Genomic and structural features of the yellow fever virus from the 2016-2017 Brazilian outbreak

Journal of General Virology

Volumn 99, Issue 4, 2018, Pages 536-548

  Gómez, Mariela Martínez ^a   de Abreu, Filipe Vieira Santos ^a,b   Dos Santos, Alexandre Araujo Cunha ^a   de Mello, Iasmim Silva ^a   Santos, Marta Pereira ^a   Ribeiro, Ieda Pereira ^a   Ferreira de Brito, Anielly ^a   de Miranda, Rafaella Moraes ^a   de Castro, Marcia Gonçalves ^a   Ribeiro, Mario Sergio ^c   da Costa Laterrière, Roberto ^d   Aguiar, Shirlei Ferreira ^e   Meira, Guilherme Louzada Silva ^e   Antunes, Deborah ^a   Torres, Pedro Henrique Monteiro ^a   Mir, Daiana ^a   Vicente, Ana Carolina Paulo ^a   Guimarães, Ana Carolina Ramos ^a   Caffarena, Ernesto Raul ^a   Bello, Gonzalo ^a   Lourenço de Oliveira, Ricardo ^a   Bonaldo, Myrna Cristina ^a   more..

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b Science and Technology of Minas Gerais   (Brazil)

^c Secretaria Estadual de Saúde   (Brazil)

^d Centro de Referências Para Imunobiológicos Especiais CRIE da Secretaria de Saúde Do Estado Do Espírito Santo   (Brazil)

^e Laboratório Central de Saúde Pública Noel Nutels LACEN RJ   (Brazil)

Author keywords

2016 2017 Brazilian outbreak; Amino acid changes; Evolution; Genetic diversity; Yellow fever virus

Indexed keywords

AMINO ACID; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5; VIRAL PROTEIN;

ALOUATTA; AMINO ACID SUBSTITUTION; ARTICLE; BRAZIL; CALLITRICHINAE; DISEASE SEVERITY; EPIDEMIC; GENETIC POLYMORPHISM; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HUMAN; MOLECULAR EVOLUTION; MOSQUITO; NONHUMAN; PHYLOGEOGRAPHY; PRIMATE; PRIORITY JOURNAL; RIO DE JANEIRO (STATE); SOUTH AMERICA; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS STRAIN; YELLOW FEVER; YELLOW FEVER VIRUS; CHEMISTRY; CLASSIFICATION; GENETICS; GENOMICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR MODEL; PHYLOGENY; VIROLOGY;

BRAZIL; DISEASE OUTBREAKS; GENOME, VIRAL; GENOMICS; GENOTYPE; HUMANS; MODELS, MOLECULAR; PHYLOGENY; VIRAL PROTEINS; YELLOW FEVER; YELLOW FEVER VIRUS;

EID: 85045098514     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.001033     Document Type: Article

References (71)

1. Barnett ED. Yellow fever: epidemiology and prevention. Clin Infect Dis 2007;44:850-856.
2. Monath TP, Vasconcelos PF. Yellow fever. J Clin Virol 2015;64: 160-173.
3. Weaver SC, Reisen WK. Present and future arboviral threats. Antiviral Res 2010;85:328-345.
4. Vasconcelos PF, Monath TP. Yellow Fever remains a potential threat to public health. Vector Borne Zoonotic Dis 2016;16:566-567.
5. Bryant JE, Holmes EC, Barrett AD. Out of Africa: a molecular perspective on the introduction of yellow fever virus into the Americas. PLoS Pathog 2007;3:e75.
6. Mutebi JP, Wang H, Li L, Bryant JE, Barrett AD. Phylogenetic and evolutionary relationships among yellow fever virus isolates in Africa. J Virol 2001;75:6999-7008.
7. Staples JE, Monath TP. Yellow fever: 100 years of discovery. JAMA 2008;300:960-962.
8. Nunes MR, Palacios G, Cardoso JF, Martins LC, Sousa EC et al. Genomic and phylogenetic characterization of Brazilian yellow fever virus strains. J Virol 2012;86:13263-13271.
9. Vasconcelos PF, Bryant JE, da Rosa TP, Tesh RB, Rodrigues SG et al. Genetic divergence and dispersal of yellow fever virus, Brazil. Emerg Infect Dis 2004;10:1578-1584.
10. Romano AP, Costa ZG, Ramos DG, Andrade MA, Jayme VS et al. Yellow fever outbreaks in unvaccinated populations, Brazil, 2008-2009. PLoS Negl Trop Dis 2014;8:e2740.
11. de Souza RP, Foster PG, Sallum MA, Coimbra TL, Maeda AY et al. Detection of a new yellow fever virus lineage within the South American genotype I in Brazil. J Med Virol 2010;82:175-185.
12. Mir D, Delatorre E, Bonaldo M, Lourenço-de-Oliveira R, Vicente AC et al. Phylodynamics of yellow fever virus in the Americas: new insights into the origin of the 2017 Brazilian outbreak. Sci Rep 2017;7: 7385.
13. Health BMo. 2017. Emergência epidemiológica de febre amarela no Brasil, no período de dezembro de 2016 a julho de 2017. http://portalarquivos.saude.gov.br/images/pdf/2017/setembro/06/2017_027.pdf [accessed 2017].
14. Pan American Health Organization. 2017. Epidemiological update -yellow fever. www.paho.org/hq/index.php?option=com_docman&-task=doc_view&Itemid=270&gid=40841g=en [accessed].
15. Bonaldo MC, Gómez MM, dos Santos AA, Abreu FVS, Ferreira-de-Brito A et al. Genome analysis of yellow fever virus of the ongoing outbreak in Brazil reveals polymorphisms. Mem Inst Oswaldo Cruz 2017;112:447-451.
16. Beasley DW, McAuley AJ, Bente DA. Yellow fever virus: genetic and phenotypic diversity and implications for detection, prevention and therapy. Antiviral Res 2015;115:48-70.
17. Carrington CV, Auguste AJ. Evolutionary and ecological factors underlying the tempo and distribution of yellow fever virus activity. Infect Genet Evol 2013;13:198-210.
18. Couto-Lima D, Madec Y, Bersot MI, Campos SS, Motta MA et al. Potential risk of re-emergence of urban transmission of yellow fever virus in Brazil facilitated by competent Aedes populations. Sci Rep 2017;7:4848.
19. Dorigatti I, Hamlet A, Aguas R, Cattarino L, Cori A et al. International risk of yellow fever spread from the ongoing outbreak in Brazil, December 2016 to May 2017. Euro Surveill 2017;22:30572.
20. Carpp LN, Galler R, Bonaldo MC. Interaction between the yellow fever virus nonstructural protein NS3 and the host protein Alix contributes to the release of infectious particles. Microbes Infect 2011; 13:85-95.
21. Patkar CG, Kuhn RJ. Yellow Fever virus NS3 plays an essential role in virus assembly independent of its known enzymatic functions. J Virol 2008;82:3342-3352.
22. Teramoto T, Balasubramanian A, Choi KH, Padmanabhan R. Serotype-specific interactions among functional domains of dengue virus 2 nonstructural proteins (NS) 5 and NS3 are crucial for viral RNA replication. J Biol Chem 2017;292:9465-9479.
23. Le Breton M, Meyniel-Schicklin L, Deloire A, Coutard B, Canard B et al. Flavivirus NS3 and NS5 proteins interaction network: a highthroughput yeast two-hybrid screen. BMC Microbiol 2011;11:234.
24. Wu RH, Tsai MH, Tsai KN, Tian JN, Wu JS et al. Mutagenesis of dengue virus protein NS2A revealed a novel domain responsible for virus-induced cytopathic effect and interactions between NS2A and NS2B transmembrane segments. J Virol 2017;91:e01836-16.
25. Zou J, Lee L, Wang QY, Xie X, Lu S et al. Mapping the Interactions between the NS4B and NS3 proteins of dengue virus. J Virol 2015; 89:3471-3483.
26. Cumberworth SL, Clark JJ, Kohl A, Donald CL. Inhibition of type I interferon induction and signalling by mosquito-borne flaviviruses. Cell Microbiol 2017;19:e12737.
27. Mathew A, Townsley E, Ennis FA. Elucidating the role of T cells in protection against and pathogenesis of dengue virus infections. Future Microbiol 2014;9:411-425.
28. Schlesinger JJ, Foltzer M, Chapman S. The Fc portion of antibody to yellow fever virus NS1 is a determinant of protection against YF encephalitis in mice. Virology 1993;192:132-141.
29. Coffey LL, Forrester N, Tsetsarkin K, Vasilakis N, Weaver SC. Factors shaping the adaptive landscape for arboviruses: implications for the emergence of disease. Future Microbiol 2013;8:155-176.
