Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Anti-Biofilm Effects of Torilis japonica Ethanol Extracts Against Staphylococcus aureus

  • Kim, Geun-Seop (Department of Integrated Life Science and Technology, Kongju National University) ;
  • Park, Chae-Rin (Department of Companion and Laboratory Animal Science, Kongju National University) ;
  • Kim, Ji-Eun (Department of Companion and Laboratory Animal Science, Kongju National University) ;
  • Kim, Hong-Kook (Department of Integrated Life Science and Technology, Kongju National University) ;
  • Kim, Byeong-Soo (Department of Companion and Laboratory Animal Science, Kongju National University)
  • Received : 2021.07.29
  • Accepted : 2021.11.26
  • Published : 2022.02.28
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Abstract

The spread of antibiotic-resistant strains of Staphylococcus aureus, a gram-positive opportunistic pathogen, has increased due to the frequent use of antibiotics. Inhibition of the quorum-sensing systems of biofilm-producing strains using plant extracts represents an efficient approach for controlling infections. Torilis japonica is a medicinal herb showing various bioactivities; however, no studies have reported the anti-biofilm effects of T. japonica extracts against drug-resistant S. aureus. In this study, we evaluated the inhibitory effects of T. japonica ethanol extract (TJE) on biofilm production in methicillin-sensitive S. aureus (MSSA) KCTC 1927, methicillin-resistant S. aureus (MRSA) KCCM 40510, and MRSA KCCM 40511. Biofilm assays showed that TJE could inhibit biofilm formation in all strains. Furthermore, the hemolysis of sheep blood was found to be reduced when the strains were treated with TJE. The mRNA expression of agrA, sarA, icaA, hla, and RNAIII was evaluated using reverse transcription-polymerase chain reaction to determine the effect of TJE on the regulation of genes encoding quorum sensing-related virulence factors in MSSA and MRSA. The expression of hla reduced in a concentration-dependent manner upon treatment with TJE. Moreover, the expression levels of other genes were significantly reduced compared to those in the control group. In conclusion, TJE can suppress biofilm formation and virulence factor-related gene expression in MSSA and MRSA strains. The extract may therefore be used to develop treatments for infections caused by antibiotic-resistant S. aureus.

Keywords

Acknowledgement

This work was supported by a research grant provided by Kongju National University in 2020.

