A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia

Yvonne McCarthy, Liang Yang, Kate B Twomey, Andrea Sass, Tim Tolker-Nielsen, Eshwar Mahenthiralingam, J Maxwell Dow, Robert P Ryan (Lead / Corresponding author)

    Research output: Contribution to journalArticle

    50 Citations (Scopus)

    Abstract

    Burkholderia cenocepacia is an opportunistic human pathogen that uses cis-2-dodecenoic acid (BDSF) as a quorum-sensing signal to control expression of virulence factors. BDSF is a signal molecule of the diffusible signal factor (DSF) family that was first described in the plant pathogen Xanthomonas campestris. The mechanism of perception of this signal and the range of functions regulated in B. cenocepacia are, however, unknown. A screen for transposon mutants unable to respond to exogenous signal identified BCAM0227 as a potential BDSF sensor. BCAM0227 is a histidine sensor kinase with an input domain unrelated to that of RpfC, the DSF sensor found in xanthomonads. Transcriptome profiling established the scope of the BDSF regulon and demonstrated that the sensor controls expression of a subset of these genes. A chimeric sensor kinase in which the input domain of BCAM0227 replaced the input domain of RpfC was active in BDSF signal perception when expressed in X. campestris. Mutation of BCAM0227 gave rise to reduced cytotoxicity to Chinese hamster ovary cells and reduced virulence to Wax moth larvae and in the agar-bead mouse model of pulmonary infection. The findings identify BCAM0227 as a novel BDSF sensor and a potential target for interference in virulence-related signalling in B. cenocepacia.
    Original languageEnglish
    Pages (from-to)1220-36
    Number of pages17
    JournalMolecular Microbiology
    Volume77
    Issue number5
    DOIs
    Publication statusPublished - Sep 2010

    Fingerprint

    Burkholderia cenocepacia
    Virulence
    Phosphotransferases
    Xanthomonas campestris
    Regulon
    Quorum Sensing
    Moths
    Waxes
    Gene Expression Profiling
    Virulence Factors
    Cricetulus
    Agar
    Larva
    bone marrow soluble immune-response suppressor
    2-dodecenoic acid
    Ovary
    Lung
    Mutation
    Infection

    Cite this

    McCarthy, Y., Yang, L., Twomey, K. B., Sass, A., Tolker-Nielsen, T., Mahenthiralingam, E., ... Ryan, R. P. (2010). A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. Molecular Microbiology, 77(5), 1220-36. https://doi.org/10.1111/j.1365-2958.2010.07285.x
    McCarthy, Yvonne ; Yang, Liang ; Twomey, Kate B ; Sass, Andrea ; Tolker-Nielsen, Tim ; Mahenthiralingam, Eshwar ; Dow, J Maxwell ; Ryan, Robert P. / A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. In: Molecular Microbiology. 2010 ; Vol. 77, No. 5. pp. 1220-36.
    @article{41cdf0626e984084a3f0f38dea6e2654,
    title = "A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia",
    abstract = "Burkholderia cenocepacia is an opportunistic human pathogen that uses cis-2-dodecenoic acid (BDSF) as a quorum-sensing signal to control expression of virulence factors. BDSF is a signal molecule of the diffusible signal factor (DSF) family that was first described in the plant pathogen Xanthomonas campestris. The mechanism of perception of this signal and the range of functions regulated in B. cenocepacia are, however, unknown. A screen for transposon mutants unable to respond to exogenous signal identified BCAM0227 as a potential BDSF sensor. BCAM0227 is a histidine sensor kinase with an input domain unrelated to that of RpfC, the DSF sensor found in xanthomonads. Transcriptome profiling established the scope of the BDSF regulon and demonstrated that the sensor controls expression of a subset of these genes. A chimeric sensor kinase in which the input domain of BCAM0227 replaced the input domain of RpfC was active in BDSF signal perception when expressed in X. campestris. Mutation of BCAM0227 gave rise to reduced cytotoxicity to Chinese hamster ovary cells and reduced virulence to Wax moth larvae and in the agar-bead mouse model of pulmonary infection. The findings identify BCAM0227 as a novel BDSF sensor and a potential target for interference in virulence-related signalling in B. cenocepacia.",
    author = "Yvonne McCarthy and Liang Yang and Twomey, {Kate B} and Andrea Sass and Tim Tolker-Nielsen and Eshwar Mahenthiralingam and Dow, {J Maxwell} and Ryan, {Robert P}",
    note = "{\circledC} 2010 Blackwell Publishing Ltd.",
    year = "2010",
    month = "9",
    doi = "10.1111/j.1365-2958.2010.07285.x",
    language = "English",
    volume = "77",
    pages = "1220--36",
    journal = "Molecular Microbiology",
    issn = "0950-382X",
    publisher = "Wiley",
    number = "5",

    }

    McCarthy, Y, Yang, L, Twomey, KB, Sass, A, Tolker-Nielsen, T, Mahenthiralingam, E, Dow, JM & Ryan, RP 2010, 'A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia', Molecular Microbiology, vol. 77, no. 5, pp. 1220-36. https://doi.org/10.1111/j.1365-2958.2010.07285.x

    A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. / McCarthy, Yvonne; Yang, Liang; Twomey, Kate B; Sass, Andrea; Tolker-Nielsen, Tim; Mahenthiralingam, Eshwar; Dow, J Maxwell; Ryan, Robert P (Lead / Corresponding author).

    In: Molecular Microbiology, Vol. 77, No. 5, 09.2010, p. 1220-36.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia

    AU - McCarthy, Yvonne

    AU - Yang, Liang

    AU - Twomey, Kate B

    AU - Sass, Andrea

    AU - Tolker-Nielsen, Tim

    AU - Mahenthiralingam, Eshwar

    AU - Dow, J Maxwell

    AU - Ryan, Robert P

    N1 - © 2010 Blackwell Publishing Ltd.

    PY - 2010/9

    Y1 - 2010/9

    N2 - Burkholderia cenocepacia is an opportunistic human pathogen that uses cis-2-dodecenoic acid (BDSF) as a quorum-sensing signal to control expression of virulence factors. BDSF is a signal molecule of the diffusible signal factor (DSF) family that was first described in the plant pathogen Xanthomonas campestris. The mechanism of perception of this signal and the range of functions regulated in B. cenocepacia are, however, unknown. A screen for transposon mutants unable to respond to exogenous signal identified BCAM0227 as a potential BDSF sensor. BCAM0227 is a histidine sensor kinase with an input domain unrelated to that of RpfC, the DSF sensor found in xanthomonads. Transcriptome profiling established the scope of the BDSF regulon and demonstrated that the sensor controls expression of a subset of these genes. A chimeric sensor kinase in which the input domain of BCAM0227 replaced the input domain of RpfC was active in BDSF signal perception when expressed in X. campestris. Mutation of BCAM0227 gave rise to reduced cytotoxicity to Chinese hamster ovary cells and reduced virulence to Wax moth larvae and in the agar-bead mouse model of pulmonary infection. The findings identify BCAM0227 as a novel BDSF sensor and a potential target for interference in virulence-related signalling in B. cenocepacia.

    AB - Burkholderia cenocepacia is an opportunistic human pathogen that uses cis-2-dodecenoic acid (BDSF) as a quorum-sensing signal to control expression of virulence factors. BDSF is a signal molecule of the diffusible signal factor (DSF) family that was first described in the plant pathogen Xanthomonas campestris. The mechanism of perception of this signal and the range of functions regulated in B. cenocepacia are, however, unknown. A screen for transposon mutants unable to respond to exogenous signal identified BCAM0227 as a potential BDSF sensor. BCAM0227 is a histidine sensor kinase with an input domain unrelated to that of RpfC, the DSF sensor found in xanthomonads. Transcriptome profiling established the scope of the BDSF regulon and demonstrated that the sensor controls expression of a subset of these genes. A chimeric sensor kinase in which the input domain of BCAM0227 replaced the input domain of RpfC was active in BDSF signal perception when expressed in X. campestris. Mutation of BCAM0227 gave rise to reduced cytotoxicity to Chinese hamster ovary cells and reduced virulence to Wax moth larvae and in the agar-bead mouse model of pulmonary infection. The findings identify BCAM0227 as a novel BDSF sensor and a potential target for interference in virulence-related signalling in B. cenocepacia.

    UR - http://www.scopus.com/inward/record.url?scp=77956165047&partnerID=8YFLogxK

    U2 - 10.1111/j.1365-2958.2010.07285.x

    DO - 10.1111/j.1365-2958.2010.07285.x

    M3 - Article

    VL - 77

    SP - 1220

    EP - 1236

    JO - Molecular Microbiology

    JF - Molecular Microbiology

    SN - 0950-382X

    IS - 5

    ER -