Lantibiotics: Insight and foresight for new paradigm

Journal of Bioscience and Bioengineering

Volumn 102, Issue 3, 2006, Pages 139-149

  Nagao, Jun ichi ^a   Asaduzzaman, Sikder M ^a   Aso, Yuji ^a   Okuda, Ken ichi ^a   Nakayama, Jiro ^a   Sonomoto, Kenji ^a,b  

^a Laboratory of Microbial Technology   (Japan)

^b Bio Architecture Center   (Japan)

Author keywords

lantibiotic; peptide engineering; post translational modification; unusual amino acid

Indexed keywords

LANTIBIOTIC; PEPTIDE ENGINEERING; POST TRANSLATIONAL MODIFICATION; UNUSUAL AMINO ACID;

AMINO ACIDS; BACTERIA; BIOSYNTHESIS; ENGINEERING; ENZYMES;

POLYPEPTIDES;

BOVICIN; BUTYRIVIBRIOCIN; EPIDERMIN; ERICIN; LACTICIN; LANTHIOPEPTIN; LANTIBIOTIC; MERSACIDIN; NISIN; NUKACIN; RUMINOCOCCIN; STREPTIN; STREPTOCOCCIN A; SUBLANCIN; SUBTILIN; UNCLASSIFIED DRUG; VANCOMYCIN; VARIACIN;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; BIOLOGICAL ACTIVITY; DRUG DESIGN; DRUG MECHANISM; DRUG SOLUBILITY; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME MODIFICATION; ESCHERICHIA COLI; GENETIC ENGINEERING; GRAM POSITIVE BACTERIUM; IMMUNE SYSTEM; IN VIVO STUDY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUSE STRAIN; NONHUMAN; STRUCTURE ACTIVITY RELATION; VANCOMYCIN RESISTANT ENTEROCOCCUS;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; BACTERIOCINS; PROTEIN ENGINEERING; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY;

POSIBACTERIA;

EID: 33749870689     PISSN: 13891723     EISSN: None     Source Type: Journal    
DOI: 10.1263/jbb.102.139     Document Type: Article

References (86)

