Establishment of a Wolbachia Superinfection in Aedes aegypti Mosquitoes as a Potential Approach for Future Resistance Management

PLoS Pathogens

Volumn 12, Issue 2, 2016, Pages

  Joubert, D Albert ^a   Walker, Thomas ^a,e   Carrington, Lauren B ^b,c   De Bruyne, Jyotika Taneja ^a   Kien, Duong Hue T ^b   Hoang, Nhat Le Thanh ^b   Chau, Nguyen Van Vinh ^d   Iturbe Ormaetxe, Iñaki ^a   Simmons, Cameron P ^b,c   O’Neill, Scott L ^a  

^a MONASH UNIVERSITY   (Australia)

^b OXFORD UNIVERSITY CLINICAL RESEARCH UNIT   (Viet Nam)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^e LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AEDES AEGYPTI; ARTICLE; CONTROLLED STUDY; DENGUE; DISEASE PREDISPOSITION; FEMALE; FERTILITY; LIFESPAN; LONGEVITY; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; SUPERINFECTION; VECTOR CONTROL; VIRUS REPLICATION; WOLBACHIA; AEDES; ANIMAL; BIOLOGICAL PEST CONTROL; DENGUE VIRUS; HUMAN; IMMUNOLOGY; INSECT VECTOR; MICROBIOLOGY; PROCEDURES; RICKETTSIACEAE INFECTION; SALIVA; VIROLOGY;

AEDES; ANIMALS; DENGUE; DENGUE VIRUS; FEMALE; HUMANS; INSECT VECTORS; PEST CONTROL, BIOLOGICAL; RICKETTSIACEAE INFECTIONS; SALIVA; SUPERINFECTION; VIRUS REPLICATION; WOLBACHIA;

EID: 84959521088     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005434     Document Type: Article

References (45)

