Skip to main content
NCBI home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 1994;139(3):273–285. doi: 10.1007/BF01310791

The role of IgG subclass of mouse monoclonal antibodies in antibody-dependent enhancement of feline infectious peritonitis virus infection of feline macrophages

T Hohdatsu 1, J Tokunaga 1, H Koyama 1
PMCID: PMC7087006  PMID: 7832635

Summary

Antibody-dependent enhancement (ADE) of feline infectious peritonitis virus (FIPV) infection was studied in feline alveolar macrophages and human monocyte cell line U937 using mouse neutralizing monoclonal antibodies (MAbs) directed to the spike protein of FIPV. Even among the MAbs that have been shown to recognize the same antigenic site, IgG 2a MAbs enhanced FIPV infection strongly, whereas IgG 1 MAbs did not. These IgG 2a MAbs enhanced the infection even when macrophages pretreated with the MAb were washed and then inoculated with the virus. Immunofluorescence flow cytometric analysis of the macrophages treated with each of the MAbs showed that the IgG 2a MAbs but not the IgG 1 MAbs bound to feline alveolar macrophages. Treatment of the IgG 2a MAb with protein A decreased the binding to the macrophages and, in parallel, diminished the ADE activity. Although no infection was observed by inoculation of FIPV to human monocyte cell line U937 cells, FIPV complexed with either the IgG 2a MAb or the IgG 1 MAb caused infection in U937 cells which are shown to express Fc gamma receptor (Fc γ R) I and II that can bind mouse IgG 2a and IgG 1, respectively. These results suggest that the enhancing activity of MAb is closely correlated with IgG subclass and that the correlation is involved in binding of MAb to Fc γ R on feline macrophage.

Keywords: U937 Cell, Flow Cytometric Analysis, Gamma Receptor, Enhance Activity, Antigenic Site

References

  • 1.Anderson CL, Guyre PM, Whitin JC, Ryan DH, Loony RJ, Fanger MW. Monoclonal antibodies to Fc receptors for IgG on human mononuclear phagocytes: antibody characterization and induction of superoxide production in a monocyte cell line. J Biol Chem. 1986;261:12856–12864. [PubMed] [Google Scholar]
  • 2.Barlough JE, Stoddart CA, Sorresso GP, Jacobson RH, Scott FW. Experimental inoculation of cats with canine coronavirus and subsequent challenge with feline infectious peritonitis virus. Lab Anim Sci. 1984;34:592–597. [PubMed] [Google Scholar]
  • 3.Cardosa MJ, Gordon S, Hirsch S, Springer TA, Porterfield JS. Interaction of West Nile virus with primary murine macrophages: role of cell activation and receptors for antibody and complement. J Virol. 1986;57:952–959. doi: 10.1128/jvi.57.3.952-959.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Chanas AC, Gould EA, Clegg JCS, Varma MGR. Monoclonal antibodies to Sindbis virus glycoprotein E1 can neutralize, enhance infectivity, and independently inhibit haemagglutination or haemolysis. J Gen Virol. 1982;58:37–46. doi: 10.1099/0022-1317-58-1-37. [DOI] [PubMed] [Google Scholar]
  • 5.Corapi WV, Olsen CW, Scott FW. Monoclonal antibody analysis of neutralization and antibody-dependent enhancement of feline infectious peritonitis virus. J Virol. 1992;66:6695–6705. doi: 10.1128/jvi.66.11.6695-6705.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Flelt HB, Wright SD, Unkeless JC. Human neutrophilic Fc-γ receptor distribution and structure. Proc Natl Acad Sci USA. 1982;79:3275–3279. doi: 10.1073/pnas.79.10.3275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Halstead SB. Pathogenesis of dengue: challenges to molecular Biology. Science. 1988;239:476–481. doi: 10.1126/science.3277268. [DOI] [PubMed] [Google Scholar]
  • 8.Halstead SB, O'Rourke EJ. Antibody-enhanced dengue virus infection in primate leukocytes. Nature. 1977;265:739–741. doi: 10.1038/265739a0. [DOI] [PubMed] [Google Scholar]
  • 9.Halstead SB, O'Rourke EJ. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by nonneutralizing antibody. J Exp Med. 1977;146:201–217. doi: 10.1084/jem.146.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Halstead SB, Venkatenshan CN, Gentry MK, Larsen LK. Heterogeneity of infection enhancement of dengue 2 strains by monoclonal antibodies. J Immunol. 1984;132:1529–1532. [PubMed] [Google Scholar]
  • 11.Hohdatsu T, Okada S, Koyama H. Characterization of monoclonal antibodies against feline infectious peritonitis virus type II and antigenic relationship between feline, porcine and canine coronaviruses. Arch Virol. 1991;117:85–95. doi: 10.1007/BF01310494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Hohdatsu T, Nakamura M, Ishizuka Y, Yamada H, Koyama H. A study on the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection in feline macrophages by monoclonal antibodies. Arch Virol. 1991;120:207–217. doi: 10.1007/BF01310476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Hohdatsu T, Yamada H, Ishizuka Y, Koyama H. Enhancement and neutralization of feline infectious peritonitis virus infection in feline macrophages by neutralizing monoclonal antibodies recognizing different epitopes. Microbiol Immunol. 1993;37:499–504. doi: 10.1111/j.1348-0421.1993.tb03242.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Kimura T, Ueba N, Minekawa Y. Studies on the mechanism of antibody-mediated enhancement of Getah virus infectivity. Biken J. 1981;24:39–45. [PubMed] [Google Scholar]
  • 15.Looney RJ, Abraham GN, Anderson CL. Human monocytes and U937 cells bear two distinct Fc receptors for IgG. J Immunol. 1986;136:1641–1647. [PubMed] [Google Scholar]
  • 16.Mady BJ, Kurane I, Erbe DV, Fanger MW, Ennis FA. Neuraminidase augments Fc γ receptor II-mediated antibody-dependent enhancement of dengue virus infection. J Gen Virol. 1993;74:839–844. doi: 10.1099/0022-1317-74-5-839. [DOI] [PubMed] [Google Scholar]
  • 17.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;68:91–98. doi: 10.1099/0022-1317-68-1-91. [DOI] [PubMed] [Google Scholar]
  • 18.Ochiai H, Kurokawa M, Hayashi K, Niwayama S. Antibody-mediated growth of influenza A NWS virus in macrophagelike cell line P388D1. J Virol. 1988;62:20–26. doi: 10.1128/jvi.62.1.20-26.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Olsen CW, Corapi WV, Jacobson RH, Simkins RA, Saif LJ, Scott FW. Identification of antigenic sites meediating antibody-dependent enhancement of feline infectious peritonitis virus infectivity. J Gen Virol. 1993;74:745–749. doi: 10.1099/0022-1317-74-4-745. [DOI] [PubMed] [Google Scholar]
  • 20.Olsen CW, Corapi WV, Ngichabe CK, Baines JD, Scott FW. Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J Virol. 1992;66:956–965. doi: 10.1128/jvi.66.2.956-965.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Pedersen NC, Black WB. Attempted immunization of cats against feline infectious peritonitis, using avirulent live virus or sublethal amounts of virulent virus. Am J Vet Res. 1983;44:229–234. [PubMed] [Google Scholar]
  • 22.Pedersen NC, Boyle JF. Immunologic phenomena in the effusive form of feline infectious peritonitis. Am J Vet Res. 1980;41:868–876. [PubMed] [Google Scholar]
  • 23.Pedersen NC, Everman JF, Mckeirnan AJ, Ott RL. Pathogenicity studies of feline coronavirus isolates 79-1146 and 79-1683. Am J Vet Res. 1984;45:2580–2585. [PubMed] [Google Scholar]
  • 24.Pedersen NC, Boyle JF, Floyd K, Fudge A, Barker J. An enteric coronavirus infection of cats and its relationship to feline infectious peritonitis. Am J Vet Res. 1981;42:368–377. [PubMed] [Google Scholar]
  • 25.Pedersen NC. Virologic and immunologic aspects of feline infectious peritonitis virus infection. Adv Exp Med Biol. 1987;218:529–550. doi: 10.1007/978-1-4684-1280-2_69. [DOI] [PubMed] [Google Scholar]
  • 26.Peiris JSM, Porterfield JS. Antibody-mediated enhancement of flavivirus replication in macrophage-like cell lines. Nature. 1979;282:509–511. doi: 10.1038/282509a0. [DOI] [PubMed] [Google Scholar]
  • 27.Schlesinger JJ, Brandriss MW. Growth of 17 D yellow fever virus in a macrophage-like cell line, U937: role of Fc and viral receptors in antibody-mediated infection. J Immunol. 1981;127:659–665. [PubMed] [Google Scholar]
  • 28.Schultz RD, Scott FW, Duncan JR, Gillespie JH. Feline immunoglobulins. Infect Immun. 1974;9:391–393. doi: 10.1128/iai.9.2.391-393.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Stoddart CA, Barlough JE, Baldwin CA, Scott FW. Attempted immunisation of cats against feline infectious peritonitis using canine coronavirus. Res Vet Sci. 1988;45:383–388. doi: 10.1016/S0034-5288(18)30970-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Stoddart ME, Gaskell RM, Harbour DA, Pearson GR. The sites of early viral replication in feline infectious peritonitis. Vet Microbiol. 1988;18:259–271. doi: 10.1016/0378-1135(88)90092-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Takeda A, Tuazon CV, Ennis FA. Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science. 1988;242:580–583. doi: 10.1126/science.2972065. [DOI] [PubMed] [Google Scholar]
  • 32.Unkeless JC. Function and heterogeneity of human Fc receptors for immunoglobulin G. J Clin Invest. 1989;83:355–361. doi: 10.1172/JCI113891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Vennema H, De Groot RJ, Harbour DA, Dalderup M, Gruffydd-Jones T, Horzinek MC, Spaan WJM. Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J Virol. 1990;64:1407–1409. doi: 10.1128/jvi.64.3.1407-1409.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Weiss RC, Scott FW. Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp Immunol Microbiol Infect Dis. 1981;4:175–189. doi: 10.1016/0147-9571(81)90003-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Woods RD, Pedersen NC. Cross-protection studies between feline infectious peritonitis and porcine transmissible gastroenteritis viruses. Vet Microbiol. 1979;4:11–16. [Google Scholar]

Articles from Archives of Virology are provided here courtesy of Nature Publishing Group

RESOURCES