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Gene drives gaining speed

  • 1.

    Serebrovsky, A. S. On the possibility of a new method for the control of insect pests. Zool. Zh. 19, 618–630 (1940).

    Google Scholar 

  • 2.

    Curtis, C. F. Possible use of translocations to fix desirable genes in insect pest populations. Nature 218, 368–369 (1968). This paper is one of the first to describe how reciprocal chromosomal translocations could be used to drive a favoured linked trait in a threshold-dependent fashion.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 3.

    Dawkins, R. The Selfish Gene Vol. 345 (Oxford University Press, 1976).

  • 4.

    Bastide, H. et al. Rapid rise and fall of selfish sex-ratio X chromosomes in Drosophila simulans: spatiotemporal analysis of phenotypic and molecular data. Mol. Biol. Evol. 28, 2461–2470 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 5.

    Corbett-Detig, R., Medina, P., Frerot, H., Blassiau, C. & Castric, V. Bulk pollen sequencing reveals rapid evolution of segregation distortion in the male germline of Arabidopsis hybrids. Evol. Lett. 3, 93–103 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 6.

    Kingan, S. B., Garrigan, D. & Hartl, D. L. Recurrent selection on the Winters sex-ratio genes in Drosophila simulans. Genetics 184, 253–265 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 7.

    McLaughlin, R. N. Jr. & Malik, H. S. Genetic conflicts: the usual suspects and beyond. J. Exp. Biol. 220, 6–17 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 8.

    Presgraves, D. C., Gerard, P. R., Cherukuri, A. & Lyttle, T. W. Large-scale selective sweep among segregation distorter chromosomes in African populations of Drosophila melanogaster. PLoS Genet. 5, e1000463 (2009).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 9.

    Seymour, D. K., Chae, E., Arioz, B. I., Koenig, D. & Weigel, D. Transmission ratio distortion is frequent in Arabidopsis thaliana controlled crosses. Heredity 122, 294–304 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 10.

    Courret, C., Chang, C. H., Wei, K. H., Montchamp-Moreau, C. & Larracuente, A. M. Meiotic drive mechanisms: lessons from Drosophila. Proc. Biol. Sci. 286, 20191430 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 11.

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

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 12.

    Merel, V., Boulesteix, M., Fablet, M. & Vieira, C. Transposable elements in Drosophila. Mob. DNA 11, 23 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 13.

    Boulesteix, M. & Biemont, C. Transposable elements in mosquitoes. Cytogenet. Genome Res. 110, 500–509 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 14.

    Lee, Y. C. & Langley, C. H. Transposable elements in natural populations of Drosophila melanogaster. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1219–1228 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 15.

    Kelleher, E. S. Reexamining the P-element invasion of Drosophila melanogaster through the lens of piRNA silencing. Genetics 203, 1513–1531 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 16.

    Majumdar, S. & Rio, D. C. P transposable elements in drosophila and other eukaryotic organisms. Microbiol. Spectr. 3, MDNA3–0004-2014 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 17.

    Burns, K. H. & Boeke, J. D. Human transposon tectonics. Cell 149, 740–752 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 18.

    Doring, H. P., Tillmann, E. & Starlinger, P. DNA sequence of the maize transposable element Dissociation. Nature 307, 127–130 (1984).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 19.

    Wallau, G. L., Capy, P., Loreto, E. & Hua-Van, A. Genomic landscape and evolutionary dynamics of mariner transposable elements within the Drosophila genus. BMC Genomics 15, 727 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 20.

    Hawkins, J. S., Hu, G., Rapp, R. A., Grafenberg, J. L. & Wendel, J. F. Phylogenetic determination of the pace of transposable element proliferation in plants: copia and LINE-like elements in Gossypium. Genome 51, 11–18 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 21.

    Biemont, C., Vieira, C., Borie, N. & Lepetit, D. Transposable elements and genome evolution: the case of Drosophila simulans. Genetica 107, 113–120 (1999).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 22.

    Buchman, A. B., Ivy, T., Marshall, J. M., Akbari, O. S. & Hay, B. A. Engineered reciprocal chromosome translocations drive high threshold, reversible population replacement in drosophila. ACS Synth. Biol. 7, 1359–1370 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 23.

