Increased replicative fitness of a dengue virus 2 clade in native mosquitoes: Potential contribution to a clade replacement event in Nicaragua

Journal of Virology

Volumn 88, Issue 22, 2014, Pages 13125-13134

  Quiner, Claire A ^a   Parameswaran, Poornima ^a   Ciota, Alexander T ^b   Ehrbar, Dylan J ^b   Dodson, Brittany L ^b   Schlesinger, Sondra ^a   Kramer, Laura D ^b,c   Harris, Eva ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WADSWORTH CENTER   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEDES AEGYPTI; ARTICLE; CLADISTICS; CONTROLLED STUDY; DENGUE VIRUS 1; DENGUE VIRUS 2; GROWTH RATE; IN VITRO STUDY; MIXED INFECTION; MOLECULAR DYNAMICS; NICARAGUA; NONHUMAN; SALIVARY GLAND; VIROGENESIS; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS REPLICATION; AEDES; ANIMAL; CELL CULTURE; CHILD; DENGUE VIRUS; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; MALE; PHYSIOLOGY; VIROLOGY;

AEDES; ANIMALS; CELLS, CULTURED; CHILD; DENGUE VIRUS; FEMALE; HUMANS; MALE; NICARAGUA; VIRUS REPLICATION;

EID: 84908373535     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01822-14     Document Type: Article

References (52)

1. Gould EA, Higgs S. 2009. Impact of climate change and other factors on emerging arbovirus diseases. Trans. R. Soc. Trop. Med. Hyg. 103:109-121. http://dx.doi.org/10.1016/j.trstmh.2008.07.025.
2. Kyle JL, Harris E. 2008. Global spread and persistence of dengue. Annu. Rev. Microbiol. 62:71-92. http://dx.doi.org/10.1146/annurev.micro.62.081307.163005.
3. 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 GR, Simmons CP, Scott TW, Farrar JJ, Hay SI. 2013. The global distribution and burden of dengue. Nature 496:504-507. http://dx.doi.org/10.1038/nature12060.
4. World Health Organization. 1997. Dengue haemorrhagic fever: diagnosis, treatment, prevention and control, 2nd ed. World Health Organization Press, Geneva, Switzerland.
5. World Health Organization. 2009. Dengue guidelines for diagnosis, treatment, prevention and control. New edition. World Health Organization Press, Geneva, Switzerland.
6. OhAinle M, Balmaseda A, Macalalad AR, Tellez Y, Zody MC, Saborio S, Nunez A, Lennon NJ, Birren BW, Gordon A, Henn MR, Harris E. 2011. Dynamics of dengue disease severity determined by the interplay between viral genetics and serotype-specific immunity. Sci. Transl. Med. 3:114ra128. http://dx.doi.org/10.1126/scitranslmed.3003084.
7. Burke DS, Nisalak A, Johnson DE, Scott RM. 1988. A prospective study of dengue infections in Bangkok. Am. J. Trop. Med. Hyg. 38:172-180.
8. Graham RR, Juffrie M, Tan R, Hayes CG, Laksono I, Ma'roef C, Erlin, Sutaryo, Porter KR, Halstead SB. 1999. A prospective seroepidemiologic study on dengue in children four to nine years of age in Yogyakarta, Indonesia. I. Studies in 1995-1996. Am. J. Trop. Med. Hyg. 61:412-419.
9. Guzman MG, Alvarez M, Rodriguez-Roche R, Bernardo L, Montes T, Vazquez S, Morier L, Alvarez A, Gould EA, Kouri G, Halstead SB. 2007. Neutralizing antibodies after infection with dengue 1 virus. Emerg. Infect. Dis. 13:282-286. http://dx.doi.org/10.3201/eid1302.060539.
10. Guzman MG, Kouri G, Valdes L, Bravo J, Vazquez S, Halstead SB. 2002. Enhanced severity of secondary dengue-2 infections: death rates in 1981 and 1997 Cuban outbreaks. Rev. Panam. Salud Publica 11:223-227. http://dx.doi.org/10.1590/S1020-49892002000400003.
11. Thein S, Aung MM, Shwe TN, Aye M, Zaw A, Aye K, Aye KM, Aaskov J. 1997. Risk factors in dengue shock syndrome. Am. J. Trop. Med. Hyg. 56:566-572.
12. Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N, Chairunsri A, Sawasdivorn S, Duangchinda T, Dong T, Rowland-Jones S, Yenchitsomanus PT, McMichael A, Malasit P, Screaton G. 2003. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat. Med. 9:921-927. http://dx.doi.org/10.1038/nm887.
13. Rothman AL. 2011. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11:532-543. http://dx.doi.org/10.1038/nri3014.
14. Halstead SB. 2003. Neutralization and antibody-dependent enhancement of dengue viruses. Adv. Virus Res. 60:421-467. http://dx.doi.org/10.1016/S0065-3527(03)60011-4.
15. Ciota AT, Kramer LD. 2010. Insights into arbovirus evolution and adaptation from experimental studies. Viruses 2:2594-2617. http://dx.doi.org/10.3390/v2122594.
16. Eigen M. 1996. On the nature of virus quasispecies. Trends Microbiol. 4:216-218. http://dx.doi.org/10.1016/0966-842X(96)20011-3.
17. Farci P, Strazzera R, Alter HJ, Farci S, Degioannis D, Coiana A, Peddis G, Usai F, Serra G, Chessa L, Diaz G, Balestrieri A, Purcell RH. 2002. Early changes in hepatitis C viral quasispecies during interferon therapy predict the therapeutic outcome. Proc. Natl. Acad. Sci. U. S. A. 99:3081-3086. http://dx.doi.org/10.1073/pnas.052712599.
18. Joos B, Trkola A, Fischer M, Kuster H, Rusert P, Leemann C, Boni J, Oxenius A, Price DA, Phillips RE, Wong JK, Hirschel B, Weber R, Gunthard HF. 2005. Low human immunodeficiency virus envelope diversity correlates with low in vitro replication capacity and predicts spontaneous control of plasma viremia after treatment interruptions. J. Virol. 79:9026-9037. http://dx.doi.org/10.1128/JVI.79.14.9026-9037.2005.
19. Sullivan DG, Bruden D, Deubner H, McArdle S, Chung M, Christensen C, Hennessy T, Homan C, Williams J, McMahon BJ, Gretch DR. 2007. Hepatitis C virus dynamics during natural infection are associated with long-term histological outcome of chronic hepatitis C disease. J. Infect. Dis. 196:239-248. http://dx.doi.org/10.1086/518895.
20. Parameswaran P, Charlebois P, Tellez Y, Nunez A, Ryan EM, Malboeuf CM, Levin JZ, Lennon NJ, Balmaseda A, Harris E, Henn MR. 2012. Genome-wide patterns of intrahuman dengue virus diversity reveal associations with viral phylogenetic clade and interhost diversity. J. Virol. 86: 8546-8558. http://dx.doi.org/10.1128/JVI.00736-12.
21. Jerzak G, Bernard KA, Kramer LD, Ebel GD. 2005. Genetic variation in West Nile virus from naturally infected mosquitoes and birds suggests quasispecies structure and strong purifying selection. J. Gen. Virol. 86: 2175-2183. http://dx.doi.org/10.1099/vir.0.81015-0.
22. Lin SR, Hsieh SC, Yueh YY, Lin TH, Chao DY, Chen WJ, King CC, Wang WK. 2004. Study of sequence variation of dengue type 3 virus in naturally infected mosquitoes and human hosts: implications for transmission and evolution. J. Virol. 78:12717-12721. http://dx.doi.org/10.1128/JVI.78.22.12717-12721.2004.
23. Thai KT, Henn MR, Zody MC, Tricou V, Nguyet NM, Charlebois P, Lennon NJ, Green L, de Vries PJ, Hien TT, Farrar J, van Doorn HR, de Jong MD, Birren BW, Holmes EC, Simmons CP. 2012. High-resolution analysis of intrahost genetic diversity in dengue virus serotype 1 infection identifies mixed infections. J. Virol. 86:835-843. http://dx.doi.org/10.1128/JVI.05985-11.
24. Tjaden NB, Thomas SM, Fischer D, Beierkuhnlein C. 2013. Extrinsic incubation period of dengue: knowledge, backlog, and applications of temperature dependence. PLoS Negl. Trop. Dis. 7:e2207. http://dx.doi.org/10.1371/journal.pntd.0002207.
25. Davis CT, Ebel GD, Lanciotti RS, Brault AC, Guzman H, Siirin M, Lambert A, Parsons RE, Beasley DW, Novak RJ, Elizondo-Quiroga D, Green EN, Young DS, Stark LM, Drebot MA, Artsob H, Tesh RB, Kramer LD, Barrett AD. 2005. Phylogenetic analysis of North American West Nile virus isolates, 2001-2004: evidence for the emergence of a dominant genotype. Virology 342:252-265. http://dx.doi.org/10.1016/j.virol.2005.07.022.
26. Ebel GD, Carricaburu J, Young D, Bernard KA, Kramer LD. 2004. Genetic and phenotypic variation of West Nile virus in New York, 2000-2003. Am. J. Trop. Med. Hyg. 71:493-500.
27. Schuh AJ, Ward MJ, Leigh Brown AJ, Barrett AD. 2014. Dynamics of the emergence and establishment of a newly dominant genotype of Japanese encephalitis virus throughout Asia. J. Virol. 88:4522-4532. http://dx.doi.org/10.1128/JVI.02686-13.
28. Harris E, Roberts TG, Smith L, Selle J, Kramer LD, Valle S, Sandoval E, Balmaseda A. 1998. Typing of dengue viruses in clinical specimens and mosquitoes by single-tube multiplex reverse transcriptase PCR. J. Clin. Microbiol. 36:2634-2639.
29. Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV. 1992. Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J. Clin. Microbiol. 30:545-551.
30. Balmaseda A, Sandoval E, Perez L, Gutierrez CM, Harris E. 1999. Application of molecular typing techniques in the 1998 dengue epidemic in Nicaragua. Am. J. Trop. Med. Hyg. 61:893-897.
31. Ciota AT, Lovelace AO, Jia Y, Davis LJ, Young DS, Kramer LD. 2008. Characterization of mosquito-adapted West Nile virus. J. Gen. Virol. 89: 1633-1642. http://dx.doi.org/10.1099/vir.0.2008/000893-0.
32. Hall GS, Little DP. 2007. Relative quantitation of virus population size in mixed genotype infections using sequencing chromatograms. J. Virol. Methods 146:22-28. http://dx.doi.org/10.1016/j.jviromet.2007.05.029.
33. Ciota AT, Payne AF, Ngo KA, Kramer LD. 2014. Consequences of in vitro host shift for St. Louis encephalitis virus. J. Gen. Virol. 95:1281-1288. http://dx.doi.org/10.1099/vir.0.063545-0.
34. Holland JJ, de la Torre JC, Clarke DK, Duarte E. 1991. Quantitation of relative fitness and great adaptability of clonal populations ofRNAviruses. J. Virol. 65:2960-2967.
35. Novella IS, Ball LA, Wertz GW. 2004. Fitness analyses of vesicular stomatitis strains with rearranged genomes reveal replicative disadvantages. J. Virol. 78:9837-9841. http://dx.doi.org/10.1128/JVI.78.18.9837-9841.2004.
36. Diamond MS, Zachariah M, Harris E. 2002. Mycophenolic acid inhibits dengue virus infection by preventing replication of viral RNA. Virology 304:211-221. http://dx.doi.org/10.1006/viro.2002.1685.
37. Martinez MA, Carrillo C, Gonzalez-Candelas F, Moya A, Domingo E, Sobrino F. 1991. Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecies. J. Virol. 65:3954-3957.
38. Hardy JL, Houk EJ, Kramer LD, Reeves WC. 1983. Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu. Rev. Entomol. 28:229-262. http://dx.doi.org/10.1146/annurev.en.28.010183.001305.
39. Lambrechts L, Fansiri T, Pongsiri A, Thaisomboonsuk B, Klungthong C, Richardson JH, Ponlawat A, Jarman RG, Scott TW. 2012. Dengue-1 virus clade replacement in Thailand associated with enhanced mosquito transmission. J. Virol. 86:1853-1861. http://dx.doi.org/10.1128/JVI.06458-11.
40. Cologna R, Rico-Hesse R. 2003. American genotype structures decrease dengue virus output from human monocytes and dendritic cells. J. Virol. 77:3929-3938. http://dx.doi.org/10.1128/JVI.77.7.3929-3938.2003.
41. Pryor MJ, Carr JM, Hocking H, Davidson AD, Li P, Wright PJ. 2001. Replication of dengue virus type 2 in human monocyte-derived macrophages: comparisons of isolates and recombinant viruses with substitutions at amino acid 390 in the envelope glycoprotein. Am. J. Trop. Med. Hyg. 65:427-434.
42. Edgil D, Diamond MS, Holden KL, Paranjape SM, Harris E. 2003. Translation efficiency determines differences in cellular infection among dengue virus type 2 strains. Virology 317:275-290. http://dx.doi.org/10.1016/j.virol.2003.08.012.
43. Schnettler E, Sterken MG, Leung JY, Metz SW, Geertsema C, Goldbach RW, Vlak JM, Kohl A, Khromykh AA, Pijlman GP. 2012. Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and mammalian cells. J. Virol. 86:13486-13500. http://dx.doi.org/10.1128/JVI.01104-12.
44. Schuessler A, Funk A, Lazear HM, Cooper DA, Torres S, Daffis S, Jha BK, Kumagai Y, Takeuchi O, Hertzog P, Silverman R, Akira S, Barton DJ, Diamond MS, Khromykh AA. 2012. West Nile virus noncoding subgenomic RNA contributes to viral evasion of the type I interferonmediated antiviral response. J. Virol. 86:5708-5718. http://dx.doi.org/10.1128/JVI.00207-12.
45. Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S, van der Aa L, Liu WJ, Palmenberg AC, Shi PY, Hall RA, Khromykh AA. 2008. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4:579-591. http://dx.doi.org/10.1016/j.chom.2008.10.007.
46. Holmes EC, Twiddy SS. 2003. The origin, emergence and evolutionary genetics of dengue virus. Infect. Genet. Evol. 3:19-28. http://dx.doi.org/10.1016/S1567-1348(03)00004-2.
47. Rico-Hesse R, Harrison LM, Salas RA, Tovar D, Nisalak A, Ramos C, Boshell J, de Mesa MT, Nogueira RM, da Rosa AT. 1997. Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 230:244-251. http://dx.doi.org/10.1006/viro.1997.8504.
48. Kanakaratne N, Wahala WM, Messer WB, Tissera HA, Shahani A, Abeysinghe N, de-Silva AM, Gunasekera M. 2009. Severe dengue epi-demics in Sri Lanka, 2003-2006. Emerg. Infect. Dis. 15:192-199. http://dx.doi.org/10.3201/eid1502.080926.
49. Messer WB, Gubler DJ, Harris E, Sivananthan K, de Silva AM. 2003. Emergence and global spread of a dengue serotype 3, subtype III virus. Emerg. Infect. Dis. 9:800-809. http://dx.doi.org/10.3201/eid0907.030038.
50. 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, liveattenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380:1559-1567. http://dx.doi.org/10.1016/S0140-6736(12)61428-7.
51. Ciota AT, Kramer LD. 2013. Vector-virus interactions and transmission dynamics of West Nile virus. Viruses 5:3021-3047. http://dx.doi.org/10.3390/v5123021.
52. Macdonald G. 1957. The epidemiology and control of malaria. Oxford University PressLondon, United Kingdom.