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Recombination among human non-polio enteroviruses: implications for epidemiology and evolution

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Abstract

Human enteroviruses (EV) belong to the Picornaviridae family and are among the most common viruses infecting humans. They consist of up to 100 immunologically and genetically distinct types: polioviruses, coxsackieviruses A and B, echoviruses, and the more recently characterized 43 EV types. Frequent recombinations and mutations in enteroviruses have been recognized as the main mechanisms for the observed high rate of evolution, thus enabling them to rapidly respond and adapt to new environmental challenges. The first signs of genetic exchanges between enteroviruses came from polioviruses many years ago, and since then recombination has been recognized, along with mutations, as the main cause for reversion of vaccine strains to neurovirulence. More recently, non-polio enteroviruses became the focus of many studies, where recombination was recognized as a frequent event and was correlated with the appearance of new enterovirus lineages and types. The accumulation of multiple inter- and intra-typic recombination events could also explain the series of successive emergences and disappearances of specific enterovirus types that could in turn explain the epidemic profile of circulation of several types. This review focuses on recombination among human non-polio enteroviruses from all four species (EV-A, EV-B, EV-C, and EV-D) and discusses the recombination effects on enterovirus epidemiology and evolution.

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Abbreviations

AFP:

Acute flaccid paralysis

CV-A:

Coxsackievirus A

CV-B:

Coxsackievirus B

E:

Echovirus

EV:

Enterovirus

EV-A:

Enterovirus A

EV-B:

Enterovirus B

EV-C:

Enterovirus C

EV-D:

Enterovirus D

HFMD:

Hand foot and mouth disease

IRES:

Internal ribosome entry site

PV:

Poliovirus

RF:

Recombinant form

UTR:

Untranslated region

VDPVs:

Vaccine-derived polioviruses

References

  1. M.A. Pallansch, R.P. Ross, Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses, in Fields Virology, 4th edn., ed. by D.M. Knipe, P.M. Howley, D.E. Griffin (Lippincott Williams & Wilkins, Philadelphia, 2001), p. 723

    Google Scholar 

  2. T. Solomon, P. Lewthwaite, D. Perera, M.J. Cardosa, P. McMinn, M.H. Ooi, Lancet Infect Dis. 10, 778 (2010)

    Article  PubMed  Google Scholar 

  3. B. Brown, M.S. Oberste, K. Maher, M.A. Pallansch, J. Virol. 77, 8973 (2003)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. V.R. Racaniello, Picornaviridae: the viruses and their replication, in Fields Virology, 5th edn., ed. by D.M. Knipe, P.M. Howley (Lippincott Williams & Wilkins, Philadelphia, 2007), p. 795

    Google Scholar 

  5. E. Domingo, V. Martin, C. Perales, C. Escarmis, Curr. Top. Microbiol. Immunol. 323, 3 (2008)

    CAS  PubMed  Google Scholar 

  6. C. Savolainen-Kopra, S. Blomqvist, Rev. Med. Virol. 20, 358 (2010)

    Article  PubMed  Google Scholar 

  7. A.N. Lukashev, Rev. Med. Virol. 15, 157 (2005)

    Article  CAS  PubMed  Google Scholar 

  8. N. Combelas, B. Holmblat, M.L. Joffret, F. Colbere-Garapin, F. Delpeyroux, Viruses 3, 1460 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. V. Pliaka, Z. Kyriakopoulou, P. Markoulatos, Exp. Rev. Vaccines. 11, 609 (2012)

    Article  CAS  Google Scholar 

  10. D. Egger, K. Bienz, J. Virol. 76, 10960 (2002)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. K. Kirkegaard, D. Baltimore, Cell 47, 433 (1986)

    Article  CAS  PubMed  Google Scholar 

  12. E. Dedepsidis, Z. Kyriakopoulou, V. Pliaka, P. Markoulatos, Virus Genes 41, 181 (2010)

    Article  CAS  PubMed  Google Scholar 

  13. L.I. Romanova, V.M. Blinov, E.A. Tolskaya, E.G. Viktorova, M.S. Kolesnikova, E.A. Guseva, V.I. Agol, Virology 155, 202 (1986)

