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PMID: 8895564 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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.

The EMBO journal ·Vol. 15 ·No. 19 ·1996-10-01 ·Pages 5191-201

Boland A, Sory MP, Iriarte M, Kerbourch C, Wattiau P, Cornelis GR

Abstract

The Yersinia Yop virulon is an anti-host system made up of four elements: (i) a type III secretion system called Ysc; (ii) a system designed to deliver bacterial proteins into eukaryotic target cells (YopB, YopD); (iii) a control element (YopN); and (iv) a set of intracellularly delivered proteins designed to disarm these cells or disrupt their communications (YopE, YopH and possibly others). YopM, another Yop protein, binds thrombin and is thus presumed to act as an extracellular effector. Here, we analyzed YopM from Y.enterocolitica and we wondered whether it could also be delivered inside eukaryotic cells. To answer this question we applied the Yop-Cya reporter strategy. Hybrids made of 141 or 100 N-terminal residues of YopM fused to Cya were delivered inside PU5-1.8 macrophages by recombinant Y.enterocolitica strains. YopB and YopD were required as translocators. Leakage of the reporters into the macrophage culture supernatant during the bacterial infection increased strongly when YopN was missing, showing that YopN is involved in the control of delivery of YopM inside eukaryotic cells. YopN itself was not delivered into the macrophages. In conclusion, YopM is translocated inside the eukaryotic cells and its physiopathological role should be revised or completed.

