Conservation of G-protein epitopes in respiratory syncytial virus (Group A) despite broad genetic diversity: Is antibody selection involved in virus evolution?

Journal of Virology

Volumn 89, Issue 15, 2015, Pages 7776-7785

  Trento, Alfonsina ^a,b   Ábrego, Leyda ^c   Rodriguez Fernandez, Rosa ^d   González Sánchez, Maria Isabel ^d   González Martínez, Felipe ^d   Delfraro, Adriana ^e   Pascale, Juan M ^c   Arbiza, Juan ^e   Melero, José A ^a,b  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c Instituto Conmemorativo Gorgas de Estudios de la Salud   (Panama)

^d HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^e UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GUANINE NUCLEOTIDE BINDING PROTEIN; INFLUENZA VIRUS HEMAGGLUTININ; MONOCLONAL ANTIBODY; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; EPIDEMIC; GENE AMPLIFICATION; GENE SEQUENCE; GENETIC DISTANCE; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN RESPIRATORY SYNCYTIAL VIRUS A; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN BINDING; RNA EXTRACTION; VIRAL GENETICS; VIRUS ISOLATION; WESTERN BLOTTING; ANTIGENIC VARIATION; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; SEQUENCE ALIGNMENT; VIROLOGY;

HUMAN RESPIRATORY SYNCYTIAL VIRUS; RESPIRATORY SYNCYTIAL VIRUS;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIGENIC VARIATION; CONSERVED SEQUENCE; EPITOPES; EVOLUTION, MOLECULAR; GENETIC VARIATION; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SEQUENCE ALIGNMENT; VIRAL ENVELOPE PROTEINS;

EID: 84937691842     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00467-15     Document Type: Article

References (53)

1. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, O'Brien KL, Roca A, Wright PF, Bruce N, Chandran A, Theodoratou E, Sutanto A, Sedyaningsih ER, Ngama M, Munywoki PK, Kartasasmita C, Simoes EA, Rudan I, Weber MW, Campbell H. 2010. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375:1545-1555. http://dx.doi.org/10.1016/S0140-6736(10)60206-1.
2. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. 2005. Respiratory syncytial virus infection in elderly and high-risk adults. NEngl J Med 352:1749-1759. http://dx.doi.org/10.1056/NEJMoa043951.
3. Collins PL, Melero JA. 2011. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res 162: 80-99. http://dx.doi.org/10.1016/j.virusres.2011.09.020.
4. Levine S, Klaiber-Franco R, Paradiso PR. 1987. Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J Gen Virol 68:2521-2524. http://dx.doi.org/10.1099/0022-1317-68-9-2521.
5. Walsh EE, Hruska J. 1983. Monoclonal antibodies to respiratory syncytial virus proteins: identification of the fusion protein. J Virol 47:171-177.
6. Gruber C, Levine S. 1985. Respiratory syncytial virus polypeptides. V. The kinetics of glycoprotein synthesis. J Gen Virol 66:1241-1247.
7. Garcia-Beato R, Martinez I, Franci C, Real FX, Garcia-Barreno B, Melero JA. 1996. Host cell effect upon glycosylation and antigenicity of human respiratory syncytial virus G glycoprotein. Virology 221:301-309. http://dx.doi.org/10.1006/viro.1996.0379.
8. Palomo C, Cane PA, Melero JA. 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. http://dx.doi.org/10.1002/(SICI)1096-9071(200004)60:4<468::AID-JMV16>3.0.CO;2-E.
9. Anderson LJ, Hierholzer JC, Tsou C, Hendry RM, Fernie BF, Stone Y, McIntosh K. 1985. Antigenic characterization of respiratory syncytial virus strains with monoclonal antibodies. J Infect Dis 151:623-633.
10. Mufson MA, Orvell C, Rafnar B, Norrby E. 1985. Two distinct subtypes of human respiratory syncytial virus. J Gen Virol 66:2111-2124. http://dx.doi.org/10.1099/0022-1317-66-10-2111.
11. Tan L, Lemey P, Houspie L, Viveen C, Jansen NJ, van Loon AM, Wiertz E, van Bleek GM, Martin DP, Coenjaerts FE. 2012. Genetic variability among complete human respiratory syncytial virus subgroup A genomes: bridging molecular evolutionary dynamics and epidemiology. PLoS One 7:e51439. http://dx.doi.org/10.1371/journal.pone.0051439.
12. Melero JA, Garcia-Barreno B, Martinez I, Pringle CR, Cane PA. 1997. Antigenic structure, evolution and immunobiology of human respiratory syncytial virus attachment (G) protein. J Gen Virol 78:2411-2418.
13. Woelk CH, Holmes EC. 2001. Variable immune-driven natural selection in the attachment (G) glycoprotein of respiratory syncytial virus (RSV). J Mol Evol 52:182-192.
14. Tan L, Coenjaerts FE, Houspie L, Viveen MC, van Bleek GM, Wiertz EJ, Martin DP, Lemey P. 2013. The comparative genomics of human respiratory syncytial virus subgroups A and B: genetic variability and molecular evolutionary dynamics. J Virol 87:8213-8226. http://dx.doi.org/10.1128/JVI.03278-12.
15. Garcia O, Martin M, Dopazo J, Arbiza J, Frabasile S, Russi J, Hortal M, Perez-Brena P, Martinez I, Garcia-Barreno B. 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.
16. Knossow M, Skehel JJ. 2006. Variation and infectivity neutralization in influenza. Immunology 119:1-7. http://dx.doi.org/10.1111/j.1365-2567.2006.02421.x.
17. Garcia-Barreno B, Palomo C, Penas C, Delgado T, Perez-Brena P, Melero JA. 1989. Marked differences in the antigenic structure of human respiratory syncytial virus F and G glycoproteins. J Virol 63:925-932.
18. Martinez I, Dopazo J, Melero JA. 1997. Antigenic structure of the human respiratory syncytial virusGglycoprotein and relevance of hypermutation events for the generation of antigenic variants. J Gen Virol 78:2419-2429.
19. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882. http://dx.doi.org/10.1093/nar/25.24.4876.
20. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 93/98/NT41. Nucleic Acids Symp Ser 41:95-98.
21. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol. Evol 30:772-780. http://dx.doi.org/10.1093/molbev/mst010.
22. Kuiken C, Yusim K, Boykin L, Richardson R. 2005. The Los Alamos hepatitis C sequence database. Bioinformatics 21:379-384. http://dx.doi.org/10.1093/bioinformatics/bth485.
23. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185-1192. http://dx.doi.org/10.1093/molbev/msi103.
24. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. http://dx.doi.org/10.1186/1471-2148-7-214.
25. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818. http://dx.doi.org/10.1093/bioinformatics/14.9.817.
26. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
27. Peret TC, Hall CB, Schnabel KC, Golub JA, Anderson LJ. 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.
28. Cane PA, Matthews DA, Pringle CR. 1994. Analysis of respiratory syncytial virus strain variation in successive epidemics in one city. J Clin Microbiol 32:1-4.
29. Agoti CN, Gitahi CW, Medley GF, Cane PA, Nokes DJ. 2013. Identification of group B respiratory syncytial viruses that lack the 60-nucleotide duplication after six consecutive epidemics of total BA dominance at coastal Kenya. Influenza Other Respir Viruses 7:1008-1012. http://dx.doi.org/10.1111/irv.12131.
30. Houspie L, Lemey P, Keyaerts E, Reijmen E, Vergote V, Vankeerberghen A, Vaeyens F, De BH, Van RM. 2013. Circulation of HRSV in Belgium: from multiple genotype circulation to prolonged circulation of predominant genotypes. PLoS One 8:e60416. http://dx.doi.org/10.1371/journal.pone.0060416.
31. Eshaghi A, Duvvuri VR, Lai R, Nadarajah JT, Li A, Patel SN, Low DE, Gubbay JB. 2012. Genetic variability of human respiratory syncytial virus A strains circulating in Ontario: a novel genotype with a 72 nucleotide G gene duplication. PLoS One 7:e32807. http://dx.doi.org/10.1371/journal.pone.0032807.