    Article  CAS  PubMed  Google Scholar 

  14. K.A. White, T.J. Morris, RNA 1, 1029 (1995)

    PubMed Central  CAS  PubMed  Google Scholar 

  15. E.V. Pilipenko, A.P. Gmyl, V.I. Agol, Nucleic Acids Res. 23, 1870 (1995)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. A.M. King, Nucleic Acids Res. 16, 11705 (1988)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. C. Runckel, O. Westesson, R. Andino, J.L. DeRisi, PLoS Pathog. 9, e1003164 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. K. Lowry, A. Woodman, J. Cook, D.J. Evans, PLoS Pathog. 10, e1004191 (2014)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  19. A.P. Gmyl, E.V. Belousov, S.V. Maslova, E.V. Khitrina, A.B. Chetverin, V.I. Agol, J. Virol. 73, 8958 (1999)

    PubMed Central  CAS  PubMed  Google Scholar 

  20. A.B. Chetverin, FEBS Lett. 460, 1 (1999)

    Article  CAS  PubMed  Google Scholar 

  21. A.P. Gmyl, RNA 9, 1221 (2003)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. P. Simmonds, J. Welch, J. Virol. 80, 483 (2006)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. C.Y. Tan, L. Ninove, J. Gaudart, A. Nougairede, C. Zandotti, L. Thirion-Perrier, R.N. Charrel, X. de Lamballerie, PLoS ONE 6, e18022 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. T. Bingjun, H. Yoshida, W. Yan, L. Lin, T. Tsuji, H. Shimizu, T. Miyamura, J. Med. Virol. 80, 670 (2008)

    Article  PubMed  CAS  Google Scholar 

  25. M. Bessaud, S. Pillet, W. Ibrahim, M.L. Joffret, B. Pozzetto, F. Delpeyroux, I. Gouandjika-Vasilache, J. Clin. Microbiol. 50, 1650 (2012)

    Article  PubMed Central  PubMed  Google Scholar 

  26. L.N. Apostol, A. Suzuki, A. Bautista, H. Galang, F.J. Paladin, N. Fuji, S. Lupisan, R. Olveda, H. Oshitani, J. Med. Virol. 84, 624 (2012)

    Article  PubMed Central  PubMed  Google Scholar 

  27. M.S. Oberste, J. Gen. Virol. 85, 1597 (2004)

    Article  CAS  PubMed  Google Scholar 

  28. S.W. Huang, D. Kiang, D.J. Smith, J.R. Wang, Exp. Biol. Med. (Maywood) 236, 899 (2011)

    Article  CAS  Google Scholar 

  29. S.C. Huang, Y.W. Hsu, H.C. Wang, S.W. Huang, D. Kiang, H.P. Tsai, S.M. Wang, C.C. Liu, K.H. Lin, I.J. Su, J.R. Wang, Virus Res. 131, 250 (2008)

    Article  CAS  PubMed  Google Scholar 

  30. S. van der Sanden, J. van Eek, D.P. Martin, H. van der Avoort, H. Vennema, M. Koopmans, Infect. Genet. Evol. 11, 886 (2011)

    Article  PubMed  Google Scholar 

  31. C. Yoke-Fun, S. AbuBakar, BMC Microbiol. 6, 74 (2006)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  32. Y. Zhang, Z. Zhu, W. Yang, J. Ren, X. Tan, Y. Wang, N. Mao, S. Xu, S. Zhu, A. Cui, Y. Zhang, D. Yan, Q. Li, X. Dong, J. Zhang, Y. Zhao, J. Wan, Z. Feng, J. Sun, S. Wang, D. Li, W. Xu, Virol. J. 7, 94 (2010)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  33. S.W. Huang, Y.W. Hsu, D.J. Smith, D. Kiang, H.P. Tsai, K.H. Lin, S.M. Wang, C.C. Liu, I.J. Su, J.R. Wang, J. Clin. Microbiol. 47, 3653 (2009)

    Article  PubMed Central  PubMed  Google Scholar 

  34. C.C. Yip, S.K. Lau, B. Zhou, M.X. Zhang, H.W. Tsoi, K.H. Chan, X.C. Chen, P.C. Woo, K.Y. Yuen, Arch. Virol. 155, 1413 (2010)

    Article  CAS  PubMed  Google Scholar 

  35. A.N. Lukashev, E.Y. Shumilina, I.S. Belalov, O.E. Ivanova, T.P. Eremeeva, V.I. Reznik, O.E. Trotsenko, J.F. Drexler, C. Drosten, J. Gen. Virol. 95, 868 (2014)

