Insect-specific viruses detected in laboratory mosquito colonies and their potential implications for experiments evaluating arbovirus vector competence

American Journal of Tropical Medicine and Hygiene

Volumn 92, Issue 2, 2015, Pages 422-428

  Bolling, Bethany G ^a,b   Vasilakis, Nikos ^a   Guzman, Hilda ^a   Widen, Steven G ^a   Wood, Thomas G ^a   Popov, Vsevolod L ^a   Thangamani, Saravanan ^a   Tesh, Robert B ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b TEXAS DEPARTMENT OF STATE HEALTH SERVICES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

AEDES ALBOPICTUS; ANIMAL EXPERIMENT; ARBOVIRUS; ARTICLE; CLINICAL EVALUATION; CLINICAL LABORATORY; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GENE SEQUENCE; HOST; INSECT VIRUS; MALE; MOSQUITO; NEXT GENERATION SEQUENCING; NONHUMAN; ORGANISM COLONY; SEQUENCE ANALYSIS; VIRUS CELL INTERACTION; VIRUS CULTURE; VIRUS DETECTION; VIRUS INFECTION; VIRUS ISOLATION; VIRUS LIKE AGENT; VIRUS REPLICATION; AEDES; ANIMAL; CELL LINE; DISEASE CARRIER; GENETICS; PHYLOGENY; PHYSIOLOGY; TRANSMISSION; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIROLOGY;

AEDES ALBOPICTUS; ARBOVIRUS; HEXAPODA;

AEDES; ANIMALS; ARBOVIRUS INFECTIONS; ARBOVIRUSES; CELL LINE; FEMALE; INSECT VECTORS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; PHYLOGENY;

EID: 84922326531     PISSN: 00029637     EISSN: 14761645     Source Type: Journal    
DOI: 10.4269/ajtmh.14-0330     Document Type: Article

References (46)

1. Weaver SC, ReisenWK, 2010. Present and future arboviral threats. Antiviral Res 85:328-345.
2. Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M, Dimopoulos G, 2011. Natural microbemediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332:855-858.
3. Glaser RL, MeolaMA, 2010. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5:e11977.
4. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN, 2008. Wolbachia and virus protection in insects. Science 322:702.
5. Ramirez JL, Souza-Neto J, Torres Cosme R, 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 Negl Trop Dis 6:e1561.
6. Chouaia B, Rossi P, Montagna M, Ricci I, Crotti E, Damiani C, Epis S, Faye I, Sagnon N, Alma A, Favia G, Daffonchio D, Bandi C, 2010. Molecular evidence for multiple infections as revealed by typing of Asaia bacterial symbionts of four mosquito species. Appl Environ Microbiol 76:7444-7450.
7. Terenius O, Lindh JM, Eriksson-Gonzales K, Bussière L, Laugen AT, Bergquist H, Titanji K, Faye I, 2012. Midgut bacterial dynamics in Aedes aegypti. FEMS Microbiol Ecol 80:556-565.
8. Bishop-Lilly KA, Turell MJ, Willner KM, Butani A, Nolan NM, Lentz SM, Akmal A, Mateczun A, Brahmbhatt TN, Sozhamannan S, Whitehouse CA, Read TD, 2010. Arbovirus detection in insect vectors by rapid, high-throughput pyrosequencing. PLoS Negl Trop Dis 4:e878.
9. Attoui H, Mohd Jaafar F, Belhouchet M, Biagini P, Cantaloube J-F, de Micco P, de Lamballerie X, 2005. Expansion of family Reoviridae to include nine-segmented dsRNA viruses: isolation and characterization of a new virus designated Aedes pseudoscutellaris reovirus assigned to a proposed genus (Dinovernavirus). Virology 343:212-223.
10. Cook S, Moureau G, Kitchen A, Gould EA, de Lamballerie X, Holmes EC, Harbach RE, 2012. Molecular evolution of the insect-specific flaviviruses. J Gen Virol 93:223-234.
11. Nasar F, Palacios G, Gorchakov RV, Guzman H, Da Rosa AP, Savji N, Popov VL, Sherman MB, Lipkin WI, Tesh RB, Weaver SC, 2012. Eilat virus, a unique alphavirus with host range restricted to insects by RNA replication. Proc Natl Acad Sci USA 109:14622-14627.
12. Quan P-L, Junglen S, Tashmukhamedova A, Conlan S, Hutchison SK, Kurth A, Ellerbrok H, Egholm M, Briese T, Leendertz FH, Lipkin WI, 2010. Moussa virus: a new member of the Rhabdoviridae family isolated from Culex decens mosquitoes in Côte d'Ivoire. Virus Res 147:17-24.
13. Tyler S, Bolling BG, Blair CD, Brault AC, Pabbaraju K, Armijos MV, Clark DC, Calisher CH, Drebot MA, 2011. Distribution and phylogenetic comparisons of a novel mosquito flavivirus sequence present in Culex tarsalis mosquitoes from western Canada with viruses isolated in California and Colorado. Am J Trop Med Hyg 85:162-168.
14. Vasilakis N, Forrester NL, Palacios G, Nasar F, Savji N, Rossi SL, Guzman H, Wood TG, Popov V, Gorchakov R, González AV, Haddow AD, Watts DM, da Rosa AP, Weaver SC, Lipkin WI, Tesh RB, 2013. Negevirus: a proposed new taxon of insectspecific viruses with wide geographic distribution. J Virol 87:2475-2488.
15. Marklewitz M, Zirkel F, Rwego IB, Heidemann H, Trippner P, Kurth A, Kallies R, Briese T, Lipkin WI, Drosten C, Gillespie TR, Junglen S, 2013. Discovery of a unique novel clade of mosquito-associated bunyaviruses. J Virol 87:12850-12865.
16. Sang RC, Gichogo A, Gachoya J, Dunster MD, Ofula V, Hunt AR, Crabtree MB, Miller BR, Dunster LM, 2003. Isolation of a new flavivirus related to cell fusing agent virus (CFAV) from field-collected flood-water Aedes mosquitoes sampled from a dambo in central Kenya. Arch Virol 148:1085-1093.
17. Bolling BG, Eisen L, Moore CG, Blair CD, 2011. Insect-specific flaviviruses from Culex mosquitoes in Colorado, with evidence of vertical transmission. Am J Trop Med Hyg 85:169-177.
18. Saiyasombat R, Bolling BG, Brault AC, Bartholomay LC, Blitvich BJ, 2011. Evidence of efficient transovarial transmission of Culex flavivirus by Culex pipiens (Diptera: Culicidae). J Med Entomol 48:1031-1038.
19. Haddow AD, Guzman H, Popov VL, Wood TG, Widen SG, Haddow AD, Tesh RB, Weaver SC, 2013. First isolation of Aedes flavivirus in the Western Hemisphere and evidence of vertical transmission in the mosquito Aedes (Stegomyia) albopictus (Diptera: Culicidae). Virology 440:134-139.
20. Bolling BG, Olea-Popelka FJ, Eisen L, Moore CG, Blair CD, 2012. Transmission dynamics of an insect-specific flavivirus in a naturally infected Culex pipiens laboratory colony and effects of co-infection on vector competence for West Nile virus. Virology 427:90-97.
