1887

Abstract

The 65 serotypes of human enteroviruses are classified into four species, (HEV) A to D, based largely on phylogenetic relationships in multiple genome regions. The 3′-non-translated region of enteroviruses is highly conserved within a species but highly divergent between species. From this information, species-specific RT-PCR primers were developed that can be used to rapidly screen collections of enterovirus isolates to identify species of interest. The four primer pairs were 100 % specific when tested against enterovirus prototype strains and panels of isolates of known serotype (a total of 193 isolates). For evaluation in a typical application, the species-specific primers were used to screen 186 previously uncharacterized non-polio enterovirus isolates. The HEV-B primers amplified 68·3 % of isolates, while the HEV-A and HEV-C primers accounted for 9·7 and 11·3 % of isolates, respectively; no isolates were amplified with the HEV-D primers. Twelve isolates (6·5 %) were amplified by more than one primer set and eight isolates (4·3 %) were not amplified by any of the four primer pairs. Serotypes were identified by partial sequencing of the VP1 capsid gene, and in every case sequencing confirmed that the species-specific PCR result was correct; the isolates that were amplified by more than one species-specific primer pair were mixtures of two (11 isolates) or three (one isolate) species of viruses. The eight isolates that were not amplified by the species-specific primers comprised four new serotypes (EV76, EV89, EV90 and EV91) that appear to be unique members of HEV-A based on VP1, 3D and 3′-non-translated region sequences.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81179-0
2006-01-01
2019-09-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/1/119.html?itemId=/content/journal/jgv/10.1099/vir.0.81179-0&mimeType=html&fmt=ahah

