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.

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2003-09-01
2019-10-22
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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. Science 285, 736–739.[CrossRef]
    [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 Immunol 153, 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 Biol 147, 683–693.[CrossRef]
    [Google Scholar]
  4. Boise, L. H. & Collins, C. M. ( 2001; ). Salmonella-induced cell death: apoptosis, necrosis or programmed cell death? Trends Microbiol 9, 64–67.[CrossRef]
    [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 Biochem 72, 248–254.[CrossRef]
    [Google Scholar]
  6. Brennan, M. A. & Cookson, B. T. ( 2000; ). Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38, 31–40.[CrossRef]
    [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 J 15, 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 A 95, 4646–4651.[CrossRef]
    [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 Microbiol 40, 76–85.[CrossRef]
    [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 Lett 230, 1–4.[CrossRef]
    [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 Pathol 151, 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 Med 187, 487–496.[CrossRef]
    [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 Immun 65, 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 Immun 68, 3608–3619.[CrossRef]
    [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 Immunol 158, 4320–4327.
    [Google Scholar]
  16. Gao, L. Y. & Abu Kwaik, Y. ( 2000; ). Hijacking of apoptotic pathways by bacterial pathogens. Microb Infect 2, 1705–1719.[CrossRef]
    [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 J 15, 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 A 96, 2396–2401.[CrossRef]
    [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 Chem 273, 32895–32900.[CrossRef]
    [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 Biochem 127, 297–305.[CrossRef]
    [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 Biochem 116, 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 Biol 60, 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 Microbiol 27, 323–336.[CrossRef]
    [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 Med 188, 2091–2097.[CrossRef]
    [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. Science 267, 2000–2003.[CrossRef]
    [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. Nature 371, 346–347.[CrossRef]
    [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. Cell 80, 401–411.[CrossRef]
    [Google Scholar]
  28. Li, P., Allen, H., Banerjee, S. & Seshadri, T. ( 1997; ). Characterization of mice deficient in interleukin-1 beta converting enzyme. J Cell Biochem 64, 27–32.[CrossRef]
    [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 A 98, 9778–9783.[CrossRef]
    [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 Chem 276, 3820–3826.[CrossRef]
    [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 A 93, 9833–9838.[CrossRef]
    [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 Immunol 5, 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 Lett 174, 89–95.[CrossRef]
    [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. Science 285, 1920–1923.[CrossRef]
    [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 Immunol 112, 205–215.[CrossRef]
    [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 Immun 65, 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 Immun 51, 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 Bacteriol 170, 2480–2484.
    [Google Scholar]
  39. Scherrer, R. & Gerhardt, P. ( 1971; ). Molecular sieving by the Bacillus megaterium cell wall and protoplast. J Bacteriol 107, 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 Microbiol 28, 1067–1079.[CrossRef]
    [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 Immunol 161, 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 Chem 272, 17907–17911.[CrossRef]
    [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 Med 185, 281–292.[CrossRef]
    [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 Immun 68, 3744–3747.[CrossRef]
    [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 Immunol 159, 5964–5972.
    [Google Scholar]
  46. Zychlinsky, A., Prevost, M. C. & Sansonetti, P. J. ( 1992; ). Shigella flexneri induces apoptosis in infected macrophages. Nature 358, 167–169.[CrossRef]
    [Google Scholar]
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