1887

Abstract

In spite of the success of the mumps vaccination, recent mumps outbreaks have been reported even among individuals with a history of mumps vaccination. For a better understanding of why the vaccination failed in cases of vaccinees who fell ill during recent mumps outbreaks, the immunological events during infection and/or vaccination should be better defined. In the work presented here we sought to identify new neutralization sites on the mumps virus surface glycoproteins. By using anti-mumps mAbs, three amino acid positions at residues 221, 323 and 373 in the F protein of mumps virus were shown to be located in at least two conformational neutralization epitopes. mAbs that specifically target these sites effectively neutralized mumps virus . The newly acquired glycosylation site at position 373 or loss of the existing one at position 323 was identified as the mechanism behind the escape from the specific mAbs. Based on the findings of this study, we suggest that the influence of the antigenic structure of the F protein should not be ignored in a thorough investigation of the underlying mechanism of the mumps vaccine failure or when making a strategy for development of a new vaccine.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.000059
2015-05-01
2019-11-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/5/982.html?itemId=/content/journal/jgv/10.1099/vir.0.000059&mimeType=html&fmt=ahah

References

  1. Arnold K. , Bordoli L. , Kopp J. , Schwede T. . ( 2006; ). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. . Bioinformatics 22:, 195–201. [CrossRef] [PubMed]
    [Google Scholar]
  2. Biasini M. , Bienert S. , Waterhouse A. , Arnold K. , Studer G. , Schmidt T. , Kiefer F. , Cassarino T. G. , Bertoni M. et al. ( 2014; ). SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. . Nucleic Acids Res 42: (Web Server issue), W252–W258. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bordoli L. , Kiefer F. , Arnold K. , Benkert P. , Battey J. , Schwede T. . ( 2009; ). Protein structure homology modeling using SWISS-MODEL workspace. . Nat Protoc 4:, 1–13. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bose S. , Heath C. M. , Shah P. A. , Alayyoubi M. , Jardetzky T. S. , Lamb R. A. . ( 2013; ). Mutations in the parainfluenza virus 5 fusion protein reveal domains important for fusion triggering and metastability. . J Virol 87:, 13520–13531. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chang A. , Dutch R. E. . ( 2012; ). Paramyxovirus fusion and entry: multiple paths to a common end. . Viruses 4:, 613–636. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chomczynski P. , Sacchi N. . ( 1987; ). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. . Anal Biochem 162:, 156–159. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cohen B. J. , Audet S. , Andrews N. , Beeler J. . WHO working group on measles plaque reduction neutralization test ( 2007; ). Plaque reduction neutralization test for measles antibodies: Description of a standardised laboratory method for use in immunogenicity studies of aerosol vaccination. . Vaccine 26:, 59–66. [CrossRef] [PubMed]
    [Google Scholar]
  8. Cseke G. , Wright D. W. , Tollefson S. J. , Johnson J. E. , Crowe J. E. Jr , Williams J. V. . ( 2007; ). Human metapneumovirus fusion protein vaccines that are immunogenic and protective in cotton rats. . J Virol 81:, 698–707. [CrossRef] [PubMed]
    [Google Scholar]
  9. Cusi M. G. , Fischer S. , Sedlmeier R. , Valassina M. , Valensin P. E. , Donati M. , Neubert W. J. . ( 2001; ). Localization of a new neutralizing epitope on the mumps virus hemagglutinin-neuraminidase protein. . Virus Res 74:, 133–137. [CrossRef] [PubMed]
    [Google Scholar]
  10. Dayan G. H. , Rubin S. . ( 2008; ). Mumps outbreaks in vaccinated populations: are available mumps vaccines effective enough to prevent outbreaks?. Clin Infect Dis 47:, 1458–1467. [CrossRef] [PubMed]
    [Google Scholar]
  11. de St Groth S. F. , Scheidegger D. . ( 1980; ). Production of monoclonal antibodies: strategy and tactics. . J Immunol Methods 35:, 1–21. [CrossRef] [PubMed]
    [Google Scholar]
  12. Forcic D. , Kosutić-Gulija T. , Santak M. , Jug R. , Ivancic-Jelecki J. , Markusic M. , Mazuran R. . ( 2010; ). Comparisons of mumps virus potency estimates obtained by 50% cell culture infective dose assay and plaque assay. . Vaccine 28:, 1887–1892. [CrossRef] [PubMed]
    [Google Scholar]
  13. Homan E. J. , Bremel R. D. . ( 2014; ). Are cases of mumps in vaccinated patients attributable to mismatches in both vaccine T-cell and B-cell epitopes?. . Hum Vaccin Immunother 10:, 290–300. [CrossRef] [PubMed]
    [Google Scholar]
  14. Houard S. , Varsanyi T. M. , Milican F. , Norrby E. , Bollen A. . ( 1995; ). Protection of hamsters against experimental mumps virus (MuV) infection by antibodies raised against the MuV surface glycoproteins expressed from recombinant vaccinia virus vectors. . J Gen Virol 76:, 421–423. [CrossRef] [PubMed]
    [Google Scholar]
