Table of Contents Author Guidelines Submit a Manuscript
Advances in Virology
Volume 2011, Article ID 109849, 8 pages
http://dx.doi.org/10.1155/2011/109849
Review Article

The Paradox of Feline Coronavirus Pathogenesis: A Review

1Laboratório de Infectologia Molecular Animal (LIMA), Universidade Federal de Viçosa, Avenida Peter Henry Rolfs, s/n Campus Universitário, 36570-000 Vicosa, MG, Brazil
2Laboratório de Doença das Aves, Universidade Federal de Minas Gerais, Avenida Antônio Carlos, 6627—Pampulha, 31270-901, Belo Horizonte, MG, Brazil

Received 1 December 2010; Revised 1 June 2011; Accepted 1 June 2011

Academic Editor: Michael Bukrinsky

Copyright © 2011 Luciana Wanderley Myrrha et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. A. F. De Vries, M. C. Horzinek, P. J. M. Rottier, and R. J. De Groot, “The genome organization of the nidovirales: similarities and differences between arteri-, toro-, and coronaviruses,” Seminars in Virology, vol. 8, no. 1, pp. 33–47, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. N. C. Pedersen, “A review of feline infectious peritonitis virus infection: 1963–2008,” Journal of Feline Medicine and Surgery, vol. 11, no. 4, pp. 225–258, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. C. Dye and S. G. Siddell, “Genomic RNA sequence of Feline coronavirus strain FIPV WSU-79/1146,” Journal of General Virology, vol. 86, no. 8, pp. 2249–2253, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. N. C. Pedersen, “Virologic and immunologic aspects of feline infectious peritonitis virus infection,” Advances in Experimental Medicine and Biology, vol. 218, pp. 529–550, 1987. View at Google Scholar · View at Scopus
  5. N. C. Pedersen, “Animal virus infections that defy vaccination: equine infectious anemia, caprine arthritis-encephalitis, maedi-visna, and feline infectious peritonitis,” Advances in Veterinary Science and Comparative Medicine, vol. 33, pp. 413–428, 1989. View at Google Scholar · View at Scopus
  6. A. Kipar, H. May, S. Menger, M. Weber, W. Leukert, and M. Reinacher, “Morphologic features and development of granulomatous vasculitis in feline infectious peritonitis,” Veterinary Pathology, vol. 42, no. 3, pp. 321–330, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. A. M. Poland, H. Vennema, J. E. Foley, and N. C. Pedersen, “Two related strains of feline infectious peritonitis virus isolated from immunocompromised cats infected with a feline enteric coronavirus,” Journal of Clinical Microbiology, vol. 34, no. 12, pp. 3180–3184, 1996. View at Google Scholar · View at Scopus
  8. P. J. M. Rottier, K. Nakamura, P. Schellen, H. Volders, and B. J. Haijema, “Acquisition of macrophage tropism during the pathogenesis of feline infectious peritonitis is determined by mutations in the feline coronavirus spike protein,” Journal of Virology, vol. 79, no. 22, pp. 14122–14130, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. H. Vennema, A. Poland, J. Foley, and N. C. Pedersen, “Feline infectious peritonitis viruses arise by mutation from endemic feline enteric coronaviruses,” Virology, vol. 243, no. 1, pp. 150–157, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. N. C. Pedersen, J. F. Boyle, K. Floyd, A. Fudge, and J. Barker, “An enteric coronavirus infection of cats and its relationship to feline infectious peritonitis,” American Journal of Veterinary Research, vol. 42, no. 3, pp. 368–377, 1981. View at Google Scholar · View at Scopus
