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Synergistic Antibacterial Activity of an Active Compound Derived from Sedum takesimense against Methicillin-Resistant Staphylococcus aureus and Its Clinical Isolates

  • Jeong, Eun-Tak (DYNE SOZE Co., Ltd.) ;
  • Park, Seul-Ki (Institute of Food Science, Pukyong National University) ;
  • Jo, Du-Min (Department of Food Science and Technology, Pukyong National University) ;
  • Khan, Fazlurrahman (Research Center for Marine Integrated Bionics Technology, Pukyong National University) ;
  • Choi, Tae Ho (DYNE SOZE Co., Ltd.) ;
  • Yoon, Tae-Mi (DYNE SOZE Co., Ltd.) ;
  • Kim, Young-Mog (Department of Food Science and Technology, Pukyong National University)
  • Received : 2021.05.12
  • Accepted : 2021.07.19
  • Published : 2021.09.28

Abstract

There are a growing number of reports of hospital-acquired infections caused by pathogenic bacteria, especially methicillin-resistant Staphylococcus aureus (MRSA). Many plant products are now being used as a natural means of exploring antimicrobial agents against different types of human pathogenic bacteria. In this research, we sought to isolate and identify an active molecule from Sedum takesimense that has possible antibacterial activity against various clinical isolates of MRSA. NMR analysis revealed that the structure of the HPLC-purified compound was 1,2,4,6-tetra-O-galloyl-glucose. The minimum inhibitory concentration (MIC) of different extract fractions against numerous pathogenic bacteria was determined, and the actively purified compound has potent antibacterial activity against multidrug-resistant pathogenic bacteria, i.e., MRSA and its clinical isolates. In addition, the combination of the active compound and β-lactam antibiotics (e.g., oxacillin) demonstrated synergistic action against MRSA, with a fractional inhibitory concentration (FIC) index of 0.281. The current research revealed an alternative approach to combating pathogenesis caused by multi-drug resistant bacteria using plant materials. Furthermore, using a combination approach in which the active plant-derived compound is combined with antibiotics has proved to be a successful way of destroying pathogens synergistically.

Keywords

Acknowledgement

This research was financially supported by the Ministry of Small and Medium-sized Enterprises (SMEs) and Startups (MSS), Korea, under the "Regional Specialized Industry Development Plus Program (R&D, S2874391)" supervised by the Korea Institute for Advancement of Technology (KIAT). This work was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (NRF-2019R1A2C1087156 and 2021R1A6A1A03039211).

References

  1. Ventola CL. 2015. The antibiotic resistance crisis: part 1: causes and threats. Pharm. Ther. 40: 277-283.
  2. Center for Disease Control (CDC). Antibiotic Resistance Threats in the United States. http://www.cdc.gov/drugresistance/threatreport-2013/. Accesed Jan. 23, 2015.
  3. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG. 2015. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28: 603-661. https://doi.org/10.1128/CMR.00134-14
  4. Kaur DC, Chate SS. 2015. Study of antibiotic resistance pattern in methicillin resistant Staphylococcus aureus with special reference to newer antibiotic. J. Glob. Infect. Dis. 7: 78-84. https://doi.org/10.4103/0974-777X.157245
  5. French GL. 2010. The continuing crisis in antibiotic resistance. Int. J. Antimicrob. Agents 36: S3-S7. https://doi.org/10.1016/S0924-8579(10)70003-0
  6. Pai V, Rao VI, Rao SP. 2010. Prevalence and antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus [MRSA] isolates at a tertiary care hospital in Mangalore, South India. J. Lab. Physicians 2: 82-84. https://doi.org/10.4103/0974-2727.72155
  7. Okwu MU, Olley M, Akpoka AO, Izevbuwa OE. 2019. Methicillin-resistant Staphylococcus aureus (MRSA) and anti-MRSA activities of extracts of some medicinal plants: a brief review. AIMS Microbiol. 5: 117-137. https://doi.org/10.3934/microbiol.2019.2.117
  8. Compean KL, Ynalvez RA. 2014. Antimicrobial activity of plant secondary metabolites: a review. Res. J. Med. Plant. 8: 204-213. https://doi.org/10.3923/rjmp.2014.204.213
  9. Sato M, Tanaka H, Yamaguchi R, Kato K, Etoh H. 2004. Synergistic effects of mupirocin and an isoflavanone isolated from Erythrina variegata on growth and recovery of methicillin-resistant Staphylococcus aureus. Int. J. Antimicrob. Agents 24: 241-246. https://doi.org/10.1016/j.ijantimicag.2004.03.020
  10. Choi JG, Kang OH, Brice OO, Lee YS, Chae HS, Oh YC, et al. 2010. Antibacterial activity of Ecklonia cava against methicillin-resistant Staphylococcus aureus and Salmonella spp. Foodborne Pathog. Dis. 7: 435-441. https://doi.org/10.1089/fpd.2009.0434
  11. Aqil F, Khan MSA, Owais M, Ahmad I. 2005. Effect of certain bioactive plant extracts on clinical isolates of β-lactamase producing methicillin resistant Staphylococcus aureus. J. Basic. Microbiol. 45: 106-114. https://doi.org/10.1002/jobm.200410355
  12. Aqil F, Ahmad I, Owais M. 2006. Evaluation of anti-methicillin-resistant Staphylococcus aureus (MRSA) activity and synergy of some bioactive plant extracts. Biotechnol. J. 1: 1093-1102. https://doi.org/10.1002/biot.200600130
  13. Cha JD, Lee JH, Choi KM, Choi SM, Park JH. 2014. Synergistic effect between cryptotanshinone and antibiotics against clinic methicillin and vancomycin-resistant Staphylococcus aureus. Evid. Based Complement. Alternat. Med. 2014: 450572.
  14. Yoon MY, Choi GJ, Choi YH, Jang KS, Park MS, Cha B, et al. 2010. Effect of polyacetylenic acids from Prunella vulgaris on various plant pathogens. Lett. Appl. Microbiol. 51: 511-517. https://doi.org/10.1111/j.1472-765X.2010.02922.x
  15. Yoon MY, Choi NH, Min BS, Choi GJ, Choi YH, Jang KS, et al. 2011. Potent in vivo antifungal activity against powdery mildews of pregnane glycosides from the roots of Cynanchum wilfordii. J. Agric. Food. Chem. 59: 12210-12216. https://doi.org/10.1021/jf2039185
  16. Gangadhar M, Bhavana P, Sunil Y, Datta S. 2011. Isolation and characterisation of gallic acid from Terminalia bellerica and its effect on carbohydrate regulatory system in vitro. Int. J. Res. Ayurveda. Pharm. 2: 559-562.
  17. Hisham DMN, Lip JM, Noh JM, Normah A, Nabilah MN. 2011. Identification and isolation of methyl gallate as a polar chemical marker for Labisia pumila Benth. J. Trop. Agric. Food. Sci. 39: 279-284.
  18. Tanaka T, Nonaka GI, Nishioka I. 1983. 7-O-Galloyl-(+)-catechin and 3-O-galloylprocyanidin B-3 from Sanguisorba officinalis. Phytochemistry 22: 2575-2578. https://doi.org/10.1016/0031-9422(83)80168-X
  19. Tanaka T, Nonaka GI, Nishioka I. 1985. Punicafolin, an ellagitannin from the leaves of Punica grantum. Phytochemistry 24: 2075-2078. https://doi.org/10.1016/S0031-9422(00)83125-8
  20. Thuong PT, Kang JH, Na KM, Jin YW, Youn JU, Seong HY, et al. 2007. Anti-oxidant constituents from Sedum takesimense. Phytochemistry 68: 2432-2438. https://doi.org/10.1016/j.phytochem.2007.05.031
  21. Wang KJ, Yang CR, Zhang YJ. 2007. Phenolic antioxidants from Chinese toon (fresh young leaves and shoots of Toona sinensis). Food Chem. 101: 365-371. https://doi.org/10.1016/j.foodchem.2006.01.044
  22. Xin-Min C, Yoshida T, Hatano T, Fukushima M, Okuda T. 1987. Galloylarbutin and other polyphenols from Bergenia purpurascens. Phytochemistry 26: 515-517. https://doi.org/10.1016/S0031-9422(00)81446-6
  23. Yang CM, Cheng HY, Lin TC, Chinag LC, Lin CC. 2007. The in vitro activity of geraniin and 1,3,4,6-tetra-O-galloyl-β-D-flucose isolated from Phyllanthus urinaria against herpes simplex virus type 1 and type 2 infection. J. Ethnopharmacol. 110: 555-558. https://doi.org/10.1016/j.jep.2006.09.039
  24. Yuan GQ, Li QQ, Qin J. 2012. Isolation of methyl gallate from Toxicodendron sylvestre and its effect on tomato bacterial wilt. Plant Dis. 96: 1143-1147 https://doi.org/10.1094/pdis-03-11-0150-re
  25. Dickson RA, Houghton PJ, Hyhinds PJ, Gibbon S. 2006. Antimicrobial, resistance-modifying effects, antioxidant and free radical scavenging activities of Mezoneuron benthamianum Bail., Securinega virosa Roxb. and Wlld. and Microglossa pyrifolia Lam. Phytother. Res. 20: 41-45. https://doi.org/10.1002/ptr.1799
  26. Wikler MA. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard. CLSI (NCCLS). 26: M7-A9.
  27. Norden CW, Wentzel H, Keleti E. 1979. Comparison of techniques for measurement of in vitro antibiotic synergism. J. Infect. Dis. 140: 629-633. https://doi.org/10.1093/infdis/140.4.629
  28. Yu HH, Kim KJ, Cha JD, Kim HK, Lee YE, Choi NY, et al. 2005. Antimicrobial activity of berberine alone and in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. J. Med. Food. 8: 454-461. https://doi.org/10.1089/jmf.2005.8.454
  29. Vu TT, Kim JC, Choi YH, Choi GJ, Jang KS, Choi TH, et al. 2013. Effect of gallotannins derived from Sedum takesimense on tomato bacterial wilt. Plant Dis. 97: 1593-1598. https://doi.org/10.1094/pdis-04-13-0350-re
  30. Odontuya, G. 2016. Anti-oxidative, acetylcholinesterase and pancreatic lipase inhibitory activities of compounds from Dasiphora fruticosa Myricaria alopecuroides and Sedum hybridum. Mong. J. Chem. 17: 42-49. https://doi.org/10.5564/mjc.v17i43.746
  31. Bensouici C, Kabouche A, Karioti A, Ozturk M, Duru ME, Bilia AR, et al. 2016. Compounds from Sedum caeruleum with antioxidant, anticholinesterase, and antibacterial activities. Pharm. Biol. 54: 174-179. https://doi.org/10.3109/13880209.2015.1028078
  32. Lee DS, Kang MS, Hwang HJ, Eom SH, Yang JY, Lee MS, et al. 2008. Synergistic effect between dieckol from Ecklonia stolonifera and β-lactams against methicillin-resistant Staphylococcus aureus. Biotechnol. Bioprocess. Eng. 13: 758-764. https://doi.org/10.1007/s12257-008-0162-9
  33. Lee DS, Eom SH, Kim YM, Kim HS, Yim MJ, Lee SH, et al. 2014. Antibacterial and synergic effects of gallic acid-grafted-chitosan with β-lactams against methicillin-resistant Staphylococcus aureus (MRSA). Can. J. Microbiol. 60: 629-638. https://doi.org/10.1139/cjm-2014-0286
  34. Cantoni LAMJ, Wenger A. Glauser MP, Bille J. 1989. Comparative efficacy of amoxicillin-clavulanate, cloxacillin, and vancomycin against methicillin-sensitive and methicillin-resistant Staphylococcus aureus endocarditis in rats. J. Infect. Dis. 159: 989-993. https://doi.org/10.1093/infdis/159.5.989
  35. Cote H, Pichette A, Simard F, Ouellette ME, Ripoll L, Mihoub M, et al. 2019. Balsacone C, a new antibiotic targeting bacterial cell membranes, inhibits clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA) without inducing resistance. Front. Microbiol. 10: 2341. https://doi.org/10.3389/fmicb.2019.02341