30. Tsetsarkin KA, Chen R, Leal G, Forrester N, Higgs S et al. Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes. Proc Natl Acad Sci USA 2011;108:7872-7877.
31. Lim SP, Koh JH, Seh CC, Liew CW, Davidson AD et al. A crystal structure of the dengue virus non-structural protein 5 (NS5) polymerase delineates interdomain amino acid residues that enhance its thermostability and de novo initiation activities. J Biol Chem 2013;288:31105-31114.
32. Zhao Y, Soh TS, Zheng J, Chan KW, Phoo WW et al. A crystal structure of the dengue virus NS5 protein reveals a novel interdomain interface essential for protein flexibility and virus replication. PLoS Pathog 2015;11:e1004682.
33. Causey OR, Kumm HW, Laemmert HW. Dispersion of forest mosquitoes in Brazil; further studies. Am J Trop Med Hyg 1950;30: 301-312.
34. Jung L, Mourthe I, Grelle CE, Strier KB, Boubli JP. Effects of local habitat variation on the behavioral ecology of two sympatric groups of brown howler monkey (Alouatta clamitans). PLoS One 2015;10: e0129789.
35. Fioravanti C. O alarme dos macacos. Revista Pesquisa Fapesp 2018.
36. Consoli R, Oliveira RL. Principais Mosquitos de Importância Sanitária no Brasil. Rio de Janeiro: Editora FIOCRUZ; 1994.
37. Ferreira-de-Brito A, Ribeiro IP, Miranda RM, Fernandes RS, Campos SS et al. First detection of natural infection of Aedes aegypti with Zika virus in Brazil and throughout South America. Mem Inst Oswaldo Cruz 2016;111:655-658.
38. Luo D, Vasudevan SG, Lescar J. The flavivirus NS2B-NS3 protease-helicase as a target for antiviral drug development. Antiviral Res 2015;118:148-158.
39. Wu J, Bera AK, Kuhn RJ, Smith JL. Structure of the Flavivirus helicase: implications for catalytic activity, protein interactions, and proteolytic processing. J Virol 2005;79:10268-10277.
40. Phoo WW, Li Y, Zhang Z, Lee MY, Loh YR et al. Structure of the NS2B-NS3 protease from Zika virus after self-cleavage. Nat Commun 2016;7:13410.
41. Lu G, Gong P. Crystal structure of the full-length Japanese encephalitis virus NS5 reveals a conserved methyltransferasepolymerase interface. PLoS Pathog 2013;9:e1003549.
42. di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A et al. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 2011;39:W13-W17.
43. Webb B, Sali A. Protein structure modeling with MODELLER. In: Kihara D (editor). Protein Structure Prediction (Methods in Molecular Biology). New York: Springer; 2014. pp. 1-15.
44. Abraham MJ, Murtola T, Schulz R, Pall S, Smith JC et al. GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 2015;1-2:19-25.
45. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL et al. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 2010;78:1950-1958.
46. Benkert P, Künzli M, Schwede T. QMEAN server for protein model quality estimation. Nucleic Acids Res 2009;37:W510-W514.
47. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 2001;98:10037-10041.
48. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 2004;32:W665-W667.
49. Bond CS, Schüttelkopf AW. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr D Biol Crystallogr 2009;65:510-512.
50. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406-425.
51. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980;16:111-120.
52. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985;39:783-791.
53. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 2015;1:vev003.
54. Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000;16:562-563.
55. Padidam M, Sawyer S, Fauquet CM. Possible emergence of newgeminiviruses by frequent recombination. Virology 1999;265:218-225.
56. Smith JM. Analyzing the mosaic structure of genes. J Mol Evol 1992;34:126-129.
57. Posada D, Crandall KA. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 2001;98:13757-13762.
58. Martin DP, Posada D, Crandall KA, Williamson C. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 2005;21:98-102.
59. Gibbs MJ, Armstrong JS, Gibbs AJ. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000;16:573-582.
60. Boni MF, Posada D, Feldman MW. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007;176:1035-1047.
61. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007;7:214.
62. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012;29: 1969-1973.
63. Suchard MA, Rambaut A. Many-core algorithms for statistical phylogenetics. Bioinformatics 2009;25:1370-1376.
64. Lemey P, Rambaut A, Welch JJ, Suchard MA. Phylogeography takes a relaxed random walk in continuous space and time. Mol Biol Evol 2010;27:1877-1885.
65. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA et al. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 2012;29:2157-2167.
66. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol 2006;4:e88.
67. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 2005;22:1185-1192.
68. Rambaut A, Suchard M, Drummond A. 2013. Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer/.
69. Rambaut A. 2014. FigTree v1.4. http://tree.bio.ed.ac.uk/software/figtree/.
70. IBGE BIoGaS. MAPAS. 2017.
71. Environment BMot. Monitoramento de biomas. 2017.