  11. T. Takano, T. Hohdatsu, Y. Hashida, Y. Kaneko, M. Tanabe, and H. Koyama, “A “possible” involvement of TNF-alpha in apoptosis induction in peripheral blood lymphocytes of cats with feline infectious peritonitis,” Veterinary Microbiology, vol. 119, no. 2–4, pp. 121–131, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. H. Vennema, “Genetic drift and genetic shift during feline coronavirus evolution,” Veterinary Microbiology, vol. 69, no. 1-2, pp. 139–141, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Dye and S. G. Siddell, “Genomic RNA sequence of feline coronavirus strain FCoV C1Je,” Journal of Feline Medicine and Surgery, vol. 9, no. 3, pp. 202–213, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. H. L. Dewerchin, E. Cornelissen, and H. J. Nauwynck, “Replication of feline coronaviruses in peripheral blood monocytes,” Archives of Virology, vol. 150, no. 12, pp. 2483–2500, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. A. Kipar, K. Baptiste, A. Barth, and M. Reinacher, “Natural FCoV infection: cats with FIP exhibit significantly higher viral loads than healthy infected cats,” Journal of Feline Medicine and Surgery, vol. 8, no. 1, pp. 69–72, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. M. Meli, A. Kipar, C. Müller et al., “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,” Journal of Feline Medicine and Surgery, vol. 6, no. 2, pp. 69–81, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. M. Battilani, T. Coradin, A. Scagliarini et al., “Quasispecies composition and phylogenetic analysis of feline coronaviruses (FCoVs) in naturally infected cats,” FEMS Immunology and Medical Microbiology, vol. 39, no. 2, pp. 141–147, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. M. A. Brown, J. L. Troyer, J. Pecon-Slattery, M. E. Roelke, and S. J. O'Brien, “Genetics and pathogenesis of feline infectious peritonitis virus,” Emerging Infectious Diseases, vol. 15, no. 9, pp. 1445–1452, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. N. C. Pedersen, J. F. Evermann, A. J. McKeirnan, and R. L. Ott, “Pathogenicity studies of feline coronavirus isolates 79-1146 and 79-1683,” American Journal of Veterinary Research, vol. 45, no. 12, pp. 2580–2585, 1984. View at Google Scholar · View at Scopus
  20. H. Vennema, J. W. A. Rossen, J. Wesseling, M. C. Horzinek, and P. J. M. Rottier, “Genomic organization and expression of the 3' end of the canine and feline enteric coronaviruses,” Virology, vol. 191, no. 1, pp. 134–140, 1992. View at Publisher · View at Google Scholar · View at Scopus
  21. A. A. P. M. Herrewegh, H. Vennema, M. C. Horzinek, P. J. M. Rottier, and R. J. De Groot, “The molecular genetics of feline coronaviruses: comparative sequence analysis of the ORF7a/7b transcription unit of different biotypes,” Virology, vol. 212, no. 2, pp. 622–631, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. N. C. Pedersen and J. W. Black, “Attempted immunization of cats against feline infectious peritonitis, using avirulent live virus or sublethal amounts of virulent virus,” American Journal of Veterinary Research, vol. 44, no. 2, pp. 229–234, 1983. View at Google Scholar
  23. M. A. Kennedy, E. Moore, R. P. Wilkes, S. B. Citino, and S. A. Kania, “Analysis of genetic mutations in the 7a7b open reading frame of coronavirus of cheetahs (Acinonyx jubatus),” American Journal of Veterinary Research, vol. 67, no. 4, pp. 627–632, 2006. View at Google Scholar
  24. M. Kennedy, N. Boedeker, P. Gibbs, and S. Kania, “Deletions in the 7a ORF of feline coronavirus associated with an epidemic of feline infectious peritonitis,” Veterinary Microbiology, vol. 81, no. 3, pp. 227–234, 2001. View at Publisher · View at Google Scholar
  25. A. A. P. M. Herrewegh, M. Mähler, H. J. Hedrich et al., “Persistence and evolution of feline coronavirus in a closed cat-breeding colony,” Virology, vol. 234, no. 2, pp. 349–363, 1997. View at Publisher · View at Google Scholar · View at PubMed
  26. H. W. Chang, R. J. de Groot, H. F. Egberink, and P. J. M. Rottier, “Feline infectious peritonitis: insights into feline coronavirus pathobiogenesis and epidemiology based on genetic analysis of the viral 3c gene,” Journal of General Virology, vol. 91, no. 2, pp. 415–420, 2010. View at Publisher · View at Google Scholar · View at PubMed
  27. D. A. Gunn-Moore, F. J. Gunn-Moore, T. J. Gruffydd-Jones, and D. A. Harbour, “Detection of FCoV quasispecies using denaturing gradient gel electrophoresis,” Veterinary Microbiology, vol. 69, no. 1-2, pp. 127–130, 1999. View at Publisher · View at Google Scholar
  28. K. K. Christianson, J. D. Ingersoll, R. M. Landon, N. E. Pfeiffer, and J. D. Gerber, “Characterization of a temperature sensitive feline infectious peritonitis coronavirus,” Archives of Virology, vol. 109, no. 3-4, pp. 185–196, 1989. View at Google Scholar
  29. B. J. Haijema, H. Volders, and P. J. M. Rottier, “Switching species tropism: an effective way to manipulate the feline coronavirus genome,” Journal of Virology, vol. 77, no. 8, pp. 4528–4538, 2003. View at Publisher · View at Google Scholar
  30. C. N. Lin, B. L. Su, H. P. Huang, J. J. Lee, M. W. Hsieh, and L. L. Chueh, “Field strain feline coronaviruses with small deletions in ORF7b associated with both enteric infection and feline infectious peritonitis,” Journal of Feline Medicine and Surgery, vol. 11, no. 6, pp. 413–419, 2009. View at Publisher · View at Google Scholar · View at PubMed
  31. N. C. Pedersen, C. E. Allen, and L. A. Lyons, “Pathogenesis of feline enteric coronavirus infection,” Journal of Feline Medicine and Surgery, vol. 10, no. 6, pp. 529–541, 2008. View at Publisher · View at Google Scholar · View at PubMed
  32. A. Kipar, M. L. Meli, K. Failing et al., “Natural feline coronavirus infection: differences in cytokine patterns in association with the outcome of infection,” Veterinary Immunology and Immunopathology, vol. 112, no. 3-4, pp. 141–155, 2006. View at Publisher · View at Google Scholar · View at PubMed
  33. E. C. Holmes, “The evolutionary genetics of emerging viruses,” Annual Review of Ecology, Evolution, and Systematics, vol. 40, pp. 353–372, 2009. View at Publisher · View at Google Scholar
  34. E. Minskaia, T. Hertzig, A. E. Gorbalenya et al., “Discovery of an RNA virus 35 exoribonuclease that is critically involved in coronavirus RNA synthesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 13, pp. 5108–5113, 2006. View at Publisher · View at Google Scholar · View at PubMed
  35. S. Makino, J. G. Keck, S. A. Stohlman, and M. M. C. Lai, “High-frequency RNA recombination of murine coronaviruses,” Journal of Virology, vol. 57, no. 3, pp. 729–737, 1986. View at Google Scholar
  36. I. Kiss, S. Kecskeméti, J. Tanyi, B. Klingeborn, and S. Belák, “Preliminary studies on feline coronavirus distribution in naturally and experimentally infected cats,” Research in Veterinary Science, vol. 68, no. 3, pp. 237–242, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. A. Moya, E. C. Holmes, and F. González-Candelas, “The population genetics and evolutionary epidemiology of RNA viruses,” Nature Reviews Microbiology, vol. 2, no. 4, pp. 279–288, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. P. S. Morahan, J. R. Connor, and K. R. Leary, “Viruses and the versatile macrophage,” British Medical Bulletin, vol. 41, no. 1, pp. 15–21, 1985. View at Google Scholar · View at Scopus
  39. C. A. Stoddart and F. W. Scott, “Intrinsic resistance of feline peritoneal macrophages to coronavirus infection correlates with in vivo virulence,” Journal of virology, vol. 63, no. 1, pp. 436–440, 1989. View at Google Scholar · View at Scopus
  40. A. L. Berg, K. Ekman, S. Belák, and M. Berg, “Cellular composition and interferon-γ expression of the local inflammatory response in feline infectious peritonitis (FIP),” Veterinary Microbiology, vol. 111, no. 1-2, pp. 15–23, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. A. Kipar, S. Bellmann, J. Kremendahl, K. Köhler, and M. Reinacher, “Cellular composition, coronavirus antigen expression and production of specific antibodies in lesions in feline infectious peritonitis,” Veterinary Immunology and Immunopathology, vol. 65, no. 2–4, pp. 243–257, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Paltrinieri, M. C. Parodi, and G. Cammarata, “In vivo diagnosis of feline infectious peritonitis by comparison of protein content, cytology, and direct immunofluorescence test on peritoneal and pleural effusions,” Journal of Veterinary Diagnostic Investigation, vol. 11, no. 4, pp. 358–361, 1999. View at Google Scholar · View at Scopus
  43. E. Cornelissen, H. L. Dewerchin, E. Van Hamme, and H. J. Nauwynck, “Absence of surface expression of feline infectious peritonitis virus (FIPV) antigens on infected cells isolated from cats with FIP,” Veterinary Microbiology, vol. 121, no. 1-2, pp. 131–137, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. D. A. Gunn-Moore, T. J. Gruffydd-Jones, and D. A. Harbour, “Detection of feline coronaviruses by culture and reverse transcriptase-polymerase chain reaction of blood samples from healthy cats and cats with clinical feline infectious peritonitis,” Veterinary Microbiology, vol. 62, no. 3, pp. 193–205, 1998. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Tekes, R. Hofmann-Lehmann, B. Bank-Wolf, R. Maier, H. J. Thiel, and V. Thiel, “Chimeric feline coronaviruses that encode type II spike protein on type I genetic background display accelerated viral growth and altered receptor usage,” Journal of Virology, vol. 84, no. 3, pp. 1326–1333, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. D. D. Addie and O. Jarrett, “Use of a reverse-transcriptase polymerase chain reaction for monitoring the shedding of feline coronavirus by healthy cats,” Veterinary Record, vol. 148, no. 21, pp. 649–653, 2001. View at Google Scholar · View at Scopus
  47. N. C. Pedersen, “An overview of feline enteric coronavirus and infectious peritonitis virus infections,” Feline Practice, vol. 23, no. 3, pp. 7–20, 1995. View at Google Scholar
  48. N. C. Petersen and J. F. Boyle, “Immunologic phenomena in the effusive form of feline infectious peritonitis,” American Journal of Veterinary Research, vol. 41, no. 6, pp. 868–876, 1980. View at Google Scholar · View at Scopus
  49. T. Hohdatsu, M. Nakamura, Y. Ishizuka, H. Yamada, and H. Koyama, “A study on the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection in feline macrophages by monoclonal antibodies,” Archives of Virology, vol. 120, no. 3-4, pp. 207–217, 1991. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Takano, C. Kawakami, S. Yamada, R. Satoh, and T. Hohdatsu, “Antibody-dependent enhancement occurs upon re-infection with the identical serotype virus in feline infectious peritonitis virus infection,” Journal of Veterinary Medical Science, vol. 70, no. 12, pp. 1315–1321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Vennema, R. J. De Groot, D. A. Harbour et al., “Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization,” Journal of Virology, vol. 64, no. 3, pp. 1407–1409, 1990. View at Google Scholar · View at Scopus
  52. H. L. Dewerchin, E. Cornelissen, and H. J. Nauwynck, “Feline infectious peritonitis virus-infected monocytes internalize viral membrane-bound proteins upon antibody addition,” Journal of General Virology, vol. 87, no. 6, pp. 1685–1690, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. A. Kipar, S. Bellmann, D. A. Gunn-Moore et al., “Histopathological alterations of lymphatic tissues in cats without feline infectious peritonitis after long-term exposure to FIP virus,” Veterinary Microbiology, vol. 69, no. 1-2, pp. 131–137, 1999. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Kipar, K. Köhler, W. Leukert, and M. Reinacher, “A comparison of lymphatic tissues from cats with spontaneous feline infectious peritonitis (FIP), cats with FIP virus infection but no FIP, and cats with no infection,” Journal of Comparative Pathology, vol. 125, no. 2-3, pp. 182–191, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. S. Paltrinieri, W. Ponti, S. Comazzi, A. Giordano, and G. Poli, “Shifts in circulating lymphocyte subsets in cats with feline infectious peritonitis (FIP): pathogenic role and diagnostic relevance,” Veterinary Immunology and Immunopathology, vol. 96, no. 3-4, pp. 141–148, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Takano, N. Azuma, Y. Hashida, R. Satoh, and T. Hohdatsu, “B-cell activation in cats with feline infectious peritonitis (FIP) by FIP-virus-induced B-cell differentiation/survival factors,” Archives of Virology, vol. 154, no. 1, pp. 27–35, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. J. E. Foley, C. Rand, and C. Leutenegger, “Inflammation and changes in cytokine levels in neurological feline infectious peritonitis,” Journal of Feline Medicine and Surgery, vol. 5, no. 6, pp. 313–322, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Hannen, U. Banning, H. Bönig et al., “Cytokine-mediated regulation of granulocyte colony-stimulating factor production,” Scandinavian Journal of Immunology, vol. 50, no. 5, pp. 461–468, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. M. A. Moore et al., “Interleukin-10 and the interleukin-10 receptor,” Annual Review of Immunology, vol. 19, pp. 683–765, 2001. View at Google Scholar
  60. G. A. Dean, T. Olivry, C. Stanton, and N. C. Pedersen, “In vivo cytokine response to experimental feline infectious peritonitis virus infection,” Veterinary Microbiology, vol. 97, no. 1-2, pp. 1–12, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. U. Boehm, T. Klamp, M. Groot, and J. C. Howard, “Cellular responses to interferon-γ,” Annual Review of Immunology, vol. 15, pp. 749–795, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. I. Kiss, A. M. Poland, and N. C. Pedersen, “Disease outcome and cytokine responses in cats immunized with an avirulent feline infectious peritonitis virus (FIPV)-UCD1 and challenge-exposed with virulent FIPV-UCD8,” Journal of Feline Medicine and Surgery, vol. 6, no. 2, pp. 89–97, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. M. E. Gelain, M. Meli, and S. Paltrinieri, “Whole blood cytokine profiles in cats infected by feline coronavirus and healthy non-FCoV infected specific pathogen-free cats,” Journal of Feline Medicine and Surgery, vol. 8, no. 6, pp. 389–399, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. A. Giordano and S. Paltrinieri, “Interferon-γ in the serum and effusions of cats with feline coronavirus infection,” Veterinary Journal, vol. 180, no. 3, pp. 396–398, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. S. J. H. Van Deventer, H. R. Buller, J. W. Ten Cate, L. A. Aarden, C. E. Hack, and A. Sturk, “Experimental endotoxemia in humans: analysis of cytokine release and coagulation, fibrinolytic, and complement pathways,” Blood, vol. 76, no. 12, pp. 2520–2526, 1990. View at Google Scholar · View at Scopus
  66. J. J. Cerón, P. D. Eckersall, and S. Martínez-Subiela, “Acute phase proteins in dogs and cats: current knowledge and future perspectives,” Veterinary Clinical Pathology, vol. 34, no. 2, pp. 85–99, 2005. View at Google Scholar
  67. S. Paltrinieri, C. Metzger, M. Battilani, V. Pocacqua, M. E. Gelain, and A. Giordano, “Serum α1-acid glycoprotein (AGP) concentration in non-symptomatic cats with feline coronavirus (FCoV) infection,” Journal of Feline Medicine and Surgery, vol. 9, no. 4, pp. 271–277, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  68. F. Ceciliani, C. Grossi, A. Giordano, V. Pocacqua, and S. Paltrinieri, “Decreased sialylation of the acute phase protein α1-acid glycoprotein in feline infectious peritonitis (FIP),” Veterinary Immunology and Immunopathology, vol. 99, no. 3-4, pp. 229–236, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. S. Duthie, P. D. Eckersall, D. D. Addie, C. E. Lawrence, and O. Jarrett, “Value of α1-acid glycoprotein in the diagnosis of feline infectious peritonitis,” Veterinary Record, vol. 141, no. 12, pp. 299–303, 1997. View at Google Scholar · View at Scopus
  70. S. Paltrinieri, M. E. Gelain, F. Ceciliani, A. M. Ribera, and M. Battilani, “Association between faecal shedding of feline coronavirus and serum α1-acid glycoprotein sialylation,” Journal of Feline Medicine and Surgery, vol. 10, no. 5, pp. 514–518, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus