Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Gene drive systems for insect disease vectors

Key Points

  • Advances in the molecular biology of insect disease vectors, particularly mosquitoes, have made it possible to express constructs that can block the transmission of pathogens such as Plasmodium in model systems. Methods for spreading constructs through natural populations are now much needed.

  • Various transposable elements (TEs) are common in insects and in their autonomous form can increase their germline copy number, thereby providing a potential transgene drive mechanism. More needs to be known about the rates of transposition of TEs in target species, with and without inserts, and the stability of inserted genes.

  • Homing endonuclease genes (HEGs) encode site-specific endonucleases and their copy number can increase through homologous repair. They have not been found in animals; research is needed to determine whether operational systems could be produced in insects.

  • Various meiotic drive mechanisms (with unequal representation of alleles at meiotic segregation) are found in insects; it might be possible to engineer artificial versions for transgene drive, particularly if naturally occurring mechanisms can be better understood.

  • Engineered underdominance has been proposed as a gene-spreading system, using combinations of lethal genes and trans-acting suppressors. The release frequencies that are required would be comparatively high with this system.

  • The inherited endosymbiotic bacterium Wolbachia is able to spread through populations using cytoplasmic incompatibility. It could be used in disease control if it could be transformed to express and secrete gene products in relevant tissues, or if a virulent strain could reduce host lifespan in target species.

Abstract

The elegant mechanisms by which naturally occurring selfish genetic elements, such as transposable elements, meiotic drive genes, homing endonuclease genes and Wolbachia, spread at the expense of their hosts provide some of the most fascinating and remarkable subjects in evolutionary genetics. These elements also have enormous untapped potential to be used in the control of some of the world's most devastating diseases. Effective gene drive systems for spreading genes that can block the transmission of insect-borne pathogens are much needed. Here we explore the potential of natural gene drive systems and discuss the artificial constructs that could be envisaged for this purpose.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: The mechanism by which homing endonuclease genes increase in frequency within a population.
Figure 2: Segregation distortion.
Figure 3: An example of an engineered underdominant system that is based on mutual suppression of lethal constructs.

References

  1. 1

    Snow, R. W., Guerra, C. A., Noor, A. M., Myint. H. Y. & Hay, S. I. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214–217 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2

    Curtis, C. F. Possible use of translocations to fix desirable genes in insect pest populations. Nature 218, 368–369 (1968). The first paper to highlight the possibility of using genetic approaches for driving anti-pathogen genes into populations of vector species.

    CAS  PubMed  Google Scholar 

  3. 3

    Knipling, E. F. et al. Genetic control of insects of public health importance. Bull. World Health Organ. 38, 421–438 (1968).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4

    Curtis, C. F. & Graves, P. M. Methods for replacement of malaria vector populations. J. Trop. Med. Hyg. 91, 43–48 (1988).

    CAS  PubMed  Google Scholar 

  5. 5

    Coates, C. J., Jasinskiene, N., Miyashiro, L. & James, A. A. Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc. Natl Acad. Sci. USA 95, 3748–3751 (1998).

    CAS  PubMed  Google Scholar 

  6. 6

    Catteruccia, F. et al. Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405, 959–962 (2000).

    CAS  PubMed  Google Scholar 

  7. 7

    Grossman, G. L. et al. Germline transformation of the malaria vector, Anopheles gambiae, with the piggyBac transposable element. Insect Mol. Biol. 10, 597–604 (2001).

    CAS  PubMed  Google Scholar 

  8. 8

    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). One of the first demonstrations of the feasibility of blocking malaria transmission in a model system, using a short peptide that interferes with Plasmodium ligand binding. The restriction of expression of the construct to the midgut after blood meals reduces fitness costs.

    CAS  PubMed  Google Scholar 

  9. 9

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

    CAS  PubMed  Google Scholar 

  10. 10

    Franz, A. W. E. et al. Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. Proc. Natl Acad. Sci. USA 103, 4198–4203 (2006). Demonstrates the reduced ability of Aedes aegypti to function as a vector for dengue following midgut expression of an inverted-repeat RNA that is based on a viral gene.

    CAS  PubMed  Google Scholar 

  11. 11

    de Lara Capurro, M. et al. Virus-expressed, recombinant single-chain antibody blocks sporozoite infection of salivary glands in Plasmodium gallinaceum-infected Aedes aegypti. Am. J. Trop. Med. Hyg. 62, 427–433 (2000).

    CAS  PubMed  Google Scholar 

  12. 12

    Osta, M. A., Christophides, G. K. & Kafatos, F. C. Effects of mosquito genes on Plasmodium development. Science 303, 2030–2032 (2004).

    CAS  PubMed  Google Scholar 

  13. 13

    Blandin, S. et al. Complement-like protein TEP1 Is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116, 661–670 (2004).

    CAS  PubMed  Google Scholar 

  14. 14

    Hurst, G. D. D. & Werren, J. H. The role of selfish genetic elements in eukaryotic evolution. Nature Rev. Genet. 2, 597–606 (2001).

    CAS  PubMed  Google Scholar 

  15. 15

    Alphey, L. et al. Malaria control with genetically manipulated insect vectors. Science 298, 119–121 (2002).

    CAS  PubMed  Google Scholar 

  16. 16

    Braig, H. R. & Yan, G. in Genetically Engineered Organisms: Assessing Environmental and Human Health Effects (eds Letournaeu, D. K. & Burrows, B. E.) 251–314 (CRC Press, Boca Raton, Florida, 2002).

    Google Scholar 

  17. 17

    James, A. A. Gene drive systems in mosquitoes: rules of the road. Trends Parasitol. 21, 64–67 (2005).

    CAS  PubMed  Google Scholar 

  18. 18

    Boete, C. & Koella, J. C. Evolutionary ideas about genetically manipulated mosquitoes and malaria control. Trends Parasitol. 19, 32–38 (2003).

    PubMed  Google Scholar 

  19. 19

    Moreira, L. A., Wang, J. I., Collins, F. H. & Jacobs-Lorena, M. Fitness of anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics 166, 1337–1341 (2004).

    PubMed  PubMed Central  Google Scholar 

  20. 20

    Catteruccia, F., Godfray, H. C. & Crisanti, A. Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes. Science 299, 1225–1227 (2003).

    CAS  PubMed  Google Scholar 

  21. 21

    Scott, T. W., Takken, W., Knols, B. G. J. & Boëte, C. The ecology of genetically manipulated mosquitoes. Science 298, 117–119 (2002).

    CAS  PubMed  Google Scholar 

  22. 22

    Charlesworth, B. & Langley, C. H. The population genetics of Drosophila transposable elements. Annu. Rev. Genet. 23, 251–287 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23

    Kidwell, M. G. Horizontal transfer of P elements and other short inverted repeat transposons. Genetica 86, 275–286 (1992).

    CAS  PubMed  Google Scholar 

  24. 24

    Engels, W. R. Invasions of P elements. Genetics 145, 11–15 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

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

    CAS  Google Scholar 

  26. 26

    Tu, Z. & Coates, C. J. Mosquito transposable elements. Insect Biochem. Mol. Biol. 34, 631–644 (2004). A review of the families of TEs that are found in mosquitoes and their different mechanisms of transposition.

    CAS  PubMed  Google Scholar 

  27. 27

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

    CAS  PubMed  Google Scholar 

  28. 28

    Ashburner, M., Hoy, M. A. & Peloquin, J. J. Prospects for the genetic transformation of arthropods. Insect Mol. Biol. 7, 201–213 (1998).

    CAS  PubMed  Google Scholar 

  29. 29

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

    CAS  PubMed  Google Scholar 

  30. 30

    Rasgon, J. L. & Gould, F. Transposable element insertion location bias and the dynamics of gene drive in mosquito populations. Insect Mol. Biol. 14, 493–500 (2005). Examines the spread of TEs when the initial insertion sites and reinsertion sites are not always on different chromosomes, and when there are fitness costs associated with TE insertions.

    CAS  PubMed  Google Scholar 

  31. 31

    O'Brochta, D. A. et al. Gene vector and transposable element behavior in mosquitoes. J. Exp. Biol. 206, 3823–3834 (2003).

    CAS  PubMed  Google Scholar 

  32. 32

    Hartl, D. L., Lozovskaya, E. R., Nurminsky, D. I. & Lohe, A. R. What restricts the activity of mariner-like transposable elements. Trends Genet. 13, 197–201 (1997).

    CAS  PubMed  Google Scholar 

  33. 33

    Kidwell, M. G. & Lisch, D. R. in Mobile DNA II (eds Craig, N., Craigie, R., Gellert, M. & Lambowitz, A.) 59–90 (ASM Press, Washington DC, 2002).

    Google Scholar 

  34. 34

    Nuzhdin, S. V. Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107, 129–137 (1999).

    CAS  PubMed  Google Scholar 

  35. 35

    Arensburger, P. et al. An active transposable element, Herves, from the African malaria mosquito Anopheles gambiae. Genetics 169, 697–708 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36

    Lampe, D. J., Grant, T. E. & Robertson, H. M. Factors affecting transposition of the Himar1 mariner transposon in vitro. Genetics 149, 179–187 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37

    Carareto, C. M. et al. Testing transposable elements as genetic drive mechanisms using Drosophila P element constructs as a model system. Genetica 101, 13–33 (1997).

    CAS  PubMed  Google Scholar 

  38. 38

    Mathiopoulos, K. D., della Torre, A., Predazzi, V., Petrarca, V. & Coluzzi, M. Cloning of inversion breakpoints in the Anopheles gambiae complex traces a transposable element at the inversion junction. Proc. Natl Acad. Sci. USA 95, 12444–12449 (1998).

    CAS  PubMed  Google Scholar 

  39. 39

    Calvo, E. et al. Nanos (nos) genes of the vector mosquitoes, Anopheles gambiae, Anopheles stephensi and Aedes aegypti. Insect Biochem. Mol. Biol. 35, 789–798 (2005).

    CAS  PubMed  Google Scholar 

  40. 40

    Eickbush, T. in Mobile DNA II (eds Craig, N., Craigie, R., Gellert, M. & Lambowitz, A.) 813–835 (ASM Press, Washington DC, 2002).

    Google Scholar 

  41. 41

    Burt, A. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. Biol. Soc. 270, 921–928 (2003). Outlines the population genetic properties of HEGs and how they could be used for driving genes into populations and for population suppression.

    CAS  Google Scholar 

  42. 42

    Gimble, F. S. Invasion of a multitude of genetic niches by mobile endonuclease genes. FEMS Microbiol. Lett. 185, 99–107 (2000).

    CAS  PubMed  Google Scholar 

  43. 43

    Jacquier, A. & Dujon, B. An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41, 383–394 (1985).

    CAS  PubMed  Google Scholar 

  44. 44

    Wessler, S. R. Homing into the origin of the AP2 DNA binding domain. Trends Plant Sci. 10, 54–56 (2005).

    CAS  PubMed  Google Scholar 

  45. 45

    Butler, M. I., Goodwin, T. J. & Poulter, R. T. Two new fungal inteins. Yeast 22, 493–501 (2005).

    CAS  PubMed  Google Scholar 

  46. 46

    Koufopanou, V. & Burt, A. Degeneration and domestication of a selfish gene in yeast: molecular evolution versus site-directed mutagenesis. Mol. Biol. Evol. 22, 609–615 (2005).

    Google Scholar 

  47. 47

    Burt, A. & Koufopanou, V. Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr. Opin. Genet. Dev. 14, 609–615 (2004).

    CAS  PubMed  Google Scholar 

  48. 48

    Gimble, F. S., Moure, C. M. & Posey, K. L. Assessing the plasticity of DNA target site recognition of the PI-SceI homing endonuclease using a bacterial two-hybrid selection system. J. Mol. Biol. 334, 993–1008 (2003).

