Repeated genomic transfers from echovirus 30 to echovirus 6 lineages indicate co-divergence between co-circulating populations of the two human enterovirus serotypes

Infection, Genetics and Evolution

Volumn 11, Issue 2, 2011, Pages 276-289

  Bailly, J L ^a   Mirand, A ^a,b   Henquell, C ^b   Archimbaud, C ^a,b   Chambon, M ^a,b   Regagnon, C ^b   Charbonne F ^a,b   Peigue Lafeuille, H ^a,b  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

Aseptic meningitis; Bayesian inference; Evolutionary history; Genetic recombination; Picornavirus

Indexed keywords

PROTEIN VP1; VIRUS PROTEIN;

ARTICLE; CLADISTICS; CONTROLLED STUDY; ECHO VIRUS; ECHO VIRUS 30; ENTEROVIRUS INFECTION; EVOLUTION; FRANCE; GENE REARRANGEMENT; GENETIC RECOMBINATION; LAST COMMON ANCESTOR; MICROBIAL POPULATION DYNAMICS; MOLECULAR CLOCK; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEROTYPE; VIRUS GENOME; VIRUS MENINGITIS; VIRUS STRAIN;

BASE SEQUENCE; BAYES THEOREM; CAPSID PROTEINS; ECHOVIRUS 6, HUMAN; ECHOVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; EVOLUTION, MOLECULAR; FRANCE; GENE TRANSFER, HORIZONTAL; GENOME, VIRAL; GENOTYPE; HUMANS; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PHYLOGENY; POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SEROTYPING;

ECHOVIRUS; ENTEROVIRUS; HUMAN ECHOVIRUS 30; HUMAN ECHOVIRUS 6; MIRIDAE; PICORNAVIRIDAE;

EID: 79951943109     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2010.06.019     Document Type: Article

References (84)

