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J Virol. 1992 Feb; 66(2): 956–965.
PMCID: PMC240797

Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages.


Antibody-dependent enhancement of virus infection is a process whereby virus-antibody complexes initiate infection of cells via Fc receptor-mediated endocytosis. We sought to investigate antibody-dependent enhancement of feline infectious peritonitis virus infection of primary feline peritoneal macrophages in vitro. Enhancement of infection was assessed, after indirect immunofluorescent-antibody labelling of infected cells, by determining the ratio between the number of cells infected in the presence and absence of virus-specific antibody. Infection enhancement was initially demonstrated by using heat-inactivated, virus-specific feline antiserum. Functional compatibility between murine immunoglobulin molecules and feline Fc receptors was demonstrated by using murine anti-sheep erythrocyte serum and an antibody-coated sheep erythrocyte phagocytosis assay. Thirty-seven murine monoclonal antibodies specific for the nucleocapsid, membrane, or spike proteins of feline infectious peritonitis virus or transmissible gastroenteritis virus were assayed for their ability to enhance the infectivity of feline infectious peritonitis virus. Infection enhancement was mediated by a subset of spike protein-specific monoclonal antibodies. A distinct correlation was seen between the ability of a monoclonal antibody to cause virus neutralization in a routine cell culture neutralization assay and its ability to mediate infection enhancement of macrophages. Infection enhancement was shown to be Fc receptor mediated by blockade of antibody-Fc receptor interaction using staphylococcal protein A. Our results are consistent with the hypothesis that antibody-dependent enhancement of feline infectious peritonitis virus infectivity is mediated by antibody directed against specific sites on the spike protein.

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  • Corapi WV, Donis RO, Dubovi EJ. Characterization of a panel of monoclonal antibodies and their use in the study of the antigenic diversity of bovine viral diarrhea virus. Am J Vet Res. 1990 Sep;51(9):1388–1394. [PubMed]
  • Fiscus SA, Teramoto YA. Antigenic comparison of feline coronavirus isolates: evidence for markedly different peplomer glycoproteins. J Virol. 1987 Aug;61(8):2607–2613. [PMC free article] [PubMed]
  • Gimenez HB, Keir HM, Cash P. In vitro enhancement of respiratory syncytial virus infection of U937 cells by human sera. J Gen Virol. 1989 Jan;70(Pt 1):89–96. [PubMed]
  • Gollins SW, Porterfield JS. Flavivirus infection enhancement in macrophages: radioactive and biological studies on the effect of antibody on viral fate. J Gen Virol. 1984 Aug;65(Pt 8):1261–1272. [PubMed]
  • Gollins SW, Porterfield JS. A new mechanism for the neutralization of enveloped viruses by antiviral antibody. Nature. 1986 May 15;321(6067):244–246. [PubMed]
  • Halstead SB, Venkateshan CN, Gentry MK, Larsen LK. Heterogeneity of infection enhancement of dengue 2 strains by monoclonal antibodies. J Immunol. 1984 Mar;132(3):1529–1532. [PubMed]
  • Henchal EA, McCown JM, Burke DS, Seguin MC, Brandt WE. Epitopic analysis of antigenic determinants on the surface of dengue-2 virions using monoclonal antibodies. Am J Trop Med Hyg. 1985 Jan;34(1):162–169. [PubMed]
  • Homsy J, Meyer M, Levy JA. Serum enhancement of human immunodeficiency virus (HIV) infection correlates with disease in HIV-infected individuals. J Virol. 1990 Apr;64(4):1437–1440. [PMC free article] [PubMed]
  • Homsy J, Meyer M, Tateno M, Clarkson S, Levy JA. The Fc and not CD4 receptor mediates antibody enhancement of HIV infection in human cells. Science. 1989 Jun 16;244(4910):1357–1360. [PubMed]
  • Hotta H, Wiharta AS, Hotta S. Antibody-mediated enhancement of dengue virus infection in mouse macrophage cell lines, Mk1 and Mm1. Proc Soc Exp Biol Med. 1984 Mar;175(3):320–327. [PubMed]
  • Jacobse-Geels HE, Daha MR, Horzinek MC. Isolation and characterization of feline C3 and evidence for the immune complex pathogenesis of feline infectious peritonitis. J Immunol. 1980 Oct;125(4):1606–1610. [PubMed]
  • Jacobse-Geels HE, Daha MR, Horzinek MC. Antibody, immune complexes, and complement activity fluctuations in kittens with experimentally induced feline infectious peritonitis. Am J Vet Res. 1982 Apr;43(4):666–670. [PubMed]
  • Jolly PE, Huso DL, Sheffer D, Narayan O. Modulation of lentivirus replication by antibodies: Fc portion of immunoglobulin molecule is essential for enhancement of binding, internalization, and neutralization of visna virus in macrophages. J Virol. 1989 Apr;63(4):1811–1813. [PMC free article] [PubMed]
  • King AA, Sands JJ, Porterfield JS. Antibody-mediated enhancement of rabies virus infection in a mouse macrophage cell line (P388D1). J Gen Virol. 1984 Jun;65(Pt 6):1091–1093. [PubMed]
  • Krilov LR, Anderson LJ, Marcoux L, Bonagura VR, Wedgwood JF. Antibody-mediated enhancement of respiratory syncytial virus infection in two monocyte/macrophage cell lines. J Infect Dis. 1989 Nov;160(5):777–782. [PubMed]
  • Lai MM. Coronavirus: organization, replication and expression of genome. Annu Rev Microbiol. 1990;44:303–333. [PubMed]
  • Mackett M, Smith GL, Moss B. Vaccinia virus: a selectable eukaryotic cloning and expression vector. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7415–7419. [PMC free article] [PubMed]
  • Mackett M, Smith GL, Moss B. General method for production and selection of infectious vaccinia virus recombinants expressing foreign genes. J Virol. 1984 Mar;49(3):857–864. [PMC free article] [PubMed]
  • Morens DM, Halstead SB. Disease severity-related antigenic differences in dengue 2 strains detected by dengue 4 monoclonal antibodies. J Med Virol. 1987 Jun;22(2):169–174. [PubMed]
  • Morens DM, Halstead SB. Measurement of antibody-dependent infection enhancement of four dengue virus serotypes by monoclonal and polyclonal antibodies. J Gen Virol. 1990 Dec;71(Pt 12):2909–2914. [PubMed]
  • Morens DM, Venkateshan CN, Halstead SB. Dengue 4 virus monoclonal antibodies identify epitopes that mediate immune infection enhancement of dengue 2 viruses. J Gen Virol. 1987 Jan;68(Pt 1):91–98. [PubMed]
  • Ochiai H, Kurokawa M, Hayashi K, Niwayama S. Antibody-mediated growth of influenza A NWS virus in macrophagelike cell line P388D1. J Virol. 1988 Jan;62(1):20–26. [PMC free article] [PubMed]
  • Ochiai H, Kurokawa M, Kuroki Y, Niwayama S. Infection enhancement of influenza A H1 subtype viruses in macrophage-like P388D1 cells by cross-reactive antibodies. J Med Virol. 1990 Apr;30(4):258–265. [PubMed]
  • Panicali D, Davis SW, Weinberg RL, Paoletti E. Construction of live vaccines by using genetically engineered poxviruses: biological activity of recombinant vaccinia virus expressing influenza virus hemagglutinin. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5364–5368. [PMC free article] [PubMed]
  • Petersen NC, Boyle JF. Immunologic phenomena in the effusive form of feline infectious peritonitis. Am J Vet Res. 1980 Jun;41(6):868–876. [PubMed]
  • Peiris JS, Gordon S, Unkeless JC, Porterfield JS. Monoclonal anti-Fc receptor IgG blocks antibody enhancement of viral replication in macrophages. Nature. 1981 Jan 15;289(5794):189–191. [PubMed]
  • Porterfield JS. Antibody-dependent enhancement of viral infectivity. Adv Virus Res. 1986;31:335–355. [PubMed]
  • Robinson WE, Jr, Kawamura T, Gorny MK, Lake D, Xu JY, Matsumoto Y, Sugano T, Masuho Y, Mitchell WM, Hersh E, et al. Human monoclonal antibodies to the human immunodeficiency virus type 1 (HIV-1) transmembrane glycoprotein gp41 enhance HIV-1 infection in vitro. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3185–3189. [PMC free article] [PubMed]
  • Schlesinger JJ, Brandriss MW. Antibody-mediated infection of macrophages and macrophage-like cell lines with 17D-yellow fever virus. J Med Virol. 1981;8(2):103–117. [PubMed]
  • Schlesinger JJ, Brandriss MW. Growth of 17D yellow fever virus in a macrophage-like cell line, U937: role of Fc and viral receptors in antibody-mediated infection. J Immunol. 1981 Aug;127(2):659–665. [PubMed]
  • Schlesinger JJ, Brandriss MW. 17D yellow fever virus infection of P388D1 cells mediated by monoclonal antibodies: properties of the macrophage Fc receptor. J Gen Virol. 1983 Jun;64(Pt 6):1255–1262. [PubMed]
  • Smith GL, Murphy BR, Moss B. Construction and characterization of an infectious vaccinia virus recombinant that expresses the influenza hemagglutinin gene and induces resistance to influenza virus infection in hamsters. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7155–7159. [PMC free article] [PubMed]
  • Stoddart CA, Scott FW. Isolation and identification of feline peritoneal macrophages for in vitro studies of coronavirus-macrophage interactions. J Leukoc Biol. 1988 Nov;44(5):319–328. [PubMed]
  • Stoddart CA, Scott FW. Intrinsic resistance of feline peritoneal macrophages to coronavirus infection correlates with in vivo virulence. J Virol. 1989 Jan;63(1):436–440. [PMC free article] [PubMed]
  • Takeda A, Tuazon CU, Ennis FA. Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science. 1988 Oct 28;242(4878):580–583. [PubMed]
  • Vennema H, de Groot RJ, Harbour DA, Dalderup M, Gruffydd-Jones T, Horzinek MC, Spaan WJ. Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J Virol. 1990 Mar;64(3):1407–1409. [PMC free article] [PubMed]
  • Vennema H, Heijnen L, Zijderveld A, Horzinek MC, Spaan WJ. Intracellular transport of recombinant coronavirus spike proteins: implications for virus assembly. J Virol. 1990 Jan;64(1):339–346. [PMC free article] [PubMed]
  • Weiss RC, Scott FW. Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp Immunol Microbiol Infect Dis. 1981;4(2):175–189. [PubMed]
  • Weiss RC, Scott FW. Pathogenesis of feline infectious peritonitis: nature and development of viremia. Am J Vet Res. 1981 Mar;42(3):382–390. [PubMed]
  • Weiss RC, Scott FW. Pathogenesis of feline infetious peritonitis: pathologic changes and immunofluorescence. Am J Vet Res. 1981 Dec;42(12):2036–2048. [PubMed]

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