1887

Abstract

In this study, ten sites on the N terminus and different surface variable regions (VRs) of the bovine parvovirus (BPV) VP2 capsid protein were selected according to an alignment of its sequence with that of the BPV-1 strain HADEN for insertion of the type O foot-and-mouth disease virus (FMDV) conserved neutralizing epitope 8E8. Ten epitope-chimeric BPV VP2 capsid proteins carrying the 8E8 epitope were expressed in Sf9 cells, and electron micrographs demonstrated that these fusion proteins self-assembled into virus-like particles (VLPs) with properties similar to those of natural BPV virions. Immunofluorescence assay (IFA) and Western blot analysis demonstrated that each of the ten epitope-chimeric VLPs reacted with both anti-BPV serum and anti-type O FMDV mAb 8E8. These results indicated that insertions of the 8E8 epitope at these sites on the BPV VP2 protein did not interfere with the immunoreactivity of VP2 or VLP formation, and that the exogenous epitope 8E8 was correctly expressed in BPV VLPs. In addition, anti-BPV IgG antibodies were induced in mice by intramuscular inoculation with each of the ten chimeric VLPs, indicating that the immunogenicity of the chimeric VLPs was not disrupted. Importantly, potent anti-FMDV viral neutralizing (VN) antibodies, which exhibited the highest titre of 1 : 176, were induced by two chimeric VLPs, rBPV-VLP-8E8(391) and rBPV-VLP-8E8(395), in which the 8E8 epitope was inserted into positions 391/392 and 395/396, respectively, in the VR VIII of BPV VP2. Our results demonstrated that the 391/392 and 395/396 positions in the VR VIII of the BPV VP2 protein can effectively display a foreign epitope, making this an attractive approach for the design of nanoparticle-vectored and epitope-based vaccines.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001194
2018-12-14
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/100/2/187.html?itemId=/content/journal/jgv/10.1099/jgv.0.001194&mimeType=html&fmt=ahah

