A novel chimeric lysin with robust antibacterial activity against planktonic and biofilm methicillin-resistant Staphylococcus aureus

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Yang, Hang ^a   Zhang, Huaidong ^a   Wang, Jing ^a   Yu, Junping ^a   Wei, Hongping ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; HYDROLASE;

BIOFILM; CHEMISTRY; CONFORMATION; DRUG EFFECT; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; BIOFILMS; HYDROLASES; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR CONFORMATION;

EID: 85008957040     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep40182     Document Type: Article

References (55)

1. Chuang, Y. Y. & Huang, Y. C. Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Asia. Lancet Infect. Dis. 13, 698-708, doi: 10. 1016/S1473-3099(13)70136-1 (2013).
2. Holland, T. L., Arnold, C. & Fowler, V. G., Jr. Clinical management of Staphylococcus aureus bacteremia: A review. JAMA 312, 1330-1341, doi: 10. 1001/jama. 2014. 9743 (2014).
3. Pasberg-Gauhl, C. A need for new generation antibiotics against MRSA resistant bacteria. Drug Disc. Today 11, 109-116, doi: 10. 1016/j. ddtec. 2014. 04. 001 (2014).
4. Otto, M. MRSA virulence and spread. Cell Microbiol. 14, 1513-1521, doi: 10. 1111/j. 1462-5822. 2012. 01832. x (2012).
5. Wu, J. A., Kusuma, C., Mond, J. J. & Kokai-Kun, J. F. Lysostaphin Disrupts Staphylococcus aureus and Staphylococcus epidermidis Biofilms on Artificial Surfaces. Antimicrob. Agents Chemother. 47, 3407-3414, doi: 10. 1128/aac. 47. 11. 3407-3414. 2003 (2003).
6. Otto, M. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Ann. Rev. Med. 64, 175-188, doi: 10. 1146/annurev-med-042711-140023 (2013).
7. Fauvart, M., De Groote, V. N. & Michiels, J. Role of persister cells in chronic infections: clinical relevance and perspectives on antipersister therapies. J. Med. Microbiol. 60, 699-709, doi: 10. 1099/jmm. 0. 030932-0 (2011).
8. Jones, S. M., Morgan, M., Humphrey, T. J. & Lappin-Scott, H. Effect of vancomycin and rifampicin on meticillin-resistant Staphylococcus aureus biofilms. Lancet 357, 40-41, doi: 10. 1016/S0140-6736(00)03572-8 (2001).
9. Pollitt, E. J., Crusz, S. A. & Diggle, S. P. Staphylococcus aureus forms spreading dendrites that have characteristics of active motility. Sci. Rep. 5, 17698, doi: 10. 1038/srep17698 (2015).
10. Szweda, P. et al. Peptidoglycan hydrolases-potential weapons against Staphylococcus aureus. Appl. Microbiol. Biotechnol. 96, 1157-1174, doi: 10. 1007/s00253-012-4484-3 (2012).
11. Rodriguez-Rubio, L. et al. Phage lytic proteins: biotechnological applications beyond clinical antimicrobials. Crit. Rev. Biotechnol. 1-11, doi: 10. 3109/07388551. 2014. 993587 (2015).
12. Yang, H., Yu, J. & Wei, H. Engineered bacteriophage lysins as novel anti-infectives. Front. Microbiol. 5, 542 (2014).
13. Pastagia, M., Schuch, R., Fischetti, V. A. & Huang, D. B. Lysins: The arrival of pathogen-directed anti-infectives. J. Med. Microbiol. 62, 1506-1516, doi: 10. 1099/jmm. 0. 061028-0 (2013).
14. Fischetti, V. A. Lysin Therapy for Staphylococcus aureus and Other Bacterial Pathogens. Curr. Top. Microbiol. Immunol. 1-12, doi: 10. 1007/82-2015-5005 (2016).
15. Resch, G., Moreillon, P. & Fischetti, V. A. A stable phage lysin (Cpl-1) dimer with increased antipneumococcal activity and decreased plasma clearance. Int. J. Antimicrob. Agents 38, 516-521, doi: 10. 1016/j. ijantimicag. 2011. 08. 009 (2011).
16. Daniel, A. et al. Synergism between a Novel Chimeric Lysin and Oxacillin Protects against Infection by Methicillin-Resistant Staphylococcus aureus. Antimicrob. Agents Chemothe 54, 1603-1612, doi: 10. 1128/aac. 01625-09 (2010).
17. Obeso, J. M., Martinez, B., Rodriguez, A. & Garcia, P. Lytic activity of the recombinant staphylococcal bacteriophage PhiH5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128, 212-218, doi: 10. 1016/j. ijfoodmicro. 2008. 08. 010 (2008).
18. Linden, S. B. et al. Biochemical and biophysical characterization of PlyGRCS, a bacteriophage endolysin active against methicillinresistant Staphylococcus aureus. Appl. Microbiol. Biotechnol. 99, 741-752, doi: 10. 1007/s00253-014-5930-1 (2015).
19. Yang, H. et al. Novel chimeric lysin with high-level antimicrobial activity against methicillin-resistant Staphylococcus aureus in vitro and in vivo. Antimicrob. Agents Chemother. 58, 536-542, doi: 10. 1128/AAC. 01793-13AAC. 01793-13 (2014).
20. Dong, Q. et al. Construction of a chimeric lysin Ply187N-V12C with extended lytic activity against staphylococci and streptococci. Microbial. Biotechnol. 8, 210-220, doi: 10. 1111/1751-7915. 12166 (2015).
21. Becker, S. C. et al. Triple-acting Lytic Enzyme Treatment of Drug-Resistant and Intracellular Staphylococcus aureus. Sci. Rep. 6, 25063, doi: 10. 1038/srep25063 (2016).
22. Yang, H. et al. A chimeolysin with extended-spectrum streptococcal host range found by an induced lysis-based rapid screening method. Sci. Rep. 5, 17257, doi: 10. 1038/srep17257 (2015).
23. Leaver-Fay, A. et al. ROSETTA3: An object-oriented software suite for the simulation and design of macromolecules. Method. Enzymol. 487, 545-574, doi: 10. 1016/B978-0-12-381270-4. 00019-6 (2011).
24. Gu, J. et al. Structural and biochemical characterization reveals LysGH15 as an unprecedented "EF-hand-like" calcium-binding phage lysin. PLoS Pathog. 10, e1004109, doi: 10. 1371/journal. ppat. 1004109 (2014).
25. Sanz-Gaitero, M., Keary, R., Garcia-Doval, C., Coffey, A. & van Raaij, M. J. Crystal structure of the lytic CHAP(K) domain of the endolysin LysK from Staphylococcus aureus bacteriophage K. Virol. J. 11, 133, doi: 10. 1186/1743-422X-11-133 (2014).
26. McGowan, S. et al. X-ray crystal structure of the streptococcal specific phage lysin PlyC. Proc. Natl. Acad. Sci. USA 109, 12752-12757, doi: 10. 1073/pnas. 1208424109 (2012).
27. Yoong, P., Schuch, R., Nelson, D. & Fischetti, V. A. Identification of a broadly active phage lytic enzyme with lethal activity against antibiotic-resistant Enterococcus faecalis and Enterococcus faecium. J. Bacteriol. 186, 4808-4812, doi: 10. 1128/JB. 186. 14. 4808-4812. 2004186/14/4808 (2004).
28. Gilmer, D. B., Schmitz, J. E., Euler, C. W. & Fischetti, V. A. Novel bacteriophage lysin with broad lytic activity protects against mixed infection by Streptococcus pyogenes and methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 57, 2743-2750, doi: 10. 1128/AAC. 02526-12AAC. 02526-12 (2013).
29. Young, R. & Gill, J. J. Phage therapy redux-What is to be done Science 350, 1163-1164, doi: 10. 1126/science. Aad6791 (2015).
30. Schuch, R. et al. Combination therapy with lysin CF-301 and antibiotic is superior to antibiotic alone for treating methicillinresistant Staphylococcus aureus-induced murine bacteremia. J. Infect. Dis. 209, 1469-1478, doi: 10. 1093/infdis/jit637 (2014).
31. Vipra, A. A. et al. Antistaphylococcal activity of bacteriophage derived chimeric protein P128. BMC Microbiol. 12, 41, doi: 10. 1186/1471-2180-12-411471-2180-12-41 (2012).
32. Huang, Y., Yang, H., Yu, J. & Wei, H. Molecular dissection of phage lysin PlySs2: integrity of the catalytic and cell wall binding domains is essential for its broad lytic activity. Virol. Sin. 30, 45-51, doi: 10. 1007/s12250-014-3535-6 (2015).
33. Payne, K., Sun, Q., Sacchettini, J. & Hatfull, G. F. Mycobacteriophage Lysin B is a novel mycolylarabinogalactan esterase. Mol. Microbiol. 73, 367-381, doi: 10. 1111/j. 1365-2958. 2009. 06775. x (2009).
34. Rossi, P. et al. Structural elucidation of the Cys-His-Glu-Asn proteolytic relay in the secreted CHAP domain enzyme from the human pathogen Staphylococcus saprophyticus. Proteins 74, 515-519, doi: 10. 1002/prot. 22267 (2009).
35. Keen, E. F. 3rd et al. Prevalence of multidrug-resistant organisms recovered at a military burn center. Burns 36, 819-825, doi: 10. 1016/j. burns. 2009. 10. 013 (2010).
36. Church, D., Elsayed, S., Reid, O., Winston, B. & Lindsay, R. Burn wound infections. Clin. Microbiol. Rev. 19, 403-434, doi: 10. 1128/ CMR. 19. 2. 403-434. 2006 (2006).