1. Adu F., Iber J., Bukbuk D., Gumede N., Yang S.J., Jorba J., Campagnoli R., Sule W.F., Yang C.F., Burns C., Pallansch M., Harry T., Kew O. Isolation of recombinant type 2 vaccine-derived poliovirus (VDPV) from a Nigerian child. Virus Res. 2007, 127:17-25.
2. Agol V.I. Recombination and other rearrangements in picornaviruses. Semin. Virol. 1997, 8:77-84.
3. Akaike H. A new look at the statistical model identification. IEEE Transact. Automat. Control 1974, 19:716-723.
4. Antona D., Lévêque N., Chomel J.J., Dubrou S., Lévy-Bruhl D., Lina B. Surveillance of enteroviruses in France, 2000-2004. Eur. J. Clin. Microbiol. Infect. Dis. 2007, 26:403-412.
5. Awadala P. The evolutionary genomics of pathogen recombination. Nature Rev. Genet. 2003, 4:50-60.
6. Bailly J.L., Mirand A., Henquell C., Archimbaud C., Chambon M., Charbonné F., Traoré O., Peigue-Lafeuille H. 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. 2009, 9:699-708.
7. Bingjun T., Yoshida H., Yan W., Lin L., Tsuji T., Shimizu H., Miyamura T. Molecular typing and epidemiology of non-polio enteroviruses isolated from Yunnan Province, the People's Republic of China. J. Med. Virol. 2008, 80:670-679.
8. Bouslama L., Nasri D., Chollet L., Belguith K., Bourlet T., Aouni M., Pozetto B., Pillet S. Natural recombination event within the capsid genomic region leading to a chimeric strain of human enterovirus B. J. Virol. 2007, 81:8944-8952.
9. Brown B., Oberste M.S., Maher K., Pallansch M.A. Complete genomic sequencing shows that poliovirus and members of human enteroviruses species C are closely related in the noncapsid region. J. Virol. 2003, 77:8973-8984.
10. Cabrerizo M., Echevarria J.E., González I., de Miguel T., Trallero G. Molecular epidemiological study of HEV-B enteroviruses involved in the increase in meningitis cases occurred in Spain during 2006. J. Med. Virol. 2008, 80:1018-1024.
11. Chambon M., Archimbaud C., Bailly J.L., Henquell C., Regagnon C., Charbonné F., Peigue-Lafeuille H. Circulation of enteroviruses and persistence of meningitis cases in the winter of 1999-2000. J. Med. Virol. 2001, 65:340-347.
12. Chomel J.J., Antona D., Thouvenot D., Lina B. Three echovirus serotypes responsible for outbreak of aseptic meningitis in Rhone-Alpes region France. Eur. J. Clin. Microbiol. Infect. Dis. 2003, 22:191-193.
13. Chan Y.F., AbuBakar S. Recombinant human enterovirus 71 in hand, foot and mouth disease patients. Emerg. Infect. Dis. 2004, 10:1468-1470.
14. Chen G.W., Huang J.H., Lo Y.L., Tsao K.C., Chang S.C. Mosaic genome structure of echovirus 30 that circulated in Taiwan in 2001. Arch. Virol. 2007, 152:1807-1817.
15. Chevaliez S., Szendroi A., Caro V., Balanant J., Guillot S., Berencsi G., Delpeyroux F. Molecular comparison of echovirus 11 strains circulating in Europe during an epidemic of multisystem hemorrhagic disease of infants indicates that evolution generally occurs by recombination. Virology 2004, 325:56-70.
16. Drummond A.J., Rambaut A., Shapiro B., Pybus O.G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 2005, 22:1185-1192.
17. Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006, 4(5):e88. 10.1371/journal.pbio.0040088.
18. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214. 10.1186/1471-2148-7-214.
19. Gibbs M.J., Armstrong J.S., Gibbs A.J. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000, 16:573-582.
20. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999, 41:95-98.
21. Heath L., van der Walt E., Varsani A., Martin D.P. Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J. Virol. 2006, 80:11827-11832.
22. Heled J., Drummond A.J. Bayesian inference of population size history from multiple loci. BMC Evol. Biol. 2008, 23:829.
23. Heled J., Drummond A.J. Bayesian inference of species trees from multilocus data. Mol. Biol. Evol. 2010, 27:570-580.
24. Higgins D., Lemey P. Multiple sequence alignment. The Phylogenetic Handbook 2009, 68-108. Cambridge University Press, Cambridge, United Kingdom. second ed. P. Lemey, M. Salemi, A.M. Vandamme (Eds.).
