Neutrophil elastase-mediated increase in airway temperature during inflammation

Annika Schmidt, Azzaq Belaaouaj, Rosi Bissinger, Garrit Koller, Laurette Malleret, Ciro D'Orazio, Martino Facchinelli, Bernhard Schulte-Hubbert, Antonio Molinaro, Otto Holst, Jutta Hammermann, Monika Schniederjans, Keith C. Meyer, Søren Damkiær Pedersen, Giorgio Piacentini, Baroukh Assael, Kenneth Bruce, Susanne Häußler, John J. LiPuma, Joachim Seelig & 2 others Dieter Worlitzsch, Gerd Döring

    Research output: Contribution to journalJournal articleResearchpeer-review

    Abstract

    Background
    How elevated temperature is generated during airway infections represents a hitherto unresolved physiological question. We hypothesized that innate immune defence mechanisms would increase luminal airway temperature during pulmonary infection.
    Methods
    We determined the temperature in the exhaled air of cystic fibrosis (CF) patients. To further test our hypothesis, a pouch inflammatory model using neutrophil elastase-deficient mice was employed. Next, the impact of temperature changes on the dominant CF pathogen Pseudomonas aeruginosa growth was tested by plating method and RNAseq.
    Results
    Here we show a temperature of ~ 38 °C in neutrophil-dominated mucus plugs of chronically infected CF patients and implicate neutrophil elastase:α1-proteinase inhibitor complex formation as a relevant mechanism for the local temperature rise. Gene expression of the main pathogen in CF, P. aeruginosa, under anaerobic conditions at 38 °C vs 30 °C revealed increased virulence traits and characteristic cell wall changes.
    Conclusion
    Neutrophil elastase mediates increase in airway temperature, which may contribute to P. aeruginosa selection during the course of chronic infection in CF.
    Original languageEnglish
    JournalJournal of Cystic Fibrosis
    Volume13
    Issue number6
    Pages (from-to)623-631
    ISSN1569-1993
    DOIs
    Publication statusPublished - 2014

    Cite this

    Schmidt, A., Belaaouaj, A., Bissinger, R., Koller, G., Malleret, L., D'Orazio, C., ... Döring, G. (2014). Neutrophil elastase-mediated increase in airway temperature during inflammation. Journal of Cystic Fibrosis, 13(6), 623-631. https://doi.org/10.1016/j.jcf.2014.03.004
    Schmidt, Annika ; Belaaouaj, Azzaq ; Bissinger, Rosi ; Koller, Garrit ; Malleret, Laurette ; D'Orazio, Ciro ; Facchinelli, Martino ; Schulte-Hubbert, Bernhard ; Molinaro, Antonio ; Holst, Otto ; Hammermann, Jutta ; Schniederjans, Monika ; Meyer, Keith C. ; Pedersen, Søren Damkiær ; Piacentini, Giorgio ; Assael, Baroukh ; Bruce, Kenneth ; Häußler, Susanne ; LiPuma, John J. ; Seelig, Joachim ; Worlitzsch, Dieter ; Döring, Gerd. / Neutrophil elastase-mediated increase in airway temperature during inflammation. In: Journal of Cystic Fibrosis. 2014 ; Vol. 13, No. 6. pp. 623-631.
    @article{ed4aff59cf0e4d97b4ea0458be359903,
    title = "Neutrophil elastase-mediated increase in airway temperature during inflammation",
    abstract = "BackgroundHow elevated temperature is generated during airway infections represents a hitherto unresolved physiological question. We hypothesized that innate immune defence mechanisms would increase luminal airway temperature during pulmonary infection. MethodsWe determined the temperature in the exhaled air of cystic fibrosis (CF) patients. To further test our hypothesis, a pouch inflammatory model using neutrophil elastase-deficient mice was employed. Next, the impact of temperature changes on the dominant CF pathogen Pseudomonas aeruginosa growth was tested by plating method and RNAseq. ResultsHere we show a temperature of ~ 38 °C in neutrophil-dominated mucus plugs of chronically infected CF patients and implicate neutrophil elastase:α1-proteinase inhibitor complex formation as a relevant mechanism for the local temperature rise. Gene expression of the main pathogen in CF, P. aeruginosa, under anaerobic conditions at 38 °C vs 30 °C revealed increased virulence traits and characteristic cell wall changes. Conclusion Neutrophil elastase mediates increase in airway temperature, which may contribute to P. aeruginosa selection during the course of chronic infection in CF.",
    author = "Annika Schmidt and Azzaq Belaaouaj and Rosi Bissinger and Garrit Koller and Laurette Malleret and Ciro D'Orazio and Martino Facchinelli and Bernhard Schulte-Hubbert and Antonio Molinaro and Otto Holst and Jutta Hammermann and Monika Schniederjans and Meyer, {Keith C.} and Pedersen, {S{\o}ren Damki{\ae}r} and Giorgio Piacentini and Baroukh Assael and Kenneth Bruce and Susanne H{\"a}u{\ss}ler and LiPuma, {John J.} and Joachim Seelig and Dieter Worlitzsch and Gerd D{\"o}ring",
    year = "2014",
    doi = "10.1016/j.jcf.2014.03.004",
    language = "English",
    volume = "13",
    pages = "623--631",
    journal = "Journal of Cystic Fibrosis",
    issn = "1569-1993",
    publisher = "Elsevier",
    number = "6",

    }

    Schmidt, A, Belaaouaj, A, Bissinger, R, Koller, G, Malleret, L, D'Orazio, C, Facchinelli, M, Schulte-Hubbert, B, Molinaro, A, Holst, O, Hammermann, J, Schniederjans, M, Meyer, KC, Pedersen, SD, Piacentini, G, Assael, B, Bruce, K, Häußler, S, LiPuma, JJ, Seelig, J, Worlitzsch, D & Döring, G 2014, 'Neutrophil elastase-mediated increase in airway temperature during inflammation', Journal of Cystic Fibrosis, vol. 13, no. 6, pp. 623-631. https://doi.org/10.1016/j.jcf.2014.03.004

    Neutrophil elastase-mediated increase in airway temperature during inflammation. / Schmidt, Annika; Belaaouaj, Azzaq; Bissinger, Rosi; Koller, Garrit; Malleret, Laurette; D'Orazio, Ciro; Facchinelli, Martino; Schulte-Hubbert, Bernhard; Molinaro, Antonio; Holst, Otto; Hammermann, Jutta; Schniederjans, Monika; Meyer, Keith C.; Pedersen, Søren Damkiær; Piacentini, Giorgio; Assael, Baroukh; Bruce, Kenneth; Häußler, Susanne; LiPuma, John J.; Seelig, Joachim; Worlitzsch, Dieter; Döring, Gerd.

    In: Journal of Cystic Fibrosis, Vol. 13, No. 6, 2014, p. 623-631.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - Neutrophil elastase-mediated increase in airway temperature during inflammation

    AU - Schmidt, Annika

    AU - Belaaouaj, Azzaq

    AU - Bissinger, Rosi

    AU - Koller, Garrit

    AU - Malleret, Laurette

    AU - D'Orazio, Ciro

    AU - Facchinelli, Martino

    AU - Schulte-Hubbert, Bernhard

    AU - Molinaro, Antonio

    AU - Holst, Otto

    AU - Hammermann, Jutta

    AU - Schniederjans, Monika

    AU - Meyer, Keith C.

    AU - Pedersen, Søren Damkiær

    AU - Piacentini, Giorgio

    AU - Assael, Baroukh

    AU - Bruce, Kenneth

    AU - Häußler, Susanne

    AU - LiPuma, John J.

    AU - Seelig, Joachim

    AU - Worlitzsch, Dieter

    AU - Döring, Gerd

    PY - 2014

    Y1 - 2014

    N2 - BackgroundHow elevated temperature is generated during airway infections represents a hitherto unresolved physiological question. We hypothesized that innate immune defence mechanisms would increase luminal airway temperature during pulmonary infection. MethodsWe determined the temperature in the exhaled air of cystic fibrosis (CF) patients. To further test our hypothesis, a pouch inflammatory model using neutrophil elastase-deficient mice was employed. Next, the impact of temperature changes on the dominant CF pathogen Pseudomonas aeruginosa growth was tested by plating method and RNAseq. ResultsHere we show a temperature of ~ 38 °C in neutrophil-dominated mucus plugs of chronically infected CF patients and implicate neutrophil elastase:α1-proteinase inhibitor complex formation as a relevant mechanism for the local temperature rise. Gene expression of the main pathogen in CF, P. aeruginosa, under anaerobic conditions at 38 °C vs 30 °C revealed increased virulence traits and characteristic cell wall changes. Conclusion Neutrophil elastase mediates increase in airway temperature, which may contribute to P. aeruginosa selection during the course of chronic infection in CF.

    AB - BackgroundHow elevated temperature is generated during airway infections represents a hitherto unresolved physiological question. We hypothesized that innate immune defence mechanisms would increase luminal airway temperature during pulmonary infection. MethodsWe determined the temperature in the exhaled air of cystic fibrosis (CF) patients. To further test our hypothesis, a pouch inflammatory model using neutrophil elastase-deficient mice was employed. Next, the impact of temperature changes on the dominant CF pathogen Pseudomonas aeruginosa growth was tested by plating method and RNAseq. ResultsHere we show a temperature of ~ 38 °C in neutrophil-dominated mucus plugs of chronically infected CF patients and implicate neutrophil elastase:α1-proteinase inhibitor complex formation as a relevant mechanism for the local temperature rise. Gene expression of the main pathogen in CF, P. aeruginosa, under anaerobic conditions at 38 °C vs 30 °C revealed increased virulence traits and characteristic cell wall changes. Conclusion Neutrophil elastase mediates increase in airway temperature, which may contribute to P. aeruginosa selection during the course of chronic infection in CF.

    U2 - 10.1016/j.jcf.2014.03.004

    DO - 10.1016/j.jcf.2014.03.004

    M3 - Journal article

    VL - 13

    SP - 623

    EP - 631

    JO - Journal of Cystic Fibrosis

    JF - Journal of Cystic Fibrosis

    SN - 1569-1993

    IS - 6

    ER -

    Schmidt A, Belaaouaj A, Bissinger R, Koller G, Malleret L, D'Orazio C et al. Neutrophil elastase-mediated increase in airway temperature during inflammation. Journal of Cystic Fibrosis. 2014;13(6):623-631. https://doi.org/10.1016/j.jcf.2014.03.004