Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1996 Oct;64(10):4242–4248. doi: 10.1128/iai.64.10.4242-4248.1996

Apoptosis of monocytes and prolonged survival of granulocytes as a result of phagocytosis of bacteria.

J Baran 1, K Guzik 1, W Hryniewicz 1, M Ernst 1, H D Flad 1, J Pryjma 1
PMCID: PMC174363  PMID: 8926095

Abstract

Monocytes and granulocytes were incubated with suspensions of Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa, or Salmonella enteritidis and, after being washed free of bacteria, cultured for up to 48 h. Every few hours, samples of cultured cells were taken for DNA isolation. Monocytes which phagocytosed bacteria showed features of apoptotic cells, as determined by light microscopy and DNA fragmentation detected by gel electrophoresis. The phenomenon was observed 2 to 4 h after phagocytosis, in contrast, control monocytes did not show signs of apoptosis until 48 h of culture. Intact control granulocytes spontaneously became apoptotic after 12 h of culture. In contrast, degradation of DNA in cells exposed to bacteria was delayed by 12 to 24 h. In conclusion, our observation suggests that granulocytes and monocytes react differently to phagocytosis of bacteria.

Full Text

The Full Text of this article is available as a PDF (526.9 KB).

Selected References

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

  1. Arai T., Hiromatsu K., Nishimura H., Kimura Y., Kobayashi N., Ishida H., Nimura Y., Yoshikai Y. Endogenous interleukin 10 prevents apoptosis in macrophages during Salmonella infection. Biochem Biophys Res Commun. 1995 Aug 15;213(2):600–607. doi: 10.1006/bbrc.1995.2174. [DOI] [PubMed] [Google Scholar]
  2. Arruda S., Bomfim G., Knights R., Huima-Byron T., Riley L. W. Cloning of an M. tuberculosis DNA fragment associated with entry and survival inside cells. Science. 1993 Sep 10;261(5127):1454–1457. doi: 10.1126/science.8367727. [DOI] [PubMed] [Google Scholar]
  3. BURTON K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J. 1956 Feb;62(2):315–323. doi: 10.1042/bj0620315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baran J., Pryjma J. The reduced expression of HLA-class II antigens and adhesion molecules on monocyte surface after phagocytosis of bacteria. Arch Immunol Ther Exp (Warsz) 1994;42(2):101–106. [PubMed] [Google Scholar]
  5. Buttke T. M., Sandstrom P. A. Oxidative stress as a mediator of apoptosis. Immunol Today. 1994 Jan;15(1):7–10. doi: 10.1016/0167-5699(94)90018-3. [DOI] [PubMed] [Google Scholar]
  6. Cassatella M. A. The production of cytokines by polymorphonuclear neutrophils. Immunol Today. 1995 Jan;16(1):21–26. doi: 10.1016/0167-5699(95)80066-2. [DOI] [PubMed] [Google Scholar]
  7. Colotta F., Re F., Polentarutti N., Sozzani S., Mantovani A. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood. 1992 Oct 15;80(8):2012–2020. [PubMed] [Google Scholar]
  8. Cox G., Oberley L. W., Hunninghake G. W. Manganese superoxide dismutase and heat shock protein 70 are not necessary for suppression of apoptosis in human peripheral blood neutrophils. Am J Respir Cell Mol Biol. 1994 May;10(5):493–498. doi: 10.1165/ajrcmb.10.5.7514009. [DOI] [PubMed] [Google Scholar]
  9. Gorczyca W., Gong J., Darzynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 1993 Apr 15;53(8):1945–1951. [PubMed] [Google Scholar]
  10. Hampton M. B., Vissers M. C., Winterbourn C. C. A single assay for measuring the rates of phagocytosis and bacterial killing by neutrophils. J Leukoc Biol. 1994 Feb;55(2):147–152. doi: 10.1002/jlb.55.2.147. [DOI] [PubMed] [Google Scholar]
  11. Jonas D., Walev I., Berger T., Liebetrau M., Palmer M., Bhakdi S. Novel path to apoptosis: small transmembrane pores created by staphylococcal alpha-toxin in T lymphocytes evoke internucleosomal DNA degradation. Infect Immun. 1994 Apr;62(4):1304–1312. doi: 10.1128/iai.62.4.1304-1312.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lee A., Whyte M. K., Haslett C. Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J Leukoc Biol. 1993 Oct;54(4):283–288. [PubMed] [Google Scholar]
  13. Liles W. C., Klebanoff S. J. Regulation of apoptosis in neutrophils--Fas track to death? J Immunol. 1995 Oct 1;155(7):3289–3291. [PubMed] [Google Scholar]
  14. Mangan D. F., Welch G. R., Wahl S. M. Lipopolysaccharide, tumor necrosis factor-alpha, and IL-1 beta prevent programmed cell death (apoptosis) in human peripheral blood monocytes. J Immunol. 1991 Mar 1;146(5):1541–1546. [PubMed] [Google Scholar]
  15. Molloy A., Laochumroonvorapong P., Kaplan G. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guérin. J Exp Med. 1994 Oct 1;180(4):1499–1509. doi: 10.1084/jem.180.4.1499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Moore K. J., Matlashewski G. Intracellular infection by Leishmania donovani inhibits macrophage apoptosis. J Immunol. 1994 Mar 15;152(6):2930–2937. [PubMed] [Google Scholar]
  17. Morel F., Doussiere J., Vignais P. V. The superoxide-generating oxidase of phagocytic cells. Physiological, molecular and pathological aspects. Eur J Biochem. 1991 Nov 1;201(3):523–546. doi: 10.1111/j.1432-1033.1991.tb16312.x. [DOI] [PubMed] [Google Scholar]
  18. Morimoto H., Bonavida B. Diphtheria toxin- and Pseudomonas A toxin-mediated apoptosis. ADP ribosylation of elongation factor-2 is required for DNA fragmentation and cell lysis and synergy with tumor necrosis factor-alpha. J Immunol. 1992 Sep 15;149(6):2089–2094. [PubMed] [Google Scholar]
  19. Perticarari S., Presani G., Banfi E. A new flow cytometric assay for the evaluation of phagocytosis and the oxidative burst in whole blood. J Immunol Methods. 1994 Mar 29;170(1):117–124. doi: 10.1016/0022-1759(94)90251-8. [DOI] [PubMed] [Google Scholar]
  20. Polla B. S., Stubbe H., Kantengwa S., Maridonneau-Parini I., Jacquier-Sarlin M. R. Differential induction of stress proteins and functional effects of heat shock in human phagocytes. Inflammation. 1995 Jun;19(3):363–378. doi: 10.1007/BF01534393. [DOI] [PubMed] [Google Scholar]
  21. Pryjma J., Baran J., Ernst M., Woloszyn M., Flad H. D. Altered antigen-presenting capacity of human monocytes after phagocytosis of bacteria. Infect Immun. 1994 May;62(5):1961–1967. doi: 10.1128/iai.62.5.1961-1967.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schmid I., Uittenbogaart C. H., Keld B., Giorgi J. V. A rapid method for measuring apoptosis and dual-color immunofluorescence by single laser flow cytometry. J Immunol Methods. 1994 Apr 15;170(2):145–157. doi: 10.1016/0022-1759(94)90390-5. [DOI] [PubMed] [Google Scholar]
  23. Sellins K. S., Cohen J. J. Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes. J Immunol. 1987 Nov 15;139(10):3199–3206. [PubMed] [Google Scholar]
  24. Wyllie A. H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 1980 Apr 10;284(5756):555–556. doi: 10.1038/284555a0. [DOI] [PubMed] [Google Scholar]
  25. Yousefi S., Green D. R., Blaser K., Simon H. U. Protein-tyrosine phosphorylation regulates apoptosis in human eosinophils and neutrophils. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10868–10872. doi: 10.1073/pnas.91.23.10868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zychlinsky A., Prevost M. C., Sansonetti P. J. Shigella flexneri induces apoptosis in infected macrophages. Nature. 1992 Jul 9;358(6382):167–169. doi: 10.1038/358167a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES