Home LiteratureArticle Details
PMID: 12198157 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group.

The EMBO journal ·Vol. 21 ·No. 17 ·2002-09-02 ·Pages 4550-9

Slamti L, Lereclus D

Abstract

PlcR is a pleiotropic regulator that activates the expression of genes encoding various virulence factors, such as phospholipases C, proteases and hemolysins, in Bacillus thuringiensis and Bacillus cereus. Here we show that the activation mechanism is under the control of a small peptide: PapR. The papR gene belongs to the PlcR regulon and is located 70 bp downstream from plcR. It encodes a 48-amino-acid peptide. Disruption of the papR gene abolished expression of the PlcR regulon, resulting in a large decrease in hemolysis and virulence in insect larvae. We demonstrated that the PapR polypeptide was secreted, then reimported via the oligopeptide permease Opp. Once inside the cell, a processed form of PapR, presumably a pentapeptide, activated the PlcR regulon by allowing PlcR to bind to its DNA target. This activating mechanism was found to be strain specific, with this specificity determined by the first residue of the penta peptide.

MeSH Terms
Amino Acid Sequence Bacillus/classification Bacillus cereus/genetics,metabolism,pathogenicity Bacillus thuringiensis/genetics,metabolism,pathogenicity Bacterial Proteins/genetics,metabolism,physiology Gene Deletion Gene Expression Regulation, Bacterial Genes, Bacterial Membrane Transport Proteins/metabolism Molecular Sequence Data Recombinant Fusion Proteins/physiology Regulon/genetics Sequence Alignment Sequence Homology, Amino Acid Species Specificity Trans-Activators/genetics,metabolism Virulence/genetics
Chemicals
Bacterial Proteins Membrane Transport Proteins PapR protein, Bacillus cereus PlcR protein, Bacillus Recombinant Fusion Proteins Trans-Activators oligopeptide permease, Bacteria
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Slamti Leyla
Unité de Biochimie Microbienne, CNRS (URA2172), Institut Pasteur, 25 rue du Docteur Roux, 75724 Paris, France. [email protected]
Lereclus Didier
References (45)
45 references, click to expand
  1. Cell-associated pheromone peptide (cCF10) production and pheromone inhibition in Enterococcus faecalis.
    J Bacteriol. 2000 Sep;182(17):4926-33 PMID: 10940037
  2. Bacillus cereus and related species.
    Clin Microbiol Rev. 1993 Oct;6(4):324-38 PMID: 8269390
  3. Sequence analysis of three Bacillus cereus loci carrying PIcR-regulated genes encoding degradative enzymes and enterotoxin.
    Microbiology. 1999 Nov;145 ( Pt 11):3129-38 PMID: 10589720
  4. The TPR snap helix: a novel protein repeat motif from mitosis to transcription.
    Trends Biochem Sci. 1991 May;16(5):173-7 PMID: 1882418
  5. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  6. Bacillus thuringiensis and its pesticidal crystal proteins.
    Microbiol Mol Biol Rev. 1998 Sep;62(3):775-806 PMID: 9729609
  7. Construction of cloning vectors for Bacillus thuringiensis.
    Gene. 1991 Dec 1;108(1):115-9 PMID: 1662180
  8. Extracellular virulence factors in Bacillus cereus endophthalmitis: methods and implication of involvement of hemolysin BL.
    Infect Immun. 1995 Feb;63(2):632-9 PMID: 7822032
  9. Analysis of cryIAa expression in sigE and sigK mutants of Bacillus thuringiensis.
    Mol Gen Genet. 1996 Apr 10;250(6):734-41 PMID: 8628234
  10. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions.
    Bioessays. 1999 Nov;21(11):932-9 PMID: 10517866
  11. Gene regulation by phosphate in enteric bacteria.
    J Cell Biochem. 1993 Jan;51(1):47-54 PMID: 8432742
  12. Overproduction of encapsulated insecticidal crystal proteins in a Bacillus thuringiensis spo0A mutant.
    Biotechnology (N Y). 1995 Jan;13(1):67-71 PMID: 9634751
  13. Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU.
    J Bacteriol. 1990 Feb;172(2):824-34 PMID: 1688843
  14. Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1549-53 PMID: 8643670
  15. High efficiency transformation of E. coli by high voltage electroporation.
    Nucleic Acids Res. 1988 Jul 11;16(13):6127-45 PMID: 3041370
  16. Nucleotide sequence of the Streptococcus faecalis plasmid gene encoding the 3'5"-aminoglycoside phosphotransferase type III.
    Gene. 1983 Sep;23(3):331-41 PMID: 6313476
  17. An exported peptide functions intracellularly to contribute to cell density signaling in B. subtilis.
    Cell. 1997 Jun 13;89(6):917-25 PMID: 9200610
  18. Pentapeptide regulation of aspartyl-phosphate phosphatases.
    Peptides. 2001 Oct;22(10):1541-7 PMID: 11587783
  19. Bacterial interference caused by autoinducing peptide variants.
    Science. 1997 Jun 27;276(5321):2027-30 PMID: 9197262
  20. Tetratrico peptide repeat interactions: to TPR or not to TPR?
    Trends Biochem Sci. 1995 Jul;20(7):257-9 PMID: 7667876
  21. A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay.
    Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8612-7 PMID: 9238025
  22. Peptides and ATP binding cassette peptide transporters.
    Res Microbiol. 2001 Apr-May;152(3-4):245-58 PMID: 11421272
  23. The incompatibility between the PlcR- and AtxA-controlled regulons may have selected a nonsense mutation in Bacillus anthracis.
    Mol Microbiol. 2001 Dec;42(5):1189-98 PMID: 11886551
  24. Replication control genes of plasmid pE194.
    J Bacteriol. 1987 Oct;169(10):4822-9 PMID: 2443486
  25. Bacillus cereus and its food poisoning toxins.
    FEMS Microbiol Lett. 1997 Dec 15;157(2):223-8 PMID: 9435100
  26. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis.
    Mol Microbiol. 1999 Jun;32(5):1043-53 PMID: 10361306
  27. Generalized transduction in Bacillus thuringiensis var. berliner 1715 using bacteriophage CP-54Ber.
    J Gen Microbiol. 1980 Nov;121(1):203-12 PMID: 7252480
  28. Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis.
    FEMS Microbiol Lett. 1989 Jul 15;51(1):211-7 PMID: 2550317
  29. The ins and outs of peptide signaling.
    Trends Microbiol. 1998 Jul;6(7):288-94 PMID: 9717218
  30. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites.
    Protein Eng. 1997 Jan;10(1):1-6 PMID: 9051728
  31. The plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects.
    Microbiology. 2000 Nov;146 ( Pt 11):2825-32 PMID: 11065361
  32. Structural and functional analysis of the promoter region involved in full expression of the cryIIIA toxin gene of Bacillus thuringiensis.
    Mol Microbiol. 1994 Jul;13(1):97-107 PMID: 7984098
  33. Characterization of an avirulent pleiotropic mutant of the insect pathogen Bacillus thuringiensis: reduced expression of flagellin and phospholipases.
    Infect Immun. 1993 Dec;61(12):4947-54 PMID: 7693592
  34. Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence.
    Mol Microbiol. 2001 May;40(4):963-75 PMID: 11401703
  35. Contribution of Bacillus thuringiensis Spores to Toxicity of Purified Cry Proteins Towards Indianmeal Moth Larvae
    Curr Microbiol. 1996 Jul;33(1):54-9 PMID: 8661690
  36. 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
  37. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria.
    Mol Microbiol. 1999 Jan;31(1):117-31 PMID: 9987115
  38. Fulminating bacteremia and pneumonia due to Bacillus cereus.
    J Clin Microbiol. 1997 Feb;35(2):504-7 PMID: 9003628
  39. Purification and characterization of recombinant human p50csk protein-tyrosine kinase from an Escherichia coli expression system overproducing the bacterial chaperones GroES and GroEL.
    Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1048-52 PMID: 7862631
  40. Construction of new insecticidal Bacillus thuringiensis recombinant strains by using the sporulation non-dependent expression system of cryIIIA and a site specific recombination vector.
    J Biotechnol. 1996 Jul 18;48(1-2):81-96 PMID: 8818275
  41. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  42. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus.
    FEMS Microbiol Lett. 1995 Jun 1;129(1):17-20 PMID: 7781985
  43. Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase.
    J Bacteriol. 1996 May;178(10):2749-56 PMID: 8631661
  44. The intracellular function of extracellular signaling peptides.
    Peptides. 2001 Oct;22(10):1519-27 PMID: 11587781
  45. Regulation of toxin and virulence gene transcription in Bacillus thuringiensis.
    Int J Med Microbiol. 2000 Oct;290(4-5):295-9 PMID: 11111901
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2002-09-02
Pages
4550-9
Language
English
Region
England
NLM ID
8208664
PMCID
PMC126190
Subset
IM
Databases
GENBANK
AF465314, AF465315, AF465316, AF465317, AF465318, AF465319, AF465320, AF465321, AF465322, AF465323, AF465324, AF465325, AF465326, AF465327, AF465328, AF465329
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]