Native Wolbachia from Aedes albopictus blocks chikungunya virus infection in cellulo

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Raquin, Vincent ^a,b   Moro, Claire Valiente ^a   Saucereau, Yoann ^a   Tran, Florence Hélène ^a   Potier, Patrick ^a   Mavingui, Patrick ^a  

^a UNIVERSITÉ LYON 1   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

AEDES ALBOPICTUS; ANIMAL CELL; ARTICLE; CELL STRUCTURE; CHIKUNGUNYA; CHIKUNGUNYA ALPHAVIRUS; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; INSECT CELL; NONHUMAN; ORGANISMAL INTERACTION; PHENOTYPE; RNA REPLICATION; SALIVARY GLAND; SIGNAL TRANSDUCTION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS LOAD; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; WOLBACHIA; AEDES; ANIMAL; CHIKUNGUNYA VIRUS; GENETICS; HUMAN; MICROBIOLOGY; PATHOGENICITY; SYMBIOSIS; TRANSMISSION; VIROLOGY;

AEDES ALBOPICTUS; ARBOVIRUS; ARTHROPODA; BACTERIA (MICROORGANISMS); CHIKUNGUNYA VIRUS; DENGUE VIRUS; WOLBACHIA;

AEDES; ANIMALS; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; HUMANS; SYMBIOSIS; VIRUS REPLICATION; WOLBACHIA;

EID: 84928741900     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125066     Document Type: Article

References (73)

1. WHO | About vector-borne diseases. In: WHO [Internet]. Available: http://www.who.int/campaigns/ world-health-day/2014/vector-borne-diseases/en/
2. Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 2007; 3: e201. doi: 10.1371/journal.ppat. 0030201 PMID: 18069894
3. Tsetsarkin KA, Weaver SC. Sequential adaptive mutations enhance efficient vector switching by Chikungunya virus and its epidemic emergence. PLoS Pathog. 2011; 7: e1002412. doi: 10.1371/journal. ppat.1002412 PMID: 22174678
4. De Lamballerie X, Leroy E, Charrel RN, Ttsetsarkin K, Higgs S, Gould EA. Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come? Virol J. 2008; 5: 33. doi: 10.1186/1743-422X-5-33 PMID: 18304328
5. Angelini R, Finarelli AC, Angelini P, Po C, Petropulacos K, Silvi G, et al. Chikungunya in north-eastern Italy: a summing up of the outbreak. Euro Surveill Bull Eur Sur Mal Transm Eur Commun Dis Bull. 2007; 12: E071122.2.
6. La Ruche G, Souarès Y, Armengaud A, Peloux-Petiot F, Delaunay P, Desprès P, et al. First two autochthonous dengue virus infections in metropolitan France, September 2010. Euro Surveill Bull Eur Sur Mal Transm Eur Commun Dis Bull. 2010; 15: 19676.
