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. 1994 Sep;68(9):5448–5459. doi: 10.1128/jvi.68.9.5448-5459.1994

Evolutionary pattern of human respiratory syncytial virus (subgroup A): cocirculating lineages and correlation of genetic and antigenic changes in the G glycoprotein.

O García 1, M Martín 1, J Dopazo 1, J Arbiza 1, S Frabasile 1, J Russi 1, M Hortal 1, P Perez-Breña 1, I Martínez 1, B García-Barreno 1, et al.
PMCID: PMC236945  PMID: 8057427

Abstract

The genetic and antigenic variability of the G glycoproteins from 76 human respiratory syncytial (RS) viruses (subgroup A) isolated during six consecutive epidemics in either Montevideo, Uruguay, or Madrid, Spain, have been analyzed. Genetic diversity was evaluated for all viruses by the RNase A mismatch cleavage method and for selected strains by dideoxy sequencing. The sequences reported here were added to those published for six isolates from Birmingham, United Kingdom, and for two reference strains (A2 and Long), to derive a phylogenetic tree of subgroup A viruses that contained two main branches and several subbranches. During the same epidemic, viruses from different branches were isolated. In addition, closely related viruses were isolated in distant places and in different years. These results illustrate the capacity of the virus to spread worldwide, influencing its mode of evolution. The antigenic analysis of all isolates was carried out with a panel of anti-G monoclonal antibodies that recognized strain-specific (or variable) epitopes. A close correlation between genetic relatedness and antigenic relatedness in the G protein was observed. These results, together with an accumulation of amino acid changes in a major antigenic area of the G glycoprotein, suggest that immune selection may be a factor influencing the generation of RS virus diversity. The pattern of RS virus evolution is thus similar to that described for influenza type B viruses, expect that the level of genetic divergence among the G glycoproteins of RS virus isolates is the highest reported for an RNA virus gene product.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akerlind-Stopner B., Utter G., Mufson M. A., Orvell C., Lerner R. A., Norrby E. A subgroup-specific antigenic site in the G protein of respiratory syncytial virus forms a disulfide-bonded loop. J Virol. 1990 Oct;64(10):5143–5148. doi: 10.1128/jvi.64.10.5143-5148.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson L. J., Hierholzer J. C., Tsou C., Hendry R. M., Fernie B. F., Stone Y., McIntosh K. Antigenic characterization of respiratory syncytial virus strains with monoclonal antibodies. J Infect Dis. 1985 Apr;151(4):626–633. doi: 10.1093/infdis/151.4.626. [DOI] [PubMed] [Google Scholar]
  3. Berton M. T., Naeve C. W., Webster R. G. Antigenic structure of the influenza B virus hemagglutinin: nucleotide sequence analysis of antigenic variants selected with monoclonal antibodies. J Virol. 1984 Dec;52(3):919–927. doi: 10.1128/jvi.52.3.919-927.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cane P. A., Matthews D. A., Pringle C. R. Analysis of relatedness of subgroup A respiratory syncytial viruses isolated worldwide. Virus Res. 1992 Sep 1;25(1-2):15–22. doi: 10.1016/0168-1702(92)90096-r. [DOI] [PubMed] [Google Scholar]
  5. Cane P. A., Matthews D. A., Pringle C. R. Identification of variable domains of the attachment (G) protein of subgroup A respiratory syncytial viruses. J Gen Virol. 1991 Sep;72(Pt 9):2091–2096. doi: 10.1099/0022-1317-72-9-2091. [DOI] [PubMed] [Google Scholar]
  6. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  7. Coates H. V., Alling D. W., Chanock R. M. An antigenic analysis of respiratory syncytial virus isolates by a plaque reduction neutralization test. Am J Epidemiol. 1966 Mar;83(2):299–313. doi: 10.1093/oxfordjournals.aje.a120586. [DOI] [PubMed] [Google Scholar]
  8. Collins P. L., Mottet G. Oligomerization and post-translational processing of glycoprotein G of human respiratory syncytial virus: altered O-glycosylation in the presence of brefeldin A. J Gen Virol. 1992 Apr;73(Pt 4):849–863. doi: 10.1099/0022-1317-73-4-849. [DOI] [PubMed] [Google Scholar]
  9. Cristina J., López J. A., Albó C., García-Barreno B., García J., Melero J. A., Portela A. Analysis of genetic variability in human respiratory syncytial virus by the RNase A mismatch cleavage method: subtype divergence and heterogeneity. Virology. 1990 Jan;174(1):126–134. doi: 10.1016/0042-6822(90)90061-u. [DOI] [PubMed] [Google Scholar]
  10. Cristina J., Moya A., Arbiza J., Russi J., Hortal M., Albo C., García-Barreno B., García O., Melero J. A., Portela A. Evolution of the G and P genes of human respiratory syncytial virus (subgroup A) studied by the RNase A mismatch cleavage method. Virology. 1991 Sep;184(1):210–218. doi: 10.1016/0042-6822(91)90837-2. [DOI] [PubMed] [Google Scholar]
  11. DeBorde D. C., Naeve C. W., Herlocher M. L., Maassab H. F. Resolution of a common RNA sequencing ambiguity by terminal deoxynucleotidyl transferase. Anal Biochem. 1986 Sep;157(2):275–282. doi: 10.1016/0003-2697(86)90626-3. [DOI] [PubMed] [Google Scholar]
  12. Domingo E., Díez J., Martínez M. A., Hernández J., Holguín A., Borrego B., Mateu M. G. New observations on antigenic diversification of RNA viruses. Antigenic variation is not dependent on immune selection. J Gen Virol. 1993 Oct;74(Pt 10):2039–2045. doi: 10.1099/0022-1317-74-10-2039. [DOI] [PubMed] [Google Scholar]
  13. Fernie B. F., Dapolito G., Cote P. J., Jr, Gerin J. L. Kinetics of synthesis of respiratory syncytial virus glycoproteins. J Gen Virol. 1985 Sep;66(Pt 9):1983–1990. doi: 10.1099/0022-1317-66-9-1983. [DOI] [PubMed] [Google Scholar]
  14. Fitch W. M., Leiter J. M., Li X. Q., Palese P. Positive Darwinian evolution in human influenza A viruses. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4270–4274. doi: 10.1073/pnas.88.10.4270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Garcia-Barreno B., Jorcano J. L., Aukenbauer T., López-Galíndez C., Melero J. A. Participation of cytoskeletal intermediate filaments in the infectious cycle of human respiratory syncytial virus (RSV). Virus Res. 1988 Mar;9(4):307–321. doi: 10.1016/0168-1702(88)90090-1. [DOI] [PubMed] [Google Scholar]
  16. García-Barreno B., Delgado T., Melero J. A. Oligo(A) sequences of human respiratory syncytial virus G protein gene: assessment of their genetic stability in frameshift mutants. J Virol. 1994 Sep;68(9):5460–5468. doi: 10.1128/jvi.68.9.5460-5468.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. García-Barreno B., Palomo C., Peñas C., Delgado T., Perez-Breña P., Melero J. A. Marked differences in the antigenic structure of human respiratory syncytial virus F and G glycoproteins. J Virol. 1989 Feb;63(2):925–932. doi: 10.1128/jvi.63.2.925-932.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. García-Barreno B., Portela A., Delgado T., López J. A., Melero J. A. Frame shift mutations as a novel mechanism for the generation of neutralization resistant mutants of human respiratory syncytial virus. EMBO J. 1990 Dec;9(12):4181–4187. doi: 10.1002/j.1460-2075.1990.tb07642.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
  20. Johnson P. R., Spriggs M. K., Olmsted R. A., Collins P. L. The G glycoprotein of human respiratory syncytial viruses of subgroups A and B: extensive sequence divergence between antigenically related proteins. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5625–5629. doi: 10.1073/pnas.84.16.5625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kanegae Y., Sugita S., Endo A., Ishida M., Senya S., Osako K., Nerome K., Oya A. Evolutionary pattern of the hemagglutinin gene of influenza B viruses isolated in Japan: cocirculating lineages in the same epidemic season. J Virol. 1990 Jun;64(6):2860–2865. doi: 10.1128/jvi.64.6.2860-2865.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Levine S., Klaiber-Franco R., Paradiso P. R. Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J Gen Virol. 1987 Sep;68(Pt 9):2521–2524. doi: 10.1099/0022-1317-68-9-2521. [DOI] [PubMed] [Google Scholar]
  23. Lopez-Galindez C., Lopez J. A., Melero J. A., de la Fuente L., Martinez C., Ortin J., Perucho M. Analysis of genetic variability and mapping of point mutations in influenza virus by the RNase A mismatch cleavage method. Proc Natl Acad Sci U S A. 1988 May;85(10):3522–3526. doi: 10.1073/pnas.85.10.3522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mallipeddi S. K., Samal S. K. Sequence variability of the glycoprotein gene of bovine respiratory syncytial virus. J Gen Virol. 1993 Sep;74(Pt 9):2001–2004. doi: 10.1099/0022-1317-74-9-2001. [DOI] [PubMed] [Google Scholar]
  25. Mateu M. G., Hernández J., Martínez M. A., Feigelstock D., Lea S., Pérez J. J., Giralt E., Stuart D., Palma E. L., Domingo E. Antigenic heterogeneity of a foot-and-mouth disease virus serotype in the field is mediated by very limited sequence variation at several antigenic sites. J Virol. 1994 Mar;68(3):1407–1417. doi: 10.1128/jvi.68.3.1407-1417.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mufson M. A., Orvell C., Rafnar B., Norrby E. Two distinct subtypes of human respiratory syncytial virus. J Gen Virol. 1985 Oct;66(Pt 10):2111–2124. doi: 10.1099/0022-1317-66-10-2111. [DOI] [PubMed] [Google Scholar]
  27. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  28. Olmsted R. A., Elango N., Prince G. A., Murphy B. R., Johnson P. R., Moss B., Chanock R. M., Collins P. L. Expression of the F glycoprotein of respiratory syncytial virus by a recombinant vaccinia virus: comparison of the individual contributions of the F and G glycoproteins to host immunity. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7462–7466. doi: 10.1073/pnas.83.19.7462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Oxford J. S., Klimov A. I., Corcoran T., Ghendon Y. Z., Schild G. C. Biochemical and serological studies of influenza B viruses: comparisons of historical and recent isolates. Virus Res. 1984;1(3):241–258. doi: 10.1016/0168-1702(84)90042-x. [DOI] [PubMed] [Google Scholar]
  30. Rota P. A., Hemphill M. L., Whistler T., Regnery H. L., Kendal A. P. Antigenic and genetic characterization of the haemagglutinins of recent cocirculating strains of influenza B virus. J Gen Virol. 1992 Oct;73(Pt 10):2737–2742. doi: 10.1099/0022-1317-73-10-2737. [DOI] [PubMed] [Google Scholar]
  31. Rota P. A., Wallis T. R., Harmon M. W., Rota J. S., Kendal A. P., Nerome K. Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology. 1990 Mar;175(1):59–68. doi: 10.1016/0042-6822(90)90186-u. [DOI] [PubMed] [Google Scholar]
  32. Rueda P., Delgado T., Portela A., Melero J. A., García-Barreno B. Premature stop codons in the G glycoprotein of human respiratory syncytial viruses resistant to neutralization by monoclonal antibodies. J Virol. 1991 Jun;65(6):3374–3378. doi: 10.1128/jvi.65.6.3374-3378.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rueda P., García-Barreno B., Melero J. A. Loss of conserved cysteine residues in the attachment (G) glycoprotein of two human respiratory syncytial virus escape mutants that contain multiple A-G substitutions (hypermutations). Virology. 1994 Feb;198(2):653–662. doi: 10.1006/viro.1994.1077. [DOI] [PubMed] [Google Scholar]
