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Static mucus impairs bacterial clearance and allows chronic infection with Pseudomonas aeruginosa in the cystic fibrosis rat

Alexander G. Henderson, Joy M. Davis, Johnathan D. Keith, Morgan E. Green, Ashley M. Oden, Steven M. Rowe, Susan E. Birket
European Respiratory Journal 2022 60: 2101032; DOI: 10.1183/13993003.01032-2021
Alexander G. Henderson
Dept of Medicine and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
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Joy M. Davis
Dept of Medicine and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
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Johnathan D. Keith
Dept of Medicine and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
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Morgan E. Green
Dept of Medicine and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
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Ashley M. Oden
Dept of Medicine and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
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Steven M. Rowe
Dept of Medicine and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
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  • ORCID record for Steven M. Rowe
Susan E. Birket
Dept of Medicine and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama at Birmingham, Birmingham, AL, USA
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  • For correspondence: susanbirket@uabmc.edu
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Abstract

Cystic fibrosis airway disease is characterised by chronic Pseudomonas aeruginosa infection. Successful eradication strategies have been hampered by a poor understanding of the mechanisms underlying conversion to chronicity. The cystic fibrosis transmembrane conductance receptor (CFTR)-knockout (KO) rat harbours a progressive defect in mucociliary transport and viscosity. KO rats were infected before and after the appearance of the mucus defect, using a clinical mucoid-isolate of P. aeruginosa embedded in agarose beads. Young KO rats that were exposed to bacteria before the development of mucociliary transport defects resolved the infection and subsequent tissue damage. However, older KO rats that were infected in the presence of hyperviscous and static mucus were unable to eradicate bacteria, but instead had bacterial persistence through 28 days post-infection that was accompanied by airway mucus occlusion and lingering inflammation. Normal rats responded to infection with increased mucociliary transport to supernormal rates, which reduced the severity of a second bacterial exposure. We conclude that the aberrant mucus present in the CF airway permits persistence of P. aeruginosa in the lung.

Abstract

This study identifies the airway mucus response to Pseudomonas aeruginosa infection, which protects the normal airway against reinfection. The failure of this response in the cystic fibrosis lung leads to chronic infection and mucus occlusion. https://bit.ly/3nDiZCj

Footnotes

  • This article has an editorial commentary: https://doi.org/10.1183/13993003.00832-2022

  • Author contributions: S.M. Rowe and S.E. Birket conceived of the experiments; A.G. Henderson, J.M. Davis, J.D. Keith, M.E. Green, A.M. Oden and S.E. Birket performed the experiments; A.G. Henderson, J.M. Davis, J.D. Keith, M.E. Green, S.M. Rowe and S.E. Birket analysed the data; S.M. Rowe and S.E. Birket contributed reagents, materials, and/or analysis tools; S.M. Rowe and S.E. Birket wrote the manuscript; and S.E. Birket supervised the project.

  • Conflict of interest: A.G. Henderson has nothing to disclose.

  • Conflict of interest: J.M. Davis has nothing to disclose.

  • Conflict of interest: J.D. Keith has nothing to disclose.

  • Conflict of interest: M.E. Green has nothing to disclose.

  • Conflict of interest: A.M. Oden has nothing to disclose.

  • Conflict of interest: S.M. Rowe has a patent “Use of μOCT as a tool for diagnosis and drug discovery” issued.

  • Conflict of interest: S.E. Birket reports grants from NIH NHLBI and Cystic Fibrosis Foundation, during the conduct of the study.

  • Support statement: This work was supported by the National Heart, Lung, and Blood Institute (1K08HL131867, S.E. Birket), the National Institute of Diabetes, Digestive and Kidney Diseases (DK072482, S.M. Rowe) and the Cystic Fibrosis Foundation (R464-CF, ROWE19R0, BIRKET20A0-KB). Funding information for this article has been deposited with the Crossref Funder Registry.

  • Received April 9, 2021.
  • Accepted January 10, 2022.
  • Copyright ©The authors 2022. For reproduction rights and permissions contact permissions{at}ersnet.org
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Static mucus impairs bacterial clearance and allows chronic infection with Pseudomonas aeruginosa in the cystic fibrosis rat
Alexander G. Henderson, Joy M. Davis, Johnathan D. Keith, Morgan E. Green, Ashley M. Oden, Steven M. Rowe, Susan E. Birket
European Respiratory Journal Sep 2022, 60 (3) 2101032; DOI: 10.1183/13993003.01032-2021

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Static mucus impairs bacterial clearance and allows chronic infection with Pseudomonas aeruginosa in the cystic fibrosis rat
Alexander G. Henderson, Joy M. Davis, Johnathan D. Keith, Morgan E. Green, Ashley M. Oden, Steven M. Rowe, Susan E. Birket
European Respiratory Journal Sep 2022, 60 (3) 2101032; DOI: 10.1183/13993003.01032-2021
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