Use of the 5′ untranslated region and VP1 region to examine the molecular diversity in enterovirus B species Free

Abstract

Human enteroviruses evolve quickly. The 5′ untranslated region (UTR) is fundamentally important for efficient viral replication and for virulence; the VP1 region correlates well with antigenic typing by neutralization, and can be used for virus identification and evolutionary studies. In order to investigate the molecular diversity in EV-B species, the 5′ UTR and VP1 regions were analysed for 208 clinical isolates from a single public-health laboratory (serving New South Wales, Australia), representing 28 EV-B types. Sequences were compared with the 5′ UTR and VP1 regions of 98 strains available in GenBank, representing the same 28 types. The genetic relationships were analysed using two types of software ( and BioNumerics). The sequence analyses of the 5′ UTR and VP1 regions of 306 EV-B strains demonstrated that: (i) comparing the two regions gives strong evidence of epidemiological linkage of strains in some serotypes; (ii) the intraserotypic genetic variation within each gene reveals that they evolve distinctly largely due to their different functions; and (iii) mutation and possible recombination in the two regions play significant roles in the molecular diversity of EV-B. Understanding the tempo and pattern of molecular diversity and evolution is of great importance in the pathogenesis of EV-B enteroviruses, information which will assist in disease prevention and control.

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2014-10-01
2024-03-28
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References

  1. Al-Hello H., Paananen A., Eskelinen M., Ylipaasto P., Hovi T., Salmela K., Lukashev A. N., Bobegamage S., Roivainen M. 2008; An enterovirus strain isolated from diabetic child belongs to a genetic subcluster of echovirus 11, but is also neutralised with monotypic antisera to coxsackievirus A9. J Gen Virol 89:1949–1959 [View Article][PubMed]
    [Google Scholar]
  2. Bailey J. M., Tapprich W. E. 2007; Structure of the 5′ nontranslated region of the coxsackievirus b3 genome: chemical modification and comparative sequence analysis. J Virol 81:650–668 [View Article][PubMed]
    [Google Scholar]
  3. Bailly J. L., Chambon M., Henquell C., Icart J., Peigue-Lafeuille H. 2000; Genomic variations in echovirus 30 persistent isolates recovered from a chronically infected immunodeficient child and comparison with the reference strain. J Clin Microbiol 38:552–557[PubMed]
    [Google Scholar]
  4. Barton D. J., O’Donnell B. J., Flanegan J. B. 2001; 5′ Cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis. EMBO J 20:1439–1448 [View Article][PubMed]
    [Google Scholar]
  5. Brown B. A., Oberste M. S., Alexander J. P. Jr, Kennett M. L., Pallansch M. A. 1999; Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73:9969–9975[PubMed]
    [Google Scholar]
  6. Cabrerizo M., Trallero G., Simmonds P. 2014; Recombination and evolutionary dynamics of human echovirus 6. J Med Virol 86:857–864 [View Article][PubMed]
    [Google Scholar]
  7. Chang K. H., Auvinen P., Hyypiä T., Stanway G. 1989; The nucleotide sequence of coxsackievirus A9; implications for receptor binding and enterovirus classification. J Gen Virol 70:3269–3280 [View Article][PubMed]
    [Google Scholar]
  8. Chapman N. M., Tu Z., Tracy S., Gauntt C. J. 1994; An infectious cDNA copy of the genome of a non-cardiovirulent coxsackievirus B3 strain: its complete sequence analysis and comparison to the genomes of cardiovirulent coxsackieviruses. Arch Virol 135:115–130 [View Article][PubMed]
    [Google Scholar]
