A novel chimeric endolysin with antibacterial activity against methicillin-resistant Staphylococcus aureus

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue JUN, 2017, Pages

  Kashani, Hamed Haddad ^a   Fahimi, Hossein ^b   Goli, Yasaman Dasteh ^c   Moniri, Rezvan ^a  

^a KASHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

^c University of Maryland   (United States)

Author keywords

Antibacterial agent; Antibiotic resistant; CHAP amidase domain; Endolysin; In silico analysis; Staphylococcus aureus; Synergistic

Indexed keywords

ANTIINFECTIVE AGENT; CYSTEINE/HISTIDINE-DEPENDENT AMIDOHYDROLASE/PEPTIDASE AND AMIDASE; ENDOLYSIN; UNCLASSIFIED DRUG; VANCOMYCIN; AMIDASE; BACTERIAL DNA; PROTEINASE; RECOMBINANT PROTEIN; VIRAL PROTEIN;

ANTIBACTERIAL ACTIVITY; ARTICLE; DISK DIFFUSION; DRUG SOLUBILITY; ESCHERICHIA COLI; GENE SEQUENCE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DOCKING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; VANCOMYCIN RESISTANT ENTEROCOCCUS; WESTERN BLOTTING; AMINO ACID SEQUENCE; BACTERIAL GENE; BACTERIOPHAGE; CELL LINE; CHEMISTRY; COMPUTER SIMULATION; DRUG COMBINATION; DRUG EFFECTS; DRUG POTENTIATION; ENTEROCOCCUS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LACTOCOCCUS LACTIS; MICROBIAL SENSITIVITY TEST; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PH; PROTEIN TERTIARY STRUCTURE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TEMPERATURE;

AMIDOHYDROLASES; AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIOPHAGES; BASE SEQUENCE; CELL LINE; CLONING, MOLECULAR; COMPUTER SIMULATION; DISK DIFFUSION ANTIMICROBIAL TESTS; DNA, BACTERIAL; DRUG COMBINATIONS; DRUG SYNERGISM; ENDOPEPTIDASES; ENTEROCOCCUS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HYDROGEN-ION CONCENTRATION; LACTOCOCCUS LACTIS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MOLECULAR DOCKING SIMULATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TEMPERATURE; VANCOMYCIN; VIRAL PROTEINS;

EID: 85027555232     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00290     Document Type: Article

References (69)

1. Abaev, I., Foster-Frey, J., Korobova, O., Shishkova, N., Kiseleva, N., Kopylov, P., et al (2013). Staphylococcal phage 2638A endolysin is lytic for Staphylococcus aureus and harbors an inter-lytic-domain secondary translational start site. Appl. Microbiol. Biotechnol. 97, 3449–3456. doi: 10.1007/s00253-012-4252-4
2. Achberger, A. M., Brox, T. I., Skidmore, M. L., and Christner, B. C. (2011). Expression and partial characterization of an ice-binding protein from a bacteriumisolated at a depth of 3,519 min the vostok ice core, antarctica. Front. Microbiol. 2:255. doi: 10.3389/fmicb.2011.00255
3. Andersson, M. I., and MacGowan, A. P. (2003). Development of the quinolones. J. Antimicrob. Chemother. 51, 1–11. doi: 10.1093/jac/dkg212
4. Anju, S., Kumar, N. S., Krishnakumar, B., and Kumar, B. D. (2015). Synergistic combination of violacein and azoles that leads to enhanced killing of major human pathogenic dermatophytic fungi Trichophyton rubrum. Front. Cell. Infect. Microbiol. 5:57. doi: 10.3389/fcimb.2015.00057
5. Bassetti, M., Baguneid, M., Bouza, E., Dryden, M., Nathwani, D., and Wilcox, M. (2014). European perspective and update on the management of complicated skin and soft tissue infections due to methicillin-resistant Staphylococcus aureus after more than 10 years of experience with linezolid. Clin. Microbiol. Infect. 20, 3–18. doi: 10.1111/1469-0691.12463
6. Becker, S. C., Dong, S., Baker, J. R., Foster-Frey, J., Pritchard, D. G., and Donovan, D. M. (2009). LysK CHAP endopeptidase domain is required for lysis of live staphylococcal cells. FEMS Microbiol. Lett. 294, 52–60. doi: 10.1111/j.1574-6968.2009.01541.x
7. Berkmen, M. (2012). Production of disulfide-bonded proteins in Escherichia coli. Protein Expr. Purif. 82, 240–251. doi: 10.1016/j.pep.2011.10.009
8. Briers, Y., Schmelcher, M., Loessner, M. J., Hendrix, J., Engelborghs, Y., Volckaert, G., et al. (2009). The high-affinity peptidoglycan binding domain of Pseudomonas phage endolysin KZ144. Biochem. Biophys. Res. Commun. 383, 187–191. doi: 10.1016/j.bbrc.2009.03.161
9. Cheng, Q., and Fischetti, V. A. (2007). Mutagenesis of a bacteriophage lytic enzyme PlyGBS significantly increases its antibacterial activity against group B streptococci. Appl. Microbiol. Biotechnol. 74, 1284–1291. doi: 10.1007/s00253-006-0771-1
10. Cheng, X., Zhang, X., Pflugrath, J. W., and Studier, F. W. (1994). The structure of bacteriophage T7 lysozyme, a zinc amidase and an inhibitor of T7 RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 91, 4034–4038. doi: 10.1073/pnas.91.9.4034
11. Daniel, A., Euler, C., Collin, M., Chahales, P., Gorelick, K. J., and Fischetti, V. A. (2010). Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 54, 1603–1612. doi: 10.1128/AAC.01625-09
12. De Lencastre, H., Oliveira, D., and Tomasz, A. (2007). Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power. Curr. Opin. Microbiol. 10, 428–435. doi: 10.1016/j.mib.2007.08.003
13. Donovan, D. M., Lardeo, M., and Foster-Frey, J. (2006). Lysis of staphylococcal mastitis pathogens by bacteriophage phi11 endolysin. FEMS Microbiol. Lett. 265, 133–139. doi: 10.1111/j.1574-6968.2006.00483.x
14. Entenza, J., Loeffler, J., Grandgirard, D., Fischetti, V., and Moreillon, P. (2005). Therapeutic effects of bacteriophage Cpl-1 lysin against Streptococcus pneumoniae endocarditis in rats. Antimicrob. Agents Chemother. 49, 4789–4792. doi: 10.1128/AAC.49.11.4789-4792.2005
15. Fahimi, H., Allahyari, H., Hassan, Z. M., and Sadeghizadeh, M. (2014). Dengue virus type-3 envelope protein domain III; expression and immunogenicity. Iran. J. Basic Med. Sci. 17, 836–843. doi: 10.22038/ijbms.2014.3710
16. Fenton, M., Casey, P. G., Hill, C., Gahan, C. G., McAuliffe, O., O'Mahony, J. et al. (2010). The truncated phage lysin CHAPk eliminates Staphylococcus aureus in the nares of mice. Bioeng. Bugs 1, 404–407. doi: 10.4161/bbug.1.6.13422
17. Fenton, M., Cooney, J. C., Ross, R. P., Sleator, R. D., McAuliffe, O., O'Mahony, J., et al. (2011a). In silico modeling of the staphylococcal bacteriophage-derived peptidase CHAPK. Bacteriophage 1, 198–206. doi: 10.4161/bact.1.4.18245
18. Fenton, M., Ross, R., McAuliffe, O., O'Mahony, J., and Coffey, A. (2011). Characterization of the staphylococcal bacteriophage lysin CHAPK. J. Appl. Microbiol. 111, 1025–1035. doi: 10.1111/j.1365-2672.2011.05119.x
19. Ferdosian, M., Khatami, M. R., Malekshahi, Z. V., Mohammadi, A., Kashani, H. H., and Shooshtari, M. B. (2015). Identification of immunotopes against Mycobacterium leprae as immune targets using PhDTm-12mer phage display peptide library. Trop. J. Pharm. Res. 14, 1153–1159. doi: 10.4314/tjpr. v14i7.5
20. Fernandes, S., Proença, D., Cantante, C., Silva, F. A., Leandro, C., Lourenço, S., et al. (2012). Novel chimerical endolysins with broad antimicrobial activity against methicillin-resistant Staphylococcus aureus. Microb. Drug Resist. 18, 333–343. doi: 10.1089/mdr.2012.0025
21. Fischetti, V. A. (2010). Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. Int. J. Med. Microbiol. 300, 357–362. doi: 10.1016/j.ijmm.2010.04.002
22. Horgan, M., O'Flynn, G., Garry, J., Cooney, J., Coffey, A., Fitzgerald, G. F., et al. (2009). Phage lysin LysK can be truncated to its CHAP domain and retain lytic activity against live antibiotic-resistant staphylococci. Appl. Environ. Microbiol. 75, 872–874. doi: 10.1128/AEM.01831-08
23. Hosseini, E. S., Moniri, R., Goli, Y. D., and Kashani, H. H. (2016). Purification of antibacterial CHAPK protein using a self-cleaving fusion tag and its activity against methicillin-resistant Staphylococcus aureus. Probiotics Antimicrob. Proteins 8, 202–210. doi: 10.1007/s12602-016-9236-8
24. Jack, R. W., Tagg, J. R., andRay, B. (1995). Bacteriocins of gram-positive bacteria. Microbiol. Rev. 59, 171–200.
25. Jalali, H. K., Salamatzadeh, A., Jalali, A. K., Kashani, H. H., Asbchin, S. A., and Issazadeh, K. (2016). Antagonistic Activity of Nocardia brasiliensis PTCC 1422 Against Isolated Enterobacteriaceae from Urinary Tract Infections. Probiotics Antimicrob. Proteins 8, 41–45. doi: 10.1007/s12602-016-9207-0
26. Jun, S. Y., Jung, G. M., Yoon, S. J., Oh, M.-D., Choi, Y.-J., Lee, W. J., et al. (2013). Antibacterial properties of a pre-formulated recombinant phage endolysin, SAL-1. Int. J. Antimicrob. Agents 41, 156–161. doi: 10.1016/j.ijantimicag.2012.10.011
27. Kashani, H. H., and Moniri, R. (2015). Expression of recombinant pET22b-LysK-cysteine/histidine-dependent amidohydrolase/peptidase bacteriophage therapeutic protein in Escherichia coli BL21 (DE3). Osong Public Health Res. Perspect. 6, 256–260. doi: 10.1016/j.phrp.2015.08.001
28. Kashani, H. H., Moshkdanian, G., Atlasi, M. A., Taherian, A. A., Naderian, H., and Nikzad, H. (2013). Expression of galectin-3 as a testis inflammatory marker in vasectomised mice. Cell J. 15, 11–18.
29. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., and Sternberg, M. J. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845–858. doi: 10.1038/nprot.2015.053
30. Kusuma, C. M., and Kokai-Kun, J. F. (2005). Comparison of four methods for determining lysostaphin susceptibility of various strains of Staphylococcus aureus. Antimicrob. Agents Chemother. 49, 3256–3263. doi: 10.1128/AAC.49.8.3256-3263.2005
31. Loessner, M. J. (2005). Bacteriophage endolysins—current state of research and applications. Curr. Opin. Microbiol. 8, 480–487. doi: 10.1016/j.mib.2005.06.002
32. Loessner, M. J., Kramer, K., Ebel, F., and Scherer, S. (2002). C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol. Microbiol. 44, 335–349. doi: 10.1046/j.1365-2958.2002.02889.x
33. Lovell, S. C., Davis, I. W., Arendall, W. B., de Bakker, P. I., Word, J. M., Prisant, M. G., et al. (2003). Structure validation by Cα geometry: φ, ψ and Cβ deviation. Proteins 50, 437–450. doi: 10.1002/prot.10286
