1887

Journal of General Virology header logo

Volume 96, Issue 3

Cell culture adaptation mutations in foot-and-mouth disease virus serotype A capsid proteins: implications for receptor interactions Free

Abstract

In this study we describe the adaptive changes fixed on the capsid of several foot-and-mouth disease virus serotype A strains during propagation in cell monolayers. Viruses passaged extensively in three cell lines (BHK-21, LFBK and IB-RS-2) consistently gained positively charged amino acids in the putative heparin-sulfate-binding pocket (VP2 βE-βF loop, VP1 C-terminus and VP3 β-B knob) surrounding the fivefold symmetry axis (VP1 βF-βG loop) and at other discrete sites on the capsid (VP3 βG-βH loop, VP1 C-terminus, VP2 βC strand and VP1 βG-βH loop). A lysine insertion in the VP1 βF-βG loop of two of the BHK-21-adapted viruses supports the biological advantage of positively charged residues acquired in cell culture. The charge transitions occurred irrespective of cell line, suggesting their possible role in ionic interaction with ubiquitous negatively charged cell-surface molecules such as glycosaminoglycans (GAG). This was supported by the ability of the cell-culture-adapted variants to replicate in the integrin-deficient, GAG-positive CHO-K1 cells and their superior fitness in competition assays compared with the lower passage viruses with WT genotypes. Substitutions fixed in the VP1 βG-βH loop (−3, −2 and +2 ‘RGD’ positions) or in the structural element known to be juxtaposed against that loop (VP1 βB-βC loop) suggest their possible role in modulating the efficiency and specificity of interaction of the ‘RGD’ motif with α-integrin receptors. The nature and location of the substitutions described in this study could be applied in the rapid cell culture adaptation of viral strains for vaccine production.

