Engineering nanoparticles to silence bacterial communication

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Miller, Kristen P ^a   Wang, Lei ^a   Chen, Yung Pin ^a   Pellechia, Perry J ^a   Benicewicz, Brian C ^a   Decho, Alan W ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Nanomedicine; Nanoparticles; Quorum quenching; Quorum sensing

Indexed keywords

BETA CYCLODEXTRIN; N ACYLHOMOSERINE LACTONE; SILICA NANOPARTICLE;

ALIIVIBRIO FISCHERI; ARTICLE; BINDING AFFINITY; BIOLUMINESCENCE; CELL COMMUNICATION; CONTROLLED STUDY; DOWN REGULATION; LUX OPERON; NONHUMAN; OPERON; OPTICAL DENSITY; POLYMERASE CHAIN REACTION; PROTON NUCLEAR MAGNETIC RESONANCE; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; THERMOGRAVIMETRY; ULTRAVIOLET SPECTROPHOTOMETRY;

BACTERIA (MICROORGANISMS); VIBRIO FISCHERI;

EID: 84927155915     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00189     Document Type: Article

References (44)

1. Allison, K. R., Brynildsen, M. P., and Collins, J. J. (2011). Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473, 216-220. doi: 10.1038/nature10069.
2. Boettcher, K. J., and Ruby, E. G. (1990). Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172, 3701-3706.
3. Bose, J. L., Kim, U., Bartkowski, W., Gunsalus, R. P., Overley, A. M., Lyell, N. L., et al. (2007). Bioluminescence in Vibrio fischeri is controlled by the redox-responsive regulator ArcA. Mol. Microbiol. 65, 538-553. doi: 10.1111/j.1365-2958.2007.05809.x.
4. Canton, R., and Morosini, M. I. (2011). Emergence and spread of antibiotic resistance following exposure to antibiotics. FEMS Microbiol. Rev. 35, 977-991. doi: 10.1111/j.1574-6976.2011.00295.x.
5. Cash, B. M., Wang, L., and Benicewicz, B. C. (2012). The preparation and characterization of carboxylic acid-coated silica nanoparticles. J. Polym. Sci. A Polym. Chem. 50, 2533-2540. doi: 10.1002/pola.26029.
6. Costerton, J. W., Cheng, K. J., Geesey, G. G., Ladd, T. I., Nickel, J. C., Dasgupta, M., et al. (1987). Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41, 435-464. doi: 10.1146/annurev.mi.41.100187.002251.
7. Davies, D. (2003). Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2, 114-122. doi: 10.1038/nrd1008.
8. Davies, D. G. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298. doi: 10.1126/science.280.5361.295.
9. De, M., Ghosh, P. S., and Rotello, V. M. (2008). Applications of nanoparticles in biology. Adv. Mater. 20, 4225-4241. doi: 10.1002/adma.200703183.
10. Defoirdt, T. (2013). Antivirulence therapy for animal production: filling an arsenal with novel weapons for sustainable disease control. PLoS Pathog. 9:e1003603. doi: 10.1371/journal.ppat.1003603.
11. Derrick, T. S., McCord, E. F., and Larive, C. K. (2002). Analysis of protein/ligand interactions with NMR diffusion measurements: the importance of eliminating the protein background. J. Magn. Reson. 155, 217-225. doi: 10.1006/jmre.2002.2513.
12. Dong, Y.-H., Wang, L.-H., and Zhang, L.-H. (2007). Quorum-quenching microbial infections: mechanisms and implications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1201-1211. doi: 10.1098/rstb.2007.2045.
13. Eberhard, A., Burlingame, A. L., Eberhard, C., Kenyon, G. L., Nealson, K. H., and Oppenheimer, N. J. (1981). Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20, 2444-2449. doi: 10.1021/bi00512a013.
14. Engebrecht, J., Nealson, K., and Silverman, M. (1983). Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32, 773-781. doi: 10.1016/0092-8674(83)90063-6.
15. Engebrecht, J., and Silverman, M. (1984). Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. U.S.A. 81, 4152-4156. doi: 10.1073/pnas.81.13.4154.
16. Hoffmann, M., Brown, E. W., Feng, P. C., Keys, C. E., Fischer, M., and Monday, S. R. (2010). PCR-based method for targeting 16S-23S rRNA intergenic spacer regions among Vibrio species. BMC Microbiol. 10:90. doi: 10.1186/1471-2180-10-90.
17. Hoiby, N., Bjarnsholt, T., Givskov, M., Molin, S., and Ciofu, O. (2010). Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35, 322-332. doi: 10.1016/j.ijantimicag.2009.12.011.
18. Hong, K.-W., Koh, C.-L., Sam, C.-K., Yin, W.-F., and Chan, K.-G. (2012). Quorum quenching revisited-from signal decays to signalling confusion. Sensors 12, 4661-4696. doi: 10.3390/s120404661.
19. Jiang, W., Kim, B. Y., Rutka, J. T., and Chan, W. C. (2008). Nanoparticle-mediated cellular response is size-dependent. Nat. Nanotechnol. 3, 145-150. doi: 10.1038/nnano.2008.30.
20. Kaplan, H. B., and Greenberg, E. P. (1985). Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J. Bacteriol. 163, 1210-1214.
21. Kato, N., Morohoshi, T., Nozawa, T., Matsumoto, H., and Ikeda, T. (2006). Control of gram-negative bacterial quorum sensing with cyclodextrin immobilized cellulose ether gel. J. Incl. Phenom. Macrocycl. Chem. 56, 55-59. doi: 10.1007/s10847-006-9060-y.
22. LaSarre, B., and Federle, M. J. (2013). Exploiting quorum sensing to confuse bacterial pathogens. Microbiol. Mol. Biol. Rev. 77, 73. doi: 10.1128/MMBR.00046-12.
23. Li, J., Wang, L., and Benicewicz, B. C. (2013a). Synthesis of Janus nanoparticles via a combination of the reversible click reaction and "grafting to" strategies. Langmuir 29, 11547-11553. doi: 10.1021/la401990d.
24. Li, L., Sun, L., Song, Y., Wu, X., Zhou, X., Liu, Z., et al. (2013b). Screening of Actinobacillus pleuropneumoniae LuxS inhibitors. Curr. Microbiol. 67, 564-571. doi: 10.1007/s00284-013-0403-9.
25. Li, Y., Krentz, T. M., Wang, L., Benicewicz, B. C., and Schadler, L. S. (2014). Ligand engineering of polymer nanocomposites: from the simple to the complex. ACS Appl. Mater. Interfaces 6, 6005-6021. doi: 10.1021/am405332a.
26. Lupp, C., and Ruby, E. G. (2005). Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. J. Bacteriol. 187, 3620-3629. doi: 10.1128/JB.187.11.3620-3629.2005.
27. Madsen, J. S., Burmolle, M., Hansen, L. H., and Sorensen, S. J. (2012). The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol. Med. Microbiol. 65, 183-195. doi: 10.1111/j.1574-695X.2012.00960.x.
28. Malvindi, M. A., Brunetti, V., Vecchio, G., Galeone, A., Cingolani, R., and Pompa, P. P. (2012). SiO2 nanoparticles biocompatibility and their potential for gene delivery and silencing. Nanoscale 4, 486-495. doi: 10.1039/C1NR11269D.
29. Ng, W. L., and Bassler, B. L. (2009). Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43, 197-222. doi: 10.1146/annurev-genet-102108-134304.
30. Pelta, M. D., Morris, G. A., Stchedroff, M. J., and Hammond, S. J. (2002). A one-shot sequence for high-resolution diffusion-ordered spectroscopy. Magn. Reson. Chem. 40, S147-S152. doi: 10.1002/mrc.1107.
31. Rahman, I. A., Vejayakumaran, P., Sipaut, C. S., Ismail, J., and Chee, C. K. (2009). Size-dependent physicochemical and optical properties of silica nanoparticles. Mater. Chem. Phys. 114, 328-332. doi: 10.1016/j.matchemphys.2008.09.068.
32. Rasko, D. A., and Sperandio, V. (2010). Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9, 117-128. doi: 10.1038/nrd3013.
33. Rizzello, L., and Pompa, P. P. (2014). Nanosilver-based antibacterial drugs and devices: mechanisms, methodological drawbacks, and guidelines. Chem. Soc. Rev. 43, 1501. doi: 10.1039/C3CS60218D.
34. Schuster, M., Sexton, D. J., Diggle, S. P., and Greenberg, E. P. (2013). Acyl-homoserine lactone quorum sensing: from evolution to application. Annu. Rev. Microbiol. 67, 43-63. doi: 10.1146/annurev-micro-092412-155635.
35. Stacy, D. M., Welsh, M. A., Rather, P. N., and Blackwell, H. E. (2012). Attenuation of quorum sensing in the pathogen Acinetobacter baumannii using non-native N-acyl homoserine lactones. ACS Chem. Biol. 7, 1719-1728. doi: 10.1021/cb300351x.
36. Stevens, A. M., Dolan, K. M., and Greenberg, E. P. (1994). Synergistic binding of the Vibrio fischeri LuxR transcriptional activator domain and RNA polymerase to the lux promoter region. Proc. Natl. Acad. Sci. U.S.A. 91, 12619-12623. doi: 10.1073/pnas.91.26.12619.
37. Stewart, P., Rayner, J., Roe, F., and Rees, W. (2001). Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J. Appl. Microbiol. 91, 525-532. doi: 10.1046/j.1365-2672.2001.01413.x.
38. Studer, S. V., Mandel, M. J., and Ruby, E. G. (2008). AinS quorum sensing regulates the Vibrio fischeri acetate switch. J. Bacteriol. 190, 5915-5923. doi: 10.1128/JB.00148-08.
39. Szejtli, J. (1998). Introduction and general overview of cyclodextrin chemistry. Chem. Rev. 98, 1743-1754. doi: 10.1021/cr970022c.
40. Vertegel, A. A., Siegel, R. W., and Dordick, J. S. (2004). Silica nanoparticle size influences the structure and enzymatic activity of adsorbed lysozyme. Langmuir 20, 6800-6807. doi: 10.1021/la0497200.
41. Visick, K. L., Foster, J., Doino, J., McFall-Ngai, M., and Ruby, E. G. (2000). Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182, 4578-4586. doi: 10.1128/JB.182.16.4578-4586.2000.
42. Wang, L., and Benicewicz, B. C. (2013). Synthesis and characterization of dye-labeled poly(methacrylic acid) grafted silica nanoparticles. ACS Macro Lett. 2, 173-176. doi: 10.1021/mz3006507.
43. Wang, L., Chen, Y. P., Miller, K. P., Cash, B. M., Jones, S., Glenn, S., et al. (2014). Functionalised nanoparticles complexed with antibiotic efficiently kill MRSA and other bacteria. Chem. Commun. 50, 12030-12033. doi: 10.1039/c4cc04936e.
44. Welsh, M. A., Eibergen, N. R., Moore, J. D., and Blackwell, H. E. (2015). Small molecule disruption of quorum sensing cross-regulation in Pseudomonas aeruginosa causes major and unexpected alterations to virulence phenotypes. J. Am. Chem. Soc. 137, 1510-1519. doi: 10.1021/ja5110798.