    Article  CAS  PubMed  Google Scholar 

  36. Y.F. Hu, F. Yang, J. Du, J. Dong, T. Zhang, Z.Q. Wu, Y. Xue, Q. Jin, J. Clin. Microbiol. 49, 2426 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. K. Zhao, X. Han, G. Wang, W. Hu, W. Zhang, X.F. Yu, Emerg. Infect. Dis. 17, 1537 (2011)

    PubMed Central  PubMed  Google Scholar 

  38. A. Xu, Z. Tao, X. Lin, Y. Liu, Y. Zhang, L. Song, H. Wang, J. Yang, Y. Li, F. Ji, L. Feng, Z. Zhao, Arch. Virol. 156, 1685 (2011)

    Article  CAS  PubMed  Google Scholar 

  39. M.S. Oberste, S. Penaranda, M.A. Pallansch, J. Virol. 78, 2948 (2004)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. B.H. Chua, P.C. McMinn, S.K. Lam, K.B. Chua, J. Gen. Virol. 82, 2629 (2001)

    CAS  PubMed  Google Scholar 

  41. M. Iwai, H. Yoshida, M. Obara, E. Horimoto, K. Nakamura, T. Takizawa, T. Kurata, M. Mizuguchi, T. Daikoku, K. Shiraki, Clin. Vaccine Immunol. 17, 764 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. G. Oprisan, M. Combiescu, S. Guillot, V. Caro, A. Combiescu, F. Delpeyroux, R. Crainic, J. Gen. Virol. 83, 2193 (2002)

    CAS  PubMed  Google Scholar 

  43. A.N. Lukashev, V.A. Lashkevich, O.E. Ivanova, G.A. Koroleva, A.E. Hinkkanen, J. Ilonen, J. Virol. 77, 10423 (2003)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. C. Kottaridi, E. Bolanaki, Z. Kyriakopoulou, E. Dedepsidis, A. Pratti, P. Markoulatos, Diagn. Microbiol. Infect. Dis. 58, 407 (2007)

    Article  CAS  PubMed  Google Scholar 

  45. E. Bolanaki, C. Kottaridi, P. Markoulatos, Z. Kyriakopoulou, L. Margaritis, T. Katsorchis, Virus Genes 35, 129 (2007)

    Article  CAS  PubMed  Google Scholar 

  46. A.M. Lindberg, P. Andersson, C. Savolainen, M.N. Mulders, T. Hovi, J. Gen. Virol. 84, 1223 (2003)

    Article  CAS  PubMed  Google Scholar 

  47. A.N. Lukashev, V.A. Lashkevich, G.A. Koroleva, J. Ilonen, A.E. Hinkkanen, J. Gen. Virol. 85, 463 (2004)

    Article  CAS  PubMed  Google Scholar 

  48. A.N. Lukashev, V.A. Lashkevich, O.E. Ivanova, G.A. Koroleva, A.E. Hinkkanen, J. Ilonen, J. Gen. Virol. 86, 3281 (2005)

    Article  CAS  PubMed  Google Scholar 

  49. Z. Kyriakopoulou, E. Dedepsidis, V. Pliaka, P. Mastorakos, A. Stamati, A. Pratti, S. Levidiotou-Stefanou, P. Markoulatos, Virus Genes 40, 183 (2010)

    Article  CAS  PubMed  Google Scholar 

  50. Z. Kyriakopoulou, V. Pliaka, D. Tsakogiannis, I.G. Ruether, D. Komiotis, C. Gartzonika, S. Levidiotou-Stefanou, P. Markoulatos, Virus Genes 44, 207 (2012)

    Article  CAS  PubMed  Google Scholar 

  51. P. Krogstad, R. Hammon, N. Halnon, J.L. Whitton, Pediatr. Infect. Dis. J. 27, 668 (2008)

    Article  PubMed  Google Scholar 

  52. Z. Tao, N. Cui, A. Xu, H. Wang, L. Song, Y. Li, G. Liu, Y. Liu, L. Feng, Virus Genes 41, 158 (2010)

    Article  CAS  PubMed  Google Scholar 

  53. Z. Tao, N. Cui, G. Liu, P. Chen, A. Xu, L. Song, F. Ji, H. Wang, Y. Song, J. Virol. 86, 13129 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. A. Mirand, C. Henquell, C. Archimbaud, H. Peigue-Lafeuille, J.L. Bailly, J. Gen. Virol. 88, 166 (2007)