1. Tagg J.R., Dajani A.S., and Wannamaker L.W. Bacteriocins of gram-positive bacteria. Bacteriol. Rev. 40 (1976) 722-756
2. Nissen-Meyer J., and Nes I.F. Ribosomally synthesized antimicrobial peptides: their function, biogenesis, and mechanism of action. Arch. Microbiol. 167 (1997) 67-77
3. Ennahar S., Sashihara T., Sonomoto K., and Ishizaki A. Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24 (2000) 85-106
4. de Vos W.M., Kuipers O.P., van der Meer J.R., and Siezen R.J. Maturation pathway of nisin and other lantibiotics: post-translationally modified antimicrobial peptides exported by gram-positive bacteria. Mol. Microbiol. 17 (1995) 427-437
5. Chatterjee C., Paul M., Xie L., and van der Donk W.A. Biosynthesis and mode of action of lantibiotics. Chem. Rev. 105 (2005) 633-684
6. McAuliffe O., Ross R.P., and Hill C. Lantibiotics: structure and mode of action. FEMS Microbiol. Rev. 25 (2005) 285-308
7. Schnell N., Entian K.-D., Schneider U., Götz F., Zahner H., Kellner R., and Jung G. Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings. Nature 333 (1988) 276-277
8. Delves-Broughton J., Blackburn P., Evans R.J., and Hugenholtz J. Applications of the bacteriocin, nisin. Antonie van Leeuwenhoek 69 (1990) 193-202
9. Delves-Broughton J. Nisin and its uses as a food preservative. Food Technol. 44 (1990) 100-117
10. Jung G. Lantibiotics: a survey. In: Jung G., and Sahl H.-G. (Eds). Nisin and novel lantibiotics. (1991), Escom, Leiden, The Netherlands 1-34
11. Gross E., and Morell J.L. The structure of nisin. J. Am. Chem. Soc. 93 (1971) 4634-4635
12. Piard J.-C., Kuipers O.P., Rollema H.S., Desmazeuad M.J., and de Vos W.M. Structure, organization and expression of the lct gene for lacticin 481, a novel lantibiotic produced by Lactococcus lactis. J. Biol. Chem. 268 (1993) 16361-16368
13. Kimura H., Matsusaki H., Sashihara T., Sonomoto K., and Ishizaki A. Purification and partial identification of bacteriocin ISK-1, a new lantibiotic produced by Pediococcus sp. ISK-1. Biosci. Biotechnol. Biochem. 62 (1998) 2341-2345
14. Sashihara T., Kimura H., Higuchi T., Adachi A., Matsusaki H., Sonomoto K., and Ishizaki A. A novel lantibiotic, nukacin ISK-1, of Staphylococcus warneri ISK-1: cloning of the structural gene and elucidation of the structure. Biosci. Biotechnol. Biochem. 64 (2000) 2420-2428
15. Breukink E., Wiedemann I., van Kraaij C., Kuipers O.P., Sahl H.-G., and de Kruijff B. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286 (1999) 2361-2364
16. Wiedemann I., Breukink E., van Kraaij C., Kuipers O.P., Bierbaum G., de Kruijff B., and Sahl H.-G. 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 (2001) 1772-1779
17. Hsu S.-T.D., Breukink E., Tischenko E., Lutters M.A., de Kruijff B., Kaptein R., Bonvin A.M., and van Nuland N.A.J. The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat. Struct. Mol. Biol. 11 (2004) 963-967
18. Kogler H., Bauch M., Fehlhaber H.-W., Griesinger C., Schubert W., and Teetz V. NMR-spectroscopic investigations on mersacidin: a survey. In: Jung G., and Sahl H.-G. (Eds). Nisin and novel lantibiotics. (1991), Escom, Leiden, The Netherlands 159-170
19. Benedict R.G., Dvonch W., Shotwell O.L., Pridham T.G., and Lindenfelser L.A. Cinnamycin, an antibiotic from Streptomyces cinnamoneus nov. sp. Antibiot. Chemother. 2 (1952) 591-594
20. Brötz H., Bierbaum G., Reynolds P.E., and Sahl H.-G. The lantibiotic mersacidin inhibits peptidoglycan biosynthesis at the level of transglycosylation. Eur. J. Biochem. 246 (1997) 193-199
21. Hsu S.-T.D., Breukink E., Bierbaum G., Sahl H.-G., de Kruijff B., Kaptein R., van Nuland N.A.J., and Bonvin A.M.J.J. NMR study of mersacidin and lipid II interaction in dodecylphosphocholine micelles. Conformational changes are a key to antimicrobial activity. J. Biol. Chem. 278 (2003) 13110-13117
22. Kruszewska D., Sahl H.-G., Bierbaum G., Pag U., Hynes S.O., and Ljungh A. Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J. Antimicrob. Chemother. 54 (2004) 648-653
23. Brötz H., Josten M., Wiedemann I., Schneider U., Götz F., Bierbaum G., and Sahl H.-G. Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics. Mol. Microbiol. 30 (1998) 317-327
24. Zendo T., Fukao M., Ueda K., Higuchi T., Nakayama J., and Sonomoto K. Identification of the lantibiotic nisin Q, a new natural nisin variant produced by Lactococcus lactis 61-14 isolated from a river in Japan. Biosci. Biotechnol. Biochem. 67 (2003) 1616-1619
25. Wescombe P.A., and Tagg J.R. Purification and characterization of streptin, a type A1 lantibiotic produced by Streptococcus pyogenes. Appl. Environ. Microbiol. 69 (2003) 2737-2747
26. Xiao H., Chen X., Chen M., Tang S., Zhao X., and Huan L. Bovicin HJ50, a novel lantibiotic produced by Streptococcus bovis HJ50. Microbiology 150 (2004) 103-108
27. Kodani S., Hudson M.E., Durrant M.C., Buttner M.J., Nodwell J.R., and Willey J.M. The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc. Natl. Acad. Sci. USA 101 (2004) 11448-11453
