1921
Volume 94, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract

Dengue fever, caused by dengue virus (DENV), is endemic in more than 100 countries. The lack of effective treatment of patients and the suboptimal efficacies of the tetravalent vaccine in trials highlight the urgent need to develop alternative strategies to lessen the burden of dengue fever. , an obligate intracellular bacterium, is being developed as a biocontrol strategy against dengue because it limits the replication of the DENV in the mosquito vector, . However, several recent studies have demonstrated the sensitivity of pathogens, vectors, and their symbionts to temperature. To understand how the tripartite interactions between the mosquito, DENV, and may change under different temperature regimes, we assessed the vector competence and transmission potential of DENV-infected mosquitoes reared at a common laboratory setting of a constant 25°C and at two diurnal temperature settings with mean of 25°C and 28°C and a fluctuating range of 8°C (±4°C). Temperature significantly affected DENV infection rate in the mosquitoes. Furthermore, temperature significantly influenced the proportion of mosquitoes that achieved transmission potential as measured by the presence of virus in the saliva. Regardless of the temperature regimes, significantly and efficiently reduced the proportion of mosquitoes achieving infection and transmission potential across all the temperature regimes studied. This work reinforces the robustness of the biocontrol strategy to field conditions in Cairns, Australia, and suggests that similar studies are required for local mosquito genotypes and field relevant temperatures for emerging field release sites globally.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.15-0801
2016-04-06
2017-09-24
Loading full text...

Full text loading...

/deliver/fulltext/14761645/94/4/812.html?itemId=/content/journals/10.4269/ajtmh.15-0801&mimeType=html&fmt=ahah

