Phylogenetic patterns of human coxsackievirus B5 arise from population dynamics between two genogroups and reveal evolutionary factors of molecular adaptation and transmission

Journal of Virology

Volumn 87, Issue 22, 2013, Pages 12249-12259

  Henquell, Cécile ^a,b   Mirand, Audrey ^a,b   Richter, Jan ^c   Schuffenecker, Isabelle ^d   Böttiger, Blenda ^e   Diedrich, Sabine ^f   Terletskaia Ladwig, Elena ^g   Christodoulou, Christina ^c   Peigue Lafeuille, Hélène ^a,b   Bailly, Jean Luc ^a,b  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^c CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^d HOSPICES CIVILS DE LYON   (France)

^e LUND UNIVERSITY HOSPITAL   (Sweden)

^f ROBERT KOCH INSTITUTE   (Germany)

^g Gisela Enders and Kollegen MVZ GbR and Institute of Virology Infectious Diseases and Epidemiology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN VP1; CAPSID PROTEIN; VIRUS DNA;

AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLADISTICS; CONTROLLED STUDY; COXSACKIE VIRUS B; COXSACKIE VIRUS B5; EUROPE; GENE CLUSTER; GENE LOCUS; GENEALOGY; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION DYNAMICS; PRIORITY JOURNAL; VIRUS STRAIN; VIRUS TRANSMISSION; ADAPTATION; AMINO ACID SEQUENCE; BAYES THEOREM; CLASSIFICATION; ENTEROVIRUS; ENTEROVIRUS INFECTION; GENETIC SELECTION; GENETICS; HUMAN; MOLECULAR GENETICS; POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; VIROLOGY; VIRUS REPLICATION;

CERCOPITHECINE HERPESVIRUS 1; COXSACKIEVIRUS;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; BAYES THEOREM; CAPSID PROTEINS; DNA, VIRAL; ENTEROVIRUS B, HUMAN; ENTEROVIRUS INFECTIONS; EVOLUTION, MOLECULAR; GENETIC VARIATION; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; SELECTION, GENETIC; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; VIRUS REPLICATION;

EID: 84886262685     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02075-13     Document Type: Article

References (63)