34. Low, K. O., Mahadi, N. M., and Illias, R. M. (2013). Optimisation of signal peptide for recombinant protein secretion in bacterial hosts. Appl. Microbiol. Biotechnol. 97, 3811–3826. doi: 10.1007/s00253-013-4831-z
35. Low, L. Y., Yang, C., Perego, M., Osterman, A., and Liddington, R. C. (2005). Structure and lytic activity of a Bacillus anthracis prophage endolysin. J. Biol. Chem. 280, 35433–35439. doi: 10.1074/jbc.M502723200
36. Magi, G., Marini, E., and Facinelli, B. (2015). Antimicrobial activity of essential oils and carvacrol, and synergy of carvacrol and erythromycin, against clinical, erythromycin-resistant Group A Streptococci. Front. Microbiol. 6:165. doi: 10.3389/fmicb.2015.00165
37. Magiorakos, A. P., Srinivasan, A., Carey, R., Carmeli, Y., Falagas, M., Giske, C., et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrugresistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268–281. doi: 10.1111/j.1469-0691.2011.03570.x
38. Manoharadas, S., Witte, A., and Bläsi, U. (2009). Antimicrobial activity of a chimeric enzybiotic towards Staphylococcus aureus. J. Biotechnol. 139, 118–123. doi: 10.1016/j.jbiotec.2008.09.003
39. Martínez-Alonso, M., González-Montalbán, N., García-Fruitós, E., and Villaverde, A. (2009). Learning about protein solubility from bacterial inclusion bodies. Microb. Cell Fact. 8:4. doi: 10.1186/1475-2859-8-4
40. McCullers, J. A., Karlstrom, A., Iverson, A. R., Loeffler, J. M., and Fischetti, V. A. (2007). Novel strategy to prevent otitis media caused by colonizing Streptococcus pneumoniae. PLoS Pathog. 3:e28. doi: 10.1371/journal.ppat.0030028
41. Nelson, D., Loomis, L., and Fischetti, V. A. (2001). Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc. Natl. Acad. Sci. U.SA. 98, 4107–4112. doi: 10.1073/pnas.061038398
42. Nelson, D., Schuch, R., Chahales, P., Zhu, S., and Fischetti, V. A. (2006). PlyC: a multimeric bacteriophage lysin. Proc. Natl. Acad. Sci. U.SA. 103, 10765–10770. doi: 10.1073/pnas.0604521103
43. Nickerson, E. K., West, T. E., Day, N. P., and Peacock, S. J. (2009). Staphylococcus aureus disease and drug resistance in resource-limited countries in south and east Asia. Lancet Infect. Dis. 9, 130–135. doi: 10.1016/S1473-3099(09)70022-2
44. Nowakowska, Z. (2007). A review of anti-infective and anti-inflammatory chalcones. Eur. J. Med. Chem. 42, 125–137. doi: 10.1016/j.ejmech.2006.09.019
45. Obeso, J. M., Martínez, B., Rodríguez, A., and García, P. (2008). Lytic activity of the recombinant staphylococcal bacteriophage φ H5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128, 212–218. doi: 10.1016/j.ijfoodmicro.2008.08.010
46. Odds, F. C. (2003). Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52, 1–1. doi: 10.1093/jac/dkg301
47. O'flaherty, S., Coffey, A., Meaney, W., Fitzgerald, G., and Ross, R. (2005). The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J. Bacteriol. 187, 7161–7164. doi: 10.1128/JB.187.20.7161-7164.2005
48. O'Flaherty, S., Ross, R., Flynn, J., Meaney, W., Fitzgerald, G., and Coffey, A. (2005). Isolation and characterization of two anti-staphylococcal bacteriophages specific for pathogenic Staphylococcus aureus associated with bovine infections. Lett. Appl. Microbiol. 41, 482–486. doi: 10.1111/j.1472-765X.2005.01781.x
49. Oliveira, H., Boas, D. V., Mesnage, S., Kluskens, L. D., Lavigne, R., Sillankorva, S., et al. (2016). Structural and enzymatic characterization of ABgp46, a novel phage endolysin with broad anti-Gram-negative bacterial activity. Front. Microbiol. 7:208. doi: 10.3389/fmicb.2016.00208
50. Pogue, J., Kaye, K., Cohen, D., and Marchaim, D. (2015). Appropriate antimicrobial therapy in the era of multidrug-resistant human pathogens. Clin. Microbiol. Infect. 21, 302–312. doi: 10.1016/j.cmi.2014.12.025
