Saturation mutagenesis of selected residues of the α-peptide of the lantibiotic lacticin 3147 yields a derivative with enhanced antimicrobial activity

Microbial Biotechnology

Volumn 6, Issue 5, 2013, Pages 564-575

  Field, Des ^a   Molloy, Evelyn M ^a   Iancu, Catalin ^b   Draper, Lorraine A ^a   O' Connor, Paula M ^c,d   Cotter, Paul D ^c,d   Hill, Colin ^a,c   Ross, R Paul ^c,d  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b DUNAREA DE JOS UNIVERSITY OF GALATI   (Romania)

^c UNIVERSITY COLLEGE CORK   (Ireland)

^d TEAGASC FOOD RESEARCH CENTRE   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

LACTICIN 3147; LANTIBIOTIC; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BIOENGINEERING; MUTAGENESIS; NONHUMAN; STAPHYLOCOCCUS AUREUS;

EID: 84882289135     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12041     Document Type: Article

References (57)

1. Appleyard, A.N., Choi, S., Read, D.M., Lightfoot, A., Boakes, S., Hoffmann, A., etal. (2009) Dissecting structural and functional diversity of the lantibiotic mersacidin. Chem Biol 16: 490-498.
2. Begley, M., Cotter, P.D., Hill, C., and Ross, R.P. (2009) Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl Environ Microbiol 75: 5451-5460.
3. Bierbaum, G., and Sahl, H.G. (2009) Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol 10: 2-18.
4. Boakes, S., Cortes, J., Appleyard, A.N., Rudd, B.A., and Dawson, M.J. (2009) Organization of the genes encoding the biosynthesis of actagardine and engineering of a variant generation system. Mol Microbiol 72: 1126-1136.
5. Boucher, H.W., Talbot, G.H., Bradley, J.S., Edwards, J.E., Gilbert, D., Rice, L.B., etal. (2009) Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48: 1-12.
6. Breukink, E., and de Kruijff, B. (2006) Lipid II as a target for antibiotics. Nat Rev Drug Discov 5: 321-332.
7. Carroll, J., Draper, L.A., O'Connor, P.M., Coffey, A., Hill, C., Ross, R.P., etal. (2010) Comparison of the activities of the lantibiotics nisin and lacticin 3147 against clinically significant mycobacteria. Int J Antimicrob Agents 36: 132-136.
8. Chan, W.C., Leyland, M., Clark, J., Dodd, H.M., Lian, L.Y., Gasson, M.J., etal. (1996) Structure-activity relationships in the peptide antibiotic nisin: antibacterial activity of fragments of nisin. FEBS Lett 390: 129-132.
9. Chen, P., Novak, J., Kirk, M., Barnes, S., Qi, F., and Caufield, P.W. (1998) Structure-activity study of the lantibiotic mutacin II from Streptococcus mutans T8 by a gene replacement strategy. Appl Environ Microbiol 64: 2335-2340.
10. Cooper, L.E., McClerren, A.L., Chary, A., and van der Donk, W.A. (2008) Structure-activity relationship studies of the two-component lantibiotic haloduracin. Chem Biol 15: 1035-1045.
11. Cotter, P.D., Hill, C., and Ross, R.P. (2005a) Bacterial lantibiotics: strategies to improve therapeutic potential. Curr Protein Pept Sci 6: 61-75.
12. Cotter, P.D., Hill, C., and Ross, R.P. (2005b) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3: 777-788.
13. Cotter, P.D., O'Connor, P.M., Draper, L.A., Lawton, E.M., Deegan, L.H., Hill, C., and Ross, R.P. (2005c) Posttranslational conversion of L-serines to d-alanines is vital for optimal production and activity of the lantibiotic lacticin 3147. Proc Natl Acad Sci USA 102: 18584-18589.
14. Cotter, P.D., Deegan, L.H., Lawton, E.M., Draper, L.A., O'Connor, P.M., Hill, C., and Ross, R.P. (2006) Complete alanine scanning of the two-component lantibiotic lacticin 3147: generating a blueprint for rational drug design. Mol Microbiol 62: 735-747.
15. Cox, C.R., Coburn, P.S., and Gilmore, M.S. (2005) Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Curr Protein Pept Sci 6: 77-84.
16. Cwirla, S.E., Peters, E.A., Barrett, R.W., and Dower, W.J. (1990) Peptides on phage: a vast library of peptides for identifying ligands. Proc Natl Acad Sci USA 87: 6378-6382.
17. Deegan, L.H., Suda, S., Lawton, E.M., Draper, L.A., Hugenholtz, F., Peschel, A., etal. (2010) Manipulation of charged residues within the two-peptide lantibiotic lacticin 3147. Microb Biotechnol 3: 222-234.
