Skip to content
1887

Abstract

Respiratory syncytial virus (RSV), or human orthopneumovirus, is a major cause of acute lower respiratory infection (ALRI), particularly in young children, causing significant morbidity and mortality. We used pathogen genomics to characterize the population structure and genetic signatures of RSV isolates circulating in children in New South Wales between 2016 and 2018 and to understand the evolutionary dynamics of these strains in the context of publicly available RSV genomes from the region and globally. Whole-genome phylogenetic analysis demonstrated the co-circulation of a few major RSV clades in the paediatric population from Sydney. The whole-genome-based genotypes A23 (RSV-A ON1-like genotype) and B6 (RSV-B BA9-like genotype) were the predominant RSV-A and RSV-B genotypes circulating during the study period, respectively. These genotypes were characterized with high levels of diversity of predicted N- and O-linked glycosylation patterns in both the G and F glycoproteins. Interestingly, a novel 72-nucleotide triplication in the sequence that corresponds to the C-terminal region of the gene was identified in four of the A23 genotype sequenced in this study. Consistently, the population dynamics analysis demonstrated a continuous increase in the effective population size of A23 and B6 genotypes globally. Further investigations including functional mapping of mutations and identifying the impact of sequence changes on virus fitness are highly required. This study highlights the potential impact of an integrated approach that uses WG-based phylogeny and studying selective pressure events in understanding the emergence and dissemination of RSV genotypes.

Funding
This study was supported by the:
  • Sydney Medical School Foundation
    • Principle Award Recipient: MoatazAbd El Ghany
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001095
2023-09-01
2025-05-15
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/9/mgen001095.html?itemId=/content/journal/mgen/10.1099/mgen.0.001095&mimeType=html&fmt=ahah

References

  1. Bryce J, Boschi-Pinto C, Shibuya K, Black RE. WHO estimates of the causes of death in children. Lancet 2005; 365:1147–1152 [View Article] [PubMed]
    [Google Scholar]
  2. Rudan I, Boschi-Pinto C, Biloglav Z, Mulholland K, Campbell H. Epidemiology and etiology of childhood pneumonia. Bull World Health Organ 2008; 86:408–416 [View Article] [PubMed]
    [Google Scholar]
  3. Rima B, Collins P, Easton A, Fouchier R, Kurath G et al. ICTV Virus Taxonomy Profile: Pneumoviridae. J Gen Virol 2017; 98:2912–2913 [View Article] [PubMed]
    [Google Scholar]
  4. Shi T, McAllister DA, O’Brien KL, Simoes EAF, Madhi SA et al. Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in young children in 2015: a systematic review and modelling study. Lancet 2017; 390:946–958 [View Article] [PubMed]
    [Google Scholar]
  5. Troeger C, Forouzanfar M, Rao PC, Khalil I, Brown A. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory tract infections in 195 countries: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect Dis 2017; 17:1133–1161 [View Article] [PubMed]
    [Google Scholar]
  6. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 2005; 352:1749–1759 [View Article] [PubMed]
    [Google Scholar]
  7. Li Y, Wang X, Blau DM, Caballero MT, Feikin DR et al. Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in children younger than 5 years in 2019: a systematic analysis. Lancet 2022; 399:2047–2064 [View Article] [PubMed]
    [Google Scholar]
  8. Li X, Willem L, Antillon M, Bilcke J, Jit M et al. Health and economic burden of respiratory syncytial virus (RSV) disease and the cost-effectiveness of potential interventions against RSV among children under 5 years in 72 Gavi-eligible countries. BMC Med 2020; 18:82 [View Article] [PubMed]
    [Google Scholar]
  9. Shi T, Denouel A, Tietjen AK, Campbell I, Moran E et al. Global disease burden estimates of respiratory syncytial virus-associated acute respiratory infection in older adults in 2015: a systematic review and meta-analysis. J Infect Dis 2019
    [Google Scholar]
  10. PATH Advancing RSV maternal immunization: A Gap Analysis Report. Seattle; 2018
  11. Graham BS. Vaccine development for respiratory syncytial virus. Curr Opin Virol 2017; 23:107–112 [View Article] [PubMed]
    [Google Scholar]
  12. Mejías A, Ramilo O. Review of palivizumab in the prophylaxis of respiratory syncytial virus (RSV) in high-risk infants. Biologics 2008; 2:433–439 [View Article] [PubMed]
    [Google Scholar]
  13. Shook BC, Lin K. Recent advances in developing antiviral therapies for respiratory syncytial virus. Top Curr Chem 2017; 375:40 [View Article] [PubMed]
    [Google Scholar]
  14. WHO WHO Global Respiratory Syncytial Virus Surveillance; 2017 https://www.who.int/teams/global-influenza-programme/global-respiratory-syncytial-virus-surveillance/objectives accessed 20 July 2020
  15. Collins PL, Fearns R, Graham BS. Respiratory syncytial virus: virology, reverse genetics, and pathogenesis of disease. Curr Top Microbiol Immunol 2013; 372:3–38 [View Article] [PubMed]
    [Google Scholar]
  16. Tan L, Coenjaerts FEJ, Houspie L, Viveen MC, van Bleek GM et al. The comparative genomics of human respiratory syncytial virus subgroups A and B: genetic variability and molecular evolutionary dynamics. J Virol 2013; 87:8213–8226 [View Article]
    [Google Scholar]
  17. Grosfeld H, Hill MG, Collins PL. RNA replication by respiratory syncytial virus (RSV) is directed by the N, P, and L proteins; transcription also occurs under these conditions but requires RSV superinfection for efficient synthesis of full-length mRNA. J Virol 1995; 69:5677–5686 [View Article] [PubMed]
    [Google Scholar]
  18. Yu Q, Hardy RW, Wertz GW. Functional cDNA clones of the human respiratory syncytial (RS) virus N, P, and L proteins support replication of RS virus genomic RNA analogs and define minimal trans-acting requirements for RNA replication. J Virol 1995; 69:2412–2419 [View Article] [PubMed]
    [Google Scholar]
  19. Shaikh FY, Crowe JE. Molecular mechanisms driving respiratory syncytial virus assembly. Future Microbiol 2013; 8:123–131 [View Article] [PubMed]
    [Google Scholar]
  20. Ghildyal R, Ho A, Jans DA. Central role of the respiratory syncytial virus matrix protein in infection. FEMS Microbiol Rev 2006; 30:692–705 [View Article] [PubMed]
    [Google Scholar]
  21. McLellan JS, Ray WC, Peeples ME. Structure and function of respiratory syncytial virus surface glycoproteins. Curr Top Microbiol Immunol 2013; 372:83–104 [View Article] [PubMed]
    [Google Scholar]
  22. Meng J, Hotard AL, Currier MG, Lee S, Stobart CC et al. Respiratory syncytial virus attachment glycoprotein contribution to infection depends on the specific fusion protein. J Virol 2016; 90:245–253 [View Article] [PubMed]
    [Google Scholar]
  23. Carter SD, Dent KC, Atkins E, Foster TL, Verow M et al. Direct visualization of the small hydrophobic protein of human respiratory syncytial virus reveals the structural basis for membrane permeability. FEBS Lett 2010; 584:2786–2790 [View Article] [PubMed]
    [Google Scholar]
  24. Spann KM, Tran KC, Collins PL. Effects of nonstructural proteins NS1 and NS2 of human respiratory syncytial virus on interferon regulatory factor 3, NF-kappaB, and proinflammatory cytokines. J Virol 2005; 79:5353–5362 [View Article] [PubMed]