21. Hobson-Peters J, Yam AW, Lu JW, Setoh YX, May FJ, Kurucz N, Walsh S, Prow NA, Davis SS, Weir R, Melville L, Hunt N, Webb RI, Blitvich BJ, Whelan P, Hall RA, 2013. A new insectspecific flavivirus from northern Australia suppresses replication of West Nile virus and Murray Valley encephalitis virus in co-infected mosquito cells. PLoS ONE 8:e56534.
22. Kent RJ, Crabtree MB, Miller BR, 2010. Transmission of West Nile virus by Culex quinquefasciatus Say infected with Culex Flavivirus Izabal. PLoS Negl Trop Dis 4:e671.
23. Higgs S, 2005. Care, maintenance, and experimental infection of mosquitoes. Marquardt WC, ed. Biology of Disease Vectors. Second edition. Burlington, MA: Elsevier, 733-739.
24. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I, 2009. ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117-1123.
25. Langmead B, Salzberg SL, 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359.
26. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP, 2011. Integrative genomics viewer. Nat Biotechnol 29:24-26.
27. Posada D, Crandall KA, 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
28. Huelsenbeck JP, Ronquist F, 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
29. Ronquist F, Huelsenbeck JP, 2003. MrBayes 3: Bayesian phylogenetic inference undermixedmodels. Bioinformatics 19:1572-1574.
30. Hoshino K, Isawa H, Tsuda Y, Sawabe K, Kobayashi M, 2009. Isolation and characterization of a new insect flavivirus from Aedes albopictus and Aedes flavopictus mosquitoes in Japan. Virology 391:119-129.
31. Stollar V, Thomas L, 1975. An agent in the Aedes aegypti cell line (Peleg) which causes fusion of Aedes albopictus cells. Virology 64:367-377.
32. Cook S, Bennett SN, Holmes EC, De Chesse R, Moureau G, de Lamballerie X, 2006. Isolation of a new strain of the flavivirus cell fusing agent virus in a natural mosquito population from Puerto Rico. J Gen Virol 87:735-748.
33. Yamanaka A, Thongrungkiat S, Ramasoota P, Konishi E, 2013. Genetic and evolutionary analysis of cell-fusing agent virus based on Thai strains isolated in 2008 and 2012. Infect Genet Evol 19:188-194.
34. Roiz D, Vázquez A, Rosso F, Arnoldi D, Girardi M, Cuevas L, Perez-Pastrana E, Sánchez-Seco MP, Tenorio A, Rizzoli A, 2012. Detection of a new insect flavivirus and isolation of Aedes flavivirus in northern Italy. Parasit Vectors 5:223.
35. Hoshino K, Isawa H, Tsuda Y, Yano K, Sasaki T, Yuda M, Takasaki T, Kobayashi M, Sawabe K, 2007. Genetic characterization of a new insect flavivirus isolated from Culex pipiens mosquito in Japan. Virology 359:405-414.
36. Cirimotich CM, Ramirez JL, Dimopoulos G, 2011. Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10:307-310.
37. Weiss B, Aksoy S, 2011. Microbiome influences on insect host vector competence. Trends Parasitol 27:514-522.
38. Ye YH, Woolfit M, Rancès E, O'Neill SL, McGraw EA, 2013. Wolbachia-associated bacterial protection in the mosquito Aedes aegypti. PLoS Negl Trop Dis 7:e2362.
39. Kambris Z, Cook PE, Phuc HK, Sinkins SP, 2009. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326:134-136.
40. Bian G, Joshi D, Dong Y, Lu P, Zhou G, Pan X, Xu Y, Dimopoulos G, Xi Z, 2013. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340:748-751.
41. Newman CM, Cerutti F, Anderson TK, Hamer GL, Walker ED, Kitron UD, Ruiz MO, Brawn JD, Goldberg TL, 2011. Culex flavivirus and West Nile virus mosquito coinfection and positive ecological association in Chicago, United States. Vector Borne Zoonotic Dis 11:1099-1105.
42. Crockett RK, Burkhalter K, Mead D, Kelly R, Brown J, Varnado W, Roy A, Horiuchi K, Biggerstaff BJ, Miller B, Nasci R, 2012. Culex flavivirus and West Nile virus in Culex quinquefasciatus populations in the southeastern United States. J Med Entomol 49:165-174.
43. Kenney J, Solberg OD, Langevin SA, Brault AC, 2014. Characterization of a novel insect-specific flavivirus from Brazil: potential for inhibition of infection of arthropod cells with medically important flaviviruses. J Gen Virol. [Epub ahead of print 2014 Aug. 21], doi:10.1099/vir.0.068031-0.
44. Brackney DE, Scott JC, Sagawa F, Woodward JE, Miller NA, Schilkey FD, Mudge J, Wilusz J, Olson KE, Blair CD, Ebel GD, 2010. C6/36 Aedes albopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl Trop Dis 4:e856.
45. Kolodziejek J, Pachler K, Bin H, Mendelson E, Shulman L, Orshan L, Nowotny N, 2013. Barkedji virus, a novel mosquitoborne flavivirus identified in Culex perexiguus mosquitoes, Israel, 2011. J Gen Virol 94:2449-2457.
46. Zirkel F, Roth H, Kurth A, Drosten C, Ziebuhr J, Junglen S, 2013. Identification and characterization of genetically divergent members of the newly established family Mesoniviridae. J Virol 87:6346-6358.