1887

Abstract

Human rhinoviruses (HRVs), which are the most frequent causative agents of acute upper respiratory tract infections, are abundant worldwide. We have identified HRV strains in environmental specimens collected in Finland, Latvia and Slovakia during the surveillance of polio- and other enteroviruses. These acid-sensitive HRV strains were isolated under conditions optimized for growth of most of the enteroviruses, i.e. in stationary human rhabdomyosarcoma cells incubated at 36 °C. Phylogenetic analysis of the sequences derived from the partial 5′ non-coding region and the capsid region coding for proteins VP4/VP2 and VP1 showed that the HRV field strains clustered together with prototype strains of the HRV minor receptor group. Partial sequences of the 3D polymerase coding region generally followed this pattern, with the exception of a set of three HRV field strains that formed a subcluster not close to any of the established HRV-A types, suggesting that recombination may have occurred during evolution of these HRV strains. Phylogenetic analysis of the VP4/VP2 capsid protein coding region showed that the ‘environmental’ HRV field strains were practically identical to HRV strains recently sequenced by others in Australia, the United States and Japan. Analysis of amino acids corresponding to the intercellular adhesion molecule-1 receptor footprint in major receptor group HRVs and also in the low-density lipoprotein receptor footprint of minor receptor group HRVs showed conservation of the ‘minor receptor group-like’ amino acids, indicating that the field strains may have maintained their minor receptor group specificity.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.008508-0
2009-06-01
2019-11-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/6/1371.html?itemId=/content/journal/jgv/10.1099/vir.0.008508-0&mimeType=html&fmt=ahah

References

  1. Arden, K. E., McErlean, P., Nissen, M. D., Sloots, T. P. & Mackay, I. M. ( 2006; ). Frequent detection of human rhinoviruses, paramyxoviruses, coronaviruses, and bocavirus during acute respiratory tract infections. J Med Virol 78, 1232–1240.[CrossRef]
    [Google Scholar]
  2. Blomqvist, S., Skyttä, A., Roivainen, M. & Hovi, T. ( 1999; ). Rapid detection of human rhinoviruses in nasopharyngeal aspirates by a microwell reverse transcription-PCR-hybridization assay. J Clin Microbiol 37, 2813–2816.
    [Google Scholar]
  3. Blomqvist, S., Savolainen, C., Råman, L., Roivainen, M. & Hovi, T. ( 2002; ). Human rhinovirus 87 and enterovirus 68 represent a unique serotype with rhinovirus and enterovirus features. J Clin Microbiol 40, 4218–4223.[CrossRef]
    [Google Scholar]
  4. Blomqvist, S., Bruu, A. L., Stenvik, M. & Hovi, T. ( 2003; ). Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J Gen Virol 84, 573–580.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  6. Brown, B., 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]
  7. Cernakova, B., Sobotova, Z., Rovny, I., Blahova, S., Roivainen, M. & Hovi, T. ( 2005; ). Isolation of vaccine-derived polioviruses in the Slovak Republic. Eur J Clin Microbiol Infect Dis 24, 438–439.[CrossRef]
    [Google Scholar]
  8. Cooney, M. K., Kenny, G. E., Tam, R. & Fox, J. P. ( 1973; ). Cross relationships among 37 rhinoviruses demonstrated by virus neutralization with potent monotypic rabbit antisera. Infect Immun 7, 335–340.
    [Google Scholar]
  9. Cooney, M. K., Fox, J. P. & Kenny, G. E. ( 1982; ). Antigenic groupings of 90 rhinovirus serotypes. Infect Immun 37, 642–647.
    [Google Scholar]
  10. Couch, R. ( 1991; ). Rhinoviruses. In Laboratory Diagnosis of Viral Infections, pp. 709–729. Edited by E. H. Lennette. New York: Marcel Dekker.
  11. Fox, J. P., Cooney, M. K. & Hall, C. E. ( 1975; ). The Seattle virus watch. V. Epidemiologic observations of rhinovirus infections, 1965–1969, in families with young children. Am J Epidemiol 101, 122–143.
    [Google Scholar]
  12. Gern, J. E. ( 2002; ). Rhinovirus respiratory infections and asthma. Am J Med 112, 19S–27S.
    [Google Scholar]
  13. Greenberg, S. B. ( 2002; ). Viral respiratory infections in elderly patients and patients with chronic obstructive pulmonary disease. Am J Med 112, 28S–32S.[CrossRef]
    [Google Scholar]
  14. Greve, J. M., Davis, G., Meyer, A. M., Forte, C. P., Yost, S. C., Marlor, C. W., Kamarck, M. E. & McClelland, A. ( 1989; ). The major human rhinovirus receptor is ICAM-1. Cell 56, 839–847.[CrossRef]
    [Google Scholar]
  15. Gruenberger, M., Wandl, R., Nimpf, J., Hiesberger, T., Schneider, W. J., Kuechler, E. & Blaas, D. ( 1995; ). Avian homologs of the mammalian low-density lipoprotein receptor family bind minor receptor group human rhinovirus. J Virol 69, 7244–7247.
    [Google Scholar]
  16. Gwaltney, J. M., Jr & Hendley, J. O. ( 1982; ). Transmission of experimental rhinovirus infection by contaminated surfaces. Am J Epidemiol 116, 828–833.
    [Google Scholar]
  17. Gwaltney, J. M., Jr, Hendley, J. O., Simon, G. & Jordan, W. S., Jr ( 1968; ). Rhinovirus infections in an industrial population. 3. Number and prevalence of serotypes. Am J Epidemiol 87, 158–166.
    [Google Scholar]
  18. Hamparian, V. V., Colonno, R. J., Cooney, M. K., Dick, E. C., Gwaltney, J. M., Jr, Hughes, J. H., Jordan, W. S., Jr, Kapikian, A. Z., Mogabgab, W. J. & other authors ( 1987; ). A collaborative report: rhinoviruses – extension of the numbering system from 89 to 100. Virology 159, 191–192.[CrossRef]
    [Google Scholar]
  19. Hayden, F. G. ( 2004; ). Rhinovirus and the lower respiratory tract. Rev Med Virol 14, 17–31.[CrossRef]
    [Google Scholar]
  20. Hendley, J. O. & Gwaltney, J. M., Jr ( 1988; ). Mechanisms of transmission of rhinovirus infections. Epidemiol Rev 10, 243–258.
    [Google Scholar]
  21. Hendley, J. O., Wenzel, R. P. & Gwaltney, J. M., Jr ( 1973; ). Transmission of rhinovirus colds by self-inoculation. N Engl J Med 288, 1361–1364.[CrossRef]
    [Google Scholar]
  22. Hillis, D. M. & Bull, J. J. ( 1993; ). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42, 182–192.[CrossRef]
    [Google Scholar]
  23. Hofer, F., Gruenberger, M., Kowalski, H., Machat, H., Huettinger, M., Kuechler, E. & Blass, D. ( 1994; ). Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Natl Acad Sci U S A 91, 1839–1842.[CrossRef]
    [Google Scholar]
  24. 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]
  25. Kapikian, A. Z., Conant, R. M., Hamparian, V. V., Chanock, R. M., Chapple, P. J., Dick, E. C., Fenters, J. D., Gwaltney, J. M., Jr, Hamre, D. & other authors ( 1967; ). Rhinoviruses: a numbering system. Nature 213, 761-–763.[CrossRef]
    [Google Scholar]
  26. Kapikian, A. Z., Conant, R. M., Hamparian, V. V., Chanock, R. M., Dick, E. C., Gwaltney, J. M., Jr, Hamre, D., Jordan, W. S., Jr, Kenny, G. E. & other authors ( 1971; ). A collaborative report: rhinoviruses – extension of the numbering system. Virology 43, 524–526.[CrossRef]
    [Google Scholar]
  27. Khan, A. G., Pichler, J., Rosemann, A. & Blaas, D. ( 2007; ). Human rhinovirus type 54 infection via heparan sulfate is less efficient and strictly dependent on low endosomal pH. J Virol 81, 4625–4632.[CrossRef]
    [Google Scholar]
  28. Kistler, A., Avila, P. C., Rouskin, S., Wang, D., Ward, T., Yagi, S., Schnurr, D., Ganem, D., DeRisi, J. L. & Boushey, H. A. ( 2007a; ). Pan-viral screening of respiratory tract infections in adults with and without asthma reveals unexpected human coronavirus and human rhinovirus diversity. J Infect Dis 196, 817–825.[CrossRef]
    [Google Scholar]
  29. Kistler, A. L., Webster, D. R., Rouskin, S., Magrini, V., Credle, J. J., Schnurr, D. P., Boushey, H. A., Mardis, E. R., Li, H. & DeRisi, J. L. ( 2007b; ). Genome-wide diversity and selective pressure in the human rhinovirus. Virol J 4, 40 [CrossRef]
    [Google Scholar]
  30. Knowles, N. J. ( 2008; ). The picornavirus home page. http://www.picornaviridae.com/
  31. Kolatkar, P. R., Bella, J., Olson, N. H., Bator, C. M., Baker, T. S. & Rossmann, M. G. ( 1999; ). Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J 18, 6249–6259.[CrossRef]
    [Google Scholar]
  32. Laine, P., Savolainen, C., Blomqvist, S. & Hovi, T. ( 2005; ). Phylogenetic analysis of human rhinovirus capsid protein VP1 and 2A protease coding sequences confirms shared genus-like relationships with human enteroviruses. J Gen Virol 86, 697–706.[CrossRef]
    [Google Scholar]
  33. Laine, P., Blomqvist, S., Savolainen, C., Andries, K. & Hovi, T. ( 2006; ). Alignment of capsid protein VP1 sequences of all human rhinovirus prototype strains: conserved motifs and functional domains. J Gen Virol 87, 129–138.[CrossRef]
    [Google Scholar]
  34. Lamson, D., Renwick, N., Kapoor, V., Liu, Z., Palacios, G., Ju, J., Dean, A., St George, K., Briese, T. & Lipkin, W. I. ( 2006; ). MassTag polymerase-chain-reaction detection of respiratory pathogens, including a new rhinovirus genotype, that caused influenza-like illness in New York State during 2004–2005. J Infect Dis 194, 1398–1402.[CrossRef]
    [Google Scholar]
  35. Lau, S. K., Yip, C. C., Tsoi, H. W., Lee, R. A., So, L. Y., Lau, Y. L., Chan, K. H., Woo, P. C. & Yuen, K. Y. ( 2007; ). Clinical features and complete genome characterization of a distinct human rhinovirus (HRV) genetic cluster, probably representing a previously undetected HRV species, HRV-C, associated with acute respiratory illness in children. J Clin Microbiol 45, 3655–3664.[CrossRef]
    [Google Scholar]
  36. Ledford, R. M., Patel, N. R., Demenczuk, T. M., Watanyar, A., Herbertz, T., Collett, M. S. & Pevear, D. C. ( 2004; ). VP1 sequencing of all human rhinovirus serotypes: insights into genus phylogeny and susceptibility to antiviral capsid-binding compounds. J Virol 78, 3663–3674.[CrossRef]
    [Google Scholar]
  37. Lee, W. M., Kiesner, C., Pappas, T., Lee, I., Grindle, K., Jartti, T., Jakiela, B., Lemanske, R. F., Jr, Shult, P. A. & Gern, J. E. ( 2007; ). A diverse group of previously unrecognized human rhinoviruses are common causes of respiratory illnesses in infants. PLoS One 2, e966 [CrossRef]
    [Google Scholar]
  38. 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]
  39. Lu, X., Holloway, B., Dare, R. K., Kuypers, J., Yagi, S., Williams, J. V., Hall, C. B. & Erdman, D. D. ( 2008; ). Real-time reverse transcription-PCR assay for comprehensive detection of human rhinoviruses. J Clin Microbiol 46, 533–539.[CrossRef]
    [Google Scholar]
  40. Marlovits, T. C., Abrahamsberg, C. & Blaas, D. ( 1998; ). Very-low-density lipoprotein receptor fragment shed from HeLa cells inhibits human rhinovirus infection. J Virol 72, 10246–10250.
    [Google Scholar]
  41. Martin, J., Samoilovich, E., Dunn, G., Lackenby, A., Feldman, E., Heath, A., Svirchevskaya, E., Cooper, G., Yermalovich, M. & Minor, P. D. ( 2002; ). Isolation of an intertypic poliovirus capsid recombinant from a child with vaccine-associated paralytic poliomyelitis. J Virol 76, 10921–10928.[CrossRef]
    [Google Scholar]
  42. McErlean, P., Shackelton, L. A., Lambert, S. B., Nissen, M. D., Sloots, T. P. & Mackay, I. M. ( 2007; ). Characterisation of a newly identified human rhinovirus, HRV-QPM, discovered in infants with bronchiolitis. J Clin Virol 39, 67–75.[CrossRef]
    [Google Scholar]
  43. Monto, A. S. & Cavallaro, J. J. ( 1972; ). The Tecumseh study of respiratory illness. IV. Prevalence of rhinovirus serotypes, 1966–1969. Am J Epidemiol 96, 352–360.