    [Google Scholar]
  25. Swedan S, Andrews J, Majumdar T, Musiyenko A, Barik S. Multiple functional domains and complexes of the two nonstructural proteins of human respiratory syncytial virus contribute to interferon suppression and cellular location. J Virol 2011; 85:10090–10100 [View Article] [PubMed]
    [Google Scholar]
  26. Bukreyev A, Yang L, Fricke J, Cheng L, Ward JM et al. The secreted form of respiratory syncytial virus G glycoprotein helps the virus evade antibody-mediated restriction of replication by acting as an antigen decoy and through effects on Fc receptor-bearing leukocytes. J Virol 2008; 82:12191–12204 [View Article] [PubMed]
    [Google Scholar]
  27. Sullender WM. Respiratory syncytial virus genetic and antigenic diversity. Clin Microbiol Rev 2000; 13:1–15 [View Article] [PubMed]
    [Google Scholar]
  28. Cane PA. Molecular epidemiology of respiratory syncytial virus. Rev Med Virol 2001; 11:103–116 [View Article] [PubMed]
    [Google Scholar]
  29. Pangesti KNA, Abd El Ghany M, Walsh MG, Kesson AM, Hill-Cawthorne GA. Molecular epidemiology of respiratory syncytial virus. Rev Med Virol 2018; 28: [View Article] [PubMed]
    [Google Scholar]
  30. Choi EH, Lee HJ. Genetic diversity and molecular epidemiology of the G protein of subgroups A and B of respiratory syncytial viruses isolated over 9 consecutive epidemics in Korea. J Infect Dis 2000; 181:1547–1556 [View Article] [PubMed]
    [Google Scholar]
  31. Peret TC, Hall CB, Hammond GW, Piedra PA, Storch GA et al. Circulation patterns of group A and B human respiratory syncytial virus genotypes in 5 communities in North America. J Infect Dis 2000; 181:1891–1896 [View Article] [PubMed]
    [Google Scholar]
  32. Liang X, Liu D-H, Chen D, Guo L, Yang H et al. Gradual replacement of all previously circulating respiratory syncytial virus A strain with the novel ON1 genotype in Lanzhou from 2010 to 2017. Medicine 2019; 98:e15542 [View Article] [PubMed]
    [Google Scholar]
  33. Agoti CN, Otieno JR, Gitahi CW, Cane PA, Nokes DJ. Rapid spread and diversification of respiratory syncytial virus genotype ON1, Kenya. Emerg Infect Dis 2014; 20:950–959 [View Article]
    [Google Scholar]
  34. Scott PD, Ochola R, Ngama M, Okiro EA, James Nokes D et al. Molecular analysis of respiratory syncytial virus reinfections in infants from coastal Kenya. J Infect Dis 2006; 193:59–67 [View Article] [PubMed]
    [Google Scholar]
  35. Agoti CN, Mwihuri AG, Sande CJ, Onyango CO, Medley GF et al. Genetic relatedness of infecting and reinfecting respiratory syncytial virus strains identified in a birth cohort from rural Kenya. J Infect Dis 2012; 206:1532–1541 [View Article] [PubMed]
    [Google Scholar]
  36. Rodriguez-Fernandez R, Tapia LI, Yang C-F, Torres JP, Chavez-Bueno S et al. Respiratory syncytial virus genotypes, host immune profiles, and disease severity in young children hospitalized with bronchiolitis. J Infect Dis 2018; 217:24–34 [View Article]
    [Google Scholar]
  37. Streng A, Goettler D, Haerlein M, Lehmann L, Ulrich K et al. Spread and clinical severity of respiratory syncytial virus A genotype ON1 in Germany, 2011-2017. BMC Infect Dis 2019; 19:613 [View Article] [PubMed]
    [Google Scholar]
  38. Tran DN, Pham TMH, Ha MT, Tran TTL, Dang TKH et al. Molecular epidemiology and disease severity of human respiratory syncytial virus in Vietnam. PLoS One 2013; 8:e45436 [View Article] [PubMed]
    [Google Scholar]
  39. Boyoglu-Barnum S, Chirkova T, Anderson LJ. Biology of infection and disease pathogenesis to guide RSV vaccine development. Front Immunol 2019; 10:1675 [View Article] [PubMed]
    [Google Scholar]
