Transgenesis and paratransgenesis to control insect-borne diseases: Current status and future challenges

Hill, 2005, Arthropod-borne diseases: vector control in the genomics era, Nat Rev Microbiol, 3, 262, 10.1038/nrmicro1101 Wimmer, 2003, Innovations: applications of insect transgenesis, Nat Rev Genet, 4, 225, 10.1038/nrg1021 Jasinskiene, 1998, Stable transformation of the yellow fever mosquito, Aedes aegypti, with the Hermes element from the housefly, Proc Natl Acad Sci U S A, 95, 3743, 10.1073/pnas.95.7.3743 Rodrigues, 2006, Germline transformation of Aedes fluviatilis (Diptera:Culicidae) with the piggyBac transposable element, Mem Inst Oswaldo Cruz, 101, 755, 10.1590/S0074-02762006000700008 Coates, 1998, Mariner transposition and transformation of the yellow fever mosquito Aedes aegypti, Proc Natl Acad Sci U S A, 95, 3748, 10.1073/pnas.95.7.3748 Pinkerton, 2000, Green fluorescent protein as a genetic marker in transgenic Aedes aegypti, Insect Mol Biol, 9, 1, 10.1046/j.1365-2583.2000.00133.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 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 Nolan, 2002, piggyBac-mediated germline transformation of the malaria mosquito Anopheles stephensi using the red fluorescent protein dsRED as a selectable marker, J Biol Chem, 277, 8759, 10.1074/jbc.C100766200 Abraham, 2005, Driving midgut-specific expression and secretion of a foreign protein in transgenic mosquitoes with AgAper1 regulatory elements, Insect Mol Biol, 14, 271, 10.1111/j.1365-2583.2004.00557.x Brown, 2003, Stable and heritable gene silencing in the malaria vector Anopheles stephensi, Nucleic Acids Res, 31, e85, 10.1093/nar/gng085 Ito, 2002, Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite, Nature, 417, 452, 10.1038/417452a Moreira, 2002, Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes, J Biol Chem, 277, 40839, 10.1074/jbc.M206647200 Kim, 2004, Ectopic expression of a cecropin transgene in the human malaria vector mosquito Anopheles gambiae (Diptera: Culicidae): effects on susceptibility to Plasmodium, J Med Entomol, 41, 447, 10.1603/0022-2585-41.3.447 Catteruccia, 2005, An Anopheles transgenic sexing strain for vector control, Nat Biotechnol, 23, 1414, 10.1038/nbt1152 Catteruccia, 2000, Stable germline transformation of the malaria mosquito Anopheles stephensi, Nature, 405, 959, 10.1038/35016096 Allen, 2001, Stable, germ-line transformation of Culex quinquefasciatus (Diptera: Culicidae), J Med Entomol, 38, 701, 10.1603/0022-2585-38.5.701 Franz, 2006, Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti, Proc Natl Acad Sci U S A, 103, 4198, 10.1073/pnas.0600479103 Rodrigues, 2008, Expression of a mutated phospholipase A2 in transgenic Aedes fluviatilis mosquitoes impacts Plasmodium gallinaceum development, Insect Mol Biol, 17, 175, 10.1111/j.1365-2583.2008.00791.x Shin, 2003, Transgenesis and reverse genetics of mosquito innate immunity, J Exp Biol, 206, 3835, 10.1242/jeb.00640 Durvasula, 1997, Prevention of insect-borne disease: an approach using transgenic symbiotic bacteria, Proc Natl Acad Sci U S A, 94, 3274, 10.1073/pnas.94.7.3274 Durvasula, 1999, Expression of a functional antibody fragment in the gut of Rhodnius prolixus via transgenic bacterial symbiont Rhodococcus rhodnii, Med Vet Entomol, 13, 115, 10.1046/j.1365-2915.1999.00175.x Durvasula, 2008, Genetic transformation of a Corynebacterial symbiont from the Chagas disease vector Triatoma infestans, Exp Parasitol, 119, 94, 10.1016/j.exppara.2007.12.020 Cheng, 1999, Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies, Insect Mol Biol, 8, 125, 10.1046/j.1365-2583.1999.810125.x Favia, 2007, Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector, Proc Natl Acad Sci U S A, 104, 9047, 10.1073/pnas.0610451104 Jin, 2009, The virulent Wolbachia strain wMelPop efficiently establishes somatic infections in the malaria vector Anopheles gambiae, Appl Environ Microbiol, 75, 3373, 10.1128/AEM.00207-09 Ren, 2008, Viral paratransgenesis in the malaria vector Anopheles gambiae, PLoS Pathog, 4, e1000135, 10.1371/journal.ppat.1000135 Ward, 2001, Aedes aegypti transducing densovirus pathogenesis and expression in Aedes aegypti and Anopheles gambiae larvae, Insect Mol Biol, 10, 397, 10.1046/j.0962-1075.2001.00276.x Lobo, 2002, Germ line transformation of the yellow fever mosquito, Aedes aegypti, mediated by transpositional insertion of a piggyBac vector, Insect Mol Biol, 11, 133, 10.1046/j.1365-2583.2002.00317.x Kokoza, 2000, Engineering blood meal-activated systemic immunity in the yellow fever mosquito Aedes aegypti, Proc Natl Acad Sci U S A, 97, 9144, 10.1073/pnas.160258197 Moreira, 2000, Robust gut-specific gene expression in transgenic Aedes aegypti mosquitoes, Proc Natl Acad Sci U S A, 97, 10895, 10.1073/pnas.97.20.10895 Kokoza, 2001, Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac[3xP3-EGFP afm], Insect Biochem Mol Biol, 31, 1137, 10.1016/S0965-1748(01)00120-5 Nirmala, 2006, Functional characterization of the promoter of the vitellogenin gene, AsVg1, of the malaria vector, Anopheles stephensi, Insect Biochem Mol Biol, 36, 694, 10.1016/j.ibmb.2006.05.011 Yoshida, 2006, Robust salivary gland-specific transgene expression in Anopheles stephensi mosquito, Insect Mol Biol, 15, 403, 10.1111/j.1365-2583.2006.00645.x Chen, 2007, The Anopheles gambiae vitellogenin gene (VGT2) promoter directs persistent accumulation of a reporter gene product in transgenic Anopheles stephensi following multiple bloodmeals, Am J Trop Med Hyg, 76, 1118, 10.4269/ajtmh.2007.76.1118 Lombardo, 2005, An Anopheles gambiae salivary gland promoter analysis in Drosophila melanogaster and Anopheles stephensi, Insect Mol Biol, 14, 207, 10.1111/j.1365-2583.2004.00549.x Bian, 2005, Transgenic alteration of Toll immune pathway in the female mosquito Aedes aegypti, Proc Natl Acad Sci U S A, 102, 13568, 10.1073/pnas.0502815102 Shin, 2003, Relish-mediated immune deficiency in the transgenic mosquito Aedes aegypti, Proc Natl Acad Sci U S A, 100, 2616, 10.1073/pnas.0537347100 Coates, 1999, Promoter-directed expression of recombinant fire-fly luciferase in the salivary glands of Hermes-transformed Aedes aegypti, Gene, 226, 317, 10.1016/S0378-1119(98)00557-5 Ghosh, 2001, Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display peptide library, Proc Natl Acad Sci U S A, 98, 13278, 10.1073/pnas.241491198 Lycett, 2002, Anti-malarial mosquitoes?, Nature, 417, 387, 10.1038/417387a Catteruccia, 2003, Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes, Science, 299, 1225, 10.1126/science.1081453 Marrelli, 2007, Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood, Proc Natl Acad Sci U S A, 104, 5580, 10.1073/pnas.0609809104 Li, 2008, Fitness of transgenic Anopheles stephensi mosquitoes expressing the SM1 peptide under the control of a vitellogenin promoter, J Hered, 99, 275, 10.1093/jhered/esn004 Irvin, 2004, Assessing fitness costs for transgenic Aedes aegypti expressing the GFP marker and transposase genes, Proc Natl Acad Sci U S A, 101, 891, 10.1073/pnas.0305511101 Hickey, 1982, Selfish DNA: a sexually-transmitted nuclear parasite, Genetics, 101, 519, 10.1093/genetics/101.3-4.519 Ribeiro, 1994, Transposable elements as population drive mechanisms: specification of critical parameter values, J Med Entomol, 31, 10, 10.1093/jmedent/31.1.10 Boete, 2002, A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control, Malar J, 1, 3, 10.1186/1475-2875-1-3 Atkinson, 2004, Trangenic mosquitoes and DNA research safeguards, 785 Adelman, 2007, nanos gene control DNA mediates developmentally regulated transposition in the yellow fever mosquito Aedes aegypti, Proc Natl Acad Sci U S A, 104, 9970, 10.1073/pnas.0701515104 O'Brochta, 2003, Gene vector and transposable element behavior in mosquitoes, J Exp Biol, 206, 3823, 10.1242/jeb.00638 Lampe, 1998, Factors affecting transposition of the Himar1 mariner transposon in vitro, Genetics, 149, 179, 10.1093/genetics/149.1.179 Engels, 1997, Invasions of P elements, Genetics, 145, 11 Fraser, 1983, Acquisition of host cell DNA sequences by baculoviruses: relationship between host DNA insertions and FP mutants of Autographa californica and Galleria mellonella nuclear polyhedrosis viruses, J Virol, 47, 287, 10.1128/JVI.47.2.287-300.1983 Sinkins, 2006, Gene drive systems for insect disease vectors, Nat Rev Genet, 7, 427, 10.1038/nrg1870 Chen, 2007, A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila, Science, 316, 597, 10.1126/science. 