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Research article

References

  1. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
    CrossRef
  2. Cho YS, Kim SK, Ahn CB, Je JY. 2011. Preparation, characterization, and antioxidant properties of gallic acidgraftedchitosans. Carbohydr. Polym. 83: 1617-1622.
    CrossRef
  3. De Lencastre H, Wu SW, Pinho MG, Ludovice AM, Filipe S, Gardete S, et al. 1999. Antibiotic resistance as a stress response:complete sequencing of a large number of chromosomal loci in Staphylococcus aureus strain COL that impact on the expression of resistance to methicillin. Microb. Drug Resist. 5:163-175.
    Pubmed CrossRef
  4. Dutton EK, Ottum SA, Bolken TC, Franke CA, Hruby DE. 2000. Expression of active monomeric and dimeric nuclease A from the gram positive Streptococcus gordonii surface protein expression system. Protein Expr. Purif. 19: 158-172.
    Pubmed CrossRef
  5. Eom SH, Lee DS, Jung YJ, Park JH, Choi JI, Yim MJ, et al. 2014. The mechanism of antibacterial activity of phlorofucofuroeckolA against methicillin-resistant Staphylococcus aureus. Appl. Microbiol. Biotechnol. 98: 9795-9804.
    Pubmed CrossRef
  6. Foster TJ. 2004. The Staphylococcus aureus “superbug”. J. Clin. Invest. 114: 1693-1696.
    Pubmed PMC CrossRef
  7. Gould FK, Brindle R, Chadwick PR, Fraise AP, Hill S, Nathwani D, et al. 2009. Guidelines (2008) for the prophylaxis and treatment of methicillin-resistant Staphylococcus aureus (MRSA) infections in the United Kingdom. J. Antimicrob. Chemother. 63: 849-861
    Pubmed CrossRef
  8. Lemaire S, Van Bambeke F, Mingeot-Leclercq MP, Glupczynski Y, Tulkens PM. 2007. Role of acidic pH in the susceptibility of intraphagocytic methicillin-resistant Staphylococcus aureus strains to meropenem and cloxacillin. Antimicrob. Agents Chemother. 51: 1627-1632
    Pubmed PMC CrossRef
  9. Kateete DP, Kimani CN, Katabazi FA, Okeng A, Okee MS, Nanteza A, et al. 2010. Identification of Staphylococcus aureus:DNase and mannitol salt agar improve the efficiency of the tube coagulase test. Ann. Clin. Microbiol. Antimicrob. 9: 1-7.
    Pubmed PMC CrossRef
  10. Lee DS, Eom SH, Kim YM, Kim HS, Yin MJ, Lee SH, et al. 2014. Antibacterial and synergic effects of gallic acid-graftedchitosan with β-lactams against methicillin-resistant Staphylococcus aureus (MRSA). Can. J. Microbiol. 60: 629-638.
    Pubmed CrossRef
  11. Lee DS, Je JY. 2013. Gallic acid-grafted-chitosan inhibits foodborne pathogens by a membrane damage mechanism. J . Agric. Food Chem. 61: 6574-6579.
    Pubmed CrossRef
  12. 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
    CrossRef
  13. Lee DS, Woo JY, Ahn CB, Je JY. 2014. Chitosanhydroxycinnamic acid conjugates: preparation, antioxidant and antimicrobial activity. Food Chem. 148: 97-104.
    Pubmed CrossRef
  14. Lee JW, Ji YJ, Lee SO, Lee IS. 2007. Effect of Saliva miltiorrhiza bunge on antimicrobial activity and resistant gene regulation against methicillin-resistant Staphylococcus aureus (MRSA). J. Microbiol. 45: 350-357.
    Pubmed
  15. Norden CW, Wentzel H, Keleti E. 1979. Comparison of techniques for measurement of in vitro antibiotic synergism. J. Infect. Dis. 140: 629-633.
    Pubmed CrossRef
  16. Nshimiyumukiza O, Kang SK, Kim HJ, Lee EH, Han HN, Kim Y, et al. 2015. Synergistic antibacterial activity of Ecklonia cava (Phaeophyceae: Laminariales) against Listeria monocytogenes (Bacillales: Listeriaceae). Fish. Aquat. Sci. 18: 1-6.
    CrossRef
  17. Olajuyigbe OO, Coopoosamy RM. 2014. Influence of firstline antibiotics on the antibacterial activities of acetone stem bark extract of Acacia mearnsii de Wild against drugresistant bacterial isolates. Evid. Based Complement. Alternat. Med. 2014: 423751.
    Pubmed PMC CrossRef
  18. Rebollo-Pérez J, Ordoñez-Tapia C, Herazo-Herazo C, ReyesRamos N. 2011. Nasal carriage of Panton Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus in healthy preschool children. Rev. Salud Pública 13: 824-832.
    CrossRef
  19. Sambrook J, Russell DW. 1989. Molecular Cloning: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  20. Vouillamoz J, Entenza JM, Hohl P, Moreillon P. 2004. LB11058, a new cephalosporin with high penicillin-binding protein 2a affinity and activity in experimental endocarditis due to homogeneously methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 48: 4322-4327.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(4): 784-789

