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References

  1. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
    Pubmed CrossRef
  2. Barber M. 1961. Methicillin-resistant staphylococci. J. Clin. Pathol. 14: 385-393.
    Pubmed PMC CrossRef
  3. Boyle-Vavra S, Daum RS. 2007. Community-acquired methicillin-resistant Staphylococcus aureus: the role of PantonValentine leukocidin. Lab. Invest. 87: 3-9.
    Pubmed CrossRef
  4. Nimmo GR. 2012. USA300 abroad: global spread of a virulent strain of community-associated methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 18: 725-734.
    Pubmed CrossRef
  5. van der Mee-Marquet NL. 2016. Whole-genome sequencing analysis, an essential tool for shedding light on the obscure evolution of Staphylococcus aureus USA300. J. Infect. Dis. 213:1362-1363.
    Pubmed CrossRef
  6. Rossolini GM, Arena F, Pecile P, Pollini S. 2014. Update on the antibiotic resistance crisis. Curr. Opin. Pharmacol. 18: 56-60.
    Pubmed CrossRef
  7. Montgomery CP, Boyle-Vavra S , Adem PV, L ee JC, H u sain AN, Clasen J, Daum RS. 2008. Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J. Infect. Dis. 198: 561-570.
    Pubmed CrossRef
  8. Montgomery CP, Boyle-Vavra S, Daum RS. 2010. Importance of the global regulators Agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection. PLoS One 5: e15177.
    Pubmed PMC CrossRef
  9. Husmann M, Dersch K, Bobkiewicz W, Beckmann E, Veerachato G, Bhakdi S. 2006. Differential role of p38 mitogen activated protein kinase for cellular recovery from attack by pore-forming S. aureus alpha-toxin or streptolysin O. Biochem. Biophys. Res. Commun. 344: 1128-1134.
    Pubmed CrossRef
  10. Berube BJ, Bubeck Wardenburg J. 2013. Staphylococcus aureus alpha-toxin: nearly a century of intrigue. Toxins (Basel) 5:1140-1166.
    PMC CrossRef
  11. Dong J, Qiu J, Wang J, Li H, Dai X, Zhang Y, et al. 2013. Apigenin alleviates the symptoms of Staphylococcus aureus pneumonia by inhibiting the production of alpha-hemolysin. FEMS Microbiol. Lett. 338: 124-131.
    Pubmed CrossRef
  12. Qiu J, Luo M, Wang J, Dong J, Li H, Leng B, et al. 2011. Isoalantolactone protects against Staphylococcus aureus pneumonia. FEMS Microbiol. Lett. 324: 147-155.
    Pubmed CrossRef
  13. Qiu J, Xiang H, H u C, Wang Q , Dong J, Li H , et al. 2011. Subinhibitory concentrations of farrerol reduce alpha-toxin expression in Staphylococcus aureus. FEMS Microbiol Lett. 315:129-133.
    Pubmed CrossRef
  14. Wang D, Yu L, Xiang H, et al. 2008. Global transcriptional profiles of Staphylococcus aureus treated with berberine chloride. FEMS Microbiol. Lett. 279: 217-225.
    Pubmed CrossRef
  15. Miski M, Ulubelen A, Johansson C, Mabry TJ. 1983. Antibacterial activity studies of flavonoids from Salvia palaestina. J. Nat. Prod. 46: 874-875.
    Pubmed CrossRef
  16. Bhatia S, McGinty D, Letizia C, Api A. 2008. Fragrance material review on sclareol. Food Chem. Toxicol. 46: S270-S274.
    Pubmed CrossRef
  17. Dimas K, Kokkinopoulos D, Demetzos C, Vaos B, Marselos M, Malamas M, Tzavaras T. 1999. The effect of sclareol on growth and cell cycle progression of human leukemic cell lines. Leukemia Res. 23: 217-234.
    CrossRef
  18. CLSI. 2005. Performance standards for antimicrobial susceptiblity testing; fifteenth informational supplement (ISBN 1-56238-556-9). CLSI Document M100-S15. Clinical Laboratory Standards Institute, Wayne, PA, USA.
  19. Ou yang P , Chen J , Sun M, Y in Z , Lin J, F u H, et al. 2016. Imperatorin inhibits the expression of alpha-hemolysin in Staphylococcus aureus strain BAA-1717 (USA300). Antonie Van Leeuwenhoek 109: 915-922.
  20. Karginov VA, Nestorovich EM, Schmidtmann F, Robinson TM, Yohannes A, Fahmi NE, et al. 2007. Inhibition of S. aureus alpha-hemolysin and B. anthracis lethal toxin by betacyclodextrin derivatives. Bioorg. Med. Chem. 15: 5424-5431.