    Article  CAS  PubMed  Google Scholar 

  55. E.C. McWilliam Leitch, M. Cabrerizo, J. Cardosa, H. Harvala, O.E. Ivanova, A.C. Kroes, A. Lukashev, P. Muir, J. Odoom, M. Roivainen, P. Susi, G. Trallero, D.J. Evans, P. Simmonds, J Virol. 84, 9292 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. E.C. McWilliam Leitch, J. Bendig, M. Cabrerizo, J. Cardosa, T. Hyypia, O.E. Ivanova, A. Kelly, A.C. Kroes, A. Lukashev, A. MacAdam, P. McMinn, M. Roivainen, G. Trallero, D.J. Evans, P. Simmonds, J. Virol. 83, 2109 (2009)

    Article  CAS  PubMed  Google Scholar 

  57. M. Cabrerizo, G. Trallero, P. Simmonds, J. Med. Virol. 86, 857 (2014)

    Article  PubMed  Google Scholar 

  58. J.L. Bailly, A. Mirand, C. Henquell, C. Archimbaud, M. Chambon, C. Regagnon, F. Charbonne, H. Peigue-Lafeuille, Infect. Genet. Evol. 11, 276 (2011)

    Article  CAS  PubMed  Google Scholar 

  59. O. Kew, V. Morris-Glasgow, M. Landaverde, C. Burns, J. Shaw, Z. Garib, J. Andre, E. Blackman, C.J. Freeman, J. Jorba, R. Sutter, G. Tambini, L. Venczel, C. Pedreira, F. Laender, H. Shimizu, T. Yoneyama, T. Miyamura, H. van Der Avoort, M.S. Oberste, D. Kilpatrick, S. Cochi, M. Pallansch, C. de Quadros, Science 296, 356 (2002)

    Article  CAS  PubMed  Google Scholar 

  60. M. Rakoto-Andrianarivelo, N. Gumede, S. Jegouic, J. Balanant, S.N. Andriamamonjy, S. Rabemanantsoa, M. Birmingham, B. Randriamanalina, L. Nkolomoni, M. Venter, B.D. Schoub, F. Delpeyroux, J.M. Reynes, J. Infect. Dis. 197, 1427 (2008)

    Article  CAS  PubMed  Google Scholar 

  61. I. Karakasiliotis, E. Paximadi, P. Markoulatos, J. Gen. Virol. 86, 3137 (2005)

    Article  CAS  PubMed  Google Scholar 

  62. Z. Kyriakopoulou, C. Kottaridi, E. Dedepsidis, E. Bolanaki, S. Levidiotou-Stefanou, P. Markoulatos, J. Clin. Microbiol. 44, 1150 (2006)

    Article  PubMed Central  PubMed  Google Scholar 

  63. E. Dedepsidis, Z. Kyriakopoulou, V. Pliaka, C. Kottaridi, E. Bolanaki, S. Levidiotou-Stefanou, D. Komiotis, P. Markoulatos, Appl. Environ. Microbiol. 73, 6697 (2007)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. E. Paximadi, I. Karakasiliotis, D. Papaventsis, G. Papageorgiou, P. Markoulatos, J. Appl. Microbiol. 104, 1153 (2008)

    Article  CAS  PubMed  Google Scholar 

  65. T. Smura, S. Blomqvist, A. Paananen, T. Vuorinen, Z. Sobotova, V. Bubovica, O. Ivanova, T. Hovi, M. Roivainen, J. Genet. Virol. 88, 2520 (2007)

    Article  CAS  Google Scholar 

  66. A. Xu, Z. Tao, H. Wang, Y. Zhang, L. Song, Y. Li, G. Liu, Y. Liu, H. Yang, Q. Fan, F. Ji, Y. Zhang, J. Yang, L. Feng, W. Xu, Z. Zhao, Virus Genes 42, 323 (2011)