References

  1. Blomqvist, S., Savolainen, C., Raman, L., Roivainen, M. & Hovi, T. ( 2002; ). Human rhinovirus 87 and enterovirus 68 represent a unique serotype with rhinovirus and enterovirus properties. J Clin Microbiol 40, 4218–4223.[CrossRef]
    [Google Scholar]
  2. Brown, B. A., Oberste, M. S., Maher, K. & Pallansch, M. A. ( 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.[CrossRef]
    [Google Scholar]
  3. Brown, D. M., Kauder, S. E., Cornell, C. T., Jang, G. M., Racaniello, V. R. & Semler, B. L. ( 2004; ). Cell-dependent role for the poliovirus 3′ noncoding region in positive-strand RNA synthesis. J Virol 78, 1344–1351.[CrossRef]
    [Google Scholar]
  4. Centers for Disease Control & Prevention ( 1997; ). Nonpolio enterovirus surveillance – United States, 1993–1996. Morbid Mortal Wkly Rep 46, 748–750.
    [Google Scholar]
  5. Centers for Disease Control & Prevention ( 2000; ). Enterovirus surveillance – United States, 1997–1999. Morbid Mortal Wkly Rep 49, 913–916.
    [Google Scholar]
  6. Centers for Disease Control & Prevention ( 2001; ). Echovirus type 13 – United States, 2001. Morbid Mortal Wkly Rep 50, 777–780.
    [Google Scholar]
  7. Centers for Disease Control & Prevention ( 2002; ). Enterovirus surveillance – United States, 2000–2001. Morbid Mortal Wkly Rep 51, 1047–1049.
    [Google Scholar]
  8. Communicable Disease Surveillance Centre ( 2000; ). Viral meningitis associated with increase in echovirus type 13. Commun Dis Rep CDR Wkly 10, 277–280.
    [Google Scholar]
  9. Hara, M., Komatsu, T., Sasaki, M. & Tagaya, I. ( 1968; ). Lack of serological relationship of ECHO virus types 1 and 12. Proc Soc Exp Biol Med 128, 683–687.[CrossRef]
    [Google Scholar]
  10. Harris, K. S., Xiang, W., Alexander, L., Lane, W. S., Paul, A. V. & Wimmer, E. ( 1994; ). Interaction of poliovirus polypeptide 3CDpro with the 5′ and 3′ termini of the poliovirus genome. Identification of viral and cellular factors needed for efficient binding. J Biol Chem 269, 27004–27014.
    [Google Scholar]
  11. Huang, Q. S., Carr, J. M., Nix, W. A. & 7 other authors ( 2003; ). An echovirus type 33 winter outbreak in New Zealand. Clin Infect Dis 37, 650–657.[CrossRef]
    [Google Scholar]
  12. Infectious Disease Surveillance Center ( 2003; ). Yearly reports of enterovirus isolation from human sources, 1982–2002: Infectious Agents Surveillance Report. http://idsc.nih.go.jp/iasr/virus/graph/ent82002.gif.
  13. Ishiko, H., Miura, R., Shimada, Y., Hayashi, A., Nakajima, H., Yamazaki, S. & Takeda, N. ( 2002; ). Human rhinovirus 87 identified as human enterovirus 68 by VP4-based molecular diagnosis. Intervirology 45, 136–141.[CrossRef]
    [Google Scholar]
  14. Keino, M., Kanno, M., Hirasawa, K., Watari, T., Mikawa, M., Saito, K., Kato, K., Katayose, M. & Yoshida, H. ( 2001; ). Isolation of echovirus type 13 from patients of aseptic meningitis. Jpn J Infect Dis 54, 249–250.
    [Google Scholar]
  15. Kilpatrick, D. R., Nottay, B., Yang, C. F., Yang, S. J., Mulders, M. N., Holloway, B. P., Pallansch, M. A. & Kew, O. M. ( 1996; ). Group-specific identification of polioviruses by PCR using primers containing mixed-base or deoxyinosine residue at positions of codon degeneracy. J Clin Microbiol 34, 2990–2996.
    [Google Scholar]
  16. Kilpatrick, D. R., Nottay, B., Yang, C. F., Yang, S. J., Da Silva, E., Penaranda, S., Pallansch, M. & Kew, O. ( 1998; ). Serotype-specific identification of polioviruses by PCR using primers containing mixed-base or deoxyinosine residues at positions of codon degeneracy. J Clin Microbiol 36, 352–357.
    [Google Scholar]
  17. Kilpatrick, D. R., Quay, J., Pallansch, M. A. & Oberste, M. S. ( 2001; ). Molecular typing of echovirus 30 isolates using degenerate RT-PCR primers. J Clin Microbiol 39, 1299–1302.[CrossRef]
    [Google Scholar]
  18. King, A. M. Q., Brown, F., Christian, P. & 8 other authors ( 2000; ). Picornaviridae. In Virus taxonomy. Seventh report of the International Committee on Taxonomy of Viruses, pp. 657–678. Edited by M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle & R. B. Wickner. San Diego: Academic Press.