  40. Okamoto M, Sakamoto M, Dapat C, Saito M, Saito-Obata M et al. Complete genome sequences of 12 human respiratory syncytial virus (human Ort Hopneumovirus) strains. Microbiol Resour Announc 2018; 7:e01017–01018 [View Article]
    [Google Scholar]
  41. Liu J, Mu Y, Dong W, Yao F, Wang L et al. Genetic variation of human respiratory syncytial virus among children with fever and respiratory symptoms in Shanghai, China, from 2009 to 2012. Infect Genet Evol 2014; 27:131–136 [View Article] [PubMed]
    [Google Scholar]
  42. Agoti CN, Otieno JR, Ngama M, Mwihuri AG, Medley GF et al. Successive respiratory syncytial virus epidemics in local populations arise from multiple variant introductions, providing insights into virus persistence. J Virol 2015; 89:11630–11642 [View Article]
    [Google Scholar]
  43. Trento A, Ábrego L, Rodriguez-Fernandez R, González-Sánchez MI, González-Martínez F et al. Conservation of G-protein epitopes in respiratory syncytial virus (Group A) despite broad genetic diversity: is antibody selection involved in virus evolution?. J Virol 2015; 89:7776–7785 [View Article] [PubMed]
    [Google Scholar]
  44. Agoti CN, Mayieka LM, Otieno JR, Ahmed JA, Fields BS et al. Examining strain diversity and phylogeography in relation to an unusual epidemic pattern of respiratory syncytial virus (RSV) in a long-term refugee camp in Kenya. BMC Infect Dis 2014; 14:178 [View Article] [PubMed]
    [Google Scholar]
  45. Ramaekers K, Rector A, Cuypers L, Lemey P, Keyaerts E et al. Towards a unified classification for human respiratory syncytial virus genotypes. Virus Evol 2020; 6:veaa052 [View Article] [PubMed]
    [Google Scholar]
  46. Nguyen TKP, Tran TH, Roberts CL, Graham SM, Marais BJ. Child pneumonia - focus on the Western Pacific Region. Paediatr Respir Rev 2017; 21:102–110 [View Article] [PubMed]
    [Google Scholar]
  47. Pangesti KNA, El Ghany MA, Kesson AM, Hill-Cawthorne GA. Respiratory syncytial virus in the Western Pacific Region: a systematic review and meta-analysis. J Glob Health 2019; 9:020431 [View Article] [PubMed]
    [Google Scholar]
  48. Saravanos GL, Sheel M, Homaira N, Dey A, Brown E et al. Respiratory syncytial virus-associated hospitalisations in Australia, 2006-2015. Med J Aust 2019; 210:447–453 [View Article] [PubMed]
    [Google Scholar]
  49. Ranmuthugala G, Brown L, Lidbury BA. Respiratory syncytial virus--the unrecognised cause of health and economic burden among young children in Australia. Commun Dis Intell Q Rep 2011; 35:177–184 [PubMed]
    [Google Scholar]
  50. Di Giallonardo F, Kok J, Fernandez M, Carter I, Geoghegan JL et al. Evolution of human Respiratory Syncytial Virus (RSV) over multiple seasons in New South Wales, Australia. Viruses 2018; 10:476 [View Article] [PubMed]
    [Google Scholar]
  51. Robertson M, Eden J-S, Levy A, Carter I, Tulloch RL et al. The spatial-temporal dynamics of respiratory syncytial virus infections across the East-West Coasts of Australia during 2016-17. Virus Evol 2021; 7:veab068 [View Article] [PubMed]
    [Google Scholar]
  52. Eden J-S, Sikazwe C, Xie R, Deng Y-M, Sullivan SG et al. Off-season RSV epidemics in Australia after easing of COVID-19 restrictions. Nat Commun 2022; 13:2884 [View Article] [PubMed]
    [Google Scholar]
  53. Agoti CN, Otieno JR, Munywoki PK, Mwihuri AG, Cane PA et al. Local evolutionary patterns of human respiratory syncytial virus derived from whole-genome sequencing. J Virol 2015; 89:3444–3454 [View Article]
    [Google Scholar]
  54. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  55. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
    [Google Scholar]
  56. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  57. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011; 29:644–652 [View Article] [PubMed]