    Article  CAS  PubMed  Google Scholar 

  67. T. Smura, S. Blomqvist, T. Hovi, M. Roivainen, Arch. Virol. 154, 1157 (2009)

    Article  CAS  PubMed  Google Scholar 

  68. M. Bessaud, M.L. Joffret, B. Holmblat, R. Razafindratsimandresy, F. Delpeyroux, PLoS ONE 6, e24823 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. T. Smura, S. Blomqvist, T. Vuorinen, O. Ivanova, E. Samoilovich, H. Al-Hello, C. Savolainen-Kopra, T. Hovi, M. Roivainen, PLoS ONE 9, e94579 (2014)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  70. A.N. Lukashev, J.F. Drexler, V.O. Kotova, E.N. Amjaga, V.I. Reznik, A.P. Gmyl, G. Grard, R. Taty Taty, O.E. Trotsenko, E.M. Leroy, C. Drosten, J. Gen. Virol. 93, 2357 (2012)

    Article  CAS  PubMed  Google Scholar 

  71. A. Piralla, L. Fiorina, C. Daleno, S. Esposito, F. Baldanti, Infect. Genet. Evol. 20, 111 (2013)

    Article  CAS  PubMed  Google Scholar 

  72. R. Tokarz, S. Haq, S. Sameroff, S.R. Howie, W.I. Lipkin, J. Gen. Virol. 94, 1995 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  73. Y. Liu, C. Wang, S. Mueller, A.V. Paul, E. Wimmer, P. Jiang, PLoS Pathog. 6, e1001066 (2010)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  74. H. Harvala, C.P. Sharp, E.M. Ngole, E. Delaporte, M. Peeters, P. Simmonds, J. Virol. 85, 4480 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. T.P. Smura, N. Junttila, S. Blomqvist, H. Norder, S. Kaijalainen, A. Paananen, L.O. Magnius, T. Hovi, M. Roivainen, J. Gen. Virol. 88, 849 (2007)

    Article  CAS  PubMed  Google Scholar 

  76. J. Santti, T. Hyypia, L. Kinnunen, M. Salminen, J. Virol. 73, 8741 (1999)

    PubMed Central  CAS  PubMed  Google Scholar 

  77. N.L. Yozwiak, P. Skewes-Cox, A. Gordon, S. Saborio, G. Kuan, A. Balmaseda, D. Ganem, E. Harris, J.L. DeRisi, J. Virol. 84, 9047 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. M.S. Oberste, K. Maher, M.A. Pallansch, J. Gen. Virol. 88, 3360 (2007)

    Article  CAS  PubMed  Google Scholar 

  79. S.D. McClenahan, G. Scherba, L. Borst, R.L. Fredrickson, P.R. Krause, C. Uhlenhaut, PLoS ONE 8, e68777 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  80. M.S. Oberste, M.M. Feeroz, K. Maher, W.A. Nix, G.A. Engel, K.M. Hasan, S. Begum, G. Oh, A.H. Chowdhury, M.A. Pallansch, L. Jones-Engel, J. Virol. 87, 558 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  81. G. Zhang, D.T. Haydon, N.J. Knowles, J.W. McCauley, J. Gen. Virol. 80(Pt 3), 639 (1999)

    CAS  PubMed  Google Scholar 

  82. A. Boros, P. Pankovics, N.J. Knowles, G. Reuter, J. Gen. Virol. 93, 1941 (2012)

    Article  CAS  PubMed  Google Scholar 

  83. M. Bessaud, S. Jegouic, M.L. Joffret, C. Barge, J. Balanant, I. Gouandjika-Vasilache, F. Delpeyroux, J. Virol. Methods 149, 277 (2008)

    Article  CAS  PubMed  Google Scholar 

  84. H.M. Liu, D.P. Zheng, L.B. Zhang, M.S. Oberste, O.M. Kew, M.A. Pallansch, J. Virol. 77, 10994 (2003)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. I. Karakasiliotis, P. Markoulatos, T. Katsorchis, Mol. Cell. Probes 18, 103 (2004)

    Article  CAS  PubMed  Google Scholar 

  86. M. Worobey, E.C. Holmes, J. Gen. Virol. 80(Pt 10), 2535 (1999)

    CAS  PubMed  Google Scholar 

  87. Z. Kyriakopoulou, E. Dedepsidis, V. Pliaka, D. Tsakogiannis, I.G. Ruether, A. Krikelis, P. Markoulatos, Clin. Microbiol. Infect. 17, 1170 (2011)

