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Applications of insect transgenesis

Abstract

The recent establishment of broadly applicable genetic transformation systems will allow the analysis of gene function in diverse insect species. This will increase our understanding of developmental and evolutionary biology. Furthermore, insect transgenesis will provide new strategies for insect pest management and methods to impair the transmission of pathogens by human disease vectors. However, these powerful techniques must be applied with great care to avoid harm to our environment.

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Figure 1: 3×P3-EGFP marker gene expression in Diptera, Lepidoptera and Coleoptera.
Figure 2: Binary expression systems.

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References

  1. Rubin, G. M. & Spradling, A. C. Genetic transformation of Drosophila with transposable element vectors. Science 218, 348–353 (1982).

    Article  CAS  Google Scholar 

  2. O'Brochta, D. A. & Atkinson, P. W. Building the better bug. Sci. Am. 279, 90–95 (1998).

    Article  CAS  Google Scholar 

  3. Handler, A. M., Gomez, S. P. & O'Brochta, D. A. A functional analysis of the P-element gene–transfer vector in insects. Arch. Insect Biochem. Physiol. 22, 373–384 (1993).

    Article  CAS  Google Scholar 

  4. Rio, D. C. & Rubin, G. M. Identification and purification of a Drosophila protein that binds to the terminal 31-base-pair inverted repeats of the P transposable element. Proc. Natl Acad. Sci. USA 85, 8929–8933 (1988).

    Article  CAS  Google Scholar 

  5. Berghammer, A. J., Klingler, M. & Wimmer, E. A. A universal marker for transgenic insects. Nature 402, 370–371 (1999).

    Article  CAS  Google Scholar 

  6. Horn, C., Jaunich, B. & Wimmer, E. A. Highly sensitive, fluorescent transformation marker for Drosophila transgenesis. Dev. Genes Evol. 210, 623–629 (2000).

    Article  CAS  Google Scholar 

  7. Hediger, M., Niessen, N., Wimmer, E. A., Dübendorfer, A. & Bopp, D. Germline transformation of the housefly Musca domestica with the lepidopteran derived transposon piggyBac. Insect Mol. Biol. 10, 113–119 (2001).

    Article  CAS  Google Scholar 

  8. Kokoza, V., Ahmed, A., Wimmer, E. A. & Raikhel, A. S. Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac[3×P3–EGFPafm]. Insect Biochem. Mol. Biol. 31, 1137–1143 (2001).

    Article  CAS  Google Scholar 

  9. Ito, J., Ghosh, A., Moreira, L. A., Wimmer, E. A. & Jacobs-Lorena, M. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417, 452–455 (2002).

    Article  CAS  Google Scholar 

  10. Thomas, J. -L., Da Rocha, M., Besse, A., Mauchamp, B. & Chavancy, G. 3×P3EGFP marker as a powerful tool to facilitate the screening of the transgenic Bombyx mori L. Insect Biochem. Mol. Biol. 32, 247–253 (2002).

    Article  CAS  Google Scholar 

  11. Uhlír×ova, M., Asahina, M., Riddiford, L. M. & Jindra, M. Inducible transgenic expression of the Ftz-F1 nuclear receptor in the silkmoth Bombyx mori. Dev. Genes Evol. 212, 145–151 (2002).

    Article  Google Scholar 

  12. Handler, A. M. & James, A. A. Insect Transgenesis: Methods and Applications (CRC, Boca Raton, Florida, 2000).

    Book  Google Scholar 

  13. Atkinson, P. W., Pinkerton, A. C. & O'Brochta, D. A. Genetic transformation systems in insects. Annu. Rev. Entomol. 46, 317–346 (2001).

    Article  CAS  Google Scholar 

  14. Handler, A. M. A current perspective on insect gene transformation. Insect Biochem. Mol. Biol. 31, 111–128 (2001).

    Article  CAS  Google Scholar 

  15. Atkinson, P. W. & James, A. A. Germline transformants spreading out to many insect species. Adv. Genet. 47, 49–86 (2002).

    Article  CAS  Google Scholar 

  16. Horn, C., Schmid, B. G. M., Pogoda, F. S. & Wimmer, E. A. Fluorescent transformation markers for insect transgenesis. Insect Biochem. Mol. Biol. 32, 1221–1235 (2002).

    Article  CAS  Google Scholar 

  17. Halfon, M. S., Kose, H., Chiba, A. & Keshishian, H. Targeted gene expression without a tissue-specific promoter: creating mosaic embryos using laser-induced single-cell heat-shock. Proc. Natl Acad. Sci. USA 94, 6255–6260 (1997).