    Pubmed PMC CrossRef
  21. Hirst RA, Yesilkaya H, Clitheroe E, Rutman A, Dufty N, Mitchell TJ, et al. 2002. Sensitivities of human monocytes and epithelial cells to pneumolysin are different. Infect. Immun. 70: 1017-1022.
    Pubmed PMC CrossRef
  22. Bubeck Wardenburg J, Schneewind O. 2008. Vaccine protection against Staphylococcus aureus pneumonia. J. Exp. Med. 205:287-294.
    Pubmed PMC CrossRef
  23. Liang X, Yan M, Ji Y. 2009. The H35A mutated alpha-toxin interferes with cytotoxicity of staphylococcal alpha-toxin. Infect. Immun. 77: 977-983.
    Pubmed PMC CrossRef
  24. Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, et al. 2010. Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill. 15: 19694.
  25. Allen RC, Popat R, Diggle SP, Brown SP. 2014. Targeting virulence: can we make evolution-proof drugs? Nat. Rev. Microbiol. 12: 300-308.
    Pubmed CrossRef
  26. Defoirdt T. 2013. Antivirulence therapy for animal production:filling an arsenal with novel weapons for sustainable disease control. PLoS Pathog. 9: e1003603.
    Pubmed PMC CrossRef
  27. Rasko DA, Sperandio V. 2010. Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9:117-128.
    Pubmed CrossRef
  28. Wang J, Qiu J, Tan W, Zhang Y, Wang H, Zhou X, et al. 2015. Fisetin inhibits Listeria monocytogenes virulence by interfering with the oligomerization of listeriolysin O. J. Infect. Dis. 211: 1376-1387.
    Pubmed CrossRef
  29. Li H, Chen Y, Zhang B, Niu X, Song M, Luo Z, et al. 2016. Inhibition of sortase A by chalcone prevents Listeria monocytogenes infection. Biochem. Pharmacol. 106: 19-29.
    Pubmed CrossRef
  30. Adhikari RP, Ajao AO, Aman MJ, Karauzum H, Sarwar J, Lydecker AD, et al. 2012. Lower antibody levels to Staphylococcus aureus exotoxins are associated with sepsis in hospitalized adults with invasive S. aureus infections. J. Infect. Dis. 206: 915-923.
    Pubmed CrossRef
  31. Fritz SA, Tiemann KM, Hogan PG, Epplin EK, Rodriguez M, Al-Zubeidi DN, et al. 2013. A serologic correlate of protective immunity against community-onset Staphylococcus aureus infection. Clin. Infect. Dis. 56: 1554-1561.
    Pubmed PMC CrossRef
  32. Kolata J, Bode LG, Holtfreter S, Steil L, Kusch H, Holtfreter B, et al. 2011. Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 11: 3914-3927.
    Pubmed CrossRef
  33. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O. 2007. Poring over pores: alpha-hemolysin and PantonValentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13: 1405-1406.
    Pubmed CrossRef
  34. Rau ch S , DeDent AC, K im H K, Bubeck Wardenburg J, Missiakas DM, Schneewind O. 2012. Abscess formation and alpha-hemolysin induced toxicity in a mouse model of Staphylococcus aureus peritoneal infection. Infect. Immun. 80:3721-3732.
    Pubmed PMC CrossRef
  35. Kennedy AD, Bubeck Wardenburg J, Gardner DJ, Long D, Whitney AR, Braughton KR, et al. 2010. Targeting of alphahemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J. Infect. Dis. 202: 1050-1058.
    Pubmed PMC CrossRef
  36. Novick RP, Ross H, Projan S, Kornblum J, Kreiswirth B, Moghazeh S. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12: 3967-3975.
    Pubmed PMC
  37. Peng H, Novick R, Kreiswirth B, Kornblum J, Schlievert P. 1988. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170: 4365-4372.
    Pubmed PMC CrossRef
  38. Ohlsen K, Ziebuhr W, Koller K-P, Hell W, Wichelhaus TA, 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.
    Pubmed PMC
  39. Worlitzsch D, Kaygin H, Steinhuber A, Dalhoff A, Botzenhart K, Döring G. 2001. Effects of amoxicillin, gentamicin, and moxifloxacin on the hemolytic activity of Staphylococcus aureus in vitro and in vivo. Antimicrob. Agents Chemother. 45:196-202.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(1): 19-25