1138595 Marshall, 2009, Malaria control with transgenic mosquitoes, PLoS Med, 6, e20, 10.1371/journal.pmed.1000020 Horn, 2003, A transgene-based, embryo-specific lethality system for insect pest management, Nat Biotechnol, 21, 64, 10.1038/nbt769 Thomas, 2000, Insect population control using a dominant, repressible, lethal genetic system, Science, 287, 2474, 10.1126/science.287.5462.2474 Krafsur, 1987, Screwworm eradication in North and Central America, Parasitol Today, 3, 131, 10.1016/0169-4758(87)90196-7 Robinson, 1999, Genetic sexing strains in the medfly, Ceratitis capitata: development, mass rearing and field application, Trends Entomol., 2, 81 Vreysen, 2000, Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique, J Econ Entomol, 93, 123, 10.1603/0022-0493-93.1.123 Carlson, 2006, Densoviruses for control and genetic manipulation of mosquitoes, Adv Virus Res, 68, 361, 10.1016/S0065-3527(06)68010-X Carlson, 1995, Molecular genetic manipulation of mosquito vectors, Annu Rev Entomol, 40, 359, 10.1146/annurev.en.40.010195.002043 Aksoy, 2008, Paratransgenesis applied for control of tsetse transmitted sleeping sickness, Adv Exp Med Biol, 627, 35, 10.1007/978-0-387-78225-6_3 Weiss, 2006, Interspecific transfer of bacterial endosymbionts between tsetse fly species: infection establishment and effect on host fitness, Appl Environ Microbiol, 72, 7013, 10.1128/AEM.01507-06 Riehle, 2007, Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut, Int J Parasitol, 37, 595, 10.1016/j.ijpara.2006.12.002 Damiani, 2008, Paternal transmission of symbiotic bacteria in malaria vectors, Curr Biol, 18, R1087, 10.1016/j.cub.2008.10.040 de Lara Capurro, 2000, 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, 10.4269/ajtmh.2000.62.427 Powers, 1996, Molecularly engineered resistance to California serogroup virus replication in mosquito cells and mosquitoes, Proc Natl Acad Sci U S A, 93, 4187, 10.1073/pnas.93.9.4187 Travanty, 2004, Using RNA interference to develop dengue virus resistance in genetically modified Aedes aegypti, Insect Biochem Mol Biol, 34, 607, 10.1016/j.ibmb.2004.03.013 Adelman, 2001, Sindbis virus-induced silencing of dengue viruses in mosquitoes, Insect Mol Biol, 10, 265, 10.1046/j.1365-2583.2001.00267.x Higgs, 1998, Engineered resistance in Aedes aegypti to a West African and a South American strain of yellow fever virus, Am J Trop Med Hyg, 58, 663, 10.4269/ajtmh.1998.58.663 Olson, 1996, Genetically engineered resistance to dengue-2 virus transmission in mosquitoes, Science, 272, 884, 10.1126/science.272.5263.884 Blair, 2000, Molecular strategies for interrupting arthropod-borne virus transmission by mosquitoes, Clin Microbiol Rev, 13, 651, 10.1128/CMR.13.4.651-661.2000 Shiao, 2001, Effect of prophenoloxidase expression knockout on the melanization of microfilariae in the mosquito Armigeres subalbatus, Insect Mol Biol, 10, 315, 10.1046/j.0962-1075.2001.00268.x Barrillas-Mury, 2005, Immune response of vectors, 785 McMeniman, 2009, Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti, Science, 323, 141, 10.1126/science.1165326 Read, 2009, Microbiology. Mosquitoes cut short, Science, 323, 51, 10.1126/science.1168659 Read, 2009, How to make evolution-proof insecticides for malaria control, PLoS Biol, 7, e1000058, 10.1371/journal.pbio.1000058 Killeen, 2000, A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control, Am J Trop Med Hyg, 62, 535, 10.4269/ajtmh.2000.62.535 Black, 2004, Population biology as a tool to study vector-borne diseases, 187 Garrett-Jones, 1964, Prognosis for interruption of malaria transmission through assessment of the mosquito's vectorial capacity, Nature, 204, 1173, 10.1038/2041173a0