Mucin glycans attenuate the virulence of Pseudomonas aeruginosa in infection.
Animals
Biofilms
Burns
/ microbiology
Epithelial Cells
/ microbiology
Female
HT29 Cells
Host-Pathogen Interactions
Humans
Mucins
/ chemistry
Mucus
/ chemistry
Polysaccharides
/ chemistry
Pseudomonas aeruginosa
/ drug effects
Quorum Sensing
Swine
Virulence
/ genetics
Wounds and Injuries
/ microbiology
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
received:
19
09
2018
accepted:
09
09
2019
pubmed:
16
10
2019
medline:
8
7
2020
entrez:
16
10
2019
Statut:
ppublish
Résumé
A slimy, hydrated mucus gel lines all wet epithelia in the human body, including the eyes, lungs, and gastrointestinal and urogenital tracts. Mucus forms the first line of defence while housing trillions of microorganisms that constitute the microbiota
Identifiants
pubmed: 31611643
doi: 10.1038/s41564-019-0581-8
pii: 10.1038/s41564-019-0581-8
pmc: PMC7157942
mid: NIHMS1539492
doi:
Substances chimiques
Mucins
0
Polysaccharides
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
2146-2154Subventions
Organisme : NIAID NIH HHS
ID : R01 AI097511
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES002109
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI061396
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103694
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI134895
Pays : United States
Organisme : NIBIB NIH HHS
ID : R01 EB017755
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008334
Pays : United States
Références
Schroeder, B. O. Fight them or feed them: how the intestinal mucus layer manages the gut microbiota. Gastroenterol. Rep. 7, 3–12 (2019).
Sadikot, R. T., Blackwell, T. S., Christman, J. W. & Prince, A. S. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am. J. Respir. Crit. Care Med. 171, 1209–1223 (2005).
pubmed: 15695491
pmcid: 2718459
Parsek, M. R. & Singh, P. K. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57, 677–701 (2003).
pubmed: 14527295
Co, J. Y. et al. Mucins trigger dispersal of Pseudomonas aeruginosa biofilms. NPJ Biofilms Microbiomes 4, 23 (2018).
pubmed: 30323945
pmcid: 6180003
Wagner, E., Wheeler, K. M. & Ribbeck, K. Mucins and their role in shaping the functions of mucus barriers. Annu. Rev. Cell Dev. Biol. 34, 189–215 (2018).
pubmed: 30296390
Toyofuku, M. et al. Quorum sensing regulates denitrification in Pseudomonas aeruginosa PAO1. J. Bacteriol. 189, 4969–4972 (2007).
pubmed: 17449629
pmcid: 1913425
Rohmer, L., Hocquet, D. & Miller, S. I. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol. 19, 341–348 (2011).
pubmed: 21600774
pmcid: 3130110
Jimenez, P. N. et al. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 76, 46–65 (2012).
pubmed: 22390972
Balasubramanian, D., Schneper, L., Kumari, H. & Mathee, K. A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res. 41, 1–20 (2013).
pubmed: 23143271
Van Der Reijden, W. A., Veerman, E. C. I. & Nieuw Amerongen, A. V. Rheological properties of commercially available polysaccharides with potential use in saliva substitutes. Biorheology 31, 631–642 (1994).
pubmed: 7696637
Jin, C. et al. Structural diversity of human gastric mucin glycans. Mol. Cell. Proteom. 16, 743–758 (2017).
Karlsson, N. G., Nordman, H., Karlsson, H., Carlstedt, I. & Hansson, G. C. Glycosylation differences between pig gastric mucin populations: a comparative study of the neutral oligosaccharides using mass spectrometry. Biochem. J. 326, 911–917 (1997).
pubmed: 9307045
pmcid: 1218750
Holmen Larsson, J. M., Thomsson, K. A., Rodriguez-Pineiro, A. M., Karlsson, H. & Hansson, G. C. Studies of mucus in mouse stomach, small intestine, and colon. III. Gastrointestinal Muc5ac and Muc2 mucin O-glycan patterns reveal a regiospecific distribution. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G357–G363 (2013).
pubmed: 23832516
pmcid: 3761246
Cummings, R. D. & Pierce, J. M. The challenge and promise of glycomics. Chem. Biol. 21, 1–15 (2014).
pubmed: 24439204
pmcid: 3955176
Xia, B., Royall, J. A., Damera, G., Sachdev, G. P. & Cummings, R. D. Altered O-glycosylation and sulfation of airway mucins associated with cystic fibrosis. Glycobiology 15, 747–775 (2005).
pubmed: 15994837
Nakano, M., Saldanha, R., Göbel, A., Kavallaris, M. & Packer, N. H. Identification of glycan structure alterations on cell membrane proteins in desoxyepothilone B resistant leukemia cells. Mol. Cell. Proteom. 10, M111.009001 (2011).
Lee, S. H. et al. Core2 O-glycan structure is essential for the cell surface expression of sucrase isomaltase and dipeptidyl peptidase-IV during intestinal cell differentiation. J. Biol. Chem. 285, 37683–37692 (2010).
pubmed: 20841351
pmcid: 2988373
Yamada, K. & Kinoshita, M. Comparative studies on the structural features of O-glycans between leukemia and epithelial cell lines. Proteome Res. 8, 521–537 (2009).
Varki, A. Biological roles of glycans. Glycobiology 27, 3–49 (2017).
pubmed: 27558841
Ventre, I. et al. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl Acad. Sci. USA 103, 171–176 (2006).
pubmed: 16373506
Basu Roy, A. & Sauer, K. Diguanylate cyclase NicD-based signalling mechanism of nutrient-induced dispersion by Pseudomonas aeruginosa. Mol. Microbiol. 94, 771–793 (2014).
pubmed: 25243483
Landry, R. M., An, D., Hupp, J. T., Singh, P. K. & Parsek, M. R. Mucin–Pseudomonas aeruginosa interactions promote biofilm formation and antibiotic resistance. Mol. Microbiol. 59, 142–151 (2006).
pubmed: 16359324
Secor, P. R., Michaels, L. A., Ratjen, A., Jennings, L. K. & Singh, P. K. Entropically driven aggregation of bacteria by host polymers promotes antibiotic tolerance in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 115, 10780–10785 (2018).
pubmed: 30275316
Cattoir, V. et al. Transcriptional response of mucoid Pseudomonas aeruginosa to human respiratory mucus. mBio 3, e00410-12 (2012).
pmcid: 3509433
Duan, K. & Surette, M. G. Environmental regulation of Pseudomonas aeruginosa PAO1 las and Rhl quorum-sensing systems. J. Bacteriol. 189, 4827–4836 (2007).
pubmed: 17449617
pmcid: 1913434
Arora, S. K., Ritchings, B. W., Almira, E. C., Lory, S. & Ramphal, R. The Pseudomonas aeruginosa flagellar cap protein, FliD, is responsible for mucin adhesion. Infect. Immun. 66, 1000–1007 (1998).
pubmed: 9488388
pmcid: 108008
Chua, S. L. et al. In vitro and in vivo generation and characterization of Pseudomonas aeruginosa biofilm-dispersed cells via c-di-GMP manipulation. Nat. Protoc. 10, 1165–1180 (2015).
pubmed: 26158442
Frenkel, E. S. & Ribbeck, K. Salivary mucins protect surfaces from colonization by cariogenic bacteria. Appl. Environ. Microbiol. 81, 332–338 (2015).
pubmed: 25344244
Kavanaugh, N. L., Zhang, A. Q., Nobile, C. J., Johnson, A. D. & Ribbeck, K. Mucins suppress virulence traits of Candida albicans. mBio 5, e01911-14 (2014).
pubmed: 25389175
pmcid: 4235211
Caldara, M. et al. Mucin biopolymers prevent bacterial aggregation by retaining cells in the free-swimming state. Curr. Biol. 22, 2325–2330 (2012).
pubmed: 23142047
pmcid: 3703787
Lieleg, O., Lieleg, C., Bloom, J., Buck, C. B. & Ribbeck, K. Mucin biopolymers as broad-spectrum antiviral agents. Biomacromolecules 13, 1724–1732 (2012).
pubmed: 22475261
pmcid: 3597216
Huang, Y., Mechref, Y. & Novotny, M. V. Microscale nonreductive release of O-linked glycans for subsequent analysis through MALDI mass spectrometry and capillary electrophoresis. Anal. Chem. 73, 6063–6069 (2001).
pubmed: 11791581
Packer, N. H., Lawson, M. A., Jardine, D. R. & Redmond, J. W. A general approach to desalting oligosaccharides released from glycoproteins. Glycoconj. J. 15, 737–747 (1998).
pubmed: 9870349
Chen, F.-T. A. & Evangelista, R. A. Profiling glycoprotein N-linked oligosaccharide by capillary electrophoresis. Electrophoresis 19, 2639–2644 (1998).
pubmed: 9848672
Guttman, A. Analysis of monosaccharide composition by capillary electrophoresis. J. Chromatogr. A 763, 271–277 (1997).
pubmed: 9129325
Taniguchi, T. et al. N-Glycosylation affects the stability and barrier function of the MUC16 mucin. J. Biol. Chem. 292, 11079–11090 (2017).
pubmed: 28487369
pmcid: 5491790
Afgan, E. et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res. 46, W537–W544 (2018).
pubmed: 29790989
pmcid: 6030816
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
Caballero, A., Thibodeaux, B., Marquart, M., Traidej, M. & O’Callaghan, R. Pseudomonas keratitis: protease IV gene conservation, distribution, and production relative to virulence and other Pseudomonas proteases. Investig. Ophthalmol. Vis. Sci. 45, 522–530 (2004).
Howe, T. R. & Iglewski, B. H. Isolation and characterization of alkaline protease-deficient mutants of Pseudomonas aeruginosa in vitro and in a mouse eye model. Infect. Immun. 43, 1058–1063 (1984).
pubmed: 6421735
pmcid: 264293
Dumas, Z., Ross-Gillespie, A. & Kümmerli, R. Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc. R. Soc. B 280, 20131055 (2013).
pubmed: 23760867
Junker, L. M. & Clardy, J. High-throughput screens for small-molecule inhibitors of Pseudomonas aeruginosa biofilm development. Antimicrob. Agents Chemother. 51, 3582–3590 (2007).
pubmed: 17664319
pmcid: 2043262
Roy, S. et al. Mixed-species biofilm compromises wound healing by disrupting epidermal barrier function. J. Pathol. 233, 331–343 (2014).
pubmed: 24771509
pmcid: 4380277
Borlee, B. R. et al. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol. Microbiol. 75, 827–842 (2010).
pubmed: 20088866
pmcid: 2847200