    CAS  PubMed  Google Scholar 

  49. 49

    Rong, Y. S. & Golic, K. G. The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 165, 1831–1842 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50

    Bibikova, M. et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell. Biol. 21, 289–297 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51

    Little, T. W. Segregation distorters. Annu. Rev. Genet. 25, 511–557 (1991).

    Google Scholar 

  52. 52

    Ganetsky, B. On the components of segregation distortion in Drosophila melanogaster. Genetics 86, 321–355 (1977).

    Google Scholar 

  53. 53

    Charlesworth, B. & Hartl, D. L. Population dynamics of the segregation distorter polymorphism of Drosophila melanogaster. Genetics 89, 171–192 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    Merrill, C., Bayraktaroglu, L., Kusano, A. & Ganetzky, B. Truncated RanGAP encoded by the Segregation Distorter locus of Drosophila. Science 283, 1742–1745 (1999).

    CAS  PubMed  Google Scholar 

  55. 55

    Wu, C. -I., Lyttle, T. W., Wu, M. -L. & Lin, G. -F. Association between a satellite DNA sequence and the responder of segregation distorter in Drosophila melanogaster. Cell 54, 179–189 (1988).

    CAS  PubMed  Google Scholar 

  56. 56

    Kusano, A., Staber, C., Chan, H. Y. E. & Ganetzky, B. Closing the (Ran)GAP on segregation distortion in Drosophila. BioEssays 25, 108–115 (2003).

    CAS  PubMed  Google Scholar 

  57. 57

    Hickey, W. A. & Craig, G. B. Genetic distortion of sex ratio in a mosquito, Aedes aegypti. Genetics 53, 1177–1196 (1966).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58

    Wood, R. J. & Ouda, N. A. The genetic basis of resistance and sensitivity to the meiotic drive gene D in the mosquito Aedes aegypti L. Genetica 72, 69–79 (1987).

    CAS  PubMed  Google Scholar 

  59. 59

    Wood, R. J. & Newton, M. E. Sex-ratio distortion caused by meiotic drive in mosquitoes. Am. Nat. 137, 379–391 (1991).

    Google Scholar 

  60. 60

    Mori, A., Chadee, D. D., Graham, D. H. & Severson, D. W. Reinvestigation of an endogenous meiotic drive system in the mosquito, Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 41, 1027–1033 (2004).

    PubMed  Google Scholar 

  61. 61

    Sweeny, T. L. & Barr, A. R. Sex ratio distortion caused by meiotic drive in a mosquito, Culex pipiens L. Genetics 88, 427–446 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. 62

    Hamilton, W. D. Extraordinary sex ratios. Science 156, 477–488 (1967).

    CAS  PubMed  Google Scholar 

  63. 63

    Lyttle, T. W. Experimental population genetics of meiotic drive systems. I. Pseudo-Y chromosomal drive as a means of eliminating cage populations of Drosophila melanogaster. Genetics 86, 413–445 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64

    Wood, R. J, Cook, L. M., Hamilton, A. & Whitelaw, A. Transporting the marker gene re (red eye) into a laboratory cage population of Aedes aegypti (Diptera: Culicidae), using meiotic drive at the MD locus. J. Med. Entomol. 14, 461–464 (1977).

    CAS  Google Scholar 

  65. 65

    Wood, R. J. Between-family variation in sex ratio in the Trinidad (T-30) strain of Aedes aegypti (L.) indicating differences in sensitivity to the meiotic drive gene MD. Genetica 46, 345–361 (1976).

    Google Scholar 

  66. 66

    Suguna, S. G., Wood, R. J., Curtis, C. F., Whitelaw, A. & Kazmi, S. J. Resistance to meiotic drive at the MD locus in an Indian wild population of Aedes aegypti. Genet. Res. 29, 123–132 (1977).

    CAS  PubMed  Google Scholar 

  67. 67

    Beeman, R. W., Friesen, K. S. & Denell, R. E. Maternal-effect selfish genes in flour beetles. Science 256, 89–92 (1992).