    Akbari, O. S. et al. Novel synthetic Medea selfish genetic elements drive population replacement in Drosophila; a theoretical exploration of Medea-dependent population suppression. ACS Synth. Biol. 3, 915–928 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 24.

    Buchman, A., Marshall, J. M., Ostrovski, D., Yang, T. & Akbari, O. S. Synthetically engineered Medea gene drive system in the worldwide crop pest Drosophila suzukii. Proc. Natl Acad. Sci. USA 115, 4725–4730 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 25.

    Champer, J., Zhao, J., Champer, S. E., Liu, J. & Messer, P. W. Population dynamics of underdominance gene drive systems in continuous space. ACS Synth. Biol. 9, 779–792 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 26.

    Chen, C. C. et al. EXO1 suppresses double-strand break induced homologous recombination between diverged sequences in mammalian cells. DNA Repair. 57, 98–106 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 27.

    Leftwich, P. T. et al. Recent advances in threshold-dependent gene drives for mosquitoes. Biochem. Soc. Trans. 46, 1203–1212 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 28.

    Raban, R. R., Marshall, J. M. & Akbari, O. S. Progress towards engineering gene drives for population control. J. Exp. Biol. 223 (Suppl. 1), jeb208181 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 29.

    Ward, C. M. et al. Medea selfish genetic elements as tools for altering traits of wild populations: a theoretical analysis. Evolution 65, 1149–1162 (2011).

    PubMed 
    Article 

    Google Scholar 

  • 30.

    Oberhofer, G., Ivy, T. & Hay, B. A. Gene drive and resilience through renewal with next generation Cleave and Rescue selfish genetic elements. Proc. Natl Acad. Sci. USA 117, 9013–9021 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 31.

    Oberhofer, G., Ivy, T. & Hay, B. A. Cleave and Rescue, a novel selfish genetic element and general strategy for gene drive. Proc. Natl Acad. Sci. USA 116, 6250–6259 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 32.

    Champer, J. et al. A toxin-antidote CRISPR gene drive system for regional population modification. Nat. Commun. 11, 1082 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 33.

    Yen, P. S. & Failloux, A. B. A review: Wolbachia-based population replacement for mosquito control shares common points with genetically modified control approaches. Pathogens 9, 404 (2020).

    PubMed Central 
    Article 
    PubMed 

    Google Scholar 

  • 34.

    O’Neill, S. L. The use of wolbachia by the world mosquito program to interrupt transmission of aedes aegypti transmitted viruses. Adv. Exp. Med. Biol. 1062, 355–360 (2018).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 35.

    Niang, E. H. A., Bassene, H., Fenollar, F. & Mediannikov, O. Biological control of mosquito-borne diseases: the potential of wolbachia-based interventions in an IVM framework. J. Trop. Med. 2018, 1470459 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 36.

    Chevalier, B. S. & Stoddard, B. L. Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucleic Acids Res. 29, 3757–3774 (2001).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 37.

    Macreadie, I. G., Scott, R. M., Zinn, A. R. & Butow, R. A. Transposition of an intron in yeast mitochondria requires a protein encoded by that intron. Cell 41, 395–402 (1985).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 38.

    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 
    Article 

    Google Scholar 

  • 39.

    Chan, Y. S., Huen, D. S., Glauert, R., Whiteway, E. & Russell, S. Optimising homing endonuclease gene drive performance in a semi-refractory species: the Drosophila melanogaster experience. PLoS ONE 8, e54130 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 40.

    Windbichler, N. et al. A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473, 212–215 (2011). This study is the first demonstration of nuclease-mediated gene drive in mosquitoes based on the homing endonuclease gene I-SceI.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 41.

    Carroll, D. Genome engineering with targetable nucleases. Annu. Rev. Biochem. 83, 409–439 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 42.

    Barrangou, R. et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709–1712 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 43.

    Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816–821 (2012). This foundational study developed the most widely used dual synthetic CRISPR system consisting of Cas9 endonuclease and gRNA components.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 44.

    Doudna, J. A., Sternberg, S. H. A Crack in Creation: Gene Editing and the Unthinkable Power to Control Evolution 281 (Houghton Mifflin Harcourt, 2017).

  • 45.

    Gantz, V. M. & Bier, E. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science 348, 442–444 (2015). This study reported the first CRISPR-based gene drive in a metazoan organism (D. melanogaster) with a specialized germline.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 46.

    Gantz, V. M. et al. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc. Natl Acad. Sci. USA 112, E6736–E6743 (2015). This study describes the first efficient CRISPR-based gene drive system in mosquitoes, which carried a dual anti-malarial effector cassette.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 47.

    Hammond, A. et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat. Biotechnol. 34, 78–83 (2016). This study describes the first efficient CRISPR-based suppression gene drive system in mosquitoes.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 48.

    Kyrou, K. et al. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat. Biotechnol. 36, 1062–1066 (2018). This study describes a highly efficient suppression gene drive system in mosquitoes targeting an invariant genome target site in the doublesex locus.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 49.

    Li, M. et al. Development of a confinable gene drive system in the human disease vector Aedes aegypti. eLife 9, e51701 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 50.

    Grunwald, H. A. et al. Super-Mendelian inheritance mediated by CRISPR-Cas9 in the female mouse germline. Nature 566, 105–109 (2019). This study provided the first proof-of-principle gene drive system in mammals, which selectively sustained drive via the female germline.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 51.

    DiCarlo, J. E., Chavez, A., Dietz, S. L., Esvelt, K. M. & Church, G. M. Safeguarding CRISPR-Cas9 gene drives in yeast. Nat. Biotechnol. 33, 1250–1255 (2015). This study demonstrated CRISPR-based gene conversion in diploid yeast, which could then be transmitted meiotically.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 52.

    Valderrama, J. A., Kulkarni, S. S., Nizet, V. & Bier, E. A bacterial gene-drive system efficiently edits and inactivates a high copy number antibiotic resistance locus. Nat. Commun. 10, 5726 (2019). This study generalizes the concept of gene drive to bacteria, where it is applied to efficiently reduce the frequency of antibiotic reistance.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    Esvelt, K. M., Smidler, A. L., Catteruccia, F. & Church, G. M. Concerning RNA-guided gene drives for the alteration of wild populations. eLife 3, e03401 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 54.

    Adolfi, A. et al. Efficient population modification gene-drive rescue system in the malaria mosquito Anopheles stephensi. Nat. Commun. 11, 5553 (2020). This study reports on the first recoded gene drive in mosquitoes that drove efficiently through both males and females based on the process of lethal/sterile mosaicism.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 55.

    Champer, J. et al. A CRISPR homing gene drive targeting a haplolethal gene removes resistance alleles and successfully spreads through a cage population. Proc. Natl Acad. Sci. USA 117, 24377–24383 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 56.

    Kandul, N. P., Liu, J., Bennett, J. B., Marshall, J. M. & Akbari, O. S. A confinable home-and-rescue gene drive for population modification. eLife 10, e65939 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 57.

    Terradas, G. et al. Inherently confinable split-drive systems in Drosophila. Nat. Commun. 12, 1480 (2021). This study further develops the strategy of inserting a recoded gene drive in genes essential for viability or reproduction in the context of split drive systems.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 58.

    Xu, X. S., Gantz, V. M., Siomava, N. & Bier, E. CRISPR/Cas9 and active genetics-based trans-species replacement of the endogenous Drosophila kni-L2 CRM reveals unexpected complexity. eLife 6, e30281 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 59.

    Lopez Del Amo, V. et al. A transcomplementing gene drive provides a flexible platform for laboratory investigation and potential field deployment. Nat. Commun. 11, 352 (2020). This study reports on the reconstitution of a full gene drive from split constituent parts.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    Guichard, A. et al. Efficient allelic-drive in Drosophila. Nat. Commun. 10, 1640 (2019). The study develops two allelic drive systems, copy-cutting and copy-grafting, to propagate favoured alleles of an essential gene.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 61.

    Kandul, N. P. et al. Assessment of a split homing based gene drive for efficient knockout of multiple genes. G3 10, 827–837 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 62.

    Xu, X.-R. S. et al. Active-genetic neutralizing elements for halting or deleting gene-drives. Mol. Cell 80, 246–262 (2020). This study reports on two drive-neutralizing systems that either inactivate (e-CHACR) or delete and replace (ERACR) a gene drive.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 63.

    Burt, A. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. Biol. Sci. 270, 921–928 (2003). This seminal modelling study provides the theoretical underpinnings for the modern gene-drive field.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 64.

