Effective antimicrobial activity of plectasin-derived antimicrobial peptides against Staphylococcus aureus infection in mammary glands

Frontiers in Microbiology

Volumn 8, Issue DEC, 2017, Pages

  Li, Lianbin ^a   Wang, Liangliang ^b   Gao, Yuqi ^a   Wang, Jianhua ^c   Zhao, Xin ^a,d  

^a NORTHWEST A F UNIVERSITY   (China)

^b TSINGHUA UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

Antimicrobial peptides; Mammary glands; Mastitis; MP1102; NZ2114; Staphylococcus aureus

Indexed keywords

INTERLEUKIN 6; PLECTASIN; POLYPEPTIDE ANTIBIOTIC AGENT; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CELL PROLIFERATION ASSAY; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; HISTOPATHOLOGY; MAMMARY GLAND; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

EID: 85036637086     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.02386     Document Type: Article

References (33)

1. Andes, D., Craig, W., Nielsen, L. A., and Kristensen, H. H. (2009). In vivo pharmacodynamic characterization of a novel plectasin antibiotic, NZ2114, in a murine infection model. Antimicrob. Agents Chemother. 53, 3003-3009. doi: 10.1128/AAC.01584-08
2. Bouchard, D. S., Rault, L., Berkova, N., Loir, Y. L., and Even, S. (2013). Inhibition of Staphylococcus aureus invasion into bovine mammary epithelial cells by contact with live Lactobacillus casei. Appl. Environ. Microbiol. 79, 877-885. doi: 10.1128/AEM.03323-12
3. Brinch, K. S., Sandberg, A., Baudoux, P., Van Bambeke, F., Tulkens, P. M., Frimodt-Moller, N., et al. (2009). Plectasin shows intracellular activity against Staphylococcus aureus in human THP-1 monocytes and in a mouse peritonitis model. Antimicrob. Agents Chemother. 53, 4801-4808. doi: 10.1128/AAC.00685-09
4. Brinch, K. S., Tulkens, P. M., Van Bambeke, F., Frimodt-Moller, N., Hoiby, N., and Kristensen, H. H. (2010). Intracellular activity of the peptide antibiotic NZ2114: studies with Staphylococcus aureus and human THP-1 monocytes, and comparison with daptomycin and vancomycin. J. Antimicrob. Chemother. 65, 1720-1724. doi: 10.1093/jac/dkq159
5. Brouillette, E., Grondin, G., Lefebvre, C., Talbot, B. G., and Malouin, F. (2004). Mouse mastitis model of infection for antimicrobial compound efficacy studies against intracellular and extracellular forms of Staphylococcus aureus. Vet. Microbiol. 101, 253-262. doi: 10.1016/j.vetmic.2004.04.008
6. Clement, S., Vaudaux, P., Francois, P., Schrenzel, J., Huggler, E., Kampf, S., et al. (2005). Evidence of an intracellular reservoir in the nasal mucosa of patients with recurrent Staphylococcus aureus rhinosinusitis. J. Infect. Dis. 192, 1023-1028. doi: 10.1086/432735
7. Damasceno, L. M., Huang, C.-J., and Batt, C. A. (2012). Protein secretion in Pichia pastoris and advances in protein production. Appl. Microbiol. Biotechnol. 93, 31-39. doi: 10.1007/s00253-011-3654-z
8. Demon, D., Breyne, K., Schiffer, G., and Meyer, E. (2013). Short communication: antimicrobial efficacy of intramammary treatment with a novel biphenomycin compound against Staphylococcus aureus, Streptococcus uberis, and Escherichia coli-induced mouse mastitis. J. Dairy Sci. 96, 7082-7087. doi: 10.3168/jds.2013-7011
9. Demon, D., Ludwig, C., Breyne, K., Guede, D., Dorner, J. C., Froyman, R., et al. (2012). The intramammary efficacy of first generation cephalosporins against Staphylococcus aureus mastitis in mice. Vet. Microbiol. 160, 141-150. doi: 10.1016/j.vetmic.2012.05.017
10. Fu, Y., Zhou, E., Wei, Z., Liang, D., Wang, W., Wang, T., et al. (2014). Glycyrrhizin inhibits the inflammatory response in mouse mammary epithelial cells and a mouse mastitis model. FEBS J. 281, 2543-2557. doi: 10.1111/febs.12801
11. Fung, H., and Demple, B. (2005). A vital role for Ape1/Ref1 protein in repairing spontaneous DNA damage in human cells. Mol. Cell 17, 463-470. doi: 10.1016/j.molcel.2004.12.029
12. Garzoni, C., and Kelley, W. L. (2009). Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol. 17, 59-65. doi: 10.1016/j.tim.2008.11.005
13. Hancock, R. E., and Sahl, H-G. (2006). Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24, 1551-1557. doi: 10.1038/nbt1267
14. Henriques, S. T., Melo, M. N., and Castanho, M. A. (2006). Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem. J. 399, 1-7. doi: 10.1042/BJ20061100
15. Hensen, S. M., Pavicic, M. J., Lohuis, J. A., and Poutrel, B. (2000). Use of bovine primary mammary epithelial cells for the comparison of adherence and invasion ability of Staphylococcus aureus strains. J. Dairy Sci. 83, 418-429. doi: 10.3168/jds.S0022-0302(00)74898-3