  • Received:
  • Accepted:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.071597-0
2015-03-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/3/553.html?itemId=/content/journal/jgv/10.1099/vir.0.071597-0&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 [View Article][PubMed]
     [Google Scholar]
  2. Baranowski E., Sevilla N., Verdaguer N., Ruiz-Jarabo C. M., Beck E., Domingo E. 1998; Multiple virulence determinants of foot-and-mouth disease virus in cell culture. J Virol 72:6362–6372[PubMed]
     [Google Scholar]
  3. Baranowski E., Ruız-Jarabo C. M., Pariente N., Verdaguer N., Domingo E. 2003; Evolution of cell recognition by viruses: a source of biological novelty with medical implications. Adv Virus Res 62:19–111 [View Article][PubMed]
     [Google Scholar]
  4. Berryman S., Clark S., Kakker N. K., Silk R., Seago J., Wadsworth J., Chamberlain K., Knowles N. J., Jackson T. 2013; Positively charged residues at the five-fold symmetry axis of cell culture-adapted foot-and-mouth disease virus permit novel receptor interactions. J Virol 87:8735–8744 [View Article][PubMed]
     [Google Scholar]
  5. Biasini M., Bienert S., Waterhouse A., Arnold K., Studer G., Schmidt T., Kiefer F., Cassarino T. G., Bertoni M.other authors 2014; swiss-model: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:Web Server issueW252-8–W258 [View Article][PubMed]
     [Google Scholar]
  6. 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 [View Article][PubMed]
     [Google Scholar]
  7. Burman A., Clark S., Abrescia N. G., Fry E. E., Stuart D. I., Jackson T. 2006; Specificity of the VP1 GH loop of foot-and-mouth disease virus for αv integrins. J Virol 80:9798–9810 [View Article][PubMed]
     [Google Scholar]
  8. Curry S., Fry E., Blakemore W., Abu Ghazaleh R., Jackson T., King A., Lea S., Newman J., Rowlands D., Stuart D. 1996; Perturbations in the surface structure of A22 Iraq foot-and-mouth disease virus accompanying coupled changes in host cell specificity and antigenicity. Structure 4:135–145 [View Article][PubMed]
     [Google Scholar]
  9. DeLano W. L. 2002 The PyMOL Molecular Graphics System Palo Alto, CA: DeLano Scientific;
     [Google Scholar]
  10. DiCara D., Burman A., Clark S., Berryman S., Howard M. J., Hart I. R., Marshall J. F., Jackson T. 2008; Foot-and-mouth disease virus forms a highly stable, EDTA-resistant complex with its principal receptor, integrin αvβ6: implications for infectiousness. J Virol 82:1537–1546 [View Article][PubMed]
     [Google Scholar]
  11. Domingo E., Díez J., Martínez M. A., Hernández J., Holguín A., Borrego B., Mateu M. G. 1993; New observations on antigenic diversification of RNA viruses. Antigenic variation is not dependent on immune selection. J Gen Virol 74:2039–2045 [View Article][PubMed]
     [Google Scholar]
  12. Duque H., Baxt B. 2003; Foot-and-mouth disease virus receptors: comparison of bovine alpha(V) integrin utilization by type A and O viruses. J Virol 77:2500–2511 [View Article][PubMed]
     [Google Scholar]
  13. Escarmís C., Carrillo E. C., Ferrer M., Arriaza J. F., Lopez N., Tami C., Verdaguer N., Domingo E., Franze-Fernández M. T. 1998; Rapid selection in modified BHK-21 cells of a foot-and-mouth disease virus variant showing alterations in cell tropism. J Virol 72:10171–10179[PubMed]
     [Google Scholar]
  14. 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 [View Article][PubMed]
     [Google Scholar]
  15. Fry E. E., Lea S. M., Jackson T., Newman J. W. I., Ellard F. M., Blakemore W. E., Abu-Ghazaleh R., Samuel A., King A. M., Stuart D. I. 1999; The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J 18:543–554 [View Article][PubMed]
     [Google Scholar]
  16. Fry E. E., Newman J. W. I., Curry S., Najjam S., Jackson T., Blakemore W., Lea S. M., Miller L., Burman A.other authors 2005; Structure of foot-and-mouth disease virus serotype A10 61 alone and complexed with oligosaccharide receptor: receptor conservation in the face of antigenic variation. J Gen Virol 86:1909–1920 [View Article][PubMed]
     [Google Scholar]
  17. Jackson T., Ellard F. M., Ghazaleh R. A., Brookes S. M., Blakemore W. E., Corteyn A. H., Stuart D. I., Newman J. W., King A. M. 1996; Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J Virol 70:5282–5287[PubMed]
     [Google Scholar]
  18. 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 [View Article][PubMed]
     [Google Scholar]
  19. King D. P., Burman A., Gold S., Shaw A. E., Jackson T., Ferris N. P. 2011; Integrin sub-unit expression in cell cultures used for the diagnosis of foot-and-mouth disease. Vet Immunol Immunopathol 140:259–265 [View Article][PubMed]
     [Google Scholar]
  20. Kumar R. M., Sanyal A., Hemadri D., Tosh C., Mohapatra J. K., Bandyopadhyay S. K. 2004; Characterization of foot-and-mouth disease serotype asial viruses grown in the presence of polyclonal antisera in serology and nucleotide sequence analysis. Arch Virol 149:1801–1814[PubMed]
     [Google Scholar]
  21. LaRocco M., Krug P. W., Kramer E., Ahmed Z., Pacheco J. M., Duque H., Baxt B., Rodriguez L. L. 2013; A continuous bovine kidney cell line constitutively expressing bovine αvβ6 integrin has increased susceptibility to foot-and-mouth disease virus. J Clin Microbiol 51:1714–1720 [View Article][PubMed]
     [Google Scholar]
  22. Lawrence P., LaRocco M., Baxt B., Rieder E. 2013; Examination of soluble integrin resistant mutants of foot-and-mouth disease virus. Virol J 10:2 [View Article][PubMed]
     [Google Scholar]
  23. Maree F. F., Blignaut B., de Beer T. A., Visser N., Rieder E. A. 2010; Mapping of amino acid residues responsible for adhesion of cell culture-adapted foot-and-mouth disease SAT type viruses. Virus Res 153:82–91 [View Article][PubMed]
     [Google Scholar]
  24. Maree F. F., Blignaut B., Aschenbrenner L., Burrage T., Rieder E. 2011; Analysis of SAT1 type foot-and-mouth disease virus capsid proteins: influence of receptor usage on the properties of virus particles. Virus Res 155:462–472 [View Article][PubMed]
     [Google Scholar]
  25. 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 [View Article][PubMed]
     [Google Scholar]
  26. Mohapatra J. K., Subramaniam S., Pandey L. K., Pawar S. S., De A., Das B., Sanyal A., Pattnaik B. 2011; Phylogenetic structure of serotype A foot-and-mouth disease virus: global diversity and the Indian perspective. J Gen Virol 92:873–879 [View Article][PubMed]
     [Google Scholar]
  27. Neff S., Sá-Carvalho D., Rieder E., Mason P. W., Blystone S. D., Brown E. J., Baxt B. 1998; Foot-and-mouth disease virus virulent for cattle utilizes the integrin α(v)β3 as its receptor. J Virol 72:3587–3594[PubMed]
     [Google Scholar]
  28. Pandey L. K., Mohapatra J. K., Subramaniam S., Sanyal A., Pande V., Pattnaik B. 2014; Evolution of serotype A foot-and-mouth disease virus capsid under neutralizing antibody pressure in vitro. Virus Res 181:72–76 [View Article][PubMed]
     [Google Scholar]
  29. Parry N., Fox G., Rowlands D., Brown F., Fry E., Acharya R., Logan D., Stuart D. 1990; Structural and serological evidence for a novel mechanism of antigenic variation in foot-and-mouth disease virus. Nature 347:569–572 [View Article][PubMed]
     [Google Scholar]
  30. Rieder E., Baxt B., Mason P. W. 1994; Animal-derived antigenic variants of foot-and-mouth disease virus type A12 have low affinity for cells in culture. J Virol 68:5296–5299[PubMed]
     [Google Scholar]
  31. Sa-Carvalho D., Rieder E., Baxt B., Rodarte R., Tanuri A., Mason P. W. 1997; Tissue culture adaptation of foot-and-mouth disease virus selects viruses that bind to heparin and are attenuated in cattle. J Virol 71:5115–5123[PubMed]
     [Google Scholar]
  32. Swaney L. M. 1988; A continuous bovine kidney cell line for routine assays of foot-and-mouth disease virus. Vet Microbiol 18:1–14 [View Article][PubMed]
     [Google Scholar]
  33. Tami C., Taboga O., Berinstein A., Núñez J. I., Palma E. L., Domingo E., Sobrino F., Carrillo E. 2003; Evidence of the coevolution of antigenicity and host cell tropism of foot-and-mouth disease virus in vivo. J Virol 77:1219–1226 [View Article][PubMed]
     [Google Scholar]
  34. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  35. Zhao Q., Pacheco J. M., Mason P. W. 2003; Evaluation of genetically engineered derivatives of a Chinese strain of foot-and-mouth disease virus reveals a novel cell-binding site which functions in cell culture and in animals. J Virol 77:3269–3280 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.071597-0
Loading
Cell culture adaptation mutations in foot-and-mouth disease virus serotype A capsid proteins: implications for receptor interactions
J. Gen. Virol. 96, 553 (2015); https://doi.org/10.1099/vir.0.071597-0
/content/journal/jgv/10.1099/vir.0.071597-0
/content/journal/jgv/10.1099/vir.0.071597-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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