1887

Abstract

On the basis of generation of an infectious cDNA clone for the BHM26 strain of bovine enterovirus cluster B (BEV-B), 22 sites on different loops of the BHM26 capsid were selected according to an alignment of its sequence with the structural motifs of BEV-A strain VG-5-27 for insertion of the foot-and-mouth disease virus (FMDV) type O-conserved neutralizing epitope 8E8. Two recombinant viruses, rBEV-A1 and rBEV-DE, in which the FMDV epitope was inserted into the VP1 B–C or D–E loops, were rescued by transfection of BHK-21 cells with the -transcribed RNA of the recombinant BHM26 genome-length cDNA constructs. The two epitope-inserted viruses were genetically stable and exhibited growth properties similar to those of their parental virus in BHK-21 and IBRS-2 cells, which are susceptible to both BEV and FMDV. However, the two recombinant BEVs (rBEVs) had a significantly lower growth titre than those of the parental virus BHM26 in MDBK and Marc145 cells, which are susceptible to BEV but not to FMDV. These results indicated that insertion of the FMDV epitope into the VP1 B–C or D–E loops of the BEV particle altered the replication properties of BEV. In addition, the two rBEVs were sensitive to neutralization by the FMDV type O-specific mAb 8E8, and anti-FMDV IgG antibodies were induced in mice by intramuscular inoculation with the rBEV-A1 and rBEV-DE viruses. Our results demonstrate that the VP1 B–C and D–E loops of the BEV-B particle can effectively display a foreign epitope, making this an attractive approach for the design of BEV-vectored and epitope-based vaccines.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.057745-0
2013-12-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/12/2691.html?itemId=/content/journal/jgv/10.1099/vir.0.057745-0&mimeType=html&fmt=ahah