    Article  CAS  PubMed  Google Scholar 

  88. S. Blomqvist, J. Gen. Virol. 84, 573 (2003)

    Article  CAS  PubMed  Google Scholar 

  89. E. Dedepsidis, V. Pliaka, Z. Kyriakopoulou, C. Brakoulias, S. Levidiotou-Stefanou, A. Pratti, Z. Mamuris, P. Markoulatos, FEMS Immunol. Med. Microbiol. 52, 343 (2008)

    Article  CAS  PubMed  Google Scholar 

  90. S. Blomqvist, C. Savolainen-Kopra, A. Paananen, L. El Bassioni, E.M. El Maamoon Nasr, L. Firstova, N. Zamiatina, T. Kutateladze, M. Roivainen, Virus Res. 151, 246 (2010)

    Article  CAS  PubMed  Google Scholar 

  91. L. Bouslama, D. Nasri, L. Chollet, K. Belguith, T. Bourlet, M. Aouni, B. Pozzetto, S. Pillet, J. Virol. 81, 8944 (2007)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  92. F. Adu, J. Iber, D. Bukbuk, N. Gumede, S.J. Yang, J. Jorba, R. Campagnoli, W.F. Sule, C.F. Yang, C. Burns, M. Pallansch, T. Harry, O. Kew, Virus Res. 127, 17 (2007)

    Article  CAS  PubMed  Google Scholar 

  93. E. Martinez-Salas, A. Pacheco, P. Serrano, N. Fernandez, J. Gen. Virol. 89, 611 (2008)

    Article  CAS  PubMed  Google Scholar 

  94. P. Florez de Sessions, E. Dobrikova, M. Gromeier, J. Virol. 81, 8396 (2007)

    Article  CAS  PubMed  Google Scholar 

  95. R. Butsch, C. Tapparel, P. Keller, K. Herzog, M. Krause, W. Wunderli, L. Kaiser, W. Bossart, Infection 41, 231 (2013)

    Article  CAS  PubMed  Google Scholar 

  96. T. Zhang, J. Du, Y. Xue, H. Su, F. Yang, Q. Jin, PLoS ONE 8, e67157 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  97. S. Jegouic, M.L. Joffret, C. Blanchard, F.B. Riquet, C. Perret, I. Pelletier, F. Colbere-Garapin, M. Rakoto-Andrianarivelo, F. Delpeyroux, PLoS Pathog. 5, e1000412 (2009)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  98. F.B. Riquet, C. Blanchard, S. Jegouic, J. Balanant, S. Guillot, M.A. Vibet, M. Rakoto-Andrianarivelo, F. Delpeyroux, J. Virol. 82, 8927 (2008)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  99. Q. Sun, Y. Zhang, S. Zhu, H. Cui, H. Tian, D. Yan, G. Huang, Z. Zhu, D. Wang, X. Li, H. Jiang, H. An, W. Xu, J. Virol. 86, 10228 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  100. C. Savolainen-Kopra, E. Samoilovich, H. Kahelin, A.K. Hiekka, T. Hovi, M. Roivainen, J. Gen. Virol. 90, 1859 (2009)

    Article  CAS  PubMed  Google Scholar 

  101. V. Pliaka, Z. Kyriakopoulou, D. Tsakogiannis, I.G. Ruether, C. Gartzonika, S. Levidiotou-Stefanou, A. Krikelis, P. Markoulatos, Eur. J. Clin. Microbiol. Infect. Dis. 29, 1513 (2010)

    Article  CAS  PubMed  Google Scholar 

  102. V. Pliaka, M.E. Filliponi, Z. Kyriakopoulou, I.G. Ruether, D. Tsakogiannis, C. Gartzonika, S. Levidiotou-Stefanou, P. Markoulatos, Clin. Microbiol. Infect. 17, 1554 (2011)

    Article  CAS  PubMed  Google Scholar 

  103. S. Cordey, T.J. Petty, M. Schibler, Y. Martinez, D. Gerlach, S. van Belle, L. Turin, E. Zdobnov, L. Kaiser, C. Tapparel, PLoS Pathog. 8, e1002826 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  104. E.C. McWilliam Leitch, M. Cabrerizo, J. Cardosa, H. Harvala, O.E. Ivanova, S. Koike, A.C. Kroes, A. Lukashev, D. Perera, M. Roivainen, P. Susi, G. Trallero, D.J. Evans, P. Simmonds, J. Virol. 86, 2676 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  105. E. Bolanaki, C. Kottaridi, P. Markoulatos, L. Margaritis, T. Katsorchis, Virus Genes 32, 249 (2006)

