1887

Abstract

It is currently unclear whether kills its phagocytic host cells by apoptosis or necrosis. This study shows that rapid necrosis ensues in macrophage-like cell lines (U937 cells differentiated by all--retinoic acid and J774 cells) infected with the strain YSH6000. The infected cells rapidly lose membrane integrity, a typical feature of necrosis, as indicated by the release of the cytoplasmic lactate dehydrogenase and the exposure of phosphatidylserine (PS) associated with the rapid uptake of propidium iodide (PI). The infected cells exhibit DNA fragmentation without nuclear condensation, and substantial involvement of either caspase-3/-7 or caspase-1 was not detected, which is also contrary to what is normally observed in apoptosis. Cytochalasin D potently inhibited -induced cell death, indicating that only internalized can cause necrosis. Osmoprotectants such as polyethylene glycols could suppress cell death, suggesting that insertion of a pore by into the host cell membrane induces the necrosis. The pore was estimated to be 2·87±0·4 nm in diameter. was also found to be able to induce apoptosis but only in one of the lines tested and under specific conditions, namely U937 cells differentiated with interferon- (U937IFN). Caspase-3/-7 but not caspase-1 activation was observed in these infected cells and the exposure of PS occurred without the uptake of PI. An avirulent strain, wild-type killed with gentamicin, and even strain JM109, could also induce apoptosis in U937IFN cells, and cytochalasin D could not prevent apoptosis. It appears therefore that -induced apoptosis of U937IFN cells is unrelated to pathogenicity and does not require bacterial internalization. Thus, can induce rapid necrosis of macrophage-like cells in a virulence-related manner by forming pores in the host cell membrane while some cells can be killed through apoptosis in a virulence-independent fashion.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26341-0
2003-09-01
2020-03-30
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/9/mic1492513.html?itemId=/content/journal/micro/10.1099/mic.0.26341-0&mimeType=html&fmt=ahah

References

  1. Aliprantis A. O., Yang R. B., Mark M. R., Suggett S., Devaux B., Radolf J. D., Kimpel G. R., Godowski P., Zychlinsky A.. 1999; Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science285:736–739
    [Google Scholar]
  2. Ayala J. M., Yamin T. T., Egger L. A., Chin J., Kostura M. J., Miller D. K.. 1994; IL-1 beta-converting enzyme is present in monocytic cells as an inactive 45-kDa precursor. J Immunol153:2592–2597
    [Google Scholar]
  3. Blocker A., Gounon P., Larquet E., Niebuhr K., Cabiaux V., Parsot C., Sansonetti P.. 1999; The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol147:683–693
    [Google Scholar]
  4. Boise L. H., Collins C. M.. 2001; Salmonella -induced cell death: apoptosis, necrosis or programmed cell death?. Trends Microbiol9:64–67
    [Google Scholar]
  5. Bradford M. M.. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72:248–254
    [Google Scholar]
  6. Brennan M. A., Cookson B. T.. 2000; Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol38:31–40
    [Google Scholar]
  7. Chen Y., Smith M. R., Thirumalai K., Zychlinsky A.. 1996; A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J15:3853–3860
    [Google Scholar]
  8. Clifton D. R., Goss R. A., Sahni S. K., Antwerp D. V., Baggs R. B., Marder V. J., Silverman D. J., Sporn L. A.. 1998; NF-kappa B-dependent inhibition of apoptosis is essential for host cell survival during Rickettsia rickettsii infection. Proc Natl Acad Sci U S A95:4646–4651
    [Google Scholar]
  9. Dacheux D., Goure J., Cabert J., Usson Y., Attree I.. 2001; Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa -infected macrophages. Mol Microbiol40:76–85
    [Google Scholar]
  10. de Torres C., Munell F., Ferrer I., Reventos J., Macaya A.. 1997; Identification of necrotic cell death by the TUNEL assay in the hypoxic-ischemic neonatal rat brain. Neurosci Lett230:1–4
    [Google Scholar]
  11. Dong Z., Saikumar P., Weinberg J. M., Venkatachalam M. A.. 1997; Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am J Pathol151:1205–1213
    [Google Scholar]
  12. Fan T., Lu H., Hu H., Shi L., McClarty G. A., Nance D. M., Greenberg A. H., Zhong G.. 1998; Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med187:487–496
    [Google Scholar]
  13. Fernandez-Prada C. M., Hoover D. L., Tall B. D., Venkatesan M. M.. 1997; Human monocyte-derived macrophages infected with virulent Shigella flexneri in vitro undergo a rapid cytolytic event similar to oncosis but not apoptosis. Infect Immun65:1486–1496
    [Google Scholar]
  14. Fernandez-Prada C. M., Hoover D. L., Tall B. D., Hartman A. B., Kopelowitz J., Venkatesan M. M.. 2000; Shigella flexneri IpaH7·8 facilitates escape of virulent bacteria from the endocytic vacuoles of mouse and human macrophages. Infect Immun68:3608–3619
    [Google Scholar]
  15. Fratazzi C., Arbeit R. D., Carini C., Remold H. G.. 1997; Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J Immunol158:4320–4327
    [Google Scholar]
  16. Gao L. Y., Abu Kwaik Y.. 2000; Hijacking of apoptotic pathways by bacterial pathogens. Microb Infect2:1705–1719
    [Google Scholar]
  17. Hakansson S., Schesser K., Persson C., Galyov E. E., Rosqvist R., Homble F., Wolf-Watz H.. 1996; The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J15:5812–5823
    [Google Scholar]
  18. Hersh D., Monack D. M., Smith M. R., Ghori N., Falkow S., Zychlinsky A.. 1999; The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A96:2396–2401
    [Google Scholar]
  19. Hilbi H., Moss J. E., Hersh D.. 7 other authors 1998; Shigella -induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem273:32895–32900
    [Google Scholar]
  20. Kato M., Nonaka T., Maki M., Kikuchi H., Imajoh-Ohmi S.. 2000; Caspases cleave the amino-terminal calpain inhibitory unit of calpastatin during apoptosis in human Jurkat T cells. J Biochem127:297–305
    [Google Scholar]
  21. Kikuchi H., Fujinawa T., Kuribayashi F., Nakanishi A., Imajoh-Ohmi S., Kanegasaki S.. 1994; Induction of essential components of the superoxide generating system in human monoblastic leukemia U937 cells. J Biochem116:742–746
    [Google Scholar]
  22. Kikuchi H., Iizuka R., Sugiyama S., Gon G., Mori H., Arai M., Mizumoto K., Imajoh-Ohmi S.. 1996; Monocytic differentiation modulates apoptotic response to cytotoxic anti-Fas antibody and tumor necrosis factor alpha in human monoblast U937 cells. J Leukoc Biol60:778–783
    [Google Scholar]
  23. Kirby J. E., Vogel J. P., Andrews H. L., Isberg R. R.. 1998; Evidence for pore-forming ability by Legionella pneumophila . Mol Microbiol27:323–336
    [Google Scholar]
  24. Kirschning C. J., Wesche H., Ayres T. M., Rothe M.. 1998; Human Toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J Exp Med188:2091–2097
    [Google Scholar]
  25. Kuida K., Lippke J. A., Ku G., Harding M. W., Livingston D. J., Su M. S., Flavell R. A.. 1995; Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science267:2000–2003
    [Google Scholar]
  26. Lazebnik Y. A., Kaufmann S. H., Desnoyers S., Poirier G. G., Earnshaw W. C.. 1994; Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature371:346–347
    [Google Scholar]
  27. Li P., Allen H., Banerjee S.. 7 other authors 1995; Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell80:401–411
    [Google Scholar]
  28. Li P., Allen H., Banerjee S., Seshadri T.. 1997; Characterization of mice deficient in interleukin-1 beta converting enzyme. J Cell Biochem64:27–32
    [Google Scholar]
