kokoza V et al (2001) Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac[3xP3-EGFP afm]. Insect Biochem Mol Biol 31:1137–1143PubMedCrossRefGoogle Scholar
  21. 21.
    Jasinskiene N et al (2000) Structure of hermes integrations in the germline of the yellow fever mosquito, Aedes aegypti. Insect Mol Biol 9:11–18PubMedCrossRefGoogle Scholar
  22. 22.
    Pinkerton AC et al (2000) Green fluorescent protein as a genetic marker in transgenic Aedes aegypti. Insect Mol Biol 9:1–10PubMedCrossRefGoogle Scholar
  23. 23.
    Moreira LA et al (2000) Robust gut-specific gene expression in transgenic Aedes aegypti mosquitoes. Proc Natl Acad Sci USA 97:10895–10898PubMedCrossRefGoogle Scholar
  24. 24.
    Coates CJ et al (2000) Purified mariner (Mos1) transposase catalyzes the integration of marked elements into the germ-line of the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol 30:1003–1008PubMedCrossRefGoogle Scholar
  25. 25.
    Nimmo DD et al (2006) High efficiency site-specific genetic engineering of the mosquito genome. Insect Mol Biol 15:129–136PubMedCrossRefGoogle Scholar
  26. 26.
    Franz AW et al (2011) Comparison of transgene expression in Aedes aegypti generated by mariner Mos1 transposition and PhiC31 site-directed recombination. Insect Mol Biol 20:587–598PubMedCrossRefGoogle Scholar
  27. 27.
    Windbichler N et al (2008) Targeting the X chromosome during spermatogenesis induces Y chromosome transmission ratio distortion and early dominant embryo lethality in Anopheles gambiae. PLoS Genet 4:e1000291PubMedCrossRefGoogle Scholar
  28. 28.
    Lobo NF et al (2006) High efficiency germ-line transformation of mosquitoes. Nat Protoc 1:1312–1317PubMedCrossRefGoogle Scholar
  29. 29.
    Windbichler N et al (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473:212–215PubMedCrossRefGoogle Scholar
  30. 30.
    Groth AC et al (2004) Construction of ­transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166:1775–1782PubMedCrossRefGoogle Scholar
  31. 31.
    O’Neill SL et al (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141–144PubMedCrossRefGoogle Scholar
  32. 32.
    Bossin H (2005) Microinjection methods for Anopheles embryos. MR4 vector component technical manual. Malaria Research and Reference Reagent Resource Center, Manassas (VA)Google Scholar
  33. 33.
    Handler AM et al (1998) The lepidopteran transposon vector, piggyBac, mediates germ-line transformation in the Mediterranean fruit fly. Proc Natl Acad Sci USA 95:7520–7525PubMedCrossRefGoogle Scholar
  34. 34.
    Sambrook J et al (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NYGoogle Scholar
  35. 35.
    Papathanos PA et al (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 10:65PubMedCrossRefGoogle Scholar
  36. 36.
    Kim W et al (2004) Ectopic expression of a cecropin transgene in the human malaria vector mosquito Anopheles gambiae (Diptera: Culicidae): effects on susceptibility to Plasmodium. J Med Entomol 41:447–455PubMedCrossRefGoogle Scholar
  37. 37.
    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:e1001003PubMedCrossRefGoogle Scholar
  38. 38.
    Isaacs AT et al (2011) Engineered resistance to Plasmodium falciparum development in transgenic Anopheles stephensi. PLoS Pathog 7:e1002017PubMedCrossRefGoogle Scholar
  39. 39.
    Abraham EG et al (2005) Driving midgut-specific expression and secretion of a foreign protein in transgenic mosquitoes with AgAper1 regulatory elements. Insect Mol Biol 14:271–279PubMedCrossRefGoogle Scholar
  40. 40.
    Jasinskiene N et al (2007) Genetic control of malaria parasite transmission: threshold levels for infection in an avian model system. Am J Trop Med Hyg 76:1072–1078PubMedGoogle Scholar
  41. 41.
    Lombardo F et al (2005) An Anopheles gambiae salivary gland promoter analysis in Drosophila melanogaster and Anopheles stephensi. Insect Mol Biol 14:207–216PubMedCrossRefGoogle Scholar
  42. 42.
    Yoshida S, Watanabe H (2006) Robust salivary gland-specific transgene expression in Anopheles stephensi mosquito. Insect Mol Biol 15:403–410PubMedCrossRefGoogle Scholar
  43. 43.
    Dinglasan RR et al (2003) Monoclonal antibody MG96 completely blocks Plasmodium yoelii development in Anopheles stephensi. Infect Immun 71:6995–7001PubMedCrossRefGoogle Scholar
  44. 44.
    Yoshida S et al (1999) A single-chain antibody fragment specific for the Plasmodium berghei ookinete protein Pbs21 confers transmission blockade in the mosquito midgut. Mol Biochem Parasitol 104:195–204PubMedCrossRefGoogle Scholar
  45. 45.
    Li F et al (2005) An anti-Chitinase malaria transmission-blocking single-chain antibody as an effector molecule for creating a Plasmodium falciparum-refractory mosquito. J Infect Dis 192:878–887PubMedCrossRefGoogle Scholar
  46. 46.
    Lal AA et al (2001) Anti-mosquito midgut antibodies block development of Plasmodium falciparum and Plasmodium vivax in multiple species of Anopheles mosquitoes and reduce vector fecundity and survivorship. Proc Natl Acad Sci USA 98:5228–5233PubMedCrossRefGoogle Scholar
  47. 47.
    Arrighi RB et al (2005) Laminin and the malaria parasite’s journey through the mosquito midgut. J Exp Biol 208:2497–2502PubMedCrossRefGoogle Scholar
  48. 48.
    Osta MA et al (2004) Effects of mosquito genes on Plasmodium development. Science 303:2030–2032PubMedCrossRefGoogle Scholar
  49. 49.
    Blandin S et al (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116:661–670PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Life SciencesImperial CollegeLondonUK

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