    Article  CAS  PubMed  Google Scholar 

  106. M. Miyoshi, R. Komagome, S. Ishida, H. Nagano, K. Takahashi, M. Okano, Arch. Virol. 158, 775 (2013)

    Article  CAS  PubMed  Google Scholar 

  107. Z. Kyriakopoulou, E. Dedepsidis, V. Pliaka, D. Tsakogiannis, A. Pratti, S. Levidiotou-Stefanou, P. Markoulatos, J. Clin. Microbiol. 48, 1513 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  108. M. Cabrerizo, J.E. Echevarria, I. Gonzalez, T. de Miguel, G. Trallero, J. Med. Virol. 80, 1018 (2008)

    Article  PubMed  Google Scholar 

  109. H.J. Boot, R.M. Schepp, F.J. van Nunen, T.G. Kimman, J. Virol. Methods 116, 35 (2004)

    Article  CAS  PubMed  Google Scholar 

  110. D.R. Kilpatrick, K. Ching, J. Iber, R. Campagnoli, C.J. Freeman, N. Mishrik, H.M. Liu, M.A. Pallansch, O.M. Kew, J. Clin. Microbiol. 42, 4313 (2004)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  111. V. Pliaka, E. Dedepsidis, Z. Kyriakopoulou, K. Mpirli, D. Tsakogiannis, A. Pratti, S. Levidiotou-Stefanou, P. Markoulatos, Mol. Cell. Probes 24, 115 (2010)

    Article  CAS  PubMed  Google Scholar 

  112. T.G. Dimitriou, V. Pliaka, Z. Kyriakopoulou, I.G. Ruether, D. Tsakogiannis, P. Fountoucidou, C. Gartzonika, S. Levidiotou-Stefanou, P. Markoulatos, Mol. Cell. Probes 28, 107 (2013)

  113. C.C. Kok, G.G. Au, Arch. Virol. 158, 765 (2013)

    Article  CAS  PubMed  Google Scholar 

  114. S. Chevaliez, A. Szendroi, V. Caro, J. Balanant, S. Guillot, G. Berencsi, F. Delpeyroux, Virology 325, 56 (2004)

    Article  CAS  PubMed  Google Scholar 

  115. C.H. Williams, S. Oikarinen, S. Tauriainen, K. Salminen, H. Hyoty, G. Stanway, J. Clin. Microbiol. 44, 441 (2006)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  116. Y.F. Hu, J. Du, R. Zhao, Y. Xue, F. Yang, Q. Jin, J. Virol. 86, 10901 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  117. Y. Zhang, X. Tan, A. Cui, N. Mao, S. Xu, Z. Zhu, J. Zhou, J. Shi, Y. Zhao, X. Wang, X. Huang, S. Zhu, Y. Zhang, W. Tang, H. Ling, W. Xu, PLoS ONE 8, e56341 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  118. C.C. Yip, S.K. Lau, P.C. Woo, S.S. Wong, T.H. Tsang, J.Y. Lo, W.K. Lam, C.C. Tsang, K.H. Chan, K.Y. Yuen, Emerg. Infect. Dis. 19, 1285 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  119. X. Chen, X. Tan, J. Li, Y. Jin, L. Gong, M. Hong, Y. Shi, S. Zhu, B. Zhang, S. Zhang, Y. Zhang, N. Mao, W. Xu, PLoS ONE 8, e82861 (2013)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  120. J.F. Han, N. Yu, Y.X. Pan, S.J. He, L.J. Xu, R.Y. Cao, Y.X. Li, S.Y. Zhu, Y. Zhang, E.D. Qin, X.Y. Che, C.F. Qin, Virus Res. 179, 212 (2014)

    Article  CAS  PubMed  Google Scholar 

  121. W. Liu, S. Wu, Y. Xiong, T. Li, Z. Wen, M. Yan, K. Qin, Y. Liu, J. Wu, PLoS ONE 9, e96051 (2014)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  122. X. Liu, N. Mao, W. Yu, Q. Chai, H. Wang, W. Wang, L. Wang, Z. Wang, W. Xu, Arch. Virol. 159, 2497 (2014)