Published online January 28, 2017 https://doi.org/10.4014/jmb.1606.06039

Copyright © The Korean Society for Microbiology and Biotechnology.

Sclareol Protects Staphylococcus aureus-Induced Lung Cell Injury via Inhibiting Alpha-Hemolysin Expression

Ping Ouyang 1, Mao Sun 1, Xuewen He 1, Kaiyu Wang 1, Zhongqiong Yin 1, Hualin Fu 1, Yinglun Li 1, Yi Geng 1, Gang Shu 1, Changliang He 1, Xiaoxia Liang 1, Weiming Lai 1, Lixia Li 1, Yuanfeng Zou 1, Xu Song 1 and Lizi Yin 1*

College of Veterinary Medicine, Sichuan Agriculture University, Chengdu 611130, P.R. China

Received: June 16, 2016; Accepted: September 20, 2016

Abstract

Staphylococcus aureus (S. aureus) is a common gram-positive bacterium that causes serious
infections in humans and animals. With the continuous emergence of methicillin-resistant
S. aureus (MRSA) strains, antibiotics have limited efficacy in treating MRSA infections.
Accordingly, novel agents that act on new targets are desperately needed to combat these
infections. S. aureus alpha-hemolysin plays an indispensable role in its pathogenicity. In this
study, we demonstrate that sclareol, a fragrant chemical compound found in clary sage, can
prominently decrease alpha-hemolysin secretion in S. aureus strain USA300 at sub-inhibitory
concentrations. Hemolysis assays, western-blotting, and RT-PCR were used to detect the
production of alpha-hemolysin in the culture supernatant. When USA300 was co-cultured
with A549 epithelial cells, sclareol could protect the A549 cells at a final concentration of 8 μg/ml.
The protective capability of sclareol against the USA300-mediated injury of A549 cells was
further shown by cytotoxicity assays and live/dead analysis. In conclusion, sclareol was
shown to inhibit the production of S. aureus alpha-hemolysin. Sclareol has potential for
development as a new agent to treat S. aureus infections.

Keywords: Methicillin-resistant Staphylococcus aureus, virulence factor, sclareol, alpha-hemolysin

References

  1. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
    Pubmed CrossRef
  2. Barber M. 1961. Methicillin-resistant staphylococci. J. Clin. Pathol. 14: 385-393.
    Pubmed KoreaMed CrossRef
  3. Boyle-Vavra S, Daum RS. 2007. Community-acquired methicillin-resistant Staphylococcus aureus: the role of PantonValentine leukocidin. Lab. Invest. 87: 3-9.
    Pubmed CrossRef
  4. Nimmo GR. 2012. USA300 abroad: global spread of a virulent strain of community-associated methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 18: 725-734.
    Pubmed CrossRef
  5. van der Mee-Marquet NL. 2016. Whole-genome sequencing analysis, an essential tool for shedding light on the obscure evolution of Staphylococcus aureus USA300. J. Infect. Dis. 213:1362-1363.
    Pubmed CrossRef
  6. Rossolini GM, Arena F, Pecile P, Pollini S. 2014. Update on the antibiotic resistance crisis. Curr. Opin. Pharmacol. 18: 56-60.
    Pubmed CrossRef
  7. Montgomery CP, Boyle-Vavra S , Adem PV, L ee JC, H u sain AN, Clasen J, Daum RS. 2008. Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J. Infect. Dis. 198: 561-570.
    Pubmed CrossRef
  8. Montgomery CP, Boyle-Vavra S, Daum RS. 2010. Importance of the global regulators Agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection. PLoS One 5: e15177.
    Pubmed KoreaMed CrossRef
  9. Husmann M, Dersch K, Bobkiewicz W, Beckmann E, Veerachato G, Bhakdi S. 2006. Differential role of p38 mitogen activated protein kinase for cellular recovery from attack by pore-forming S. aureus alpha-toxin or streptolysin O. Biochem. Biophys. Res. Commun. 344: 1128-1134.
    Pubmed CrossRef
  10. Berube BJ, Bubeck Wardenburg J. 2013. Staphylococcus aureus alpha-toxin: nearly a century of intrigue. Toxins (Basel) 5:1140-1166.
    KoreaMed CrossRef
  11. Dong J, Qiu J, Wang J, Li H, Dai X, Zhang Y, et al. 2013. Apigenin alleviates the symptoms of Staphylococcus aureus pneumonia by inhibiting the production of alpha-hemolysin. FEMS Microbiol. Lett. 338: 124-131.
    Pubmed CrossRef
  12. Qiu J, Luo M, Wang J, Dong J, Li H, Leng B, et al. 2011. Isoalantolactone protects against Staphylococcus aureus pneumonia. FEMS Microbiol. Lett. 324: 147-155.
    Pubmed CrossRef
  13. Qiu J, Xiang H, H u C, Wang Q , Dong J, Li H , et al. 2011. Subinhibitory concentrations of farrerol reduce alpha-toxin expression in Staphylococcus aureus. FEMS Microbiol Lett. 315:129-133.
    Pubmed CrossRef
  14. Wang D, Yu L, Xiang H, et al. 2008. Global transcriptional profiles of Staphylococcus aureus treated with berberine chloride. FEMS Microbiol. Lett. 279: 217-225.
    Pubmed CrossRef
  15. Miski M, Ulubelen A, Johansson C, Mabry TJ. 1983. Antibacterial activity studies of flavonoids from Salvia palaestina. J. Nat. Prod. 46: 874-875.
    Pubmed CrossRef
  16. Bhatia S, McGinty D, Letizia C, Api A. 2008. Fragrance material review on sclareol. Food Chem. Toxicol. 46: S270-S274.
    Pubmed CrossRef
  17. Dimas K, Kokkinopoulos D, Demetzos C, Vaos B, Marselos M, Malamas M, Tzavaras T. 1999. The effect of sclareol on growth and cell cycle progression of human leukemic cell lines. Leukemia Res. 23: 217-234.
    CrossRef
  18. CLSI. 2005. Performance standards for antimicrobial susceptiblity testing; fifteenth informational supplement (ISBN 1-56238-556-9). CLSI Document M100-S15. Clinical Laboratory Standards Institute, Wayne, PA, USA.
  19. Ou yang P , Chen J , Sun M, Y in Z , Lin J, F u H, et al. 2016. Imperatorin inhibits the expression of alpha-hemolysin in Staphylococcus aureus strain BAA-1717 (USA300). Antonie Van Leeuwenhoek 109: 915-922.
  20. Karginov VA, Nestorovich EM, Schmidtmann F, Robinson TM, Yohannes A, Fahmi NE, et al. 2007. Inhibition of S. aureus alpha-hemolysin and B. anthracis lethal toxin by betacyclodextrin derivatives. Bioorg. Med. Chem. 15: 5424-5431.
    Pubmed KoreaMed CrossRef
  21. Hirst RA, Yesilkaya H, Clitheroe E, Rutman A, Dufty N, Mitchell TJ, et al. 2002. Sensitivities of human monocytes and epithelial cells to pneumolysin are different. Infect. Immun. 70: 1017-1022.
    Pubmed KoreaMed CrossRef
  22. Bubeck Wardenburg J, Schneewind O. 2008. Vaccine protection against Staphylococcus aureus pneumonia. J. Exp. Med. 205:287-294.
    Pubmed KoreaMed CrossRef
  23. Liang X, Yan M, Ji Y. 2009. The H35A mutated alpha-toxin interferes with cytotoxicity of staphylococcal alpha-toxin. Infect. Immun. 77: 977-983.
    Pubmed KoreaMed CrossRef
  24. Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, et al. 2010. Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill. 15: 19694.
  25. Allen RC, Popat R, Diggle SP, Brown SP. 2014. Targeting virulence: can we make evolution-proof drugs? Nat. Rev. Microbiol. 12: 300-308.
    Pubmed CrossRef
  26. Defoirdt T. 2013. Antivirulence therapy for animal production:filling an arsenal with novel weapons for sustainable disease control. PLoS Pathog. 9: e1003603.
    Pubmed KoreaMed CrossRef
  27. Rasko DA, Sperandio V. 2010. Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9:117-128.
    Pubmed CrossRef
  28. Wang J, Qiu J, Tan W, Zhang Y, Wang H, Zhou X, et al. 2015. Fisetin inhibits Listeria monocytogenes virulence by interfering with the oligomerization of listeriolysin O. J. Infect. Dis. 211: 1376-1387.
    Pubmed CrossRef
  29. Li H, Chen Y, Zhang B, Niu X, Song M, Luo Z, et al. 2016. Inhibition of sortase A by chalcone prevents Listeria monocytogenes infection. Biochem. Pharmacol. 106: 19-29.
    Pubmed CrossRef
  30. Adhikari RP, Ajao AO, Aman MJ, Karauzum H, Sarwar J, Lydecker AD, et al. 2012. Lower antibody levels to Staphylococcus aureus exotoxins are associated with sepsis in hospitalized adults with invasive S. aureus infections. J. Infect. Dis. 206: 915-923.
    Pubmed CrossRef
  31. Fritz SA, Tiemann KM, Hogan PG, Epplin EK, Rodriguez M, Al-Zubeidi DN, et al. 2013. A serologic correlate of protective immunity against community-onset Staphylococcus aureus infection. Clin. Infect. Dis. 56: 1554-1561.
    Pubmed KoreaMed CrossRef
  32. Kolata J, Bode LG, Holtfreter S, Steil L, Kusch H, Holtfreter B, et al. 2011. Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 11: 3914-3927.
    Pubmed CrossRef
  33. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O. 2007. Poring over pores: alpha-hemolysin and PantonValentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13: 1405-1406.
    Pubmed CrossRef
  34. Rau ch S , DeDent AC, K im H K, Bubeck Wardenburg J, Missiakas DM, Schneewind O. 2012. Abscess formation and alpha-hemolysin induced toxicity in a mouse model of Staphylococcus aureus peritoneal infection. Infect. Immun. 80:3721-3732.
    Pubmed KoreaMed CrossRef
  35. Kennedy AD, Bubeck Wardenburg J, Gardner DJ, Long D, Whitney AR, Braughton KR, et al. 2010. Targeting of alphahemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J. Infect. Dis. 202: 1050-1058.
    Pubmed KoreaMed CrossRef
  36. Novick RP, Ross H, Projan S, Kornblum J, Kreiswirth B, Moghazeh S. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12: 3967-3975.
    Pubmed KoreaMed
  37. Peng H, Novick R, Kreiswirth B, Kornblum J, Schlievert P. 1988. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170: 4365-4372.
    Pubmed KoreaMed CrossRef
  38. Ohlsen K, Ziebuhr W, Koller K-P, Hell W, Wichelhaus TA, 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.
    Pubmed KoreaMed
  39. Worlitzsch D, Kaygin H, Steinhuber A, Dalhoff A, Botzenhart K, Döring G. 2001. Effects of amoxicillin, gentamicin, and moxifloxacin on the hemolytic activity of Staphylococcus aureus in vitro and in vivo. Antimicrob. Agents Chemother. 45:196-202.
    Pubmed KoreaMed CrossRef