References

  1. Arnold G. F. , Velasco P. K. , Holmes A. K. , Wrin T. , Geisler S. C. , Phung P. , Tian Y. , Resnick D. A. , Ma X. . & other authors ( 2009; ). Broad neutralization of human immunodeficiency virus type 1 (HIV-1) elicited from human rhinoviruses that display the HIV-1 gp41 ELDKWA epitope. . J Virol 83:, 5087–5100. [CrossRef] [PubMed]
    [Google Scholar]
  2. Berinstein A. , Roivainen M. , Hovi T. , Mason P. W. , Baxt B. . ( 1995; ). Antibodies to the vitronectin receptor (integrin αVβ3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. . J Virol 69:, 2664–2666.[PubMed]
    [Google Scholar]
  3. Chai Z. , Wang H. , Zhou G. , Yang D. , Wang J. , Yu L. . ( 2013; ). Adenovirus-vectored type Asia1 foot-and-mouth disease virus (FMDV) capsid proteins as a vehicle to display a conserved, neutralising epitope of type O FMDV. . J Virol Methods 188:, 175–182. [CrossRef] [PubMed]
    [Google Scholar]
  4. Chu J. Q. , Lee Y. J. , Park J. N. , Kim S. M. , Lee K. N. , Ko Y. J. , Lee H. S. , Cho I. S. , Kim B. , Park J. H. . ( 2013; ). Construction of a bovine enterovirus-based vector expressing a foot-and-mouth disease virus epitope. . J Virol Methods 189:, 101–104. [CrossRef] [PubMed]
    [Google Scholar]
  5. Draper S. J. , Heeney J. L. . ( 2010; ). Viruses as vaccine vectors for infectious diseases and cancer. . Nat Rev Microbiol 8:, 62–73. [CrossRef] [PubMed]
    [Google Scholar]
  6. Duque H. , Baxt B. . ( 2003; ). Foot-and-mouth disease virus receptors: comparison of bovine αV integrin utilization by type A and O viruses. . J Virol 77:, 2500–2511. [CrossRef] [PubMed]
    [Google Scholar]
  7. Eckhart L. , Raffelsberger W. , Ferko B. , Klima A. , Purtscher M. , Katinger H. , Rüker F. . ( 1996; ). Immunogenic presentation of a conserved gp41 epitope of human immunodeficiency virus type 1 on recombinant surface antigen of hepatitis B virus. . J Gen Virol 77:, 2001–2008. [CrossRef] [PubMed]
    [Google Scholar]
  8. Evans D. J. , McKeating J. , Meredith J. M. , Burke K. L. , Katrak K. , John A. , Ferguson M. , Minor P. D. , Weiss R. A. , Almond J. W. . ( 1989; ). An engineered poliovirus chimaera elicits broadly reactive HIV-1 neutralizing antibodies. . Nature 339:, 385–388, 340. [CrossRef] [PubMed]
    [Google Scholar]
  9. Fox G. , Parry N. R. , Barnett P. V. , McGinn B. , Rowlands D. J. , Brown F. . ( 1989; ). The cell attachment site on foot-and-mouth disease virus includes the amino acid sequence RGD (arginine-glycine-aspartic acid). . J Gen Virol 70:, 625–637. [CrossRef] [PubMed]
    [Google Scholar]
  10. Goens S. D. , Botero S. , Zemla A. , Zhou C. E. , Perdue M. L. . ( 2004; ). Bovine enterovirus 2: complete genomic sequence and molecular modelling of a reference strain and a wild-type isolate from endemically infected US cattle. . J Gen Virol 85:, 3195–3203. [CrossRef] [PubMed]
    [Google Scholar]
  11. Hoey E. M. , Martin S. J. . ( 1974; ). A possible precursor containing RNA of a bovine enterovirus: the provirion 11. . J Gen Virol 24:, 515–524. [CrossRef] [PubMed]
    [Google Scholar]
  12. Huck R. A. , Cartwright S. F. . ( 1964; ). Isolation and classification of viruses from cattle during outbreaks of mucosal or respiratory disease and from herds with reproductive disorders. . J Comp Pathol 74:, 346–365.[PubMed] [CrossRef]
    [Google Scholar]
  13. Jackson T. , Sheppard D. , Denyer M. , Blakemore W. , King A. M. . ( 2000; ). The epithelial integrin αvβ6 is a receptor for foot-and-mouth disease virus. . J Virol 74:, 4949–4956. [CrossRef] [PubMed]
    [Google Scholar]
  14. Jackson T. , Mould A. P. , Sheppard D. , King A. M. . ( 2002; ). Integrin αvβ1 is a receptor for foot-and-mouth disease virus. . J Virol 76:, 935–941. [CrossRef] [PubMed]
    [Google Scholar]
  15. Jackson T. , Clark S. , Berryman S. , Burman A. , Cambier S. , Mu D. , Nishimura S. , King A. M. . ( 2004; ). Integrin αvβ8 functions as a receptor for foot-and-mouth disease virus: role of the β-chain cytodomain in integrin-mediated infection. . J Virol 78:, 4533–4540. [CrossRef] [PubMed]
    [Google Scholar]
  16. Kärber G. . ( 1931; ). Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. . Arch Exp Pathol Pharmak 162:, 480–483. [CrossRef] [PubMed]
    [Google Scholar]
  17. Kitson J. D. , Burke K. L. , Pullen L. A. , Belsham G. J. , Almond J. W. . ( 1991; ). Chimeric polioviruses that include sequences derived from two independent antigenic sites of foot-and-mouth disease virus (FMDV) induce neutralizing antibodies against FMDV in guinea pigs. . J Virol 65:, 3068–3075.[PubMed]
    [Google Scholar]
  18. Knowles N. J. , Barnett I. T. . ( 1985; ). A serological classification of bovine enteroviruses. . Arch Virol 83:, 141–155. [CrossRef] [PubMed]
    [Google Scholar]
  19. Laird M. E. , Desrosiers R. C. . ( 2007; ). Infectivity and neutralization of simian immunodeficiency virus with FLAG epitope insertion in gp120 variable loops. . J Virol 81:, 10838–10848. [CrossRef] [PubMed]
    [Google Scholar]
  20. Ley V. , Higgins J. , Fayer R. . ( 2002; ). Bovine enteroviruses as indicators of fecal contamination. . Appl Environ Microbiol 68:, 3455–3461. [CrossRef] [PubMed]
    [Google Scholar]
  21. Li Y. , Chang J. , Wang Q. , Yu L. . ( 2012; ). Isolation of two Chinese bovine enteroviruses and sequence analysis of their complete genomes. . Arch Virol 157:, 2369–2375. [CrossRef] [PubMed]
    [Google Scholar]
  22. Mason P. W. , Rieder E. , Baxt B. . ( 1994; ). RGD sequence of foot-and-mouth disease virus is essential for infecting cells via the natural receptor but can be bypassed by an antibody-dependent enhancement pathway. . Proc Natl Acad Sci U S A 91:, 1932–1936. [CrossRef] [PubMed]