MeSH Terms
Adenylate Cyclase Toxin Adenylyl Cyclases Bacterial Outer Membrane Proteins/genetics,metabolism,physiology Bacterial Proteins/genetics,metabolism Biological Transport Cytosol/metabolism Genes, Bacterial/genetics Genes, Reporter/genetics HeLa Cells/microbiology Humans Macrophages/metabolism,microbiology Membrane Proteins Molecular Sequence Data Mutation Protein Precursors/genetics Recombinant Fusion Proteins Regulon/genetics Yersinia enterocolitica/metabolism,pathogenicity
Chemicals
Adenylate Cyclase Toxin Bacterial Outer Membrane Proteins Bacterial Proteins Membrane Proteins Protein Precursors Recombinant Fusion Proteins YopB protein, Yersinia YopD protein, Yersinia yopM protein, Yersinia YopN protein, Yersinia Adenylyl Cyclases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Boland A
Microbial Pathogenesis Unit, International Institute of Cellular and Molecular Pathology and Faculté de Médecine, Université Catholique de Louvain, Brussels, Belgium.
Sory M P
Iriarte M
Kerbourch C
Wattiau P
Cornelis G R
References (54)
54 references, click to expand
  1. Restriction of DNA in Yersinia enterocolitica detected by recipient ability for a derepressed R factor from Escherichia coli.
    J Gen Microbiol. 1975 Apr;87(2):285-91 PMID: 1095683
  2. High-affinity alpha-thrombin binding to platelet glycoprotein Ib alpha: identification of two binding domains.
    Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6334-8 PMID: 8022782
  3. Improved tools for biological sequence comparison.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444-8 PMID: 3162770
  4. 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
  5. Homology between virF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator.
    J Bacteriol. 1989 Jan;171(1):254-62 PMID: 2644192
  6. 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
  7. Identification of additional virulence determinants on the pYV plasmid of Yersinia enterocolitica W227.
    Infect Immun. 1989 Aug;57(8):2534-41 PMID: 2545628
  8. Sequence and molecular characterization of a multicopy invasion plasmid antigen gene, ipaH, of Shigella flexneri.
    J Bacteriol. 1990 Apr;172(4):1905-15 PMID: 1690703
  9. The lcrE gene is part of an operon in the lcr region of Yersinia enterocolitica O:3.
    J Bacteriol. 1990 Jun;172(6):3152-62 PMID: 2160939
  10. Oral immunization of mice with a live recombinant Yersinia enterocolitica O:9 strain that produces the cholera toxin B subunit.
    Infect Immun. 1990 Aug;58(8):2420-8 PMID: 2370100
  11. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia.
    Science. 1990 Aug 3;249(4968):553-6 PMID: 2166336
  12. Secretion of Yop proteins by Yersiniae.
    Infect Immun. 1990 Sep;58(9):2840-9 PMID: 2129533
  13. YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice.
    Infect Immun. 1990 Oct;58(10):3262-71 PMID: 2401564
  14. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  15. Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant.
    Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1187-91 PMID: 1705028
  16. Analysis of the V antigen lcrGVH-yopBD operon of Yersinia pseudotuberculosis: evidence for a regulatory role of LcrH and LcrV.
    J Bacteriol. 1991 Mar;173(5):1607-16 PMID: 1705541
  17. Secretion of hybrid proteins by the Yersinia Yop export system.
    J Bacteriol. 1991 Mar;173(5):1677-85 PMID: 1999387
  18. The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis.
    Mol Microbiol. 1991 Apr;5(4):977-86 PMID: 1857212
  19. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption.
    Infect Immun. 1991 Dec;59(12):4562-9 PMID: 1937815
  20. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica.
    Gene. 1991 Dec 20;109(1):137-41 PMID: 1756974
  21. YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion.
    J Bacteriol. 1994 Aug;176(15):4534-42 PMID: 8045883
  22. Essential role of YopD in inhibition of the respiratory burst of macrophages by Yersinia enterocolitica.
    Infect Immun. 1994 Oct;62(10):4445-53 PMID: 7927708
  23. Individual chaperones required for Yop secretion by Yersinia.
    Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10493-7 PMID: 7937981
  24. The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD.
    EMBO J. 1994 Nov 15;13(22):5293-302 PMID: 7957095
  25. 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
  26. Yersinia pathogenicity factors.
    Curr Top Microbiol Immunol. 1994;192:243-63 PMID: 7859508
  27. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells.
    Mol Microbiol. 1994 Nov;14(3):583-94 PMID: 7885236
  28. Differential effects of deletions in lcrV on secretion of V antigen, regulation of the low-Ca2+ response, and virulence of Yersinia pestis.
    J Bacteriol. 1995 May;177(9):2530-42 PMID: 7730287
  29. Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells.
    Infect Immun. 1995 Aug;63(8):3117-24 PMID: 7622239
  30. Environmental modulation of gene expression and pathogenesis in Yersinia.
    Trends Microbiol. 1995 Aug;3(8):310-7 PMID: 8528615
  31. The chaperone-like protein YerA of Yersinia pseudotuberculosis stabilizes YopE in the cytoplasm but is dispensible for targeting to the secretion loci.
    Mol Microbiol. 1995 May;16(4):635-47 PMID: 7476159
  32. 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
  33. Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell.
    Mol Microbiol. 1995 Oct;18(1):135-50 PMID: 8596454
  34. Differential secretion of interleukin-8 by human epithelial cell lines upon entry of virulent or nonvirulent Yersinia enterocolitica.
    Infect Immun. 1996 Jun;64(6):2106-13 PMID: 8675314
  35. Mutational analysis of the Yersinia enterocolitica virC operon: characterization of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR.
    Mol Microbiol. 1995 Oct;18(2):343-55 PMID: 8709853
  36. Customized secretion chaperones in pathogenic bacteria.
    Mol Microbiol. 1996 Apr;20(2):255-62 PMID: 8733225
  37. The cytosolic SycE and SycH chaperones of Yersinia protect the region of YopE and YopH involved in translocation across eukaryotic cell membranes.
    Mol Microbiol. 1996 Jun;20(6):1261-71 PMID: 8809777
  38. A novel protein, LcrQ, involved in the low-calcium response of Yersinia pseudotuberculosis shows extensive homology to YopH.
    J Bacteriol. 1992 May;174(10):3355-63 PMID: 1577700
  39. Expression of the eukaryotic Trypanosoma cruzi CRA gene in Yersinia enterocolitica and induction of an immune response against CRA in mice.
    Infect Immun. 1992 Sep;60(9):3830-6 PMID: 1500192
  40. Yersinia pestis YopM: thrombin binding and overexpression.
    Infect Immun. 1992 Dec;60(12):5242-52 PMID: 1452357
  41. The Yersinia tyrosine phosphatase: specificity of a bacterial virulence determinant for phosphoproteins in the J774A.1 macrophage.
    J Exp Med. 1992 Dec 1;176(6):1625-30 PMID: 1281213
  42. YopB and YopD constitute a novel class of Yersinia Yop proteins.
    Infect Immun. 1993 Jan;61(1):71-80 PMID: 8418066
  43. A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant.
    Nature. 1993 Feb 25;361(6414):730-2 PMID: 8441468
  44. Identification of protein coding regions by database similarity search.
    Nat Genet. 1993 Mar;3(3):266-72 PMID: 8485583
  45. SycE, a chaperone-like protein of Yersinia enterocolitica involved in Ohe secretion of YopE.
    Mol Microbiol. 1993 Apr;8(1):123-31 PMID: 8497188
  46. Multiple effects of lcrD mutations in Yersinia pestis.
    J Bacteriol. 1993 Jun;175(11):3536-45 PMID: 8501057
  47. A low-Ca2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis.
    J Bacteriol. 1994 Feb;176(3):569-79 PMID: 8300512
  48. 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
  49. Localization and characterization of an alpha-thrombin-binding site on platelet glycoprotein Ib alpha.
    J Biol Chem. 1994 Mar 4;269(9):6478-84 PMID: 8119999
  50. YscN, the putative energizer of the Yersinia Yop secretion machinery.
    J Bacteriol. 1994 Mar;176(6):1561-9 PMID: 8132449
  51. Calmodulin-activated bacterial adenylate cyclases as virulence factors.
    Trends Microbiol. 1993 Aug;1(5):187-92 PMID: 8143137
  52. Regulation and polarized transfer of the Yersinia outer proteins (Yops) involved in antiphagocytosis.
    Trends Microbiol. 1994 Jan;2(1):14-9 PMID: 8162430
  53. The lcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium.
    J Bacteriol. 1994 May;176(9):2619-26 PMID: 8169210
  54. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1996-10-01
Pages
5191-201
Language
English
Region
England
NLM ID
8208664
PMCID
PMC452263
Subset
IM
Databases
GENBANK
Z69926
External Links
PubMed source PMC Full Text View journal details
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