Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1984 Sep;51(3):643–649. doi: 10.1128/jvi.51.3.643-649.1984

Macrophage Fc receptors control infectivity and neutralization of canine distemper virus-antibody complexes.

M J Appel, S G Mendelson, W W Hall
PMCID: PMC255817  PMID: 6471166

Abstract

Dogs that are persistently infected or that become moribund after exposure to canine distemper virus (CDV) have antibody that neutralized CDV when tested in dog lung macrophage cultures but failed to neutralize CDV when tested in epithelial, fibroblastic, or lymphatic cells. The antibody attached to protein A and was found in the immunoglobulin G fraction. The antibody bound complement and lysed CDV-infected target cells. The neutralizing activity in macrophages could be abolished (i) by pepsin digestion and removal of Fc portions from the antibody, (ii) by blocking the Fc receptors of macrophages with heat-treated normal dog serum, and (iii) by binding of protein A to Fc portions of the antibody. It was concluded that attachment of the CDV-antibody complex to Fc receptors of macrophages was essential for virus neutralization. If this attachment was hindered, the CDV-antibody complex became infectious for macrophages. In contrast, serum from recovering dogs neutralized CDV when tested in epithelial, fibroblastic, or lymphatic cells as well as in macrophages.

Full text

PDF
643

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albrecht P., Herrmann K., Burns G. R. Role of virus strain in conventional and enhanced measles plaque neutralization test. J Virol Methods. 1981 Dec;3(5):251–260. doi: 10.1016/0166-0934(81)90062-8. [DOI] [PubMed] [Google Scholar]
  2. Appel M. J., Jones O. R. Use of alveolar macrophages for cultivation of canine distemper virus. Proc Soc Exp Biol Med. 1967 Nov;126(2):571–574. doi: 10.3181/00379727-126-32509. [DOI] [PubMed] [Google Scholar]
  3. Appel M. J., Shek W. R., Summers B. A. Lymphocyte-mediated immune cytotoxicity in dogs infected with virulent canine distemper virus. Infect Immun. 1982 Aug;37(2):592–600. doi: 10.1128/iai.37.2.592-600.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Appel M., Robson D. S. A microneutralization test for canine distemper virus. Am J Vet Res. 1973 Nov;34(11):1459–1463. [PubMed] [Google Scholar]
  5. Brandt W. E., McCown J. M., Gentry M. K., Russell P. K. Infection enhancement of dengue type 2 virus in the U-937 human monocyte cell line by antibodies to flavivirus cross-reactive determinants. Infect Immun. 1982 Jun;36(3):1036–1041. doi: 10.1128/iai.36.3.1036-1041.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coggins L. African swine fever virus. Pathogenesis. Prog Med Virol. 1974;18(0):48–63. [PubMed] [Google Scholar]
  7. Della-Porta A. J., Westaway E. G. A multi-hit model for the neutralization of animal viruses. J Gen Virol. 1978 Jan;38(1):1–19. doi: 10.1099/0022-1317-38-1-1. [DOI] [PubMed] [Google Scholar]
  8. Einstein L. P., Schneeberger E. E., Colten H. R. Synthesis of the second component of complement by long-term primary cultures of human monocytes. J Exp Med. 1976 Jan 1;143(1):114–126. doi: 10.1084/jem.143.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fujinami R. S., Oldstone M. B. Alterations in expression of measles virus polypeptides by antibody: molecular events in antibody-induced antigenic modulation. J Immunol. 1980 Jul;125(1):78–85. [PubMed] [Google Scholar]
  10. Halstead S. B., O'Rourke E. J. Antibody-enhanced dengue virus infection in primate leukocytes. Nature. 1977 Feb 24;265(5596):739–741. doi: 10.1038/265739a0. [DOI] [PubMed] [Google Scholar]
  11. Helenius A., Marsh M., White J. Inhibition of Semliki forest virus penetration by lysosomotropic weak bases. J Gen Virol. 1982 Jan;58(Pt 1):47–61. doi: 10.1099/0022-1317-58-1-47. [DOI] [PubMed] [Google Scholar]
  12. Henson J. B., McGuire T. C. Equine infectious anemia. Prog Med Virol. 1974;18(0):143–159. [PubMed] [Google Scholar]
  13. KJELLEN L. E., SCHLESINGER R. W. Influence of host cell on residual infectivity of neutralized vesicular stomatitis virus. Virology. 1959 Feb;7(2):236–239. doi: 10.1016/0042-6822(59)90189-8. [DOI] [PubMed] [Google Scholar]
  14. Klevjer-Anderson P., McGuire T. C. Neutralizing antibody response of rabbits and goats to caprine arthritis-encephalitis virus. Infect Immun. 1982 Nov;38(2):455–461. doi: 10.1128/iai.38.2.455-461.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LAFFERTY K. J. THE INTERACTION BETWEEN VIRUS AND ANTIBODY. I. KINETIC STUDIES. Virology. 1963 Sep;21:61–75. doi: 10.1016/0042-6822(63)90305-2. [DOI] [PubMed] [Google Scholar]
  16. Littman B. H., Ruddy S. Production of the second component of complement by human monocytes: stimulation by antigen-activated lymphocytes or lymphokines. J Exp Med. 1977 May 1;145(5):1344–1352. doi: 10.1084/jem.145.5.1344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Majer M. Virus sensitization. Curr Top Microbiol Immunol. 1972;58:69–84. doi: 10.1007/978-3-642-65357-5_2. [DOI] [PubMed] [Google Scholar]
  18. Marsh M., Matlin K., Simons K., Reggio H., White J., Kartenbeck J., Helenius A. Are lysosomes a site of enveloped-virus penetration? Cold Spring Harb Symp Quant Biol. 1982;46(Pt 2):835–843. doi: 10.1101/sqb.1982.046.01.078. [DOI] [PubMed] [Google Scholar]
  19. Müller W., Hanauske-Abel H., Loos M. Biosynthesis of the first component of complement by human and guinea pig peritoneal macrophages: evidence for an independent production of the C1 subunits. J Immunol. 1978 Oct;121(4):1578–1584. [PubMed] [Google Scholar]
  20. Notkins A. L., Mage M., Ashe W. K., Mahar S. Neutralization of sensitized lactic dehydrogenase virus by anti-gammglobulin. J Immunol. 1968 Feb;100(2):314–320. [PubMed] [Google Scholar]
  21. Oldstone M. B., Dixon F. J. Pathogenesis of chronic disease associated with persistent lymphocytic choriomeningitis viral infection. I. Relationship of antibody production to disease in neonatally infected mice. J Exp Med. 1969 Mar 1;129(3):483–505. doi: 10.1084/jem.129.3.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Peiris J. S., Gordon S., Unkeless J. C., Porterfield J. S. Monoclonal anti-Fc receptor IgG blocks antibody enhancement of viral replication in macrophages. Nature. 1981 Jan 15;289(5794):189–191. doi: 10.1038/289189a0. [DOI] [PubMed] [Google Scholar]
  23. Petersen N. C., Boyle J. F. Immunologic phenomena in the effusive form of feline infectious peritonitis. Am J Vet Res. 1980 Jun;41(6):868–876. [PubMed] [Google Scholar]
  24. Poole B., Ohkuma S. Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J Cell Biol. 1981 Sep;90(3):665–669. doi: 10.1083/jcb.90.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Porter D. D., Larsen A. E., Porter H. G. The pathogenesis of Aleutian disease of mink. I. In vivo viral replication and the host antibody response to viral antigen. J Exp Med. 1969 Sep 1;130(3):575–593. doi: 10.1084/jem.130.3.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Poulsen F., Hjort T. A simple method for the production of F(ab')2 preparations by pepsin digestion of total serum protein. Acta Pathol Microbiol Scand C. 1980 Oct;88(5):241–245. doi: 10.1111/j.1699-0463.1980.tb00101.x. [DOI] [PubMed] [Google Scholar]
  27. Prineas J. W., Graham J. S. Multiple sclerosis: capping of surface immunoglobulin G on macrophages engaged in myelin breakdown. Ann Neurol. 1981 Aug;10(2):149–158. doi: 10.1002/ana.410100205. [DOI] [PubMed] [Google Scholar]
  28. Shek W. R., Schultz R. D., Appel M. J. Natural and immune cytolysis of canine distemper virus-infected target cells. Infect Immun. 1980 Jun;28(3):724–734. doi: 10.1128/iai.28.3.724-734.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Steplewski Z., Lubeck M. D., Koprowski H. Human macrophages armed with murine immunoglobulin G2a antibodies to tumors destroy human cancer cells. Science. 1983 Aug 26;221(4613):865–867. doi: 10.1126/science.6879183. [DOI] [PubMed] [Google Scholar]
  30. Summers B. A., Greisen H. A., Appel M. J. Does virus persist in the uvea in multiple sclerosis, as in canine distemper encephalomyelitis? Lancet. 1983 Aug 13;2(8346):372–375. doi: 10.1016/s0140-6736(83)90346-x. [DOI] [PubMed] [Google Scholar]
  31. Tsai S. C., Summers B. A., Appel M. J. Interferon in cerebrospinal fluid. A marker for viral persistence of canine distemper encephalomyelitis. Arch Virol. 1982;72(4):257–265. doi: 10.1007/BF01315222. [DOI] [PubMed] [Google Scholar]
  32. Warr G. W., Hart I. R. Binding of canine IgM and IgG to protein A of Staphylococcus aureus: a simple method for the isolation of canine immunoglobulins from serum and the lymphocyte surface. Am J Vet Res. 1979 Jul;40(7):922–926. [PubMed] [Google Scholar]
  33. Whaley K. Biosynthesis of the complement components and the regulatory proteins of the alternative complement pathway by human peripheral blood monocytes. J Exp Med. 1980 Mar 1;151(3):501–516. doi: 10.1084/jem.151.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES