Molecular characterization of human rhinovirus field strains isolated during surveillance of enteroviruses

Journal of General Virology

Volumn 90, Issue 6, 2009, Pages 1371-1381

  Blomqvist, Soile ^a   Savolainen Kopra, Carita ^a   Paananen, Anja ^a   Hovi, Tapani ^a   Roivainen, Merja ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; LOW DENSITY LIPOPROTEIN RECEPTOR; PROTEIN VP1; PROTEIN VP2; PROTEIN VP4; VIRUS PROTEIN; VIRUS RNA;

AMINO ACID ANALYSIS; ARTICLE; AUSTRALIA; CONTROLLED STUDY; ENTEROVIRUS; FINLAND; GEOGRAPHIC DISTRIBUTION; HUMAN RHINOVIRUS; JAPAN; LATVIA; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SLOVAKIA; STRAIN DIFFERENCE; STRAIN IDENTIFICATION; UNITED STATES; VIRUS ISOLATION; 5' UNTRANSLATED REGION; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETIC RECOMBINATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; RHINOVIRUS;

ENTEROVIRUS; HUMAN RHINOVIRUS SP.; MIRIDAE;

5' UNTRANSLATED REGIONS; CLUSTER ANALYSIS; ENVIRONMENTAL MICROBIOLOGY; EVOLUTION, MOLECULAR; FINLAND; HUMANS; LATVIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECOMBINATION, GENETIC; RHINOVIRUS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SLOVAKIA; VIRAL NONSTRUCTURAL PROTEINS; VIRAL STRUCTURAL PROTEINS;

EID: 67649227467     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.008508-0     Document Type: Article

References (77)

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.
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.
3. Blomqvist, S., Savolainen, C., Raoman, 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.
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.
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.
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.
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.
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.
9. Cooney, M. K., Fox, J. P. & Kenny, G. E. (1982). Antigenic groupings of 90 rhinovirus serotypes. Infect Immun 37, 642-647.
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.
12. Gern, J. E. (2002). Rhinovirus respiratory infections and asthma. Am J Med 112, 19S-27S.
13. Greenberg, S. B. (2002). Viral respiratory infections in elderly patients and patients with chronic obstructive pulmonary disease. Am J Med 112, 28S-32S.
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.
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.
16. Gwaltney, J. M., Jr & Hendley, J. O. (1982). Transmission of experimental rhinovirus infection by contaminated surfaces. Am J Epidemiol 116, 828-833.
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.
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.
19. Hayden, F. G. (2004). Rhinovirus and the lower respiratory tract. Rev Med Virol 14, 17-31.
20. Hendley, J. O. & Gwaltney, J. M., Jr (1988). Mechanisms of transmission of rhinovirus infections. Epidemiol Rev 10, 243-258.
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.
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.
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.
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.
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.
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.
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.
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). Panviral 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
40. Marlovits, T. C., Abrahamsberg, C. & Blaas, D. (1998). Very-lowdensity lipoprotein receptor fragment shed from HeLa cells inhibits human rhinovirus infection. J Virol 72, 10246-10250.
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.
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.
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.
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.
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.
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.
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.
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.
49. Papadopoulos, N. G. (2004). Do rhinoviruses cause pneumonia in children? Paediatr Respir Rev 5, S191-S195.
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.
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.
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.
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.
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.
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.
56. Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
57. Santti, J., Hyypia, T., Kinnunen, L. & Salminen, M. (1999). Evidence of recombination among enteroviruses. J Virol 73, 8741-8749.
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.
59. Savolainen, C., Mulders, M. N. & Hovi, T. (2002b). Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons. Virus Res 85, 41-46.
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.
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.
62. Simmonds, P. & Welch, J. (2006). Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80, 483-493.
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.
64. Stott, E. J. (1969). Rhinovirus infections in Glasgow in 1962-66. Bull World Health Organ 41, 947-952.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.