    CAS  PubMed  Google Scholar 

  68. 68

    Beeman, R. W. & Friesen, K. S. Properties and natural occurrence of maternal-effect selfish genes ('Medea' factors) in the red flour beetle, Tribolium castaneum. Heredity 82, 529–534 (1999).

    PubMed  Google Scholar 

  69. 69

    Wade, M. J. & Beeman, R. W. The population dynamics of maternal-effect selfish genes. Genetics 138, 1309–1314 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. 70

    Hartl, D. L. & Clark, A. G. Principles of Population Genetics (Sinauer Associates, Sunderland, Massachusetts, 1989).

    Google Scholar 

  71. 71

    Serebrovskii, A. S. On the possibility of a new method for the control of insect pests. Zool. Zh. 19, 618–690 (1940).

    Google Scholar 

  72. 72

    Robinson, A. S. Progress in the use of chromosomal translocations for the control of insect pests. Biol. Rev. 51, 1–24 (1976).

    CAS  PubMed  Google Scholar 

  73. 73

    Curtis, C. F. Genetic control of insect pests: growth industry or lead balloon? Biol. J. Linn. Soc. Lond. 26, 359–374 (1985).

    Google Scholar 

  74. 74

    Davis, S. A., Bax, N. & Grewe, P. Engineered underdominance allows efficient and economical introgression of traits into pest populations. J. Theor. Biol. 212, 83–98 (2001). Outlines two novel approaches for driving genes into natural populations by causing decreased fitness in a subset of offspring from mating of individuals of the engineered and natural strains.

    CAS  PubMed  Google Scholar 

  75. 75

    Gould, F. & Schliekelman, P. Population genetics of autocidal control and strain replacement. Annu. Rev. Entomol. 49, 193–217 (2004). Contrasts the population genetic properties of several classical and molecular methods of gene drive and genetic suppression of populations.

    CAS  PubMed  Google Scholar 

  76. 76

    Magori, K. & Gould, F. Genetically engineered underdominance for manipulation of pest populations: a deterministic model. Genetics 16 Jan 2006 [Epub ahead of print].

  77. 77

    O'Neill, S. L., Hoffmann, A. A. & Werren, J. H. (eds) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (Oxford Univ. Press, Oxford, 1997).

    Google Scholar 

  78. 78

    Werren, J. H. Biology of Wolbachia. Annu. Rev. Entomol. 42, 587–609 (1997).

    CAS  PubMed  Google Scholar 

  79. 79

    Turelli, M. & Hoffmann, A. A. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440–442 (1991).

    CAS  PubMed  Google Scholar 

  80. 80

    Dobson, S. L., Marsland, E. J., Veneti, Z., Bourtzis, K. & O'Neill, S. L. Characterization of Wolbachia host cell range via the in vitro establishment of infections. Appl. Environ. Microbiol. 68, 656–660 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. 81

    Curtis, C. F. & Sinkins, S. P. Wolbachia as a possible means of driving genes into populations. Parasitology 116, 111–115 (1998).

    Google Scholar 

  82. 82

    Turelli, M. & Hoffmann, A. A. Microbe-induced cytoplasmic incompatibility as a mechanism for introducing genes into arthropod populations. Insect Mol. Biol. 8, 243–255 (1999).

    CAS  PubMed  Google Scholar 

  83. 83

    Sinkins, S. P. & O'Neill, S. L. in Insect Transgenesis: Methods and Applications (eds Handler, A. M. & James, A. A.) 271–288 (CRC Press, Boca Raton, Florida, 2000). Reviews in more depth the potential uses of Wolbachia in insect control.

    Google Scholar 

  84. 84

    Dobson, S. L. Reversing Wolbachia-based population replacement. Trends Parasitol. 19, 128–133 (2003).

    PubMed  Google Scholar 

  85. 85

    Hoffman, A. A. & Turelli, M. in Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (eds O'Neill, S. L., Hoffmann, A. A. & Werren, J. H.) 42–80 (Oxford Univ. Press, Oxford, 1997).

