Construction of a multiplex promoter reporter platform to monitor Staphylococcus aureus virulence gene expression and the identification of usnic acid as a potent suppressor of psm gene expression

Frontiers in Microbiology

Volumn 7, Issue AUG, 2016, Pages

  Gao, Peng ^a   Wang, Yanli ^a   Villanueva, Iván ^b   Ho, Pak Leung ^a,c   Davies, Julian ^b   Kao, Richard Yi Tsun ^a,c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c THE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Anti virulence; Bacterial infection; Beta lactams; MRSA; Virulence factors

Indexed keywords

AMPICILLIN; CHLORAMPHENICOL; OLIGONUCLEOTIDE; USNIC ACID;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM CULTURE; CELL INVASION ASSAY; CONTROLLED STUDY; DISK DIFFUSION; DNA SEQUENCE; GENE EXPRESSION; GENE REPRESSION; GENETIC MANIPULATION; GENETIC SCREENING; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS AUREUS; ULTRAVIOLET SPECTROPHOTOMETRY;

EID: 84989311404     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01344     Document Type: Article

References (34)

1. Anderson, M. J., Lin, Y. C., Gillman, A. N., Parks, P. J., Schlievert, P. M., and Peterson, M. L. (2012). Alpha-toxin promotes Staphylococcus aureus mucosal biofilm formation. Front. Cell. Infect. Microbiol. 2:64. doi: 10.3389/fcimb.2012.00064
2. Bateman, B. T., Donegan, N. P., Jarry, T. M., Palma, M., and Cheung, A. L. (2001). Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect. Immun. 69, 7851-7857. doi: 10.1128/IAI.69.12.7851-7857.2001
3. Beard, S. J., Salisbury, V., Lewis, R. J., Sharpe, J. A., and MacGowan, A. P. (2002). Expression of lux genes in a clinical isolate of Streptococcus pneumoniae: using bioluminescence to monitor gemifloxacin activity. Antimicrob. Agents Chemother. 46, 538-542. doi: 10.1128/AAC.46.2.538-542.2002
4. Blot, S. I., Vandewoude, K. H., Hoste, E. A., and Colardyn, F. A. (2002). Outcome and attributable mortality in critically Ill patients with bacteremia involving methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Arch. Intern. Med. 162, 2229-2235. doi: 10.1001/archinte.162.19.2229
5. Cheng, A. G., Kim, H. K., Burts, M. L., Krausz, T., Schneewind, O., and Missiakas, D. M. (2009). Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J. 23, 3393-3404. doi: 10.1096/fj.09-135467
6. Cheung, A. L., Schmidt, K., Bateman, B., and Manna, A. C. (2001). SarS, a SarA homolog repressible by agr, is an activator of protein A synthesis in Staphylococcus aureus. Infect. Immun. 69, 2448-2455. doi: 10.1128/IAI.69.4.2448-2455.2001
7. Cheung, A. L., and Zhang, G. (2002). Global regulation of virulence determinants in Staphylococcus aureus by the SarA protein family. Front. Biosci. 7, d1825-d1842. doi: 10.2741/cheung
8. Crossley, K. B. (2010). Staphylococci in Human Disease. Chichester; Hoboken, NJ: Wiley-Blackwell
9. Dancer, S. J. (2008). The effect of antibiotics on methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 61, 246-253. doi: 10.1093/jac/dkm465
10. Day, S. R., Moore, C. M., Kundzins, J. R., and Sifri, C. D. (2012). Community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus virulence toward Caenorhabditis elegans compared. Virulence 3, 576-582. doi: 10.4161/viru.22120
11. Francolini, I., Norris, P., Piozzi, A., Donelli, G., and Stoodley, P. (2004). Usnic acid, a natural antimicrobial agent able to inhibit bacterial biofilm formation on polymer surfaces. Antimicrob. Agents Chemother. 48, 4360-4365. doi: 10.1128/AAC.48.11.4360-4365.2004
12. Gao, J., and Stewart, G. C. (2004). Regulatory elements of the Staphylococcus aureus protein A (Spa) promoter. J. Bacteriol. 186, 3738-3748. doi: 10.1128/JB.186.12.3738-3748.2004
13. 2 inhibition in vitro and in vivo. J. Infect. Dis. 176, 431-438. doi: 10.1086/514061
14. Herbert, S., Ziebandt, A. K., Ohlsen, K., Schäfer, T., Hecker, M., Albrecht, D., et al. (2010). Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect. Immun. 78, 2877-2889. doi: 10.1128/IAI.00088-10
15. Ho, P. L., Chuang, S. K., Choi, Y. F., Lee, R. A., Lit, A. C., Ng, T. K., et al. (2008). Community-associated methicillin-resistant and methicillin-sensitive Staphylococcus aureus: skin and soft tissue infections in Hong Kong. Diagn. Microbiol. Infect. Dis. 61, 245-250. doi: 10.1016/j.diagmicrobio.2007.12.015
16. Ji, Y. (2007). Methicillin-resistant Staphylococcus aureus (MRSA) protocols. Methods Mol. Biol. 391, v. doi: 10.1007/978-1-59745-468-1
17. Kobayashi, S. D., Malachowa, N., Whitney, A. R., Braughton, K. R., Gardner, D. J., Long, D., et al. (2011). Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection. J. Infect. Dis. 204, 937-941. doi: 10.1093/infdis/jir441
18. Kuroda, H., Kuroda, M., Cui, L., and Hiramatsu, K. (2007). Subinhibitory concentrations of beta-lactam induce haemolytic activity in Staphylococcus aureus through the SaeRS two-component system. FEMS Microbiol. Lett. 268, 98-105. doi: 10.1111/j.1574-6968.2006.00568.x
19. Liang, X., and Ji, Y. (2007). Comparative analysis of staphylococcal adhesion and internalization by epithelial cells. Methods Mol. Biol. 391, 145-151. doi: 10.1007/978-1-59745-468-1_11
20. Löffler, B., Hussain, M., Grundmeier, M., Bruck, M., Holzinger, D., Varga, G., et al. (2010). Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog. 6:e1000715. doi: 10.1371/journal.ppat.1000715
21. Maciag-Dorszynska, M., Wegrzyn, G., and Guzow-Krzeminska, B. (2014). Antibacterial activity of lichen secondary metabolite usnic acid is primarily caused by inhibition of RNA and DNA synthesis. FEMS Microbiol. Lett. 353, 57-62. doi: 10.1111/1574-6968.12409
22. Mesak, L. R., Qi, S., Villanueva, I., Miao, V., and Davies, J. (2010). Staphylococcus aureus promoter-lux reporters for drug discovery. J. Antibiot. 63, 492-498. doi: 10.1038/ja.2010.74
23. Ohlsen, K., Koller, K. P., and Hacker, J. (1997). Analysis of expression of the alpha-toxin gene (hla) of Staphylococcus aureus by using a chromosomally encoded hla::lacZ gene fusion. Infect. Immun. 65, 3606-3614
24. Ohlsen, K., Ziebuhr, W., Koller, K. P., Hell, W., Wichelhaus, T. A., and Hacker, J. (1998). Effects of subinhibitory concentrations of antibiotics on alpha-toxin (hla) gene expression of methicillin-sensitive and methicillin-resistant Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 42, 2817-2823
25. Peacock, S. J., Moore, C. E., Justice, A., Kantzanou, M., Story, L., Mackie, K., et al. (2002). Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect. Immun. 70, 4987-4996. doi: 10.1128/IAI.70.9.4987-4996.2002
26. Qazi, S. N., Counil, E., Morrissey, J., Rees, C. E., Cockayne, A., Winzer, K., et al. (2001). agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect. Immun. 69, 7074-7082. doi: 10.1128/IAI.69.11.7074-7082.2001
27. Qiu, J., Feng, H., Lu, J., Xiang, H., Wang, D., Dong, J., et al. (2010a). Eugenol reduces the expression of virulence-related exoproteins in Staphylococcus aureus. Appl. Environ. Microbiol. 76, 5846-5851. doi: 10.1128/AEM.00704-10
28. Qiu, J., Wang, D., Xiang, H., Feng, H., Jiang, Y., Xia, L., et al. (2010b). Subinhibitory concentrations of thymol reduce enterotoxins A and B and alpha-hemolysin production in Staphylococcus aureus isolates. PLoS ONE 5:e9736. doi: 10.1371/journal.pone.0009736
29. Qiu, J., Zhang, X., Luo, M., Li, H., Dong, J., Wang, J., et al. (2011). Subinhibitory concentrations of perilla oil affect the expression of secreted virulence factor genes in Staphylococcus aureus. PLoS ONE 6:e16160. doi: 10.1371/journal.pone.0016160
30. Sacar, M., Sacar, S., Cevahir, N., Onem, G., Teke, Z., Asan, A., et al. (2010). Comparison of antimicrobial agents as therapy for experimental endocarditis: caused by methicillin-resistant Staphylococcus aureus. Tex. Heart Inst. J. 37, 400-404
31. Schmidt, K. A., Manna, A. C., and Cheung, A. L. (2003). SarT influences sarS expression in Staphylococcus aureus. Infect. Immun. 71, 5139-5148. doi: 10.1128/IAI.71.9.5139-5148.2003
32. Schwartz, K., Syed, A. K., Stephenson, R. E., Rickard, A. H., and Boles, B. R. (2012). Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog. 8:e1002744. doi: 10.1371/journal.ppat.1002744
33. Stevens, D. L., Ma, Y., Salmi, D. B., McIndoo, E., Wallace, R. J., and Bryant, A. E. (2007). Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 195, 202-211. doi: 10.1086/510396
34. Zielinska, A. K., Beenken, K. E., Joo, H. S., Mrak, L. N., Griffin, L. M., Luong, T. T., et al. (2011). Defining the strain-dependent impact of the Staphylococcal accessory regulator (sarA) on the alpha-toxin phenotype of Staphylococcus aureus. J. Bacteriol. 193, 2948-2958. doi: 10.1128/JB.01517-10