Proposals for the classification of human rhinovirus species A, B and C into genotypically assigned types

Journal of General Virology

Volumn 94, Issue PART8, 2013, Pages 1791-1806

  McIntyre, Chloe L ^a   Knowles, Nick J ^b   Simmonds, Peter ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE; PROTEIN VP1; PROTEIN VP2;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; DISEASE TRANSMISSION; ENTEROVIRUS; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HUMAN RHINOVIRUS; HUMAN RHINOVIRUS A; HUMAN RHINOVIRUS B; HUMAN RHINOVIRUS C; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SEROTYPE; VIRUS ISOLATION; VIRUS REPLICATION;

CLUSTER ANALYSIS; GENOTYPE; HUMANS; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; RHINOVIRUS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS; VIROLOGY;

EID: 84880171452     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.053686-0     Document Type: Article

References (71)

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., Savolainen-Kopra, C., Paananen, A., Hovi, T. & Roivainen, M. (2009). Molecular characterization of human rhinovirus field strains isolated during surveillance of enteroviruses. J Gen Virol 90, 1371-1381.
3. Bochkov, Y. A., Palmenberg, A. C., Lee, W.-M., Rathe, J. A., Amineva, S. P., Sun, X., Pasic, T. R., Jarjour, N. N., Liggett, S. B. & Gern, J. E. (2011). Molecular modeling, organ culture and reverse genetics for a newly identified human rhinovirus C. Nat Med 17, 627-632.
4. Brown, B. A., Maher, K., Flemister, M. R., Naraghi-Arani, P., Uddin, M., Oberste, M. S. & Pallansch, M. A. (2009). Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. J Gen Virol 90, 1713-1723.
5. Cooney, M. K., Fox, J. P. & Kenny, G. E. (1982). Antigenic groupings of 90 rhinovirus serotypes. Infect Immun 37, 642-647.
6. de Vries, M., Pyrc, K., Berkhout, R., Vermeulen-Oost, W., Dijkman, R., Jebbink, M. F., Bruisten, S., Berkhout, B. & van der Hoek, L. (2008). Human parechovirus type 1, 3, 4, 5, and 6 detection in picornavirus cultures. J Clin Microbiol 46, 759-762.
7. Gaunt, E. R., Harvala, H., McIntyre, C., Templeton, K. E. & Simmonds, P. (2011). Disease burden of the most commonly detected respiratory viruses in hospitalized patients calculated using the disability adjusted life year (DALY) model. J Clin Virol 52, 215-221.
8. Gibbs, M. J., Armstrong, J. S. & Gibbs, A. J. (2000). Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16, 573-582.
9. Guindon, S. & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696-704.
10. Gutman, J. A., Peck, A. J., Kuypers, J. & Boeckh, M. (2007). Rhinovirus as a cause of fatal lower respiratory tract infection in adult stem cell transplantation patients: a report of two cases. Bone Marrow Transplant 40, 809-811.
11. 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.
12. Han, T. H., Chung, J. Y., Hwang, E. S. & Koo, J. W. (2009). Detection of human rhinovirus C in children with acute lower respiratory tract infections in South Korea. Arch Virol 154, 987-991.
13. Harvala, H., McIntyre, C. L., McLeish, N. J., Kondracka, J., Palmer, J., Molyneaux, P., Gunson, R., Bennett, S., Templeton, K. & Simmonds, P. (2012). High detection frequency and viral loads of human rhinovirus species A to C in fecal samples; diagnostic and clinical implications. J Med Virol 84, 536-542.
14. Henquell, C., Mirand, A., Deusebis, A.-L., Regagnon, C., Archimbaud, C., Chambon, M., Bailly, J.-L., Gourdon, F., Hermet, E. & other authors (2012). Prospective genotyping of human rhinoviruses in children and adults during the winter of 2009-2010. J Clin Virol 53, 280-284.
15. Hofer, F., Gruenberger, M., Kowalski, H., Machat, H., Huettinger, M., Kuechler, E. & Blaas, 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.
16. Ison, M. G., Hayden, F. G., Kaiser, L., Corey, L. & Boeckh, M. (2003). Rhinovirus infections in hematopoietic stem cell transplant recipients with pneumonia. Clin Infect Dis 36, 1139-1143.
17. Kaida, A., Kubo, H., Takakura, K., Togawa, M., Shiomi, M., Kohdera, U. & Iritani, N. (2011). Molecular epidemiology of human rhinovirus C in patients with acute respiratory tract infections in Osaka City, Japan. Jpn J Infect Dis 64, 488-492.
18. Kaiser, L., Aubert, J.-D., Pache, J.-C., Deffernez, C., Rochat, T., Garbino, J., Wunderli, W., Meylan, P., Yerly, S. & other authors (2006). Chronic rhinoviral infection in lung transplant recipients. Am J Respir Crit Care Med 174, 1392-1399.
19. Kapikian, A., Conant, R. & Hamparian, V. (1967). Rhinoviruses: a numbering system. Nature 213, 761-763.
20. Kapikian, A., Conant, R., Hamparian, V., Chanock, R., Dick, E., Gwaltney, J., Jr, Hamre, D., Jordan, W., Jr, Kenny, G. & other authors (1971). A collaborative report: rhinoviruses extension of the numbering system. Virology 43, 524-526.
21. Khetsuriani, N., Lu, X., Teague, W. G., Kazerouni, N., Anderson, L. J. & Erdman, D. D. (2008). Novel human rhinoviruses and exacerbation of asthma in children. Emerg Infect Dis 14, 1793-1796.
22. Kiang, D., Newbower, E. C., Yeh, E., Wold, L., Chen, L. & Schnurr, D. P. (2009). An algorithm for the typing of enteroviruses and correlation to serotyping by viral neutralization. J Clin Virol 45, 334-340.
23. Kilpatrick, D. R., Nottay, B., Yang, C. F., Yang, S. J., Da Silva, E., Pen ̃ aranda, 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 degen-eracy. J Clin Microbiol 36, 352-357.
24. 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.
25. 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.
26. Knowles, N. J., Hovi, T., Hyypia, T., King, A. M. Q., Lindberg, A. M., Pallansch, M. A., Palmenberg, A. C., Simmonds, P., Skern, T. & other authors (2012). Picornaviridae. In Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses, pp. 855-880. Edited by A. M. Q. King,
27. M. J. Adams, E. B. Carstens & E. J. Lefkowitz. San Diego: Elsevier. Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H. & Frost, S. D. W. (2006). GARD: a genetic algorithm for recombination detection. Bioinformatics 22, 3096-3098.
28. 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.
29. Lau, S. K. P., Yip, C. C. Y., 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.
30. 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.
31. 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.
32. Linsuwanon, P., Payungporn, S., Suwannakarn, K., Chieochansin, T., Theamboonlers, A. & Poovorawan, Y. (2011). Complete coding sequence characterization and comparative analysis of the putative novel human rhinovirus (HRV) species C and B. Virol J 8, 5. (BioMed Central Ltd.).
33. Martin, D. & Rybicki, E. (2000). RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562-563.
34. Martin, D. P., Posada, D., Crandall, K. A. & Williamson, C. (2005). A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21, 98-102.
35. Martin, D. P., Lemey, P., Lott, M., Moulton, V., Posada, D. & Lefeuvre, P. (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26, 2462-2463.
36. 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.
37. McIntyre, C. L., McWilliam Leitch, E. C., Savolainen-Kopra, C., Hovi, T. & Simmonds, P. (2010). Analysis of genetic diversity and sites of recombination in human rhinovirus species C. J Virol 84, 10297-10310.
38. McIntyre, C., Savolainen-Kopra, C., Hovi, T. & Simmonds, P. (2013). Recombination in the evolution of human rhinovirus genomes. Arch Virol [Epub ahead of print].
39. McWilliam Leitch, E. C., Harvala, H., Robertson, I., Ubillos, I., Templeton, K. & Simmonds, P. (2009). Direct identification of human enterovirus serotypes in cerebrospinal fluid by amplification and sequencing of the VP1 region. J Clin Microbiol 44, 119-124.
40. Miller, E. K., Lu, X., Erdman, D. D., Poehling, K. A., Zhu, Y., Griffin, M. R., Hartert, T. V., Anderson, L. J., Weinberg, G. A. & other authors (2007). Rhinovirus-associated hospitalizations in young children. J Infect Dis 195, 773-781.
41. Miller, E. K., Edwards, K. M., Weinberg, G. A., Iwane, M. K., Griffin, M. R., Hall, C. B., Zhu, Y., Szilagyi, P. G., Morin, L. L. & other authors http://vir.sgmjournals.org 1805 (2009). A novel group of rhinoviruses is associated with asthma hospitalizations. J Allergy Clin Immunol 123, 98-104, e1.
42. Mirand, A., Rouveyrol, F., Chambon, M., Archimbaud, C., Regagnon, C., Bailly, J.-L., Peigue-Lafeuille, H. & Henquell, C. (2009). Enterovirus genotyping directly from original clinical specimens: prospective application to a severe neonatal infection. J Clin Virol 44, 177-178.
43. Mizuta, K., Hirata, A., Suto, A., Aoki, Y., Ahiko, T., Itagaki, T., Tsukagoshi, H., Morita, Y., Obuchi, M. & other authors (2010). Phylogenetic and cluster analysis of human rhinovirus species A (HRV-A) isolated from children with acute respiratory infections in Yamagata, Japan. Virus Res 147, 265-274.
44. Monto, A. S. (2002). The seasonality of rhinovirus infections and its implications for clinical recognition. Clin Ther 24, 1987-1997.
45. Nix, W. A., Oberste, M. S. & Pallansch, M. A. (2006). Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 44, 2698-2704.
46. 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.
47. Oberste, M. S., Maher, K., Kilpatrick, D. R. & Pallansch, M. A. (1999a). Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73, 1941-1948.
48. Oberste, M. S., Maher, K., Kilpatrick, D. R., Flemister, M. R., Brown, B. A. & Pallansch, M. A. (1999b). Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 37, 1288-1293.
49. Oberste, M. S., Maher, K. & Pallansch, M. A. (2002). Molecular phylogeny and proposed classification of the simian picornaviruses. J Virol 76, 1244-1251.
50. Oberste, M. S., Michele, S. M., Maher, K., Schnurr, D., Cisterna, D., Junttila, N., Uddin, M., Chomel, J.-J., Lau, C.-S. & other authors (2004). Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. J Gen Virol 85, 3205-3212.
51. Oberste, M. S., Maher, K., Nix, W. A., Michele, S. M., Uddin, M., Schnurr, D., al-Busaidy, S., Akoua-Koffi, C. & Pallansch, M. A. (2007). Molecular identification of 13 new enterovirus types, EV79-88, EV97, and EV100-101, members of the species Human Enterovirus B. Virus Res 128, 34-42.
52. Olenec, J. P., Kim, W. K., Lee, W.-M., Vang, F., Pappas, T. E., Salazar, L. E. P., Evans, M. D., Bork, J., Roberg, K. & other authors (2010). Weekly monitoring of children with asthma for infections and illness during common cold seasons. J Allergy Clin Immunol 125, 1001-1006, e1.
53. Padidam, M., Sawyer, S. & Fauquet, C. M. (1999). Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218-225.
54. Posada, D. & Crandall, K. A. (2001). Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98, 13757-13762.
55. Rathe, J. A., Liu, X., Tallon, L. J., Gern, J. E. & Liggett, S. B. (2010). Full-genome sequence and analysis of a novel human rhinovirus strain within a divergent HRV-A clade. Arch Virol 155, 83-87.
56. Renwick, N., Schweiger, B., Kapoor, V., Liu, Z., Villari, J., Bullmann, R., Miething, R., Briese, T. & Lipkin, W. I. (2007). A recently identified rhinovirus genotype is associated with severe respiratory-tract infection in children in Germany. J Infect Dis 196, 1754-1760.
57. Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
58. 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.
59. Silva, P. A., Diedrich, S., de Paula Cardoso, D. & Schreier, E. (2008). Identification of enterovirus serotypes by pyrosequencing using multiple sequencing primers. J Virol Methods 148, 260-264.
60. Simmonds, P. (2012). SSE: a nucleotide and amino acid sequence anal ysis platform. BMC Res Notes 5, 50.
61. Simmonds, P., McIntyre, C., Savolainen-Kopra, C., Tapparel, C., Mackay, I. M. & Hovi, T. (2010). Proposals for the classification of human rhinovirus species C into genotypically assigned types. J Gen Virol 91, 2409-2419.
62. Smith, J. M. (1992). Analyzing the mosaic structure of genes. J Mol Evol 34, 126-129.
63. Smura, T., Blomqvist, S., Paananen, A., Vuorinen, T., Sobotová, Z., Bubovica, V., Ivanova, O., Hovi, T. & Roivainen, M. (2007a). Enterovirus surveillance reveals proposed new serotypes and provides new insight into enterovirus 59-untranslated region evolution. J Gen Virol 88, 2520-2526.
64. Smura, T. P., Junttila, N., Blomqvist, S., Norder, H., Kaijalainen, S., Paananen, A., Magnius, L. O., Hovi, T. & Roivainen, M. (2007b). Enterovirus 94, a proposed new serotype in human enterovirus species D. J Gen Virol 88, 849-858.
65. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731-2739.
66. Tapparel, C., Junier, T., Gerlach, D., Van-Belle, S., Turin, L., Cordey, S., Muhlemann, K., Regamey, N., Aubert, J.-D. & other authors (2009). New respiratory enterovirus and recombinant rhinoviruses among circulating picornaviruses. Emerg Infect Dis 15, 719-726.
67. Uncapher, C. R., DeWitt, C. M. & Colonno, R. J. (1991). The major and minor group receptor families contain all but one human rhinovirus serotype. Virology 180, 814-817.
68. 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.
69. Wisdom, A., Leitch, E. C., Gaunt, E., Harvala, H. & Simmonds, P. (2009a). Screening respiratory samples for detection of human rhinoviruses (HRVs) and enteroviruses: comprehensive VP4-VP2 typing reveals high incidence and genetic diversity of HRV species C. J Clin Microbiol 47, 3958-3967.
70. Wisdom, A., Kutkowska, A. E., McWilliam Leitch, E. C., Gaunt, E., Templeton, K., Harvala, H. & Simmonds, P. (2009b). Genetics, recombination and clinical features of human rhinovirus species C (HRV-C) infections; interactions of HRV-C with other respiratory viruses. PLoS ONE 4, e8518.
71. Yozwiak, N. L., Skewes-Cox, P., Gordon, A., Saborio, S., Kuan, G., Balmaseda, A., Ganem, D., Harris, E. & DeRisi, J. L. (2010). Human enterovirus 109: a novel interspecies recombinant enterovirus isolated from a case of acute pediatric respiratory illness in Nicaragua. J Virol 84, 9047-9058.