  19. Lindberg, A. M., Andersson, P., Savolainen, C., Mulders, M. N. & 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.[CrossRef]
    [Google Scholar]
  20. Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E. & Ilonen, J. ( 2003; ). Recombination in circulating enteroviruses. J Virol 77, 10423–10431.[CrossRef]
    [Google Scholar]
  21. 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.[CrossRef]
    [Google Scholar]
  22. Melchers, W. J., Hoenderop, J. G., Bruins Slot, H. J., Pleij, C. W., Pilipenko, E. V., Agol, V. I. & Galama, J. M. ( 1997; ). Kissing of the two predominant hairpin loops in the coxsackie B virus 3′ untranslated region is the essential structural feature of the origin of replication required for negative-strand RNA synthesis. J Virol 71, 686–696.
    [Google Scholar]
  23. Mellits, K. H., Meredith, J. M., Rohll, J. B., Evans, D. J. & Almond, J. W. ( 1998; ). Binding of a cellular factor to the 3′ untranslated region of the RNA genomes of entero- and rhinoviruses plays a role in virus replication. J Gen Virol 79, 1715–1723.
    [Google Scholar]
  24. Melnick, J. L., Tagaya, I. & von Magnus, H. ( 1974; ). Enteroviruses 69, 70, and 71. Intervirology 4, 369–370.
    [Google Scholar]
  25. Merkle, I., van Ooij, M. J. M., van Kuppeveld, F. J. M., Glaudemans, D. H. R. F., Galama, J. M. D., Henke, A., Zell, R. & Melchers, W. J. G. ( 2002; ). Biological significance of a human enterovirus B-specific RNA element in the 3′ nontranslated region. J Virol 76, 9900–9909.[CrossRef]
    [Google Scholar]
  26. Mirmomeni, M. H., Hughes, P. J. & Stanway, G. ( 1997; ). An RNA tertiary structure in the 3′ untranslated region of enteroviruses is necessary for efficient replication. J Virol 71, 2363–2370.
    [Google Scholar]
  27. Mullins, J. A., Khetsuriani, N., Nix, W. A. & 10 other authors ( 2004; ). Emergence of echovirus type 13 as a prominent enterovirus. Clin Infect Dis 38, 70–77.[CrossRef]
    [Google Scholar]
  28. Nakazono, N. & Kondo, K. ( 1989; ). Virus isolation of enterovirus 70. In Acute Hemorrhagic Conjunctivitis, pp. 295–306. Edited by K. Ishii, H. Uchida, K. Miyamura & S. Yamazaki. Tokyo: University of Tokyo Press.
  29. Norder, H., Bjerregaard, L. & Magnius, L. O. ( 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.
    [Google Scholar]
  30. 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.[CrossRef]
    [Google Scholar]
  31. Oberste, M. S., Maher, K., Kilpatrick, D. R., Flemister, M. R., Brown, B. A. & Pallansch, M. A. ( 1999a; ). Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 37, 1288–1293.
    [Google Scholar]
  32. 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.
    [Google Scholar]
  33. Oberste, M. S., Maher, K., Flemister, M. R., Marchetti, G., Kilpatrick, D. R. & Pallansch, M. A. ( 2000; ). Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. J Clin Microbiol 38, 1170–1174.
    [Google Scholar]
  34. Oberste, M. S., Schnurr, D., Maher, K., al-Busaidy, S. & Pallansch, M. A. ( 2001; ). Molecular identification of new picornaviruses and characterization of a proposed enterovirus 73 serotype. J Gen Virol 82, 409–416.
    [Google Scholar]
  35. Oberste, M. S., Maher, K. & Pallansch, M. A. ( 2002; ). Molecular phylogeny and classification of the simian picornaviruses. J Virol 76, 1244–1251.[CrossRef]
    [Google Scholar]
  36. Oberste, M. S., Nix, W. A., Kilpatrick, D. R., Flemister, M. R. & Pallansch, M. A. ( 2003a; ). 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.[CrossRef]
    [Google Scholar]
  37. Oberste, M. S., Nix, W. A., Maher, K. & Pallansch, M. A. ( 2003b; ). Improved molecular identification of enteroviruses by RT-PCR and amplicon sequencing. J Clin Virol 26, 375–377.[CrossRef]
    [Google Scholar]
  38. Oberste, M. S., Maher, K. & Pallansch, M. ( 2004a; ). Evidence for frequent recombination within Human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78, 855–867.[CrossRef]
