Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation

Mette Elena Skindersø, Louise Zeuthen, Susanne Brix Pedersen, Lisbeth Nielsen Fink, James Lazenby, Christine Whittall, Paul Williams, Stephen P. Diggle, Hanne Frøkiær, Margaret Cooley, Michael Christian Givskov

    Research output: Contribution to journalJournal articleResearchpeer-review

    Abstract

    Pseudomonas aeruginosa releases a wide array of toxins and tissue-degrading enzymes. Production of these malicious virulence factors is controlled by interbacterial communication in a process known as quorum sensing. An increasing body of evidence reveals that the bacterial signal molecule N-(3-oxododecanoyl)-l-homoserine lactone (OdDHL) exhibits both quorum-sensing signalling and immune-modulating properties. Recently, yet another quorum-sensing signal molecule, the Pseudomonas quinolone signal (PQS), has been shown to affect cytokine release by mitogen-stimulated human T cells. In the present article we demonstrate that both OdDHL and PQS decrease the production of interleukin-12 (IL-12) by Escherichia coli lipopolysaccharide-stimulated bone marrow-derived dendritic cells (BM-DCs) without altering their IL-10 release. Moreover, BM-DCs exposed to PQS and OdDHL during antigen stimulation exhibit a decreased ability to induce T-cell proliferation in vitro. Collectively, this suggests that OdDHL and PQS change the maturation pattern of stimulated DCs away from a proinflammatory T-helper type I directing response, thereby decreasing the antibacterial activity of the adaptive immune defence. OdDHL and PQS thus seem to possess dual activities in the infection process: as inducers of virulence factors as well as immune-modulators facilitating the infective properties of this pathogen.
    Original languageEnglish
    JournalF E M S Immunology and Medical Microbiology
    Volume55
    Issue number3
    Pages (from-to)335-345
    ISSN0928-8244
    DOIs
    Publication statusPublished - 2009

    Keywords

    • dendritic cell
    • quorum sensing
    • immunomodulation
    • PQS
    • Pseudomonas aeruginosa
    • OdDHL

    Cite this

    Skindersø, Mette Elena ; Zeuthen, Louise ; Pedersen, Susanne Brix ; Fink, Lisbeth Nielsen ; Lazenby, James ; Whittall, Christine ; Williams, Paul ; Diggle, Stephen P. ; Frøkiær, Hanne ; Cooley, Margaret ; Givskov, Michael Christian. / Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation. In: F E M S Immunology and Medical Microbiology. 2009 ; Vol. 55, No. 3. pp. 335-345.
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    abstract = "Pseudomonas aeruginosa releases a wide array of toxins and tissue-degrading enzymes. Production of these malicious virulence factors is controlled by interbacterial communication in a process known as quorum sensing. An increasing body of evidence reveals that the bacterial signal molecule N-(3-oxododecanoyl)-l-homoserine lactone (OdDHL) exhibits both quorum-sensing signalling and immune-modulating properties. Recently, yet another quorum-sensing signal molecule, the Pseudomonas quinolone signal (PQS), has been shown to affect cytokine release by mitogen-stimulated human T cells. In the present article we demonstrate that both OdDHL and PQS decrease the production of interleukin-12 (IL-12) by Escherichia coli lipopolysaccharide-stimulated bone marrow-derived dendritic cells (BM-DCs) without altering their IL-10 release. Moreover, BM-DCs exposed to PQS and OdDHL during antigen stimulation exhibit a decreased ability to induce T-cell proliferation in vitro. Collectively, this suggests that OdDHL and PQS change the maturation pattern of stimulated DCs away from a proinflammatory T-helper type I directing response, thereby decreasing the antibacterial activity of the adaptive immune defence. OdDHL and PQS thus seem to possess dual activities in the infection process: as inducers of virulence factors as well as immune-modulators facilitating the infective properties of this pathogen.",
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    author = "Skinders{\o}, {Mette Elena} and Louise Zeuthen and Pedersen, {Susanne Brix} and Fink, {Lisbeth Nielsen} and James Lazenby and Christine Whittall and Paul Williams and Diggle, {Stephen P.} and Hanne Fr{\o}ki{\ae}r and Margaret Cooley and Givskov, {Michael Christian}",
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    language = "English",
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    Skindersø, ME, Zeuthen, L, Pedersen, SB, Fink, LN, Lazenby, J, Whittall, C, Williams, P, Diggle, SP, Frøkiær, H, Cooley, M & Givskov, MC 2009, 'Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation', F E M S Immunology and Medical Microbiology, vol. 55, no. 3, pp. 335-345. https://doi.org/10.1111/j.1574-695X.2008.00533.x

    Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation. / Skindersø, Mette Elena; Zeuthen, Louise; Pedersen, Susanne Brix; Fink, Lisbeth Nielsen; Lazenby, James; Whittall, Christine; Williams, Paul; Diggle, Stephen P.; Frøkiær, Hanne; Cooley, Margaret; Givskov, Michael Christian.

    In: F E M S Immunology and Medical Microbiology, Vol. 55, No. 3, 2009, p. 335-345.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation

    AU - Skindersø, Mette Elena

    AU - Zeuthen, Louise

    AU - Pedersen, Susanne Brix

    AU - Fink, Lisbeth Nielsen

    AU - Lazenby, James

    AU - Whittall, Christine

    AU - Williams, Paul

    AU - Diggle, Stephen P.

    AU - Frøkiær, Hanne

    AU - Cooley, Margaret

    AU - Givskov, Michael Christian

    PY - 2009

    Y1 - 2009

    N2 - Pseudomonas aeruginosa releases a wide array of toxins and tissue-degrading enzymes. Production of these malicious virulence factors is controlled by interbacterial communication in a process known as quorum sensing. An increasing body of evidence reveals that the bacterial signal molecule N-(3-oxododecanoyl)-l-homoserine lactone (OdDHL) exhibits both quorum-sensing signalling and immune-modulating properties. Recently, yet another quorum-sensing signal molecule, the Pseudomonas quinolone signal (PQS), has been shown to affect cytokine release by mitogen-stimulated human T cells. In the present article we demonstrate that both OdDHL and PQS decrease the production of interleukin-12 (IL-12) by Escherichia coli lipopolysaccharide-stimulated bone marrow-derived dendritic cells (BM-DCs) without altering their IL-10 release. Moreover, BM-DCs exposed to PQS and OdDHL during antigen stimulation exhibit a decreased ability to induce T-cell proliferation in vitro. Collectively, this suggests that OdDHL and PQS change the maturation pattern of stimulated DCs away from a proinflammatory T-helper type I directing response, thereby decreasing the antibacterial activity of the adaptive immune defence. OdDHL and PQS thus seem to possess dual activities in the infection process: as inducers of virulence factors as well as immune-modulators facilitating the infective properties of this pathogen.

    AB - Pseudomonas aeruginosa releases a wide array of toxins and tissue-degrading enzymes. Production of these malicious virulence factors is controlled by interbacterial communication in a process known as quorum sensing. An increasing body of evidence reveals that the bacterial signal molecule N-(3-oxododecanoyl)-l-homoserine lactone (OdDHL) exhibits both quorum-sensing signalling and immune-modulating properties. Recently, yet another quorum-sensing signal molecule, the Pseudomonas quinolone signal (PQS), has been shown to affect cytokine release by mitogen-stimulated human T cells. In the present article we demonstrate that both OdDHL and PQS decrease the production of interleukin-12 (IL-12) by Escherichia coli lipopolysaccharide-stimulated bone marrow-derived dendritic cells (BM-DCs) without altering their IL-10 release. Moreover, BM-DCs exposed to PQS and OdDHL during antigen stimulation exhibit a decreased ability to induce T-cell proliferation in vitro. Collectively, this suggests that OdDHL and PQS change the maturation pattern of stimulated DCs away from a proinflammatory T-helper type I directing response, thereby decreasing the antibacterial activity of the adaptive immune defence. OdDHL and PQS thus seem to possess dual activities in the infection process: as inducers of virulence factors as well as immune-modulators facilitating the infective properties of this pathogen.

    KW - dendritic cell

    KW - quorum sensing

    KW - immunomodulation

    KW - PQS

    KW - Pseudomonas aeruginosa

    KW - OdDHL

    U2 - 10.1111/j.1574-695X.2008.00533.x

    DO - 10.1111/j.1574-695X.2008.00533.x

    M3 - Journal article

    C2 - 19187218

    VL - 55

    SP - 335

    EP - 345

    JO - F E M S Immunology and Medical Microbiology

    JF - F E M S Immunology and Medical Microbiology

    SN - 0928-8244

    IS - 3

    ER -