    Google Scholar 

  86. 86

    Rasgon, J. L. & Scott, T. W. Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter values and infection dynamics in natural populations. Genetics 165, 2029–3208 (2004).

    Google Scholar 

  87. 87

    Sinkins, S. P. Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem. Mol. Biol. 34, 723–729 (2004).

    CAS  PubMed  Google Scholar 

  88. 88

    Sinkins, S. P., Braig, H. R. & O'Neill, S. L. Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc. Biol. Soc. 261, 325–330 (1995).

    CAS  Google Scholar 

  89. 89

    Sinkins, S. P. & Godfray, H. C. J. Use of Wolbachia to drive nuclear transgenes through insect populations. Proc. Biol. Soc. 271, 1421–1426 (2004).

    CAS  Google Scholar 

  90. 90

    Min, K. T. & Benzer, S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl Acad. Sci. USA 94, 10792–10796 (1997).

    CAS  PubMed  Google Scholar 

  91. 91

    Brownstein, J. S., Hett, E. & O'Neill, S. L. The potential of virulent Wolbachia to modulate disease transmission by insects. J. Invert. Pathol. 84, 24–29 (2003).

    CAS  Google Scholar 

  92. 92

    Wu, M. et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2, 327–341 (2004). The first published Wolbachia genome sequence, from Drosophila melanogaster , has greatly increased molecular understanding of the bacterium and therefore how it might be manipulated.

    CAS  Google Scholar 

  93. 93

    Masui, S. et al. Bacteriophage WO and virus-like particles in Wolbachia, an endosymbiont of arthropods. Biochem. Biophys. Res. Commun. 283, 1099–1104 (2001).

    CAS  PubMed  Google Scholar 

  94. 94

    Fujii, Y., Kubo, T., Ishikawa, H. & Sasaki, T. Isolation and characterization of the bacteriophage WO from Wolbachia, an arthropod endosymbiont. Biochem. Biophys. Res. Commun. 317, 1183–1188 (2004).

    CAS  PubMed  Google Scholar 

  95. 95

    Sanogo, Y. O. & Dobson, S. L. Molecular discrimination of Wolbachia in the Culex pipiens complex: evidence for variable bacteriophage hyperparasitism. Insect Mol. Biol. 13, 365–369 (2004).

    CAS  PubMed  Google Scholar 

  96. 96

    Dotson, E. M., Plikaytis, B., Shinnick, T. M., Durvasula, R. V. & Beard, C. B. Transformation of Rhodococcus rhodnii, a symbiont of the Chagas disease vector Rhodnius prolixus, with integrative elements of the L1 mycobacteriophage. Infect. Genet. Evol. 3, 103–109 (2003).

    CAS  PubMed  Google Scholar 

  97. 97

    Sinkins, S. P. et al. Wolbachia variability and host effects associated with crossing type in Culex mosquitoes. Nature 436, 257–260 (2005).

    CAS  PubMed  Google Scholar 

  98. 98

    Iturbe-Ormaetxe, I., Burke, G. R., Riegler, M. & O'Neill, S. L. Distribution, expression, and motif variability of ankyrin domain genes in Wolbachia pipientis. J. Bacteriol. 187, 5136–5145 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. 99

    Zabalou, S. et al. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc. Natl Acad. Sci. USA 101, 15042–15045 (2004).

    CAS  PubMed  Google Scholar 

  100. 100

    Xi, Z., Khoo, C. C. & Dobson, S. L. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310, 326–328 (2005). A demonstration that Wolbachia is able to show high rates of maternal transmission and cytoplasmic incompatibility after transfer into the naturally uninfected dengue vector, the mosquito Aedes aegypti.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

For comments on Table 1 we thank L. Alphey, P. Atkinson, A. Hoffman, Y. Huang, K. Magori, D. O'Brochta and J. Rasgon.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Steven P. Sinkins.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Steven Sinkins's laboratory web site

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sinkins, S., Gould, F. Gene drive systems for insect disease vectors. Nat Rev Genet 7, 427–435 (2006). https://doi.org/10.1038/nrg1870

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing