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The complete genome sequences for a novel enterovirus type, enterovirus 96, reflect multiple recombinations

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Abstract

Enterovirus 96 (EV-96) is a recently described genotype in the species Human enterovirus C. So far, only partial genome sequences of this enterovirus type have been available. In this study, we report complete genome sequences for two EV-96 strains isolated from healthy children during enterovirus surveillance in Finland. Sequence analysis revealed substantial nucleotide divergence between EV-96 strains and suggested several recombination events between EV-96 and other HEV-C types.

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References

  1. Andersson P, Edman K, Lindberg AM (2002) Molecular analysis of the echovirus 18 prototype: evidence of interserotypic recombination with echovirus 9. Virus Res 85:71–83

    Article  PubMed  CAS  Google Scholar 

  2. Arita M, Zhu SL, Yoshida H, Yoneyama T, Miyamura T, Shimizu H (2005) A Sabin 3-derived poliovirus recombinant contained a sequence homologous with indigenous human enterovirus species C in the viral polymerase coding region. J Virol 79:12650–12657

    Article  PubMed  CAS  Google Scholar 

  3. Bailly JL, Cardoso MC, Labbe A, Peigue-Lafeuille H (2004) Isolation and identification of an enterovirus 77 recovered from a refugee child from Kosovo, and characterization of the complete virus genome. Virus Res 99:147–155

    Article  PubMed  CAS  Google Scholar 

  4. Bingjun T, Yoshida H, Yan W, Lin L, Tsuji T, Shimizu H, Miyamura T (2008) Molecular typing and epidemiology of non-polio enteroviruses isolated from Yunnan Province, the People’s Republic of China. J Med Virol 80:670–679

    Article  PubMed  Google Scholar 

  5. Blomqvist S, Paananen A, Savolainen-Kopra C, Hovi T, Roivainen M (2008) Eight years of experience with molecular identification of human enteroviruses. J Clin Microbiol 46:2410–2413

    Article  PubMed  Google Scholar 

  6. Brown B, Oberste MS, Maher K, Pallansch MA (2003) Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J Virol 77:8973–8984

    Article  PubMed  CAS  Google Scholar 

  7. Chevaliez S, Szendroi A, Caro V, Balanant J, Guillot S, Berencsi G, Delpeyroux F (2004) 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 325:56–70

    Article  PubMed  CAS  Google Scholar 

  8. Junttila N, Leveque N, Kabue JP, Cartet G, Mushiya F, Muyembe-Tamfum JJ, Trompette A, Lina B, Magnius LO, Chomel JJ, Norder H (2007) New enteroviruses, EV-93 and EV-94, associated with acute flaccid paralysis in the Democratic Republic of the Congo. J Med Virol 79:393–400

    Article  PubMed  Google Scholar 

  9. Lindberg AM, Andersson P, Savolainen C, Mulders MN, Hovi T (2003) 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 84:1223–1235

    Article  PubMed  CAS  Google Scholar 

  10. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160

    PubMed  CAS  Google Scholar 

  11. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, Ilonen J (2003) Recombination in circulating enteroviruses. J Virol 77:10423–10431

    Article  PubMed  CAS  Google Scholar 

  12. Lukashev AN, Lashkevich VA, Koroleva GA, Ilonen J, Hinkkanen AE (2004) Recombination in uveitis-causing enterovirus strains. J Gen Virol 85:463–470

    Article  PubMed  CAS  Google Scholar 

  13. Lukashev AN (2005) Role of recombination in evolution of enteroviruses. Rev Med Virol 15:157–167

    Article  PubMed  CAS  Google Scholar 

  14. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, Ilonen J (2005) Recombination in circulating Human enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 86:3281–3290

    Article  PubMed  CAS  Google Scholar 

  15. Lukashev AN, Ivanova OE, Eremeeva TP, Gmyl LV (2008) Analysis of echovirus 30 isolates from Russia and new independent states revealing frequent recombination and reemergence of ancient lineages. J Clin Microbiol 46:665–670

    Article  PubMed  Google Scholar 

  16. McWilliam Leitch EC, Bendig J, Cabrerizo M, Cardosa J, Hyypia T, Ivanova OE, Kelly A, Kroes AC, Lukashev A, MacAdam A, McMinn P, Roivainen M, Trallero G, Evans DJ, Simmonds P (2009) Transmission networks and population turnover of echovirus 30. J Virol 83:2109–2118

    Article  PubMed  CAS  Google Scholar 

  17. Mirand A, Henquell C, Archimbaud C, Peigue-Lafeuille H, Bailly JL (2007) Emergence of recent echovirus 30 lineages is marked by serial genetic recombination events. J Gen Virol 88:166–176

    Article  PubMed  CAS  Google Scholar 

  18. Norder H, Bjerregaard L, Magnius LO (2002) Open reading frame sequence of an Asian enterovirus 73 strain reveals that the prototype from California is recombinant. J Gen Virol 83:1721–1728

    PubMed  CAS  Google Scholar 

  19. Norder H, Bjerregaard L, Magnius L, Lina B, Aymard M, Chomel JJ (2003) Sequencing of ‘untypable’ enteroviruses reveals two new types, EV-77 and EV-78, within human enterovirus type B and substitutions in the BC loop of the VP1 protein for known types. J Gen Virol 84:827–836

    Article  PubMed  CAS  Google Scholar 

  20. Oberste MS, Maher K, Kilpatrick DR, Pallansch MA (1999) Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73:1941–1948

    PubMed  CAS  Google Scholar 

  21. Oberste MS, Maher K, Flemister MR, Marchetti G, Kilpatrick DR, Pallansch MA (2000) Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. J Clin Microbiol 38:1170–1174

    PubMed  CAS  Google Scholar 

  22. Oberste M, Schnurr D, Maher K, al-Busaidy S, Pallansch M (2001) Molecular identification of new picornaviruses and characterization of a proposed enterovirus 73 serotype. J Gen Virol 82:409–416

    PubMed  CAS  Google Scholar 

  23. Oberste MS, Nix WA, Maher K, Pallansch MA (2003) Improved molecular identification of enteroviruses by RT-PCR and amplicon sequencing. J Clin Virol 26:375–377

    Article  PubMed  CAS  Google Scholar 

  24. Oberste MS, Michele SM, Maher K, Schnurr D, Cisterna D, Junttila N, Uddin M, Chomel JJ, Lau CS, Ridha W, al-Busaidy S, Norder H, Magnius LO, Pallansch MA (2004) Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. J Gen Virol 85:3205–3212

    Article  PubMed  CAS  Google Scholar 

  25. Oberste MS, Penaranda S, Maher K, Pallansch MA (2004) Complete genome sequences of all members of the species Human enterovirus A. J Gen Virol 85:1597–1607

    Article  PubMed  CAS  Google Scholar 

  26. Oberste MS, Maher K, Pallansch MA (2004) Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78:855–867

    Article  PubMed  CAS  Google Scholar 

  27. Oberste MS, Penaranda S, Pallansch MA (2004) RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 78:2948–2955

    Article  PubMed  CAS  Google Scholar 

  28. Oberste MS, Maher K, Michele SM, Belliot G, Uddin M, Pallansch MA (2005) Enteroviruses 76, 89, 90 and 91 represent a novel group within the species Human enterovirus A. J Gen Virol 86:445–451

    Article  PubMed  CAS  Google Scholar 

  29. Oberste MS, Maher K, Williams AJ, Dybdahl-Sissoko N, Brown BA, Gookin MS, Penaranda S, Mishrik N, Uddin M, Pallansch MA (2006) Species-specific RT-PCR amplification of human enteroviruses: a tool for rapid species identification of uncharacterized enteroviruses. J Gen Virol 87:119–128

