Pseudomonas aeruginosa sabotages the generation of host proresolving lipid mediators

Flitter, Becca A.; Hvorecny, Kelli L.; Ono, Emiko; Eddens, Taylor; Yang, Jun; Kwak, Daniel H.; Bahl, Christopher D.; Hampton, Thomas H.; Morisseau, Christophe; Hammock, Bruce D.; Liu, Xinyu; Lee, Janet S.; Kolls, Jay K.; Levy, Bruce D.; Madden, Dean R.; Bomberger, Jennifer M.

doi:10.1073/pnas.1610242114

Title: Pseudomonas aeruginosa sabotages the generation of host proresolving lipid mediators

Journal Article · Thu Dec 15 00:00:00 EST 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1610242114· OSTI ID:1409591

Flitter, Becca A. ^[1]; Hvorecny, Kelli L. ^[2]; Ono, Emiko ^[3]; Eddens, Taylor ^[1]; Yang, Jun ^[4]; Kwak, Daniel H. ^[5]; Bahl, Christopher D. ^[2]; Hampton, Thomas H. ^[2]; Morisseau, Christophe ^[4]; Hammock, Bruce D. ^[4]; Liu, Xinyu ^[5]; Lee, Janet S. ^[5]; Kolls, Jay K. ^[1]; Levy, Bruce D. ^[3]; Madden, Dean R. ^[2]; Bomberger, Jennifer M. ^[1]

Univ. of Pittsburgh, PA (United States). School of Medicine
Geisel School of Medicine at Dartmouth, Hanover, NH (United States)
Harvard Medical School, Boston, MA (United States). Brigham and Women’s Hospital
Univ. of California, Davis, CA (United States)
Univ. of Pittsburgh, PA (United States)

Recurrent Pseudomonas aeruginosa infections coupled with robust, damaging neutrophilic inflammation characterize the chronic lung disease cystic fibrosis (CF). The proresolving lipid mediator, 15-epi lipoxin A₄ (15-epi LXA₄), plays a critical role in limiting neutrophil activation and tissue inflammation, thus promoting the return to tissue homeostasis. In this work w we show that a secreted P. aeruginosa epoxide hydrolase, cystic fibrosis transmembrane conductance regulator inhibitory factor (Cif), can disrupt 15-epi LXA₄ transcellular biosynthesis and function. In the airway, 15-epi LXA₄ production is stimulated by the epithelial-derived eicosanoid 14,15-epoxyeicosatrienoic acid (14,15-EET). Cif sabotages the production of 15-epi LXA₄ by rapidly hydrolyzing 14,15-EET into its cognate diol, eliminating a proresolving signal that potently suppresses IL-8–driven neutrophil transepithelial migration in vitro. Retrospective analyses of samples from patients with CF supported the translational relevance of these preclinical findings. Elevated levels of Cif in bronchoalveolar lavage fluid were correlated with lower levels of 15-epi LXA₄, increased IL-8 concentrations, and impaired lung function. Together, these findings provide structural, biochemical, and immunological evidence that the bacterial epoxide hydrolase Cif disrupts resolution pathways during bacterial lung infections. The data also suggest that Cif contributes to sustained pulmonary inflammation and associated loss of lung function in patients with CF

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Gilead Sciences Research Scholars in Cystic Fibrosis Award; Cystic Fibrosis Foundation; Munck-Pfefferkorn Award

Grant/Contract Number:: SC0012704; K99/R00HL098342; P30DK072506; T32AI060525; P01GM095467; U24AI118656; U24DK097154; R01AI091699; P20GM113132; P30GM106394; T32GM008704; GM-0800; MADDEN08G0; STANTO19R0

OSTI ID:: 1409591

Report Number(s):: BNL-114643-2017-JA

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, Issue 1; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 47 works

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Pseudomonas aeruginosa
epoxide hydrolase
inflammation
lipoxin
cystic fibrosis

Title: Pseudomonas aeruginosa sabotages the generation of host proresolving lipid mediators

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