1. Michos AG, Syriopoulou VP, Hadjichristodoulou C, Daikos GL, Lagona E, Douridas P, Mostrou G, Theodoridou M. 2007. Aseptic meningitis in children: analysis of 506 cases. PLoS One 2:e674. doi:10.1371/journal.pone.0000674.
2. Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF, Wang JR, Shi SR. 1999. An epidemic of enterovirus 71 infection in Taiwan. N. Engl. J. Med. 341:929-935.
3. Louie JK, Hacker JK, Gonzales R, Mark J, Maselli JH, Yagi S, Drew WL. 2005. Characterization of viral agents causing acute respiratory infection in a San Francisco University Medical Center clinic during the influenza season. Clin. Infect. Dis. 41:822-828.
4. Nathanson N. 2008. The pathogenesis of poliomyelitis: what we don't know. Adv. Virus Res. 71:1-50.
5. Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, Ji F, Wang XJ, Gao YJ, Chen L, An HQ, Li DX, Wang SW, Xu AQ, Wang ZJ, Xu WB. 2009. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J. Clin. Virol. 44:262-267.
6. Hogle JM, Chow M, Filman DJ. 1985. Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229:1358-1365.
7. Mateu MG. 1995. Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res. 38:1-24.
8. Duintjer Tebbens RJ, Pallansch MA, Chumakov KM, Halsey NA, Hovi T, Minor PD, Modlin JF, Patriarca PA, Sutter RW, Wright PF, Wassilak SG, Cochi SL, Kim JH, Thompson KM. 2013. Expert review on poliovirus immunity and transmission. Risk Anal. 33:544-605.
9. Stanway G, Brown P, Christian P, Hovi T, Hyypiä T, King NJ, Knowles NJ, Lemon SM, Minor PD, Pallansch MA, Palmemberg AC, Skern T. 2005. Family Picornaviridae, p 757-778. In Fauquet CM, Mayo MA, ManiloffJ, Desselberger U, Ball LA (ed), Virus taxonomy. Eighth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, UK.
10. Oberste MS, Maher K, Kennett ML, Campbell JJ, Carpenter MS, Schnurr D, Pallansch MA. 1999. Molecular epidemiology and genetic diversity of echovirus type 30 (E30): genotypes correlate with temporal dynamics of E30 isolation. J. Clin. Microbiol. 37:3928-3933.
11. Santti J, Harvala H, Kinnunnen L, Hyypia T. 2000. Molecular epidemiology and evolution of coxsackievirus A9. J. Gen. Virol. 81:1361-1372.
12. Podin Y, Gias EL, Ong F, Leong YW, Yee SF, Yusof MA, Perera D, Teo B, Wee TY, Yao SC, Yao SK, Kiyu A, Arif MT, Cardosa MJ. 2006. Sentinel surveillance for human enterovirus 71 in Sarawak, Malaysia: lessons from the first 7 years. BMC Public Health 6:180. doi:10.1186/1471-2458-6-180.
13. Khetsuriani N, Lamonte-Fowlkes A, Oberste S, Pallansch MA, Centers for Disease Control and Prevention. 2006. Enterovirus surveillance- United States, 1970-2005. MMWR Surveill. Summ.55(SS-08):1-20.
14. Antona D, Lévêque N, Chomel JJ, Dubrou S, Lévy-Bruhl D, Lina B. 2007. Surveillance of enteroviruses in France, 2000-2004. Eur. J. Clin. Microbiol. Infect. Dis. 26:403-412.
15. Tully DC, Fares MA. 2008. The tale of a modern animal plague: tracing the evolutionary history and determining the time-scale for foot and mouth disease virus. Virology 382:250-256.
16. Guan D, van der Sanden S, Zeng H, Li W, Zheng H, Ma C, Su J, Liu Z, Guo X, Zhang X, Liu L, Koopmans M, Ke C. 2012. Population dynamics and genetic diversity of C4 strains of human enterovirus 71 in Mainland China, 1998-2010. PLoS One 7:e44386. doi:10.1371/journal.pone.0044386.
17. Bailly JL, Mirand A, Henquell C, Archimbaud C, Chambon M, Charbonné F, Traoré O, Peigue-Lafeuille H. 2009. Phylogeography of circulating populations of human echovirus 30 over 50 years: nucleotide polymorphism and signature of purifying selection in the VP1 capsid protein gene. Infect. Genet. Evol. 9:699-708.
18. van der Sanden S, van der Avoort H, Lemey P, Uslu G, Koopmans M. 2010. Evolutionary trajectory of the VP1 gene of human enterovirus 71 genogroup B and C viruses. J. Gen. Virol. 91:1949-1958.