25. Jegouic S., Joffret M.L., Blanchard C., Riquet F.B., Perret C., Pelletier I., Colbere-Garapin F., Rakoto-Andrianavelo M., Delpeyroux F. Recombination between polioviruses and co-circulating coxsackie A viruses: role in the emergence of pathogenic vaccine-derived polioviruses. PLoS Pathog. 2009, 5:e1000412.
26. Kapusinszky B., Szomor K.N., Farkas A., Takács M., Berencsi G. Detection of non-polio enteroviruses in Hungary 2000-2008 and molecular epidemiology of enterovirus 71, coxsackievirus A16, and echovirus 30. Virus Genes 2010, 40:163-173.
27. Kass R.E., Raftery A.E. Bayes factors and model uncertainty. J. Am. Stat. Assoc. 1995, 90:773-795.
28. Kew O., Morris-Glasgow V., Landaverde M., Burns C., Shaw J., Garib Z., André J., Blackman E., Freeman C.J., Jorba J., Sutter R., Tambini G., Venczel L., Pedreira C., Laender F., Shimizu H., Yoneyama T., Miyamura T., van Der Avoort H., Oberste M.S., Kilpatrick D., Cochi S., Pallansch M., de Quadros C. Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 2002, 296:356-359.
29. Khetsuriani N., Lamonte A., Oberste M.S., Pallansch M. Neonatal enterovirus infections reported to the national enterovirus surveillance system in the United States, 1983-2003. Pediatr. Infect. Dis. J. 2006, 25:889-893.
30. Ledinko N. Genetic recombination with poliovirus type 1Studies of crosses between a normal horse serum-resistant mutant and several guanidine-resistant mutants of the same strain. Virology 1963, 20:107-119.
31. Lemey P., Pybus O.G., Rambaut A., Drummond A.J., Robertson D.L., Roques P., Worobey M., Vandamme A.M. The molecular population genetics of HIV-1 group O. Genetics 2004, 167:1059-1068.
32. Lemey P., Posada D. Introduction to recombination. The Phylogenetic Handbook 2009, 493-518. Cambridge University Press, United Kingdom. second ed. P. Lemey, M. Salemi, A.M. Vandamme (Eds.).
33. Lindberg A.M., Andersson P., Savolainen C., Mulders M.N., Hovi T. Evolution of the genome of Human enterovirus B: incongruence between phylogenies of the VP1 and 3CD regions indicates frequent recombination within the species. J. Gen. Virol. 2003, 84:1223-1235.
34. 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. J. Virol. 1999, 73:152-160.
35. Lukashev A.N., Lashkevich V.A., Ivanova O.E., Koroleva G.A., Hinkkanen A.E., Ilonen J. Recombination in circulating enteroviruses. J. Virol. 2003, 77:10423-10431.
36. Lukashev A.N., Lashkevich V.A., Koroleva G.A., Ilonen J., Hinkkanen A.E. Recombination in uveitis-causing enterovirus strains. J. Gen. Virol. 2004, 85:463-470.
37. Lukashev A.N., Lashkevich V.A., Ivanova O.E., Koroleva G.A., Hinkkanen A.E., Ilonen J. Recombination in circulating human enterovirus B: independent evolution of structural and non structural genome regions. J. Gen. Virol. 2005, 86:3281-3290.
38. Mao N., Zhao L., Zhu Z., Chen X., Zhou S., Zhang Y., Cui A., Ji Y., Xu S., Xu W. An aseptic meningitis outbreak caused by echovirus 6 in Anhui Province China. J. Med. Virol. 2010, 82:441-445.
39. Martin D., Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000, 16:562-563.
40. Martin D.P., Posada D., Crandall K.A., Williamson C. A modified BOOTSCAN algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res. Hum. Retroviruses 2005, 21:98-102.
41. Maynard Smith J. Analyzing the mosaic structure of genes. J. Mol. Evol. 1992, 34:126-129.
42. McWilliam Leitch E.C., Bendig J., Cabrerizo M., Cardosa J., Hyypiä T., Ivanova O.E., Kelly A., Kroes A.C., Lukashev A., MacAdam A., McMinn P., Roivainen M., Trallero G., Evans D.J., Simmonds P. Transmission networks and population turnover of echovirus 30. J. Virol. 2009, 83:2109-2118.
43. Mirand A., Archimbaud C., Henquell C., Michel Y., Chambon M., Peigue-Lafeuille H., Bailly J.L. Prospective identification of HEV-B enteroviruses during the 2005 outbreak. J. Med. Virol. 2006, 78:1624-1634.
44. Mirand A., Henquell C., Archimbaud C., Peigue-Lafeuille H., Bailly J.L. Emergence of recent echovirus 30 lineages is marked by serial genetic recombination events. J. Gen. Virol. 2007, 88:166-176.
45. Mirand A., Henquell C., Archimbaud C., Chambon M., Charbonné F., Peigue-Lafeuille H., Bailly J.L. Prospective identification of enteroviruses involved in meningitis in 2006 through direct genotyping in cerebrospinal fluid. J. Clin. Microbiol. 2008, 46:87-96.
46. Mirand A., Schuffenecker I., Henquell C., Billaud G., Jugie G., Falcon D., Mahul A., Archimbaud C., Terletskaia-Ladwig E., Diedrich S., Huemer H.P., Enders M., Lina B., Peigue-Lafeuille H., Bailly J.-L. Phylogenetic evidence for a recent dissemination of two populations of human enterovirus 71 in European countries. J. Gen. Virol. 2010, 10.1099/vir.0.021741-0.
47. Oberste M.S., Maher K., Kennett M.L., Campbell J.J., Carpenter M.S., Schnurr D., Pallansch M.A. Molecular epidemiology and genetic diversity of echovirus type 30 (E30): genotypes correlate with temporal dynamics of E30 isolation. J. Clin. Microbiol. 1999, 37:3928-3933.
48. Oberste M.S., Maher K., Kilpatrick D.R., Pallansch M.A. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol. 1999, 73:1941-1948.
49. Oberste M.S., Maher K., Pallansch M.A. Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J. Virol. 2004, 78:855-867.
50. Oberste M.S., Penaranda S., Pallansch M.A. RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J. Virol. 2004, 78:2948-2955.
51. Oprisan G., Combiescu M., Guillot S., Caro V., Combiescu A., Delpeyroux F., Crainic R. Natural genetic recombination between co-circulating heterotypic enteroviruses. J. Gen. Virol. 2002, 83:2193-2200.
52. Ortner B., Huang C.W., Schmid D., Mutz I., Wewalka G., Allerberger F., Yang J.Y., Huemer H.P. Epidemiology of enterovirus types causing neurological disease in Austria 1999-2007: detection of clusters of echovirus 30 and enterovirus 71 and analysis of prevalent genotypes. J. Med. Virol. 2009, 81:317-324.
53. Padidam M., Sawyer S., Fauquet C.M. Possible emergence of new geminiviruses by frequent recombination. Virology 1999, 265:218-225.
54. Palacios G., Casas I., Cisterna D., Trallero G., Tenorio A., Freire C. Molecular epidemiology of echovirus 30: temporal circulation and prevalence of single lineages. J. Virol. 2002, 76:4940-4949.
55. Pallansch M.A., Roos R. Enteroviruses: polioviruses, coxsackieviruses, echoviruses and newer enteroviruses. Fields Virology 2007, 839-893. Lippincott Williams and Wilkins, Philadelphia, PA. 5th ed. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus (Eds.).
56. Papa A., Skoura L., Dumaidi K., Spiliopoulou A., Antoniadis A., Frantzidou F. Molecular epidemiology of echovirus 6 in Greece. Eur. J. Clin. Microbiol. Infect. Dis. 2009, 28:682-687.
57. Posada D., Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
58. Posada D., Crandall K.A. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. USA 2001, 98:13757-13762.
59. Posada D., Crandall K.A., Holmes E.C. Recombination in evolutionary genomics. Annu. Rev. Genet. 2002, 36:75-97.
60. Posada D., Buckley T.R. Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Syst. Biol. 2004, 53:793-808.
61. Racaniello V.R. Picornaviridae: the viruses and their replication. Fields Virology 2007, 795-838. Lippincott Williams and Wilkins, Philadelphia, PA. 5th ed. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus (Eds.).
62. Rakoto-Andrianarivelo M., Guillot S., Iber J., Balanant J., Blondel B., Riquet F., Martin J., Kew O., Randriamanalina B., Razafinimpiasa L., Rousset D., Delpeyroux F. Co-circulation and evolution of polioviruses and species C enteroviruses in a district of Madagascar. PLoS Pathog. 2007, 3(12):e191.
63. Richter J., Koptides D., Tryfonos C., Christodoulou C. Molecular typing of enteroviruses associated with meningitis in Cyprus, 2000-2002. J. Gen. Virol. 2006, 55:1035-1041.
64. Rodríguez F., Oliver J.L., Marín A., Medina J.R. The general stochastic model of nucleotide substitution. J. Theor. Biol. 1990, 142:485-501.
65. Roth B., Enders M., Arents A., Pfitzner A., Terletskaia-Ladwig E. Epidemiologic aspects and laboratory features of enteroviruses infections in Western Germany 2000-2005. J. Med. Virol. 2007, 79:956-962.
66. Russell C.A., Jones T.C., Barr I.G., Cox N.J., Garten R.J., Gregory V., Gust I.D., Hampson A.W., Hay A.J., Hurt A.C., de Jong J.C., Kelso A., Klimov A.I., Kageyama T., Komadina N., Lapedes A.S., Lin Y.P., Mosterin A., Obuchi M., Odagiri T., Osterhaus A.D., Rimmelzwaan G.F., Shaw M.W., Skepner E., Stohr K., Tashiro M., Fouchier R.A., Smith D.J. The global circulation of seasonal influenza A (H3N2) viruses. Science 2008, 320:340-346.
67. Salminen M.O., Carr J.K., Burke D.S., McCutchan F.E. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res. Hum. Retroviruses 1995, 11:1423-1425.
68. Salminen M., Martin D. Detecting and characterizing individual recombination events. The Phylogenetic Handbook 2009, 519-548. Cambridge University Press, Cambridge, United Kingdom. second ed. P. Lemey, M. Salemi, A.M. Vandamme (Eds.).
69. Santti J., Hyypiä T., Kinnunen L., Salminen M. Evidence of recombination among enteroviruses. J. Virol. 1999, 73:8741-8749.
70. Savolainen C., Hovi T., Mulders M.N. Molecular epidemiology of echovirus 30 in Europe: succession of dominant sublineages within a single major genotype. Arch. Virol. 2001, 146:521-537.
71. Schierup M.H., Hein J. Consequences of recombination on traditional phylogenetic analysis. Genetics 2000, 156:879-891.
72. Shimizu H., Thorley B., Paladin F.J., Brussen K.A., Stambos V., Yuen L., Utama A., Tano Y., Arita M., Yoshida H., Yoneyama T., Benegas A., Roesel S., Pallansch M., Kew O., Miyamura T. Circulation of type 1 vaccine-derived poliovirus in the Philippines in 2001. J. Virol. 2004, 78:13512-13521.
73. Simmonds P. Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J. Virol. 2006, 80:11124-11140.
74. Stanway G., Brown P., Christian P., Hovi T., Hyypiä T., King N.J., Knowles N.J., Lemon S.M., Minor P.D., Pallansch M.A., Palmemberg A.C., Skern T. Family Picornaviridae. Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses 2005, 757-778. Elsevier/Academic Press. C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Eds.).
75. Suchard M.A., Weiss R.E., Sinsheimer J.S. Bayesian selection of continuous-time Markov chain evolutionary models. Mol. Biol. Evol. 2001, 18:1001-1013.
76. Swofford D.L. PAUP*: Phylogenetic Analysis Using Parsimony (*and Pother methods), Version 4.0 [computer program] 2003, Sinauer Associates, Sunderland, (Massachusetts).
77. Thoelen I., Lemey P., Van der Donck I., Beuselinck K., Lindberg A.M., Van Ranst M. Molecular typing and epidemiology of enteroviruses identified from an outbreak of aseptic meningitis in Belgium during the summer of 2000. J. Med. Virol. 2003, 70:420-429.
78. Thorne J.L., Kishino H., Felsenstein J. Inching toward reality: an improved likelihood model of sequence evolution. J. Mol. Evol. 1992, 34:3-16.
79. Worobey M., Rambaut A., Holmes E.C. Widespread intra-serotype recombination in natural populations of dengue virus. Proc. Natl. Acad. Sci. USA 1999, 96:7352-7357.
80. Worobey M., Holmes E.C. Evolutionary aspects of recombination in RNA viruses. J. Gen. Virol. 1999, 80:2535-2543.
81. Worobey M. A novel approach to detecting and measuring recombination: new insights into evolution in viruses, bacteria, and mitochondria. Mol. Biol. Evol. 2001, 18:1425-1434.
82. Yang C.F., Naguib T., Yang S.J., Nasr E., Jorba J., Ahmed N., Campagnoli R., van der Avoort H., Shimizu H., Yoneyama T., Miyamura T., Pallansch M., Kew O. Circulation of endemic type 2 vaccine-derived poliovirus in Egypt from 1983 to 1993. J. Virol. 2003, 77:8366-8377.
83. Zhang Y., Zhang F., Zhu S., Chen L., Yan D., Wang D., Tang R., Zhu H., Hou X., An H., Zhang H., Xu W. A Sabin 2-related poliovirus recombinant contains a homologous sequence of human enterovirus species C in the viral polymerase coding region. Arch. Virol. 2010, 155:197-205.
84. Zhuang J., Jetzt A.E., Sun G., Yu H., Klarmann G., Ron Y., Preston B.D., Dougherty J.P. Human immunodeficiency virus type 1 recombination: rate, fidelity, and putative hot spots. J. Virol. 2002, 76:11273-11282.