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Pseudomonas aeruginosa pili and flagella mediate distinct binding and signaling events at the apical and basolateral surface of airway epithelium.
Open accessAbstract
Pseudomonas aeruginosa, an important opportunistic pathogen of man, exploits numerous factors for initial attachment to the host, an event required to establish bacterial infection. In this paper, we rigorously explore the role of two major bacterial adhesins, type IV pili (Tfp) and flagella, in bacterial adherence to distinct host receptors at the apical (AP) and basolateral (BL) surfaces of polarized lung epithelial cells and induction of subsequent host signaling and pathogenic events. Using an isogenic mutant of P. aeruginosa that lacks flagella or utilizing beads coated with purified Tfp, we establish that Tfp are necessary and sufficient for maximal binding to host N-glycans at the AP surface of polarized epithelium. In contrast, experiments utilizing a P. aeruginosa isogenic mutant that lacks Tfp or using beads coated with purified flagella demonstrate that flagella are necessary and sufficient for maximal binding to heparan sulfate (HS) chains of heparan sulfate proteoglycans (HSPGs) at the BL surface of polarized epithelium. Using two different cell-free systems, we demonstrate that Tfp-coated beads show highest binding affinity to complex N-glycan chains coated onto plastic plates and preferentially aggregate with beads coated with N-glycans, but not with single sugars or HS. In contrast, flagella-coated beads bind to or aggregate preferentially with HS or HSPGs, but demonstrate little binding to N-glycans. We further show that Tfp-mediated binding to host N-glycans results in activation of phosphatidylinositol 3-kinase (PI3K)/Akt pathway and bacterial entry at the AP surface. At the BL surface, flagella-mediated binding to HS activates the epidermal growth factor receptor (EGFR), adaptor protein Shc, and PI3K/Akt, and induces bacterial entry. Remarkably, flagella-coated beads alone can activate EGFR and Shc. Together, this work provides new insights into the intricate interactions between P. aeruginosa and lung epithelium that may be potentially useful in the development of novel treatments for P. aeruginosa infections.
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“For example the exposure of apical receptors like integrins permit the adhesion of bacteria such as S. aureus and P. aeruginosa (Sanford et al., 1978; Davison and Sanford, 1981; Bucior et al., 2012; Smith and McCullers, 2014).”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Bucior et al., 2012
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BackgroundThe Role of PiuA, an Outer Membrane Iron Receptor, in the Pathogenesis of Pseudomonas Aeruginosa
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Characterization of a Type IV Pilus Biogenesis Operon in Pseudomonas aeruginosa
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“Differentiated airway epithelial 418 models have been utilised previously to study a number of bacterial pathogens, including 419 Pseudomonas aeruginosa [47-49], Haemophilus influenzae [50-52], Neisseria meningitidis 420 [53] and Mycoplasma pneumoniae [38, 41].”
BackgroundCutaneous Manifestations of Gram‐negative Infections
Faust, S. N., Gbesemete, D. F., & Heyderman, R. S. (2019) · Harper's Textbook of Pediatric Dermatology · doi:10.1002/9781119142812.ch38
Understanding the complications of pseudomonas aeruginosa biofilm exudates on wound healing
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The role of antibody in the killing of Pseudomonas aeruginosa by human sera
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Metadata
- Authors
- Bucior, I., Pielage, J. F., & Engel, J. N.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Bucior, Iwona
- Pielage, Julia F.
- Engel, Joanne N.
- ORCID
- Engel, Joanne N.
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-04-05
- Volume
- 8
- Issue
- 4
- Pages
- e1002616
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC3320588
- OpenAlex
- W2073200952
- Cited by
- 221
- References
- 66
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 13 · 2023: 21 · 2022: 15 · 2021: 13 · 2020: 17 · 2019: 17 · 2018: 15 · 2017: 20 · 2016: 14 · 2015: 10 · 2014: 24 · 2013: 14 · 2012: 2
- FWCI
- 6.42
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (P01AI053194, R01AI065902)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Keywords
- Pseudomonas aeruginosa, type IV pili, bacterial flagellum, bacterial adhesion, lung epithelium, N-glycans, heparan sulfate proteoglycans, phosphatidylinositol 3-kinase/Akt signaling, epidermal growth factor receptor, Shc adaptor protein, bacterial invasion, host-pathogen interaction, airway infection
- MeSH terms
- Bacterial Adhesion, Cell Line, Enzyme Activation, Flagella, Heparin, Humans, Lung, Mutation, Fimbriae, Bacterial, Pseudomonas aeruginosa, Pseudomonas Infections, Adhesins, Bacterial, Heparan Sulfate Proteoglycans, Phosphatidylinositol 3-Kinases, Respiratory Mucosa, Proto-Oncogene Proteins c-akt, ErbB Receptors
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