  29. Ma F., Zhang C., Prasad K. V., Freeman G. J., Schlossman S. F.. 2001; Molecular cloning of Porimin, a novel cell surface receptor mediating oncotic cell death. Proc Natl Acad Sci U S A98:9778–9783
    [Google Scholar]
  30. Mehta V. B., Hart J., Wewers M. D.. 2001; ATP-stimulated release of interleukin (IL)-1b and IL-18 requires priming by lipopolysaccharide and is independent of caspase-1 cleavage. J Biol Chem276:3820–3826
    [Google Scholar]
  31. Monack D. M., Raupach B., Hromocky A. E., Falkow S.. 1996; Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci U S A93:9833–9838
    [Google Scholar]
  32. Moran O., Zegarra-Moran O., Virginio C., Gusmani L., Rottini G. D.. 1992; Physical characterization of the pore forming cytolysine from Gardnerella vaginalis . FEMS Microbiol Immunol5:63–69
    [Google Scholar]
  33. Nonaka T., Kuwae A., Sasakawa C., Imajoh-Ohmi S.. 1999; Shigella flexneri YSH6000 induces two types of cell death, apoptosis and oncosis, in the differentiated human monoblastic cell line U937. FEMS Microbiol Lett174:89–95
    [Google Scholar]
  34. Orth K., Palmer L. E., Bao Z. Q., Stewart S., Rudolph A. E., Bliska J. B., Dixon J. E.. 1999; Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science285:1920–1923
    [Google Scholar]
  35. Rogler G., Hausmann M., Vogl D., Aschenbrenner E., Andus T., Falk W., Andreesen R., Scholmerich J., Gross V.. 1998; Isolation and phenotypic characterization of colonic macrophages. Clin Exp Immunol112:205–215
    [Google Scholar]
  36. Ruckdeschel K., Roggenkamp A., Lafont V., Mangeat P., Hessemann J., Rouot B.. 1997; Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect Immun65:4813–4821
    [Google Scholar]
  37. Sasakawa C., Kamata K., Sakai T., Murayama S. Y., Makino S., Yoshikawa M.. 1986; Molecular alteration of the 140-megadalton plasmid associated with loss of virulence and Congo red binding activity in Shigella flexneri . Infect Immun51:470–475
    [Google Scholar]
  38. Sasakawa C., Kamata K., Sakai T., Makino S., Yamada M., Okada N., Yoshikawa M.. 1988; Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J Bacteriol170:2480–2484
    [Google Scholar]
  39. Scherrer R., Gerhardt P.. 1971; Molecular sieving by the Bacillus megaterium cell wall and protoplast. J Bacteriol107:718–735
    [Google Scholar]
  40. Schesser K., Spiik A. K., Dukuzumuremyi J. M., Neurath M. F., Pettersson S., Wolf-Watz H.. 1998; The yopJ locus is required for Yersinia -mediated inhibition of NF-kappaB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol Microbiol28:1067–1079
    [Google Scholar]
  41. Schonbeck U., Mach F., Libby P.. 1998; Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol161:3340–3346
    [Google Scholar]
  42. Thornberry N. A., Rano T. A., Peterson E. P.. 9 other authors 1997; A combinatorial approach defines specificities of members of the caspase family and granzyme B. J Biol Chem272:17907–17911
    [Google Scholar]
  43. Watarai M., Kamata Y., Kozaki S., Sasakawa C.. 1997; rho, a small GTP-binding protein, is essential for Shigella invasion of epithelial cells. J Exp Med185:281–292
    [Google Scholar]
  44. Watson P. R., Gautier A. V., Paulin S. M., Bland A. P., Jones P. W., Wallis T. S.. 2000; Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis. Infect Immun68:3744–3747
    [Google Scholar]
  45. Wewers M. D., Dare H. A., Winnard A. V., Parker J. M., Miller D. K.. 1997; IL-1 beta-converting enzyme (ICE) is present and functional in human alveolar macrophages: macrophage IL-1 beta release limitation is ICE independent. J Immunol159:5964–5972
    [Google Scholar]
  46. Zychlinsky A., Prevost M. C., Sansonetti P. J.. 1992; Shigella flexneri induces apoptosis in infected macrophages. Nature358:167–169
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26341-0
Loading
/content/journal/micro/10.1099/mic.0.26341-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error