  9. Chen G. W., Huang J. H., Lo Y. L., Tsao K. C., Chang S. C. 2007; Mosaic genome structure of echovirus type 30 that circulated in Taiwan in 2001. Arch Virol 152:1807–1817 [View Article][PubMed]
    [Google Scholar]
  10. Chevaliez S., Szendröi 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 [View Article][PubMed]
    [Google Scholar]
  11. Cramblett H. G., Haynes R. E., Azimi P. H., Hilty M. D., Wilder M. H. 1973; Nosocomial infection with echovirus type II in handicapped and premature infants. Pediatrics 51:603–607[PubMed]
    [Google Scholar]
  12. De Jesus N., Franco D., Paul A., Wimmer E., Cello J. 2005; Mutation of a single conserved nucleotide between the cloverleaf and internal ribosome entry site attenuates poliovirus neurovirulence. J Virol 79:14235–14243 [View Article][PubMed]
    [Google Scholar]
  13. Domingo E., Holland J. J. 1997; RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178 [View Article][PubMed]
    [Google Scholar]
  14. Drake J. W., Holland J. J. 1999; Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96:13910–13913 [View Article][PubMed]
    [Google Scholar]
  15. Faustini A., Fano V., Muscillo M., Zaniratti S., La Rosa G., Tribuzi L., Perucci C. A. 2006; An outbreak of aseptic meningitis due to echovirus 30 associated with attending school and swimming in pools. Int J Infect Dis 10:291–297 [View Article][PubMed]
    [Google Scholar]
  16. Harvala H., Kalimo H., Dahllund L., Santti J., Hughes P., Hyypiä T., Stanway G. 2002; Mapping of tissue tropism determinants in coxsackievirus genomes. J Gen Virol 83:1697–1706[PubMed]
    [Google Scholar]
  17. Harvala H., Kalimo H., Stanway G., Hyypiä T. 2003; Pathogenesis of coxsackievirus A9 in mice: role of the viral arginine-glycine-aspartic acid motif. J Gen Virol 84:2375–2379 [View Article][PubMed]
    [Google Scholar]
  18. Henquell C., Mirand A., Richter J., Schuffenecker I., Böttiger B., Diedrich S., Terletskaia-Ladwig E., Christodoulou C., Peigue-Lafeuille H., Bailly J. L. 2013; Phylogenetic patterns of human coxsackievirus B5 arise from population dynamics between two genogroups and reveal evolutionary factors of molecular adaptation and transmission. J Virol 87:12249–12259 [View Article][PubMed]
    [Google Scholar]
  19. Kopecka H., Brown B., Pallansch M. 1995; Genotypic variation in coxsackievirus B5 isolates from three different outbreaks in the United States. Virus Res 38:125–136 [View Article][PubMed]
    [Google Scholar]
  20. Kottaridi C., Bolanaki E., Mamuris Z., Stathopoulos C., Markoulatos P. 2006; Molecular phylogeny of VP1, 2A, and 2B genes of echovirus isolates: epidemiological linkage and observations on genetic variation. Arch Virol 151:1117–1132 [View Article][PubMed]
    [Google Scholar]
  21. Kumar S., Nei M., Dudley J., Tamura K. 2008; MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306 [View Article][PubMed]
    [Google Scholar]
  22. Lee C. K., Kono K., Haas E., Kim K. S., Drescher K. M., Chapman N. M., Tracy S. 2005; Characterization of an infectious cDNA copy of the genome of a naturally occurring, avirulent coxsackievirus B3 clinical isolate. J Gen Virol 86:197–210 [View Article][PubMed]
    [Google Scholar]
  23. Lim B. K., Peter A. K., Xiong D., Narezkina A., Yung A., Dalton N. D., Hwang K. K., Yajima T., Chen J., Knowlton K. U. 2013; Inhibition of coxsackievirus-associated dystrophin cleavage prevents cardiomyopathy. J Clin Invest 123:5146–5151 [View Article][PubMed]
    [Google Scholar]
  24. Lukashev A. N., Lashkevich V. A., Ivanova O. E., Koroleva G. A., Hinkkanen A. E., Ilonen J. 2003a; Recombination in circulating enteroviruses. J Virol 77:10423–10431 [View Article][PubMed]
    [Google Scholar]