19. Bedford T, Cobey S, Beerli P, Pascual M. 2010. Global migration dynamics underlie evolution and persistence of human influenza A (H3N2). PLoS Pathog. 6:e1000918. doi:10.1371/journal.ppat.1000918.
20. Haydon DT, Bastos AD, Knowles NJ, Samuel AR. 2001. Evidence for positive selection in foot-and-mouth disease virus capsid genes from field isolates. Genetics 157:7-15.
21. Tee KK, Lam TTY, Chan YF, Bible JM, Kamarulzaman A, Tong CYW, Takebe Y, Pybus OG. 2010. Evolutionary genetics of human enterovirus 71: origin, population dynamics, natural selection and seasonal periodicity of the VP1 gene. J. Virol. 84:3339-3350.
22. Kistler AL, Webster DR, Rouskin S, Magrini V, Credle JJ, Schnurr DP, Boushey HA, Mardis ER, Li H, DeRisi JL. 2007. Genome-wide diversity and selective pressure in the human rhinovirus. Virol. J. 4:40. doi:10.1186/1743-422X-4-40.
23. Lewis-Rogers N, Bendall ML, Crandall KA. 2009. Phylogenetic relationships and molecular adaptation dynamics of human rhinoviruses. Mol. Biol. Evol. 26:969-981.
24. Tracy S, Gauntt C. 2008. Group B coxsackievirus virulence. Curr. Top. Microbiol. Immunol. 323:49-63.
25. Wikswo ME, Khetsuriani N, Fowlkes AL, Zheng X, Peñaranda S, Verma N, Shulman ST, Sircar K, Robinson CC, Schmidt T, Schnurr D, Oberste MS. 2009. Increased activity of coxsackievirus B1 strains associated with severe disease among young infants in the United States, 2007-2008. Clin. Infect. Dis. 49:e44-e51.
26. Roth B, Enders M, Arents A, Pfitzner A, Terletskaia-Ladwig E. 2007. Epidemiologic aspects and laboratory features of enterovirus infections in Western Germany, 2000-2005. J. Med. Virol. 79:956-962.
27. Trallero G, Avellon A, Otero A, De Miguel T, Pérez C, Rabella N, Rubio G, Echevarria JE, Cabrerizo M. 2010. Enteroviruses in Spain over the decade 1998-2007: virological and epidemiological studies. J. Clin. Virol. 47:170-176.
28. Han JF, Jiang T, Fan XL, Yang LM, Yu M, Cao RY, Wang JZ, Qin ED, Qin CF. 2012. Recombination of human coxsackievirus B5 in hand, foot, and mouth disease patients, China. Emerg. Infect. Dis. 18:351-353.
29. Rezig D, Fares W, Seghier M, Yahia AB, Touzi H, Triki H. 2011. Update on molecular characterization of coxsackievirus B5 strains. J. Med. Virol. 83:1247-1254.
30. Baek K, Yeo S, Lee B, Park K, Song J, Yu J, Rheem I, Kim J, Hwang S, Choi Y, Cheon D, Park J. 2011. Epidemics of enterovirus infection in Chungnam Korea, 2008 and 2009. Virol. J. 8:297. doi:10.1186/1743-422X-8-297.
31. Gullberg M, Tolf C, Jonsson N, Mulders MN, Savolainen-Kopra C, Hovi T, Van Ranst M, Lemey P, Hafenstein S, Lindberg AM. 2010. Characterization of a putative ancestor of coxsackievirus B5. J. Virol. 84: 9695-9708.
32. Bailly JL, Mirand A, Henquell C, Archimbaud C, Chambon M, Regagnon C, Charbonné F, Peigue-Lafeuille H. 2011. Repeated genomic transfers from echovirus 30 to echovirus 6 lineages indicate co-divergence between co-circulating populations of the two human enterovirus serotypes. Infect. Genet. Evol. 11:276-289.
33. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88. doi:10.1371/journal.pbio.0040088.
34. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214. doi:10.1186/1471-2148-7-214.
35. Suchard MA, Weiss RE, Sinsheimer JS. 2001. Bayesian selection of continuous-time Markov chain evolutionary models. Mol. Biol. Evol. 18: 1001-1013.
36. Shapiro B, Rambaut A, Drummond AJ. 2006. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol. Biol. Evol. 23:7-9.
37. Kass RE, Raftery AE. 1995. Bayes factors and model uncertainty. J. Am. Stat. Assoc. 90:773-795.
38. Minin VN, Bloomquist EW, Suchard MA. 2008. Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol. Biol. Evol. 25:1459-1471.
39. Stadler T, Kouyos R, von Wyl V, Yerly S, Böni J, Bürgisser P, Klimkait T, Joos B, Rieder P, Xie D, Günthard HF, Drummond AJ, Bonhoeffer S, Swiss HIV Cohort Study. 2012. Estimating the basic reproductive number from viral sequence data. Mol. Biol. Evol. 29:347-357.
40. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV. 2012. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol. Biol. Evol. 29:2157-2167.
41. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22:1185-1192.
42. Kosakovsky Pond SL, Frost SD. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22:1208-1222.
43. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K. 2013. FUBAR: A Fast, Unconstrained Bayesian AppRoximation for inferring selection. Mol. Biol. Evol. 30:1196-1202.
44. Pupko T, Pe'er I, Shamir R, Graur D. 2000. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol. Biol. Evol. 17: 890-896.
45. Yang Z, Kumar S, Nei M. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641-1650.
46. Nielsen R. 2002. Mapping mutations on phylogenies. Syst. Biol. 51:729-739.
47. Koelle K, Cobey S, Grenfell B, Pascual M. 2006. Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science 314:1898-1903.
48. Kosakovsky Pond SL, Murrell B, Fourment M, Frost SD, Delport W, Scheffler K. 2011. A random effects branch-site model for detecting episodic diversifying selection. Mol. Biol. Evol. 28:3033-3043.
49. Brown F, Talbot P, Burrows R. 1973. Antigenic differences between isolates of swine vesicular disease virus and their relationships to coxsackie B5 virus. Nature 245:315-316.
50. Borrego B, Carra E, García-Ranea JA, Brocchi E. 2002. Characterization of neutralization sites on the circulating variant of swine vesicular disease virus (SVDV): a new site is shared by SVDV and the related coxsackie B5 virus. J. Gen. Virol. 83:35-44.
51. Borrego B, García-Ranea JA, Douglas A, Brocchi E. 2002. Mapping of linear epitopes on the capsid proteins of swine vesicular disease virus using monoclonal antibodies. J. Gen. Virol. 83:1387-1395.
52. Verdaguer N, Jimenez-Clavero MA, Fita I, Ley V. 2003. Structure of swine vesicular disease virus: mapping of changes occurring during adaptation of human coxsackie B5 virus to infect swine. J. Virol. 77:9780-9789.
53. Fry EE, Knowles NJ, Newman JW, Wilsden G, Rao Z, King AM, Stuart DI. 2003. Crystal structure of swine vesicular disease virus and implications for host adaptation. J. Virol. 77:5475-5486.
54. Muckelbauer JK, Kremer M, Minor I, Diana G, Dutko FJ, Groarke J, Pevear DC, Rossmann MG. 1995. The structure of coxsackievirus B3 at 3.5 Å resolution. Structure 3:653-667.
55. Ferguson NM, Galvani AP, Bush RM. 2003. Ecological and immunological determinants of influenza evolution. Nature 422:428-433.
56. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science 305:371-376.
57. Woolhouse ME. 2002. Population biology of emerging and re-emerging pathogens. Trends Microbiol. 10:S3-S7.
58. Allicock OM, Lemey P, Tatem AJ, Pybus OG, Bennett SN, Mueller BA, Suchard MA, Foster JE, Rambaut A, Carrington CV. 2012. Phylogeography and population dynamics of dengue viruses in the Americas. Mol. Biol. Evol. 29:1533-1543.
59. Grenfell BT, Pybus OG, Gog JR, Wood JL, Daly JM, Mumford JA, Holmes EC. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-332.
60. Pybus OG, Rambaut A. 2009. Evolutionary analysis of the dynamics of viral infectious disease. Nat. Rev. Genet. 10:540-550.
61. Chambon M, Archimbaud C, Bailly JL, Henquell C, Regagnon C, Charbonné F, Peigue-Lafeuille H. 2001. Circulation of enteroviruses and persistence of meningitis cases in the winter of 1999-2000. J. Med. Virol. 65:340-347.
62. Kamo M, Sasaki A. 2002. The effect of cross-immunity and seasonal forcing in a multi-strain epidemic model. Physica D 165:228-241.
63. Pybus OG, Rambaut A, Belshaw R, Freckleton RP, Drummond AJ, Holmes EC. 2007. Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. Mol. Biol. Evol. 24: 845-852.