Genetic variability and molecular evolution of the human respiratory syncytial virus subgroup B attachment G protein

Journal of Virology

Volumn 79, Issue 14, 2005, Pages 9157-9167

  Zlateva, Kalina T ^a   Lemey, Philippe ^a   Moës, Elien ^a,b   Vandamme, Anne Mieke ^a   Van Ranst, Marc ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATTACHMENT G PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ACUTE RESPIRATORY TRACT DISEASE; ANTIGENIC VARIATION; ARTICLE; CODON; EVOLUTIONARY RATE; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; IMMUNOPATHOGENESIS; INFANT DISEASE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; REINFECTION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL PNEUMOVIRUS SUBGROUP A; RESPIRATORY SYNCYTIAL PNEUMOVIRUS SUBGROUP B; VIRUS INFECTIVITY; VIRUS STRAIN;

AMINO ACID SEQUENCE; EVOLUTION, MOLECULAR; GLYCOSYLATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VARIATION (GENETICS); VIRAL ENVELOPE PROTEINS;

HUMAN RESPIRATORY SYNCYTIAL VIRUS; HYDRANGEA RINGSPOT VIRUS; SUBGROUP B;

EID: 21644450676     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.14.9157-9167.2005     Document Type: Article

References (75)

1. Anderson, L. J., J. C. Hierholzer, C. Tsou, R. M. Hendry, B. F. Fernie, Y. Stone, and K. McIntosh. 1985. Antigenic characterization of respiratory syncytial virus strains with monoclonal antibodies. J. Infect. Dis. 151:626-633.
2. Cane, P. A., and C. R, Pringle. 1995. Evolution of subgroup A respiratory syncytial virus: evidence for progressive accumulation of amino acid changes in the attachment protein. J. Virol. 69:2918-2925.
3. Cane, P. A., D. A. Matthews, and C. R. Pringle. 1993. Frequent polymerase errors observed in a restricted area of clones derived from the attachment (G) protein gene of respiratory syncytial virus. J. Virol. 67:1090-1093.
4. Cane, P. A., D. A. Matthews, and C. R. Pringle. 1991. Identification of variable domains of the attachment (G) protein of subgroup A respiratory syncytial viruses. J. Gen. Virol. 72:2091-2096.
5. Coggins, W. B., E. J. Lefkowitz, and W. M. Sullender. 1998. Genetic variability among group A and group B respiratory syncytial viruses in a children's hospital. J. Clin. Microbiol. 36:3552-3557.
6. Collins, P. L., R. M. Chanock, and B. R. Murphy. 2001. Respiratory syncytial virus, p. 1443-1485. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed. Lippincott Williams and Wilkins, Philadelphia, Pa.
7. Connors, M., P. L. Collins, C. Y. Firestone, and B. R. Murphy. 1991. Respiratory syncytial virus (RSV) F, G, M2 (22K), and N proteins each induce resistance to RSV challenge, but resistance induced by M2 and N proteins is relatively short-lived. J. Virol. 65:1634-1637.
8. Crandall, K. A., C. R. Kelsey, H. Imamichi, H. C. Lane, and N. P. Salzman. 1999. Parallel evolution of drug resistance in HIV: failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Mol. Biol. Evol. 16:372-382.
9. Dowell, S. F., L. J. Anderson, H. E. Gary, Jr., D. D. Erdman, J. F. Plouffe, T. M. File, Jr., B. J. Marston, and R. F. Breiman. 1996. Respiratory syncytial virus is an important cause of community-acquired lower respiratory infection among hospitalized adults. J. Infect. Dis. 174:456-462.
10. England, J. A., L. J. Anderson, and F. S. Rhame. 1991. Nosocomial transmission of respiratory syncytial virus in immunocompromised adults. J. Clin. Microbiol. 29:115-119.
11. Falsey, A. R., and E. E. Walsh. 2000. Respiratory syncytial virus infection in adults. Clin. Microbiol. Rev. 13:371-384.
12. Fleming, D. M., and K. W. Cross. 1993. Respiratory syncytial virus or influenza? Lancet 342:1507-1510.
13. Garcia, O., M. Martin, J. Dopazo, J. Arbiza, S. Frabasile, J. Russi, M. Hortal, P. Perez-Brena, I. Martinez, B. Garcia-Barreno, and J. A. Melero. 1994. Evolutionary pattern of human respiratory syncytial virus (subgroup A): cocirculating lineages and correlation of genetic and antigenic changes in the G glycoprotein. J. Virol. 68:5448-5459.
