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Inhibitory Effects of Streptomyces sp. MBTH32 Metabolites on Sortase A and Sortase A-Mediated Cell Clumping of Staphylococcus aureus to Fibrinogen

  • Chung, Beomkoo (Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University) ;
  • Kwon, Oh-Seok (Natural Products Research Institute, College of Pharmacy, Seoul National University) ;
  • Shin, Jongheon (Natural Products Research Institute, College of Pharmacy, Seoul National University) ;
  • Oh, Ki-Bong (Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University)
  • Received : 2019.06.13
  • Accepted : 2019.08.28
  • Published : 2019.10.28

Abstract

Sortase A (SrtA), a type of transpeptidase responsible for anchoring surface proteins to the peptidoglycan cell wall, is important in the virulence of gram-positive bacteria. Three compounds were isolated from marine-derived Streptomyces sp. MBTH32 using various chromatography techniques. The structures of these compounds were determined based on spectroscopic data and comparisons with previously reported data. Among the metabolites tested, lumichrome showed strong inhibitory activity against Staphylococcus aureus SrtA without affecting cell viability. The results of cell clumping activity assessment suggest the potential for using this compound to treat S. aureus infection by inhibiting SrtA activity.

Keywords

References

  1. Tortorella E, Tedesco P, Palma Esposito F, January G, Fani R, Jaspars M, et al. 2018. Antibiotics from deep-sea microorganisms: current discoveries and perspectives. Mar. Drugs 16: pii: E355.
  2. Tyler PA. 2003. Ecosystems of the deep oceans, pp. 1-4. 1st Ed. Elsevier Science, Amsterdam.
  3. Wright PC, Westacott RE, Burja AM. 2003. Piezotolerance as a metabolic engineering tool for the biosynthesis of natural products. Biomol. Eng. 20: 325-331. https://doi.org/10.1016/S1389-0344(03)00042-X
  4. Bull AT, Ward AC, Goodfellow M. 2000. Search and discovery strategies for biotechnology: the paradigm shift. Microbiol. Mol. Biol. Rev. 64: 573-606. https://doi.org/10.1128/MMBR.64.3.573-606.2000
  5. Blunt JW, Carroll AR, Copp BR, Davis RA, Keyzers RA, Prinsep MR. 2018. Marine natural products. Nat. Prod. Rep. 35: 8-53. https://doi.org/10.1039/C7NP00052A
  6. Brana AF, Sarmiento-Vizcaino A, Perez-Victoria I, Otero L, Fernandez J, Palacios JJ, et al. 2017. Branimycins B and C, antibiotics produced by the abyssal actinobacterium Pseudonocardia carboxydivorans M-227. J. Nat. Prod. 80: 569-573. https://doi.org/10.1021/acs.jnatprod.6b01107
  7. Le TC, Yang I, Yoon YJ, Nam SJ, Fenical W. 2016. Ansalactams B-D illustrate further biosynthetic plasticity within the ansamycin pathway. Org. Lett. 18: 2256-2259. https://doi.org/10.1021/acs.orglett.6b00892
  8. Song Y, Li Q, Liu X, Chen Y, Zhang Y, Sun A, et al. 2014. Cyclic hexapeptides from the deep South China Sea-derived Streptomyces scopuliridis SCSIO ZJ46 active against pathogenic gram-positive bacteria. J. Nat. Prod. 77: 1937-1941. https://doi.org/10.1021/np500399v
  9. Pan HQ, Zhang SY, Wang N, Li ZL, Hua HM, Hu JC, et al. 2013. New spirotetronate antibiotics, lobophorins H and I, from a South China Sea-derived Streptomyces sp. 12A 35. Mar. Drugs 11: 3891-3901. https://doi.org/10.3390/md11103891
  10. Cossart P, Jonquieres R. 2000. Sortase, a universal target for therapeutic agents against Gram-positive bacteria? Proc. Natl. Acad. Sci. USA 97: 5013-5015. https://doi.org/10.1073/pnas.97.10.5013
  11. Mazmanian SK, Liu G, Jensen ER, Lenoy E, Schneewind O. 2000. Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc. Natl. Acad. Sci. USA 97: 5510-5515. https://doi.org/10.1073/pnas.080520697
  12. Wesson CA, Liou LE, Todd KM, Bohach GA, Trumble WR, Bayles KW. 1998. Staphylococcus aureus A gr a nd S ar g lobal regulators influence internalization and induction of apoptosis. Infect. Immun. 66: 5238-5243. https://doi.org/10.1128/IAI.66.11.5238-5243.1998
  13. Mazmanian SK, Ton-That H, Su K, Schneewind O. 2002. An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc. Natl. Acad. Sci. USA 99: 2293-2298. https://doi.org/10.1073/pnas.032523999
  14. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, et al. 2003. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909. https://doi.org/10.1126/science.1081147
  15. Frankel BA, Bentley M, Kruger RG, McCafferty DG. 2004. Vinyl sulfones: inhibitors of SrtA, a transpeptidase required for cell wall protein anchoring and virulence in Staphylococcus aureus. J. Am. Chem. Soc. 126: 3404-3405. https://doi.org/10.1021/ja0390294
  16. Sibbald MJ, Yang XM, Tsompanidou E, Qu D, Hecker M, Becher D, et al. 2012. Partially overlapping substrate specificities of staphylococcal group A sortases. Proteomics 12: 3049-3062. https://doi.org/10.1002/pmic.201200144
  17. Cascioferro S, Raffa D, Maggio B, Raimondi MV, Schillaci D, Daidone G. 2015. Sortase A inhibitors: recent advances and future perspectives. J. Med. Chem. 58: 9108-9123. https://doi.org/10.1021/acs.jmedchem.5b00779
  18. Kang H, Jensen PR, Fenical W. 1996. Isolation of microbial antibiotics from a marine ascidian of the genus Didemnum. J. Org. Chem. 61: 1543-1546. https://doi.org/10.1021/jo951794g
  19. Martinez-Luis S, Gomez JF, Spadafora C, Guzman HM, Gutierrez M. 2012. Antitrypanosomal alkaloids from the marine bacterium Bacillus pumilus. Molecules 17: 11146-11155. https://doi.org/10.3390/molecules170911146
  20. Andrioli WJ, Lopes AA, Cavalcanti BC, Pessoa C, Nanayakkara NPD, Bastos JK. 2017. Isolation and characterization of 2-pyridone alkaloids and alloxazines from Beauveria bassiana. Nat. Prod. Res. 31: 1920-1929. https://doi.org/10.1080/14786419.2016.1269091
  21. Lee KY, Shin DS, Yoon JM, Kang HJ, Oh KB. 2002. Expression of sortase, a transpeptidase for cell wall sorting reaction, from Staphylococcus aureus ATCC 6538p in Escherichia coli. J. Microbiol. Biotechnol. 12: 530-533.
  22. Oh KB, Kim SH, Lee J, Cho WJ, Lee T, Kim S. 2004. Discovery of diarylacrylonitriles as a novel series of small molecule sortase A inhibitors. J. Med. Chem. 47: 2418-2421. https://doi.org/10.1021/jm0498708
  23. Hu P, Huang P, Chen WM. 2013. Curcumin inhibits the sortase Aactivity of the Streptococcus mutans UA 159. Appl. Biochem. Biotechnol. 171: 396-402. https://doi.org/10.1007/s12010-013-0378-9
  24. Kim SH, Shin DS, Oh MN, Chung SC, Lee JS, Oh KB. 2004. Inhibition of the bacterial surface protein anchoring transpeptidase sortase by isoquinoline alkaloids. Biosci. Biotechnol. Biochem. 68: 421-424. https://doi.org/10.1271/bbb.68.421
  25. Jonsson M, Mazmanian SK, Schneewind O, Bremell T, Tarkowski A. 2003. The role of Staphylococcus aureus sortase A and sortase B in murine arthritis. Microbes Infect. 5: 775-780. https://doi.org/10.1016/S1286-4579(03)00143-6
  26. Weinstein MP, Limbago B, Patel JB, Mathers AJ, Burnham C, Mazzulli T, et al. 2018. Methods for Dilution Antimicrobial Susceptibility Test for Bacteria That Grow aerobically, pp. 15-50. 11th Ed. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania.
  27. Lineweaver H, Burk D. 1934. The determination of enzyme dissociation constants. J. Am. Chem. Soc. 56: 658-666. https://doi.org/10.1021/ja01318a036
  28. Alksne LE, Projan SJ. 2000. Bacterial virulence as a target for antimicrobial chemotherapy. Curr. Opin. Biotechnol. 11: 625-636. https://doi.org/10.1016/S0958-1669(00)00155-5
  29. Zhang B, Teng Z, Li X, Lu G, Deng X, Niu X, Wang J. 2017. Chalcone attenuates Staphylococcus aureus virulence by targeting sortase A and alpha-hemolysin. Front. Microbiol. 8: 1715. https://doi.org/10.3389/fmicb.2017.01715
  30. Weiss WJ, Lenoy E, Murphy T, Tardio L, Burgio P, Projan SJ, et al. 2004. Effect of srtA and srtB gene expression on the virulence of Staphylococcus aureus in animal models of infection. J. Antimicrob. Chemother. 53: 480-486. https://doi.org/10.1093/jac/dkh078

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