18. Dischinger, J., Josten, M., Szekat, C., Sahl, H.G., and Bierbaum, G. (2009) Production of the novel two-peptide lantibiotic lichenicidin by Bacillus licheniformis DSM 13. PLoS ONE 4: e6788.
19. Field, D., Collins, B., Cotter, P.D., Hill, C., and Ross, R.P. (2007) A system for the random mutagenesis of the two-peptide lantibiotic lacticin 3147: analysis of mutants producing reduced antibacterial activities. J Mol Microbiol Biotechnol 13: 226-234.
20. Field, D., Connor, P.M., Cotter, P.D., Hill, C., and Ross, R.P. (2008) The generation of nisin variants with enhanced activity against specific gram-positive pathogens. Mol Microbiol 69: 218-230.
21. Field, D., Hill, C., Cotter, P.D., and Ross, R.P. (2010a) The dawning of a 'Golden era' in lantibiotic bioengineering. Mol Microbiol 78: 1077-1087.
22. Field, D., Quigley, L., O'Connor, P.M., Rea, M.C., Daly, K., Cotter, P.D., etal. (2010b) Studies with bioengineered Nisin peptides highlight the broad-spectrum potency of Nisin V. Microb Biotechnol 3: 473-486.
23. Field, D., Begley, M., O'Connor, P.M., Daly, K.M., Hugenholtz, F., Cotter, P.D., etal. (2012) Bioengineered nisin a derivatives with enhanced activity against both Gram positive and Gram negative pathogens. PLoS ONE 7: e46884.
24. Galvez, A., Abriouel, H., Lopez, R.L., and Ben Omar, N. (2007) Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120: 51-70.
25. Holo, H., Jeknic, Z., Daeschel, M., Stevanovic, S., and Nes, I.F. (2001) Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology 147: 643-651.
26. Hsu, S.T., Breukink, E., Bierbaum, G., Sahl, H.G., de Kruijff, B., Kaptein, R., etal. (2003) NMR study of mersacidin and lipid II interaction in dodecylphosphocholine micelles. Conformational changes are a key to antimicrobial activity. J Biol Chem 278: 13110-13117.
27. Hyink, O., Balakrishnan, M., and Tagg, J.R. (2005) Streptococcus rattus strain BHT produces both a class I two-component lantibiotic and a class II bacteriocin. FEMS Microbiol Lett 252: 235-241.
28. Islam, M.R., Shioya, K., Nagao, J., Nishie, M., Jikuya, H., Zendo, T., etal. (2009) Evaluation of essential and variable residues of nukacin ISK-1 by NNK scanning. Mol Microbiol 72: 1438-1447.
29. Jing, W., Hunter, H.N., Hagel, J., and Vogel, H.J. (2003) The structure of the antimicrobial peptide Ac-RRWWRF-NH2 bound to micelles and its interactions with phospholipid bilayers. J Pept Res 61: 219-229.
30. van Kraaij, C., Breukink, E., Rollema, H.S., Siezen, R.J., Demel, R.A., De Kruijff, B., and Kuipers, O. (1997) Influence of charge differences in the C-terminal part of nisin on antimicrobial activity and signaling capacity. Eur J Biochem 247: 114-120.
31. van Kraaij, C., Breukink, E., Rollema, H.S., Bongers, R.S., Kosters, H.A., de Kruijff, B., and Kuipers, O. (2000) Engineering a disulfide bond and free thiols in the lantibiotic nisin Z. Eur J Biochem 267: 901-909.
32. Kuipers, O.P., Bierbaum, G., Ottenwalder, B., Dodd, H.M., Horn, N., Metzger, J., etal. (1996) Protein engineering of lantibiotics. Antonie Van Leeuwenhoek 69: 161-169.
33. Lawton, E.M., Cotter, P.D., Hill, C., and Ross, R.P. (2007a) Identification of a novel two-peptide lantibiotic, haloduracin, produced by the alkaliphile Bacillus halodurans C-125. FEMS Microbiol Lett 267: 64-71.
34. Lawton, E.M., Ross, R.P., Hill, C., and Cotter, P.D. (2007b) Two-peptide lantibiotics: a medical perspective. Mini Rev Med Chem 7: 1236-1247.
35. Liu, W., and Hansen, J.N. (1992) Enhancement of the chemical and antimicrobial properties of subtilin by site-directed mutagenesis. J Biol Chem 267: 25078-25085.
36. McClerren, A.L., Cooper, L.E., Quan, C., Thomas, P.M., Kelleher, N.L., and van der Donk, W.A. (2006) Discovery and in vitro biosynthesis of haloduracin, a two-component lantibiotic. Proc Natl Acad Sci USA 103: 17243-17248.
37. Majchrzykiewicz, J.A., Lubelski, J., Moll, G.N., Kuipers, A., Bijlsma, J.J., Kuipers, O.P., and Rink, R. (2010) Production of a class II two-component lantibiotic of Streptococcus pneumoniae using the class I nisin synthetic machinery and leader sequence. Antimicrob Agents Chemother 54: 1498-1505.
38. Morgan, S.M., O'Connor, P.M., Cotter, P.D., Ross, R.P., and Hill, C. (2005) Sequential actions of the two component peptides of the lantibiotic lacticin 3147 explain its antimicrobial activity at nanomolar concentrations. Antimicrob Agents Chemother 49: 2606-2611.
39. Navaratna, M.A., Sahl, H.G., and Tagg, J.R. (1999) Identification of genes encoding two-component lantibiotic production in Staphylococcus aureus C55 and other phage group II S. aureus strains and demonstration of an association with the exfoliative toxin B gene. Infect Immun 67: 4268-4271.
40. O'Connor, E.B., Cotter, P.D., O'Connor, P., O'Sullivan, O., Tagg, J.R., Ross, R.P., and Hill, C. (2007) Relatedness between the two-component lantibiotics lacticin 3147 and staphylococcin C55 based on structure, genetics and biological activity. BMC Microbiol 7: 24.
41. Oman, T.J., Lupoli, T.J., Wang, T.S., Kahne, D., Walker, S., and van der Donk, W.A. (2011) Haloduracin alpha binds the peptidoglycan precursor lipid II with 2:1 stoichiometry. J Am Chem Soc 133: 17544-17547.
42. Piper, C., Cotter, P.D., Ross, R.P., and Hill, C. (2009a) Discovery of medically significant lantibiotics. Curr Drug Discov Technol 6: 1-18.
43. Piper, C., Draper, L.A., Cotter, P.D., Ross, R.P., and Hill, C. (2009b) A comparison of the activities of lacticin 3147 and nisin against drug-resistant Staphylococcus aureus and Enterococcus species. J Antimicrob Chemother 64: 546-551.
44. Rink, R., Wierenga, J., Kuipers, A., Kluskens, L.D., Driessen, A.J., Kuipers, O.P., and Moll, G.N. (2007) Dissection and modulation of the four distinct activities of nisin by mutagenesis of rings A and B and by C-terminal truncation. Appl Environ Microbiol 73: 5809-5816.
45. Rollema, H.S., Kuipers, O.P., Both, P., de Vos, W.M., and Siezen, R.J. (1995) Improvement of solubility and stability of the antimicrobial peptide nisin by protein engineering. Appl Environ Microbiol 61: 2873-2878.
46. Rouse, S., Field, D., Daly, K.M., O'Connor, P.M., Cotter, P.D., Hill, C., and Ross, R.P. (2012) Bioengineered nisin derivatives with enhanced activity in complex matrices. Microb Biotechnol 5: 501-508.
47. Sanderson, J.M., and Whelan, E.J. (2004) Characterisation of the interactions of aromatic amino acids with diacetyl phosphatidylcholine. Phys Chem Chem Phys 6: 1012-1017.
48. Schnell, N., Entian, K.D., Schneider, U., Gotz, F., Zahner, H., Kellner, R., and Jung, G. (1988) Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings. Nature 333: 276-278.
49. Scott, J.K., and Smith, G.P. (1990) Searching for peptide ligands with an epitope library. Science 249: 386-390.
50. Skaugen, M., Nissen-Meyer, J., Jung, G., Stevanovic, S., Sletten, K., Inger, C., etal. (1994) In vivo conversion of L-serine to d-alanine in a ribosomally synthesized polypeptide. J Biol Chem 269: 27183-27185.
51. Suda, S., Lawton, E.M., Wistuba, D., Cotter, P.D., Hill, C., and Ross, R.P. (2011) Homologues and bioengineered derivatives of LtnJ vary in their ability to form D-alanine in the lantibiotic lacticin 3147. J Bacteriol 194: 708-714.
52. Szekat, C., Jack, R.W., Skutlarek, D., Farber, H., and Bierbaum, G. (2003) Construction of an expression system for site-directed mutagenesis of the lantibiotic mersacidin. Appl Environ Microbiol 69: 3777-3783.
53. Wiedemann, I., Breukink, E., van Kraaij, C., Kuipers, O.P., Bierbaum, G., de Kruijff, B., and Sahl, H.G. (2001) Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. J Biol Chem 276: 1772-1779.
54. Wiedemann, I., Bottiger, T., Bonelli, R.R., Wiese, A., Hagge, S.O., Gutsmann, T., etal. (2006) The mode of action of the lantibiotic lacticin 3147 - a complex mechanism involving specific interaction of two peptides and the cell wall precursor lipid II. Mol Microbiol 61: 285-296.
55. Willey, J.M., and van der Donk, W.A. (2007) Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 61: 477-501.
56. Yonezawa, H., and Kuramitsu, H.K. (2005) Genetic analysis of a unique bacteriocin, Smb, produced by Streptococcus mutans GS5. Antimicrob Agents Chemother 49: 541-548.
57. Yuan, J., Zhang, Z.Z., Chen, X.Z., Yang, W., and Huan, L.D. (2004) Site-directed mutagenesis of the hinge region of nisinZ and properties of nisinZ mutants. Appl Microbiol Biotechnol 64: 806-815.