Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

Infection and Immunity logoLink to Infection and Immunity
. 1996 May;64(5):1789–1793. doi: 10.1128/iai.64.5.1789-1793.1996

Intracellular survival and replication of Erysipelothrix rhusiopathiae within murine macrophages: failure of induction of the oxidative burst of macrophages.

Y Shimoji 1, Y Yokomizo 1, Y Mori 1
PMCID: PMC173993  PMID: 8613392

Abstract

We investigated the ability of a virulent wild-type parent strain and acapsular avirulent transposon mutants to enter and survive intracellularly within murine peritoneal macrophages. In the presence of normal or immune serum, the parent and mutant strains were both ingested; however, the number of ingested bacteria was three- to fourfold greater in the case of mutant strains than in the case of the parent strain. The parent strain, but not the mutant strains, survived and replicated intracellularly when ingested in the presence of normal serum, whereas both the parent and the mutant strains were readily killed when ingested in the presence of immune serum. To further investigate the mechanism by which the parent strain can survive and replicate within macrophages, we studied the oxidative burst response of macrophages to these strains by measuring chemiluminescence and intracellular reduction of Nitro Blue Tetrazolium dye. Challenge exposure of macrophages with either the parent strain preopsonized with immune serum or the mutant strains preopsonized with normal or immune serum induced a strong oxidative burst, whereas the level was very low when the parent strain was preopsonized with normal serum. Phagocytosis of either the parent strain, in the presence of immune serum, or the mutant strains, in the presence of normal or immune serum, by macrophages reduced large amounts of intracellular Nitro Blue Tetrazolium, whereas minimal amounts were reduced by the parent strain in the presence of normal serum. These results suggest that virulent E. rhusiopathiae can survive and subsequently replicate within murine macrophages when ingested in the presence of normal serum and that the reduced production of reactive oxidative metabolites by macrophages may, in part, be responsible for this occurrence.

Full Text

The Full Text of this article is available as a PDF (409.1 KB).

Selected References

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

  1. Beaman L., Beaman B. L. Monoclonal antibodies demonstrate that superoxide dismutase contributes to protection of Nocardia asteroides within the intact host. Infect Immun. 1990 Sep;58(9):3122–3128. doi: 10.1128/iai.58.9.3122-3128.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Czuprynski C. J., Hamilton H. L. Bovine neutrophils ingest but do not kill Haemophilus somnus in vitro. Infect Immun. 1985 Nov;50(2):431–436. doi: 10.1128/iai.50.2.431-436.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Czuprynski C. J., Henson P. M., Campbell P. A. Killing of Listeria monocytogenes by inflammatory neutrophils and mononuclear phagocytes from immune and nonimmune mice. J Leukoc Biol. 1984 Feb;35(2):193–208. doi: 10.1002/jlb.35.2.193. [DOI] [PubMed] [Google Scholar]
  4. Densen P., Mandell G. L. Gonococcal interactions with polymorphonuclear neutrophils: importance of the phagosome for bactericidal activity. J Clin Invest. 1978 Dec;62(6):1161–1171. doi: 10.1172/JCI109235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Densen P., Mandell G. L. Phagocyte strategy vs. microbial tactics. Rev Infect Dis. 1980 Sep-Oct;2(5):817–838. doi: 10.1093/clinids/2.5.817. [DOI] [PubMed] [Google Scholar]
  6. Dijkmans B. A., Leijh P. C., Braat A. G., van Furth R. Effect of bacterial competition on the opsonization, phagocytosis, and intracellular killing of microorganisms by granulocytes. Infect Immun. 1985 Jul;49(1):219–224. doi: 10.1128/iai.49.1.219-224.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Drevets D. A., Campbell P. A. Macrophage phagocytosis: use of fluorescence microscopy to distinguish between extracellular and intracellular bacteria. J Immunol Methods. 1991 Aug 28;142(1):31–38. doi: 10.1016/0022-1759(91)90289-r. [DOI] [PubMed] [Google Scholar]
  8. Drevets D. A., Campbell P. A. Roles of complement and complement receptor type 3 in phagocytosis of Listeria monocytogenes by inflammatory mouse peritoneal macrophages. Infect Immun. 1991 Aug;59(8):2645–2652. doi: 10.1128/iai.59.8.2645-2652.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drevets D. A., Canono B. P., Campbell P. A. Listericidal and nonlistericidal mouse macrophages differ in complement receptor type 3-mediated phagocytosis of L. monocytogenes and in preventing escape of the bacteria into the cytoplasm. J Leukoc Biol. 1992 Jul;52(1):70–79. doi: 10.1002/jlb.52.1.70. [DOI] [PubMed] [Google Scholar]
  10. Franzon V. L., Arondel J., Sansonetti P. J. Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun. 1990 Feb;58(2):529–535. doi: 10.1128/iai.58.2.529-535.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harmon B. G., Adams L. G., Frey M. Survival of rough and smooth strains of Brucella abortus in bovine mammary gland macrophages. Am J Vet Res. 1988 Jul;49(7):1092–1097. [PubMed] [Google Scholar]
  12. Hondalus M. K., Diamond M. S., Rosenthal L. A., Springer T. A., Mosser D. M. The intracellular bacterium Rhodococcus equi requires Mac-1 to bind to mammalian cells. Infect Immun. 1993 Jul;61(7):2919–2929. doi: 10.1128/iai.61.7.2919-2929.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ishibashi Y., Arai T. Roles of the complement receptor type 1 (CR1) and type 3 (CR3) on phagocytosis and subsequent phagosome-lysosome fusion in Salmonella-infected murine macrophages. FEMS Microbiol Immunol. 1990 Sep;2(2):89–96. doi: 10.1111/j.1574-6968.1990.tb03505.x. [DOI] [PubMed] [Google Scholar]
  14. Kreutzer D. L., Dreyfus L. A., Robertson D. C. Interaction of polymorphonuclear leukocytes with smooth and rough strains of Brucella abortus. Infect Immun. 1979 Mar;23(3):737–742. doi: 10.1128/iai.23.3.737-742.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kumagai K., Itoh K., Hinuma S., Tada M. Pretreatment of plastic Petri dishes with fetal calf serum. A simple method for macrophage isolation. J Immunol Methods. 1979;29(1):17–25. doi: 10.1016/0022-1759(79)90121-2. [DOI] [PubMed] [Google Scholar]
  16. Lachmann P. G., Deicher H. Solubilization and characterization of surface antigenic components of Erysipelothrix rhusiopathiae T28. Infect Immun. 1986 Jun;52(3):818–822. doi: 10.1128/iai.52.3.818-822.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Leijh P. C., van den Barselaar M. T., Daha M. R., van Furth R. Stimulation of the intracellular killing of Staphylococcus aureus by monocytes: regulation by immunoglobulin G and complement components C3/C3b and B/Bb. J Immunol. 1982 Jul;129(1):332–337. [PubMed] [Google Scholar]
  18. Leijh P. C., van den Barselaar M. T., Dubbeldeman-Rempt I., van Furth R. Kinetics of intracellular killing of Staphylococcus aureus and Escherichia coli by human granulocytes. Eur J Immunol. 1980 Oct;10(10):750–757. doi: 10.1002/eji.1830101005. [DOI] [PubMed] [Google Scholar]
  19. Mandell G. L. Catalase, superoxide dismutase, and virulence of Staphylococcus aureus. In vitro and in vivo studies with emphasis on staphylococcal--leukocyte interaction. J Clin Invest. 1975 Mar;55(3):561–566. doi: 10.1172/JCI107963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miller R. M., Garbus J., Hornick R. B. Lack of enhanced oxygen consumption by polymorphonuclear leukocytes on phagocytosis of virulent Salmonella typhi. Science. 1972 Mar 3;175(4025):1010–1011. doi: 10.1126/science.175.4025.1010. [DOI] [PubMed] [Google Scholar]
  21. Mosser D. M., Edelson P. J. The third component of complement (C3) is responsible for the intracellular survival of Leishmania major. 1987 May 28-Jun 3Nature. 327(6120):329–331. doi: 10.1038/327329b0. [DOI] [PubMed] [Google Scholar]
  22. Payne N. R., Horwitz M. A. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J Exp Med. 1987 Nov 1;166(5):1377–1389. doi: 10.1084/jem.166.5.1377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shimoji Y., Yokomizo Y., Sekizaki T., Mori Y., Kubo M. Presence of a capsule in Erysipelothrix rhusiopathiae and its relationship to virulence for mice. Infect Immun. 1994 Jul;62(7):2806–2810. doi: 10.1128/iai.62.7.2806-2810.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Timoney J. The effect of decomplementation on Erysipelothrix rhusiopathiae infection in the mouse. Immunology. 1970 Oct;19(4):561–567. [PMC free article] [PubMed] [Google Scholar]
  25. Timoney J. The inactivation of Erysipelothrix rhuopathiae in macrophages from normal and immune mice. Res Vet Sci. 1969 May;10(3):301–302. [PubMed] [Google Scholar]
  26. Timoney J. The inactivation of Erysipelothrix rhusiopathiae in pig buffy-coat leucocytes. Res Vet Sci. 1970 Mar;11(2):189–190. [PubMed] [Google Scholar]
  27. Wilson C. B., Tsai V., Remington J. S. Failure to trigger the oxidative metabolic burst by normal macrophages: possible mechanism for survival of intracellular pathogens. J Exp Med. 1980 Feb 1;151(2):328–346. doi: 10.1084/jem.151.2.328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wood R. L. Swine erysipelas--a review of prevalence and research. J Am Vet Med Assoc. 1984 Apr 15;184(8):944–949. [PubMed] [Google Scholar]
  29. Wright S. D., Silverstein S. C. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J Exp Med. 1983 Dec 1;158(6):2016–2023. doi: 10.1084/jem.158.6.2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Yokomizo Y., Isayama Y. Antibody activities of IgM and IgG fractions from rabbit anti-Erysipelothrix rhusiopathiae sera. Res Vet Sci. 1972 May;13(3):294–296. [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES