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References

  1. Klein E, Smith DL, Laxminarayan R. 2007. Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005. Emerg. Infect. Dis 13: 1840-1846.
    Pubmed PMC CrossRef
  2. Levy SB, Marshall B. 2004. Antibacterial resistance worldwide:causes, challenges and responses. Nat. Med. 10: S122-S129.
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  8. Haydon DJ, Stokes NR, Ure R, Galbraith G, Bennett JM, Brown DR, et al. 2008. An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321: 1673-1675.
    Pubmed CrossRef
  9. Sun N, Chan FY, Lu YJ, Neves MA, Lui HK, Wang Y et al. 2014. Rational design of berberine-based FtsZ inhibitors with broad-spectrum antibacterial activity. PLoS One 9: e97514.
    Pubmed PMC CrossRef
  10. Wang J, Galgoci A, Kodali S, Herath KB, Jayasuriya H, Dorso K, et al. 2003. Discovery of a small molecule that inhibits cell division by blocking FtsZ, a novel therapeutic target of antibiotics. J. Biol. Chem 278: 44424-44428.
    Pubmed CrossRef
  11. Stokes NR, Sievers J, Barker S, Bennett JM, Brown DR, Collins I, et al. 2005. Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay. J. Biol. Chem. 280: 39709-39715.
    Pubmed CrossRef
  12. Domadia PN, Bhunia A, Sivaraman J, Swarup S, Dasgupta D. 2008. Berberine targets assembly of Escherichia coli c ell division protein FtsZ. Biochemistry 47: 3225-3234.
    Pubmed CrossRef
  13. Beuria TK, Santra MK, Panda D. 2005. Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling. Biochemistry 44: 16584-16593.
    Pubmed CrossRef
  14. Park YS, Grove CI, Gonzalez-Lopez M, Urgaonkar S, Fettinger JC, Shaw JT. 2011. Synthesis of (-)-viriditoxin: a 6,6’-binaphthopyran-2-one that targets the bacterial cell division protein FtsZ. Angew. Chem. Int. Ed. Engl. 50: 3730-3733.
    Pubmed PMC CrossRef
  15. Stokes NR, Baker N, Bennett JM, Berry J, Collins I, Czaplewski LG, et al. 2013. An improved small-molecule inhibitor of FtsZ with superior in vitro potency, drug-like properties, and in vivo efficacy. Antimicrob. Agents Chemother. 57: 317-325.
    Pubmed PMC CrossRef
  16. Fleck WF, Strauss DG, Meyer J, Porstendorfer G. 1978. Fermentation, isolation, and biological activity of maduramycin:a new antibiotic from Actinomadura rubra. Z. Allg. Mikrobiol. 18: 389-398.
    Pubmed CrossRef
  17. Marchand C, Beutler JA, Wamiru A, Budihas S, Mollmann U, Heinisch L et al. 2008. Madurahydroxylactone derivatives as dual inhibitors of human immunodeficiency virus type 1 integrase and RNase H. Antimicrob. Agents Chemother. 52: 361-364.
    Pubmed PMC CrossRef
  18. Heinisch L, Roemer E, Jutten P, Haas W, Werner W, Mollmann U. 1999. Semisynthetic derivatives of madura hydroxylactone and their antibacterial activities. J. Antibiot. (Tokyo) 52: 1029-1041.
    CrossRef
  19. Strauss DG, Baum M, Fleck WF. 1986. Butylmaduramycin, a new antibiotic from Actinomadura rubra. J. Basic Microbiol. 26: 169-172.
    Pubmed CrossRef
  20. Zheng CJ, Sohn MJ, Kim WG. 2009. Vinaxanthone, a new FabI inhibitor from Penicillium sp. J. Antimicrob. Chemother. 63: 949-953.
    Pubmed CrossRef

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Note

J. Microbiol. Biotechnol. 2017; 27(11): 1994-1998

Published online November 28, 2017 https://doi.org/10.4014/jmb.1708.08044

Copyright © The Korean Society for Microbiology and Biotechnology.

Madurahydroxylactone, an Inhibitor of Staphylococcus aureus FtsZ from Nonomuraea sp. AN100570

Bo-Min Kim 1, 2, Ha-Young Choi 1, Geon-Woo Kim 1, Chang-Ji Zheng 3, Young-Ho Kim 3 and Won-Gon Kim 1*

1Superbacteria Research Center, Korea Research Institute of Bioscience and Biotechnology, Yusong, Daejeon 34141, Republic of Korea, 2College of Pharmacy, Chungnam National University, Daejeon 34134, Republic of Korea, 3Key Laboratory of Natural Resources of Changbai Mountain & Functional Molecules, Ministry of Education, Yanbian University College of Pharmacy, Yanji 133002, P.R. China

Received: August 18, 2017; Accepted: September 6, 2017

Abstract

FtsZ, a bacterial cell-division protein, is an attractive antibacterial target. In the screening for
an inhibitor of Staphylococcus aureus FtsZ, madurahydroxylactone (1) and its related
derivatives 2-5 were isolated from Nonomuraea sp. AN100570. Compound 1 inhibited S. aureus
FtsZ with an IC50 of 53.4 μM and showed potent antibacterial activity against S. aureus and
MRSA with an MIC of 1 μg/ml, whereas 2-5 were weak or inactive. Importantly, 1 induced
cell elongation in the cell division phenotype assay, whereas 2-5 did not. It indicates that 1
exhibits its potent antibacterial activity via inhibition of FtsZ, and the hydroxyl group and
hydroxylactone ring of 1 are critical for the activity. Thus, madurahydroxylactone is a new
type of inhibitor of FtsZ.

Keywords: Madurahydroxylactone, FtsZ, inhibitor, Nonomuraea, antibacterial

References

  1. Klein E, Smith DL, Laxminarayan R. 2007. Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005. Emerg. Infect. Dis 13: 1840-1846.
    Pubmed KoreaMed CrossRef
  2. Levy SB, Marshall B. 2004. Antibacterial resistance worldwide:causes, challenges and responses. Nat. Med. 10: S122-S129.
    Pubmed CrossRef
  3. Brown ED, Wright GD. 2016. Antibacterial drug discovery in the resistance era. Nature 529: 336-343.
    Pubmed CrossRef
  4. Butler MS, Cooper MA. 2012. Screening strategies to identify new antibiotics. Curr. Drug Targets 13: 373-387.
    Pubmed CrossRef
  5. Lock RL, Harry EJ. 2008. Cell-division inhibitors: new insights for future antibiotics. Nat. Rev. Drug Discov. 7: 324-338.
    Pubmed CrossRef
  6. Vollmer W. 2006. The prokaryotic cytoskeleton: a putative target for inhibitors and antibiotic s? Appl. Microbiol. Biotechnol. 73: 37-47.
    Pubmed CrossRef
  7. Kapoor S, Panda D. 2009. Targeting FtsZ for antibacterial therapy: a promising avenue. Expert Opin. Ther. Targets 13: 1037-1051.
    Pubmed CrossRef
  8. Haydon DJ, Stokes NR, Ure R, Galbraith G, Bennett JM, Brown DR, et al. 2008. An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321: 1673-1675.
    Pubmed CrossRef
  9. Sun N, Chan FY, Lu YJ, Neves MA, Lui HK, Wang Y et al. 2014. Rational design of berberine-based FtsZ inhibitors with broad-spectrum antibacterial activity. PLoS One 9: e97514.
    Pubmed KoreaMed CrossRef
  10. Wang J, Galgoci A, Kodali S, Herath KB, Jayasuriya H, Dorso K, et al. 2003. Discovery of a small molecule that inhibits cell division by blocking FtsZ, a novel therapeutic target of antibiotics. J. Biol. Chem 278: 44424-44428.
    Pubmed CrossRef
  11. Stokes NR, Sievers J, Barker S, Bennett JM, Brown DR, Collins I, et al. 2005. Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay. J. Biol. Chem. 280: 39709-39715.
    Pubmed CrossRef
  12. Domadia PN, Bhunia A, Sivaraman J, Swarup S, Dasgupta D. 2008. Berberine targets assembly of Escherichia coli c ell division protein FtsZ. Biochemistry 47: 3225-3234.
    Pubmed CrossRef
  13. Beuria TK, Santra MK, Panda D. 2005. Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling. Biochemistry 44: 16584-16593.
    Pubmed CrossRef
  14. Park YS, Grove CI, Gonzalez-Lopez M, Urgaonkar S, Fettinger JC, Shaw JT. 2011. Synthesis of (-)-viriditoxin: a 6,6’-binaphthopyran-2-one that targets the bacterial cell division protein FtsZ. Angew. Chem. Int. Ed. Engl. 50: 3730-3733.
    Pubmed KoreaMed CrossRef
  15. Stokes NR, Baker N, Bennett JM, Berry J, Collins I, Czaplewski LG, et al. 2013. An improved small-molecule inhibitor of FtsZ with superior in vitro potency, drug-like properties, and in vivo efficacy. Antimicrob. Agents Chemother. 57: 317-325.
    Pubmed KoreaMed CrossRef
  16. Fleck WF, Strauss DG, Meyer J, Porstendorfer G. 1978. Fermentation, isolation, and biological activity of maduramycin:a new antibiotic from Actinomadura rubra. Z. Allg. Mikrobiol. 18: 389-398.
    Pubmed CrossRef
  17. Marchand C, Beutler JA, Wamiru A, Budihas S, Mollmann U, Heinisch L et al. 2008. Madurahydroxylactone derivatives as dual inhibitors of human immunodeficiency virus type 1 integrase and RNase H. Antimicrob. Agents Chemother. 52: 361-364.
    Pubmed KoreaMed CrossRef
  18. Heinisch L, Roemer E, Jutten P, Haas W, Werner W, Mollmann U. 1999. Semisynthetic derivatives of madura hydroxylactone and their antibacterial activities. J. Antibiot. (Tokyo) 52: 1029-1041.
    CrossRef
  19. Strauss DG, Baum M, Fleck WF. 1986. Butylmaduramycin, a new antibiotic from Actinomadura rubra. J. Basic Microbiol. 26: 169-172.
    Pubmed CrossRef
  20. Zheng CJ, Sohn MJ, Kim WG. 2009. Vinaxanthone, a new FabI inhibitor from Penicillium sp. J. Antimicrob. Chemother. 63: 949-953.
    Pubmed CrossRef