Evolutionary and molecular analysis of the emergent severe fever with thrombocytopenia syndrome virus

Epidemics

Volumn 5, Issue 1, 2013, Pages 1-10

  Lam, Tommy Tsan Yuk ^a   Liu, Wei ^b   Bowden, Thomas A ^c   Cui, Ning ^d   Zhuang, Lu ^b   Liu, Kun ^b   Zhang, Yao Yun ^b   Cao, Wu Chun ^b   Pybus, Oliver G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d The 154 Hospital   (China)

Author keywords

Evolution; Nucleoprotein structure; Phlebovirus; Phylogenetic; Severe fever with thrombocytopenia syndrome; Tick borne disease

Indexed keywords

ARTICLE; BUNYAVIRUS; BUNYAVIRUS INFECTION; CHINA; CLINICAL FEATURE; FEVER; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; LEUKOPENIA; MOLECULAR CLOCK; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHLEBOVIRUS; PHYLOGENY; PRIORITY JOURNAL; RIFT VALLEY FEVER BUNYAVIRUS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SEVERE FEVER WITH THROMBOCYTOPENIA SYNDROME VIRUS; THROMBOCYTOPENIA; UNINDEXED SEQUENCE; VIROGENESIS; VIRUS ASSEMBLY; VIRUS NUCLEOCAPSID; VIRUS TRANSMISSION;

ANIMALS; BUNYAVIRIDAE INFECTIONS; CHINA; EVOLUTION, MOLECULAR; FEVER; GENOME, VIRAL; HUMANS; LEUKOPENIA; PHLEBOVIRUS; SEQUENCE ANALYSIS, DNA; SURVIVAL RATE; THROMBOCYTOPENIA;

EID: 84867434974     PISSN: 17554365     EISSN: 18780067     Source Type: Journal    
DOI: 10.1016/j.epidem.2012.09.002     Document Type: Article

References (78)

1. Bao C.J., Guo X.L., Qi X., Hu J.L., Zhou M.H., Varma J.K., Cui L.B., Yang H.T., Jiao Y.J., Klena J.D., Li L.X., Tao W.Y., Li X., Chen Y., Zhu Z., Xu K., Shen A.H., Wu T., Peng H.Y., Li Z.F., Shan J., Shi Z.Y., Wang H. A family cluster of infections by a newly recognized bunyavirus in eastern China, 2007: further evidence of person-to-person transmission. Clinical Infectious Diseases 2011, 53:1208-1214.
2. Beaty B.J., Bishop D.H. Bunyavirus-vector interactions. Virus Research 1988, 10:289-301.
3. Biek R., Henderson J.C., Waller L.A., Rupprecht C.E., Real L.A. A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7993-7998.
4. Bird B.H., Khristova M.L., Rollin P.E., Ksiazek T.G., Nichol S.T. Complete genome analysis of 33 ecologically and biologically diverse Rift Valley fever virus strains reveals widespread virus movement and low genetic diversity due to recent common ancestry. Journal of Virology 2007, 81:2805-2816.
5. Boni M.F., Posada D., Feldman M.W. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007, 176:1035-1047.
6. Bowden T.A., Crispin M., Graham S.C., Harvey D.J., Grimes J.M., Jones E.Y., Stuart D.I. Unusual molecular architecture of the machupo virus attachment glycoprotein. Journal of Virology 2009, 83:8259-8265.
7. Bowden T.A., Jones E.Y., Stuart D.I. Cells under siege: viral glycoprotein interactions at the cell surface. Journal of Structural Biology 2011, 175:120-126.
8. Bowen M.D., Trappier S.G., Sanchez A.J., Meyer R.F., Goldsmith C.S., Zaki S.R., Dunster L.M., Peters C.J., Ksiazek T.G., Nichol S.T. A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 2001, 291:185-190.
9. Bridgen A., Weber F., Fazakerley J.K., Elliott R.M. Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:664-669.
10. Carrington C.V., Foster J.E., Pybus O.G., Bennett S.N., Holmes E.C. Invasion and maintenance of dengue virus type 2 and type 4 in the Americas. Journal of Virology 2005, 79:14680-14687.
11. Chare E.R., Gould E.A., Holmes E.C. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. Journal of General Virology 2003, 84:2691-2703.
12. Chothia C., Lesk A.M. The relation between the divergence of sequence and structure in proteins. EMBO Journal 1986, 5:823-826.
13. Deyde V.M., Khristova M.L., Rollin P.E., Ksiazek T.G., Nichol S.T. Crimean-Congo hemorrhagic fever virus genomics and global diversity. Journal of Virology 2006, 80:8834-8842.
14. Drummond A.J., Ho S.Y., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biology 2006, 4:e88.
15. Drummond A.J., Nicholls G.K., Rodrigo A.G., Solomon W. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 2002, 161:1307-1320.
16. Drummond A.J., Rambaut A., Shapiro B., Pybus O.G. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 2005, 22:1185-1192.
17. Drummond A.J., Suchard M.A. Bayesian random local clocks, or one rate to rule them all. BMC Biology 2010, 8:114.
18. Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 2012, 29:1969-1973.
19. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113.
20. Elliott R.M. Bunyaviruses: General Features 2008, Elsevier Academic Press, Oxford. third ed.
21. Ferron F., Li Z., Danek E.I., Luo D., Wong Y., Coutard B., Lantez V., Charrel R., Canard B., Walz T., Lescar J. The hexamer structure of Rift Valley fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathogens 2011, 7:e1002030.
22. Froissart R., Roze D., Uzest M., Galibert L., Blanc S., Michalakis Y. Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLoS Biology 2005, 3:e89.
23. Frost S.D., Volz E.M. Viral phylodynamics and the search for an 'effective number of infections'. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2010, 365:1879-1890.
24. Gerrard S.R., Li L., Barrett A.D., Nichol S.T. Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. Journal of Virology 2004, 78:8922-8926.
25. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
26. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 2003, 52:696-704.
27. Huiskonen J.T., Overby A.K., Weber F., Grunewald K. Electron cryo-microscopy and single-particle averaging of Rift Valley fever virus: evidence for GN-GC glycoprotein heterodimers. Journal of Virology 2009, 83:3762-3769.
28. Kang K., Tang X.Y., Xu B.L., You A.G., Huang X.Y., Du Y.H., Wang H.F., Zhao G.H., Chen H.M., Liu G.H., Meng F.J. Analysis of the epidemic characteristics of fever and thrombocytopenia syndrome in Henan province, 2007-2011. Zhonghua Yu Fang Yi Xue Za Zhi 2012, 46:106-109.
29. Kijak G.H., McCutchan F.E. HIV diversity, molecular epidemiology, and the role of recombination. Current Infectious Disease Reports 2005, 7:480-488.
30. Klempa B., Stanko M., Labuda M., Ulrich R., Meisel H., Kruger D.H. Central European Dobrava Hantavirus isolate from a striped field mouse (Apodemus agrarius). Journal of Clinical Microbiology 2005, 43:2756-2763.
31. Kosakovsky Pond S.L., Frost S.D. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution 2005, 22:1208-1222.
32. Kosakovsky Pond S.L., Posada D., Gravenor M.B., Woelk C.H., Frost S.D. GARD: a genetic algorithm for recombination detection. Bioinformatics 2006, 22:3096-3098.
33. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. Journal of Molecular Biology 2007, 372:774-797.
34. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 2001, 305:567-580.
35. Lam T.T., Hon C.C., Lemey P., Pybus O.G., Shi M., Tun H.M., Li J., Jiang J., Holmes E.C., Leung F.C. Phylodynamics of H5N1 avian influenza virus in Indonesia. Molecular Ecology 2012, 21:3062-3077.
36. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
37. Liu Q., Liu J. Fever with thrombocytopenia syndrome virus infection in 17 clinical observation cases. Chinese Journal of Internal Medicine 2011, 50:785-786.
38. Liu Y., Li Q., Hu W., Wu J., Wang Y., Mei L., Walker D.H., Ren J., Yu X.J. Person-to-person transmission of severe fever with thrombocytopenia syndrome virus. Vector Borne and Zoonotic Diseases 2012, 12:156-160.
39. Lole K.S., Bollinger R.C., Paranjape R.S., Gadkari D., Kulkarni S.S., Novak N.G., Ingersoll R., Sheppard H.W., Ray S.C. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. Journal of Virology 1999, 73:152-160.
40. Lukashev A.N. Evidence for recombination in Crimean-Congo hemorrhagic fever virus. Journal of General Virology 2005, 86:2333-2338.
41. Martin D., Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000, 16:562-563.
42. Martin D.P., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010, 26:2462-2463.
43. McGuffin L.J., Bryson K., Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 2000, 16:404-405.
44. Medina R.A., Torres-Perez F., Galeno H., Navarrete M., Vial P.A., Palma R.E., Ferres M., Cook J.A., Hjelle B. Ecology, genetic diversity, and phylogeographic structure of andes virus in humans and rodents in Chile. Journal of Virology 2009, 83:2446-2459.
45. Ministry of Health, China, 2010. Announcement of the guidelines for preventing and controlling the severe fever with thrombocytopenia syndrome disease. Available at: http://www.moh.gov.cn/publicfiles/business/htmlfiles/wsb/pwsyw/201009/49245.htm.
46. Olsen C.W. The emergence of novel swine influenza viruses in North America. Virus Research 2002, 85:199-210.
47. Padidam M., Sawyer S., Fauquet C.M. Possible emergence of new geminiviruses by frequent recombination. Virology 1999, 265:218-225.
48. Palacios G., Tesh R., Travassos da Rosa A., Savji N., Sze W., Jain K., Serge R., Guzman H., Guevara C., Nunes M.R., Nunes-Neto J.P., Kochel T., Hutchison S., Vasconcelos P.F., Lipkin W.I. Characterization of the Candiru antigenic complex (Bunyaviridae: Phlebovirus), a highly diverse and reassorting group of viruses affecting humans in tropical America. Journal of Virology 2011, 85:3811-3820.
49. Parrish C.R., Holmes E.C., Morens D.M., Park E.C., Burke D.S., Calisher C.H., Laughlin C.A., Saif L.J., Daszak P. Cross-species virus transmission and the emergence of new epidemic diseases. Microbiology and Molecular Biology Reviews 2008, 72:457-470.
50. Pepin M., Bouloy M., Bird B.H., Kemp A., Paweska J. Rift Valley fever virus(Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Veterinary Research 2010, 41:61.
51. Perrone L.A., Narayanan K., Worthy M., Peters C.J. The S segment of Punta Toro virus (Bunyaviridae, Phlebovirus) is a major determinant of lethality in the Syrian hamster and codes for a type I interferon antagonist. Journal of Virology 2007, 81:884-892.
52. Pond S.L., Frost S.D., Muse S.V. HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21:676-679.
53. Posada D., Crandall K.A. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:13757-13762.
54. Pupko T., Pe'er I., Shamir R., Graur D. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Molecular Biology and Evolution 2000, 17:890-896.
55. Pybus O.G., Rambaut A. Evolutionary analysis of the dynamics of viral infectious disease. Nature Reviews Genetics 2009, 10:540-550.
56. Rambaut, A., Drummond, A.J., 2007. Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer.
57. Raymond D.D., Piper M.E., Gerrard S.R., Smith J.L. Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:11769-11774.
58. Rodriguez L.L., Owens J.H., Peters C.J., Nichol S.T. Genetic reassortment among viruses causing hantavirus pulmonary syndrome. Virology 1998, 242:99-106.
59. Sall A.A., Zanotto P.M., Sene O.K., Zeller H.G., Digoutte J.P., Thiongane Y., Bouloy M. Genetic reassortment of Rift Valley fever virus in nature. Journal of Virology 1999, 73:8196-8200.
60. Saluzzo J.F., Smith J.F. Use of reassortant viruses to map attenuating and temperature-sensitive mutations of the Rift Valley fever virus MP-12 vaccine. Vaccine 1990, 8:369-375.
61. Sherman M.B., Freiberg A.N., Holbrook M.R., Watowich S.J. Single-particle cryo-electron microscopy of Rift Valley fever virus. Virology 2009, 387:11-15.
62. Shimodaira H., Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 1999, 16:1114-1116.
63. Shope R.E., Rozhon E.J., Bishop D.H. Role of the middle-sized bunyavirus RNA segment in mouse virulence. Virology 1981, 114:273-276.
64. Sironen T., Vaheri A., Plyusnin A. Molecular evolution of Puumala hantavirus. Journal of Virology 2001, 75:11803-11810.
65. Smith J.M. Analyzing the mosaic structure of genes. Journal of Molecular Evolution 1992, 34:126-129.
66. Turell M.J., Saluzzo J.F., Tammariello R.F., Smith J.F. Generation and transmission of Rift Valley fever viral reassortants by the mosquito Culex pipiens. Journal of General Virology 1990, 71(Pt 10):2307-2312.
67. Vaney M.C., Rey F.A. Class II enveloped viruses. Cellular Microbiology 2011, 13:1451-1459.
68. Vialat P., Billecocq A., Kohl A., Bouloy M. The S segment of rift valley fever phlebovirus (Bunyaviridae) carries determinants for attenuation and virulence in mice. Journal of Virology 2000, 74:1538-1543.
69. Woelk C.H., Holmes E.C. Reduced positive selection in vector-borne RNA viruses. Molecular Biology and Evolution 2002, 19:2333-2336.
70. Worobey M., Holmes E.C. Evolutionary aspects of recombination in RNA viruses. Journal of General Virology 1999, 80(Pt 10):2535-2543.
71. Xu B., Liu L., Huang X., Ma H., Zhang Y., Du Y., Wang P., Tang X., Wang H., Kang K., Zhang S., Zhao G., Wu W., Yang Y., Chen H., Mu F., Chen W. Metagenomic analysis of fever, thrombocytopenia and leukopenia syndrome (FTLS) in Henan Province, China: discovery of a new bunyavirus. PLoS Pathogens 2011, 7:e1002369.
72. Yu B., Zhang Y., Peng J.-S., Zhou G.-Q., Luo T.-Y., Hu Q., He Y.-W., Wang W., Tian J.-H., Kong D.-G., Quan Y.-X., Dai Y.-A., Wang Q.-F., Liu X.-X., Li W., Li W. Epidemiological study on data involving 61 hospitalized cases with Huaiyangshan hemorrhagic fever in Wuhan, Hubei province. Chinese Journal of Epidemiology 2012, 33(1).
73. Yu X.J., Liang M.F., Zhang S.Y., Liu Y., Li J.D., Sun Y.L., Zhang L., Zhang Q.F., Popov V.L., Li C., Qu J., Li Q., Zhang Y.P., Hai R., Wu W., Wang Q., Zhan F.X., Wang X.J., Kan B., Wang S.W., Wan K.L., Jing H.Q., Lu J.X., Yin W.W., Zhou H., Guan X.H., Liu J.F., Bi Z.Q., Liu G.H., Ren J., Wang H., Zhao Z., Song J.D., He J.R., Wan T., Zhang J.S., Fu X.P., Sun L.N., Dong X.P., Feng Z.J., Yang W.Z., Hong T., Zhang Y., Walker D.H., Wang Y., Li D.X. Fever with thrombocytopenia associated with a novel bunyavirus in China. New England Journal of Medicine 2011, 364:1523-1532.
74. Zhang Y., Zhang H., Dong X., Yuan J., Yang X., Zhou P., Ge X., Li Y., Wang L.F., Shi Z. Hantavirus outbreak associated with laboratory rats in Yunnan, China. Infection, Genetics and Evolution 2010, 10:638-644.
75. Zhang Y.Z., He Y.W., Dai Y.A., Xiong Y., Zheng H., Zhou D.J., Li J., Sun Q., Luo X.L., Cheng Y.L., Qin X.C., Tian J.H., Chen X.P., Yu B., Jin D., Guo W.P., Li W., Wang W., Peng J.S., Zhang G.B., Zhang S., Chen X.M., Wang Y., Li M.H., Li Z., Lu S., Ye C., de Jong M.D., Xu J. Hemorrhagic fever caused by a novel Bunyavirus in China: pathogenesis and correlates of fatal outcome. Clinical Infectious Diseases 2012, 54:527-533.
76. Zhang Y.Z., Zhou D.J., Qin X.C., Tian J.H., Xiong Y., Wang J.B., Chen X.P., Gao D.Y., He Y.W., Jin D., Sun Q., Guo W.P., Wang W., Yu B., Li J., Dai Y.A., Li W., Peng J.S., Zhang G.B., Zhang S., Chen X.M., Wang Y., Li M.H., Lu X., Ye C., de Jong M.D., Xu J. The ecology, genetic diversity, and phylogeny of Huaiyangshan virus in China. Journal of Virology 2012, 86:2864-2868.
77. Zhang Y.Z., Zhou D.J., Xiong Y., Chen X.P., He Y.W., Sun Q., Yu B., Li J., Dai Y.A., Tian J.H., Qin X.C., Jin D., Cui Z., Luo X.L., Li W., Lu S., Wang W., Peng J.S., Guo W.P., Li M.H., Li Z.J., Zhang S., Chen C., Wang Y., de Jong M.D., Xu J. Hemorrhagic fever caused by a novel tick-borne Bunyavirus in Huaiyangshan, China. Zhonghua Liu Xing Bing Xue Za Zhi 2011, 32:209-220.
78. Zuo S.Q., Fang L.Q., Zhan L., Zhang P.H., Jiang J.F., Wang L.P., Ma J.Q., Wang B.C., Wang R.M., Wu X.M., Yang H., Cao Z.W., Cao W.C. Geo-spatial hotspots of hemorrhagic fever with renal syndrome and genetic characterization of Seoul variants in Beijing, China. PLoS Neglected Tropical Diseases 2011, 5:e945.