References

  1. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532. https://doi.org/10.1056/NEJM199808203390806
  2. Welte T, Kantecki M, Stone GG, Hammond, J. 2019. Ceftaroline fosamil as a potential treatment option for Staphylococcus aureus community-acquired pneumonia in adults. Int. J. Antimicrob. Agents. 54: 410-422. https://doi.org/10.1016/j.ijantimicag.2019.08.012
  3. Tomczak H, Wrobel J, Jenerowicz D, Sadowska-Przytocka A, Wachal M, Adamski Z, et al. 2019. The role of Staphylococcus aureus in atopic dermatitis: microbiological and immunological implications. Advances in Dermatology and Allergology/Postepy Dermatologii i Alergologii. 36: 485. https://doi.org/10.5114/ada.2018.77056
  4. Barber M. 1961. Methicillin-resistant staphylococci. J. Clin. Pathol. 14: 385-393. https://doi.org/10.1136/jcp.14.4.385
  5. Peacock Jr, James E, Marsik FJ, Wenzel RP. 1980. Methicillin-resistant Staphylococcus aureus: introduction and spread within a hospital. Ann. Intern. Med. 93: 526-532. https://doi.org/10.7326/0003-4819-93-4-526
  6. Rossetti S, D'Alessandro L, Pellegrino F, Carrasco MA. 2012. The effect of ketorolac on biofilm of Staphylococcus epidermidis isolated from post-cataract endophthalmitis. J. Ophthalmic. Inflamm. Infect. 2: 89-93. https://doi.org/10.1007/s12348-012-0070-1
  7. Novick RP, Geisinger E. 2008. Quorum sensing in staphylococci. Annu. Rev. Genet. 42: 541-564. https://doi.org/10.1146/annurev.genet.42.110807.091640
  8. Bryers JD. 2008. Medical biofilms. Biotechnol. Bioeng. 100: 1-18. https://doi.org/10.1002/bit.21838
  9. Yarwood JM, Schlievert, PM. 2003. Quorum sensing in Staphylococcus infections. J. Clin. Invest. 112: 1620-1625. https://doi.org/10.1172/jci20442
  10. Leid JG, Shirtliff ME, Costerton JW, Stoodley AP. 2002. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect. Immun. 70: 6339-6345. https://doi.org/10.1128/IAI.70.11.6339-6345.2002
  11. Kirmusaoglu S. 2016. Staphylococcal biofilms: pathogenicity, mechanism and regulation of biofilm formation by quorum-sensing system and antibiotic resistance mechanisms of biofilm-embedded microorganisms. pp. 189-209. Microbial Biofilms-Importance and Applications. Intech, Croatia.
  12. Kong KF, Vuong C, Otto M. 2006. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol. 296: 133-139. https://doi.org/10.1016/j.ijmm.2006.01.042
  13. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21: 319-346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
  14. Painter KL, Krishna A, Wigneshweraraj S, Edwards AM. 2014. What role does the quorum-sensing accessory gene regulator system play during Staphylococcus aureus bacteremia. Trends Microbiol. 22: 676-685. https://doi.org/10.1016/j.tim.2014.09.002
  15. Cheung GY, Wang R, Khan BA, Sturdevant DE, Otto M. 2011. Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect. Immun. 79: 1927-1935. https://doi.org/10.1128/IAI.00046-11
  16. Sheagren JN. 1984. Staphylococcus aureus: the persistent pathogen. N. Engl. J. Med. 310: 1437-1442. https://doi.org/10.1056/NEJM198405313102206
  17. Heinrichs JH, Bayer MG, Cheung AL. 1996. Characterization of the sar locus and its interaction with agr in Staphylococcus aureus. J. Bacteriol. 178: 418-423. https://doi.org/10.1128/jb.178.2.418-423.1996
  18. Queck SY, Jameson-Lee M, Villaruz AE, Bach THL, Khan BA, Sturdevant DE, et al. 2008. RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell. 32: 150-158. https://doi.org/10.1016/j.molcel.2008.08.005
  19. Koenig RL, Ray JL, Maleki SJ, Smeltzer MS, Hurlburt BK. 2004. Staphylococcus aureus AgrA binding to the RNAIII-agr regulatory region. J. Bacteriol. 186: 7549-7555. https://doi.org/10.1128/JB.186.22.7549-7555.2004
  20. Janzon L, Lofdahl S, Arvidson S. 1989. Identification and nucleotide sequence of the delta-lysin gene, hld, adjacent to the accessory gene regulator (agr) of Staphylococcus aureus. Mol. Gen. Genet. 219: 480-485. https://doi.org/10.1007/BF00259623
  21. Janzon L, Arvidson S. 1990. The role of the delta-lysin gene (hld) in the regulation of virulence genes by the accessory gene regulator (agr) in Staphylococcus aureus. EMBO J. 9: 1391-1399. https://doi.org/10.1002/j.1460-2075.1990.tb08254.x
  22. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67: 5427-5433. https://doi.org/10.1128/iai.67.10.5427-5433.1999
  23. Namvar AE, Asghari B, Ezzatifar F, Azizi G, Lari AR. 2013. Detection of the intercellular adhesion gene cluster (ica) in clinical Staphylococcus aureus isolates. GMS. Hyg. Infect. Control. 8: Doc03.
  24. Chen Y, Liu T, Wang K, Hou C, Cai S, Huang Y, et al. 2016. Baicalein inhibits Staphylococcus aureus biofilm formation and the quorum sensing system in vitro. PLoS One 11: e0153468. https://doi.org/10.1371/journal.pone.0153468
  25. Wu SC, Liu F, Zhu K, Shen, JZ. 2019. Natural products that target virulence factors in antibiotic-resistant Staphylococcus aureus. J. Agric. Food. Chem. 67: 13195-13211. https://doi.org/10.1021/acs.jafc.9b05595
  26. Oh MS, Kim DR, Kang JW, Yu TW, Park JY, Kim DM, et al. 2005. Study on antioxidant potency of Cuscutae semen, Psoraleae fructus, Cnidii fructus and Epimedii herba by DPPH method. Herbal Formula Sci. 13: 101-110.
  27. Park GB, Kim EJ, Son YJ, Yoon DH, Sung GH, Aravinthan A, et al. 2017. Anti-inflammatory effect of torilidis fructus ethanol extract through inhibition of Src. Pharm. Biol. 55: 2074-2082 https://doi.org/10.1080/13880209.2017.1362011
  28. Nam GH, Wee JH, Kim SY, Baek JY, Kim YM. 2019. Inhibitory effect of the ethanol extract of Torilis Japonica decandolle on adipocyte differentiation in 3T3-L1 cells. J. Life Sci. 29: 1016-1022.
  29. Kim GS, Choe YH, Kim HK, Kim BS. 2018. Characteristics of lactic acid bacteria isolated from traditional wheat Nuruk and their effects on nitric oxide production in mouse nacrophage. Korean Soc. Biotechnol. Bioeng. J. 33: 192-199.
  30. Pitts B, Hamilton MA, Zelver N, Stewart PS. 2003. A microtiter-plate screening method for biofilm disinfection and removal. J. Microbiol. Methods 54: 269-276. https://doi.org/10.1016/S0167-7012(03)00034-4
  31. Larzabal M, Mercado EC, Vilte DA, Salazar-Gonzalez H, Cataldi A, Navarro-Garcia F. 2010. Designed coiled-coil peptides inhibit the type three secretion system of enteropathogenic Escherichia coli. PLoS One 5: e9046. https://doi.org/10.1371/journal.pone.0009046
  32. Stefanovic O, Stanojevic D, Comic L. 2009. Inhibitory effect of Torilis anthriscus on growth of microorganisms. Cent. Eur. J. Biol. 4: 493-498. https://doi.org/10.2478/s11535-009-0045-x
  33. Hong S, Kim O. 2013. The effects of Torilis fructus extracts against enteropathogenic Escherichia coli in Piglets. Korean J. Vet. Serv. 36: 283-289. https://doi.org/10.7853/KJVS.2013.36.4.283
  34. O'Gara JP. 2007. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 270: 179-188. https://doi.org/10.1111/j.1574-6968.2007.00688.x
  35. Stapleton PD, Taylor PW. 2002. Methicillin resistance in Staphylococcus aureus: mechanisms and modulation. Sci. Prog. 85: 57-72. https://doi.org/10.3184/003685002783238870
  36. Maree CL, Daum RS, Boyle-Vavra S, Matayoshi K, Miller LG. 2007. Community-associated methicillin-resistant Staphylococcus aureus isolates and healthcare-associated infections. Emerg. Infect. Dis. 13: 236. https://doi.org/10.3201/eid1302.060781
  37. Fitzgerald JR. 2012. Livestock-associated Staphylococcus aureus: origin, evolution and public health threat. Trends Microbiol. 20: 192-198. https://doi.org/10.1016/j.tim.2012.01.006
  38. Kaasch AJ, Barlow G, Edgeworth JD, Fowler Jr VG, Hellmich M, Hopkins S, et al. 2014. Staphylococcus aureus bloodstream infection: a pooled analysis of five prospective, observational studies J. Infect. 68: 242-251 https://doi.org/10.1016/j.jinf.2013.10.015
  39. Arciola, CR, Campoccia D, Ravaioli S, Montanaro L. 2015. Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Front. Cell. Infect. Microbiol. 5: 7. https://doi.org/10.3389/fcimb.2015.00007
  40. Lee JH, Park JH, Cho HS, Joo SW, Cho MH, Lee JT. 2013. Anti-biofilm activities of quercetin and tannic acid against Staphylococcus aureus. Biofouling 29: 491-499 https://doi.org/10.1080/08927014.2013.788692
  41. Ming D, Wang D, Cao F, Xiang H, Mu D, Cao J, et al. 2017. Kaempferol inhibits the primary attachment phase of biofilm formation in Staphylococcus aureus. Front. Microbiol. 8: 2263 https://doi.org/10.3389/fmicb.2017.02263
  42. Qian W, Liu M, Fu Y, Zhang J, Liu W, Li J, et al. 2020. Antibicrobial mechanism of luteolin against Staphylococcus aureus and Listeria monocytogenes and its antibiofilm properties. Microb. Pathog. 142: 104056 https://doi.org/10.1016/j.micpath.2020.104056
  43. Quave CL, Plano LR, Bennett BC. 2011. Quorum sensing inhibitors of Staphylococcus aureus from Italian medicinal plans. Planta Med. 77: 188-195. https://doi.org/10.1055/s-0030-1250145
  44. Kitajima J, Suzuki N, Ishikawa T, Tanaka Y. 1998. New hemiterpenoid pentol and monoterpenoid glycoside of Torilis japonica fruit and consideration of the origin of apiose. Chem. Pharm. Bull. 46: 1583-1586. https://doi.org/10.1248/cpb.46.1583
  45. Cho SI, Kang SS, Kim KR, Kim TH, Lee EB. 1999. Isolation of torilin from Torilis japonica fruit and its analgesic and anti-inflammatory activities. Korean J. Pharm. 30: 137-144.