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      Combating mosquito-borne diseases using genetic control technologies

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          Abstract

          Mosquito-borne diseases, such as dengue and malaria, pose significant global health burdens. Unfortunately, current control methods based on insecticides and environmental maintenance have fallen short of eliminating the disease burden. Scalable, deployable, genetic-based solutions are sought to reduce the transmission risk of these diseases. Pathogen-blocking Wolbachia bacteria, or genome engineering-based mosquito control strategies including gene drives have been developed to address these problems, both requiring the release of modified mosquitoes into the environment. Here, we review the latest developments, notable similarities, and critical distinctions between these promising technologies and discuss their future applications for mosquito-borne disease control.

          Abstract

          Mosquito-borne diseases pose significant global health burdens. In this review, the authors explore Wolbachia and genome engineering approaches to mosquito-borne disease population control.

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          Most cited references95

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          Wolbachia: master manipulators of invertebrate biology.

          Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.
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            Concerning RNA-guided gene drives for the alteration of wild populations.

            Gene drives may be capable of addressing ecological problems by altering entire populations of wild organisms, but their use has remained largely theoretical due to technical constraints. Here we consider the potential for RNA-guided gene drives based on the CRISPR nuclease Cas9 to serve as a general method for spreading altered traits through wild populations over many generations. We detail likely capabilities, discuss limitations, and provide novel precautionary strategies to control the spread of gene drives and reverse genomic changes. The ability to edit populations of sexual species would offer substantial benefits to humanity and the environment. For example, RNA-guided gene drives could potentially prevent the spread of disease, support agriculture by reversing pesticide and herbicide resistance in insects and weeds, and control damaging invasive species. However, the possibility of unwanted ecological effects and near-certainty of spread across political borders demand careful assessment of each potential application. We call for thoughtful, inclusive, and well-informed public discussions to explore the responsible use of this currently theoretical technology.
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              Suppression of a Field Population of Aedes aegypti in Brazil by Sustained Release of Transgenic Male Mosquitoes

              The increasing burden of dengue, and the relative failure of traditional vector control programs highlight the need to develop new control methods. SIT using self-limiting genetic technology is one such promising method. A self-limiting strain of Aedes aegypti, OX513A, has already reached the stage of field evaluation. Sustained releases of OX513A Ae. aegypti males led to 80% suppression of a target wild Ae. aegypti population in the Cayman Islands in 2010. Here we describe sustained series of field releases of OX513A Ae. aegypti males in a suburb of Juazeiro, Bahia, Brazil. This study spanned over a year and reduced the local Ae. aegypti population by 95% (95% CI: 92.2%-97.5%) based on adult trap data and 81% (95% CI: 74.9-85.2%) based on ovitrap indices compared to the adjacent no-release control area. The mating competitiveness of the released males (0.031; 95% CI: 0.025-0.036) was similar to that estimated in the Cayman trials (0.059; 95% CI: 0.011 – 0.210), indicating that environmental and target-strain differences had little impact on the mating success of the OX513A males. We conclude that sustained release of OX513A males may be an effective and widely useful method for suppression of the key dengue vector Ae. aegypti. The observed level of suppression would likely be sufficient to prevent dengue epidemics in the locality tested and other areas with similar or lower transmission.
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                Author and article information

                Contributors
                oakbari@ucsd.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                19 July 2021
                19 July 2021
                2021
                : 12
                : 4388
                Affiliations
                [1 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Division of Biological Sciences, Section of Cell and Developmental Biology, , University of California, ; San Diego, CA USA
                [2 ]GRID grid.47840.3f, ISNI 0000 0001 2181 7878, Division of Epidemiology and Biostatistics, School of Public Health, , University of California, ; Berkeley, CA USA
                [3 ]GRID grid.510960.b, ISNI 0000 0004 7798 3869, Innovative Genomics Institute, ; Berkeley, CA USA
                [4 ]GRID grid.63622.33, ISNI 0000 0004 0388 7540, Arthropod Genetics, , The Pirbright Institute, ; Pirbright, UK
                [5 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Department of Entomology, , The Pennsylvania State University, ; University Park, PA USA
                [6 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, The Center for Infectious Disease Dynamics, , The Pennsylvania State University, ; University Park, PA USA
                [7 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, The Huck Institutes of the Life Sciences, , The Pennsylvania State University, ; University Park, PA USA
                [8 ]GRID grid.9227.e, ISNI 0000000119573309, Present Address: State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, , Chinese Academy of Sciences, ; Beijing, China
                Author information
                http://orcid.org/0000-0002-4106-6167
                http://orcid.org/0000-0003-0665-0066
                http://orcid.org/0000-0003-0603-7341
                http://orcid.org/0000-0002-4050-8429
                http://orcid.org/0000-0002-6853-9884
                Article
                24654
                10.1038/s41467-021-24654-z
                8290041
                34282149
                c26c7b16-e3a3-4c9b-ba47-69bb9828319f
                © The Author(s) 2021

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 23 May 2021
                : 30 June 2021
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000185, United States Department of Defense | Defense Advanced Research Projects Agency (DARPA);
                Award ID: HR0011-17-2-0047
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100006492, Division of Intramural Research, National Institute of Allergy and Infectious Diseases (Division of Intramural Research of the NIAID);
                Award ID: R21RAI149161A
                Award ID: R01AI151004
                Award Recipient :
                Categories
                Review Article
                Custom metadata
                © The Author(s) 2021

                Uncategorized
                animal breeding,crispr-cas systems
                Uncategorized
                animal breeding, crispr-cas systems

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