7. Leparc-Goffart I, Nougairede A, Cassadou S, Prat C, de Lamballerie X. Chikungunya in the Americas. Lancet. 2014; 383: 514. doi: 10.1016/S0140-6736(14)60185-9 PMID: 24506907
8. WHO | Chikungunya-France. In: WHO [Internet]. Available: http://www.who.int/csr/don/23-october-2014-chikungunya/en/
9. Bonizzoni M, Gasperi G, Chen X, James AA. The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol. 2013; 29: 460-468. doi: 10.1016/j.pt.2013.07.003 PMID: 23916878
10. Benedict MQ, Levine RS, Hawley WA, Lounibos LP. Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis Larchmt N. 2007; 7: 76-85. doi: 10.1089/vbz. 2006.0562 PMID: 17417960
11. David J-P, Coissac E, Melodelima C, Poupardin R, Riaz MA, Chandor-Proust A, et al. Transcriptome response to pollutants and insecticides in the dengue vector Aedes aegypti using next-generation sequencing technology. BMC Genomics. 2010; 11: 216. doi: 10.1186/1471-2164-11-216 PMID: 20356352
12. Christodoulou M. Biological vector control of mosquito-borne diseases. Lancet Infect Dis. 2011; 11: 84-85. PMID: 21351390
13. Slatko BE, Luck AN, Dobson SL, Foster JM. Wolbachia endosymbionts and human disease control. Mol Biochem Parasitol. 2014; 195: 88-95. doi: 10.1016/j.molbiopara.2014.07.004 PMID: 25046729
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: 748-751. doi: 10.1126/science.1236192 PMID: 23661760
15. 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 Negl Trop Dis. 2014; 8:e2688. doi: 10.1371/journal.pntd.0002688 PMID: 24587459
16. 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: e38544. doi: 10.1371/journal.pone.0038544 PMID: 22685581
17. Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol. 2008; 6: 741-751. doi: 10.1038/nrmicro1969 PMID: 18794912
18. Bian G, Xu Y, Lu P, Xie Y, Xi Z. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog. 2010; 6: e1000833. doi: 10.1371/journal.ppat.1000833 PMID: 20368968
19. 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: 1268-1278. doi: 10.1016/j.cell.2009.11.042 PMID: 20064373
20. Van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K, Day A, et al. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis. 2012; 6: e1892. doi: 10.1371/journal.pntd.0001892 PMID: 23133693
21. Hussain M, Lu G, Torres S, Edmonds JH, Kay BH, Khromykh AA, et al. Effect of Wolbachia on replication of West Nile virus in a mosquito cell line and adult mosquitoes. J Virol. 2013; 87: 851-858. doi: 10.1128/JVI.01837-12 PMID: 23115298
22. Zélé F, Nicot A, Berthomieu A, Weill M, Duron O, Rivero A. Wolbachia increases susceptibility to Plasmodium infection in a natural system. Proc Biol Sci. 2014; 281: 20132837. doi: 10.1098/rspb.2013. 2837 PMID: 24500167
23. Zouache K, Voronin D, Tran-Van V, Mousson L, Failloux A-B, Mavingui P. Persistent Wolbachia and cultivable bacteria infection in the reproductive and somatic tissues of the mosquito vector Aedes albopictus. PloS One. 2009; 4: e6388. doi: 10.1371/journal.pone.0006388 PMID: 19633721
24. Zouache K, Raharimalala FN, Raquin V, Tran-Van V, Raveloson LHR, Ravelonandro P, et al. Bacterial diversity of field-caught mosquitoes, Aedes albopictus and Aedes aegypti, from different geographic regions of Madagascar. FEMS Microbiol Ecol. 2011; 75: 377-389. doi: 10.1111/j.1574-6941.2010.01012.x PMID: 21175696
25. Mousson L, Zouache K, Arias-Goeta C, Raquin V, Mavingui P, Failloux A-B. The Native Wolbachia Symbionts Limit Transmission of Dengue Virus in Aedes albopictus. PLoS Negl Trop Dis. 2012; 6: e1989. doi: 10.1371/journal.pntd.0001989 PMID: 23301109
26. Mousson L, Martin E, Zouache K, Madec Y, Mavingui P, Failloux AB. Wolbachia modulates Chikungunya replication in Aedes albopictus. Mol Ecol. 2010; 19: 1953-1964. doi: 10.1111/j.1365-294X.2010. 04606.x PMID: 20345686
27. Caragata EP, Rancès E, Hedges LM, Gofton AW, Johnson KN, O' Neill SL, et al. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog. 2013; 9: e1003459. doi: 10.1371/journal. ppat.1003459 PMID: 23825950
28. Caragata EP, Rancès E, O'Neill SL, McGraw EA. Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol. 2014; 67: 205-218. doi: 10.1007/s00248-013-0339-4 PMID: 24337107
29. Voronin D, Cook DAN, Steven A, Taylor MJ. Autophagy regulates Wolbachia populations across diverse symbiotic associations. Proc Natl Acad Sci U S A. 2012; 109: E1638-1646. doi: 10.1073/pnas. 1203519109 PMID: 22645363
30. Brennan LJ, Keddie BA, Braig HR, Harris HL. The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PloS One. 2008; 3: e2083. doi: 10.1371/journal.pone.0002083 PMID: 18461124
31. Hussain M, Frentiu FD, Moreira LA, O'Neill SL, Asgari S. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc Natl Acad Sci U S A. 2011; 108: 9250-9255. doi: 10.1073/pnas.1105469108 PMID: 21576469
32. Rancès E, Ye YH, Woolfit M, McGraw EA, O'Neill SL. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog. 2012; 8: e1002548. doi: 10.1371/journal.ppat.1002548 PMID: 22383881
33. Hussain M, O'Neill SL, Asgari S. Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs. RNA Biol. 2013; 10: 1868-1875. doi: 10.4161/rna.27392 PMID: 24351659
34. Hughes GL, Ren X, Ramirez JL, Sakamoto JM, Bailey JA, Jedlicka AE, et al. Wolbachia infections in Anopheles gambiae cells: transcriptomic characterization of a novel host-symbiont interaction. PLoS Pathog. 2011; 7: e1001296. doi: 10.1371/journal.ppat.1001296 PMID: 21379333
35. Frentiu FD, Robinson J, Young PR, McGraw EA, O'Neill SL. Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PloS One. 2010; 5: e13398. doi: 10.1371/journal.pone. 0013398 PMID: 20976219
36. O 'Neill SL, Pettigrew MM, Sinkins SP, Braig HR, Andreadis TG, Tesh RB. In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Mol Biol. 1997; 6: 33-39. PMID: 9013253
37. Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney M-C, et al. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 2006; 3: e263. doi: 10.1371/journal.pmed.0030263 PMID: 16700631
38. Dubrulle M, Mousson L, Moutailler S, Vazeille M, Failloux A-B. Chikungunya virus and Aedes mosquitoes: saliva is infectious as soon as two days after oral infection. PloS One. 2009; 4: e5895. doi: 10. 1371/journal.pone.0005895 PMID: 19521520
39. Payne AF, Binduga-Gajewska I, Kauffman EB, Kramer LD. Quantitation of flaviviruses by fluorescent focus assay. J Virol Methods. 2006; 134: 183-189. doi: 10.1016/j.jviromet.2006.01.003 PMID: 16510196
40. Venard CM-P, Crain PR, Dobson SL. SYTO11 staining vs FISH staining: a comparison of two methods to stain Wolbachia pipientis in cell cultures. Lett Appl Microbiol. 2011; 52: 168-176. doi: 10.1111/j.1472-765X.2010.02986.x PMID: 21214605
41. Fenollar F, La Scola B, Inokuma H, Dumler JS, Taylor MJ, Raoult D. Culture and phenotypic characterization of a Wolbachia pipientis isolate. J Clin Microbiol. 2003; 41: 5434-5441. PMID: 14662922
42. Voronin D, Tran-Van V, Potier P, Mavingui P. Transinfection and growth discrepancy of Drosophila Wolbachia strain wMel in cell lines of the mosquito Aedes albopictus. J Appl Microbiol. 2010; 108: 2133-2141. doi: 10.1111/j.1365-2672.2009.04621.x PMID: 19951376
43. Raquin V, Wannagat M, Zouache K, Legras-Lachuer C, Moro CV, Mavingui P. Detection of dengue group viruses by fluorescence in situ hybridization. Parasit Vectors. 2012; 5: 243. doi: 10.1186/1756-3305-5-243 PMID: 23110979
44. Bonilauri P, Bellini R, Calzolari M, Angelini R, Venturi L, Fallacara F, et al. Chikungunya virus in Aedes albopictus, Italy. Emerg Infect Dis. 2008; 14: 852-854.: doi: 10.3201/eid1405.071144 PMID: 18439383
45. Tsetsarkin KA, Chen R, Yun R, Rossi SL, Plante KS, Guerbois M, et al. Multi-peaked adaptive landscape for chikungunya virus evolution predicts continued fitness optimization in Aedes albopictus mosquitoes. Nat Commun. 2014; 5: 4084. doi: 10.1038/ncomms5084 PMID: 24933611
46. Delatte H, Paupy C, Dehecq JS, Thiria J, Failloux AB, Fontenille D. [Aedes albopictus, vector of chikungunya and dengue viruses in Reunion Island: biology and control]. Parasite Paris Fr. 2008; 15: 3-13.
47. Ponlawat A, Scott JG, Harrington LC. Insecticide susceptibility of Aedes aegypti and Aedes albopictus across Thailand. J Med Entomol. 2005; 42: 821-825. PMID: 16363166
48. Blagrove MSC, Arias-Goeta C, Di Genua C, Failloux A-B, Sinkins SP. A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits Chikungunya virus. PLoS Negl Trop Dis. 2013; 7: e2152. doi: 10.1371/journal.pntd.0002152 PMID: 23556030
49. Blagrove MSC, Arias-Goeta C, Failloux A-B, Sinkins SP. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proc Natl Acad Sci U S A. 2012; 109: 255-260. doi: 10.1073/pnas.1112021108 PMID: 22123944
50. Lu P, Bian G, Pan X, Xi Z. Wolbachia Induces Density-Dependent Inhibition to Dengue Virus in Mosquito Cells. PLoS Negl Trop Dis. 2012; 6: e1754. doi: 10.1371/journal.pntd.0001754 PMID: 22848774
51. McMeniman CJ, Lane AM, Fong AWC, Voronin DA, Iturbe-Ormaetxe I, Yamada R, et al. Host adaptation of a Wolbachia strain after long-term serial passage in mosquito cell lines. Appl Environ Microbiol. 2008; 74: 6963-6969. doi: 10.1128/AEM.01038-08 PMID: 18836024
52. Fallon AM, Witthuhn BA. Proteasome activity in a naïve mosquito cell line infected with Wolbachia pipientis wAlbB. In Vitro Cell Dev Biol Anim. 2009; 45: 460-466. doi: 10.1007/s11626-009-9193-6 PMID: 19296184
53. Fallon AM, Baldridge GD, Higgins LA, Witthuhn BA. Wolbachia from the planthopper Laodelphax striatellus establishes a robust, persistent, streptomycin-resistant infection in clonal mosquito cells. In Vitro Cell Dev Biol Anim. 2013; 49: 66-73. doi: 10.1007/s11626-012-9571-3 PMID: 23271364
54. Khoo CCH, Venard CMP, Fu Y, Mercer DR, Dobson SL. Infection, growth and maintenance of Wolbachia pipientis in clonal and non-clonal Aedes albopictus cell cultures. Bull Entomol Res. 2013; 103: 251-260. doi: 10.1017/S0007485312000648 PMID: 23113940
55. Salazar MI, Richardson JH, Sánchez-Vargas I, Olson KE, Beaty BJ. Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol. 2007; 7: 9. doi: 10.1186/1471-2180-7-9 PMID: 17263893
56. 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. Appl Environ Microbiol. 2012; 78: 6922-6929. doi: 10.1128/AEM.01727-12 PMID: 22843518
57. Kingsolver MB, Huang Z, Hardy RW. Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol. 2013; 425: 4921-4936. doi: 10.1016/j.jmb.2013.10.006 PMID: 24120681
58. Brackney DE, Scott JC, Sagawa F, Woodward JE, Miller NA, Schilkey FD, et al. C6/36 Aedes albopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl Trop Dis. 2010; 4: e856.: doi: 10.1371/journal.pntd.0000856 PMID: 21049065
59. Zhang G, Hussain M, O'Neill SL, Asgari S. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proc Natl Acad Sci U S A. 2013; 110: 10276-10281. doi: 10.1073/pnas.1303603110 PMID: 23733960
60. Zhang G, Hussain M, Asgari S. Regulation of arginine methyltransferase 3 by a Wolbachia-induced microRNA in Aedes aegypti and its effect on Wolbachia and dengue virus replication. Insect Biochem Mol Biol. 2014; 53: 81-88. doi: 10.1016/j.ibmb.2014.08.003 PMID: 25158106
61. Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B, Vavre F. Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog. 2009; 5: e1000630. doi: 10.1371/journal.ppat. 1000630 PMID: 19851452
62. Schaible UE, Kaufmann SHE. Iron and microbial infection. Nat Rev Microbiol. 2004; 2: 946-953. doi:10.1038/nrmicro1046 PMID: 15550940
63. Krejbich-Trotot P, Gay B, Li-Pat-Yuen G, Hoarau J-J, Jaffar-Bandjee M-C, Briant L, et al. Chikungunya triggers an autophagic process which promotes viral replication. Virol J. 2011; 8: 432. doi: 10.1186/1743-422X-8-432 PMID: 21902836
64. Baldridge GD, Baldridge AS, Witthuhn BA, Higgins L, Markowski TW, Fallon AM. Proteomic profiling of a robust Wolbachia infection in an Aedes albopictus mosquito cell line. Mol Microbiol. 2014; 94: 537-556. doi: 10.1111/mmi.12768 PMID: 25155417
65. Darby AC, Christina Gill A, Armstrong SD, Hartley CS, Xia D, Wastling JM, et al. Integrated transcriptomic and proteomic analysis of the global response of Wolbachia to doxycycline-induced stress. ISME J. 2014; 8: 925-937. doi: 10.1038/ismej.2013.192 PMID: 24152719
66. Kambris Z, Blagborough AM, Pinto SB, Blagrove MSC, Godfray HCJ, Sinden RE, et al. Wolbachia stimulates immune gene expression and inhibits Plasmodium development in Anopheles gambiae. PLoS Pathog. 2010; 6: e1001143. doi: 10.1371/journal.ppat.1001143 PMID: 20949079
67. Ramirez JL, Short SM, Bahia AC, Saraiva RG, Dong Y, Kang S, et al. Chromobacterium Csp-P Reduces Malaria and Dengue Infection in Vector Mosquitoes and Has Entomopathogenic and In Vitro Anti-pathogen Activities. PLoS Pathog. 2014; 10: e1004398. doi: 10.1371/journal.ppat.1004398 PMID: 25340821
68. Fansiri T, Fontaine A, Diancourt L, Caro V, Thaisomboonsuk B, Richardson JH, et al. Genetic mapping of specific interactions between Aedes aegypti mosquitoes and dengue viruses. PLoS Genet. 2013; 9: e1003621. doi: 10.1371/journal.pgen.1003621 PMID: 23935524
69. Richards SL, Anderson SL, Lord CC, Tabachnick WJ. Effects of virus dose and extrinsic incubation temperature on vector competence of Culex nigripalpus (Diptera: Culicidae) for St. Louis encephalitis virus. J Med Entomol. 2012; 49: 1502-1506. PMID: 23270182
70. Carrington LB, Seifert SN, Armijos MV, Lambrechts L, Scott TW. Reduction of Aedes aegypti vector competence for dengue virus under large temperature fluctuations. Am J Trop Med Hyg. 2013; 88: 689-697. doi: 10.4269/ajtmh.12-0488 PMID: 23438766
71. Jupatanakul N, Sim S, Dimopoulos G. The Insect Microbiome Modulates Vector Competence for Arboviruses. Viruses. 2014; 6: 4294-4313. doi: 10.3390/v6114294 PMID: 25393895
72. Murdock CC, Blanford S, Hughes GL, Rasgon JL, Thomas MB. Temperature alters Plasmodium blocking by Wolbachia. Sci Rep. 2014; 4: 3932. doi: 10.1038/srep03932 PMID: 24488176
73. Hughes GL, Dodson BL, Johnson RM, Murdock CC, Tsujimoto H, Suzuki Y, et al. Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes. Proc Natl Acad Sci U S A. 2014; 111: 12498-12503. doi: 10.1073/pnas.1408888111 PMID: 25114252