37. Idelevich, E. A. et al. In vitro activity against Staphylococcus aureus of a novel antimicrobial agent, PRF-119, a recombinant chimeric bacteriophage endolysin. Antimicrob. Agents Chemother. 55, 4416-4419, doi: 10. 1128/AAC. 00217-11 (2011).
38. Mao, J., Schmelcher, M., Harty, W. J., Foster-Frey, J. & Donovan, D. M. Chimeric Ply187 endolysin kills Staphylococcus aureus more effectively than the parental enzyme. FEMS Microbiol. Lett. 342, 30-36, doi: 10. 1111/1574-6968. 12104 (2013).
39. Fernandes, S. et al. Novel chimerical endolysins with broad antimicrobial activity against methicillin-resistant Staphylococcus aureus. Microbial. Drug Resist. 18, 333-343, doi: 10. 1089/mdr. 2012. 0025 (2012).
40. George, S. E. et al. Biochemical characterization and evaluation of cytotoxicity of antistaphylococcal chimeric protein P128. BMC Res. Note 5, 280, doi: 10. 1186/1756-0500-5-280 (2012).
41. Loessner, M. J., Gaeng, S. & Scherer, S. Evidence for a holin-like protein gene fully embedded out of frame in the endolysin gene of Staphylococcus aureus bacteriophage 187. J. Bacteriol. 181, 4452-4460 (1999).
42. Eugster, M. R. & Loessner, M. J. Wall teichoic acids restrict access of bacteriophage endolysin Ply118, Ply511, and PlyP40 cell wall binding domains to the Listeria monocytogenes peptidoglycan. J. Bacteriol. 194, 6498-6506, doi: 10. 1128/JB. 00808-12JB. 00808-12 (2012).
43. Cheng, Q., Nelson, D., Zhu, S. & Fischetti, V. A. Removal of group B streptococci colonizing the vagina and oropharynx of mice with a bacteriophage lytic enzyme. Antimicrob. Agents Chemother. 49, 111-117, doi: 10. 1128/AAC. 49. 1. 111-117. 2005 (2005).
44. Nelson, D., Schuch, R., Chahales, P., Zhu, S. & Fischetti, V. A. PlyC: A multimeric bacteriophage lysin. Proc. Natl. Acad. Sci. USA 103, 10765-10770, doi: 10. 1073/pnas. 0604521103 (2006).
45. Lai, M. J. et al. Antibacterial activity of Acinetobacter baumannii phage varphiAB2 endolysin (LysAB2) against both gram-positive and gram-negative bacteria. Appl. Microbiol. Biotechnol. 90, 529-539, doi: 10. 1007/s00253-011-3104-y (2011).
46. Chan, W. T., Verma, C. S., Lane, D. P. & Gan, S. K. A comparison and optimization of methods and factors affecting the transformation of Escherichia coli. Bioscience Rep. 33, doi: 10. 1042/BSR20130098 (2013).
47. Yang, H. et al. Existence of separate domains in lysin PlyG for recognizing Bacillus anthracis spores and vegetative cells. Antimicrob. Agents Chemother. 56, 5031-5039, doi: 10. 1128/AAC. 00891-12AAC. 00891-12 (2012).
48. Nelson, D., Loomis, L. & Fischetti, V. A. Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc. Natl. Acad. Sci. U S A 98, 4107-4112, doi: 10. 1073/pnas. 061038398 (2001).
49. Yoong, P., Schuch, R., Nelson, D. & Fischetti, V. A. PlyPH, a bacteriolytic enzyme with a broad pH range of activity and lytic action against Bacillus anthracis. J. Bacteriol. 188, 2711-2714, doi: 10. 1128/JB. 188. 7. 2711-2714. 2006 (2006).
50. Mataraci, E. & Dosler, S. In vitro activities of antibiotics and antimicrobial cationic peptides alone and in combination against methicillin resistance Staphylococcus aureus biofilms. Antimicrob. Agents Chemother. 56, 6366-6371, doi: 10. 1128/AAC. 01180-12 (2012).
51. Croes, S. et al. Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. Aureus lineage. BMC Microbiol. 9, 229, doi: 10. 1186/1471-2180-9-229 (2009).
52. Brisbois, E. J. et al. Optimized polymeric film-based nitric oxide delivery inhibits bacterial growth in a mouse burn wound model. Acta Biomater. 10, 4136-4142, doi: 10. 1016/j. Actbio. 2014. 06. 032S1742-7061(14)00288-8 (2014).
53. Lyskov, S. et al. Serverification of molecular modeling applications: The Rosetta Online Server that Includes Everyone (ROSIE). PloS one 8, e63906, doi: 10. 1371/journal. pone. 0063906 (2013).
54. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132, doi: 10. 1107/ S0907444904019158 (2004).
55. Chen, V. B. et al. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21, doi: 10. 1107/S0907444909042073 (2010).