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Antimicrobial Peptides Encounter Resistance of Aureolysin during Their Action on Staphylococcus aureus Biofilm

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Abstract

Antimicrobial peptides (AMPs) are promising candidates as new anti-biofilm agents to cope with biofilm-related infections. To date, numerous studies have evaluated the efficacy of AMPs as anti-biofilm agents. However, studies related to the mechanism of their anti-biofilm action are still lacking. Similar to other antibiotics, AMPs also require greater quantity and time to kill bacteria embedded in the biofilm, as compared to killing planktonic cells. This study has been conducted as an attempt to elucidate reasons of this negligible anti-biofilm activity of AMPs. We found that AMPs (100 µg/mL) processed with methicillin resistant Staphylococcus aureus (MRSA) biofilms were degraded into fragments over time, with significantly reduced antimicrobial activity due to exposure to aureolysin, an extracellular protease known to regulate the biofilm growth cycle of S. aureus. As such, it was determined that AMPs encounter resistance of aureolysin during their action on S. aureus biofilm.

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References

  1. Lebeaux, D., J. M. Ghigo, and C. Beloin (2014) Biofilm-related infections: bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiol. Mol. Biol. Rev. 78: 510–543.

    Article  Google Scholar 

  2. Vestby, L. K., T. Grønseth, R. Simm, and L. L. Nesse (2020) Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics. 9: 59.

    Article  CAS  Google Scholar 

  3. Høiby, N., T. Bjarnsholt, M. Givskov, S. Molin, and O. Ciofu (2010) Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents. 35: 322–332.

    Article  Google Scholar 

  4. Conlon, B. P., S. E. Rowe, and K. Lewis (2015) Persister cells in biofilm associated infections. pp. 1–9. In: G. Donelli (ed.). Biofilm-based Healthcare-associated Infections: Volume II. Springer, Cham, Switzerland.

    Google Scholar 

  5. Khadke, S. K., J. H. Lee, J. T. Woo, and J. Lee (2019) Inhibitory effects of honokiol and magnolol on biofilm formation by Acinetobacter baumannii. Biotechnol. Bioprocess Eng. 24: 359–365.

    Article  CAS  Google Scholar 

  6. Roy, R., M. Tiwari, G. Donelli, and V. Tiwari (2018) Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence. 9: 522–554.

    Article  CAS  Google Scholar 

  7. Chung, P. Y. and R. Khanum (2017) Antimicrobial peptides as potential anti-biofilm agents against multidrug-resistant bacteria. J. Microbiol. Immunol. Infect. 50: 405–410.

    Article  CAS  Google Scholar 

  8. Di Somma, A., A. Moretta, C. Canè, A. Cirillo, and A. Duilio (2020) Antimicrobial and antibiofilm peptides. Biomolecules. 10: 652.

    Article  Google Scholar 

  9. Kumar, P., J. N. Kizhakkedathu, and S. K. Straus (2018) Antimicrobial peptides: diversity, mechanism of action and strategies to improve the activity and biocompatibility in vivo. Biomolecules. 8: 4.

    Article  Google Scholar 

  10. Yasir, M., M. D. P. Willcox, and D. Dutta (2018) Action of antimicrobial peptides against bacterial biofilms. Materials. 11:2468.

    Article  Google Scholar 

  11. Park, S. C., M. Y. Lee, J. Y. Kim, H. Kim, M. Jung, M. K. Shin, W. K. Lee, G. W. Cheong, J. R. Lee, and M. K. Jang (2019) Anti-biofilm effects of synthetic antimicrobial peptides against drug-resistant Pseudomonas aeruginosa and Staphylococcus aureus planktonic cells and biofilm. Molecules. 24: 4560.

    Article  CAS  Google Scholar 

  12. Shin, S. H., B. Kim, S. Park, S. Jo, and I. H. Lee (2014) Haloganan: a novel antimicrobial peptide for treatment of wound infections. Peptides. 62: 137–143.

    Article  CAS  Google Scholar 

  13. Jang, W. S., C. H. Kim, K. N. Kim, S. Y. Park, J. H. Lee, S. M. Son, and I. H. Lee (2003) Biological activities of synthetic analogs of halocidin, an antimicrobial peptide from the tunicate Halocynthia aurantium. Antimicrob. Agents Chemother. 47: 2481–2486.

    Article  CAS  Google Scholar 

  14. Jang, W. S., K. N. Kim, Y. S. Lee, M. H. Nam, and I. H. Lee (2002) Halocidin: a new antimicrobial peptide from hemocytes of the solitary tunicate, Halocynthia aurantium. FEBS Lett. 521: 81–86.

    Article  CAS  Google Scholar 

  15. O’Toole, G. A. (2011) Microtiter dish biofilm formation assay. J. Vis. Exp. 47: 2437.

    Google Scholar 

  16. Lehrer, R. I., M. Rosenman, S. S. Harwig, R. Jackson, and P. Eisenhauer (1991) Ultrasensitive assays for endogenous antimicrobial polypeptides. J. Immunol. Methods. 137: 167–173.

    Article  CAS  Google Scholar 

  17. Hazzalin, C. A. and L. C. Mahadevan (2017) Acid-urea gel electrophoresis and western blotting of histones. pp. 173–198. In: B. Guillemette and L. R. Gaudreau (eds.). Histones: Methods and Protocols. Humana Press, New York, NY, USA.

