Genotyping coronaviruses associated with feline infectious peritonitis Open Access

Abstract

Feline coronavirus (FCoV) infections are endemic among cats worldwide. The majority of infections are asymptomatic or result in only mild enteric disease. However, approximately 5 % of cases develop feline infectious peritonitis (FIP), a systemic disease that is a frequent cause of death in young cats. In this study, we report the complete coding genome sequences of six FCoVs: three from faecal samples from healthy cats and three from tissue lesion samples from cats with confirmed FIP. The six samples were obtained over a period of 8 weeks at a single-site cat rescue and rehoming centre in the UK. We found amino acid differences located at 44 positions across an alignment of the six virus translatomes and, at 21 of these positions, the differences fully or partially discriminated between the genomes derived from the faecal samples and the genomes derived from the tissue lesion samples. In this study, two amino acid differences fully discriminated the two classes of genomes: these were both located in the S2 domain of the virus surface glycoprotein gene. We also identified deletions in the 3c protein ORF of genomes from two of the FIP samples. Our results support previous studies that implicate S protein mutations in the pathogenesis of FIP.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.000084
2015-06-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/6/1358.html?itemId=/content/journal/jgv/10.1099/vir.0.000084&mimeType=html&fmt=ahah

References

  1. Addie D. D. 2000; Clustering of feline coronaviruses in multicat households. Vet J 159:8–9 [View Article][PubMed]
    [Google Scholar]
  2. Addie D. D., Jarrett O. 1992; A study of naturally occurring feline coronavirus infections in kittens. Vet Rec 130:133–137 [View Article][PubMed]
    [Google Scholar]
  3. Bank-Wolf B. R., Stallkamp I., Wiese S., Moritz A., Tekes G., Thiel H. J. 2014; Mutations of 3c and spike protein genes correlate with the occurrence of feline infectious peritonitis. Vet Microbiol 173:177–188 [View Article][PubMed]
    [Google Scholar]
  4. Barker E. N., Tasker S., Gruffydd-Jones T. J., Tuplin C. K., Burton K., Porter E., Day M. J., Harley R., Fews D. et al. 2013; Phylogenetic analysis of feline coronavirus strains in an epizootic outbreak of feline infectious peritonitis. J Vet Intern Med 27:445–450 [View Article][PubMed]
    [Google Scholar]
  5. Bos E. C., Luytjes W., Spaan W. J. 1997; The function of the spike protein of mouse hepatitis virus strain A59 can be studied on virus-like particles: cleavage is not required for infectivity. J Virol 71:9427–9433[PubMed]
    [Google Scholar]
  6. Chang H. W., de Groot R. J., Egberink H. F., Rottier P. J. 2010; Feline infectious peritonitis: insights into feline coronavirus pathobiogenesis and epidemiology based on genetic analysis of the viral 3c gene. J Gen Virol 91:415–420[PubMed] [CrossRef]
    [Google Scholar]
  7. Chang H. W., Egberink H. F., Halpin R., Spiro D. J., Rottier P. J. 2012; Spike protein fusion peptide and feline coronavirus virulence. Emerg Infect Dis 18:1089–1095 [View Article][PubMed]
    [Google Scholar]
  8. Coleman C. M., Frieman M. B. 2014; Coronaviruses: important emerging human pathogens. J Virol 88:5209–5212 [View Article][PubMed]
    [Google Scholar]
  9. de Groot-Mijnes J. D., van Dun J. M., van der Most R. G., de Groot R. J. 2005; Natural history of a recurrent feline coronavirus infection and the role of cellular immunity in survival and disease. J Virol 79:1036–1044 [View Article][PubMed]
    [Google Scholar]
  10. de Haan C. A., Stadler K., Godeke G. J., Bosch B. J., Rottier P. J. 2004; Cleavage inhibition of the murine coronavirus spike protein by a furin-like enzyme affects cell–cell but not virus–cell fusion. J Virol 78:6048–6054 [View Article][PubMed]
    [Google Scholar]
