Opening the toolkit for genetic analysis and control of Anopheles mosquito vectors

World Health Organization, 2018 The Anopheles gambiae Genomes Consortium, 2017, Genetic diversity of the African malaria vector Anopheles gambiae, Nature, 552, 96, 10.1038/nature24995 Catteruccia, 2009, RNAi in the malaria vector, Anopheles gambiae, Methods Mol Biol, 555, 63, 10.1007/978-1-60327-295-7_5 Simoes, 2017, Immune regulation of plasmodium is anopheles species specific and infection intensity dependent, MBio, 8, 10.1128/mBio.01631-17 Osta, 2004, Innate immunity in the malaria vector Anopheles gambiae: comparative and functional genomics, J Exp Biol, 207, 2551, 10.1242/jeb.01066 Blandin, 2004, Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae, Cell, 116, 661, 10.1016/S0092-8674(04)00173-4 Ingham, 2017, The transcription factor Maf-S regulates metabolic resistance to insecticides in the malaria vector Anopheles gambiae, BMC Genom, 18, 669, 10.1186/s12864-017-4086-7 Doran, 2017, Mosquito aging modulates the heart rate and the proportional directionality of heart contractions, J Insect Physiol, 101, 47, 10.1016/j.jinsphys.2017.06.013 Krzywinska, 2016, A maleness gene in the malaria mosquito Anopheles gambiae, Science, 353, 67, 10.1126/science.aaf5605 Du, 2017, Suppression of Laccase 2 severely impairs cuticle tanning and pathogen resistance during the pupal metamorphosis of Anopheles sinensis (Diptera: Culicidae), Parasit Vectors, 10, 171, 10.1186/s13071-017-2118-4 Mysore, 2017, Yeast interfering RNA larvicides targeting neural genes induce high rates of Anopheles larval mortality, Malar J, 16, 461, 10.1186/s12936-017-2112-5 Lycett, 2006, Anopheles gambiae P450 reductase is highly expressed in oenocytes and in vivo knockdown increases permethrin susceptibility, Insect Mol Biol, 15, 321, 10.1111/j.1365-2583.2006.00647.x Grossman, 2001, Germline transformation of the malaria vector, Anopheles gambiae, with the piggyBac transposable element, Insect Mol Biol, 10, 597, 10.1046/j.0962-1075.2001.00299.x Catteruccia, 2000, Stable germline transformation of the malaria mosquito Anopheles stephensi, Nature, 405, 959, 10.1038/35016096 Adelman, 2016, Chapter 8 – gene insertion and deletion in mosquitoes, 139 Wang, 2013, Genetic approaches to interfere with malaria transmission by vector mosquitoes, Trends Biotechnol, 31, 185, 10.1016/j.tibtech.2013.01.001 O’Brochta, 2012, Gal4-based enhancer-trapping in the malaria mosquito Anopheles stephensi, G3 (Bethesda), 2, 1305, 10.1534/g3.112.003582 Adolfi, 2018, Multi-tissue GAL4-mediated gene expression in all Anopheles gambiae life stages using an endogenous polyubiquitin promoter, Insect Biochem Mol Biol, 96, 1, 10.1016/j.ibmb.2018.03.005 Meredith, 2013, Next-generation site-directed transgenesis in the malaria vector mosquito Anopheles gambiae: self-docking strains expressing germline-specific phiC31 integrase, PLoS ONE, 8, e59264, 10.1371/journal.pone.0059264 Hammond, 2016, A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae, Nat Biotechnol, 34, 78, 10.1038/nbt.3439 Volohonsky, 2015, Tools for Anopheles gambiae transgenesis, G3 (Bethesda), 5, 1151, 10.1534/g3.115.016808 Lycett, 2004, Conditional expression in the malaria mosquito Anopheles stephensi with tet-on and tet-off systems, Genetics, 167, 1781, 10.1534/genetics.104.028175 Marinotti, 2013, Development of a population suppression strain of the human malaria vector mosquito, Anopheles stephensi, Malar J, 12, 142, 10.1186/1475-2875-12-142 Lynd, 2012, Development of the bi-partite Gal4-UAS system in the African malaria mosquito, Anopheles gambiae, PLoS ONE, 7, e31552, 10.1371/journal.pone.0031552 Riabinina, 2016, Organization of olfactory centres in the malaria mosquito Anopheles gambiae, Nat Commun, 7, 13010, 10.1038/ncomms13010 Guha, 2017, Programmable genome editing tools and their regulation for efficient genome engineering, Comput Struct Biotechnol J, 15, 146, 10.1016/j.csbj.2016.12.006 Windbichler, 2008, Targeting the X chromosome during spermatogenesis induces Y chromosome transmission ratio distortion and early dominant embryo lethality in Anopheles gambiae, PLoS Genet, 4, e1000291, 10.1371/journal.pgen.1000291 Yamamoto, 2018, Malaria infectivity of xanthurenic acid-deficient anopheline mosquitoes produced by TALEN-mediated targeted mutagenesis, Transgenic Res, 27, 51, 10.1007/s11248-018-0057-2 Volohonsky, 2017, transgenic expression of the anti-parasitic factor TEP1 in the malaria mosquito Anopheles gambiae, PLoS Pathog, 13, e1006113, 10.1371/journal.ppat.1006113 Smidler, 2013, Targeted mutagenesis in the malaria mosquito using TALE nucleases, PLoS ONE, 8, e74511, 10.1371/journal.pone.0074511 Li, 2018, Highly efficient site-specific mutagenesis in malaria mosquitoes using CRISPR, G3 (Bethesda), 8, 653, 10.1534/g3.117.1134 Gantz, 2015, Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi, Proc Natl Acad Sci U S A, 112, E6736, 10.1073/pnas.1521077112 Dong, 2018, CRISPR/Cas9-mediated gene knockout of Anopheles gambiae FREP1 suppresses malaria parasite infection, PLoS Pathog, 14, e1006898, 10.1371/journal.ppat.1006898 Wang, 2015, 2A self-cleaving peptide-based multi-gene expression system in the silkworm Bombyx mori, Sci Rep, 5, 16273, 10.1038/srep16273 Bui, 2018, Live calcium imaging of Aedes aegypti neuronal tissues reveals differential importance of chemosensory systems for life-history-specific foraging strategies, bioRxiv Hammond, 2017, Gene drives to fight malaria: current state and future directions, Pathog Glob Health, 111, 412, 10.1080/20477724.2018.1438880 Godfray, 2017, How driving endonuclease genes can be used to combat pests and disease vectors, BMC Biol, 15, 81, 10.1186/s12915-017-0420-4 Burt, 2018, Gene drive to reduce malaria transmission in sub-Saharan Africa, J Respons Innov, 5, S66, 10.1080/23299460.2017.1419410 Galizi, 2014, A synthetic sex ratio distortion system for the control of the human malaria mosquito, Nat Commun, 5, 3977, 10.1038/ncomms4977 Galizi, 2016, A CRISPR-Cas9 sex-ratio distortion system for genetic control, Sci Rep, 6, 31139, 10.1038/srep31139 Criscione, 2016, GUY1 confers complete female lethality and is a strong candidate for a male-determining factor in Anopheles stephensi, Elife, 5, 10.7554/eLife.19281 Bernardini, 2014, Site-specific genetic engineering of the Anopheles gambiae Y chromosome, Proc Natl Acad Sci U S A, 111, 7600, 10.1073/pnas.1404996111 Carballar-Lejarazu, 2017, Population modification of Anopheline species to control malaria transmission, Pathog Glob Health, 111, 424, 10.1080/20477724.2018.1427192 Zhang, 2015, Anopheles midgut FREP1 mediates plasmodium invasion, J Biol Chem, 290, 16490, 10.1074/jbc.M114.623165 Isaacs, 2011, Engineered resistance