14. Garcia-Barreno, B., T. Delgado, and J. A. Melero. 1994. Oligo(A) sequences of human respiratory syncytial virus G protein gene: assessment of their genetic stability in frameshift mutants. J. Virol. 68:5460-5468.
15. Garcia-Barreno, B., A. Portela, T. Delgado, J. A. Lopez, and J. A. Melero. 1990. Frame-shift mutations as a novel mechanism for the generation of neutralization resistant mutants of human respiratory syncytial virus. EMBO J. 9:4181-4187.
16. Glezen, P., and F. W. Denny. 1973. Epidemiology of acute lower respiratory disease in children. N. Engl. J. Med. 288:498-505.
17. Grenfell, B. T., O. G. Pybus, J. R. Gog, J. L. Wood, J. M. Daly, J. A. Mumford, and E. C. Holmes. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-332.
18. Hall, C. B., E. E. Walsh, C. E. Long, and K. C. Schnabel. 1991. Immunity to and frequency of reinfection with respiratory syncytial virus. J. Infect. Dis. 163:693-698.
19. Hall, C. B., E. E. Walsh, K. C. Schnabel, C. E. Long, K. M. McConnochie, S. W. Hildreth, and L. J. Anderson. 1990. Occurrence of groups A and B of respiratory syncytial virus over 15 years: associated epidemiologic and clinical characteristics in hospitalized and ambulatory children. J. Infect. Dis. 162:1283-1290.
20. Hall, C. B., A. E. Kopelman, R. G. Douglas, Jr., J. M. Geiman, and M. P. Meagher. 1979. Neonatal respiratory syncytial virus infection. N. Engl. J. Med. 300:393-396.
21. Han, L. L., J. P. Alexander, and L. J. Anderson. 1999. Respiratory syncytial virus pneumonia among the elderly: an assessment of disease burden. J. Infect. Dis. 179:25-30.
22. Hansen, J. E., O. Lund, N. Tolstrup, A. A. Gooley, K. L. Williams, and S. Brunak. 1998. NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj. J. 15:115-130.
23. Henderson, F. W., A. M. Collier, W. A. Clyde, Jr., and F. W. Denny. 1979. Respiratory-syncytial-virus infections, reinfections and immunity. A prospective, longitudinal study in young children. N. Engl. J. Med. 300:530-534.
24. Hendry, R. M., L. T. Pierik, and K. McIntosh. 1989. Prevalence of respiratory syncytial virus subgroups over six consecutive outbreaks: 1981-1987. J. Infect. Dis. 160:185-190.
25. Holberg, C. J., A. L. Wright, F. D. Martinez, C. G. Ray, L. M. Taussig, and M. D. Lebowitz. 1991. Risk factors for respiratory syncytial virus-associated lower respiratory illnesses in the first year of life. Am. J. Epidemiol. 133:1135-1151.
26. Jenkins, G. M., A. Rambaut, O. G. Pybus, and E. C. Holmes. 2002. Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J. Mol. Evol. 54:156-165.
27. Johnson, P. R., M. K. Spriggs, R. A. Olmsted, and P. L. Collins. 1987. The G glycoprotein of human respiratory syncytial viruses of subgroups A and B: extensive sequence divergence between antigenically related proteins. Proc. Natl. Acad. Sci. USA 84:5625-5629.
28. Julenius, K., A. Molgaard, R. Gupta, and S. Brunak. 2005. Prediction, conservation analysis and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15:153-164.
29. Kamasaki, H., H. Tsutsumi, K. Seki, and S. Chiba. 2001. Genetic variability of respiratory syncytial virus subgroup B strain isolated during the last 20 years from the same region in Japan: existence of time-dependent linear genetic drifts. Arch. Virol. 146:457-466.
30. Karron, R. A., D. A. Buonagurio, A. F. Georgiu, S. S. Whitehead, J. E. Adamus, M. L. Clements-Mann, D. O. Harris, V. B. Randolph, S. A. Udem, B. R. Murphy, and M. S. Sidhu. 1997. Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc. Natl. Acad. Sci. USA 94:13961-13966.
31. Li, W. H. 1997. Molecular evolution. Sinauer Assoc., Sunderland, MA.
32. Martinez, I., O. Valdes, A. Delfraro, J. Arbiza, J. Russi, and J. A. Melero. 1999. Evolutionary pattern of the G glycoprotein of human respiratory syncytial viruses from antigenic group B: the use of alternative termination codons and lineage diversification. J. Gen. Virol. 80:125-130.
33. Martinez, I., J. Dopazo, and J. A. Melero. 1997. Antigenic structure of the human respiratory syncytial virus G glycoprotein and relevance of hypermutation events for the generation of antigenic variants. J. Gen. Virol. 78:2419-2429.
34. Melero, J. A., B. Garcia-Barreno, I. Martinez, C. R. Pringle, and P. A. Cane. 1997. Antigenic structure, evolution and immunobiology of human respiratory syncytial virus attachment (G) protein. J. Gen. Virol. 78:2411-2418.
35. Muelenaer, P. M., F. W. Henderson, V. G. Hemming, E. E. Walsh, L. J. Anderson, G. A. Prince, and B. R. Murphy. 1991. Group-specific serum antibody responses in children with primary and recurrent respiratory syn-cytial virus infections. J. Infect. Dis. 164:15-21.
36. Mufson, M. A., R. B. Belshe, C. Orvell, and E. Norrby. 1988. Respiratory syncytial virus epidemics: variable dominance of subgroups A and B strains among children, 1981-1986. J. Infect. Dis. 157:143-148.
37. Mufson, M. A., R. B. Belshe, C. Orvell, and E. Norrby. 1987. Subgroup characteristics of respiratory syncytial virus strains recovered from children with two consecutive infections. J. Clin. Microbiol. 25:1535-1539.
38. Mufson, M. A., C. Orvell, B. Rafnar, and E. Norrby. 1985. Two distinct subtypes of human respiratory syncytial virus. J. Gen. Virol. 66:2111-2124.
39. Murry, A. R., and S. F. Dowell. 1997. Respiratory syncytial virus: not just for kids. Hosp. Pract. 32:87-88.
40. Nagai, K., H. Kamasaki, Y. Kuroiwa, L. Okita, and H. Tsutsumi. 2004. Nosocomial outbreak of respiratory syncytial virus subgroup B variants with the 60 nucleotides-duplicated G protein gene. J. Med. Virol. 74:161-165.
41. Nicholas, K. B., H. B. Nicholas, and D. W. Deerfield. 1997. GeneDoc: analysis and visualization of genetic variation. Embnet News 4:14.
42. Nielsen, R., and Z. Yang. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929-936.
43. Palomo, C., P. A. Cane, and J. A. Melero. 2000. Evaluation of the antibody specificities of human convalescent-phase sera against the attachment (G) protein of human respiratory syncytial virus: influence of strain variation and carbohydrate side chains. J. Med. Virol. 60:468-474.
44. Palomo, C., B. Garcia-Barreno, C. Penas, and J. A. Melero. 1991. The G protein of human respiratory syncytial virus: significance of carbohydrate side-chains and the C-terminal end to its antigenicity. J. Gen. Virol. 72:669-675.
45. Peret, T. C., C. B. Hall, G. W. Hammond, P. A. Piedra, G. A. Storch, W. M. Sullender, C. Tsou, and L. J. Anderson. 2000. Circulation patterns of group A and B human respiratory syncytial virus genotypes in 5 communities in North America. J. Infect. Dis. 181:1891-1896.
46. Peret, T. C., C. B. Hall, K. C. Schnabel, J. A. Golub, and L. J. Anderson. 1998. Circulation patterns of genetically distinct group A and B strains of human respiratory syncytial virus in a community. J. Gen. Virol. 79:2221-2229.
47. Posada, D., and K. A. Crandall. 2001. Selecting the best-fit model of nucleotide substitution. Syst. Biol. 50:580-601.
48. Rambaut, A. 2000. Estimating the rate of molecular evolution: incorporating non-contemporaneous sequences into maximum likelihood phytogenies. Bioinformatics 16:395-399.
49. Roca, A., M. P. Loscertales, L. Quinto, P. Perez-Brena, N. Vaz, P. L. Alonso, and J. C. Saiz. 2001. Genetic variability among group A and B respiratory syncytial viruses in Mozambique: identification of a new cluster of group B isolates. J. Gen. Virol. 82:103-111.
50. Rueda, P., C. Palomo, B. Garcia-Barreno, and J. A. Melero. 1995. The three C-terminal residues of human respiratory syncytial virus G glycoprotein (Long strain) are essential for integrity of multiple epitopes distinguishable by antiidiotypic antibodies. Viral Immunol. 8:37-46.
51. Rueda, P., T. Delgado, A. Portela, J. A. Melero, and B. Garcia-Barreno. 1991. Premature stop codons in the G glycoprotein of human respiratory syncytial viruses resistant to neutralization by monoclonal antibodies. J. Virol. 65:3374-3378.
52. Sanz, M. C., O. M. Kew, and L. J. Anderson. 1994. Genetic heterogeneity of the attachment glycoprotein G among group A respiratory syncytial viruses. Virus Res. 33:203-217.
53. Scott, P. D., R. Ochola, M. Ngama, E. A. Okiro, D. J. Nokes, G. F. Medley, and P. A. Cane. 2004. Molecular epidemiology of respiratory syncytial virus in Kilifi district, Kenya. J. Med. Virol. 74:344-354.
54. Sullender, W. M., M. A. Mufson, G. A. Prince, L. J. Anderson, and G. W. Wertz. 1998. Antigenic and genetic diversity among the attachment proteins of group A respiratory syncytial viruses that have caused repeat infections in children. J. Infect. Dis. 178:925-932.
55. Sullender, W. M., M. A. Mufson, L. J. Anderson, and G. W. Wertz. 1991. Genetic diversity of the attachment protein of subgroup B respiratory syncytial viruses. J. Virol. 65:5425-5434.
56. Swofford, D. L. 1998. PAUP* 4.0: phylogenetic analysis using parsimony. Sinauer Assoc., Sunderland, MA.
57. Taylor, G., E. J. Stott, M. Bew, B. F. Fernie, P. J. Cote, A. P. Collins, M. Hughes, and J. Jebbett. 1984. Monoclonal antibodies protect against respiratory syncytial virus infection in mice. Immunology 52:137-142.
58. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
59. Trente, A., M. Galiano, C. Videla, G. Carballal, B. Garcia-Barreno, J. A. Melero, and C. Palomo. 2003. Major changes in the G protein of human respiratory syncytial virus isolates introduced by a duplication of 60 nucleotides. J. Gen. Virol. 84:3115-3120.
60. Venter, M., M. Collinson, and B. D. Schoub. 2002. Molecular epidemiological analysis of community circulating respiratory syncytial virus in rural South Africa: comparison of viruses and genotypes responsible for different disease manifestations. J. Med. Virol. 68:452-461.
61. Venter, M., S. A. Madhi, C. T. Tiemessen, and B. D. Schoub. 2001. Genetic diversity and molecular epidemiology of respiratory syncytial virus over four consecutive seasons in South Africa: identification of new subgroup A and B genotypes. J. Gen. Virol. 82:2117-2124.
62. Vidal, S., J. Curran, and D. Kolakofsky. 1990. A stuttering model for paramyxovirus P mRNA editing. EMBO J. 9:2017-2022.
63. Vidal, S., J. Curran, and D. Kolakofsky. 1990. Editing of the Sendai virus P/C mRNA by G insertion occurs during mRNA synthesis via a virus-encoded activity. J. Virol. 64:239-246.
64. Walsh, E. E., J. J. Schlesinger, and M. W. Brandriss. 1984. Protection from respiratory syncytial virus infection in cotton rats by passive transfer of monoclonal antibodies. Infect. Immun. 43:756-758.
65. Waris, M. 1991. Pattern of respiratory syncytial virus epidemics in Finland: two-year cycles with alternating prevalence of groups A and B. J. Infect. Dis. 163:464-469.
66. Wathen, M. W., P. A. Aeed, and A. P. Elhammer. 1991. Characterization of oligosaccharide structures on a chimeric respiratory syncytial virus protein expressed in insect cell line Sf9. Biochemistry 30:2863-2868.
67. Wertz, G. W., M. Krieger, and L. A. Ball. 1989. Structure and cell surface maturation of the attachment glycoprotein of human respiratory syncytial virus in a cell line deficient in O glycosylation. J. Virol. 63:4767-4776.
68. Wertz, G. W., P. L. Collins, Y. Huang, C. Gruber, S. Levine, and L. A. Ball. 1985. Nucleotide sequence of the G protein gene of human respiratory syncytial virus reveals an unusual type of viral membrane protein. Proc. Natl. Acad. Sci. USA 82:4075-4079.
69. Wilson, S. D., K. Roberts, K. Hammond, J. G. Ayres, and P. A. Cane. 2000. Estimation of incidence of respiratory syncytial virus infection in schoolchildren using salivary antibodies. J. Med. Virol. 61:81-84.
70. Woelk, C. H., and E. C. Holmes. 2001. Variable immune-driven natural selection in the attachment (G) glycoprotein of respiratory syncytial virus (RSV). J. Mol. Evol. 52:182-192.
71. Xia, X., and Z. Xie. 2001. DAMBE: software package for data analysis in molecular biology and evolution, J. Hered. 92:371-373.
72. Yang, Z., and J. P. Bielawski. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15:496-503.
73. Yang, Z., R. Nielsen, N. Goldman, and A. M. Pedersen. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449 .
74. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556 .
75. Zlateva, K. T., P. Lemey, A.-M. Vandamme, and M. Van Ranst. 2004. Molecular evolution and circulation patterns of human respiratory syncytial virus subgroup A: positively selected sites in the attachment G glycoprotein. J. Virol. 78:4675-4683.