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. 1984 Apr;73(4):987–991. doi: 10.1172/JCI111324

Antibody-mediated bacterial adhesion to cytomegalovirus-induced Fc receptors. Potential relationship to secondary infections complicating herpesvirus infections.

P A Mackowiak, M Marling-Cason, J W Smith, J P Luby
PMCID: PMC425111  PMID: 6323540

Abstract

Cytomegalovirus (CMV) and other viruses within the herpes group have recently been shown to induce Fc receptors in infected monolayers. We have examined the possibility that such receptors might facilitate the adherence of antibody-coated bacteria to CMV-infected cells. To do this, we infected confluent human embryonic lung (HEL) cell monolayers with CMV (strain AD 169) and then used a double radiolabel assay to measure adherence of Escherichia coli 06 to both infected and control monolayers. We examined infected monolayers 48 h after viral seeding, at which time 30-60% of the cells exhibited characteristic cytopathic changes. We compared the adherence of untreated E. coli 06 with the adherence of E. coli 06 that had been preincubated for 1 h at 37 degrees C with either nonimmune or anti-E. coli 06 antiserum. Pretreatment of the E. coli 06 with specific antiserum significantly enhanced its adherence to CMV-infected, but not to control, monolayers (P less than 0.01 by the Mann-Whitney U test). We did not see such enhancement when we used anti-E. coli 06 antiserum to treat a nontypable E. coli. The augmented adherence of antibody-coated E. coli 06 to CMV-infected monolayers was abrogated by pretreating the monolayers with nonimmune serum or purified Fc fragments, but not by pretreating with IgA, IgM, or 1 mM trypan blue. Preincubating HEL cell monolayers with 100 U/ml human leukocyte interferon for 72 h at 37 degrees C did not affect the adherence of antibody-coated E. coli 06 to the monolayers. To determine if antibody-coated bacteria that adhered to the surface of CMV-infected monolayers might themselves act as receptors for microorganisms with Fc binding potential, we compared the adherence of Cowan strain Staphylococcus aureus to CMV-infected and control monolayers that had been preincubated with antibody-coated E. coli 06. The S. aureus adhered significantly better to the former monolayers (P less than 0.001). These results illustrate a previously unrecognized mechanism by which certain herpesviruses might enhance the adherence of secondary pathogens to nonphagocytic cell populations. Such a mechanism, if active in vivo, might facilitate the colonization of mucosal surfaces by these pathogenic microorganisms, and in this way might contribute to both the reported predisposition of CMV-infected patients to secondary infections and to the high prevalence of S. aureus in the vaginal flora of women with histories of genital herpes.