    Article  PubMed  CAS  Google Scholar 

  30. Oberste MS, Maher K, Nix WA, Michele SM, Uddin M, Schnurr D, al-Busaidy S, Akoua-Koffi C, Pallansch MA (2007) Molecular identification of 13 new enterovirus types, EV79-88, EV97, and EV100-101, members of the species Human Enterovirus B. Virus Res 128:34–42

    Article  PubMed  CAS  Google Scholar 

  31. Oprisan G, Combiescu M, Guillot S, Caro V, Combiescu A, Delpeyroux F, Crainic R (2002) Natural genetic recombination between co-circulating heterotypic enteroviruses. J Gen Virol 83:2193–2200

    PubMed  CAS  Google Scholar 

  32. Pallansch MA, Roos RP (2001) Enteroviruses: polioviruses, coxsackieviruses, echoviruses and newer enteroviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (eds) Fields virology, vol 4. Lippincot Williams and Wilkins, Philadelphia, pp 723–775

    Google Scholar 

  33. Salminen MO, Carr JK, Burke DS, McCutchan FE (1995) Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 11:1423–1425

    Article  PubMed  CAS  Google Scholar 

  34. Santti J, Hyypia T, Kinnunen L, Salminen M (1999) Evidence of recombination among enteroviruses. J Virol 73:8741–8749

    PubMed  CAS  Google Scholar 

  35. Simmonds P, Welch J (2006) Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80:483–493

    Article  PubMed  CAS  Google Scholar 

  36. Smura TP, Junttila N, Blomqvist S, Norder H, Kaijalainen S, Paananen A, Magnius LO, Hovi T, Roivainen M (2007) Enterovirus 94, a proposed new serotype in human enterovirus species D. J Gen Virol 88:849–858

    Article  PubMed  CAS  Google Scholar 

  37. Smura T, Blomqvist S, Paananen A, Vuorinen T, Sobotova Z, Bubovica V, Ivanova O, Hovi T, Roivainen M (2007) Enterovirus surveillance reveals proposed new serotypes and provides new insight into enterovirus 5′-untranslated region evolution. J Gen Virol 88:2520–2526

    Article  PubMed  CAS  Google Scholar 

  38. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  39. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  40. WHO (2001). World Health Organization., Geneva, Switzerland

  41. Yoke-Fun C, AbuBakar S (2006) Phylogenetic evidence for inter-typic recombination in the emergence of human enterovirus 71 subgenotypes. BMC Microbiol 6:74

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Sigrid Juselius Foundation, Helsinki, Finland. The Regional Reference Laboratory work is supported by WHO. We thank Tytti Vuorinen (Department of Virology, University of Turku) for providing virus isolates, Carita Savolainen-Kopra and Marja-Leena Simonen for helpful discussions and Päivi Klemola for PAA sequence.

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Authors and Affiliations

  1. Gastrointestinal Infections Unit, Division of Health Protection, Department of Infectious Disease Surveillance and Control, National Institute for Health and Welfare (THL), P O Box 30, 00271, Helsinki, Finland

    Teemu Smura, Soile Blomqvist, Tapani Hovi & Merja Roivainen

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  1. Teemu Smura
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  2. Soile Blomqvist
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  3. Tapani Hovi
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  4. Merja Roivainen
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Correspondence to Teemu Smura.

Additional information

Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank databases under the accession numbers FJ751914 and FJ751915.

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Supplementary material (DOC 22 kb)

705_2009_418_MOESM2_ESM.tif

Phylogenetic trees constructed from the partial VP1 sequences (359 nt) of HEV-C strains. The EV-96 strains sequenced in this study are indicated by arrows. MEGA version 4.0 was used for the sequence alignment, and phylogenetic tree construction was done using the neighbour-joining method (1000 bootstrap replicates) and Tamura-Nei model of substitution (TIF 109 kb)

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Smura, T., Blomqvist, S., Hovi, T. et al. The complete genome sequences for a novel enterovirus type, enterovirus 96, reflect multiple recombinations. Arch Virol 154, 1157–1161 (2009). https://doi.org/10.1007/s00705-009-0418-5

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  • DOI: https://doi.org/10.1007/s00705-009-0418-5

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