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

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)

    PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    PubMed Central  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  Article  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)

    CAS  PubMed  Article  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)

    PubMed  Article  Google Scholar 

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

    PubMed Central  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    CAS  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  PubMed  Article  CAS  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  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)

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Article  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)

    PubMed Central  PubMed  Article  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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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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  • DOI: https://doi.org/10.1007/s11262-014-1152-y

Keywords

  • Recombination
  • Enteroviruses
  • Evolution
  • Molecular epidemiology