    [Google Scholar]
  23. Mattion N. M. , Reilly P. A. , DiMichele S. J. , Crowley J. C. , Weeks-Levy C. . ( 1994; ). Attenuated poliovirus strain as a live vector: expression of regions of rotavirus outer capsid protein VP7 by using recombinant Sabin 3 viruses. . J Virol 68:, 3925–3933.[PubMed]
    [Google Scholar]
  24. Mattion N. M. , Reilly P. A. , Camposano E. , Wu S. L. , DiMichele S. J. , Ishizaka S. T. , Fantini S. E. , Crowley J. C. , Weeks-Levy C. . ( 1995; ). Characterization of recombinant polioviruses expressing regions of rotavirus VP4, hepatitis B surface antigen, and herpes simplex virus type 2 glycoprotein D. . J Virol 69:, 5132–5137.[PubMed]
    [Google Scholar]
  25. Neff S. , Baxt B. . ( 2001; ). The ability of integrin αvβ3 To function as a receptor for foot-and-mouth disease virus is not dependent on the presence of complete subunit cytoplasmic domains. . J Virol 75:, 527–532. [CrossRef] [PubMed]
    [Google Scholar]
  26. Neff S. , Mason P. W. , Baxt B. . ( 2000; ). High-efficiency utilization of the bovine integrin αvβ3 as a receptor for foot-and-mouth disease virus is dependent on the bovine β3 subunit. . J Virol 74:, 7298–7306. [CrossRef] [PubMed]
    [Google Scholar]
  27. Pantophlet R. , Wang M. , Aguilar-Sino R. O. , Burton D. R. . ( 2009; ). The human immunodeficiency virus type 1 envelope spike of primary viruses can suppress antibody access to variable regions. . J Virol 83:, 1649–1659. [CrossRef] [PubMed]
    [Google Scholar]
  28. Plotkin S. A. . ( 2001; ). Immunologic correlates of protection induced by vaccination. . Pediatr Infect Dis J 20:, 63–75. [CrossRef] [PubMed]
    [Google Scholar]
  29. Reed L. J. , Muench H. . ( 1938; ). A simple method of estimating fifty percent endpoints. . Am J Epidemiol 27:, 493–497. [CrossRef] [PubMed]
    [Google Scholar]
  30. Ren X. , Sodroski J. , Yang X. . ( 2005; ). An unrelated monoclonal antibody neutralizes human immunodeficiency virus type 1 by binding to an artificial epitope engineered in a functionally neutral region of the viral envelope glycoproteins. . J Virol 79:, 5616–5624. [CrossRef] [PubMed]
    [Google Scholar]
  31. Rong R. , Bibollet-Ruche F. , Mulenga J. , Allen S. , Blackwell J. L. , Derdeyn C. A. . ( 2007; ). Role of V1V2 and other human immunodeficiency virus type 1 envelope domains in resistance to autologous neutralization during clade C infection. . J Virol 81:, 1350–1359. [CrossRef] [PubMed]
    [Google Scholar]
  32. Rossmann M. G. . ( 2002; ). Picornavirus structure overview. . In Molecular Biology of Picornaviruses, pp. 27–38. Edited by Semler B. L. , Wimmer E. . . Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  33. Seago J. , Jackson T. , Doel C. , Fry E. , Stuart D. , Harmsen M. M. , Charleston B. , Juleff N. . ( 2012; ). Characterization of epitope-tagged foot-and-mouth disease virus. . J Gen Virol 93:, 2371–2381. [CrossRef] [PubMed]
    [Google Scholar]
  34. Sedlik C. , Saron M. , Sarraseca J. , Casal I. , Leclerc C. . ( 1997; ). Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic T cells. . Proc Natl Acad Sci U S A 94:, 7503–7508. [CrossRef] [PubMed]
    [Google Scholar]
  35. Smyth M. S. , Martin J. H. . ( 2001; ). Structural, biochemical and electrostatic basis of serotype specificity in bovine enteroviruses. . Arch Virol 146:, 347–355. [CrossRef] [PubMed]
    [Google Scholar]
  36. Smyth M. , Tate J. , Hoey E. , Lyons C. , Martin S. , Stuart D. . ( 1995; ). Implications for viral uncoating from the structure of bovine enterovirus. . Nat Struct Biol 2:, 224–231. [CrossRef] [PubMed]
    [Google Scholar]
  37. Thomas J. M. , Klimstra W. B. , Ryman K. D. , Heidner H. W. . ( 2003; ). Sindbis virus vectors designed to express a foreign protein as a cleavable component of the viral structural polyprotein. . J Virol 77:, 5598–5606. [CrossRef] [PubMed]
    [Google Scholar]
  38. Varsani A. , Williamson A. L. , de Villiers D. , Becker I. , Christensen N. D. , Rybicki E. P. . ( 2003; ). Chimeric human papillomavirus type 16 (HPV-16) L1 particles presenting the common neutralizing epitope for the L2 minor capsid protein of HPV-6 and HPV-16. . J Virol 77:, 8386–8393. [CrossRef] [PubMed]
    [Google Scholar]
  39. Vieira J. , Messing J. . ( 1991; ). New pUC-derived cloning vectors with different selectable markers and DNA replication origins. . Gene 100:, 189–194. [CrossRef] [PubMed]
    [Google Scholar]
  40. Wang H. , Xue M. , Yang D. , Zhou G. , Wu D. , Yu L. . ( 2012; ). Insertion of type O-conserved neutralizing epitope into the foot-and-mouth disease virus type Asia1 VP1 G-H loop: effect on viral replication and neutralization phenotype. . J Gen Virol 93:, 1442–1448. [CrossRef] [PubMed]
    [Google Scholar]
  41. Yang D. , Zhang C. , Zhao L. , Zhou G. , Wang H. , Yu L. . ( 2011; ). Identification of a conserved linear epitope on the VP1 protein of serotype O foot-and-mouth disease virus by neutralising monoclonal antibody 8E8. . Virus Res 155:, 291–299. [CrossRef] [PubMed]
    [Google Scholar]
  42. Zell R. , Krumbholz A. , Dauber M. , Hoey E. , Wutzler P. . ( 2006; ). Molecular-based reclassification of the bovine enteroviruses. . J Gen Virol 87:, 375–385. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.057745-0
Loading
/content/journal/jgv/10.1099/vir.0.057745-0
Loading

Data & Media loading...

Supplements

Supplementary material 

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