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José Robson de Almeida.
Genetic methods of manipulating or eradicating disease vector populations have long been discussed as an attractive alternative to existing control measures because of their potential advantages in terms of effectiveness and species specificity1, 2, 3. The development of genetically engineered malaria-resistant mosquitoes has shown, as a proof of principle, the possibility of targeting the mosquito’s ability to serve as a disease vector4, 5, 6, 7. The translation of these achievements into control measures requires an effective technology to spread a genetic modification from laboratory mosquitoes to field populations8. We have suggested previously that homing endonuclease genes (HEGs), a class of simple selfish genetic elements, could be exploited for this purpose9. Here we demonstrate that a synthetic genetic element, consisting of mosquito regulatory regions10 and the homing endonuclease gene I-SceI11, 12, 13, can substantially increase its transmission to the progeny in transgenic mosquitoes of the human malaria vector Anopheles gambiae. We show that the I-SceIelement is able to invade receptive mosquito cage populations rapidly, validating mathematical models for the transmission dynamics of HEGs. Molecular analyses confirm that expression of I-SceI in the male germline induces high rates of site-specific chromosomal cleavage and gene conversion, which results in the gain of the I-SceI gene, and underlies the observed genetic drive. These findings demonstrate a new mechanism by which genetic control measures can be implemented. Our results also show in principle how sequence-specific genetic drive elements like HEGs could be used to take the step from the genetic engineering of individuals to the genetic engineering of populations.
Imperial College London, Department of Life Sciences, South Kensington Campus, London, SW7 2AZ, UK
Nikolai Windbichler,
Miriam Menichelli,
Philippos Aris Papathanos,
Austin Burt &
Andrea Crisanti
Department of Biochemistry, University of Washington, Seattle, Washington 98195, USA
Summer B. Thyme &
David Baker
Graduate Program in Biomolecular Structure and Design, University of Washington, Seattle, Washington 98195, USA
Summer B. Thyme &
David Baker
Department of Pathology, University of Washington, Seattle, Washington 98195, USA
Hui Li,
Umut Y. Ulge &
Raymond J. Monnat
Graduate Program in Molecular and Cellular Biology, University of Washington, Seattle, Washington 98195, USA
Umut Y. Ulge &
Raymond J. Monnat
Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA
Blake T. Hovde &
Raymond J. Monnat
Howard Hughes Medical Institute, University of Washington, Seattle, Washington 98195, USA
David Baker
Imperial College London, Department of Life Sciences, Silwood Park Campus, Ascot, SL5 7PY, UK
Austin Burt
Department of Experimental Medicine, University of Perugia, Via Del Giochetto, 06122 Perugia, Italy
Andrea Crisanti
Contributions
N.W. designed the experiments. N.W., M.M. and P.A.P. performed the experiments. N.W. and P.A.P. generated the transgenic lines. M.M. maintained mosquito populations. N.W. analysed the data. A.B. and N.W. generated the population dynamic models. A.C. and A.B. inspired the work and wrote the paper together with N.W. HEG redesign and target site cleavage analyses were performed by S.B.T., H.L., U.Y.U. (contributed equally) and B.T.H. with guidance from D.B. and R.J.M. All authors read and approved the final manuscript.
Competing financial interests
The authors declare no competing financial interests.