References

  1. Correia BE, Bates JT, Loomis RJ, Baneyx G, Carrico C et al. Proof of principle for epitope-focused vaccine design. Nature 2014; 507:201–206 [View Article][PubMed]
    [Google Scholar]
  2. Burton DR. Antibodies, viruses and vaccines. Nat Rev Immunol 2002; 2:706–713 [View Article][PubMed]
    [Google Scholar]
  3. Burton DR, Poignard P, Stanfield RL, Wilson IA. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 2012; 337:183–186 [View Article][PubMed]
    [Google Scholar]
  4. Grubman MJ, Baxt B. Foot-and-mouth disease. Clin Microbiol Rev 2004; 17:465–493 [View Article][PubMed]
    [Google Scholar]
  5. Bachrach HL. Foot-and-mouth disease. Annu Rev Microbiol 1968; 22:201–244 [View Article][PubMed]
    [Google Scholar]
  6. Arias A, Lázaro E, Escarmís C, Domingo E. Molecular intermediates of fitness gain of an RNA virus: characterization of a mutant spectrum by biological and molecular cloning. J Gen Virol 2001; 82:1049–1060 [View Article][PubMed]
    [Google Scholar]
  7. Domingo E, Escarmís C, Baranowski E, Ruiz-Jarabo CM, Carrillo E et al. Evolution of foot-and-mouth disease virus. Virus Res 2003; 91:47–63 [View Article][PubMed]
    [Google Scholar]
  8. Sobrino F, Sáiz M, Jiménez-Clavero MA, Núñez JI, Rosas MF et al. Foot-and-mouth disease virus: a long known virus, but a current threat. Vet Res 2001; 32:1–30 [View Article][PubMed]
    [Google Scholar]
  9. Brownlie J. Strategic decisions to evaluate before implementing a vaccine programme in the face of a foot-and-mouth disease (FMD) outbreak. Vet Rec 2001; 148:358–360[PubMed]
    [Google Scholar]
  10. Doel TR. FMD vaccines. Virus Res 2003; 91:81–99 [View Article][PubMed]
    [Google Scholar]
  11. Yang D, Zhang C, Zhao L, Zhou G, Wang H et al. 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 2011; 155:291–299 [View Article][PubMed]
    [Google Scholar]
  12. Wang H, Zhao L, Li W, Zhou G, Yu L. Identification of a conformational epitope on the VP1 G-H Loop of type Asia1 foot-and-mouth disease virus defined by a protective monoclonal antibody. Vet Microbiol 2011; 148:189–199 [View Article][PubMed]
    [Google Scholar]
  13. Chai Z, Wang H, Zhou G, Yang D, Wang J et al. 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 2013; 188:175–182 [View Article][PubMed]
    [Google Scholar]
  14. Chang J, Li Y, Yang D, Wang F, Jiang Z et al. VP1 B-C and D-E loops of bovine enterovirus cluster B can effectively display foot-and-mouth disease virus type O-conserved neutralizing epitope. J Gen Virol 2013; 94:2691–2699 [View Article][PubMed]
    [Google Scholar]
  15. Seth A, Oh DB, Lim YT. Nanomaterials for enhanced immunity as an innovative paradigm in nanomedicine. Nanomedicine 2015; 10:959–975 [View Article][PubMed]
    [Google Scholar]
  16. Grgacic EV, Anderson DA. Virus-like particles: passport to immune recognition. Methods 2006; 40:60–65 [View Article][PubMed]
    [Google Scholar]
  17. Feng H, Liang M, Wang HL, Zhang T, Zhao PS et al. Recombinant canine parvovirus-like particles express foreign epitopes in silkworm pupae. Vet Microbiol 2011; 154:49–57 [View Article][PubMed]
    [Google Scholar]
  18. Reed AP, Jones EV, Miller TJ. Nucleotide sequence and genome organization of canine parvovirus. J Virol 1988; 62:266–276[PubMed]
    [Google Scholar]
  19. Gallo Calderón M, Wilda M, Boado L, Keller L, Malirat V et al. Study of canine parvovirus evolution: comparative analysis of full-length VP2 gene sequences from Argentina and international field strains. Virus Genes 2012; 44:32–39 [View Article][PubMed]
    [Google Scholar]
  20. Parrish CR. Emergence, natural history, and variation of canine, mink, and feline parvoviruses. Adv Virus Res 1990; 38:403–450[PubMed]
    [Google Scholar]
  21. Sedlik C, Saron M, Sarraseca J, Casal I, Leclerc C. Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic T cells. Proc Natl Acad Sci USA 1997; 94:7503–7508 [View Article][PubMed]
    [Google Scholar]
  22. Pan Q, He K, Huang K. Development of recombinant porcine parvovirus-like particles as an antigen carrier formed by the hybrid VP2 protein carrying immunoreactive epitope of porcine circovirus type 2. Vaccine 2008; 26:2119–2126 [View Article][PubMed]
    [Google Scholar]
  23. Amexis G, Young NS. Parvovirus B19 empty capsids as antigen carriers for presentation of antigenic determinants of dengue 2 virus. J Infect Dis 2006; 194:790–794 [View Article][PubMed]
    [Google Scholar]
  24. Kailasan S, Halder S, Gurda B, Bladek H, Chipman PR et al. Structure of an enteric pathogen, bovine parvovirus. J Virol 2015; 89:2603–2614 [View Article][PubMed]
    [Google Scholar]
  25. Gurda BL, Parent KN, Bladek H, Sinkovits RS, Dimattia MA et al. Human bocavirus capsid structure: insights into the structural repertoire of the parvoviridae. J Virol 2010; 84:5880–5889 [View Article][PubMed]
    [Google Scholar]
  26. Schellenbacher C, Roden R, Kirnbauer R. Chimeric L1-L2 virus-like particles as potential broad-spectrum human papillomavirus vaccines. J Virol 2009; 83:10085–10095 [View Article][PubMed]
    [Google Scholar]
  27. Pankrac J, Klein K, McKay PF, King DFL, Bain K et al. A heterogeneous human immunodeficiency virus-like particle (VLP) formulation produced by a novel vector system. NPJ Vaccines 2018; 3:2 [View Article][PubMed]
    [Google Scholar]
  28. Zhou Y, Zhang C, Liu Q, Gong S, Geng L et al. A virus-like particle vaccine protects mice against coxsackievirus A10 lethal infection. Antiviral Res 2018; 152:124–130 [View Article][PubMed]
    [Google Scholar]
  29. Kim AR, Lee DH, Lee SH, Rubino I, Choi HJ et al. Protection induced by virus-like particle vaccine containing tandem repeat gene of respiratory syncytial virus G protein. PLoS One 2018; 13:e0191277 [View Article][PubMed]
    [Google Scholar]
  30. Kushnir N, Streatfield SJ, Yusibov V. Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine 2012; 31:58–83 [View Article][PubMed]
    [Google Scholar]
  31. Roldão A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM. Virus-like particles in vaccine development. Expert Rev Vaccines 2010; 9:1149–1176 [View Article][PubMed]
    [Google Scholar]
  32. Woo WP, Doan T, Herd KA, Netter HJ, Tindle RW. Hepatitis B surface antigen vector delivers protective cytotoxic T-lymphocyte responses to disease-relevant foreign epitopes. J Virol 2006; 80:3975–3984 [View Article][PubMed]
    [Google Scholar]
  33. Varsani A, Williamson AL, de Villiers D, Becker I, Christensen ND et al. 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 2003; 77:8386–8393 [View Article][PubMed]
    [Google Scholar]
  34. Chen KC, Shull BC, Moses EA, Lederman M, Stout ER et al. Complete nucleotide sequence and genome organization of bovine parvovirus. J Virol 1986; 60:1085–1097[PubMed]
    [Google Scholar]
  35. Plotkin SA. Immunologic correlates of protection induced by vaccination. Pediatr Infect Dis J 2001; 20:63–75 [View Article][PubMed]
    [Google Scholar]
  36. Laird ME, Desrosiers RC. Infectivity and neutralization of simian immunodeficiency virus with FLAG epitope insertion in gp120 variable loops. J Virol 2007; 81:10838–10848 [View Article][PubMed]
    [Google Scholar]
  37. Pantophlet R, Wang M, Aguilar-Sino RO, Burton DR. The human immunodeficiency virus type 1 envelope spike of primary viruses can suppress antibody access to variable regions. J Virol 2009; 83:1649–1659 [View Article][PubMed]
    [Google Scholar]
  38. Ren X, Sodroski J, Yang X. 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 2005; 79:5616–5624 [View Article][PubMed]
    [Google Scholar]
  39. Rong R, Bibollet-Ruche F, Mulenga J, Allen S, Blackwell JL et al. Role of V1V2 and other human immunodeficiency virus type 1 envelope domains in resistance to autologous neutralization during clade C infection. J Virol 2007; 81:1350–1359 [View Article][PubMed]
    [Google Scholar]
  40. Kitson JD, Burke KL, Pullen LA, Belsham GJ, Almond JW. 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 1991; 65:3068–3075[PubMed]
    [Google Scholar]
  41. Mattion NM, Reilly PA, Dimichele SJ, Crowley JC, Weeks-Levy C. Attenuated poliovirus strain as a live vector: expression of regions of rotavirus outer capsid protein VP7 by using recombinant Sabin 3 viruses. J Virol 1994; 68:3925–3933[PubMed]
    [Google Scholar]
  42. Mattion NM, Reilly PA, Camposano E, Wu SL, Dimichele SJ et al. Characterization of recombinant polioviruses expressing regions of rotavirus VP4, hepatitis B surface antigen, and herpes simplex virus type 2 glycoprotein D. J Virol 1995; 69:5132–5137[PubMed]
    [Google Scholar]
  43. Reisdorph N, Thomas JJ, Katpally U, Chase E, Harris K et al. Human rhinovirus capsid dynamics is controlled by canyon flexibility. Virology 2003; 314:34–44 [View Article][PubMed]
    [Google Scholar]
  44. Wang H, Xue M, Yang D, Zhou G, Wu D et al. 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 2012; 93:1442–1448 [View Article][PubMed]
    [Google Scholar]
  45. Correia BE, Ban YE, Holmes MA, Xu H, Ellingson K et al. Computational design of epitope-scaffolds allows induction of antibodies specific for a poorly immunogenic HIV vaccine epitope. Structure 2010; 18:1116–1126 [View Article][PubMed]
    [Google Scholar]
  46. Ofek G, Guenaga FJ, Schief WR, Skinner J, Baker D et al. Elicitation of structure-specific antibodies by epitope scaffolds. Proc Natl Acad Sci USA 2010; 107:17880–17887 [View Article][PubMed]
    [Google Scholar]
  47. Mclellan JS, Correia BE, Chen M, Yang Y, Graham BS et al. Design and characterization of epitope-scaffold immunogens that present the motavizumab epitope from respiratory syncytial virus. J Mol Biol 2011; 409:853–866 [View Article][PubMed]
    [Google Scholar]
  48. Azoitei ML, Correia BE, Ban YE, Carrico C, Kalyuzhniy O et al. Computation-guided backbone grafting of a discontinuous motif onto a protein scaffold. Science 2011; 334:373–376 [View Article][PubMed]
    [Google Scholar]
  49. Azoitei ML, Ban YE, Julien JP, Bryson S, Schroeter A et al. Computational design of high-affinity epitope scaffolds by backbone grafting of a linear epitope. J Mol Biol 2012; 415:175–192 [View Article][PubMed]
    [Google Scholar]
  50. Pierce BG, Boucher EN, Piepenbrink KH, Ejemel M, Rapp CA et al. Structure-Based Design of Hepatitis C Virus Vaccines That Elicit Neutralizing Antibody Responses to a Conserved Epitope. J Virol 2017; 91: [View Article][PubMed]
    [Google Scholar]
  51. McCraw DM, O'Donnell JK, Taylor KA, Stagg SM, Chapman MS. Structure of adeno-associated virus-2 in complex with neutralizing monoclonal antibody A20. Virology 2012; 431:40–49 [View Article][PubMed]
    [Google Scholar]
  52. Chipman PR, Agbandje-McKenna M, Kajigaya S, Brown KE, Young NS et al. Cryo-electron microscopy studies of empty capsids of human parvovirus B19 complexed with its cellular receptor. Proc Natl Acad Sci USA 1996; 93:7502–7506 [View Article][PubMed]
    [Google Scholar]
  53. Kern A, Schmidt K, Leder C, Müller OJ, Wobus CE et al. Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J Virol 2003; 77:11072–11081 [View Article][PubMed]
    [Google Scholar]
  54. Abinanti FR, Warfield MS. Recovery of a hemadsorbing virus (HADEN) from the gastrointestinal tract of calves. Virology 1961; 14:288–289 [View Article][PubMed]
    [Google Scholar]
  55. Storz J, Leary JJ, Carlson JH, Bates RC. Parvoviruses associated with diarrhea in calves. J Am Vet Med Assoc 1978; 173:624–627[PubMed]
    [Google Scholar]
  56. Storz J, Young S, Carroll EJ, Bates RC, Bowen RA et al. Parvovirus infection of the bovine fetus: distribution of infection, antibody response, and age-related susceptibility. Am J Vet Res 1978; 39:1099–1102[PubMed]
    [Google Scholar]
  57. Poppensiek GC, Kahrs RF. Twenty-five years of progress in understanding major infectious diseases of dairy cattle. J Dairy Sci 1981; 64:1443–1464 [View Article][PubMed]
    [Google Scholar]
  58. Durham PJ, Johnson RH, Isles H, Parker RJ, Holroyd RG et al. Epidemiological studies of parvovirus infections in calves on endemically infected properties. Res Vet Sci 1985; 38:234–240 [View Article][PubMed]
    [Google Scholar]
  59. Durham PJ, Lax A, Johnson RH. Pathological and virological studies of experimental parvoviral enteritis in calves. Res Vet Sci 1985; 38:209–219 [View Article][PubMed]
    [Google Scholar]
  60. Manteufel J, Truyen U. Animal bocaviruses: a brief review. Intervirology 2008; 51:328–334 [View Article][PubMed]
    [Google Scholar]
  61. Jordan EK, Sever JL. Fetal damage caused by parvoviral infections. Reprod Toxicol 1994; 8:161–189 [View Article][PubMed]
    [Google Scholar]
  62. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol 1938; 27:493–497 [View Article]
    [Google Scholar]
  63. Kärber G. Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Arch Exp Pathol Pharmak 1931; 162:480–483 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001194
Loading
/content/journal/jgv/10.1099/jgv.0.001194
Loading

Data & Media loading...

Supplements

Supplementary File 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