  25. Lukashev A. N., Lashkevich V. A., Koroleva G. A., Ilonen J., Karganova G. G., Reznik V. I., Hinkkanen A. E. 2003b; Molecular epidemiology of enteroviruses causing uveitis and multisystem hemorrhagic disease of infants. Virology 307:45–53 [View Article][PubMed]
    [Google Scholar]
  26. Lukashev A. N., Lashkevich V. A., Koroleva G. A., Ilonen J., Hinkkanen A. E. 2004; Recombination in uveitis-causing enterovirus strains. J Gen Virol 85:463–470 [View Article][PubMed]
    [Google Scholar]
  27. Lukashev A. N., Lashkevich V. A., Ivanova O. E., Koroleva G. A., Hinkkanen A. E., Ilonen J. 2005; Recombination in circulating human enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 86:3281–3290 [View Article][PubMed]
    [Google Scholar]
  28. Lukashev A. N., Ivanova O. E., Eremeeva T. P., Gmyl L. V. 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 [View Article][PubMed]
    [Google Scholar]
  29. Martín J., Dunn G., Hull R., Patel V., Minor P. D. 2000; Evolution of the Sabin strain of type 3 poliovirus in an immunodeficient patient during the entire 637-day period of virus excretion. J Virol 74:3001–3010 [View Article][PubMed]
    [Google Scholar]
  30. McMinn P., Stratov I., Nagarajan L., Davis S. 2001; Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clin Infect Dis 32:236–242 [View Article][PubMed]
    [Google Scholar]
  31. McWilliam Leitch E. C., Bendig J., Cabrerizo M., Cardosa J., Hyypiä T., Ivanova O. E., Kelly A., Kroes A. C. M., Lukashev A.& other authors ( 2009; Transmission networks and population turnover of echovirus 30. J Virol 83:2109–2118 [View Article][PubMed]
    [Google Scholar]
  32. McWilliam Leitch E. C., Cabrerizo M., Cardosa J., Harvala H., Ivanova O. E., Kroes A. C. M., Lukashev A., Muir P., Odoom J.& other authors ( 2010; Evolutionary dynamics and temporal/geographical correlates of recombination in the human enterovirus echovirus types 9, 11, and 30. J Virol 84:9292–9300 [View Article][PubMed]
    [Google Scholar]
  33. Murray K. E., Steil B. P., Roberts A. W., Barton D. J. 2004; Replication of poliovirus RNA with complete internal ribosome entry site deletions. J Virol 78:1393–1402 [View Article][PubMed]
    [Google Scholar]
  34. Nicholson R., Pelletier J., Le S. Y., Sonenberg N. 1991; Structural and functional analysis of the ribosome landing pad of poliovirus type 2: in vivo translation studies. J Virol 65:5886–5894[PubMed]
    [Google Scholar]
  35. Norder H., Bjerregaard L., Magnius L., Lina B., Aymard M., Chomel J. J. 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 [View Article][PubMed]
    [Google Scholar]
  36. Oberste M. S., Maher K., Kennett M. L., Campbell J. J., Carpenter M. S., Schnurr D., Pallansch M. A. 1999a; Molecular epidemiology and genetic diversity of echovirus type 30 (E30): genotypes correlate with temporal dynamics of E30 isolation. J Clin Microbiol 37:3928–3933[PubMed]
    [Google Scholar]
  37. Oberste M. S., Maher K., Kilpatrick D. R., Pallansch M. A. 1999b; Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73:1941–1948[PubMed]
    [Google Scholar]
  38. Oberste M. S., Nix W. A., Kilpatrick D. R., Flemister M. R., Pallansch M. A. 2003; Molecular epidemiology and type-specific detection of echovirus 11 isolates from the Americas, Europe, Africa, Australia, southern Asia and the Middle East. Virus Res 91:241–248 [View Article][PubMed]
    [Google Scholar]
  39. Oberste M. S., Maher K., Pallansch M. A. 2004a; Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78:855–867 [View Article][PubMed]
    [Google Scholar]
  40. Oberste M. S., Michele S. M., Maher K., Schnurr D., Cisterna D., Junttila N., Uddin M., Chomel J. J., Lau C. S.& other authors ( 2004b; Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. J Gen Virol 85:3205–3212 [View Article][PubMed]
    [Google Scholar]
  41. Oberste M. S., Peñaranda S., Maher K., Pallansch M. A. 2004c; Complete genome sequences of all members of the species human enterovirus A. J Gen Virol 85:1597–1607 [View Article][PubMed]
    [Google Scholar]
  42. Oberste M. S., Peñaranda S., Pallansch M. A. 2004d; RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 78:2948–2955 [View Article][PubMed]
    [Google Scholar]
  43. Oberste M. S., Maher K., Williams A. J., Dybdahl-Sissoko N., Brown B. A., Gookin M. S., Peñaranda S., Mishrik N., Uddin M., Pallansch M. A. 2006; Species-specific RT-PCR amplification of human enteroviruses: a tool for rapid species identification of uncharacterized enteroviruses. J Gen Virol 87:119–128 [View Article][PubMed]
    [Google Scholar]
  44. Paananen A., Savolainen-Kopra C., Kaijalainen S., Vaarala O., Hovi T., Roivainen M. 2007; Genetic and phenotypic diversity of echovirus 30 strains and pathogenesis of type 1 diabetes. J Med Virol 79:945–955 [View Article][PubMed]
    [Google Scholar]
  45. Palacios G., Casas I., Cisterna D., Trallero G., Tenorio A., Freire C. 2002; Molecular epidemiology of echovirus 30: temporal circulation and prevalence of single lineages. J Virol 76:4940–4949 [View Article][PubMed]
    [Google Scholar]
  46. Pallansch M., Roos R. 2007; Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Fields Virology, 5th edn. pp. 839–894 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus S. E. Philadelphia, PA: Lippincott Williams &Wilkins;
    [Google Scholar]
  47. Pöyry T., Kinnunen L., Hyypiä T., Brown B., Horsnell C., Hovi T., Stanway G. 1996; Genetic and phylogenetic clustering of enteroviruses. J Gen Virol 77:1699–1717 [View Article][PubMed]
    [Google Scholar]
  48. Rezig D., Ben Yahia A., Ben Abdallah H., Bahri O., Triki H. 2004; Molecular characterization of coxsackievirus B5 isolates. J Med Virol 72:268–274 [View Article][PubMed]
    [Google Scholar]
  49. Roivainen M., Piirainen L., Hovi T., Virtanen I., Riikonen T., Heino J., Hyypiä T. 1994; Entry of coxsackievirus A9 into host cells: specific interactions with α v β 3 integrin, the vitronectin receptor. Virology 203:357–365 [View Article][PubMed]
    [Google Scholar]
  50. Rossmann M. G., Arnold E., Erickson J. W., Frankenberger E. A., Griffith J. P., Hecht H.-J., Johnson J. E., Kamer G., Luo M.& other authors ( 1985; Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317:145–153 [View Article][PubMed]
    [Google Scholar]
  51. Sane F., Caloone D., Gmyr V., Engelmann I., Belaich S., Kerr-Conte J., Pattou F., Desailloud R., Hober D. 2013; Coxsackievirus B4 can infect human pancreas ductal cells and persist in ductal-like cell cultures which results in inhibition of Pdx1 expression and disturbed formation of islet-like cell aggregates. Cell Mol Life Sci 70:4169–4180 [View Article][PubMed]
    [Google Scholar]
  52. Santti J., Hyypiä T., Kinnunen L., Salminen M. 1999; Evidence of recombination among enteroviruses. J Virol 73:8741–8749[PubMed]
    [Google Scholar]
  53. Shiroki K., Ishii T., Aoki T., Ota Y., Yang W. X., Komatsu T., Ami Y., Arita M., Abe S.& other authors ( 1997; Host range phenotype induced by mutations in the internal ribosomal entry site of poliovirus RNA. J Virol 71:1–8[PubMed]
    [Google Scholar]
  54. Siafakas N., Papaventsis D., Levidiotou-Stefanou S., Vamvakopoulos N. C., Markoulatos P. 2005; Classification and structure of echovirus 5′-UTR sequences. Virus Genes 31:293–306 [View Article][PubMed]
    [Google Scholar]
  55. Simmonds P., Welch J. 2006; Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80:483–493 [View Article][PubMed]
    [Google Scholar]