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Selected References

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

  1. Adler R., Glorioso J. C., Cossman J., Levine M. Possible role of Fc receptors on cells infected and transformed by herpesvirus: escape from immune cytolysis. Infect Immun. 1978 Aug;21(2):442–447. doi: 10.1128/iai.21.2.442-447.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Austin R. M., Daniels C. A. The role of protein A in the attachment of staphylococci to influenza-infected cells. Lab Invest. 1978 Aug;39(2):128–132. [PubMed] [Google Scholar]
  3. Cantell K., Hirvonen S., Mogensen K. E., Pyhälä L. Human leukocyte interferon: production, purification, stability, and animal experiments. In Vitro Monogr. 1974;(3):35–38. [PubMed] [Google Scholar]
  4. Chatterjee S. N., Fiala M., Weiner J., Stewart J. A., Stacey B., Warmer N. Primary cytomegalovirus and opportunistic infections. Incidence in renal transplant recipients. JAMA. 1978 Nov 24;240(22):2446–2449. [PubMed] [Google Scholar]
  5. Cines D. B., Lyss A. P., Bina M., Corkey R., Kefalides N. A., Friedman H. M. Fc and C3 receptors induced by herpes simplex virus on cultured human endothelial cells. J Clin Invest. 1982 Jan;69(1):123–128. doi: 10.1172/JCI110422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dickler H. B. Lymphocyte receptors for immunoglobulin. Adv Immunol. 1976;24:167–214. doi: 10.1016/s0065-2776(08)60330-2. [DOI] [PubMed] [Google Scholar]
  7. Ebersole J. L., Molinari J. A. Secretory antibody responses in axenic mice to perorally administered Staphylococcus aureus. Immunology. 1978 Mar;34(3):379–387. [PMC free article] [PubMed] [Google Scholar]
  8. Fridman W. H., Gresser I., Bandu M. T., Aguet M., Neauport-Sautes C. Interferon enhances the expression of Fc gamma receptors. J Immunol. 1980 May;124(5):2436–2441. [PubMed] [Google Scholar]
  9. Guckian J. C., Christensen W. D., Fine D. P. Trypan blue inhibits complement-mediated phagocytosis by human polymorphonuclear leukocytes. J Immunol. 1978 May;120(5):1580–1586. [PubMed] [Google Scholar]
  10. Guinan M. E., Dan B. B., Guidotti R. J., Reingold A. L., Schmid G. P., Bettoli E. J., Lossick J. G., Shands K. N., Kramer M. A., Hargrett N. T. Vaginal colonization with Staphylococcus aureus in healthy women: a review of four studies. Ann Intern Med. 1982 Jun;96(6 Pt 2):944–947. doi: 10.7326/0003-4819-96-6-944. [DOI] [PubMed] [Google Scholar]
  11. Gönczöl E., Boldogh I., Váczi L. IgG-Fc-binding receptors in cells abortively infected, or transformed, by human cytomegalovirus. Acta Microbiol Acad Sci Hung. 1981;28(2):157–164. [PubMed] [Google Scholar]
  12. Jones S. R., Smith J. W., Sanford J. P. Localization of urinary-tract infections by detection of antibody-coated bacteria in urine sediment. N Engl J Med. 1974 Mar 14;290(11):591–593. doi: 10.1056/NEJM197403142901103. [DOI] [PubMed] [Google Scholar]
  13. Rand K. H., Pollard R. B., Merigan T. C. Increased pulmonary superinfections in cardiac-transplant patients undergoing primary cytomegalovirus infection. N Engl J Med. 1978 Apr 27;298(17):951–953. doi: 10.1056/NEJM197804272981705. [DOI] [PubMed] [Google Scholar]
  14. Rubin R. H., Cosimi A. B., Tolkoff-Rubin N. E., Russell P. S., Hirsch M. S. Infectious disease syndromes attributable to cytomegalovirus and their significance among renal transplant recipients. Transplantation. 1977 Dec;24(6):458–464. doi: 10.1097/00007890-197712000-00010. [DOI] [PubMed] [Google Scholar]
  15. Sakuma S., Furukawa T., Plotkin S. A. The characterization of IgG receptor induced by human cytomegalovirus. Proc Soc Exp Biol Med. 1977 Jun;155(2):168–172. doi: 10.3181/00379727-155-39767. [DOI] [PubMed] [Google Scholar]
  16. Sanford B. A., Shelokov A., Ramsay M. A. Bacterial adherence to virus-infected cells: a cell culture model of bacterial superinfection. J Infect Dis. 1978 Feb;137(2):176–181. doi: 10.1093/infdis/137.2.176. [DOI] [PubMed] [Google Scholar]
  17. Sarov I., Abady I. The morphogenesis of human cytomegalovirus. Isolation and polypeptide characterization of cytomegalovirions and dense bodies. Virology. 1975 Aug;66(2):464–473. doi: 10.1016/0042-6822(75)90218-4. [DOI] [PubMed] [Google Scholar]
  18. Schalén C., Christensen P., Grubb A., Samuelsson G., Svensson M. L. Demonstration of separate receptors for human IgA and IgG in group A streptococci type 4. Separation of the solubilized receptors from group- and type-specific antigens, lipoteichoic acid and peptidoglycan. Acta Pathol Microbiol Scand C. 1980 Apr;88(2):77–82. doi: 10.1111/j.1699-0463.1980.tb00076.x. [DOI] [PubMed] [Google Scholar]
  19. Smith J. W., Kaijser B. The local immune response to Escherichia coli O and K antigen in experimental pyelonephritis. J Clin Invest. 1976 Aug;58(2):276–281. doi: 10.1172/JCI108469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Stephens C. G., Reed W. P., Kronvall G., Williams R. C., Jr Reactions between certain strains of pneumococci and Fc of IgG. J Immunol. 1974 Jun;112(6):1955–1960. [PubMed] [Google Scholar]
  21. Walker J. Antibody responses of monkeys to oral and local immunization with Streptococcus mutans. Infect Immun. 1981 Jan;31(1):61–70. doi: 10.1128/iai.31.1.61-70.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Westmoreland D., Watkins J. F. The IgG receptor induced by herpes simplex virus: studies using radioiodinated IgG. J Gen Virol. 1974 Jul;24(1):167–178. doi: 10.1099/0022-1317-24-1-167. [DOI] [PubMed] [Google Scholar]

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