  34. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  35. Sakaguchi T., Toyoda T., Gotoh B., Inocencio N. M., Kuma K., Miyata T., Nagai Y. Newcastle disease virus evolution. I. Multiple lineages defined by sequence variability of the hemagglutinin-neuraminidase gene. Virology. 1989 Apr;169(2):260–272. doi: 10.1016/0042-6822(89)90151-7. [DOI] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Satake M., Coligan J. E., Elango N., Norrby E., Venkatesan S. Respiratory syncytial virus envelope glycoprotein (G) has a novel structure. Nucleic Acids Res. 1985 Nov 11;13(21):7795–7812. doi: 10.1093/nar/13.21.7795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sourdis J., Nei M. Relative efficiencies of the maximum parsimony and distance-matrix methods in obtaining the correct phylogenetic tree. Mol Biol Evol. 1988 May;5(3):298–311. doi: 10.1093/oxfordjournals.molbev.a040497. [DOI] [PubMed] [Google Scholar]
  39. Storch G. A., Park C. S., Dohner D. E. RNA fingerprinting of respiratory syncytial virus using ribonuclease protection. Application to molecular epidemiology. J Clin Invest. 1989 Jun;83(6):1894–1902. doi: 10.1172/JCI114096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Stott E. J., Taylor G., Ball L. A., Anderson K., Young K. K., King A. M., Wertz G. W. Immune and histopathological responses in animals vaccinated with recombinant vaccinia viruses that express individual genes of human respiratory syncytial virus. J Virol. 1987 Dec;61(12):3855–3861. doi: 10.1128/jvi.61.12.3855-3861.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Studier F. W. Analysis of bacteriophage T7 early RNAs and proteins on slab gels. J Mol Biol. 1973 Sep 15;79(2):237–248. doi: 10.1016/0022-2836(73)90003-x. [DOI] [PubMed] [Google Scholar]
  42. Sullender W. M., Mufson M. A., Anderson L. J., Wertz G. W. Genetic diversity of the attachment protein of subgroup B respiratory syncytial viruses. J Virol. 1991 Oct;65(10):5425–5434. doi: 10.1128/jvi.65.10.5425-5434.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Taylor G., Stott E. J., Bew M., Fernie B. F., Cote P. J., Collins A. P., Hughes M., Jebbett J. Monoclonal antibodies protect against respiratory syncytial virus infection in mice. Immunology. 1984 May;52(1):137–142. [PMC free article] [PubMed] [Google Scholar]
  44. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Walsh E. E., Hall C. B., Briselli M., Brandriss M. W., Schlesinger J. J. Immunization with glycoprotein subunits of respiratory syncytial virus to protect cotton rats against viral infection. J Infect Dis. 1987 Jun;155(6):1198–1204. doi: 10.1093/infdis/155.6.1198. [DOI] [PubMed] [Google Scholar]
  46. Wertz G. W., Collins P. L., Huang Y., Gruber C., Levine S., Ball L. A. Nucleotide sequence of the G protein gene of human respiratory syncytial virus reveals an unusual type of viral membrane protein. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4075–4079. doi: 10.1073/pnas.82.12.4075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wertz G. W., Krieger M., Ball L. A. Structure and cell surface maturation of the attachment glycoprotein of human respiratory syncytial virus in a cell line deficient in O glycosylation. J Virol. 1989 Nov;63(11):4767–4776. doi: 10.1128/jvi.63.11.4767-4776.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wiley D. C., Wilson I. A., Skehel J. J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature. 1981 Jan 29;289(5796):373–378. doi: 10.1038/289373a0. [DOI] [PubMed] [Google Scholar]
  49. Winter E., Yamamoto F., Almoguera C., Perucho M. A method to detect and characterize point mutations in transcribed genes: amplification and overexpression of the mutant c-Ki-ras allele in human tumor cells. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7575–7579. doi: 10.1073/pnas.82.22.7575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yamashita M., Krystal M., Fitch W. M., Palese P. Influenza B virus evolution: co-circulating lineages and comparison of evolutionary pattern with those of influenza A and C viruses. Virology. 1988 Mar;163(1):112–122. doi: 10.1016/0042-6822(88)90238-3. [DOI] [PubMed] [Google Scholar]

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