    [Google Scholar]
  39. Oberste, M. S., Maher, K., Schnurr, D. & 9 other authors ( 2004b; ). Enterovirus 68 is associated with respiratory illness and shares biological features with both the enteroviruses and the rhinoviruses. J Gen Virol 85, 2577–2584.[CrossRef]
    [Google Scholar]
  40. Oberste, M. S., Michele, S. M., Maher, K. & 11 other authors ( 2004c; ). Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. J Gen Virol 85, 3205–3212.[CrossRef]
    [Google Scholar]
  41. Oberste, M. S., Peñaranda, S., Maher, K. & Pallansch, M. A. ( 2004d; ). Complete genome sequences of all members of the species Human enterovirus A. J Gen Virol 85, 1597–1607.[CrossRef]
    [Google Scholar]
  42. Oberste, M. S., Peñaranda, S. & Pallansch, M. A. ( 2004e; ). RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 78, 2948–2955.[CrossRef]
    [Google Scholar]
  43. Oberste, M. S., Maher, K., Michele, S. M., Uddin, M., Belliot, G. & Pallansch, M. A. ( 2005; ). Enteroviruses 76, 89, 90 and 91 represent a novel group within the species Human enterovirus A. J Gen Virol 86, 445–451.[CrossRef]
    [Google Scholar]
  44. 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.
    [Google Scholar]
  45. Pilipenko, E. V., Gmyl, A. P., Maslova, S. V., Svitkin, Y. V., Sinyakov, A. N. & Agol, V. I. ( 1992a; ). Prokaryotic-like cis elements in the cap-independent internal initiation of translation on picornavirus RNA. Cell 68, 119–131.[CrossRef]
    [Google Scholar]
  46. Pilipenko, E. V., Maslova, S. V., Sinyakov, A. N. & Agol, V. I. ( 1992b; ). Towards identification of cis-acting elements involved in the replication of enterovirus and rhinovirus RNAs: a proposal for the existence of tRNA-like terminal structures. Nucleic Acids Res 20, 1739–1745.[CrossRef]
    [Google Scholar]
  47. Pilipenko, E. V., Poperechny, K. V., Maslova, S. V., Melchers, W. J., Slot, H. J. & Agol, V. I. ( 1996; ). Cis-element, oriR, involved in the initiation of (−) strand poliovirus RNA: a quasi-globular multi-domain RNA structure maintained by tertiary (‘kissing’) interactions. EMBO J 15, 5428–5436.
    [Google Scholar]
  48. Pöyry, T., Kinnunen, L., Hyypia, T., Brown, B., Horsnell, C., Hovi, T. & Stanway, G. ( 1996; ). Genetic and phylogenetic clustering of enteroviruses. J Gen Virol 77, 1699–1717.[CrossRef]
    [Google Scholar]
  49. Rohll, J. B., Moon, D. H., Evans, D. J. & Almond, J. W. ( 1995; ). The 3′ untranslated region of picornaviruses RNA: features required for efficient genome replication. J Virol 69, 7835–7844.
    [Google Scholar]
  50. Rotbart, H. A. & Romero, J. R. ( 1995; ). Laboratory diagnosis of enteroviral infections. In Human Enterovirus Infections, pp. 401–418. Edited by H. A. Rotbart. Washington, DC: ASM Press.
  51. Strikas, R. A., Anderson, L. J. & Parker, R. A. ( 1986; ). Temporal and geographic patterns of isolates of nonpolio enterovirus in the United States, 1970–1983. J Infect Dis 153, 346–351.[CrossRef]
    [Google Scholar]
  52. Twisselmann, B. ( 2000; ). Cluster of cases of viral meningitis caused by echovirus type 13 in Germany: Eurosurveillance Weekly. http://www.eurosurveillance.org/ew/2000/001005.asp#3.
  53. Yang, C.-F., De, L., Yang, S.-J., Ruiz Gómez, J., Ramiro Cruz, J., Holloway, B. P., Pallansch, M. A. & Kew, O. M. ( 1992; ). Genotype-specific in vitro amplification of sequences of the wild type 3 polioviruses from Mexico and Guatemala. Virus Res 24, 277–296.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81179-0
Loading
/content/journal/jgv/10.1099/vir.0.81179-0
Loading

Data & Media loading...

vol. , part 1, pp. 119 - 128

Identities of 186 Bangladesh non-polio enterovirus isolates screened with species-specific PCR

Amplification of 65 enterovirus reference strains and 12 simian enteroviruses using species-specific RT-PCR primers

Amplification of a panel of 115 enterovirus and rhinovirus clinical isolates of known serotype using species-specific RT-PCR primers [Single PDF file](333 KB)



PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error