Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

${\alpha}$-Cyperone Alleviates Lung Cell Injury Caused by Staphylococcus aureus via Attenuation of ${\alpha}$-Hemolysin Expression

  • Luo, M. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Qiu, J. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Zhang, Y. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Wang, J. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Dong, J. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Li, H. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Leng, B. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Zhang, Q. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Dai, X. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University) ;
  • Niu, X. (College of Quartermaster Technology, Jilin University) ;
  • Zhao, S. (The Second Hospital of Jilin University) ;
  • Deng, X. (Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary Medicine, Jilin University)
  • Received : 2012.02.09
  • Accepted : 2012.03.16
  • Published : 2012.08.28
Download PDF
⟨ Previous Next ⟩

Abstract

In this study, we aimed to evaluate the effect of ${\alpha}$-cyperone on S. aureus. We used a hemolysin test to examine the hemolytic activity in supernatants of S. aureus cultured with increasing concentrations of ${\alpha}$-cyperone. In addition, we evaluated the production of ${\alpha}$-hemolysin (Hla) by Western blotting. Real-time RT-PCR was performed to test the expression of hla (the gene encoding Hla) and agr (accessory gene regulator). Furthermore, we investigated the protective effect of ${\alpha}$-cyperone on Hla-induced injury of A549 lung cells by live/dead and cytotoxicity assays. We showed that in the presence of subinhibitory concentrations of ${\alpha}$-cyperone, Hla production was markedly inhibited. Moreover, ${\alpha}$-cyperone protected lung cells from Hla-induced injury. These findings indicate that ${\alpha}$-cyperone is a promising inhibitor of Hla production by S. aureus and protects lung cells from this bacterium. Thus, ${\alpha}$-cyperone may provide the basis for a new strategy to combat S. aureus pneumonia.

Keywords

References

  1. Bhakdi, S. and J. Tranum-Jensen. 1991. Alpha-toxin of Staphylococcus aureus. Microbiol. Rev. 55: 733-751.
  2. Boyle-Vavra, S. and R. S. Daum. 2007. Community-acquired methicillin-resistant Staphylococcus aureus: The role of Panton-Valentine leukocidin. Lab. Invest. 87: 3-9. https://doi.org/10.1038/labinvest.3700501
  3. Bramley, A. J., A. H. Patel, M. O'Reilly, R. Foster, and T. J. Foster. 1989. Roles of alpha-toxin and beta-toxin in virulence of Staphylococcus aureus for the mouse mammary gland. Infect. Immun. 57: 2489-2494.
  4. Bubeck Wardenburg, J., T. Bae, M. Otto, F. R. Deleo, and O. Schneewind. 2007. Poring over pores: Alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13: 1405-1406. https://doi.org/10.1038/nm1207-1405
  5. Callegan, M. C., L. S. Engel, J. M. Hill, and R. J. O'Callaghan. 1994. Corneal virulence of Staphylococcus aureus: Roles of alpha-toxin and protein A in pathogenesis. Infect. Immun. 62: 2478-2482.
  6. Cegelski, L., G. R. Marshall, G. R. Eldridge, and S. J. Hultgren. 2008. The biology and future prospects of antivirulence therapies. Nat. Rev. Microbiol. 6: 17-27. https://doi.org/10.1038/nrmicro1818
  7. Clinical and Laboratory Standards Institute. 2005. Performance Standards for Antimicrobial Susceptibility Testing; Fifteenth Informational Supplement. CLSI/NCCLS document; M100-S15.
  8. Gouaux, E. 1998. ${\alpha}$-Hemolysin from Staphylococcus aureus: An archetype of ${\beta}$-barrel, channel-forming toxins. J. Struct. Biol. 121: 110-122. https://doi.org/10.1006/jsbi.1998.3959
  9. Jia, W., X. Wang, D. Xu, A. Zhao, and Y. Zhang. 2006. Common traditional Chinese medicinal herbs for dysmenorrhea. Phytother. Res. 20: 819-824. https://doi.org/10.1002/ptr.1905
  10. Kilani, S., M. Ben Sghaier, I. Limem, I. Bouhlel, J. Boubaker, W. Bhouri, et al. 2008. In vitro evaluation of antibacterial, antioxidant, cytotoxic and apoptotic activities of the tubers infusion and extracts of Cyperus rotundus. Bioresour. Technol. 99: 9004-9008. https://doi.org/10.1016/j.biortech.2008.04.066
  11. Kilani, S., I. Bouhlel, R. Ben Ammar, M. Ben Sghair, I. Skandrani, J. Boubaker, et al. 2007. Chemical investigation of different extracts and essential oil from the tubers of (Tunisian) Cyperus rotundus. Correlation with their antiradical and antimutagenic properties. Ann. Microbiol. 57: 657-664. https://doi.org/10.1007/BF03175369
  12. Kilani, S., J. Ledauphin, I. Bouhlel, M. Ben Sghaier, J. Boubaker, I. Skandrani, et al. 2008. Comparative study of Cyperus rotundus essential oil by a modified GC/MS analysis method. Evaluation of its antioxidant, cytotoxic, and apoptotic effects. Chem. Biodivers. 5: 729-742. https://doi.org/10.1002/cbdv.200890069
  13. Klevens, R. M., M. A. Morrison, J. Nadle, S. Petit, K. Gershman, S. Ray, et al. 2007. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771. https://doi.org/10.1001/jama.298.15.1763
  14. Kollef, M. H., L. E. Morrow, M. S. Niederman, K. V. Leeper, A. Anzueto, L. Benz-Scott, and F. J. Rodino. 2006. Clinical characteristics and treatment patterns among patients with ventilator-associated pneumonia. Chest 129: 1210-1218. https://doi.org/10.1378/chest.129.5.1210
  15. Kuehnert, M. J., H. A. Hill, B. A. Kupronis, J. I. Tokars, S. L. Solomon, and D. B. Jernigan. 2005. Methicillin-resistant-Staphylococcus aureus hospitalizations, United States. Emerg. Infect. Dis. 11: 868-872. https://doi.org/10.3201/eid1106.040831
  16. Labandeira-Rey, M., F. Couzon, S. Boisset, E. L. Brown, M. Bes, Y. Benito, et al. 2007. Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315: 1130-1133. https://doi.org/10.1126/science.1137165
  17. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685. https://doi.org/10.1038/227680a0
  18. Lina, G., Y. Piemont, F. Godail-Gamot, M. Bes, M. O. Peter, V. Gauduchon, et al. 1999. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 29: 1128-1132. https://doi.org/10.1086/313461
  19. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532. https://doi.org/10.1056/NEJM199808203390806
  20. Mandell, L. A., R. G. Wunderink, A. Anzueto, J. G. Bartlett, G. D. Campbell, N. C. Dean, et al. 2007. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin. Infect. Dis. 44: S27-S72. https://doi.org/10.1086/511159
  21. McElroy, M. C., H. R. Harty, G. E. Hosford, G. M. Boylan, J. F. Pittet, and T. J. Foster. 1999. Alpha-toxin damages the airblood barrier of the lung in a rat model of Staphylococcus aureus-induced pneumonia. Infect. Immun. 67: 5541-5544.
  22. Ohlsen, K., W. Ziebuhr, K. P. Koller, W. Hell, T. A. Wichelhaus, and J. Hacker. 1998. Effects of subinhibitory concentrations of antibiotics on alpha-toxin (hla) gene expression of methicillinsensitive and methicillin-resistant Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 42: 2817-2823.
  23. Patel, A. H., P. Nowlan, E. D. Weavers, and T. Foster. 1987. Virulence of protein A-deficient and alpha-toxin-deficient mutants of Staphylococcus aureus isolated by allele replacement. Infect. Immun. 55: 3103-3110.
  24. Qiu, J. Z., M. J. Luo, J. F. Wang, J. Dong, H. E. Li, B. F. Leng, et al. 2011. Isoalantolactone protects against Staphylococcus aureus pneumonia. FEMS Microbiol. Lett. 324: 147-155. https://doi.org/10.1111/j.1574-6968.2011.02397.x
  25. Ragle, B. E., V. A. Karginov, and J. B. Wardenburg. 2010. Prevention and treatment of Staphylococcus aureus pneumonia with a beta-cyclodextrin derivative. Antimicrob. Agents Chemother. 54: 298-304. https://doi.org/10.1128/AAC.00973-09
  26. Ragle, B. E. and J. B. Wardenburg. 2009. Anti-alpha-hemolysin monoclonal antibodies mediate protection against Staphylococcus aureus pneumonia. Infect. Immun. 77: 2712-2718. https://doi.org/10.1128/IAI.00115-09
  27. Rasko, D. A. and V. Sperandio. 2010. Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9: 117-128. https://doi.org/10.1038/nrd3013
  28. Raut, N. A. and N. J. Gaikwad. 2006. Antidiabetic activity of hydro-ethanolic extract of Cyperus rotundus in alloxan induced diabetes in rats. Fitoterapia 77: 585-588. https://doi.org/10.1016/j.fitote.2006.09.006
  29. Rowe, G. E. and R. A. Welch. 1994. Assays of hemolytic toxins. Methods Enzymol. 235: 657-667.
  30. Rubin, R. J., C. A. Harrington, A. Poon, K. Dietrich, J. A. Greene, and A. Moiduddin. 1999. The economic impact of Staphylococcus aureus infection in New York City hospitals. Emerg. Infect. Dis. 5: 9-17. https://doi.org/10.3201/eid0501.990102
  31. Sambanthamoorthy, K., M. S. Smeltzer, and M. O. Elasri. 2006. Identification and characterization of msa (SA1233), a gene involved in expression of SarA and several virulence factors in Staphylococcus aureus. Microbiology 152: 2559-2572. https://doi.org/10.1099/mic.0.29071-0
  32. Song, L., M. R. Hobaugh, C. Shustak, S. Cheley, H. Bayley, and J. E. Gouaux. 1996. Structure of staphylococcal ${\alpha}$-hemolysin, a heptameric transmembrane pore. Science 274: 1859-1866. https://doi.org/10.1126/science.274.5294.1859
  33. Wang, J., J. Qiu, J. Dong, H. Li, M. Luo, X. Dai, et al. 2011. Chrysin protects mice from Staphylococcus aureus pneumonia. J. Appl. Microbiol. 111: 1551-1558. https://doi.org/10.1111/j.1365-2672.2011.05170.x
  34. Wardenburg, J. B., A. M. Palazzolo-Ballance, M. Otto, O. Schneewind, and F. R. DeLeo. 2008. Panton-Valentine leukocidin is not a virulence determinant in murine models of communityassociated methicillin-resistant Staphylococcus aureus disease. J. Infect. Dis. 198: 1166-1170. https://doi.org/10.1086/592053
  35. Wardenburg, J. B., R. J. Patel, and O. Schneewind. 2007. Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect. Immun. 75: 1040-1044. https://doi.org/10.1128/IAI.01313-06
  36. Wardenburg, J. B. and O. Schneewind. 2008. Vaccine protection against Staphylococcus aureus pneumonia. J. Exp. Med. 205: 287-294. https://doi.org/10.1084/jem.20072208

Cited by

  1. The Hexane Fraction of Cyperus rotundus Prevents Non-Alcoholic Fatty Liver Disease Through the Inhibition of Liver X Receptor α-Mediated Activation of Sterol Regulatory Element Binding Protein-1 vol.43, pp.3, 2012, https://doi.org/10.1142/s0192415x15500305
  2. Investigational therapies targeting quorum-sensing for the treatment of Staphylococcus aureus infections vol.24, pp.5, 2012, https://doi.org/10.1517/13543784.2015.1019062
  3. Plant Natural Products Targeting Bacterial Virulence Factors vol.116, pp.16, 2012, https://doi.org/10.1021/acs.chemrev.6b00184
  4. Chemical Composition, Antioxidant, Antimicrobial and Cytotoxic Activities of Essential Oil from Premna microphylla Turczaninow vol.22, pp.3, 2012, https://doi.org/10.3390/molecules22030381
  5. Resurgence of the Interest in Microorganisms and Plants as Sources of Secondary Metabolites for Treating Staphylococcal Infections vol.9, pp.1, 2019, https://doi.org/10.2174/2210315508666180604101323
  6. Natural Products That Target Virulence Factors in Antibiotic-Resistant Staphylococcus aureus vol.67, pp.48, 2012, https://doi.org/10.1021/acs.jafc.9b05595
  7. Plant Derived Natural Products against Pseudomonas aeruginosa and Staphylococcus aureus : Antibiofilm Activity and Molecular Mechanisms vol.25, pp.21, 2012, https://doi.org/10.3390/molecules25215024
  8. Novel Treatments and Preventative Strategies Against Food-Poisoning Caused by Staphylococcal Species vol.10, pp.2, 2012, https://doi.org/10.3390/pathogens10020091