    [Google Scholar]
  58. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  59. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  60. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  61. Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL et al. MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol 2018; 14:e1005944 [View Article] [PubMed]
    [Google Scholar]
  62. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article] [PubMed]
    [Google Scholar]
  63. Wang S, Sundaram JP, Spiro D. VIGOR, an annotation program for small viral genomes. BMC Bioinformatics 2010; 11:451 [View Article] [PubMed]
    [Google Scholar]
  64. Berriman M, Rutherford K. Viewing and annotating sequence data with Artemis. Briefings in Bioinformatics 2003; 4:124–132 [View Article]
    [Google Scholar]
  65. Carver T, Berriman M, Tivey A, Patel C, Böhme U et al. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 2008; 24:2672–2676 [View Article] [PubMed]
    [Google Scholar]
  66. Kuraku S, Zmasek CM, Nishimura O, Katoh K. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res 2013; 41:W22–8 [View Article] [PubMed]
    [Google Scholar]
  67. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  68. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
    [Google Scholar]
  69. Sagulenko P, Puller V, Neher RA. Treetime: maximum-likelihood phylodynamic analysis. Virus Evol 2018; 4:vex042 [View Article] [PubMed]
    [Google Scholar]
  70. R. Gupta EJaSB NetNGlyc 1.0 Server; 2004 https://services.healthtech.dtu.dk/services/NetNGlyc-1.0/ accessed 20 July 2020
  71. Hansen JE, Lund O, Tolstrup N, Gooley AA, Williams KL et al. NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj J 1998; 15:115–130 [View Article] [PubMed]
    [Google Scholar]
  72. Wickham H. ggplot2 Elegant Graphics for Data Analysis, 2nd ed. 2016 ed Cham: Springer International Publishing; 2016
    [Google Scholar]
  73. Schobel SA, Stucker KM, Moore ML, Anderson LJ, Larkin EK et al. Respiratory syncytial virus whole-genome sequencing identifies convergent evolution of sequence duplication in the C-terminus of the G gene. Sci Rep 2016; 6:26311 [View Article] [PubMed]
    [Google Scholar]
  74. Graf EH, Simmon KE, Tardif KD, Hymas W, Flygare S et al. Unbiased detection of respiratory viruses by use of RNA sequencing-based metagenomics: a systematic comparison to a commercial PCR panel. J Clin Microbiol 2016; 54:1000–1007 [View Article] [PubMed]
    [Google Scholar]
  75. O’Flaherty BM, Li Y, Tao Y, Paden CR, Queen K et al. Comprehensive viral enrichment enables sensitive respiratory virus genomic identification and analysis by next generation sequencing. Genome Res 2018; 28:869–877 [View Article] [PubMed]
    [Google Scholar]
  76. Malboeuf CM, Yang X, Charlebois P, Qu J, Berlin AM et al. Complete viral RNA genome sequencing of ultra-low copy samples by sequence-independent amplification. Nucleic Acids Res 2013; 41:e13 [View Article] [PubMed]
    [Google Scholar]
  77. Kumaria R, Iyer LR, Hibberd ML, Simões EAF, Sugrue RJ. Whole genome characterization of non-tissue culture adapted HRSV strains in severely infected children. Virol J 2011; 8:372 [View Article] [PubMed]
    [Google Scholar]
  78. Goya S, Valinotto LE, Tittarelli E, Rojo GL, Nabaes Jodar MS et al. An optimized methodology for whole genome sequencing of RNA respiratory viruses from nasopharyngeal aspirates. PLoS One 2018; 13:e0199714 [View Article] [PubMed]
    [Google Scholar]
  79. Beerenwinkel N, Günthard HF, Roth V, Metzner KJ. Challenges and opportunities in estimating viral genetic diversity from next-generation sequencing data. Front Microbio 2012; 3:329 [View Article]
    [Google Scholar]