References

  1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GRW, Simmons CP, Scott TW, Farrar JJ, Hay SI, , 2013. The global distribution and burden of dengue. Nature 496: 504507.[Crossref]
  2. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martinez E, Nathan MB, Pelegrino JL, Simmons C, Yoksan S, Peeling RW, , 2010. Dengue: a continuing global threat. Nat Rev Microbiol 8: S7S16.[Crossref]
  3. Kyle JL, Harris E, , 2008. Global spread and persistence of dengue. Annu Rev Microbiol 62: 7192.[Crossref]
  4. Ross TM, , 2010. Dengue virus. Clin Lab Med 30: 149160.[Crossref]
  5. Halstead SB, , 2008. Dengue virus-mosquito interactions. Annu Rev Entomol 53: 273291.[Crossref]
  6. Gubler DJ, , 2002. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10: 100103.[Crossref]
  7. Sabchareon A, Wallace D, Sirivichayakul C, Limkittikul K, Chanthavanich P, Suvannadabba S, Jiwariyavej V, Dulyachai W, Pengsaa K, Wartel TA, Moureau A, Saville M, Bouckenooghe A, Viviani S, Tornieporth NG, Lang J, , 2012. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380: 15591567.[Crossref]
  8. McGraw EA, O'Neill SL, , 2013. Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol 11: 181193.[Crossref]
  9. Capeding MR, Tran NH, Hadinegoro SR, Ismail HI, Chotpitayasunondh T, Chua MN, Luong CQ, Rusmil K, Wirawan DN, Nallusamy R, Pitisuttithum P, Thisyakorn U, Yoon IK, van der Vliet D, Langevin E, Laot T, Hutagalung Y, Frago C, Boaz M, Wartel TA, Tornieporth NG, Saville M, Bouckenooghe A, CYDS Group, , 2014. Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial. Lancet 384: 13581365.[Crossref]
  10. Zug R, Koehncke A, Hammerstein P, , 2012. Epidemiology in evolutionary time: the case of Wolbachia horizontal transmission between arthropod host species. J Evol Biol 25: 21492160.[Crossref]
  11. Werren JH, Baldo L, Clark ME, , 2008. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741751.[Crossref]
  12. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN, , 2008. Wolbachia and virus protection in insects. Science 322: 702.[Crossref]
  13. Teixeira L, Ferreira A, Ashburner M, , 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster PLoS Biol 6: e2.[Crossref]
  14. Caragata EP, Rances E, Hedges LM, Gofton AW, Johnson KN, O'Neill SL, McGraw EA, , 2013. Dietary cholesterol modulates pathogen blocking by Wolbachia . PLoS Pathog 9: e1003459.[Crossref]
  15. Zhang G, Hussain M, O'Neill SL, Asgari S, , 2013. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti . Proc Natl Acad Sci USA 110: 1027610281.[Crossref]
  16. Xi Z, Khoo CC, Dobson SL, , 2005. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310: 326328.[Crossref]
  17. McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang YF, O'Neill SL, , 2009. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti . Science 323: 141144.[Crossref]
  18. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, Leong YS, Dong Y, Axford J, Kriesner P, Lloyd AL, Ritchie SA, O'Neill SL, Hoffmann AA, , 2011. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450453.[Crossref]
  19. Bian G, Xu Y, Lu P, Xie Y, Xi Z, , 2010. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti . PLoS Pathog 6: e1000833.[Crossref]
  20. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, Greenfield M, Durkan M, Leong YS, Dong Y, Cook H, Axford J, Callahan AG, Kenny N, Omodei C, McGraw EA, Ryan PA, Ritchie SA, Turelli M, O'Neill SL, , 2011. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454457.[Crossref]
  21. Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips B, Billington K, Axford JK, Montgomery B, Turley AP, O'Neill SL, , 2014. Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 8: e3115.[Crossref]
  22. Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, van den Hurk A, McGraw EA, O'Neill SL, , 2014. Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia . PLoS Negl Trop Dis 8: e2688.[Crossref]
  23. Kramer LD, Ebel GD, , 2003. Dynamics of flavivirus infection in mosquitoes. Adv Virus Res 60: 187232.[Crossref]
  24. Macdonald G, , 1951. The Epidemiology and Control of Malaria. London and New York: Oxford University Press.
  25. Bosio CF, Beaty BJ, Black WC, , 1998. Quantitative genetics of vector competence for dengue-2 virus in Aedes aegypti . Am J Trop Med Hyg 59: 965970.
  26. Anderson JR, Rico-Hesse R, , 2006. Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus. Am J Trop Med Hyg 75: 886892.
  27. Lambrechts L, Chevillon C, Albright RG, Thaisomboonsuk B, Richardson JH, Jarman RG, Scott TW, , 2009. Genetic specificity and potential for local adaptation between dengue viruses and mosquito vectors. BMC Evol Biol 9: 160.[Crossref]
  28. Ramirez JL, Souza-Neto J, Cosme RT, Rovira J, Ortiz A, Pascale JM, Dimopoulos G, , 2012. Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Neglect Trop Dis 6: e1561.[Crossref]
  29. Alto BW, Lounibos LP, Higgs S, Juliano SA, , 2005. Larval competition differentially affects Arbovirus infection in Aedes mosquitoes. Ecology 86: 32793288.[Crossref]
  30. Grimstad PR, Walker ED, , 1991. Aedes triseriatus (Diptera: Culicidae) and La Crosse virus. IV. Nutritional deprivation of larvae affects the adult barriers to infection and transmission. J Med Entomol 28: 378386.[Crossref]
  31. Watts DM, Burke DS, Harrison BA, Whitmire RE, Nisalak A, , 1987. Effect of temperature on the vector efficiency of Aedes aegypti for dengue-2 virus. Am J Trop Med Hyg 36: 143152.
  32. Thomas MB, Blanford S, , 2003. Thermal biology in insect-parasite interactions. Trends Ecol Evol 18: 344350.[Crossref]
  33. Turell MJ, Rossi CA, Bailey CL, , 1985. Effect of extrinsic incubation temperature on the ability of Aedes taeniorhynchus and Culex pipiens to transmit Rift Valley fever virus. Am J Trop Med Hyg 34: 12111218.