16. Kluytmans, J., Van Belkum, A., and Verbrugh, H. (1997). Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10, 505-520
17. Kuang, Y., Jia, H., Miyanaga, K., and Tanji, Y. (2009). Effect of milk on antibacterial activity of tetracycline against Escherichia coli and Staphylococcus aureus isolated from bovine mastitis. Appl. Microbiol. Biotechnol. 84, 135-142. doi: 10.1007/s00253-009-2008-6
18. Madani, F., Lindberg, S., Langel, U., Futaki, S., and Graslund, A. (2011). Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys. 2011:414729. doi: 10.1155/2011/414729
19. Mygind, P. H., Fischer, R. L., Schnorr, K. M., Hansen, M. T., Sonksen, C. P., Ludvigsen, S., et al. (2005). Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 437, 975-980. doi: 10.1038/nature04051
20. Narayana, J. L., Huang, H. N., Wu, C. J., and Chen, J. Y. (2015). Epinecidin-1 antimicrobial activity: in vitro membrane lysis and in vivo efficacy against Helicobacter pylori infection in a mouse model. Biomaterials 61, 41-51. doi: 10.1016/j.biomaterials.2015.05.014
21. Nazemi, S., Aalbaek, B., Kjelgaard-Hansen, M., Safayi, S., Klaerke, D. A., and Knight, C. H. (2014). Expression of acute phase proteins and inflammatory cytokines in mouse mammary gland following Staphylococcus aureus challenge and in response to milk accumulation. J. Dairy Res. 81, 445-454. doi: 10.1017/S0022029914000454
22. Peyrusson, F., Butler, D., Tulkens, P. M., and Van Bambeke, F. (2015). Cellular pharmacokinetics and intracellular activity of the novel peptide deformylase inhibitor GSK1322322 against Staphylococcus aureus laboratory and clinical strains with various resistance phenotypes: studies with human THP-1 monocytes and J774 murine macrophages. Antimicrob. Agents Chemother. 59, 5747-5760. doi: 10.1128/AAC.00827-15
23. Rodríguez-Rojas, A., Makarova, O., and Rolff, J. (2014). Antimicrobials, stress and mutagenesis. PLOS Pathog. 10:e1004445. doi: 10.1371/journal.ppat.1004445
24. Schmelcher, M., Powell, A. M., Becker, S. C., Camp, M. J., and Donovan, D. M. (2012). Chimeric phage lysins act synergistically with lysostaphin to kill mastitis-causing Staphylococcus aureus in murine mammary glands. Appl. Environ. Microbiol. 78, 2297-2305. doi: 10.1128/AEM.07050-11
25. Schmelcher, M., Powell, A. M., Camp, M. J., Pohl, C. S., and Donovan, D. M. (2015). Synergistic streptococcal phage ΔSA2 and B30 endolysins kill streptococci in cow milk and in a mouse model of mastitis. Appl. Microbiol. Biotechnol. 99, 8475-8486. doi: 10.1007/s00253-015-6579-0
26. Schneider, T., Kruse, T., Wimmer, R., Wiedemann, I., Sass, V., Pag, U., et al. (2010). Plectasin, a fungal defensin, targets the bacterial cell wall precursor Lipid II. Science 328, 1168-1172. doi: 10.1126/science.1185723
27. Takeshima, K., Chikushi, A., Lee, K. K., Yonehara, S., and Matsuzaki, K. (2003). Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J. Biol. Chem. 278, 1310-1315. doi: 10.1074/jbc.M208762200
28. Wang, L., Si, W., Xue, H., and Zhao, X. (2017). A fibronectin-binding protein (FbpA) of Weissella cibaria inhibits colonization and infection of Staphylococcus aureus in mammary glands. Cell. Microbiol. 19:e12731. doi: 10.1111/cmi.12731
29. Wiegand, I., Hilpert, K., and Hancock, R. E. (2008). Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3, 163-175. doi: 10.1038/nprot.2007.521
30. Zasloff, M. (2016). "Antimicrobial peptides: do they have a future as therapeutics?," in Antimicrobial Peptides, eds J. Harder and J. M. Schröder (Basel: Springer Press), 147-154. doi: 10.1007/978-3-319-24199-9_10
31. Zecconi, A., and Scali, F. (2013). Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases. Immunol. Lett. 150, 12-22. doi: 10.1016/j.imlet.2013.01.004
32. Zhang, Y., Teng, D., Mao, R., Wang, X., Xi, D., Hu, X., et al. (2014). High expression of a plectasin-derived peptide NZ2114 in Pichia pastoris and its pharmacodynamics, postantibiotic and synergy against Staphylococcus aureus. Appl. Microbiol. Biotechnol. 98, 681-694. doi: 10.1007/s00253-013-4881-2
33. Zhang, Y., Teng, D., Wang, X., Mao, R., Cao, X., Hu, X., et al. (2015). In vitro and in vivo characterization of a new recombinant antimicrobial peptide, MP1102, against methicillin-resistant Staphylococcus aureus. Appl. Microbiol. Biotechnol. 99, 6255-6266. doi: 10.1007/s00253-015-6394-7