    Article  CAS  PubMed  Google Scholar 

  123. T. Smura, L. Kakkola, S. Blomqvist, P. Klemola, A. Parsons, H. Kallio-Kokko, C. Savolainen-Kopra, D.E. Kainov, M. Roivainen, Infect. Genet. Evol. 16C, 234 (2013)

    Article  CAS  Google Scholar 

  124. Q. Sun, Y. Zhang, S. Zhu, H. Tian, G. Huang, H. Cui, X. Li, D. Yan, Z. Zhu, J. Li, P. Zheng, H. Jiang, B. Zhang, X. Tan, H. Zhu, H. An, W. Xu, PLoS ONE 8, e55480 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  125. H. Ma, X. Huang, K. Kang, X. Li, X. Tang, Y. Ren, Y. Wang, G. Zhao, B. Xu, Arch. Virol. 158, 2169 (2013)

    Article  CAS  PubMed  Google Scholar 

  126. Z. Wu, J. Du, T. Zhang, Y. Xue, F. Yang, Q. Jin, J. Clin. Microbiol. 51, 3083 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  127. H. Xiao, K. Huang, L. Li, X. Wu, L. Zheng, C. Wan, W. Zhao, C. Ke, B. Zhang, Arch. Virol. 159, 379 (2014)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  128. X. Tian, Y. Zhang, S. Gu, Y. Fan, Q. Sun, B. Zhang, S. Yan, W. Xu, X. Ma, W. Wang, PLoS ONE 9, e90379 (2014)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  129. L. Hu, Y. Zhang, M. Hong, S. Zhu, D. Yan, D. Wang, X. Li, Z. Zhu, Tsewang, W. Xu, Sci. Rep. 4, 6035 (2014)

    PubMed Central  CAS  PubMed  Google Scholar 

  130. J. Wang, Y. Zhang, M. Hong, X. Li, S. Zhu, D. Yan, D. Wang, H. An, Tsewang, J. Han, W. Xu, Arch. Virol. 157, 1593 (2012)

    Article  CAS  PubMed  Google Scholar 

  131. G. Sun, M. Yi, H. Tian, C. Shao, S. Yang, J. Han, X. Wang, Y. Wang, Q. Shen, H. Wang, S. Shao, Y. Yang, W. Zhang, Arch. Virol. 159, 333 (2014)

    Article  CAS  PubMed  Google Scholar 

  132. X. Liu, Z. Tao, H. Wang, X. Lin, L. Song, Y. Li, L. Zhang, S. Wang, N. Cui, A. Xu, Y. Song, Virus Genes 49, 38 (2014)

    Article  CAS  PubMed  Google Scholar 

  133. Z. Tao, N. Cui, X. Lin, H. Wang, L. Song, Y. Li, L. Zhang, X. Liu, S. Wang, A. Xu, Y. Song, Arch. Virol. 159, 2809 (2014)

    Article  CAS  PubMed  Google Scholar 

  134. A. Piralla, C. Daleno, A. Scala, D. Greenberg, V. Usonis, N. Principi, F. Baldanti, S. Esposito, PLoS ONE 8, e60641 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  135. J. Lu, H. Zheng, Y. Zhang, X. Guo, D. Wu, H. Li, L. Liu, H. Zeng, L. Yi, L. Fang, Y. Mo, W. Xu, C. Ke, PLoS ONE 9, e86877 (2014)

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by Research Grants of the Postgraduate Programme ‘Applications of Molecular Biology-Genetics. Diagnostic Biomarkers,’ code 3817 of the University of Thessaly, School of Health Sciences, Department of Biochemistry & Biotechnology.

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  1. Department of Biochemistry & Biotechnology, School of Health Sciences, University of Thessaly, 26, Ploutonos & Aeolou Str., 41221, Larissa, Greece

    Zaharoula Kyriakopoulou, Vaia Pliaka, Grigoris D. Amoutzias & Panayotis Markoulatos

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  1. Zaharoula Kyriakopoulou
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  2. Vaia Pliaka
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Correspondence to Panayotis Markoulatos.

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Kyriakopoulou, Z., Pliaka, V., Amoutzias, G.D. et al. Recombination among human non-polio enteroviruses: implications for epidemiology and evolution. Virus Genes 50, 177–188 (2015). https://doi.org/10.1007/s11262-014-1152-y

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