Design of a polypeptide FRET substrate that facilitates study of the antimicrobial protease lysostaphin

Biochemical Journal

Volumn 418, Issue 3, 2009, Pages 615-624

  Bardelang, Philip ^a   Vankemmelbeke, Mireille ^a   Zhang, Ying ^a   Jarvis, Hannah ^a   Antoniadou, Eleni ^a   Rochette, Sophie ^a   Thomas, Neil R ^a   Penfold, Christopher N ^a   James, Richard ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Colicin E9; Endopeptidase; Fluorescence resonance energy transfer assay (FRET assay); Lysostaphin; LytM; Staphylococcus aureus

Indexed keywords

COLICIN E9; ENDOPEPTIDASE; FLUORESCENCE RESONANCE ENERGY TRANSFER ASSAY (FRET ASSAY); LYSOSTAPHIN; LYTM; STAPHYLOCOCCUS AUREUS;

AMINES; AMINO ACIDS; CELL MEMBRANES; ENERGY TRANSFER; ENZYME INHIBITION; FLUORESCENCE; ORGANIC ACIDS; RESONANCE;

SUBSTRATES;

DEOXYRIBONUCLEASE; GLYCINE; GREEN FLUORESCENT PROTEIN; LYSOSTAPHIN; MUTANT PROTEIN; PENTAGLYCINE; PROTEINASE; SERINE; UNCLASSIFIED DRUG; LYSOSTAPHIN ENDOPEPTIDASE; PEPTIDE;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL CELL WALL; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; STAPHYLOCOCCUS AUREUS; CHEMISTRY; DRUG EFFECT; GENETICS; METABOLISM; MOLECULAR CLONING; SITE DIRECTED MUTAGENESIS; SYNTHESIS;

STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

CLONING, MOLECULAR; ENDOPEPTIDASES; FLUORESCENCE RESONANCE ENERGY TRANSFER; LYSOSTAPHIN; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; STAPHYLOCOCCUS AUREUS;

EID: 62149090699     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081765     Document Type: Article

References (47)

1. Schindler, C. A. and Schuhardt, V. T. (1964) Lysostaphin: a new bacteriolytic agent for the Staphylococcus. Proc. Natl. Acad. Sci. U.S.A. 51, 414-421
2. Recsei, P. A., Gruss, A. D. and Novick, R. P. (1987) Cloning, sequence, and expression of the lysostaphin gene from Staphylococcus simulans. Proc. Natl. Acad. Sci. U.S.A. 84, 1127-1131
3. Thumm, G. and Gotz, F. (1997) Studies on prolysostaphin processing and characterization of the lysostaphin immunity factor (Lif) of Staphylococcus simulans biovar staphylolyticus. Mol. Microbiol. 23, 1251-1265
4. Baba, T. and Schneewind, O. (1996) Target cell specificity of a bacteriocin molecule: a C-terminal signal directs lysostaphin to the cell wall of Staphylococcus aureus. EMBO J. 15, 4789-4797
5. Trayer, H. R. and Buckley, C. E. (1970) Molecular properties of lysostaphin, a bacteriolytic agent specific for Staphylococcus aureus. J. Biol. Chem. 245, 4842-4846
6. Schleifer, K. H. and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477
7. Schneewind, O., Fowler, A. and Faull, K. F. (1995) Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science 268, 103-106
8. Xu, N., Huang, Z. H., de Jonge, B. L. and Gage, D. A. (1997) Structural characterization of peptidoglycan muropeptides by matrix-assisted laser desorption ionization mass spectrometry and postsource decay analysis. Anal. Biochem. 248, 7-14
9. Climo, M. W., Patron, R. L., Goldstein, B. P. and Archer, G. L. (1998) Lysostaphin treatment of experimental methicillin-resistant Staphylococcus aureus aortic valve endocarditis. Antimicrob. Agents Chemother. 42, 1355-1360
10. Dajcs, J. J., Hume, E. B., Moreau, J. M., Caballero, A. R., Cannon, B. M. and O'Callaghan, R. J. (2000) Lysostaphin treatment of methicillin-resistant Staphylococcus aureus keratitis in the rabbit. Invest. Ophthalmol. Visual Sci. 41, 1432-1437
11. Walsh, S., Shah, A. and Mond, J. (2003) Improved pharmacokinetics and reduced antibody reactivity of lysostaphin conjugated to polyethylene glycol. Antimicrob. Agents Chemother. 47, 554-558
12. Climo, M. W., Ehlert, K. and Archer, G. L. (2001) Mechanism and suppression of lysostaphin resistance in oxacillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 45, 1431-1437
13. Kerr, D. E., Plaut, K., Bramley, A. J., Williamson, C. M., Lax, A. J., Moore, K., Wells, K. D. and Wall, R. J. (2001) Lysostaphin expression in mammary glands confers protection against staphylococcal infection in transgenic mice. Nat. Biotechnol. 19, 66-70
14. Kokai-Kun, J. F., Walsh, S. M., Chanturiya, T. and Mond, J. J. (2003) Lysostaphin cream eradicates Staphylococcus aureus nasal colonization in a cotton rat model. Antimicrob. Agents Chemother. 47, 1589-1597
15. Wu, J. A., Kusuma, C., Mond, J. J. and Kokai-Kun, J. F. (2003) Lysostaphin disrupts Staphylococcus aureus and Staphylococcus epidermidis biofilms on artificial surfaces. Antimicrob. Agents Chemother. 47, 3407-3414
16. Shah, A., Mond, J. and Walsh, S. (2004) Lysostaphin-coated catheters eradicate Staphylococccus aureus challenge and block surface colonization. Antimicrob. Agents Chemother. 48, 2704-2707
17. Wall, R. J., Powell, A. M., Paape, M. J., Kerr, D. E., Bannerman, D. D., Pursel, V. G., Wells, K. D., Talbot, N. and Hawk, H. W. (2005) Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat. Biotechnol. 23, 445-451
18. Grundling, A. and Schneewind, O. (2006) Cross-linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus. J. Bacteriol. 188, 2463-2472
19. Sugai, M., Fujiwara, T., Akiyama, T., Ohara, M., Komatsuzawa, H., Inoue, S. and Suginaka, H. (1997) Purification and molecular characterization of glycylglycine endopeptidase produced by Staphylococcus capitis EPK1. J. Bacteriol. 179, 1193-1202
20. Ramadurai, L. and Jayaswal, R. K. (1997) Molecular cloning, sequencing, and expression of lytM, a unique autolytic gene of Staphylococcus aureus. J. Bacteriol. 179, 3625-3631
21. Simmonds, R. S., Simpson, W. J. and Tagg, J. R. (1997) Cloning and sequence analysis of zooA, a Streptococcus zooepidemicus gene encoding a bacteriocin-like inhibitory substance having a domain structure similar to that of lysostaphin. Gene 189, 255-261
22. Hickey, R. M., Twomey, D. P., Ross, R. P. and Hill, C. (2003) Production of enterolysin A by a raw milk enterococcal isolate exhibiting multiple virulence factors. Microbiology 149, 655-664
23. Beukes, M., Bierbaum, G., Sahl, H. G. and Hastings, J. W. (2000) Purification and partial characterization of a murein hydrolase, millericin B, produced by Streptococcus milleri NMSCC 061. Appl. Environ. Microbiol. 66, 23-28
24. Kline, S. A., de la Harpe, J. and Blackburn, P. (1994) A colorimetric microtiter plate assay for lysostaphin using a hexaglycine substrate. Anal. Biochem. 217, 329-331
25. Zhou, R., Chen, S. and Recsei, P. (1988) A dye release assay for determination of lysostaphin activity. Anal. Biochem. 171, 141-144
26. Odintsov, S. G., Sabala, I., Marcyjaniak, M. and Bochtler, M. (2004) Latent LytM at 1.3 Å resolution. J. Mol. Biol. 335, 775-785
27. Warfield, R., Bardelang, P., Saunders, H., Chan, W. C., Penfold, C., James, R. and Thomas, N. R. (2006) Internally quenched peptides for the study of lysostaphin: an antimicrobial protease that kills Staphylococcus aureus. Org. Biomol. Chem. 4, 3626-3638
28. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
29. Szweda, P., Pladzyk, R., Kotlowski, R. and Kur, J. (2001) Cloning, expression, and purification of the Staphylococcus simulans lysostaphin using the intein-chitin-binding domain (CBD) system. Protein Expression Purif. 22, 467-471
30. Lai, A. C., Tran, S. and Simmonds, R. S. (2002) Functional characterization of domains found within a lytic enzyme produced by Streptococcus equi subsp. zooepidemicus. FEMS Microbiol. Lett. 215, 133-138
31. Garinot-Schneider, C., Penfold, C. N., Moore, G. R., Kleanthous, C. and James, R. (1997) Identification of residues in the putative TolA box which are essential for the toxicity of the endonuclease toxin colicin E9. Microbiology 143, 2931-2938
32. Sarkar, G. and Sommer, S. S. (1990) The megaprimer method of site-directed mutagenesis. BioTechniques 8, 404-407
33. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326
34. Kessler, E., Safrin, M., Olson, J. C. and Ohman, D. E. (1993) Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J. Biol. Chem. 268, 7503-7508
35. Cox, R. A., Conquest, C., Mallaghan, C. and Marples, R. R. (1995) A major outbreak of methicillin-resistant Staphylococcus aureus caused by a new phage-type (EMRSA-16). J. Hosp. Infect. 29, 87-106
36. Forster, T. (1948) Intermolecular energy transfer and fluorescence. Ann. Phys. 2, 55-75
37. Kraynov, V. S., Chamberlain, C., Bokoch, G. M., Schwartz, M. A., Slabaugh, S. and Hahn, K. M. (2000) Localized Rac activation dynamics visualized in living cells. Science 290, 333-337
38. Collins, E. S., Whittaker, S. B., Tozawa, K., MacDonald, C., Boetzel, R., Penfold, C. N., Reilly, A., Clayden, N. J., Osborne, M. J., Hemmings, A. M. et al. (2002) Structural dynamics of the membrane translocation domain of colicin E9 and its interaction with TolB. J. Mol. Biol. 318, 787-804
39. Liu, Y., Kati, W., Chen, C. M., Tripathi, R., Molla, A. and Kohlbrenner, W. (1999) Use of a fluorescence plate reader for measuring kinetic parameters with inner filter effect correction. Anal. Biochem. 267, 331-335
40. Simmonds, R. S., Pearson, L., Kennedy, R. C. and Tagg, J. R. (1996) Mode of action of a lysostaphin-like bacteriolytic agent produced by Streptococcus zooepidemicus 4881. Appl. Environ. Microbiol. 62, 4536-4541
41. Firczuk, M., Mucha, A. and Bochtler, M. (2005) Crystal structures of active LytM. J. Mol. Biol. 354, 578-590
42. Sugai, M., Fujiwara, T., Ohta, K., Komatsuzawa, H., Ohara, M. and Suginaka, H. (1997) epr, which encodes glycylglycine endopeptidase resistance, is homologous to femAB and affects serine content of peptidoglycan cross bridges in Staphylococcus capitis and Staphylococcus aureus. J. Bacteriol. 179, 4311-4318
43. DeHart, H. P., Heath, H. E., Heath, L. S., LeBlanc, P. A. and Sloan, G. L. (1995) The lysostaphin endopeptidase resistance gene (epr) specifies modification of peptidoglycan cross bridges in Staphylococcus simulans and Staphylococcus aureus. Appl. Environ. Microbiol. 61, 1475-1479
44. Ehlert, K., Tschierske, M., Mori, C., Schröder, W. and Berger-Bächi, B. (2000) Site-specific serine incorporation by Lif and Epr into positions 3 and 5 of the staphylococcal peptidoglycan interpeptide bridge. J. Bacteriol. 182, 2635-2638
45. Tozawa, K., Macdonald, C. J., Penfold, C. N., James, R., Kleanthous, C., Clayden, N. J. and Moore, G. R. (2005) Clusters in an intrinsically disordered protein create a protein-binding site: the TolB-binding region of colicin E9. Biochemistry 44, 11496-11507
46. Fujiwara, T., Aoki, S., Komatsuzawa, H., Nishida, T., Ohara, M., Suginaka, H. and Sugai, M. (2005) Mutation analysis of the histidine residues in the glycylglycine endopeptidase ALE-1. J. Bacteriol. 187, 480-487
47. Heath, L. S., Gargis, S. R., Smithberg, S. R., Johnson, H. P., Heath, H. E., Leblanc, P. A. and Sloan, G. L. (2005) Plasmid-specified FemABX-like immunity factor in Staphylococcus sciuri DD 4747. FEMS Microbiol. Lett. 249, 227-231