    North, A. R., Burt, A. & Godfray, H. C. J. Modelling the potential of genetic control of malaria mosquitoes at national scale. BMC Biol. 17, 26 (2019). This study provides a comprehensive analysis of the perfomance of suppressive gene drives following iterative releases across various topographies.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 65.

    North, A. R., Burt, A. & Godfray, H. C. J. Modelling the suppression of a malaria vector using a CRISPR-Cas9 gene drive to reduce female fertility. BMC Biol. 18, 98 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 66.

    Collins, C. M., Bonds, J. A. S., Quinlan, M. M. & Mumford, J. D. Effects of the removal or reduction in density of the malaria mosquito, Anopheles gambiae s.l., on interacting predators and competitors in local ecosystems. Med. Vet. Entomol. 33, 1–15 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 67.

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

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 68.

    Gantz, V. M. & Bier, E. The dawn of active genetics. Bioessays 38, 50–63 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 69.

    Macias, V. M. & James, A. A. in Genetic Control of Malaria and Dengue (ed. Adelman, Z. N.) 423–444 (Elsevier Academic Press, 2015).

  • 70.

    Eckhoff, P. A., Wenger, E. A., Godfray, H. C. & Burt, A. Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics. Proc. Natl Acad. Sci. USA 114, E255–E264 (2017). This study provides a detailed analysis of drive parameters relevant to both suppression-based and modification-based drives and is the first to model a drive in the context of a two-dimensional environment.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 71.

    Hammond, A. M. et al. The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLoS Genet. 13, e1007039 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 72.

    Joyce, E. F., Paul, A., Chen, K. E., Tanneti, N. & McKim, K. S. Multiple barriers to nonhomologous DNA end joining during meiosis in Drosophila. Genetics 191, 739–746 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 73.

    Bozas, A., Beumer, K. J., Trautman, J. K. & Carroll, D. Genetic analysis of zinc-finger nuclease-induced gene targeting in Drosophila. Genetics 182, 641–651 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 74.

    Do, A. T., Brooks, J. T., Le Neveu, M. K. & LaRocque, J. R. Double-strand break repair assays determine pathway choice and structure of gene conversion events in Drosophila melanogaster. G3 4, 425–432 (2014).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 75.

    Wei, D. S. & Rong, Y. S. A genetic screen for DNA double-strand break repair mutations in Drosophila. Genetics 177, 63–77 (2007).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 76.

    Lin, C. C. & Potter, C. J. Non-Mendelian dominant maternal effects caused by CRISPR/Cas9 transgenic components in Drosophila melanogaster. G3 6, 3685–3691 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 77.

    Champer, J. et al. Novel CRISPR/Cas9 gene drive constructs reveal insights into mechanisms of resistance allele formation and drive efficiency in genetically diverse populations. PLoS Genet. 13, e1006796 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 78.

    Anopheles gambiae 1000 Genomes Consortiumet al. Genetic diversity of the African malaria vector Anopheles gambiae. Nature 552, 96–100 (2017).

    Article 
    CAS 

    Google Scholar 

  • 79.

    Deredec, A., Burt, A. & Godfray, H. C. The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179, 2013–2026 (2008).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 80.

    Fasulo, B. et al. A fly model establishes distinct mechanisms for synthetic CRISPR/Cas9 sex distorters. PLoS Genet. 16, e1008647 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 81.

    Galizi, R. et al. A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nat. Commun. 5, 3977 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 82.

    Galizi, R. et al. A CRISPR-Cas9 sex-ratio distortion system for genetic control. Sci. Rep. 6, 31139 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 83.

    Turner, J. M. Meiotic sex chromosome inactivation. Development 134, 1823–1831 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 84.

    Simoni, A. et al. A male-biased sex-distorter gene drive for the human malaria vector Anopheles gambiae. Nat. Biotechnol. 38, 1054–1060 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 85.

    Carballar-Lejarazu, R. & et al. Next-generation gene drive for population modification of the malaria vector mosquito, Anopheles gambiae.Proc. Natl Acad. Sci. USA 117, 22805–22814 (2020). This study describes a modification gene drive that propagates with high efficiency through both males and females.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 86.

    Pham, T. B. et al. Experimental population modification of the malaria vector mosquito, Anopheles stephensi. PLoS Genet. 15, e1008440 (2019).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 87.

    Dong, Y., Simoes, M. L. & Dimopoulos, G. Versatile transgenic multistage effector-gene combinations for Plasmodium falciparum suppression in Anopheles. Sci. Adv. 6, eaay5898 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 88.

    Dong, Y. et al. Engineered anopheles immunity to Plasmodium infection. PLoS Pathog. 7, e1002458 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 89.

    Isaacs, A. T. et al. Transgenic Anopheles stephensi coexpressing single-chain antibodies resist Plasmodium falciparum development. Proc. Natl Acad. Sci. USA 109, E1922–E1930 (2012). This study demonstrates 100% protection against parasite transmission in transgenic mosquitoes carrying a dual anti-parasite effector cassette.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 90.

    Haber, J. E. TOPping off meiosis. Mol. Cell 57, 577–581 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 91.

    Hammond, A. et al. Regulating the expression of gene drives is key to increasing their invasive potential and the mitigation of resistance. PLoS Genet. 17, e1009321 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 92.

    Lee, Y. et al. Genome-wide divergence among invasive populations of Aedes aegypti in California. BMC Genomics 20, 204 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 93.

    Callaway, E. Gene drives thwarted by emergence of resistant organisms. Nature 542, 15 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 94.

    Unckless, R. L., Clark, A. G. & Messer, P. W. Evolution of resistance against CRISPR/Cas9 gene drive. Genetics 205, 827–841 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 95.

    Drury, D. W., Dapper, A. L., Siniard, D. J., Zentner, G. E. & Wade, M. J. CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Sci. Adv. 3, e1601910 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 96.

    Schmidt, H. et al. Abundance of conserved CRISPR-Cas9 target sites within the highly polymorphic genomes of Anopheles and Aedes mosquitoes. Nat. Commun. 11, 1425 (2020). This study provides computational evidence that conserved CRISPR cleavage sites are abundant in the genome.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 97.

    Akbari, O. S. et al. Safeguarding gene drive experiments in the laboratory. Science 349, 927–929 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 98.

    Li, J. et al. Genome-block expression-assisted association studies discover malaria resistance genes in Anopheles gambiae. Proc. Natl Acad. Sci. USA 110, 20675–20680 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 99.

    Niu, G. et al. The fibrinogen-like domain of FREP1 protein is a broad-spectrum malaria transmission-blocking vaccine antigen. J. Biol. Chem. 292, 11960–11969 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 100.

    Zhang, G. et al. Anopheles midgut FREP1 mediates plasmodium invasion. J. Biol. Chem. 290, 16490–16501 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 101.

    Dong, Y., Simoes, M. L., Marois, E. & Dimopoulos, G. CRISPR/Cas9 -mediated gene knockout of Anopheles gambiae FREP1 suppresses malaria parasite infection. PLoS Pathog. 14, e1006898 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 102.

    Simoes, M. L., Caragata, E. P. & Dimopoulos, G. Diverse host and restriction factors regulate mosquito-pathogen interactions. Trends Parasitol. 34, 603–616 (2018).

    PubMed 
    Article 

    Google Scholar 

  • 103.

    Nash, A. et al. Integral gene drives for population replacement. Biol. Open 8, bio037762 (2019). This study describes a bipartite drive system that can enable testing of anti-parasite effector cassettes under standard mosquito confinement protocols.

    CAS 
    PubMed 

    Google Scholar 

  • 104.

    Enayati, A., Hanafi-Bojd, A. A., Sedaghat, M. M., Zaim, M. & Hemingway, J. Evolution of insecticide resistance and its mechanisms in Anopheles stephensi in the WHO Eastern Mediterranean Region. Malar. J. 19, 258 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 105.

    Ffrench-Constant, R. H., Williamson, M. S., Davies, T. G. & Bass, C. Ion channels as insecticide targets. J. Neurogenet. 30, 163–177 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 106.

    Silva, J. J. & Scott, J. G. Conservation of the voltage-sensitive sodium channel protein within the Insecta. Insect Mol. Biol. 29, 9–18 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 107.

    Casida, J. E. & Durkin, K. A. Novel GABA receptor pesticide targets. Pestic. Biochem. Physiol. 121, 22–30 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 108.

    Ihara, M., Buckingham, S. D., Matsuda, K. & Sattelle, D. B. Modes of action, resistance and toxicity of insecticides targeting nicotinic acetylcholine receptors. Curr. Med. Chem. 24, 2925–2934 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 109.

    Thapa, S., Lv, M. & Xu, H. Acetylcholinesterase: a primary target for drugs and insecticides. Mini Rev. Med. Chem. 17, 1665–1676 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 110.

    Kleinstiver, B. P. et al. Engineered CRISPR-Cas12a variants with increased activities and improved targeting ranges for gene, epigenetic and base editing. Nat. Biotechnol. 37, 276–282 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 111.

    Walton, R. T., Christie, K. A., Whittaker, M. N. & Kleinstiver, B. P. Unconstrained genome targeting with near-PAMless engineered CRISPR-Cas9 variants. Science 368, 290–296 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 112.

    Committee on Gene Drive Research in Non-Human Organisms: Recommendations for Responsible Conduct; Board on Life Sciences; Division on Earth and Life Studies; National Academies of Sciences, Engineering, and Medicine. Gene Drives on the Horizon: Advancing Science, Navigating Uncertainty, and Aligning Research with Public Values (The National Academies Press, 2016). This comprehensive advisory and historical review document summarizes consensus views for how to safely rear and study gene-drive systems in the laboratory.

  • 113.

    Adelman, Z. et al. Rules of the road for insect gene drive research and testing. Nat. Biotechnol. 35, 716–718 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 114.

    James, S. et al. Pathway to deployment of gene drive mosquitoes as a potential biocontrol tool for elimination of malaria in Sub-Saharan Africa: recommendations of a scientific working group(dagger). Am. J. Trop. Med. Hyg. 98, 1–49 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 115.

    James, S. L., Marshall, J. M., Christophides, G. K., Okumu, F. O. & Nolan, T. Toward the definition of efficacy and safety criteria for advancing gene drive-modified mosquitoes to field testing. Vector Borne Zoonotic Dis. 20, 237–251 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 116.

    Warmbrod, K. L. et al. Gene Drives: Pursuing Opportunities, Minimizing Risk – A Johns Hopkins University Report on Responsible Governance (Johns Hopkins Bloomberg School of Public Health, Center for Health Security, Johns Hopkins University, 2020).

  • 117.

    Vella, M. R., Gunning, C. E., Lloyd, A. L. & Gould, F. Evaluating strategies for reversing CRISPR-Cas9 gene drives. Sci. Rep. 7, 11038 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 118.

    Rode, N. O., Courtier-Orgogozo, V. & Debarre, F. Can a population targeted by a CRISPR-based homing gene drive be rescued? G3 10, 3403–3415 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 119.

    Fedoroff, N., Wessler, S. & Shure, M. Isolation of the transposable maize controlling elements Ac and Ds. Cell 35, 235–242 (1983).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 120.

    Paix, A. et al. Precision genome editing using synthesis-dependent repair of Cas9-induced DNA breaks. Proc. Natl Acad. Sci. USA 114, E10745–E10754 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 121.

    Wu, B., Luo, L. & Gao, X. J. Cas9-triggered chain ablation of cas9 as a gene drive brake. Nat. Biotechnol. 34, 137–138 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 122.

    Taxiarchi, C. et al. A genetically encoded anti-CRISPR protein constrains gene drive spread and prevents population suppression. Nat. Commun. 12, 3977 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 123.

    Conklin, B. R. On the road to a gene drive in mammals. Nature 566, 43–45 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 124.

    Salkeld, D. J. Vaccines for conservation: plague, prairie dogs & black-footed ferrets as a case study. Ecohealth 14, 432–437 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 125.

    Teem, J. L. et al. Genetic biocontrol for invasive species. Front. Bioeng. Biotechnol. 8, 452 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 126.

    Godwin, J. et al. Rodent gene drives for conservation: opportunities and data needs. Proc. Biol. Sci. 286, 20191606 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 127.

    McFarlane, G. R., Whitelaw, C. B. A. & Lillico, S. G. CRISPR-based gene drives for pest control. Trends Biotechnol. 36, 130–133 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 128.

    Klompe, S. E., Vo, P. L. H., Halpin-Healy, T. S. & Sternberg, S. H. Transposon-encoded CRISPR-Cas systems direct RNA-guided DNA integration. Nature 571, 219–225 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 129.

    Koonin, E. V., Makarova, K. S., Wolf, Y. I. & Krupovic, M. Evolutionary entanglement of mobile genetic elements and host defence systems: guns for hire. Nat. Rev. Genet. 21, 119–131 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 130.

    Strecker, J. et al. RNA-guided DNA insertion with CRISPR-associated transposases. Science 365, 48–53 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 131.

    Peters, J. E., Makarova, K. S., Shmakov, S. & Koonin, E. V. Recruitment of CRISPR-Cas systems by Tn7-like transposons. Proc. Natl Acad. Sci. USA 114, E7358–E7366 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 132.

    Wiegand, T. & Wiedenheft, B. CRISPR Surveillance Turns Transposon Taxi. CRISPR J. 3, 10–12 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 133.

    Hamilton, T. A. et al. Efficient inter-species conjugative transfer of a CRISPR nuclease for targeted bacterial killing. Nat. Commun. 10, 4544 (2019).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 134.

    Price, V. J. et al. Enterococcus faecalis CRISPR-cas is a robust barrier to conjugative antibiotic resistance dissemination in the murine intestine. mSphere 4, e00464-19 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 135.

    Rodrigues, M., McBride, S. W., Hullahalli, K., Palmer, K. L. & Duerkop, B. A. Conjugative delivery of CRISPR-Cas9 for the selective depletion of antibiotic-resistant enterococci. Antimicrob. Agents Chemother. 63, e01454-19 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 136.

    Carraro, N. et al. Plasmid-like replication of a minimal streptococcal integrative and conjugative element. Microbiology 162, 622–632 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 137.

    Brophy, J. A. N. et al. Engineered integrative and conjugative elements for efficient and inducible DNA transfer to undomesticated bacteria. Nat. Microbiol. 3, 1043–1053 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 138.

    Bikard, D. et al. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat. Biotechnol. 32, 1146–1150 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 139.

    Citorik, R. J., Mimee, M. & Lu, T. K. Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat. Biotechnol. 32, 1141–1145 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 140.

    Yosef, I., Manor, M., Kiro, R. & Qimron, U. Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc. Natl Acad. Sci. USA 112, 7267–7272 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 141.

    Park, J. Y. et al. Genetic engineering of a temperate phage-based delivery system for CRISPR/Cas9 antimicrobials against Staphylococcus aureus. Sci. Rep. 7, 44929 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 142.

    Pazda, M., Kumirska, J., Stepnowski, P. & Mulkiewicz, E. Antibiotic resistance genes identified in wastewater treatment plant systems – a review. Sci. Total. Env. 697, 134023 (2019).

    CAS 
    Article 

    Google Scholar 

  • 143.

    Kraemer, S. A., Ramachandran, A. & Perron, G. G. Antibiotic pollution in the environment: from microbial ecology to public policy. Microorganisms 7, 180 (2019).

    CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 

  • 144.

    Ram, G., Ross, H. F., Novick, R. P., Rodriguez-Pagan, I. & Jiang, D. Conversion of staphylococcal pathogenicity islands to CRISPR-carrying antibacterial agents that cure infections in mice. Nat. Biotechnol. 36, 971–976 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 145.

    Bier, E. & Nizet, V. Driving to safety: CRISPR-based genetic approaches to reducing antibiotic resistance. Trends Genet. https://doi.org/10.1016/j.tig.2021.02.007 (2021).

    Article 
    PubMed 

    Google Scholar 

  • 146.

    Rossati, A. et al. Climate, environment and transmission of malaria. Infez. Med. 24, 93–104 (2016).

    PubMed 

    Google Scholar 

  • 147.

    Fontenille, D. & Powell, J. R. From anonymous to public enemy: how does a mosquito become a feared arbovirus vector? Pathogens 9, 265 (2020).

    PubMed Central 
    Article 
    PubMed 

    Google Scholar 

  • 148.

    Lidani, K. C. F. et al. Chagas disease: from discovery to a worldwide health problem. Front. Public Health 7, 166 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 149.

    Buscher, P., Cecchi, G., Jamonneau, V. & Priotto, G. Human African trypanosomiasis. Lancet 390, 2397–2409 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 150.

    Desjeux, P. Leishmaniasis: current situation and new perspectives. Comp. Immunol. Microbiol. Infect. Dis. 27, 305–318 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 151.

    Saxena, V., Bolling, B. G. & Wang, T. West nile virus. Clin. Lab. Med. 37, 243–252 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 152.

    Simon, L. V., Kong, E. L. & Graham, C. in St. Louis Encephalitis (StatPearls, 2020).

  • 153.

    Feng, X. et al. Optimized CRISPR tools and site-directed transgenesis towards gene drive development in Culex quinquefasciatus mosquitoes. Nat. Commun. 12, 2960 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 154.

    Nepomichene, T. N., Andrianaivolambo, L., Boyer, S. & Bourgouin, C. Efficient method for establishing F1 progeny from wild populations of Anopheles mosquitoes. Malar. J. 16, 21 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 155.

    Marchand, R. P. A new cage for observing mating behavior of wild Anopheles gambiae in the laboratory. J. Am. Mosq. Control. Assoc. 1, 234–236 (1985).

    CAS 
    PubMed 

    Google Scholar 

  • 156.

    Nunes-da-Fonseca, R., Berni, M., Tobias-Santos, V., Pane, A. & Araujo, H. M. Rhodnius prolixus: from classical physiology to modern developmental biology. Genesis https://doi.org/10.1002/dvg.22995 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 157.

    Chaverra-Rodriguez, D. et al. Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing. Nat. Commun. 9, 3008 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 158.

    Macias, V. M. et al. Cas9-mediated gene-editing in the malaria mosquito anopheles stephensi by ReMOT Control. G3 10, 1353–1360 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 159.

    Chaverra-Rodriguez, D. et al. Germline mutagenesis of Nasonia vitripennis through ovarian delivery of CRISPR-Cas9 ribonucleoprotein. Insect Mol. Biol. 29, 569–577 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 160.

    Heu, C. C., McCullough, F. M., Luan, J. & Rasgon, J. L. CRISPR-Cas9-based genome editing in the silverleaf whitefly (Bemisia tabaci). CRISPR J. 3, 89–96 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 161.

    Prowse, T. A., Adikusuma, F., Cassey, P., Thomas, P. & Ross, J. V. A Y-chromosome shredding gene drive for controlling pest vertebrate populations. eLife 8, e41873 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 162.

    Carballar-Lejarazu, R. & James, A. A. Population modification of Anopheline species to control malaria transmission. Pathog. Glob. Health 111, 424–435 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 163.

    Annas, G. J. et al. A code of ethics for gene drive research. CRISPR J. 4, 19–24 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 164.

    Bier, E. & Sober, E. Gene editing and the war against malaria. Am. Sci. 108, 162–169 (2020).

    Article 

    Google Scholar 

  • 165.

    Long, K. C. et al. Core commitments for field trials of gene drive organisms. Science 370, 1417–1419 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 166.

    Kormos, A. et al. Application of the relationship-based model to engagement for field trials of genetically engineered malaria vectors.Am. J. Trop. Med. Hyg. 104, 805–811 (2020).

    PubMed Central 
    PubMed 

    Google Scholar 

  • 167.

    World Health Organization. Guidance framework for testing of genetically modified mosquitoes. WHO http://apps.who.int/iris/bitstream/10665/127889/1/9789241507486_eng.pdf (2014).

  • 168.

    Smith, D. L., McKenzie, F. E., Snow, R. W. & Hay, S. I. Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol. 5, e42 (2007).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 169.

    Brauer, F., Castillo-Chavez, C., Mubayi, A. & Towers, S. Some models for epidemics of vector-transmitted diseases. Infect. Dis. Model. 1, 79–87 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 170.

    Deredec, A., Godfray, H. C. & Burt, A. Requirements for effective malaria control with homing endonuclease genes. Proc. Natl Acad. Sci. USA 108, E874–E880 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 171.

    Escalante, A. A. & Pacheco, M. A. Malaria molecular epidemiology: an evolutionary genetics perspective. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.AME-0010-2019 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 172.

    Selvaraj, P. et al. Vector genetics, insecticide resistance and gene drives: An agent-based modeling approach to evaluate malaria transmission and elimination. PLoS Comput. Biol. 16, e1008121 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 


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