Surface-attached molecules control Staphylococcus aureus quorum sensing and biofilm development

Nature Microbiology

Volumn 2, Issue , 2017, Pages

  Kim, Minyoung Kevin ^a   Zhao, Aishan ^a   Wang, Ashley ^a   Brown, Zachary Z ^a   Muir, Tom W ^a   Stone, Howard A ^b   Bassler, Bonnie L ^a,c  

^a PRINCETON UNIVERSITY   (United States)

^b Princeton University   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOINDUCER PEPTIDE 1; BACTERIAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BIOFILM; CLICK CHEMISTRY; CONTROLLED STUDY; COVALENT BOND; NONHUMAN; PRIORITY JOURNAL; QUORUM SENSING; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTY; DRUG EFFECT; ENVIRONMENTAL MICROBIOLOGY; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; SECOND MESSENGER;

BIOFILMS; ENVIRONMENTAL MICROBIOLOGY; QUORUM SENSING; SECOND MESSENGER SYSTEMS; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTIES;

EID: 85019660155     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2017.80     Document Type: Article

References (55)

1. Wang, B., & Muir, T. W. Regulation of virulence in Staphylococcus aureus: molecular mechanisms and remaining puzzles. Cell Chem. Biol. 23, 214-224 (2016
2. Kong, K. F., Vuong, C., & Otto, M. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol. 296, 133-139 (2006
3. Drescher, K., et al. Architectural transitions in Vibrio cholerae biofilms at single-cell resolution. Proc. Natl Acad. Sci. USA 113, E2066-E2072 (2016
4. Yan, J., Sharo, A. G., Stone, H. A., Wingreen, N. S., & Bassler, B. L. Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging. Proc. Natl Acad. Sci. USA 113, E5337-E5343 (2016
5. Nadell, C. D., Drescher, K., & Foster, K. R. Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14, 589-600 (2016
6. Waters, C. M., & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319-346 (2005
7. Papenfort, K., & Bassler, B. L. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14, 576-588 (2016
8. Novick, R. P., & Geisinger, E. Quorum sensing in staphylococci. Annu. Rev. Genet. 42, 541-564 (2008
9. Dinges, M. M., Orwin, P. M., & Schlievert, P. M. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13, 16-34 (2000
10. Arvidson, S., & Tegmark, K. Regulation of virulence determinants in Staphylococcus aureus. Int. J. Med. Microbiol. 291, 159-170 (2001
11. Hammer, B. K., & Bassler, B. L. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50, 101-104 (2003
12. Hsiao, A., et al. Members of the human gut microbiota involved in recovery from Vibrio cholerae infection. Nature 515, 423-426 (2014
13. Ismail, A. S., Valastyan, J. S., & Bassler, B. L. A host-produced autoinducer-2 mimic activates bacterial quorum sensing. Cell Host Microbe 19, 470-480 (2016
14. O'Loughlin, C. T., et al. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc. Natl Acad. Sci. USA 110, 17981-17986 (2013
15. Sully, E. K., et al. Selective chemical inhibition of agr quorum sensing in Staphylococcus aureus promotes host defense with minimal impact on resistance. PLoS Pathog. 10, e1004174 (2014
16. Otto, M. Quorum-sensing control in Staphylococci-a target for antimicrobial drug therapy? FEMS Microbiol. Lett. 241, 135-141 (2004
17. Cegelski, L., Marshall, G. R., Eldridge, G. R., & Hultgren, S. J. The biology and future prospects of antivirulence therapies. Nat. Rev. Microbiol. 6, 17-27 (2008
18. Kim, M. K., Ingremeau, F. B., Zhao, A., Bassler, B. L., & Stone, H. A. Local and global consequence of flow on bacterial quorum sensing. Nat. Microbiol. 1, 15005 (2016
19. Lu, H. D., et al. Modulating Vibrio cholerae quorum-sensing-controlled communication using autoinducer-loaded nanoparticles. Nano Lett. 15, 2235-2241 (2015
20. Persat, A., et al. The mechanical world of bacteria. Cell 161, 988-997 (2015
21. Kim, M. K., Drescher, K., Pak, O. S., Bassler, B. L., & Stone, H. A. Filaments in curved streamlines: rapid formation of Staphylococcus aureus biofilm streamers. New J. Phys. 16, 065024 (2014
22. Broderick, A. H., et al. Surface coatings that promote rapid release of peptidebased AgrC inhibitors for attenuation of quorum sensing in Staphylococcus aureus. Adv. Healthc. Mater. 3, 97-105 (2014
23. Ho, K. K. K., et al. Quorum sensing inhibitory activities of surface immobilized antibacterial dihydropyrrolones via click chemistry. Biomaterials 35, 2336-2345 (2014
24. Lowy, F. D. Staphylococcus aureus infections. New Engl. J. Med. 339, 2026-2027 (1998
25. Gordon, R. J., & Lowy, F. D. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin. Infect. Dis. 46, S350-S359 (2008
26. Zhang, L. S., Gray, L., Novick, R. P., & Ji, G. Y. Transmembrane topology of AgrB, the protein involved in the post-translational modification of AgrD in Staphylococcus aureus. J. Biol. Chem. 277, 34736-34742 (2002
27. Wang, B. Y., Zhao, A. S., Novick, R. P., & Muir, T. W. Key driving forces in the biosynthesis of autoinducing peptides required for staphylococcal virulence. Proc. Natl Acad. Sci. USA 112, 10679-10684 (2015
28. Lina, G., et al. Transmembrane topology and histidine protein kinase activity of AgrC, the agr signal receptor in Staphylococcus aureus. Mol. Microbiol. 28, 655-662 (1998
29. Wang, B. Y., Zhao, A. S., Novick, R. P., & Muir, T.W. Activation and inhibition of the receptor histidine kinase AgrC occurs through opposite helical transduction motions. Mol. Cell 53, 929-940 (2014
30. Koenig, R. L., Ray, J. L., Maleki, S. J., Smeltzer, M. S., & Hurlburt, B. K. Staphylococcus aureus AgrA binding to the RNAIII-agr regulatory region. J. Bacteriol. 186, 7549-7555 (2004
31. Fechter, P., Caldelari, I., Lioliou, E., & Romby, P. Novel aspects of RNA regulation in Staphylococcus aureus. FEBS Lett. 588, 2523-2529 (2014
32. Lyon, G. J., Wright, J. S., Muir, T. W., & Novick, R. P. Key determinants of receptor activation in the agr autoinducing peptides of Staphylococcus aureus. Biochemistry 41, 10095-10104 (2002
33. Hong, V., Presolski, S. I., Ma, C., & Finn, M. G. Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation. Angew. Chem. Int. Ed. 48, 9879-9883 (2009
34. Emilsson, G., et al. Strongly stretched protein resistant poly(ethylene glycol) brushes prepared by grafting-to. ACS Appl. Mater. Inter. 7, 7505-7515 (2015
35. Cisar, E. A., Geisinger, E., Muir, T. W., & Novick, R. P. Symmetric signalling within asymmetric dimers of the Staphylococcus aureus receptor histidine kinase AgrC. Mol. Microbiol. 74, 44-57 (2009
36. Vollmer, W., Blanot, D., & de Pedro, M. A. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149-167 (2008
37. Traber, K. E., et al. Agr function in clinical Staphylococcus aureus isolates. Microbiology 154, 2265-2274 (2008
38. Khodaparast, S., Kim, M. K., Silpe, J., & Stone, H. A. Bubble-driven detachment of bacteria from confined microgeometries. Environ. Sci. Technol. 51, 1340-1347 (2017
39. Vasilev, K., Cook, J., & Griesser, H. J. Antibacterial surfaces for biomedical devices. Expert Rev. Med. Devices 6, 553-567 (2009
40. Gallo, J., Holinka, M., & Moucha, C. S. Antibacterial surface treatment for orthopaedic implants. Int. J. Mol. Sci. 15, 13849-13880 (2014
41. Lee, J. J., et al. Synthetic ligand-coated magnetic nanoparticles for microfluidic bacterial separation from blood. Nano Lett. 14, 1-5 (2014
42. Boles, B. R., & Horswill, A. R. agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4, e1000052 (2008
43. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2, 114-122 (2003
44. Painter, K. L., Krishna, A., Wigneshweraraj, S., & Edwards, A. M. What role does the quorum-sensing accessory gene regulator system play during Staphylococcus aureus bacteremia? Trends Microbiol. 22, 676-685 (2014
45. Huycke, M. M., Spiegel, C. A., & Gilmore, M. S. Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis. Antimicrob. Agents Chemother. 35, 1626-1634 (1991
46. Cook, L. C., & Federle, M. J. Peptide pheromone signaling in Streptococcus and Enterococcus. FEMS Microbiol. Rev. 38, 473-492 (2014
47. Nakayama, J., et al. Development of a peptide antagonist against fsr quorum sensing of Enterococcus faecalis. ACS Chem. Biol. 8, 804-811 (2013
48. Gray, B., Hall, P., & Gresham, H. Targeting agr-and agr-like quorum sensing systems for development of common therapeutics to treat multiple Gram-positive bacterial infections. Sensors 13, 5130-5166 (2013
49. Fujii, T., et al. Two homologous agr-like quorum-sensing systems cooperatively control adherence, cell morphology, and cell viability properties in Lactobacillus plantarum WCFS1. J. Bacteriol. 190, 7655-7665 (2008
50. Wang, I. N., Smith, D. L., & Young, R. Holins: the protein clocks of bacteriophage infections. Annu. Rev. Microbiol. 54, 799-825 (2000
51. Goedhart, J., et al. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat. Commun. 3, 751 (2012
52. Nadell, C. D., Drescher, K., Wingreen, N. S., & Bassler, B. L. Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J. 9, 1700-1709 (2015
53. Chen, J., Yoong, P., Ram, G., Torres, V. J., & Novick, R. P. Single-copy vectors for integration at the SaPI1 attachment site for Staphylococcus aureus. Plasmid 76, 1-7 (2014
54. Lyon, G. J., Mayville, P., Muir, T. W., & Novick, R. P. Rational design of a global inhibitor of the virulence response in Staphylococcus aureus, based in part on localization of the site of inhibition to the receptor-histidine kinase, AgrC. Proc. Natl Acad. Sci. USA 97, 13330-13335 (2000
55. Charpentier, E., et al. Novel cassette-based shuttle vector system for Gram-positive bacteria. Appl. Environ. Microbiol. 70, 6076-6085 (2004