Skip to main content
Erschienen in: Archives of Virology 11/2017

20.07.2017 | Original Article

Antibody-dependent enhancement of serotype II feline enteric coronavirus infection in primary feline monocytes

verfasst von: Tomomi Takano, Mamiko Nakaguchi, Tomoyoshi Doki, Tsutomu Hohdatsu

Erschienen in: Archives of Virology | Ausgabe 11/2017

Einloggen, um Zugang zu erhalten

Abstract

Feline coronavirus (FCoV) has been classified into two biotypes: avirulent feline coronavirus (feline enteric coronavirus: FECV) and virulent feline coronavirus (feline infectious peritonitis virus: FIPV). In FIPV infection, antibody-dependent enhancement (ADE) has been reported and was shown to be associated with severe clinical disease. On the other hand, the potential role of ADE in FECV infection has not been examined. In this study, using laboratory strains of serotype II FIPV WSU 79-1146 (FIPV 79-1146) and serotype II FECV WSU 79-1683 (FECV 79-1683), we investigated the relationship between ADE and induction of inflammatory cytokines, which are pathogenesis-related factors, for each strain. As with ADE of FIPV 79-1146 infection, a monoclonal antibody against the spike protein of FCoV (mAb 6-4-2) enhanced FECV 79-1683 replication in U937 cells and primary feline monocytes. However, the ADE activity of FECV 79-1683 was lower than that of FIPV 79-1146. Moreover, mRNA levels of inflammatory cytokines (TNF-α, IL-1β, and IL-6) significantly increased with ADE of FIPV 79-1146 infection in primary feline monocytes, but FECV 79-1683 did not demonstrate an increase in these levels. In conclusion, infection of monocytes by FECV was enhanced by antibodies, but the efficiency of infection was lower than that of FIPV.
Literatur
1.
Zurück zum Zitat Belouzard S, Millet JK, Licitra BN, Whittaker GR (2012) Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses 4:1011–1033CrossRefPubMedPubMedCentral Belouzard S, Millet JK, Licitra BN, Whittaker GR (2012) Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses 4:1011–1033CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Brown MA, Troyer JL, Pecon-Slattery J, Roelke ME, O’Brien SJ (2009) Genetics and pathogenesis of feline infectious peritonitis virus. Emerg Infect Dis 15:1445–1452CrossRefPubMedPubMedCentral Brown MA, Troyer JL, Pecon-Slattery J, Roelke ME, O’Brien SJ (2009) Genetics and pathogenesis of feline infectious peritonitis virus. Emerg Infect Dis 15:1445–1452CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Desmarets LM, Theuns S, Olyslaegers DA, Dedeurwaerder A, Vermeulen BL, Roukaerts ID, Nauwynck HJ (2013) Establishment of feline intestinal epithelial cell cultures for the propagation and study of feline enteric coronaviruses. Vet Res 44:71CrossRefPubMedPubMedCentral Desmarets LM, Theuns S, Olyslaegers DA, Dedeurwaerder A, Vermeulen BL, Roukaerts ID, Nauwynck HJ (2013) Establishment of feline intestinal epithelial cell cultures for the propagation and study of feline enteric coronaviruses. Vet Res 44:71CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Dewerchin HL, Cornelissen E, Nauwynck HJ (2005) Replication of feline coronaviruses in peripheral blood monocytes. Arch Virol 150:2483–2500CrossRefPubMed Dewerchin HL, Cornelissen E, Nauwynck HJ (2005) Replication of feline coronaviruses in peripheral blood monocytes. Arch Virol 150:2483–2500CrossRefPubMed
6.