  80. Manso CF, Bibby DF, Mbisa JL. Efficient and unbiased metagenomic recovery of RNA virus genomes from human plasma samples. Sci Rep 2017; 7:4173 [View Article] [PubMed]
    [Google Scholar]
  81. Holmes EC. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol 2003; 11:543–546 [View Article] [PubMed]
    [Google Scholar]
  82. Maurier F, Beury D, Fléchon L, Varré JS, Touzet H et al. A complete protocol for whole-genome sequencing of virus from clinical samples: application to Coronavirus Oc43. Virology 2019; 531:141–148
    [Google Scholar]
  83. Grad YH, Newman R, Zody M, Yang X, Murphy R et al. Within-host whole-genome deep sequencing and diversity analysis of human respiratory syncytial virus infection reveals dynamics of genomic diversity in the absence and presence of immune pressure. J Virol 2014; 88:7286–7293
    [Google Scholar]
  84. Lau JW, Kim Y-I, Murphy R, Newman R, Yang X et al. Deep sequencing of RSV from an adult challenge study and from naturally infected infants reveals heterogeneous diversification dynamics. Virology 2017; 510:289–296 [View Article] [PubMed]
    [Google Scholar]
  85. Langedijk AC, Lebbink RJ, Naaktgeboren C, Evers A, Viveen MC et al. Global molecular diversity of RSV - the “INFORM RSV” study. BMC Infect Dis 2020; 20:450 [View Article] [PubMed]
    [Google Scholar]
  86. Chen J, Qiu X, Avadhanula V, Shepard SS, Kim D et al. Novel and extendable genotyping system for human respiratory syncytial virus based on whole‐genome sequence analysis. Influenza Resp Viruses 2022; 16:492–500 [View Article]
    [Google Scholar]
  87. Goya S, Galiano M, Nauwelaers I, Trento A, Openshaw PJ et al. Toward unified molecular surveillance of RSV: a proposal for genotype definition. Influenza Other Respi Viruses 2020; 14:274–285 [View Article]
    [Google Scholar]
  88. Melero JA, Mas V, McLellan JS. Structural, antigenic and immunogenic features of respiratory syncytial virus glycoproteins relevant for vaccine development. Vaccine 2017; 35:461–468 [View Article]
    [Google Scholar]
  89. Zimmer G, Trotz I, Herrler G. N-glycans of F protein differentially affect fusion activity of human respiratory syncytial virus. J Virol 2001; 75:4744–4751 [View Article]
    [Google Scholar]
  90. García-beato R, Martínez I, Francí C, Real FX, García-barreno B. Host cell effect upon glycosylation and antigenicity of human respiratory syncytial virus G glycoprotein. Virology 1996; 221:301–309 [View Article]
    [Google Scholar]
  91. Leemans A, Boeren M, Van der Gucht W, Pintelon I, Roose K et al. Removal of the N-glycosylation sequon at position N116 located in p27 of the respiratory syncytial virus fusion protein elicits enhanced antibody responses after DNA immunization. Viruses 2018; 10:426 [View Article] [PubMed]
    [Google Scholar]
  92. Okamoto M, Dapat CP, Sandagon AMD, Batangan-Nacion LP, Lirio IC et al. Molecular characterization of respiratory syncytial virus in children with repeated infections with subgroup B in the Philippines. J Infect Dis 2018; 218:1045–1053 [View Article]
    [Google Scholar]
  93. Abou-El-Hassan H, Massaad E, Soudani N, Assaf-Casals A, Shaker R et al. Detection of ON1 and novel genotypes of human respiratory syncytial virus and emergence of palivizumab resistance in Lebanon. PLoS One 2019; 14:e0212687 [View Article] [PubMed]
    [Google Scholar]
  94. García-Barreno B, Palomo C, Peñas C, Delgado T, Perez-Breña P et al. Marked differences in the antigenic structure of human respiratory syncytial virus F and G glycoproteins. J Virol 1989; 63:925–932 [View Article] [PubMed]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001095
Loading
/content/journal/mgen/10.1099/mgen.0.001095
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error