1. Hertig M, Wolbach SB, Studies on Rickettsia-Like Micro-Organisms in Insects. The Journal of medical research. 1924;44(3):329–74 7. 19972605
2. Werren JH, Baldo L, Clark ME, Wolbachia: master manipulators of invertebrate biology. Nature reviews Microbiology. 2008;6(10):741–51. doi: 10.1038/nrmicro196918794912
3. Zug R, Hammerstein P, Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PloS one. 2012;7(6):e38544. doi: 10.1371/journal.pone.003854422685581
4. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH, How many species are infected with Wolbachia?—A statistical analysis of current data. FEMS microbiology letters. 2008;281(2):215–20. doi: 10.1111/j.1574-6968.2008.01110.x18312577
5. Werren JH, O'Neill SL, O'Neill SL, Hoffmann AA, Werren JH, The evolution of heritable symbionts. In: Influential Passengers. New York: Oxford University Press; 1997. p. 1–41.
6. Stouthamer R, Breeuwer JA, Hurst GD, Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual review of microbiology. 1999;53:71–102. 10547686
7. Yen JH, Barr AR, The etiological agent of cytoplasmic incompatibility in Culex pipiens. Journal of invertebrate pathology. 1973;22(2):242–50. 4206296
8. Atyame CM, Labbe P, Dumas E, Milesi P, Charlat S, Fort P, et al. Wolbachia divergence and the evolution of cytoplasmic incompatibility in Culex pipiens. PloS one. 2014;9(1):e87336. doi: 10.1371/journal.pone.008733624498078
9. McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang YF, et al. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science. 2009;323(5910):141–4. doi: 10.1126/science.116532619119237
10. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell. 2009;139(7):1268–78. doi: 10.1016/j.cell.2009.11.04220064373
11. Teixeira L, Ferreira A, Ashburner M, The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS biology. 2008;6(12):e2. doi: 10.1371/journal.pbio.100000219222304
12. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature. 2011;476(7361):450–3. doi: 10.1038/nature1035521866159
13. Kambris Z, Cook PE, Phuc HK, Sinkins SP, Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science. 2009;326(5949):134–6. Epub 2009/10/03. doi: 10.1126/science.117753119797660
14. Bian G, Joshi D, Dong Y, Lu P, Zhou G, Pan X, et al. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science. 2013;340(6133):748–51. doi: 10.1126/science.123619223661760
15. Hughes GL, Rivero A, Rasgon JL, Wolbachia can enhance Plasmodium infection in mosquitoes: implications for malaria control?PLoS pathogens. 2014;10(9):e1004182. doi: 10.1371/journal.ppat.100418225187984
16. Murdock CC, Blanford S, Hughes GL, Rasgon JL, Thomas MB, Temperature alters Plasmodium blocking by Wolbachia. Scientific reports. 2014;4:3932. doi: 10.1038/srep0393224488176
17. Caragata EP, Rances E, Hedges LM, Gofton AW, Johnson KN, O'Neill SL, et al. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS pathogens. 2013;9(6):e1003459. doi: 10.1371/journal.ppat.100345923825950
18. Rances E, Ye YH, Woolfit M, McGraw EA, O'Neill SL, The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS pathogens. 2012;8(2):e1002548. doi: 10.1371/journal.ppat.100254822383881
19. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature. 2011;476(7361):454–7. doi: 10.1038/nature1035621866160
20. Iturbe-Ormaetxe I, Walker T, SL ON Wolbachia and the biological control of mosquito-borne disease. EMBO reports. 2011;12(6):508–18. doi: 10.1038/embor.2011.8421546911
21. Min KT, Benzer S, Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proceedings of the National Academy of Sciences of the United States of America. 1997;94(20):10792–6. 9380712
22. Suh E, Mercer DR, Fu Y, Dobson SL, Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Applied and environmental microbiology. 2009;75(24):7783–8. doi: 10.1128/AEM.01331-0919820149
23. Zhukova MV, Kiseleva E, The virulent Wolbachia strain wMelPop increases the frequency of apoptosis in the female germline cells of Drosophila melanogaster. BMC microbiology. 2012;12Suppl 1:S15. doi: 10.1186/1471-2180-12-S1-S1522375935
24. Turelli M, Cytoplasmic incompatibility in populations with overlapping generations. Evolution; international journal of organic evolution. 2010;64(1):232–41. doi: 10.1111/j.1558-5646.2009.00822.x19686264
25. Bian G, Xu Y, Lu P, Xie Y, Xi Z, The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS pathogens. 2010;6(4):e1000833. doi: 10.1371/journal.ppat.100083320368968
26. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, Sullivan W, Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS pathogens. 2005;1(2):e14. 16228015
27. Serbus LR, Sullivan W, A cellular basis for Wolbachia recruitment to the host germline. PLoS pathogens. 2007;3(12):e190. 18085821
28. Sinkins SP, Braig HR, O'Neill SL, Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proceedings Biological sciences / The Royal Society. 1995;261(1362):325–30. 8587875
29. Yeap HL, Axford JK, Popovici J, Endersby NM, Iturbe-Ormaetxe I, Ritchie SA, et al. Assessing quality of life-shortening Wolbachia-infected Aedes aegypti mosquitoes in the field based on capture rates and morphometric assessments. Parasites & vectors. 2014;7:58.
30. Nguyen TH, Nguyen HL, Nguyen TY, Vu SN, Tran ND, Le TN, et al. Field evaluation of the establishment potential of wmelpop Wolbachia in Australia and Vietnam for dengue control. Parasites & vectors. 2015;8:563.
31. Ferguson NM, Kien DT, Clapham H, Aguas R, Trung VT, Chau TN, et al. Modeling the impact on virus transmission of Wolbachia-mediated blocking of dengue virus infection of Aedes aegypti. Science translational medicine. 2015;7(279):279ra37. doi: 10.1126/scitranslmed.301037025787763
32. Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, van den Hurk A, et al. Limited Dengue Virus Replication in Field-Collected Aedes aegypti Mosquitoes Infected with Wolbachia. PLoS neglected tropical diseases. 2014;8(2):e2688. Epub 2014/03/04. doi: 10.1371/journal.pntd.000268824587459
33. Pan X, Zhou G, Wu J, Bian G, Lu P, Raikhel AS, et al. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(1):E23–31. doi: 10.1073/pnas.111693210822123956
34. Chrostek E, Marialva MS, Esteves SS, Weinert LA, Martinez J, Jiggins FM, et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS genetics. 2013;9(12):e1003896. Epub 2013/12/19. doi: 10.1371/journal.pgen.100389624348259
35. Rances E, Johnson TK, Popovici J, Iturbe-Ormaetxe I, Zakir T, Warr CG, et al. The toll and Imd pathways are not required for wolbachia-mediated dengue virus interference. Journal of virology. 2013;87(21):11945–9. doi: 10.1128/JVI.01522-1323986574
36. Molloy JC, Sinkins SP, Wolbachia Do Not Induce Reactive Oxygen Species-Dependent Immune Pathway Activation in Aedes albopictus. Viruses. 2015;7(8):4624–39. doi: 10.3390/v708283626287231
37. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN, Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Applied and environmental microbiology. 2012;78(19):6922–9. doi: 10.1128/AEM.01727-1222843518
38. Martinez J, Longdon B, Bauer S, Chan YS, Miller WJ, Bourtzis K, et al. Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS pathogens. 2014;10(9):e1004369. doi: 10.1371/journal.ppat.100436925233341
39. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN, Wolbachia and virus protection in insects. Science. 2008;322(5902):702. Epub 2008/11/01. doi: 10.1126/science.116241818974344
40. Holmes EC, Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. Journal of virology. 2003;77(20):11296–8. 14512579
41. Nguyen T, Nguyen H, Nguyen T, SN V ND T Le T, et al. Field evaluation of the establishment potential of wMelpop Wolbachia in Australia and Vietnam for dengue control. PLoS neglected tropical diseases. Submitted.
42. Russell BM, Kay BH, Shipton W, Survival of Aedes aegypti (Diptera: Culicidae) eggs in surface and subterranean breeding sites during the northern Queensland dry season. Journal of medical entomology. 2001;38(3):441–5. 11372971
43. Trpis M, Dry season survival of Aedes aegypti eggs in various breeding sites in the Dar es Salaam area, Tanzania. Bulletin of the World Health Organization. 1972;47(3):433–7. 4539825
44. Hoffmann AA, Goundar AA, Long SA, Johnson PH, Ritchie SA, Invasion of Wolbachia at the residential block level is associated with local abundance of Stegomyia aegypti, yellow fever mosquito, populations and property attributes. Medical and veterinary entomology. 2014;28Suppl 1:90–7. doi: 10.1111/mve.1207725171611
45. Nguyet MN, Duong TH, Trung VT, Nguyen TH, Tran CN, Long VT, et al. Host and viral features of human dengue cases shape the population of infected and infectious Aedes aegypti mosquitoes. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(22):9072–7. doi: 10.1073/pnas.130339511023674683