Zurück zum Zitat Dye C, Temperton N, Siddell SG (2007) Type I feline coronavirus spike glycoprotein fails to recognize aminopeptidase N as a functional receptor on feline cell lines. J Gen Virol 88:1753–1760CrossRefPubMedPubMedCentral Dye C, Temperton N, Siddell SG (2007) Type I feline coronavirus spike glycoprotein fails to recognize aminopeptidase N as a functional receptor on feline cell lines. J Gen Virol 88:1753–1760CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat de Groot RJ, Baker SC, Baric R, Enjuanes L, Gorbalenya AE, Holmes KV, Perlman S, Poon L, Rottier PJM, Talbot PJ, Woo PCY, Ziebuhr J (2011) Family Coronaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy, ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, pp 806–828 de Groot RJ, Baker SC, Baric R, Enjuanes L, Gorbalenya AE, Holmes KV, Perlman S, Poon L, Rottier PJM, Talbot PJ, Woo PCY, Ziebuhr J (2011) Family Coronaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy, ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, pp 806–828
8.
Zurück zum Zitat Hohdatsu T, Izumiya Y, Yokoyama Y, Kida K, Koyama H (1998) Differences in virus receptor for type I and type II feline infectious peritonitis virus. Arch Virol 143:839–850CrossRefPubMed Hohdatsu T, Izumiya Y, Yokoyama Y, Kida K, Koyama H (1998) Differences in virus receptor for type I and type II feline infectious peritonitis virus. Arch Virol 143:839–850CrossRefPubMed
9.
Zurück zum Zitat Hohdatsu T, Nakamura M, Ishizuka Y, Yamada H, Koyama H (1991) A study on the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection in feline macrophages by monoclonal antibodies. Arch Virol 120:207–217CrossRefPubMed Hohdatsu T, Nakamura M, Ishizuka Y, Yamada H, Koyama H (1991) A study on the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection in feline macrophages by monoclonal antibodies. Arch Virol 120:207–217CrossRefPubMed
10.
Zurück zum Zitat Hohdatsu T, Okada S, Ishizuka Y, Yamada H, Koyama H (1992) The prevalence of types I and II feline coronavirus infections in cats. J Vet Med Sci 54:557–562CrossRefPubMed Hohdatsu T, Okada S, Ishizuka Y, Yamada H, Koyama H (1992) The prevalence of types I and II feline coronavirus infections in cats. J Vet Med Sci 54:557–562CrossRefPubMed
11.
Zurück zum Zitat Hohdatsu T, Sasamoto T, Okada S, Koyama H (1991) Antigenic analysis of feline coronaviruses with monoclonal antibodies (MAbs): preparation of MAbs which discriminate between FIPV strain 79-1146 and FECV strain 79-1683. Vet Microbiol 28:13–24CrossRefPubMed Hohdatsu T, Sasamoto T, Okada S, Koyama H (1991) Antigenic analysis of feline coronaviruses with monoclonal antibodies (MAbs): preparation of MAbs which discriminate between FIPV strain 79-1146 and FECV strain 79-1683. Vet Microbiol 28:13–24CrossRefPubMed
12.
Zurück zum Zitat Hohdatsu T, Yamada M, Tominaga R, Makino K, Kida K, Koyama H (1998) Antibody-dependent enhancement of feline infectious peritonitis virus infection in feline alveolar macrophages and human monocyte cell line U937 by serum of cats experimentally or naturally infected with feline coronavirus. J Vet Med Sci 60:49–55CrossRefPubMed Hohdatsu T, Yamada M, Tominaga R, Makino K, Kida K, Koyama H (1998) Antibody-dependent enhancement of feline infectious peritonitis virus infection in feline alveolar macrophages and human monocyte cell line U937 by serum of cats experimentally or naturally infected with feline coronavirus. J Vet Med Sci 60:49–55CrossRefPubMed
13.
Zurück zum Zitat Kipar A, Meli ML, Baptiste KE, Bowker LJ, Lutz H (2010) Sites of feline coronavirus persistence in healthy cats. J Gen Virol 91:1698–1707CrossRefPubMed Kipar A, Meli ML, Baptiste KE, Bowker LJ, Lutz H (2010) Sites of feline coronavirus persistence in healthy cats. J Gen Virol 91:1698–1707CrossRefPubMed
14.
Zurück zum Zitat Kummrow M, Meli ML, Haessig M, Goenczi E, Poland A, Pedersen NC, Hofmann-Lehmann R, Lutz H (2005) Feline coronavirus serotypes 1 and 2: seroprevalence and association with disease in Switzerland. Clin Diagn Lab Immunol 12:1209–1215PubMedPubMedCentral Kummrow M, Meli ML, Haessig M, Goenczi E, Poland A, Pedersen NC, Hofmann-Lehmann R, Lutz H (2005) Feline coronavirus serotypes 1 and 2: seroprevalence and association with disease in Switzerland. Clin Diagn Lab Immunol 12:1209–1215PubMedPubMedCentral
15.
Zurück zum Zitat Lin CN, Su BL, Wang CH, Hsieh MW, Chueh TJ, Chueh LL (2009) Genetic diversity and correlation with feline infectious peritonitis of feline coronavirus type I and II: a 5-year study in Taiwan. Vet Microbiol 136:233–239CrossRefPubMed Lin CN, Su BL, Wang CH, Hsieh MW, Chueh TJ, Chueh LL (2009) Genetic diversity and correlation with feline infectious peritonitis of feline coronavirus type I and II: a 5-year study in Taiwan. Vet Microbiol 136:233–239CrossRefPubMed
16.
Zurück zum Zitat Meli M, Kipar A, Müller C, Jenal K, Gönczi E, Borel N, Lutz H (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 6:69–81CrossRefPubMed Meli M, Kipar A, Müller C, Jenal K, Gönczi E, Borel N, Lutz H (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 6:69–81CrossRefPubMed
17.
Zurück zum Zitat Moore BD, Balasuriya UB, Watson JL, Bosio CM, MacKay RJ, MacLachlan NJ (2003) Virulent and avirulent strains of equine arteritis virus induce different quantities of TNF-α and other proinflammatory cytokines in alveolar and blood-derived equine macrophages. Virology 314:662–670CrossRefPubMed Moore BD, Balasuriya UB, Watson JL, Bosio CM, MacKay RJ, MacLachlan NJ (2003) Virulent and avirulent strains of equine arteritis virus induce different quantities of TNF-α and other proinflammatory cytokines in alveolar and blood-derived equine macrophages. Virology 314:662–670CrossRefPubMed
18.
Zurück zum Zitat Motokawa K, Hohdatsu T, Hashimoto H, Koyama H (1996) Comparison of the amino acid sequence and phylogenetic analysis of the peplomer, integral membrane and nucleocapsid proteins of feline, canine and porcine coronaviruses. Microbiol Immunol 40:425–433CrossRefPubMed Motokawa K, Hohdatsu T, Hashimoto H, Koyama H (1996) Comparison of the amino acid sequence and phylogenetic analysis of the peplomer, integral membrane and nucleocapsid proteins of feline, canine and porcine coronaviruses. Microbiol Immunol 40:425–433CrossRefPubMed
19.
Zurück zum Zitat Olsen CW, Corapi WV, Ngichabe CK, Baines JD, Scott FW (1992) Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J Virol 66:956–965PubMedPubMedCentral Olsen CW, Corapi WV, Ngichabe CK, Baines JD, Scott FW (1992) Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J Virol 66:956–965PubMedPubMedCentral
20.
Zurück zum Zitat Pedersen NC (2009) A review of feline infectious peritonitis virus infection: 1963–2008. J Feline Med Surg 11:225–258CrossRefPubMed Pedersen NC (2009) A review of feline infectious peritonitis virus infection: 1963–2008. J Feline Med Surg 11:225–258CrossRefPubMed
21.
Zurück zum Zitat Pedersen NC (2014) An update on feline infectious peritonitis: Virology and immunopathogenesis. Vet J 201:123–132CrossRefPubMed Pedersen NC (2014) An update on feline infectious peritonitis: Virology and immunopathogenesis. Vet J 201:123–132CrossRefPubMed
22.
Zurück zum Zitat Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493–497 Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493–497
23.
Zurück zum Zitat Regan AD, Shraybman R, Cohen RD, Whittaker GR (2008) Differential role for low pH and cathepsin-mediated cleavage of the viral spike protein during entry of serotype II feline coronaviruses. Vet Microbiol 132:235–248CrossRefPubMedPubMedCentral Regan AD, Shraybman R, Cohen RD, Whittaker GR (2008) Differential role for low pH and cathepsin-mediated cleavage of the viral spike protein during entry of serotype II feline coronaviruses. Vet Microbiol 132:235–248CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Rottier PJM, Nakamura K, Schellen P, Volders H, Haijema BJ (2005) Acquisition of macrophage tropism during the pathogenesis of feline infectious peritonitis is determined by mutations in the feline coronavirus spike protein. J Virol 79:14122–14130CrossRefPubMedPubMedCentral Rottier PJM, Nakamura K, Schellen P, Volders H, Haijema BJ (2005) Acquisition of macrophage tropism during the pathogenesis of feline infectious peritonitis is determined by mutations in the feline coronavirus spike protein. J Virol 79:14122–14130CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Shiba N, Maeda K, Kato H, Mochizuki M, Iwata H (2007) Differentiation of feline coronavirus type I and II infections by virus neutralization test. Vet Microbiol 124:348–352CrossRefPubMed Shiba N, Maeda K, Kato H, Mochizuki M, Iwata H (2007) Differentiation of feline coronavirus type I and II infections by virus neutralization test. Vet Microbiol 124:348–352CrossRefPubMed
26.
Zurück zum Zitat Takada A, Kawaoka Y (2003) Antibody-dependent enhancement of viral infection: molecular mechanisms and in vivo implications. Rev Med Virol 13:387–398CrossRefPubMed Takada A, Kawaoka Y (2003) Antibody-dependent enhancement of viral infection: molecular mechanisms and in vivo implications. Rev Med Virol 13:387–398CrossRefPubMed
27.
Zurück zum Zitat Takano T, Azuma N, Hashida Y, Satoh R, Hohdatsu T (2009) B-cell activation in cats with feline infectious peritonitis (FIP) by FIP-virus-induced B-cell differentiation/survival factors. Arch Virol 154:27–35CrossRefPubMed Takano T, Azuma N, Hashida Y, Satoh R, Hohdatsu T (2009) B-cell activation in cats with feline infectious peritonitis (FIP) by FIP-virus-induced B-cell differentiation/survival factors. Arch Virol 154:27–35CrossRefPubMed
28.
Zurück zum Zitat Takano T, Azuma N, Satoh M, Toda A, Hashida Y, Satoh R, Hohdatsu T (2009) Neutrophil survival factors (TNF-alpha, GM-CSF, and G-CSF) produced by macrophages in cats infected with feline infectious peritonitis virus contribute to the pathogenesis of granulomatous lesions. Arch Virol 154:775–781CrossRefPubMed Takano T, Azuma N, Satoh M, Toda A, Hashida Y, Satoh R, Hohdatsu T (2009) Neutrophil survival factors (TNF-alpha, GM-CSF, and G-CSF) produced by macrophages in cats infected with feline infectious peritonitis virus contribute to the pathogenesis of granulomatous lesions. Arch Virol 154:775–781CrossRefPubMed
29.
Zurück zum Zitat Takano T, Hohdatsu T, Hashida Y, Kaneko Y, Tanabe M, Koyama H (2007) A “possible” involvement of TNF-alpha in apoptosis induction in peripheral blood lymphocytes of cats with feline infectious peritonitis. Vet Microbiol 119:121–131CrossRefPubMed Takano T, Hohdatsu T, Hashida Y, Kaneko Y, Tanabe M, Koyama H (2007) A “possible” involvement of TNF-alpha in apoptosis induction in peripheral blood lymphocytes of cats with feline infectious peritonitis. Vet Microbiol 119:121–131CrossRefPubMed
30.
Zurück zum Zitat Takano T, Hohdatsu T, Toda A, Tanabe M, Koyama H (2007) TNF-alpha, produced by feline infectious peritonitis virus (FIPV)-infected macrophages, upregulates expression of type II FIPV receptor feline aminopeptidase N in feline macrophages. Virology 364:64–72CrossRefPubMed Takano T, Hohdatsu T, Toda A, Tanabe M, Koyama H (2007) TNF-alpha, produced by feline infectious peritonitis virus (FIPV)-infected macrophages, upregulates expression of type II FIPV receptor feline aminopeptidase N in feline macrophages. Virology 364:64–72CrossRefPubMed
31.
Zurück zum Zitat Takano T, Katada Y, Moritoh S, Ogasawara M, Satoh K, Satoh R, Hohdatsu T (2008) Analysis of the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection: aminopeptidase N is not important and a process of acidification of the endosome is necessary. J Gen Virol 89:1025–1029CrossRefPubMed Takano T, Katada Y, Moritoh S, Ogasawara M, Satoh K, Satoh R, Hohdatsu T (2008) Analysis of the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection: aminopeptidase N is not important and a process of acidification of the endosome is necessary. J Gen Virol 89:1025–1029CrossRefPubMed
32.
Zurück zum Zitat Takano T, Katoh Y, Doki T, Hohdatsu T (2013) Effect of chloroquine on feline infectious peritonitis virus infection in vitro and in vivo. Antivir Res 99:100–107CrossRefPubMed Takano T, Katoh Y, Doki T, Hohdatsu T (2013) Effect of chloroquine on feline infectious peritonitis virus infection in vitro and in vivo. Antivir Res 99:100–107CrossRefPubMed
33.
Zurück zum Zitat Takano T, Kawakami C, Yamada S, Satoh R, Hohdatsu T (2008) Antibody-dependent enhancement occurs upon re-infection with the identical serotype virus in feline infectious peritonitis virus infection. J Vet Med Sci 70:1315–1321CrossRefPubMed Takano T, Kawakami C, Yamada S, Satoh R, Hohdatsu T (2008) Antibody-dependent enhancement occurs upon re-infection with the identical serotype virus in feline infectious peritonitis virus infection. J Vet Med Sci 70:1315–1321CrossRefPubMed
34.
Zurück zum Zitat Vennema H, De Groot RJ, Harbour DA, Dalderup M, Gruffydd-Jones T, Horzinek MC, Spaan WJ (1990) Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J Virol 64:1407–1409PubMedPubMedCentral Vennema H, De Groot RJ, Harbour DA, Dalderup M, Gruffydd-Jones T, Horzinek MC, Spaan WJ (1990) Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J Virol 64:1407–1409PubMedPubMedCentral
35.
Zurück zum Zitat Watanabe R, Matsuyama S, Taguchi F (2006) Receptor-independent infection of murine coronavirus: analysis by spinoculation. J Virol 80:4901–4908CrossRefPubMedPubMedCentral Watanabe R, Matsuyama S, Taguchi F (2006) Receptor-independent infection of murine coronavirus: analysis by spinoculation. J Virol 80:4901–4908CrossRefPubMedPubMedCentral
Metadaten
Titel
Antibody-dependent enhancement of serotype II feline enteric coronavirus infection in primary feline monocytes
verfasst von
Tomomi Takano
Mamiko Nakaguchi
Tomoyoshi Doki
Tsutomu Hohdatsu
Publikationsdatum
20.07.2017
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 11/2017
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-017-3489-8

Weitere Artikel der Ausgabe 11/2017

Archives of Virology 11/2017 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.