  34. Black WC, Bennett KE, Gorrochotegui-Escalante N, Barillas-Mury CV, Fernandez-Salas I, Munoz MD, Farfan-Ale JA, Olson KE, Beaty BJ, , 2002. Flavivirus susceptibility in Aedes aegypti . Arch Med Res 33: 379388.[Crossref]
  35. Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D, Kittayapong P, Edman JD, , 2000. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: blood feeding frequency. J Med Entomol 37: 89101.[Crossref]
  36. Lambrechts L, Paaijmans KP, Fansiri T, Carrington LB, Kramer LD, Thomas MB, Scott TW, , 2011. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti . Proc Natl Acad Sci USA 108: 74607465.[Crossref]
  37. Carrington LB, Armijos MV, Lambrechts L, Scott TW, , 2013. Fluctuations at a low mean temperature accelerate dengue virus transmission by Aedes aegypti . PLoS Negl Trop Dis 7: e2735.[Crossref]
  38. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB, , 2010. Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107: 1513515139.[Crossref]
  39. Mouton L, Henri H, Charif D, Bouletreau M, Vavre F, , 2007. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol Lett 3: 210213.[Crossref]
  40. Zhang XZ, Sheng J, Plevka P, Kuhn RJ, Diamond MS, Rossmann MG, , 2013. Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci USA 110: 67956799.[Crossref]
  41. Lu P, Bian G, Pan X, Xi Z, , 2012. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 6: e1754.[Crossref]
  42. Murdock CC, Blanford S, Hughes GL, Rasgon JL, Thomas MB, , 2014. Temperature alters Plasmodium blocking by Wolbachia . Sci Rep 4: 3932.[Crossref]
  43. Hanna JN, Ritchie SA, , 2009. Outbreaks of dengue in north Queensland, 1990–2008. Commun Dis Intell 33: 3233.
  44. Available at: weatherzone.com. Accessed January 2015.
  45. Ye YH, Carrasco AM, Frentiu FD, Chenoweth SF, Beebe NW, van den Hurk AF, Simmons CP, O'Neill SL, McGraw EA, , 2015. Wolbachia reduces the transmission potential of Dengue-infected Aedes aegypti . PLoS Negl Trop Dis 9: e0003894.[Crossref]
  46. Ritchie SA, Pyke AT, Hall-Mendelin S, Day A, Mores CN, Christofferson RC, Gubler DJ, Bennett SN, van den Hurk AF, , 2013. An explosive epidemic of DENV-3 in Cairns, Australia. PLoS One 8: e68137.[Crossref]
  47. Ye YH, Ng TS, Frentiu FD, Walker T, van den Hurk AF, O'Neill SL, Beebe NW, McGraw EA, , 2014. Comparative susceptibility of mosquito populations in North Queensland, Australia to oral infection with dengue virus. Am J Trop Med Hyg 90: 422430.[Crossref]
  48. Richards SL, Pesko K, Alto BW, Mores CN, , 2007. Reduced infection in mosquitoes exposed to blood meals containing previously frozen flaviviruses. Virus Res 129: 224227.[Crossref]
  49. Kien DTH, Tuan TV, Hanh TNT, Chau TNB, Huy HLA, Wills BA, Simmons CP, , 2011. Validation of an internally controlled one-step real-time multiplex RT-PCR assay for the detection and quantitation of dengue virus RNA in plasma. J Virol Methods 177: 168173.[Crossref]
  50. Ferguson NM, Kien DT, Clapham H, Aguas R, Trung VT, Chau TN, Popovici J, Ryan PA, O'Neill SL, McGraw EA, Long VT, Dui le T, Nguyen HL, Chau NV, Wills B, Simmons CP, , 2015. Modeling the impact on virus transmission of Wolbachia-mediated blocking of dengue virus infection of Aedes aegypti . Sci Transl Med 7: 279ra37.[Crossref]
  51. Benjamini Y, Hochberg Y, , 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289300.
  52. Wiwatanaratanabutr I, Kittayapong P, , 2009. Effects of crowding and temperature on Wolbachia infection density among life cycle stages of Aedes albopictus . J Invertebr Pathol 102: 220224.[Crossref]
  53. Clancy DJ, Hoffmann AA, , 1998. Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans . Entomol Exp Appl 86: 1324.[Crossref]
  54. Reynolds KT, Thomson LJ, Hoffmann AA, , 2003. The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster . Genetics 164: 10271034.
  55. Murdock CC, Paaijmans KP, Cox-Foster D, Read AF, Thomas MB, , 2012. Rethinking vector immunology: the role of environmental temperature in shaping resistance. Nat Rev Microbiol 10: 869876.[Crossref]
  56. Rances E, Ye YH, Woolfit M, McGraw EA, O'Neill SL, , 2012. The relative importance of innate immune priming in wolbachia-mediated dengue interference. PLoS Pathog 8: e1002548.[Crossref]
  57. Pan XL, Zhou GL, Wu JH, Bian GW, Lu P, Raikhel AS, Xi ZY, , 2012. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti . Proc Natl Acad Sci USA 109: E23E31.[Crossref]
  58. Ramirez JL, Short SM, Bahia AC, Saraiva RG, Dong Y, Kang S, Tripathi A, Mlambo G, Dimopoulos G, , 2014. Chromobacterium Csp_P reduces malaria and dengue infection in vector mosquitoes and has entomopathogenic and in vitro anti-pathogen activities. PLoS Pathog 10: e1004398.[Crossref]
  59. Prado SS, Hung KY, Daugherty MP, Almeida RP, , 2010. Indirect effects of temperature on stink bug fitness, via maintenance of gut-associated symbionts. Appl Environ Microbiol 76: 12611266.[Crossref]
  60. Zouache K, Fontaine A, Vega-Rua A, Mousson L, Thiberge JM, Lourenco-De-Oliveira R, Caro V, Lambrechts L, Failloux AB, , 2014. Three-way interactions between mosquito population, viral strain and temperature underlying chikungunya virus transmission potential. Proc Biol Sci 281.[Crossref]
  61. Alto BW, Bettinardi D, , 2013. Temperature and dengue virus infection in mosquitoes: independent effects on the immature and adult stages. Am J Trop Med Hyg 88: 497505.[Crossref]
  62. Buckner EA, Alto BW, Philip Lounibos L, , 2015. Larval temperature-food effects on adult mosquito infection and vertical transmission of dengue-1 virus. J Med Entomol 53: 9198.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.15-0801
Loading
/content/journals/10.4269/ajtmh.15-0801
Loading

Data & Media loading...

  • Received : 08 Nov 2015
  • Accepted : 04 Jan 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error