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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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“The flagella and TFP are adhesins for host cells [22].”
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Bertuzzi, M., Hayes, G., & Bignell, E. (2019) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuy045 · Cited by 31
Taouai, M., Chakroun, K., Sommer, R., Michaud, G., Giacalone, D., Maaouia, M. A. B., Vallin, A., Mathiron, D., Abidi, R., Darbre, T., et al. (2019) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.9b00481 · Cited by 28
“aeruginosa as do the negatively charged glycosaminoglycan heparane sulfates of host cell walls.(57)”
BackgroundWolfson, E. B., Elvidge, J., Tahoun, A. A. E., Gillespie, T., Mantell, J., McAteer, S. P., Rossez, Y., Paxton, E. A., Lane, F. M., Shaw, D. J., et al. (2020) · Microbiology · doi:10.1099/mic.0.000959 · Cited by 28
“Pseudomonas aeruginosa flagella bind to MUC1 and heparin-sulphated proteoglycans and E. coli flagella bind to ganglio-side receptor GM1 and charged glycerolipids, resulting in immuno-modulation and invasion [28, 52–54].”
BackgroundTan, R. M., Kuang, Z., Hao, Y., & Lau, G. W. (2013) · Journal of Innate Immunity · doi:10.1159/000354304 · Cited by 28
McDaniel, M. S., Lindgren, N. R., Billiot, C. E., Valladares, K. N., Sumpter, N. A., & Swords, W. E. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.03846-22 · Cited by 27
Heparin, Heparan Sulphate and Sepsis: Potential New Options for Treatment
Hogwood, J., Gray, E., & Mulloy, B. (2023) · Pharmaceuticals · doi:10.3390/ph16020271 · Cited by 28
“aeruginosa utilises interactions between its pili and host N-glycans to attach to and invade the apical surface of fully polarised epithelial cells, at the basolateral surface interactions between bacterial flagella and host HS perform the same function [58,59].”
BackgroundWagener, B. M., Hu, R.-H., Wu, S., Pittet, J., Ding, Q., & Che, P. (2021) · Toxins · doi:10.3390/toxins13110776 · Cited by 26
Epithelial Uptake of Flagella Initiates Proinflammatory Signaling
Parker, D., & Prince, A. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059932 · Cited by 26
“through the paracellular spaces to reach the basolateral aspects of the polarized airway epithelium [31], where in vitro studies suggest that attachment occurs [5].”
BackgroundEvidence for intracellular Pseudomonas aeruginosa
Resko, Z. J., Suhi, R. F., Thota, A. V., & Kroken, A. R. (2024) · Journal of Bacteriology · doi:10.1128/jb.00109-24 · Cited by 25
“Other bacterial surface factors that are predicted to influence surface attachment and subsequent invasion include the flagella, which is thought to facilitate cellular association through binding of N-glycans of polarized epithelial cells (55, 56).”
BackgroundTorres, I. M., Demirdjian, S., Vargas, J., Goodale, B. C., & Berwin, B. L. (2017) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00524.2016 · Cited by 23
Glycobiology of syndecan-1 in bacterial infections
Aquino, R. S., Teng, Y. H.-F., & Park, P. W. (2018) · Biochemical Society Transactions · doi:10.1042/bst20170395 · Cited by 23
“For example, while both Gram-positive Staphylococcus aureus [16] and Gram-negative Pseudomonas aeruginosa [17] can bind to HS, they do not bind to Sdc1 [18,19].”
BackgroundBanerjee, P., Chanchal, & Jain, D. (2019) · ACS Chemical Biology · doi:10.1021/acschembio.9b00255 · Cited by 23
Molecular interactions betweenNeisseria meningitidisand its human host
Coureuil, M., Jamet, A., Bille, E., Lécuyer, H., Bourdoulous, S., & Nassif, X. (2019) · Cellular Microbiology · doi:10.1111/cmi.13063 · Cited by 22
Beasley, K. L., Cristy, S. A., Elmassry, M. M., Dzvova, N., Colmer‐Hamood, J. A., & Hamood, A. N. (2020) · PLoS ONE · doi:10.1371/journal.pone.0240351 · Cited by 22
“To survive within different host niches and to combat host defenses, P . aeruginosa adjusts the production of numerous extracellular and cell-associated virulence factors [10–15].”
Shippy, D. C., Eakley, N. M., Mikheil, D. M., & Fadl, A. A. (2014) · Current Microbiology · doi:10.1007/s00284-014-0521-z · Cited by 22
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“The bind between the adhesins with a membrane receptor initiates bacterial attachment to the epithelial cells [22].”
BackgroundReceptor recognition by meningococcal type IV pili relies on a specific complex N -glycan
Guennec, L. L., Virion, Z., Bouzinba-Ségard, H., Masselot, C. R., Léonard, R., Nassif, X., Bourdoulous, S., & Coureuil, M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1919567117 · Cited by 22
“For instance, Tfp of Vibrio parahaemolyticus, a naturally occurring bacterium common in coastal waters, can interact with chitin, a long-chain polymer of N-acetylglucosamine abundantly found in the ocean (8), while Tfp from Pseudomonas aeruginosa, an important opportunistic pathogen causing acute and chronic pulmonary…”
BackgroundGu, M., Su, W., Dai, J., Wang, J., Jia, X., Yao, J., Zhang, G., Zhu, Q., & Pang, Z. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.116899 · Cited by 21
Host cell binding of the flagellar tip protein ofCampylobacter jejuni
Freitag, C. M., Strijbis, K., & van Putten, J. P. M. (2016) · Cellular Microbiology · doi:10.1111/cmi.12714 · Cited by 20
Synthesized Heparan Sulfate Competitors Attenuate Pseudomonas aeruginosa Lung Infection
Lorè, N. I., Veraldi, N., Riva, C., Sipione, B., Spagnuolo, L., Fino, I. D., Melessike, M., Calzi, E., Bragonzi, A., Naggi, A., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19010207 · Cited by 20
“aeruginosa and a binding site for bacterial flagella, and this could suggest another role during infection [32,33].”
BackgroundGarai, P., Lahiri, A., Ghosh, D., Chatterjee, J., & Chakravortty, D. (2015) · Microbiology · doi:10.1099/mic.0.000204 · Cited by 20
Yamazaki, K., Kashimoto, T., Morita, M., Kado, T., Matsuda, K., Yamasaki, M., & Ueno, S. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00123 · Cited by 19
“Adhesion and Biofilm Formation Type IV pili are known to play a role in cell adhesion, twitching motility, and the uptake of foreign genes (Paranjpye and Strom, 2005; Bucior et al., 2012).”
BackgroundCnm of Streptococcus mutans is important for cell surface structure and membrane permeability
Naka, S., Matsuoka, D., Goto, K., Misaki, T., Nagasawa, Y., Ito, S., Nomura, R., Nakano, K., & Matsumoto‐Nakano, M. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.994014 · Cited by 19
“Surface components for bacterial contact with environmental niches are involved in bacterial adhesion to and invasion of a host, and escape from host defense systems (Bucior et al., 2012; Chagnot et al., 2013).”
BackgroundAssessing Pseudomonas Virulence Using Host Cells
Bucior, I., Tran, C. S., & Engel, J. N. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-0473-0_57 · Cited by 19
Pletzer, D., Sun, E., Ritchie, C., Wilkinson, L., Liu, L. T., Trimble, M. J., Wolfmeier, H., Blimkie, T. M., & Hancock, R. E. W. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008444 · Cited by 19
“To establish an infection, it has been proposed that Pseudomonas type IV pili are involved in binding to the apical epithelial surface, while flagellar-mediated motility is proposed to be important for the colonization of the basolateral surface of airway epithelium [7].”
BackgroundAl-kafaween, M. A., Hilmi, A. B. M., Al‐Jamal, H. A. N., Elsahoryi, N. A., Jaffar, N., & Zahri, M. K. (2020) · PubMed Central · doi:10.30498/ijb.2020.2542 · Cited by 19
“aeruginosa, and each represents important virulence factors with respect to binding and signaling for cell–cell communication (43, 44).”
BackgroundDemirdjian, S., Hopkins, D. C., Cumbal, N., Lefort, C. T., & Berwin, B. L. (2020) · Infection and Immunity · doi:10.1128/iai.00011-20 · Cited by 18
“basolateral surface of the polarized epithelium (21, 22).”
BackgroundLiu, Y., Hussain, F., Negm, O. H., Paiva, A. C., Halliday, N., Dubern, J., Singh, S., Muntaka, S., Wheldon, L. M., Luckett, J., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.03018 · Cited by 18
Pseudomonas aeruginosa clinical blood isolates display significant phenotypic variability
Scheffler, R. J., Bratton, B. P., & Gitai, Z. (2022) · PLoS ONE · doi:10.1371/journal.pone.0270576 · Cited by 17
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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