    Article  CAS  Google Scholar 

  18. Horn, C. & Wimmer, E. A. A versatile vector set for animal transgenesis. Dev. Genes Evol. 210, 630–637 (2000).

    Article  CAS  Google Scholar 

  19. Hannon, G. J. RNA interference. Nature 418, 244–251 (2002).

    Article  CAS  Google Scholar 

  20. Bucher, G., Scholten, J. & Klingler, M. Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12, R85–R86 (2002).

    Article  CAS  Google Scholar 

  21. Kennerdell, J. R. & Carthew, R. W. Heritable gene silencing in Drosophila using double-stranded RNA. Nature Biotechnol. 18, 896–898 (2000).

    Article  CAS  Google Scholar 

  22. Hughes, C. L. & Kaufman, T. C. A diverse approach to arthropod development. Evol. Dev. 2, 6–8 (2000).

    Article  CAS  Google Scholar 

  23. Cooley, L., Kelley, R. & Spradling, A. Insertional mutagenesis of the Drosophila genome with single P elements. Science 239, 1121–1128 (1988).

    Article  CAS  Google Scholar 

  24. O'Kane, C. J. & Gehring W. J. Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl Acad. Sci. USA 84, 9123–9127 (1987).

    Article  CAS  Google Scholar 

  25. Horn, C., Offen, N., Nystedt, S., Häcker, U. & Wimmer, E. A. piggyBac-based insertional mutagenesis and enhancer detection as a tool for functional insect genomics. Genetics 163 (in the press).

  26. Raff R. A. The Shape of Life (The Univ. of Chicago Press, Chicago, Illinois, 1996).

    Book  Google Scholar 

  27. Garstang W. The theory of recapitulation: a critical restatement of the biogenetic law. Zool. J. Linn. Soc. 35, 81–101 (1922).

    Article  Google Scholar 

  28. Jacob, F. Evolution and tinkering. Science 196, 1161–1166 (1977).

    Article  CAS  Google Scholar 

  29. Duboule, D. & Wilkins, A. S. The evolution of “bricolage”. Trends Genet. 14, 54–59 (1998).

    Article  CAS  Google Scholar 

  30. Tautz, D. Evolution of transcriptional regulation. Curr. Opin. Genet. Dev. 10, 575–579 (2000).

    Article  CAS  Google Scholar 

  31. Ludwig, M. Z., Patel, N. H. & Kreitman, M. Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. Development 125, 949–958 (1998).

    CAS  PubMed  Google Scholar 

  32. Ludwig, M. Z., Bergman, C., Patel, N. H. & Kreitman, M. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403, 564–567 (2000).

    Article  CAS  Google Scholar 

  33. Wolff, C., Schröder, R., Schulz, C., Tautz, D. & Klingler, M. Regulation of the Tribolium homologues of caudal and hunchback in Drosophila: evidence for maternal gradient systems in a short germ embryo. Development 125, 3645–3654 (1998).

    CAS  PubMed  Google Scholar 

  34. Rivera-Pomar, R. & Jäckle, H. From gradients to stripes in Drosophila embryogenesis: filling in the gaps. Trends. Genet. 12, 478–483 (1996).

    Article  CAS  Google Scholar 

  35. Sander, K. Specification of the basic body pattern in insect embryogenesis. Adv. Insect Physiol. 12, 125–238 (1976).

    Article  Google Scholar 

  36. Adams, M. D. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185–2195 (2000).

    Article  Google Scholar 

  37. Holt, R. A. et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129–149 (2002).

    Article  CAS  Google Scholar 

  38. Tomita M. et al. Transgenic silkworms produce recombinant human type III procollagen in cocoons. Nature Biotechnol. 21, 52–56 (2003).

    Article  CAS  Google Scholar 

  39. Hoy, M. A. Insect Molecular Genetics (Academic Press, San Diego, California, 1994).

    Book  Google Scholar 

  40. Krafsur, E. S. Sterile insect technique for suppressing and eradicating insect population: 55 years and counting. J. Agric. Entomol. 15, 303–317 (1998).

    Google Scholar 

  41. Hendrichs, J., Franz, G. & Rendon, P. Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. J. Appl. Entomol. 119, 371–377 (1995).

    Article  Google Scholar 

  42. Robinson, A. S. & Franz, G. in Insect Transgenesis: Methods and Applications (eds Handler, A. M. & James, A. A.) 307–318 (CRC, Boca Raton, Florida, 2000).

    Book  Google Scholar 

  43. Hagler, J. R. & Jackson, C. G. Methods for marking insects: current techniques and future prospects. Annu. Rev. Entomol. 46, 511–543 (2001).

    Article  CAS  Google Scholar 

  44. Peloquin, J. J., Thibault, S. T., Staten, R. & Miller, T. A. germline transformation of pink bollworm (Lepidoptera: gelechiidae) mediated by the piggyBac transposable element. Insect Mol. Biol. 9, 323–333 (2000).

    Article  CAS  Google Scholar 

  45. Handler, A. M. & Harrell, R. A. Polyubiquitin-regulated DsRed marker for transgenic insects. Biotechniques 31, 820, 824–828 (2001).

    CAS  PubMed  Google Scholar 

  46. Heinrich, J. C. & Scott, M. J. A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterile-release program. Proc. Natl Acad. Sci. USA 97, 8229–8232 (2000).

    Article  CAS  Google Scholar 

  47. Thomas, D. D., Donnelly, C. A., Wood, R. J. & Alphey, L. S. Insect population control using a dominant, repressible, lethal genetic system. Science 287, 2474–2476 (2000).

    Article  CAS  Google Scholar 

  48. Horn, C. & Wimmer, E. A. A transgene-based embryo-specific lethality system for insect pest mangement. Nature Biotechnol. 21, 64–70 (2003).

    Article  CAS  Google Scholar 

  49. Higgs, S. et al. Engineered resistance in Aedes aegypti to a West African and a South American strain of yellow fever virus. Am. J. Trop. Med. Hyg. 58, 663–670 (1998).

    Article  CAS  Google Scholar 

  50. Olson, K. E. et al. Genetically engineered resistance to dengue-2 virus transmission in mosquitoes. Science 272, 884–886 (1996).

    Article  CAS  Google Scholar 

  51. Adelman, Z. N., Blair, C. D., Carlson, J. O., Beaty, B. J. & Olson, K. E. Sindbis virus-induced silencing of dengue viruses in mosquitoes. Insect Mol. Biol. 10, 265–273 (2001).

    Article  CAS  Google Scholar 

  52. Olson, K. E. et al. Developing arbovirus resistance in mosquitoes. Insect Biochem. Mol. Biol. 32, 1333–1343 (2002).

    Article  CAS  Google Scholar 

  53. Ribeiro, J. M. & Kidwell, M. G. Transposable elements as population drive mechanisms: specification of critical parameter values. J. Med. Entomol. 31, 10–16 (1994).

    Article  CAS  Google Scholar 

  54. Lycett, G. J. & Kafatos, F. C. Anti-malarial mosquitoes? Nature 417, 387–388 (2002).

    Article  CAS  Google Scholar 

  55. National Research Council. Animal Biotechnology: Science-based Concerns (The National Academic Press, Washington, District of Columbia, 2002).

  56. Atkinson, P. W. Genetic engineering in insects of agricultural importance. Insect Biochem. Mol. Biol. 32, 1237–1242 (2002).

    Article  CAS  Google Scholar 

  57. Gehring, W. J. The genetic control of eye development and its implications for the evolution of the various eye-types. Int. J. Dev. Biol. 46, 65–73 (2002).

    Google Scholar 

  58. Ghosh, A. K., Moreira, L. A. & Jacobs-Lorena, M. Plasmodium–mosquito interactions, phage display libraries and transgenic mosquitoes impaired for malaria transmission. Insect Biochem. Mol. Biol. 32, 1325–1331 (2002).

    Article  CAS  Google Scholar 

  59. Ghosh, A. K., Ribolla, P. E & Jacobs-Lorena, M. Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display peptide library. Proc. Natl Acad. Sci. USA 98, 13278–13281 (2001).

    Article  CAS  Google Scholar 

  60. Moreira, L. A. et al. Robust gut–specific gene expression in transgenic Aedes aegypti mosquitoes. Proc. Natl Acad. Sci. USA 97, 10895–10898 (2000).

    Article  CAS  Google Scholar 

  61. Moreira, L. A. et al. Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J. Biol. Chem. 277, 40839–40843 (2002).

    Article  CAS  Google Scholar 

  62. Wirth, D. F. Biological revelations. Nature 419, 495–496 (2002).

    Article  CAS  Google Scholar 

  63. Duffy, J. B. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34, 1–15 (2002).

    Article  CAS  Google Scholar 

  64. Szüts, D. & Bienz, M. LexA chimeras reveal the function of Drosophila Fos as a context-dependent transcriptional activator. Proc. Natl Acad. Sci. USA 97, 5351–5356 (2000).

    Article  Google Scholar 

  65. Bello, B., Resendez-Perez, D. & Gehring, W. J. Spatial and temporal targeting of gene expression in Drosophila by means of a tetracycline-dependent transactivator system. Development 125, 2193–2202 (1998).

    CAS  PubMed  Google Scholar 

  66. Lewandoski, M. Conditional control of gene expression in the mouse. Nature Rev. Genet. 2, 743–755 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

I am grateful to B. Jaunich and F. Pogoda for technical assistance and wish to thank V. Kokoza, J.-L. Thomas and M. Jindra for providing photographs. I apologize to all the authors whose important work I did not cite owing to the strict space restrictions of this article. Work in my laboratory is supported by the European Molecular Biology Organization Young Investigator Programme, the Deutsche Forschungsgemeinschaft, the Fonds der Chemischen Industrie, the Bundesministerium für Bildung und Forschung and especially by the Robert Bosch Foundation who provided an independent junior research group.

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DATABASES

LocusLink

eve

hsp70

FURTHER INFORMATION

Anopheles gambiae Genome View

Berkeley Drosophila Genome Project

Drosophila Genome Project at the Human Genome Sequencing Center at Baylor College of Medicine

Genome News Network — moth DNA sequenced

International Lepidopteran Genome Project

Mosquito Genome Browser

TheMosquitoGenomicsWWW.Server

National Human Genome Research Institute

The piggyBac Web site

SilkBase

Glossary

BALANCER CHROMOSOMES

Chromosomes that contain inversions and visible markers. Balancer chromosomes facilitate crossing schemes by suppressing recombination between homologues and by being easily detected.

BLASTODERM

The layer of cells that completely surrounds an internal mass of yolk in an insect embryo.

CASTE FORMATION

The development of different groups of individuals of predictable morphological types or behaviour that have specialized tasks in a colony of social insects.

DIAPAUSE

A resting phase in the life cycle of an organism. It is a period of suspended growth or development, characterized by greatly reduced metabolic activity.

GERM PLASM

Cytoplasm that is localized to a certain region within the insect oocyte that is necessary for the correct development of germ cells.

HAEMOCOEL

The large body cavity of insects in which haemolymph (insect blood) flows.

HORIZONTAL GENE TRANSFER

The transfer of genetic material between the genomes of two organisms, which usually belong to different species.

MACROEVOLUTIONARY EVENT

Evolution that occurs above the species level and over protracted periods of geological time (for example, speciation, morphological change and extinction).

MICROEVOLUTIONARY EVENT

A minor evolutionary event that is usually observed over a short period of time. It consists of changes in gene frequencies, chromosome structure or number in a population over a few generations.

NAIVE MICE

Mice that have not been exposed to a particular pathogen or parasite.

NON-AUTONOMOUS

A non-autonomous transposon is not able to transpose by itself, but will transpose if transposase activity is provided by an independent source.

ONTOGENY

The course of development and growth of an individual from egg to maturity.

ORTHOLOGUES

Homologous genes in different species, the lineage of which derives from a common ancestral gene without gene duplication or horizontal transmission.

PAIR-RULE GENES

Genes expressed as transverse stripes in alternate segment equivalents of a developing insect embryo.

PHAGE DISPLAY LIBRARY

A heterogeneous mixture of recombinant phage clones, each carrying a different foreign DNA insert and, therefore, displaying a different peptide on their surface.

PHENOCOPY

An experimentally or environmentally induced phenotypic variation that resembles the effect of a known gene mutation.

PHYLOGENY

The evolutionary history of a group or lineage.

RNA INTERFERENCE

(RNAi). A process by which double-stranded RNA silences specifically the expression of homologous genes through degradation of their cognate mRNA.

STABILIZING SELECTION

Selection for the mean or intermediate phenotype. Consequently, peripheral variants are eliminated, maintaining an existing state of adaptation in a stable environment.

STRIPE ELEMENT

A cis-regulatory DNA sequence that acts as an enhancer of gene expression and mediates regionally restricted expression of zygotic developmental genes in transverse stripes.

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Wimmer, E. Applications of insect transgenesis. Nat Rev Genet 4, 225–232 (2003). https://doi.org/10.1038/nrg1021

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