    [Google Scholar]
  44. Mosser, A. G., Brockman-Schneider, R., Amineva, S., Burchell, L., Sedgwick, J. B., Busse, W. W. & Gern, J. E. ( 2002; ). Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J Infect Dis 185, 734–743.[CrossRef]
    [Google Scholar]
  45. Nokso-Koivisto, J., Raty, R., Blomqvist, S., Kleemola, M., Syrjanen, R., Pitkaranta, A., Kilpi, T. & Hovi, T. ( 2004; ). Presence of specific viruses in the middle ear fluids and respiratory secretions of young children with acute otitis media. J Med Virol 72, 241–248.[CrossRef]
    [Google Scholar]
  46. 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]
  47. Oberste, M. S., Nix, W. A., Maher, K. & Pallansch, M. A. ( 2003; ). Improved molecular identification of enteroviruses by RT-PCR and amplicon sequencing. J Clin Virol 26, 375–377.[CrossRef]
    [Google Scholar]
  48. Oberste, M. S., Maher, K., Schnurr, D., Flemister, M. R., Lovchik, J. C., Peters, H., Sessions, W., Kirk, C., Chatterjee, N. & other authors ( 2004; ). 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]
  49. Papadopoulos, N. G. ( 2004; ). Do rhinoviruses cause pneumonia in children? Paediatr Respir Rev 5, S191–S195.[CrossRef]
    [Google Scholar]
  50. Papadopoulos, N. G., Sanderson, G., Hunter, J. & Johnston, S. L. ( 1999; ). Rhinoviruses replicate effectively at lower airway temperatures. J Med Virol 58, 100–104.[CrossRef]
    [Google Scholar]
  51. Peltola, V., Waris, M., Osterback, R., Susi, P., Ruuskanen, O. & Hyypia, T. ( 2008; ). Rhinovirus transmission within families with children: incidence of symptomatic and asymptomatic infections. J Infect Dis 197, 382–389.[CrossRef]
    [Google Scholar]
  52. Pitkaranta, A., Arruda, E., Malmberg, H. & Hayden, F. G. ( 1997; ). Detection of rhinovirus in sinus brushings of patients with acute community-acquired sinusitis by reverse transcription-PCR. J Clin Microbiol 35, 1791–1793.
    [Google Scholar]
  53. Pitkaranta, A., Virolainen, A., Jero, J., Arruda, E. & Hayden, F. G. ( 1998; ). Detection of rhinovirus, respiratory syncytial virus, and coronavirus infections in acute otitis media by reverse transcriptase polymerase chain reaction. Pediatrics 102, 291–295.[CrossRef]
    [Google Scholar]
  54. Pitkaranta, A., Starck, M., Savolainen, S., Poyry, T., Suomalainen, I., Hyypia, T., Carpen, O. & Vaheri, A. ( 2001; ). Rhinovirus RNA in the maxillary sinus epithelium of adult patients with acute sinusitis. Clin Infect Dis 33, 909–911.[CrossRef]
    [Google Scholar]
  55. Puro, V., Minosse, C., Cappiello, G., Lauria, F. N. & Capobianchi, M. R. ( 2005; ). Rhinovirus and lower respiratory tract infection in adults. Clin Infect Dis 40, 1068–1069.[CrossRef]
    [Google Scholar]
  56. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  57. Santti, J., Hyypia, T., Kinnunen, L. & Salminen, M. ( 1999; ). Evidence of recombination among enteroviruses. J Virol 73, 8741–8749.
    [Google Scholar]
  58. Savolainen, C., Blomqvist, S., Mulders, M. N. & Hovi, T. ( 2002a; ). Genetic clustering of all 102 human rhinovirus prototype strains: serotype 87 is close to human enterovirus 70. J Gen Virol 83, 333–340.
    [Google Scholar]
  59. Savolainen, C., Mulders, M. N. & Hovi, T. ( 2002b; ). Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons. Virus Res 85, 41–46.[CrossRef]
    [Google Scholar]
  60. Savolainen, C., Laine, P., Mulders, M. N. & Hovi, T. ( 2004; ). Sequence analysis of human rhinoviruses in the RNA-dependent RNA polymerase coding region reveals large within-species variation. J Gen Virol 85, 2271–2277.[CrossRef]
    [Google Scholar]
  61. Savolainen-Kopra, C., Blomqvist, S., Kilpi, T., Roivainen, M. & Hovi, T. ( 2009; ). Novel species of human rhinoviruses in acute otitis media. Pediatr Infect Dis J 28, 59–61.[CrossRef]
    [Google Scholar]
  62. Simmonds, P. & Welch, J. ( 2006; ). Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80, 483–493.[CrossRef]
    [Google Scholar]
  63. Staunton, D. E., Merluzzi, V. J., Rothlein, R., Barton, R., Marlin, S. D. & Springer, T. A. ( 1989; ). A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56, 849–853.[CrossRef]
    [Google Scholar]
  64. Stott, E. J. ( 1969; ). Rhinovirus infections in Glasgow in 1962–66. Bull World Health Organ 41, 947–952.
    [Google Scholar]
  65. Tamura, K., Nei, M. & Kumar, S. ( 2004; ). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101, 11030–11035.[CrossRef]
    [Google Scholar]
  66. 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.[CrossRef]
    [Google Scholar]
  67. Tapparel, C., Junier, T., Gerlach, D., Cordey, S., Van Belle, S., Perrin, L., Zdobnov, E. M. & Kaiser, L. ( 2007; ). New complete genome sequences of human rhinoviruses shed light on their phylogeny and genomic features. BMC Genomics 8, 224 [CrossRef]
    [Google Scholar]
  68. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  69. Tomassini, J. E., Graham, D., DeWitt, C. M., Lineberger, D. W., Rodkey, J. A. & Colonno, R. J. ( 1989; ). cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc Natl Acad Sci U S A 86, 4907–4911.[CrossRef]
    [Google Scholar]
  70. Verdaguer, N., Fita, I., Reithmayer, M., Moser, R. & Blaas, D. ( 2004; ). X-ray structure of a minor group human rhinovirus bound to a fragment of its cellular receptor protein. Nat Struct Mol Biol 11, 429–434.[CrossRef]
    [Google Scholar]
  71. Vesa, S., Kleemola, M., Blomqvist, S., Takala, A., Kilpi, T. & Hovi, T. ( 2001; ). Epidemiology of documented viral respiratory infections and acute otitis media in a cohort of children followed from two to twenty-four months of age. Pediatr Infect Dis J 20, 574–581.[CrossRef]
    [Google Scholar]
  72. Vlasak, M., Blomqvist, S., Hovi, T., Hewat, E. & Blaas, D. ( 2003; ). Sequence and structure of human rhinoviruses reveal the basis of receptor discrimination. J Virol 77, 6923–6930.[CrossRef]
    [Google Scholar]
  73. Vlasak, M., Goesler, I. & Blaas, D. ( 2005a; ). Human rhinovirus type 89 variants use heparan sulfate proteoglycan for cell attachment. J Virol 79, 5963–5970.[CrossRef]
    [Google Scholar]
  74. Vlasak, M., Roivainen, M., Reithmayer, M., Goesler, I., Laine, P., Snyers, L., Hovi, T. & Blaas, D. ( 2005b; ). The minor receptor group of human rhinovirus (HRV) includes HRV23 and HRV25, but the presence of a lysine in the VP1 HI loop is not sufficient for receptor binding. J Virol 79, 7389–7395.[CrossRef]
    [Google Scholar]
  75. WHO ( 2003; ). Guidelines for Environmental Surveillance of Poliovirus Circulation. Geneva, Switzerland: World Health Organization.
  76. WHO ( 2004; ). Polio Laboratory Manual. Geneva, Switzerland: World Health Organization.
  77. Winther, B., McCue, K., Ashe, K., Rubino, J. R. & Hendley, J. O. ( 2007; ). Environmental contamination with rhinovirus and transfer to fingers of healthy individuals by daily life activity. J Med Virol 79, 1606–1610.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.008508-0
Loading
/content/journal/jgv/10.1099/vir.0.008508-0
Loading

Data & Media loading...

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