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Research ArticleInflammation, Immunopharmacology, and Asthma

Influence of Influenza A Infection on Capsaicin-Induced Responses in Murine Airways

Samuel J. Taylor, Tracy S. Mann and Peter J. Henry
Journal of Pharmacology and Experimental Therapeutics February 2012, 340 (2) 377-385; DOI: https://doi.org/10.1124/jpet.111.187872
Samuel J. Taylor
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Tracy S. Mann
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Peter J. Henry
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Abstract

The principal aim of the study was to determine the influence of influenza A virus infection on capsaicin-induced relaxation responses in mouse isolated tracheal segments and clarify the underlying mechanisms. Anesthetized mice were intranasally inoculated with influenza A/PR-8/34 virus (VIRUS) or vehicle (SHAM), and 4 days later tracheal segments were harvested for isometric tension recording and biochemical and histologic analyses. Capsaicin induced dose-dependent relaxation responses in carbachol-contracted SHAM trachea (e.g., 10 μM capsaicin produced 66 ± 4% relaxation; n = 11), which were significantly inhibited by capsazepine [transient receptor potential vanilloid type 1 (TRPV1) antagonist], (2S,3S)-3-{[3,5-bis(trifluoromethyl)phenyl]methoxy}-2-phenylpiperidine hydrochloride (L-733,060) [neurokinin 1 (NK1) receptor antagonist], indomethacin [cyclooxygenase (COX) inhibitor], and the combination of 6-isopropoxy-9-oxoxanthene-2-carboxylic acid (AH6809) and 7-[5α-([1S,1α(Z)-biphenyl]-4-ylmethoxy)-2β-(4-morpholinyl)-3-oxocyclopentyl]-4-heptenoic acid, calcium salt, hydrate (AH23848) [E-prostanoid (EP)2 and EP4 receptor antagonists, respectively], indicating that capsaicin-induced relaxation involved the TRPV1-mediated release of substance P (SP), activation of epithelial NK1 receptors, and production of COX products capable of activating relaxant EP2/EP4 receptors. Consistent with this postulate, capsaicin-induced relaxation was associated with the significant release of SP and prostaglandin E2 (PGE2) from mouse tracheal segments. As expected, influenza A virus infection was associated with widespread disruption of the tracheal epithelium. Tracheal segments from VIRUS mice responded weakly to capsaicin (7 ± 3% relaxation) and were 25-fold less responsive to SP than tracheas from SHAM mice. In contrast, relaxation responses to exogenous PGE2 and the β-adrenoceptor agonist isoprenaline were not inhibited in VIRUS trachea. Virus infection was associated with impaired capsaicin-induced release of PGE2, but the release of SP was not affected. In summary, influenza A virus infection profoundly inhibits capsaicin- and SP-induced relaxation responses, most likely by inhibiting the production of PGE2.

Footnotes

  • This work was supported by the National Health and Medical Research Council of Australia.

  • Article, publication date, and citation information can be found at http://jpet.aspetjournals.org.

    http://dx.doi.org/10.1124/jpet.111.187872.

  • ABBREVIATIONS:

    TRP
    transient receptor potential
    TRPV1
    TRP vanilloid type 1
    VIRUS
    influenza A/PR-8/34 virus
    SHAM
    vehicle
    PG
    prostaglandin
    SP
    substance P
    EP
    E-prostanoid
    CDRC
    cumulative dose-response curve
    NK
    neurokinin
    COX
    cyclooxygenase
    EC40
    effective concentration of agonist inducing a 40% relaxation response to baseline
    Emax
    maximum response
    BAL
    bronchoalveolar lavage
    ELISA
    enzyme-linked immunosorbent assay
    PBS
    phosphate-buffered saline
    L-733,060
    (2S,3S)-3-{[3,5-bis(trifluoromethyl)phenyl]methoxy}-2-phenylpiperidine hydrochloride
    AH6809
    6-isopropoxy-9-oxoxanthene-2-carboxylic acid
    AH23848
    7-[5α-([1S,1α(Z)-biphenyl]-4-ylmethoxy)-2β-(4-morpholinyl)-3-oxocyclopentyl]-4-heptenoic acid, calcium salt, hydrate.

  • Received September 8, 2011.
  • Accepted November 4, 2011.
  • Copyright © 2012 by The American Society for Pharmacology and Experimental Therapeutics
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Journal of Pharmacology and Experimental Therapeutics: 340 (2)
Journal of Pharmacology and Experimental Therapeutics
Vol. 340, Issue 2
1 Feb 2012
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Research ArticleInflammation, Immunopharmacology, and Asthma

Influenza A and Sensory Nerve Function in Mouse Airways

Samuel J. Taylor, Tracy S. Mann and Peter J. Henry
Journal of Pharmacology and Experimental Therapeutics February 1, 2012, 340 (2) 377-385; DOI: https://doi.org/10.1124/jpet.111.187872

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Research ArticleInflammation, Immunopharmacology, and Asthma

Influenza A and Sensory Nerve Function in Mouse Airways

Samuel J. Taylor, Tracy S. Mann and Peter J. Henry
Journal of Pharmacology and Experimental Therapeutics February 1, 2012, 340 (2) 377-385; DOI: https://doi.org/10.1124/jpet.111.187872
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