Home LiteratureArticle Details
PMID: 12897002 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The virulence activator AphA links quorum sensing to pathogenesis and physiology in Vibrio cholerae by repressing the expression of a penicillin amidase gene on the small chromosome.

Journal of bacteriology ·Vol. 185 ·No. 16 ·2003-08-00 ·Pages 4825-36

Kovacikova G, Lin W, Skorupski K

Abstract

Activation of the tcpPH promoter on the Vibrio pathogenicity island by AphA and AphB initiates the Vibrio cholerae virulence cascade and is regulated by quorum sensing through the repressive action of HapR on aphA expression. To further understand how the chromosomally encoded AphA protein activates tcpPH expression, site-directed mutagenesis was used to identify the base pairs critical for AphA binding and transcriptional activation. This analysis revealed a region of partial dyad symmetry, TATGCA-N6-TNCNNA, that is important for both of these activities. Searching the V. cholerae genome for this binding site permitted the identification of a second one upstream of a penicillin V amidase (PVA) gene on the small chromosome. AphA binds to and footprints this site, which overlaps the pva transcriptional start, consistent with its role as a repressor at this promoter. Since aphA expression is under quorum-sensing control, the response regulators LuxO and HapR also influence pva expression. Thus, pva is repressed at low cell density when AphA levels are high, and it is derepressed at high cell density when AphA levels are reduced. Penicillin amidases are thought to function as scavengers for phenylacetylated compounds in the nonparasitic environment. That AphA oppositely regulates the expression of pva from that of virulence, together with the observation that PVA does not play a role in virulence, suggests that these activities are coordinated to serve V. cholerae in different biological niches.

MeSH Terms
Aminohydrolases/genetics,metabolism Bacterial Proteins/genetics,metabolism Base Sequence Binding Sites Chromosomes, Bacterial Fimbriae Proteins/genetics,metabolism Gene Expression Regulation, Bacterial Molecular Sequence Data Mutagenesis, Site-Directed Penicillin Amidase/genetics,metabolism Promoter Regions, Genetic Transcription Factors/genetics,metabolism Vibrio cholerae/enzymology,genetics,growth & development,pathogenicity Virulence
Chemicals
Bacterial Proteins TCPP protein, Vibrio cholerae TcpH protein, Vibrio cholerae Transcription Factors Fimbriae Proteins acetylpolyamine amidohydrolase Penicillin Amidase Aminohydrolases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kovacikova Gabriela
Department of Microbiology and Immunology, Dartmouth Medical School, Hanover, New Hampshire 03755, USA.
Lin Wei
Skorupski Karen
References (44)
44 references, click to expand
  1. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998-9002 PMID: 2461560
  2. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR.
    J Bacteriol. 1988 Jun;170(6):2575-83 PMID: 2836362
  3. Regulatory cascade controls virulence in Vibrio cholerae.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5403-7 PMID: 2052618
  4. The role of penicillin amidases in nature and in industry.
    Trends Biochem Sci. 1991 Jan;16(1):36-40 PMID: 2053136
  5. Carbon regulation and the role in nature of the Escherichia coli penicillin acylase (pac) gene.
    Mol Microbiol. 1992 Aug;6(15):2175-82 PMID: 1406257
  6. Cloning and expression of a conjugated bile acid hydrolase gene from Lactobacillus plantarum by using a direct plate assay.
    Appl Environ Microbiol. 1992 Dec;58(12):3792-8 PMID: 1476424
  7. Cholera.
    Clin Microbiol Rev. 1995 Jan;8(1):48-86 PMID: 7704895
  8. Cloning and characterization of a conjugated bile acid hydrolase gene from Clostridium perfringens.
    Appl Environ Microbiol. 1995 Jul;61(7):2514-20 PMID: 7618863
  9. Positive selection vectors for allelic exchange.
    Gene. 1996 Feb 22;169(1):47-52 PMID: 8635748
  10. Lysogenic conversion by a filamentous phage encoding cholera toxin.
    Science. 1996 Jun 28;272(5270):1910-4 PMID: 8658163
  11. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae.
    Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):265-70 PMID: 8990197
  12. A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains.
    Mol Microbiol. 1997 Jan;23(2):323-31 PMID: 9044266
  13. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites.
    Protein Eng. 1997 Jan;10(1):1-6 PMID: 9051728
  14. Phase variation in tcpH modulates expression of the ToxR regulon in Vibrio cholerae.
    Mol Microbiol. 1997 Sep;25(6):1099-111 PMID: 9350866
  15. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae.
    Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):730-4 PMID: 9435261
  16. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3134-9 PMID: 9501228
  17. Analysis of ToxR-dependent transcription activation of ompU, the gene encoding a major envelope protein in Vibrio cholerae.
    Mol Microbiol. 1998 Jul;29(1):235-46 PMID: 9701817
  18. A new level in the Vibrio cholerae ToxR virulence cascade: AphA is required for transcriptional activation of the tcpPH operon.
    Mol Microbiol. 1999 Feb;31(3):763-71 PMID: 10048021
  19. Penicillin V acylase crystal structure reveals new Ntn-hydrolase family members.
    Nat Struct Biol. 1999 May;6(5):414-6 PMID: 10331865
  20. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria.
    Nature. 1999 May 27;399(6734):375-9 PMID: 10360577
  21. A Vibrio cholerae LysR homolog, AphB, cooperates with AphA at the tcpPH promoter to activate expression of the ToxR virulence cascade.
    J Bacteriol. 1999 Jul;181(14):4250-6 PMID: 10400582
  22. Molecular cloning and transcriptional regulation of ompT, a ToxR-repressed gene in Vibrio cholerae.
    Mol Microbiol. 2000 Jan;35(1):189-203 PMID: 10632889
  23. Differential activation of the tcpPH promoter by AphB determines biotype specificity of virulence gene expression in Vibrio cholerae.
    J Bacteriol. 2000 Jun;182(11):3228-38 PMID: 10809704
  24. Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade.
    J Bacteriol. 2000 Aug;182(15):4295-303 PMID: 10894740
  25. The Vibrio cholerae ToxR/TcpP/ToxT virulence cascade: distinct roles for two membrane-localized transcriptional activators on a single promoter.
    Mol Microbiol. 2000 Oct;38(1):67-84 PMID: 11029691
  26. Inducible metabolism of phenolic acids in Pediococcus pentosaceus is encoded by an autoregulated operon which involves a new class of negative transcriptional regulator.
    J Bacteriol. 2000 Dec;182(23):6724-31 PMID: 11073918
  27. pepA, a gene mediating pH regulation of virulence genes in Vibrio cholerae.
    J Bacteriol. 2001 Jan;183(1):178-88 PMID: 11114915
  28. Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter.
    Mol Microbiol. 2001 Jul;41(2):393-407 PMID: 11489126
  29. Quorum sensing in bacteria.
    Annu Rev Microbiol. 2001;55:165-99 PMID: 11544353
  30. Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation.
    Mol Microbiol. 2002 Jan;43(1):119-34 PMID: 11849541
  31. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):3129-34 PMID: 11854465
  32. ToxR interferes with CRP-dependent transcriptional activation of ompT in Vibrio cholerae.
    Mol Microbiol. 2002 Mar;43(6):1577-89 PMID: 11952906
  33. Binding site requirements of the virulence gene regulator AphB: differential affinities for the Vibrio cholerae classical and El Tor tcpPH promoters.
    Mol Microbiol. 2002 Apr;44(2):533-47 PMID: 11972789
  34. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae.
    Cell. 2002 Aug 9;110(3):303-14 PMID: 12176318
  35. Mechanism of ToxT-dependent transcriptional activation at the Vibrio cholerae tcpA promoter.
    J Bacteriol. 2002 Oct;184(20):5533-44 PMID: 12270810
  36. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter.
    Mol Microbiol. 2002 Nov;46(4):1135-47 PMID: 12421317
  37. A new colorimetric method for the determination of 6-aminopenicillanic acid.
    Anal Biochem. 1978 May;86(1):118-26 PMID: 207197
  38. Molecular cloning of Bacillus sphaericus penicillin V amidase gene and its expression in Escherichia coli and Bacillus subtilis.
    Appl Environ Microbiol. 1985 May;49(5):1084-9 PMID: 3923928
  39. Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein.
    Cell. 1987 Jan 30;48(2):271-9 PMID: 3802195
  40. Sequencing and heterologous expression of the gene encoding penicillin V amidase from Bacillus sphaericus.
    Gene. 1986;45(2):175-81 PMID: 3026906
  41. Culture conditions for stimulating cholera toxin production by Vibrio cholerae O1 El Tor.
    Microbiol Immunol. 1986;30(11):1075-83 PMID: 3543624
  42. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector.
    Gene. 1986;48(1):119-31 PMID: 3549457
  43. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2833-7 PMID: 2883655
  44. Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter.
    J Bacteriol. 1989 Mar;171(3):1288-93 PMID: 2646275
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2003-08-00
Pages
4825-36
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC166470
Subset
IM
Grants
NIAID NIH HHS · R01 AI041558 · United States
NIAID NIH HHS · R29 AI041558 · United States
NIAID NIH HHS · AI-41558 · United States
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: product@genelibs.com