Published online April 28, 2016 https://doi.org/10.4014/jmb.1511.11046

Copyright © The Korean Society for Microbiology and Biotechnology.

Synergistic Antibacterial Effect and Antibacterial Action Mode of Chitosan-Ferulic Acid Conjugate against Methicillin-Resistant Staphylococcus aureus

Sung-Hwan Eom 1, Shin-Kook Kang 2, Dae-Sung Lee 3, Jeong-In Myeong 4, Jinhwan Lee 4, Hyun-Woo Kim 5, Kyoung-Ho Kim 6, Jae-Young Je 7, Won-Kyo Jung 8, 9 and Young-Mog Kim 2, 9*

1Korea Food Research Institute, Sungnam 13539, Republic of Korea, 2Department of Food Science and Technology, Pukyong National University, Busan 48513, Republic of Korea, 3National Marine Biodiversity Institute of Korea, Seocheon 33662, Republic of Korea, 4Aquaculture Management Division, National Institute of Fisheries Science, Busan 46083, Republic of Korea, 5Department of Marine Biology, Pukyong National University, Busan 48513, Republic of Korea, 6Department of Microbiology, Pukyong National University, Busan 48513, Republic of Korea, 7Department of Marine-Bio Convergence Science, Pukyong National University, Busan 48513, Republic of Korea, 8Department of Biomedical Engineering, Pukyong National University, Busan 48513, Republic of Korea, 9Marine-Integrated Bionics Research Center, Pukyong National University, Busan 48513, Republic of Korea

Received: November 17, 2015; Accepted: December 30, 2015

Abstract

We evaluated the synergistic antibacterial effect in combination with the chitosan-ferulic acid
conjugate (CFA) and β-lactam antibiotics, such as ampicillin, penicillin, and oxacillin, against
methicillin-resistant Staphylococcus aureus (MRSA) using fractional inhibitory concentration
(FIC) indices. CFA clearly reversed the antibacterial activity of ampicillin, penicillin, and
oxacillin against MRSA in the combination mode. Among these antibiotics, the combination of
oxacillin-CFA resulted in a ΣFICmin range of 0.250 and ΣFICmax of 0.563, suggesting that the
oxacillin-CFA combination resulted in an antibacterial synergy effect against MRSA. In
addition, we determined that CFA inhibited the mRNA expression of gene mecA and the
production of PBP2a, which is a key determinant for β-lactam antibiotic resistance, in a dosedependent manner. Thus, the results obtained in this study supported the idea on the
antibacterial action mechanism that oxacillin will restore the antibacterial activity against
MRSA through the suppression of PBP2a production by CFA.

Keywords: Antibacterial activity, chitosan-ferulic acid conjugate, fractional inhibitory concentration, mecA gene, methicillin-resistant Staphylococcus aureus, synergy effect

References

  1. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
    CrossRef
  2. Cho YS, Kim SK, Ahn CB, Je JY. 2011. Preparation, characterization, and antioxidant properties of gallic acidgraftedchitosans. Carbohydr. Polym. 83: 1617-1622.
    CrossRef
  3. De Lencastre H, Wu SW, Pinho MG, Ludovice AM, Filipe S, Gardete S, et al. 1999. Antibiotic resistance as a stress response:complete sequencing of a large number of chromosomal loci in Staphylococcus aureus strain COL that impact on the expression of resistance to methicillin. Microb. Drug Resist. 5:163-175.
    Pubmed CrossRef
  4. Dutton EK, Ottum SA, Bolken TC, Franke CA, Hruby DE. 2000. Expression of active monomeric and dimeric nuclease A from the gram positive Streptococcus gordonii surface protein expression system. Protein Expr. Purif. 19: 158-172.
    Pubmed CrossRef
  5. Eom SH, Lee DS, Jung YJ, Park JH, Choi JI, Yim MJ, et al. 2014. The mechanism of antibacterial activity of phlorofucofuroeckolA against methicillin-resistant Staphylococcus aureus. Appl. Microbiol. Biotechnol. 98: 9795-9804.
    Pubmed CrossRef
  6. Foster TJ. 2004. The Staphylococcus aureus “superbug”. J. Clin. Invest. 114: 1693-1696.
    Pubmed KoreaMed CrossRef
  7. Gould FK, Brindle R, Chadwick PR, Fraise AP, Hill S, Nathwani D, et al. 2009. Guidelines (2008) for the prophylaxis and treatment of methicillin-resistant Staphylococcus aureus (MRSA) infections in the United Kingdom. J. Antimicrob. Chemother. 63: 849-861
    Pubmed CrossRef
  8. Lemaire S, Van Bambeke F, Mingeot-Leclercq MP, Glupczynski Y, Tulkens PM. 2007. Role of acidic pH in the susceptibility of intraphagocytic methicillin-resistant Staphylococcus aureus strains to meropenem and cloxacillin. Antimicrob. Agents Chemother. 51: 1627-1632
    Pubmed KoreaMed CrossRef
  9. Kateete DP, Kimani CN, Katabazi FA, Okeng A, Okee MS, Nanteza A, et al. 2010. Identification of Staphylococcus aureus:DNase and mannitol salt agar improve the efficiency of the tube coagulase test. Ann. Clin. Microbiol. Antimicrob. 9: 1-7.
    Pubmed KoreaMed CrossRef
  10. Lee DS, Eom SH, Kim YM, Kim HS, Yin MJ, Lee SH, et al. 2014. Antibacterial and synergic effects of gallic acid-graftedchitosan with β-lactams against methicillin-resistant Staphylococcus aureus (MRSA). Can. J. Microbiol. 60: 629-638.
    Pubmed CrossRef
  11. Lee DS, Je JY. 2013. Gallic acid-grafted-chitosan inhibits foodborne pathogens by a membrane damage mechanism. J . Agric. Food Chem. 61: 6574-6579.
    Pubmed CrossRef
  12. 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
    CrossRef
  13. Lee DS, Woo JY, Ahn CB, Je JY. 2014. Chitosanhydroxycinnamic acid conjugates: preparation, antioxidant and antimicrobial activity. Food Chem. 148: 97-104.
    Pubmed CrossRef
  14. Lee JW, Ji YJ, Lee SO, Lee IS. 2007. Effect of Saliva miltiorrhiza bunge on antimicrobial activity and resistant gene regulation against methicillin-resistant Staphylococcus aureus (MRSA). J. Microbiol. 45: 350-357.
    Pubmed
  15. Norden CW, Wentzel H, Keleti E. 1979. Comparison of techniques for measurement of in vitro antibiotic synergism. J. Infect. Dis. 140: 629-633.
    Pubmed CrossRef
  16. Nshimiyumukiza O, Kang SK, Kim HJ, Lee EH, Han HN, Kim Y, et al. 2015. Synergistic antibacterial activity of Ecklonia cava (Phaeophyceae: Laminariales) against Listeria monocytogenes (Bacillales: Listeriaceae). Fish. Aquat. Sci. 18: 1-6.
    CrossRef
  17. Olajuyigbe OO, Coopoosamy RM. 2014. Influence of firstline antibiotics on the antibacterial activities of acetone stem bark extract of Acacia mearnsii de Wild against drugresistant bacterial isolates. Evid. Based Complement. Alternat. Med. 2014: 423751.
    Pubmed KoreaMed CrossRef
  18. Rebollo-Pérez J, Ordoñez-Tapia C, Herazo-Herazo C, ReyesRamos N. 2011. Nasal carriage of Panton Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus in healthy preschool children. Rev. Salud Pública 13: 824-832.
    CrossRef
  19. Sambrook J, Russell DW. 1989. Molecular Cloning: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  20. Vouillamoz J, Entenza JM, Hohl P, Moreillon P. 2004. LB11058, a new cephalosporin with high penicillin-binding protein 2a affinity and activity in experimental endocarditis due to homogeneously methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 48: 4322-4327.
    Pubmed KoreaMed CrossRef