  15. Johansen P. G. , Marshall R. D. , Neuberger A. . ( 1961; ). Carbohydrates in protein. 3. The preparation and some of the properties of a glycopeptide from hen’s-egg albumin. . Biochem J 78:, 518–527.[PubMed] [CrossRef]
    [Google Scholar]
  16. Kövamees J. , Rydbeck R. , Örvell C. , Norrby E. . ( 1990; ). Hemagglutinin-neuraminidase (HN) amino acid alterations in neutralization escape mutants of Kilham mumps virus. . Virus Res 17:, 119–129. [CrossRef] [PubMed]
    [Google Scholar]
  17. Lamb R. A. , Paterson R. G. , Jardetzky T. S. . ( 2006; ). Paramyxovirus membrane fusion: lessons from the F and HN atomic structures. . Virology 344:, 30–37. [CrossRef] [PubMed]
    [Google Scholar]
  18. Mahy B. W. J. , Kangro H. O. . ( 1995; ). Haemagglutination. . In Virology methods manuals, pp. 41–43. Edited by Mahy B.W.J. , Kangro H.O. . . London, UK:: Academic Press;.
    [Google Scholar]
  19. Malley R. , DeVincenzo J. , Ramilo O. , Dennehy P. H. , Meissner H. C. , Gruber W. C. , Sanchez P. J. , Jafri H. , Balsley J. et al. ( 1998; ). Reduction of respiratory syncytial virus (RSV) in tracheal aspirates in intubated infants by use of humanized monoclonal antibody to RSV F protein. . J Infect Dis 178:, 1555–1561. [CrossRef] [PubMed]
    [Google Scholar]
  20. Merz D. C. , Scheid A. , Choppin P. W. . ( 1980; ). Importance of antibodies to the fusion glycoprotein of paramyxoviruses in the prevention of spread of infection. . J Exp Med 151:, 275–288. [CrossRef] [PubMed]
    [Google Scholar]
  21. Norrby E. , Utter G. , Örvell C. , Appel M. J. . ( 1986; ). Protection against canine distemper virus in dogs after immunization with isolated fusion protein. . J Virol 58:, 536–541.[PubMed]
    [Google Scholar]
  22. Örvell C. . ( 1978; ). Structural polypeptides of mumps virus. . J Gen Virol 41:, 527–539. [CrossRef] [PubMed]
    [Google Scholar]
  23. Örvell C. . ( 1984; ). The reactions of monoclonal antibodies with structural proteins of mumps virus. . J Immunol 132:, 2622–2629.[PubMed]
    [Google Scholar]
  24. Örvell C. , Grandien M. . ( 1982; ). The effects of monoclonal antibodies on biologic activities of structural proteins of Sendai virus. . J Immunol 129:, 2779–2787.[PubMed]
    [Google Scholar]
  25. Örvell C. , Alsheikhly A. R. , Kalantari M. , Johansson B. . ( 1997; ). Characterization of genotype-specific epitopes of the HN protein of mumps virus. . J Gen Virol 78:, 3187–3193.[PubMed] [CrossRef]
    [Google Scholar]
  26. Paterson R. G. , Lamb R. A. , Moss B. , Murphy B. R. . ( 1987; ). Comparison of the relative roles of the F and HN surface glycoproteins of the paramyxovirus simian virus 5 in inducing protective immunity. . J Virol 61:, 1972–1977.[PubMed]
    [Google Scholar]
  27. Rubin S. A. , Link M. A. , Sauder C. J. , Zhang C. , Ngo L. , Rima B. K. , Duprex W. P. . ( 2012; ). Recent mumps outbreaks in vaccinated populations: no evidence of immune escape. . J Virol 86:, 615–620. [CrossRef] [PubMed]
    [Google Scholar]
  28. Šantak M. , Kosutić-Gulija T. , Tesović G. , Ljubin-Sternak S. , Gjenero-Margan I. , Betica-Radić L. , Forcić D. . ( 2006; ). Mumps virus strains isolated in Croatia in 1998 and 2005: Genotyping and putative antigenic relatedness to vaccine strains. . J Med Virol 78:, 638–643. [CrossRef] [PubMed]
    [Google Scholar]
  29. Šantak M. , Lang-Balija M. , Ivancic-Jelecki J. , Košutić-Gulija T. , Ljubin-Sternak S. , Forcic D. . ( 2013; ). Antigenic differences between vaccine and circulating wild-type mumps viruses decreases neutralization capacity of vaccine-induced antibodies. . Epidemiol Infect 141:, 1298–1309. [CrossRef] [PubMed]
    [Google Scholar]
  30. Tecle T. , Johansson B. , Yun Z. , Örvell C. . ( 2000; ). Antigenic and genetic characterization of the fusion (F) protein of mumps virus strains. . Arch Virol 145:, 1199–1210. [CrossRef] [PubMed]
    [Google Scholar]
  31. Togashi T. , Örvell C. , Vartdal F. , Norrby E. . ( 1981; ). Production of antibodies against measles virions by use of the mouse hybridoma technique. . Arch Virol 67:, 149–157. [CrossRef] [PubMed]
    [Google Scholar]
  32. Toyoda T. , Gotoh B. , Sakaguchi T. , Kida H. , Nagai Y. . ( 1988; ). Identification of amino acids relevant to three antigenic determinants on the fusion protein of Newcastle disease virus that are involved in fusion inhibition and neutralization. . J Virol 62:, 4427–4430.[PubMed]
    [Google Scholar]
  33. Wolinsky J. S. , Waxham M. N. , Server A. C. . ( 1985; ). Protective effects of glycoprotein-specific monoclonal antibodies on the course of experimental mumps virus meningoencephalitis. . J Virol 53:, 727–734.[PubMed]
    [Google Scholar]
  34. Yin H. S. , Wen X. , Paterson R. G. , Lamb R. A. , Jardetzky T. S. . ( 2006; ). Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. . Nature 439:, 38–44. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.000059
Loading
/content/journal/jgv/10.1099/vir.0.000059
Loading

Data & Media loading...

Supplements

Supplementary Data



PDF

Most Cited This Month

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