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PMID: 9393811 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The interleukin 1beta-converting enzyme, caspase 1, is activated during Shigella flexneri-induced apoptosis in human monocyte-derived macrophages.

Infection and immunity ·Vol. 65 ·No. 12 ·1997-12-00 ·Pages 5165-70

Hilbi H, Chen Y, Thirumalai K, Zychlinsky A

Abstract

Shigella, the etiological agent of bacillary dysentery, rapidly kills human monocyte-derived macrophages in vitro. Wild-type Shigella flexneri, but not a nonvirulent derivative, induced human macrophage apoptosis as determined by morphology and terminal deoxynucleotidyltransferase-mediated dUTP-biotin nick end labeling (TUNEL). Shigella-mediated macrophage cell death was blocked by the peptide inhibitors of caspases, acetyl-Tyr-Val-Ala-Asp-aldehyde (acetyl-YVAD-CHO) and acetyl-Tyr-Val-Ala-Asp-chloromethylketone (acetyl-YVAD-CMK). Protection from apoptosis by YVAD was observed in monocytes matured in the presence or absence of colony-stimulating factors (CSF) like macrophage-CSF or granulocyte-macrophage-CSF. Furthermore, lipopolysaccharide (LPS) or gamma interferon (IFN-gamma) rendered human macrophages partially resistant to Shigella cytotoxicity. Macrophages stimulated with either LPS or IFN-gamma were also protected by YVAD from Shigella-induced cell death. During Shigella infections of human macrophages, interleukin-1beta (IL-1beta) was cleaved to the mature form. IL-1beta maturation was severely retarded by YVAD, indicating that IL-1beta-converting enzyme (ICE; caspase 1) is activated in Shigella-induced apoptosis. The finding that Shigella induces apoptosis in human macrophages by activating ICE supports the hypothesis that the acute inflammation characteristic of shigellosis is initially triggered by apoptotic macrophages which release mature IL-1beta during programmed cell death.

MeSH Terms
Apoptosis Caspase 1 Cells, Cultured Cysteine Endopeptidases/metabolism Dysentery, Bacillary/enzymology,pathology Humans Interleukin-1/metabolism Macrophages/enzymology,microbiology,pathology Monocytes Shigella flexneri
Chemicals
Interleukin-1 Cysteine Endopeptidases Caspase 1
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Hilbi H
The Skirball Institute, Department of Microbiology, New York University School of Medicine, New York 10016, USA.
Chen Y
Thirumalai K
Zychlinsky A
References (30)
30 references, click to expand
  1. Human monocyte-derived macrophages infected with virulent Shigella flexneri in vitro undergo a rapid cytolytic event similar to oncosis but not apoptosis.
    Infect Immun. 1997 Apr;65(4):1486-96 PMID: 9119491
  2. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells.
    J Bacteriol. 1993 Sep;175(18):5899-906 PMID: 8376337
  3. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme.
    Science. 1997 Jan 10;275(5297):206-9 PMID: 8999548
  4. In situ characterization of inflammatory responses in the rectal mucosae of patients with shigellosis.
    Infect Immun. 1997 Feb;65(2):739-49 PMID: 9009337
  5. Involvement of a plasmid in the invasive ability of Shigella flexneri.
    Infect Immun. 1982 Mar;35(3):852-60 PMID: 6279518
  6. An ICE-like protease is a common mediator of apoptosis induced by diverse stimuli in human monocytic THP.1 cells.
    FEBS Lett. 1995 Oct 30;374(2):303-8 PMID: 7589559
  7. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis.
    Infect Immun. 1989 Mar;57(3):858-63 PMID: 2645214
  8. Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production.
    Nature. 1997 Apr 10;386(6625):619-23 PMID: 9121587
  9. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis.
    J Exp Med. 1994 Oct 1;180(4):1307-19 PMID: 7931064
  10. Rapid killing of actinomycin D-treated tumor cells by human mononuclear cells. I. Effectors belong to the monocyte-macrophage lineage.
    J Immunol. 1984 Feb;132(2):936-44 PMID: 6690624
  11. ICE/CED-3 proteasesin apoptosis.
    Trends Cell Biol. 1996 Jul;6(7):245-8 PMID: 15157443
  12. Bacterial entry into epithelial cells: the paradigm of Shigella.
    Trends Microbiol. 1996 Jun;4(6):220-6 PMID: 8795157
  13. Human ICE/CED-3 protease nomenclature.
    Cell. 1996 Oct 18;87(2):171 PMID: 8861900
  14. Activation-induced apoptosis in human macrophages: developmental regulation of a novel cell death pathway by macrophage colony-stimulating factor and interferon gamma.
    J Exp Med. 1995 Jan 1;181(1):127-36 PMID: 7806999
  15. Clinical isolates of Shigella species induce apoptosis in macrophages.
    J Infect Dis. 1997 Feb;175(2):470-3 PMID: 9203676
  16. Morphology of rectal mucosa of patients with shigellosis.
    Rev Infect Dis. 1991 Mar-Apr;13 Suppl 4:S314-8 PMID: 2047656
  17. Shigella sonnei plasmids: evidence that a large plasmid is necessary for virulence.
    Infect Immun. 1981 Oct;34(1):75-83 PMID: 6271687
  18. Role of interleukin-1 in the pathogenesis of experimental shigellosis.
    J Clin Invest. 1995 Aug;96(2):884-92 PMID: 7635983
  19. In vivo apoptosis in Shigella flexneri infections.
    Infect Immun. 1996 Dec;64(12):5357-65 PMID: 8945588
  20. IpaB mediates macrophage apoptosis induced by Shigella flexneri.
    Mol Microbiol. 1994 Feb;11(4):619-27 PMID: 8196540
  21. Plasmid-mediated early killing of eucaryotic cells by Shigella flexneri as studied by infection of J774 macrophages.
    Infect Immun. 1987 Mar;55(3):521-7 PMID: 3546130
  22. Apoptosis in human monocytes: possible role in chronic inflammatory diseases.
    J Periodontol. 1993 May;64(5 Suppl):461-6 PMID: 8315569
  23. Shigella flexneri induces apoptosis in infected macrophages.
    Nature. 1992 Jul 9;358(6382):167-9 PMID: 1614548
  24. A bacterial invasin induces macrophage apoptosis by binding directly to ICE.
    EMBO J. 1996 Aug 1;15(15):3853-60 PMID: 8670890
  25. Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri.
    J Clin Invest. 1994 Sep;94(3):1328-32 PMID: 8083373
  26. IpaB, a Shigella flexneri invasin, colocalizes with interleukin-1 beta-converting enzyme in the cytoplasm of macrophages.
    Infect Immun. 1997 Feb;65(2):787-93 PMID: 9009343
  27. Apoptosis as a proinflammatory event: what can we learn from bacteria-induced cell death?
    Trends Microbiol. 1997 May;5(5):201-4 PMID: 9160509
  28. Shigella flexneri is trapped in polymorphonuclear leukocyte vacuoles and efficiently killed.
    Infect Immun. 1997 Jan;65(1):110-5 PMID: 8975899
  29. 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):1541-6 PMID: 1993844
  30. Differential regulation of human monocyte programmed cell death (apoptosis) by chemotactic factors and pro-inflammatory cytokines.
    J Immunol. 1991 Nov 15;147(10):3408-12 PMID: 1940344
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1997-12-00
Pages
5165-70
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC175744
Subset
IM
Grants
NIAID NIH HHS · AI37720 · United States
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