32. Prifert C, Streng A, Krempl CD, Liese J, Weissbrich B. 2013. Novel respiratory syncytial virus a genotype, Germany, 2011-2012. Emerg Infect Dis 19:1029-1030. http://dx.doi.org/10.3201/eid1906.121582.
33. Martinelli M, Frati ER, Zappa A, Ebranati E, Bianchi S, Pariani E, Amendola A, Zehender G, Tanzi E. 2014. Phylogeny and population dynamics of respiratory syncytial virus (Rsv) A and B. Virus Res 189:293-302. http://dx.doi.org/10.1016/j.virusres.2014.06.006.
34. Agoti CN, Otieno JR, Gitahi CW, Cane PA, Nokes DJ. 2014. Rapid spread and diversification of respiratory syncytial virus genotype ON1, Kenya. Emerg Infect Dis 20:950-959. http://dx.doi.org/10.3201/eid2006.131438.
35. Galiano MC, Luchsinger V, Videla CM, De Souza L, Puch SS, Palomo C, Ricarte C, Ebekian B, Avendano L, Carballal G. 2005. Intragroup antigenic diversity of human respiratory syncytial virus (group A) isolated in Argentina and Chile. J Med Virol 77:311-316. http://dx.doi.org/10.1002/jmv.20456.
36. Adams O, Werzmirzowsky J, Hengel H. 2013. Genetic analysis and antigenic characterization of human respiratory syncytial virus group A viruses isolated in Germany 1996-2008. Virus Genes 47:210-218. http://dx.doi.org/10.1007/s11262-013-0936-9.
37. Garcia-Barreno B, Delgado T, Akerlind-Stopner B, Norrby E, Melero JA. 1992. Location of the epitope recognized by monoclonal antibody 63G on the primary structure of human respiratory syncytial virus G glycoprotein and the ability of synthetic peptides containing this epitope to induce neutralizing antibodies. J Gen Virol 73:2625-2630. http://dx.doi.org/10.1099/0022-1317-73-10-2625.
38. Palomo C, Garcia-Barreno B, Penas C, Melero JA. 1991. The G protein of human respiratory syncytial virus: significance of carbohydrate sidechains and the C-terminal end to its antigenicity. J Gen Virol 72:669-675. http://dx.doi.org/10.1099/0022-1317-72-3-669.
39. Trento A, Casas I, Calderon A, Garcia-Garcia ML, Calvo C, Perez-Brena P, Melero JA. 2010. Ten years of global evolution of the human respiratory syncytial virus BA genotype with a 60-nucleotide duplication in the G protein gene. J Virol 84:7500-7512. http://dx.doi.org/10.1128/JVI.00345-10.
40. Henderson FW, Collier AM, Clyde WA, Jr, Denny FW. 1979. Respiratory-syncytial-virus infections, reinfections and immunity. A prospective, longitudinal study in young children. N Engl J Med 300:530-534.
41. Galiano MC, Palomo C, Videla CM, Arbiza J, Melero JA, Carballal G. 2005. Genetic and antigenic variability of human respiratory syncytial virus (groups a and b) isolated over seven consecutive seasons in Argentina (1995 to 2001). J Clin Microbiol 43:2266-2273. http://dx.doi.org/10.1128/JCM.43.5.2266-2273.2005.
42. Cane PA. 1997. Analysis of linear epitopes recognised by the primary human antibody response to a variable region of the attachment (G) protein of respiratory syncytial virus. J Med Virol 51:297-304. http://dx.doi.org/10.1002/(SICI)1096-9071(199704)51:4<297::AID-JMV7>3.0.CO;2-0.
43. Anderson LJ, Bingham P, Hierholzer JC. 1988. Neutralization of respiratory syncytial virus by individual and mixtures of F and G protein monoclonal antibodies. J Virol 62:4232-4238.
44. Magro M, Mas V, Chappell K, Vazquez M, Cano O, Luque D, Terron MC, Melero JA, Palomo C. 2012. Neutralizing antibodies against the preactive form of respiratory syncytial virus fusion protein offer unique possibilities for clinical intervention. Proc Natl Acad Sci USA 109:3089-3094. http://dx.doi.org/10.1073/pnas.1115941109.
45. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A, Modjarrad K, Zheng Z, Zhao M, Xia N, Kwong PD, Graham BS. 2013. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340:1113-1117. http://dx.doi.org/10.1126/science.1234914.
46. Yui I, Fujino M, Sawada A, Nakayama T. 2014. Novel clinical features of recurrent human respiratory syncytial virus infections. J Med Virol 86: 1629-1638. http://dx.doi.org/10.1002/jmv.23809.
47. Agoti CN, Mwihuri AG, Sande CJ, Onyango CO, Medley GF, Cane PA, Nokes DJ. 2012. Genetic relatedness of infecting and reinfecting respiratory syncytial virus strains identified in a birth cohort from rural kenya. J Infect Dis 206:1532-1541. http://dx.doi.org/10.1093/infdis/jis570.
48. Sande CJ, Mutunga MN, Medley GF, Cane PA, Nokes DJ. 2013. Groupand genotype-specific neutralizing antibody responses against respiratory syncytial virus in infants and young children with severe pneumonia. J Infect Dis 207:489-492. http://dx.doi.org/10.1093/infdis/jis700.
49. Zlateva KT, Lemey P, Vandamme AM, Van RM. 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. http://dx.doi.org/10.1128/JVI.78.9.4675-4683.2004.
50. Gaunt ER, Jansen RR, Poovorawan Y, Templeton KE, Toms GL, Simmonds P. 2011. Molecular epidemiology and evolution of human respiratory syncytial virus and human metapneumovirus. PLoS One 6:e17427. http://dx.doi.org/10.1371/journal.pone.0017427.
51. Pretorius MA, van NS, Tempia S, Moyes J, Cohen C, Madhi SA, Venter M. 2013. Replacement and positive evolution of subtype A and B respiratory syncytial virus G-protein genotypes from 1997-2012 in South Africa. J Infect Dis 208(Suppl 3):S227-S237. http://dx.doi.org/10.1093/infdis/jit477.
52. Kim YJ, Kim DW, Lee WJ, Yun MR, Lee HY, Lee HS, Jung HD, Kim K. 2014. Rapid replacement of human respiratory syncytial virus A with the ON1 genotype having 72 nucleotide duplication in G gene. Infect Genet Evol 26:103-112. http://dx.doi.org/10.1016/j.meegid.2014.05.007.
53. Botosso VF, Zanotto PM, Ueda M, Arruda E, Gilio AE, Vieira SE, Stewien KE, Peret TC, Jamal LF, Pardini MI, Pinho JR, Massad E, Sant'anna OA, Holmes EC, Durigon EL. 2009. Positive selection results in frequent reversible amino acid replacements in the G protein gene of human respiratory syncytial virus. PLoS Pathog 5:e1000254. http://dx.doi.org/10.1371/journal.ppat.1000254.