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PMID: 9356502 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein.

Mills SD, Boland A, Sory MP, van der Smissen P, Kerbourch C, Finlay BB, Cornelis GR

Abstract

Yersiniae, causative agents of plague and gastrointestinal diseases, secrete and translocate Yop effector proteins into the cytosol of macrophages, leading to disruption of host defense mechanisms. It is shown in this report that Yersinia enterocolitica induces apoptosis in macrophages and that this effect depends on YopP. Functional secretion and translocation mechanisms are required for YopP to act, strongly suggesting that this protein exerts its effect intracellularly, after translocation into the macrophages. YopP shows a high level of sequence similarity with AvrRxv, an avirulence protein from Xanthomonas campestris, a plant pathogen that induces programmed cell death in plant cells. This indicates possible similarities between the strategies used by pathogenic bacteria to elicit programmed cell death in both plant and animal hosts.

MeSH Terms
Amino Acid Sequence Animals Apoptosis Bacterial Proteins/genetics,metabolism Cell Line Macrophages/microbiology,pathology Mice Molecular Sequence Data Yersinia Infections/metabolism,pathology Yersinia enterocolitica
Chemicals
Bacterial Proteins YopP protein, Yersinia
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Mills S D
Biotechnology Laboratory, University of British Columbia, Vancouver, British Columbia V6T 1Z3 Canada.
Boland A
Sory M P
van der Smissen P
Kerbourch C
Finlay B B
Cornelis G R
References (37)
37 references, click to expand
  1. Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis.
    J Bacteriol. 1994 Aug;176(15):4543-8 PMID: 8045884
  2. Cocaine induces apoptosis in cortical neurons of fetal mice.
    J Neurochem. 1997 Jun;68(6):2442-50 PMID: 9166738
  3. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells.
    Mol Microbiol. 1994 Nov;14(3):583-94 PMID: 7885236
  4. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12.
    Nature. 1985 Sep 19-25;317(6034):262-4 PMID: 2995819
  5. Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase.
    Infect Immun. 1995 Feb;63(2):681-5 PMID: 7822039
  6. Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells?
    Trends Microbiol. 1997 Apr;5(4):148-56 PMID: 9141189
  7. Exploitation of mammalian host cell functions by bacterial pathogens.
    Science. 1997 May 2;276(5313):718-25 PMID: 9115192
  8. YscN, the putative energizer of the Yersinia Yop secretion machinery.
    J Bacteriol. 1994 Mar;176(6):1561-9 PMID: 8132449
  9. Customized secretion chaperones in pathogenic bacteria.
    Mol Microbiol. 1996 Apr;20(2):255-62 PMID: 8733225
  10. Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y.enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus.
    EMBO J. 1996 Oct 1;15(19):5191-201 PMID: 8895564
  11. Sacrifice in the face of foes: pathogen-induced programmed cell death in plants.
    Trends Microbiol. 1996 Jan;4(1):10-15 PMID: 8824789
  12. Identification of dying cells--in situ staining.
    Methods Cell Biol. 1995;46:29-39 PMID: 7541886
  13. Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization.
    J Exp Med. 1997 Mar 3;185(5):855-66 PMID: 9120391
  14. Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein.
    Infect Immun. 1988 Aug;56(8):2139-43 PMID: 3294185
  15. YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis.
    Mol Microbiol. 1996 Jun;20(5):1057-69 PMID: 8809758
  16. Anatomical methods in cell death.
    Methods Cell Biol. 1995;46:1-27 PMID: 7609651
  17. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):11998-2002 PMID: 8618831
  18. Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes.
    Microb Pathog. 1987 May;2(5):367-79 PMID: 3507556
  19. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  20. Salmonella typhimurium invasion induces apoptosis in infected macrophages.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9833-8 PMID: 8790417
  21. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell.
    Cell. 1996 Dec 27;87(7):1307-16 PMID: 8980236
  22. The cytotoxic protein YopE of Yersinia obstructs the primary host defence.
    Mol Microbiol. 1990 Apr;4(4):657-67 PMID: 2191183
  23. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  24. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption.
    Infect Immun. 1991 Dec;59(12):4562-9 PMID: 1937815
  25. Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato
    Science. 1996 Dec 20;274(5295):2063-5 PMID: 8953034
  26. Shigella flexneri induces apoptosis in infected macrophages.
    Nature. 1992 Jul 9;358(6382):167-9 PMID: 1614548
  27. A bacterial invasin induces macrophage apoptosis by binding directly to ICE.
    EMBO J. 1996 Aug 1;15(15):3853-60 PMID: 8670890
  28. Salmonella spp. are cytotoxic for cultured macrophages.
    Mol Microbiol. 1996 Sep;21(5):1101-15 PMID: 8885278
  29. Direct repeat sequences in the cagA gene of Helicobacter pylori: a ghost of a chance encounter?
    Mol Microbiol. 1997 Jan;23(2):409-10 PMID: 9044274
  30. Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998.
    Mol Plant Microbe Interact. 1993 Sep-Oct;6(5):616-27 PMID: 8274773
  31. 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. 1996 Nov 1;15(21):5812-23 PMID: 8918459
  32. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  33. The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane.
    Mol Microbiol. 1996 May;20(3):593-603 PMID: 8736538
  34. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells.
    EMBO J. 1994 Feb 15;13(4):964-72 PMID: 8112310
  35. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase
    Science. 1996 Dec 20;274(5295):2060-3 PMID: 8953033
  36. SycE, a chaperone-like protein of Yersinia enterocolitica involved in Ohe secretion of YopE.
    Mol Microbiol. 1993 Apr;8(1):123-31 PMID: 8497188
  37. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells.
    Mol Microbiol. 1997 Mar;23(5):861-7 PMID: 9076724
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-11-11
Pages
12638-43
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC25065
Subset
IM
Databases
GENBANK
AF023202
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