51. Proença, D., Fernandes, S., Leandro, C., Silva, F. A., Santos, S., Lopes, F., et al. (2012). Phage endolysins with broad antimicrobial activity against Enterococcus faecalis clinical strains. Microb. Drug Resist. 18, 322–332. doi: 10.1089/mdr.2012.0024
52. Rashel, M., Uchiyama, J., Ujihara, T., Uehara, Y., Kuramoto, S., Sugihara, S., et al. (2007). Efficient elimination of multidrug-resistant Staphylococcus aureus by cloned lysin derived frombacteriophage ΔΔMR11. J. Infect. Dis. 196, 1237–1247. doi: 10.1086/521305
53. Reich, P. J., Boyle, M. G., Hogan, P. G., Johnson, A. J., Wallace, M. A., Elward, A. M., et al. (2016). Emergence of community-associated Methicillin-resistant Staphylococcus aureus strains in the neonatal intensive care unit: an infection prevention and patient Safety Challenge. Clin. Microbiol. Infect. 22, 645.e1–8. doi: 10.1016/j.cmi.2016.04.013
54. Rinas, U., Hoffmann, F., Betiku, E., Estapé, D., and Marten, S. (2007). Inclusion body anatomy and functioning of chaperone-mediated in vivo inclusion body disassembly during high-level recombinant protein production in Escherichia coli. J. Biotechnol. 127, 244–257. doi: 10.1016/j.jbiotec.2006.07.004
55. Ritchie, D. W., and Venkatraman, V. (2010). Ultra-fast FFT protein docking on graphics processors. Bioinformatics 26, 2398–2405. doi: 10.1093/bioinformatics/btq444
56. Rosano, G. L., and Ceccarelli, E. A. (2014). Recombinant protein expression in Escherichia coli: advances and challenges. Front. Microbiol. 5:172. doi: 10.3389/fmicb.2014.00172
57. Roy, A., Kucukural, A., and Zhang, Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725–738. doi: 10.1038/nprot.2010.5
58. Salge, T. O., Vera, A., Antons, D., and Cimiotti, J. P. (2016). Fighting MRSA infections in hospital care: how organizational factors matter. Health Serv. Res. 52, 959–983. doi: 10.1111/1475-6773.12521
59. Sanz-Gaitero, M., Keary, R., Garcia-Doval, C., Coffey, A., and van Raaij, M. J. (2014). Crystal structure of the lytic CHAP K domain of the endolysin LysK from Staphylococcus aureus bacteriophage K. Virol. J. 11:1. doi: 10.1186/1743-422X-11-133
60. Sass, P., and Bierbaum, G. (2007). Lytic activity of recombinant bacteriophage ϕ11 and φ 12 endolysins on whole cells and biofilms of Staphylococcus aureus. Appl. Environ. Microbiol. 73, 347–352. doi: 10.1128/AEM.01616-06
61. Schmelcher, M., and Loessner, M. J. (2016). Bacteriophage endolysins: applications for food safety. Curr. Opin. Biotechnol. 37, 76–87. doi: 10.1016/j.copbio.2015.10.005
62. Schuch, R., Nelson, D., and Fischetti, V. A. (2002). A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418, 884–889. doi: 10.1038/nature01026
63. Sharif, A., Kashani, H. H., Nasri, E., Soleimani, Z., and Sharif, M. R. (2017). The role of probiotics in the treatment of dysentery: a randomized double-blind clinical trial. Probiotics Antimicrob. Proteins doi: 10.1007/s12602-017-9271-0. [Epub ahead of print].
64. Sharif, M. R., Kashani, H. H., Ardakani, A. T., Kheirkhah, D., Tabatabaei, F., and Sharif, A. (2016). The effect of a yeast probiotic on acute diarrhea in children. Probiotics Antimicrob. Proteins 8, 211–214. doi: 10.1007/s12602-016-9221-2
65. Ventura, S., and Villaverde, A. (2006). Protein quality in bacterial inclusion bodies. Trends Biotechnol. 24, 179–185. doi: 10.1016/j.tibtech.2006.02.007
66. Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., and Zhang, Y. (2015). The I-TASSER Suite: protein structure and function prediction. Nat. Methods 12, 7–8. doi: 10.1038/nmeth.3213
67. Yang, J., and Zhang, Y. (2015). I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res. 43, W174–W181. doi: 10.1093/nar/gkv342
68. Yoon, S. H., Kim, S. K., and Kim, J. F. (2010). Secretory production of recombinant proteins in Escherichia coli. Recent Pat. Biotechnol. 4, 23–29. doi: 10.2174/187220810790069550
69. Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. doi: 10.1186/1471-2105-9-40