  11. de Vries R. D., Mesman A. W., Geijtenbeek T. B., Duprex W. P., de Swart R. L. 2012; The pathogenesis of measles. Curr Opin Virol 2:248–255 [View Article][PubMed]
    [Google Scholar]
  12. Desmarets L. M., Theuns S., Olyslaegers D. A., Dedeurwaerder A., Vermeulen B. L., Roukaerts I. D., Nauwynck H. J. 2013; Establishment of feline intestinal epithelial cell cultures for the propagation and study of feline enteric coronaviruses. Vet Res 44:71 [View Article][PubMed]
    [Google Scholar]
  13. Dewerchin H. L., Cornelissen E., Nauwynck H. J. 2005; Replication of feline coronaviruses in peripheral blood monocytes. Arch Virol 150:2483–2500 [View Article][PubMed]
    [Google Scholar]
  14. Dye C., Siddell S. G. 2007; Genomic RNA sequence of feline coronavirus strain FCoV C1Je. J Feline Med Surg 9:202–213 [View Article][PubMed]
    [Google Scholar]
  15. Dye C., Helps C. R., Siddell S. G. 2008; Evaluation of real-time RT-PCR for the quantification of FCoV shedding in the faeces of domestic cats. J Feline Med Surg 10:167–174 [View Article][PubMed]
    [Google Scholar]
  16. Grabherr M. G., Haas B. J., Yassour M., Levin J. Z., Thompson D. A., Amit I., Adiconis X., Fan L., Raychowdhury R. et al. 2011; Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652 [View Article][PubMed]
    [Google Scholar]
  17. Haijema B. J., Volders H., Rottier P. J. 2004; Live, attenuated coronavirus vaccines through the directed deletion of group-specific genes provide protection against feline infectious peritonitis. J Virol 78:3863–3871 [View Article][PubMed]
    [Google Scholar]
  18. Heald-Sargent T., Gallagher T. 2012; Ready, set, fuse! The coronavirus spike protein and acquisition of fusion competence. Viruses 4:557–580 [View Article][PubMed]
    [Google Scholar]
  19. Herrewegh A. A., Smeenk I., Horzinek M. C., Rottier P. J., de Groot R. J. 1998; Feline coronavirus type II strains 79-1683 and 79-1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J Virol 72:4508–4514[PubMed]
    [Google Scholar]
  20. Hsieh L. E., Chueh L. L. 2014; Identification and genotyping of feline infectious peritonitis-associated single nucleotide polymorphisms in the feline interferon-γ gene. Vet Res 45:57 [View Article][PubMed]
    [Google Scholar]
  21. Kipar A., Meli M. L. 2014; Feline infectious peritonitis: still an enigma?. Vet Pathol 51:505–526 [View Article][PubMed]
    [Google Scholar]
  22. Kipar A., Bellmann S., Kremendahl J., Köhler K., Reinacher M. 1998; Cellular composition, coronavirus antigen expression and production of specific antibodies in lesions in feline infectious peritonitis. Vet Immunol Immunopathol 65:243–257 [View Article][PubMed]
    [Google Scholar]
  23. Kipar A., May H., Menger S., Weber M., Leukert W., Reinacher M. 2005; Morphologic features and development of granulomatous vasculitis in feline infectious peritonitis. Vet Pathol 42:321–330 [View Article][PubMed]
    [Google Scholar]
  24. Kipar A., Meli M. L., Baptiste K. E., Bowker L. J., Lutz H. 2010; Sites of feline coronavirus persistence in healthy cats. J Gen Virol 91:1698–1707 [View Article][PubMed]
    [Google Scholar]
  25. Licitra B. N., Millet J. K., Regan A. D., Hamilton B. S., Rinaldi V. D., Duhamel G. E., Whittaker G. R. 2013; Mutation in spike protein cleavage site and pathogenesis of feline coronavirus. Emerg Infect Dis 19:1066–1073 [View Article][PubMed]
    [Google Scholar]
  26. Masters P. S., Perlman S. 2013; Coronaviridae. In Fields Virology, 6th edn. pp. 825–854 Edited by Knipe D. M., Howley P. M., Cohen J. I., Griffin D. E., Lamb R. A., Martin M. A., Racaniello V. R., Roizman B. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  27. Meli M., Kipar A., Müller C., Jenal K., Gönczi E., Borel N., Gunn-Moore D., Chalmers S., Lin F. et al. 2004; High viral loads despite absence of clinical and pathological findings in cats experimentally infected with feline coronavirus (FCoV) type I and in naturally FCoV-infected cats. J Feline Med Surg 6:69–81 [View Article][PubMed]
    [Google Scholar]
  28. Millet J. K., Whittaker G. R. 2014; Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc Natl Acad Sci U S A 111:15214–15219 [View Article][PubMed]
    [Google Scholar]
  29. Pedersen N. C. 2009; A review of feline infectious peritonitis virus infection: 1963–2008. J Feline Med Surg 11:225–258 [View Article][PubMed]
    [Google Scholar]
  30. Pedersen N. C. 2014a). An update on feline infectious peritonitis: diagnostics and therapeutics. Vet J 201:133–141 [View Article][PubMed]
    [Google Scholar]
  31. Pedersen N. C. 2014b). An update on feline infectious peritonitis: virology and immunopathogenesis. Vet J 201:123–132 [View Article][PubMed]
    [Google Scholar]
  32. Pedersen N. C., Liu H., Scarlett J., Leutenegger C. M., Golovko L., Kennedy H., Kamal F. M. 2012; Feline infectious peritonitis: role of the feline coronavirus 3c gene in intestinal tropism and pathogenicity based upon isolates from resident and adopted shelter cats. Virus Res 165:17–28 [View Article][PubMed]
    [Google Scholar]
  33. Pedersen N. C., Liu H., Gandolfi B., Lyons L. A. 2014; The influence of age and genetics on natural resistance to experimentally induced feline infectious peritonitis. Vet Immunol Immunopathol 162:33–40 [View Article][PubMed]
    [Google Scholar]
  34. Perlman S., Netland J. 2009; Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7:439–450 [View Article][PubMed]
    [Google Scholar]
  35. Porter E. 2014 Virus and host determinants of feline coronavirus pathogenicity PhD thesis University of Bristol; Bristol, UK:
    [Google Scholar]
  36. Porter E., Tasker S., Day M. J., Harley R., Kipar A., Siddell S. G., Helps C. R. 2014; Amino acid changes in the spike protein of feline coronavirus correlate with systemic spread of virus from the intestine and not with feline infectious peritonitis. Vet Res 45:49 [View Article][PubMed]
    [Google Scholar]
  37. Regan A. D., Cohen R. D., Whittaker G. R. 2009; Activation of p38 MAPK by feline infectious peritonitis virus regulates pro-inflammatory cytokine production in primary blood-derived feline mononuclear cells. Virology 384:135–143 [View Article][PubMed]
    [Google Scholar]
  38. Reguera J., Santiago C., Mudgal G., Ordoño D., Enjuanes L., Casasnovas J. M. 2012; Structural bases of coronavirus attachment to host aminopeptidase N and its inhibition by neutralizing antibodies. PLoS Pathog 8:e1002859 [View Article][PubMed]
    [Google Scholar]
  39. Satoh R., Furukawa T., Kotake M., Takano T., Motokawa K., Gemma T., Watanabe R., Arai S., Hohdatsu T. 2011; Screening and identification of T helper 1 and linear immunodominant antibody-binding epitopes in the spike 2 domain and the nucleocapsid protein of feline infectious peritonitis virus. Vaccine 29:1791–1800 [View Article][PubMed]
    [Google Scholar]
  40. Tekes G., Spies D., Bank-Wolf B., Thiel V., Thiel H. J. 2012; A reverse genetics approach to study feline infectious peritonitis. J Virol 86:6994–6998 [View Article][PubMed]
    [Google Scholar]
  41. Thiel V., Thiel H. J., Tekes G. 2014; Tackling feline infectious peritonitis via reverse genetics. Bioengineered 5:396–400 [View Article][PubMed]
    [Google Scholar]
  42. Wicht O., Burkard C., de Haan C. A., van Kuppeveld F. J., Rottier P. J., Bosch B. J. 2014; Identification and characterization of a proteolytically primed form of the murine coronavirus spike proteins after fusion with the target cell. J Virol 88:4943–4952 [View Article][PubMed]
    [Google Scholar]
  43. Ziebuhr J. 2005; The coronavirus replicase. Curr Top Microbiol Immunol 287:57–94[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.000084
Loading
/content/journal/jgv/10.1099/vir.0.000084
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited Most Cited RSS feed