  56. Stuart A. D., McKee T. A., Williams P. A., Harley C., Shen S., Stuart D. I., Brown T. D., Lea S. M. 2002; Determination of the structure of a decay accelerating factor-binding clinical isolate of echovirus 11 allows mapping of mutants with altered receptor requirements for infection. J Virol 76:7694–7704 [View Article][PubMed]
    [Google Scholar]
  57. Takeda N., Tanimura M., Miyamura K. 1994; Molecular evolution of the major capsid protein VP1 of enterovirus 70. J Virol 68:854–862[PubMed]
    [Google Scholar]
  58. Tam P. E., Weber-Sanders M. L., Messner R. P. 2003; Multiple viral determinants mediate myopathogenicity in coxsackievirus B1-induced chronic inflammatory myopathy. J Virol 77:11849–11854 [View Article][PubMed]
    [Google Scholar]
  59. Tracy S., Chapman N. M., Drescher K. M., Kono K., Tapprich W. 2006; Evolution of virulence in picornaviruses. Curr Top Microbiol Immunol 299:193–209[PubMed]
    [Google Scholar]
  60. Tu Z., Chapman N. M., Hufnagel G., Tracy S., Romero J. R., Barry W. H., Zhao L., Currey K., Shapiro B. 1995; The cardiovirulent phenotype of coxsackievirus B3 is determined at a single site in the genomic 5′ nontranslated region. J Virol 69:4607–4618[PubMed]
    [Google Scholar]
  61. Wikswo M. E., Khetsuriani N., Fowlkes A. L., Zheng X., Peñaranda S., Verma N., Shulman S. T., Sircar K., Robinson C. C.& other authors ( 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 [View Article][PubMed]
    [Google Scholar]
  62. Williams C. H., Kajander T., Hyypiä T., Jackson T., Sheppard D., Stanway G. 2004; Integrin α v β 6 is an RGD-dependent receptor for coxsackievirus A9. J Virol 78:6967–6973 [View Article][PubMed]
    [Google Scholar]
  63. Willian S., Tracy S., Chapman N., Leser S., Romero J., Shapiro B., Currey K. 2000; Mutations in a conserved enteroviral RNA oligonucleotide sequence affect positive strand viral RNA synthesis. Arch Virol 145:2061–2086 [View Article][PubMed]
    [Google Scholar]
  64. Yin H., Berg A.-K., Westman J., Hellerström C., Frisk G. 2002; Complete nucleotide sequence of a coxsackievirus B-4 strain capable of establishing persistent infection in human pancreatic islet cells: effects on insulin release, proinsulin synthesis, and cell morphology. J Med Virol 68:544–557 [View Article][PubMed]
    [Google Scholar]
  65. Zhang T., Du J., Xue Y., Su H., Yang F., Jin Q. 2013; Epidemics and frequent recombination within species in outbreaks of human enterovirus B-associated hand, foot and mouth disease in Shandong China in 2010 and 2011. PLoS ONE 8:e67157 [View Article][PubMed]
    [Google Scholar]
  66. Zhao Y. N., Perlin D. S., Park S., Jiang R. J., Chen L., Chen Y., Gardiner R., Jiang Q. W. 2006; FDJS03 isolates causing an outbreak of aseptic meningitis in China that evolved from a distinct echovirus 30 lineage imported from countries of the Commonwealth of Independent States. J Clin Microbiol 44:4142–4148 [View Article][PubMed]
    [Google Scholar]
  67. Zhou F., Kong F., McPhie K., Ratnamohan M., Donovan L., Zeng F., Gilbert G. L., Dwyer D. E. 2009; Identification of 20 common human enterovirus serotypes by use of a reverse transcription-PCR-based reverse line blot hybridization assay. J Clin Microbiol 47:2737–2743 [View Article][PubMed]
    [Google Scholar]
  68. Zhou F., Kong F., McPhie K., Ratnamohan M., Gilbert G. L., Dwyer D. E. 2010; Molecular identification and analysis of nonserotypeable human enteroviruses. J Clin Microbiol 48:1276–1282 [View Article][PubMed]
    [Google Scholar]
  69. Zhou F., Kong F., Wang B., McPhie K., Gilbert G. L., Dwyer D. E. 2011; Molecular characterization of enterovirus 71 and coxsackievirus A16 using the 5′ untranslated region and VP1 region. J Med Microbiol 60:349–358 [View Article][PubMed]
    [Google Scholar]
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