    Chapter  Google Scholar 

  18. Sugimoto, S., F. Sato, R. Miyakawa, A. Chiba, S. Onodera, S. Hori, and Y. Mizunoe (2018) Broad impact of extracellular DNA on biofilm formation by clinically isolated Methicillin-resistant and -sensitive strains of Staphylococcus aureus. Sci. Rep. 8: 2254.

    Article  Google Scholar 

  19. Kaplan, J. B., E. A. Izano, P. Gopal, M. T. Karwacki, S. Kim, J. L. Bose, K. W. Bayles, and A. R. Horswill (2012) Low levels of β-lactam antibiotics induce extracellular DNA release and biofilm formation in Staphylococcus aureus. mBio. 3: e00198–12.

    Article  CAS  Google Scholar 

  20. Lister, J. L. and A. R. Horswill (2014) Staphylococcus aureus biofilms: recent developments in biofilm dispersal. Front. Cell. Infect. Microbiol. 4: 178.

    Article  Google Scholar 

  21. Wang, S., A. P. Breslawec, E. Alvarez, M. Tyrlik, C. Li, and M. B. Poulin (2019) Differential recognition of deacetylated PNAG oligosaccharides by a biofilm degrading glycosidase. ACS Chem. Biol. 14: 1998–2005.

    Article  CAS  Google Scholar 

  22. Wu, J. and C. Xi (2010) Enzymatic method for extracting extracellular DNA in biofilm matrix. Cold Spring Harb. Protoc. 2010: pdb.prot5456.

    Article  Google Scholar 

  23. Tam, K. and V. J. Torres (2019) Staphylococcus aureus secreted toxins and extracellular enzymes. Microbiol. Spectr. 7: GPP3-0039-2018.

    Article  Google Scholar 

  24. Björklind, A. and H. Jörnvall (1974) Substrate specificity of three different extracellular proteolytic enzymes from Staphylococcus aureus. Biochim. Biophys. Acta. 370: 524–529.

    Article  Google Scholar 

  25. Sieprawska-Lupa, M., P. Mydel, K. Krawczyk, K. Wójcik, M. Puklo, B. Lupa, P. Suder, J. Silberring, M. Reed, J. Pohl, W. Shafer, F. McAleese, T. Foster, J. Travis, and J. Potempa (2004) Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrob. Agents Chemother. 48: 4673–4679.

    Article  CAS  Google Scholar 

  26. Sonesson, A., K. Przybyszewska, S. Eriksson, M. Mörgelin, S. Kjellström, J. Davies, J. Potempa, and A. Schmidtchen (2017) Identification of bacterial biofilm and the Staphylococcus aureus derived protease, staphopain, on the skin surface of patients with atopic dermatitis. Sci. Rep. 7: 8689.

    Article  Google Scholar 

  27. Shin, Y. P., H. J. Park, S. H. Shin, Y. S. Lee, S. Park, S. Jo, Y. H. Lee, and I. H. Lee (2010) Antimicrobial activity of a halocidin-derived peptide resistant to attacks by proteases. Antimicrob. Agents Chemother. 54: 2855–2866.

    Article  CAS  Google Scholar 

  28. Boles, B. R. and A. R. Horswill (2011) Staphylococcal biofilm disassembly. Trends Microbiol. 19: 449–455.

    Article  CAS  Google Scholar 

  29. Speziale, P., G. Pietrocola, T. J. Foster, and J. A. Geoghegan (2014) Protein-based biofilm matrices in staphylococci. Front. Cell. Infect. Microbiol. 4: 171.

    Article  Google Scholar 

  30. Mootz, J. M., C. L. Malone, L. N. Shaw, and A. R. Horswill (2013) Staphopains modulate Staphylococcus aureus biofilm integrity. Infect. Immun. 81: 3227–3238.

    Article  CAS  Google Scholar 

  31. Hiltunen, A. K., K. Savijoki, T. A. Nyman, I. Miettinen, P. Ihalainen, J. Peltonen, and A. Fallarero (2019) Structural and functional dynamics of Staphylococcus aureus biofilms and biofilm matrix proteins on different clinical materials. Microorganisms. 7: 584.

    Article  CAS  Google Scholar 

  32. Boles, B. R. and A. R. Horswill (2008) agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4: e1000052.

    Article  Google Scholar 

  33. Loughran, A. J., D. N. Atwood, A. C. Anthony, N. S. Harik, H. J. Spencer, K. E. Beenken, and M. S. Smeltzer (2014) Impact of individual extracellular proteases on Staphylococcus aureus biofilm formation in diverse clinical isolates and their isogenic sarA mutants. Microbiologyopen. 3: 897–909.

    Article  CAS  Google Scholar 

  34. Chiang, W. C., M. Nilsson, P. Ø. Jensen, N. Høiby, T. E. Nielsen, M. Givskov, and T. Tolker-Nielsen (2013) Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 57: 2352–2361.

    Article  CAS  Google Scholar 

  35. Arciola, C. R., D. Campoccia, S. Ravaioli, and L. Montanaro (2015) Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Front. Cell. Infect. Microbiol. 5: 7.

    Article  Google Scholar 

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Seo, S., Jung, J., Kim, C.Y. et al. Antimicrobial Peptides Encounter Resistance of Aureolysin during Their Action on Staphylococcus aureus Biofilm. Biotechnol Bioproc E 26, 216–222 (2021). https://doi.org/10.1007/s12257-020-0384-z

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