to Plasmodium falciparum development in transgenic Anopheles stephensi, PLoS Pathog, 7, e1002017, 10.1371/journal.ppat.1002017 Isaacs, 2012, Transgenic Anopheles stephensi coexpressing single-chain antibodies resist Plasmodium falciparum development, Proc Natl Acad Sci U S A, 109, E1922, 10.1073/pnas.1207738109 Ribeiro, 1994, Transposable elements as population drive mechanisms: specification of critical parameter values, J Med Entomol, 31, 10, 10.1093/jmedent/31.1.10 Macias, 2017, Gene drive for mosquito control: where did it come from and where are we headed?, Int J Environ Res Public Health, 14, 10.3390/ijerph14091006 Windbichler, 2011, A synthetic homing endonuclease-based gene drive system in the human malaria mosquito, Nature, 473, 212, 10.1038/nature09937 Gantz, 2016, The dawn of active genetics, Bioessays, 38, 50, 10.1002/bies.201500102 Marshall, 2017, Overcoming evolved resistance to population-suppressing homing-based gene drives, Sci Rep, 7, 3776, 10.1038/s41598-017-02744-7 Hammond, 2017, The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito, PLoS Genet, 13, e1007039, 10.1371/journal.pgen.1007039 Benedict, 2018, Recommendations for laboratory containment and management of gene drive systems in arthropods, Vector Borne Zoonotic Dis, 18, 2, 10.1089/vbz.2017.2121 Adelman, 2017, Developing standard operating procedures for gene drive research in disease vector mosquitoes, Pathog Glob Health, 111, 436, 10.1080/20477724.2018.1424514 Kolopack, 2017, Informed consent in field trials of gene-drive mosquitoes, Gates Open Res, 1, 14, 10.12688/gatesopenres.12771.1 Min, 2018, Harnessing gene drive, J Respons Innov, 5, S40, 10.1080/23299460.2017.1415586 Lambert, 2018, The use of driving endonuclease genes to suppress mosquito vectors of malaria in temporally variable environments, Malar J, 17, 154, 10.1186/s12936-018-2259-8 Eckhoff, 2017, Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics, Proc Natl Acad Sci U S A, 114, E255, 10.1073/pnas.1611064114 Beaghton, 2017, Requirements for driving antipathogen effector genes into populations of disease vectors by homing, Genetics, 205, 1587, 10.1534/genetics.116.197632 Pike, 2014, Characterization of the Rel2-regulated transcriptome and proteome of Anopheles stephensi identifies new anti-Plasmodium factors, Insect Biochem Mol Biol, 52, 82, 10.1016/j.ibmb.2014.06.005 Wang, 2013, Ability of TEP1 in intestinal flora to modulate natural resistance of Anopheles dirus, Exp Parasitol, 134, 460, 10.1016/j.exppara.2013.04.003 Bahia, 2013, The role of reactive oxygen species in Anopheles aquasalis response to Plasmodium vivax infection, PLoS ONE, 8, e57014, 10.1371/journal.pone.0057014 Brown, 2003, Stable and heritable gene silencing in the malaria vector Anopheles stephensi, Nucleic Acids Res, 31, e85, 10.1093/nar/gng085 Perera, 2002, Germ-line transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac/EGFP transposon vector is routine and highly efficient, Insect Mol Biol, 11, 291, 10.1046/j.1365-2583.2002.00336.x Lycett, 2012, The Anopheles gambiae alpha-tubulin-1b promoter directs neuronal, testes and developing imaginal tissue specific expression and is a sensitive enhancer detector, Insect Mol Biol, 21, 79, 10.1111/j.1365-2583.2011.01112.x Andrés, 2016, Auditory efferent system modulates mosquito hearing, Curr Biol, 26, 2028, 10.1016/j.cub.2016.05.077