28. 1H-NMR and matrix assisted laser desorption/ionization time-of-flight mass spectrometry. J. Protein Chem. 20 (2001) 501-506
29. Dougherty B.A., Hill C., Weidman J.F., Richardson D.R., Venter J.C., and Ross R.P. Sequence and analysis of the 60 kb conjugative, bacteriocin-producing plasmid pMRC01 from Lactococcus lactis DPC3147. Mol. Microbiol. 29 (1998) 1029-1038
30. Aso Y., Koga H., Sashihara T., Nagao J., Kanemasa Y., Nakayama J., and Sonomoto K. Description of complete DNA sequence of two plasmids from the nukacin ISK-1 producer, Staphylococcus warneri ISK-1. Plasmid 53 (2005) 164-178
31. Sahl H.-G., Jack R.W., and Bierbaum G. Biosynthesis and biological activities of lantibiotics with unique post-translational modifications. Eur. J. Biochem. 230 (1995) 827-853
32. Ingram L.C. Synthesis of the antibiotic nisin: formation of lanthionine and β-methyl-lanthionine. Biochim. Biophys. Acta 184 (1969) 216-219
33. Altena K., Guder A., Cramer C., and Bierbaum G. Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster. Appl. Environ. Microbiol. 66 (2000) 2565-2571
34. Widdick D.A., Dodd H.M., Barraille P., White J., Stein T.H., Chater K.F., Gasson M.J., and Bibb M.J. Cloning and engineering of the cinnamycin biosynthetic gene cluster from Streptomyces cinnamoneus DSM 40005. Proc. Natl. Acad. Sci. USA 100 (2003) 4316-4321
35. van der Meer J.R., Rollema H.S., Siezen R.J., Beerthuyzen M.M., Kuipers O.P., and de Vos W.M. Influence of amino acids substitutions in the nisin leader peptide on biosynthesis and secretion of nisin by Lactococcus lactis. J. Biol. Chem. 269 (1994) 3555-3562
36. Chen P., Qi F., Novak J., Krull R.E., and Caufield P.W. Effect of amino acid substitutions in conserved residues in the leader peptide on biosynthesis of the lantibiotic mutacin II. FEMS Microbiol. Lett. 195 (2001) 139-144
37. Kuipers A., de Boef E., Rink R., Fekken S., Kluskens L.D., Driessen A.J.M., Leenhouts K., Kuipers O.P., and Moll G.N. NisT, the transporter of the lantibiotic nisin, can transport fully modified, dehydrated and unmodified prenisin and fusions of the leader peptide with non-lantibiotic peptides. J. Biol. Chem. 279 (2004) 22176-22182
38. Kluskens L.D., Kuipers A., Rink R., de Boef E., Fekken S., Driessen A.J.M., Kuipers O.P., and Moll G.N. Post-translational modification of therapeutic peptides by NisB, the dehydratase of the lantibiotic nisin. Biochemistry 44 (2005) 12827-12834
39. Meyer C., Bierbaum G., Heidrich C., Reis M., Süling J., Iglesias-Wind M.I., Kempter C., Molitor E., and Sahl H.-G. Nucleotide sequence of the lantibiotic Pep5 biosynthetic gene cluster and functional analysis of PepP and PepC. Evidence for a role of PepC in thioether formation. Eur. J. Biochem. 232 (1995) 478-489
40. Uguen P., Le Pennec J.-P., and Dufour A. Lantibiotic biosynthesis: interaction between prelacticin 481 and its putative modification enzyme, LctM. J. Bacteriol. 182 (2000) 5262-5266
41. Aso Y., Nagao J., Koga H., Okuda K., Kanemasa Y., Sashihara T., Nakayama J., and Sonomoto K. Heterologous expression and functional analysis of the gene cluster for the biosynthesis of and immunity to the lantibiotic, nukacin ISK-1. J. Biosci. Bioeng. 98 (2004) 429-436
42. Siegers K., Heinzman S., and Entian K.-D. Biosynthesis of lantibiotic nisin: posttranslational modification of its prepeptide occurs at a multimeric membrane-associated lanthionine synthetase complex. J. Biol. Chem. 271 (1996) 12294-12301
43. Koponen O., Tolonen M., Qiao M., Wahlstrom G., Helin J., and Saris P.E.J. NisB is required for dehydration and NisC for the lanthionine formation in the post-translational modification of nisin. Microbiology 148 (2002) 3561-3568
44. Li B., Yu J.P., Brunzelle J.S., Moll G.N., van der Donk W.A., and Nair S.K. Structure and mechanism of the lantibiotic cyclase involved in nisin biosynthesis. Science 311 (2006) 1464-1467
45. Okeley N.M., Paul M., Stasser J.P., Blackburn N., and van der Donk W.A. SpaC and NisC, the cyclases involved in subtilin and nisin biosynthesis, are zinc proteins. Biochemistry 42 (2003) 13613-13624
46. Nagao J., Aso Y., Sashihara T., Shioya K., Adachi A., Nakayama J., and Sonomoto K. Localization and interaction of the biosynthetic proteins for the lantibiotic, nukacin ISK-1. Biosci. Biotechnol. Biochem. 69 (2005) 1341-1347
47. Xie L., Miller L.M., Chatterjee C., Averin O., Kelleher N.L., and van der Donk W.A. Lacticin 481: in vitro reconstitution of lantibiotic synthetase activity. Science 303 (2004) 679-681
48. Nagao J., Harada Y., Shioya K., Aso Y., Zendo T., Nakayama J., and Sonomoto K. Lanthionine introduction into nukacin ISK-1 prepeptide by co-expression with the modification enzyme NukM in Escherichia coli. Biochem. Biophys. Res. Commun. 336 (2005) 507-513
49. Chatterjee C., Miller L.M., Leung Y.L., Xie L., Yi M., Kelleher N.L., and van der Donk W.A. Lanticin 481 synthetase phosphorylates its substrate during lantibiotic production. J. Am. Chem. Soc. 127 (2005) 15332-15333
50. Miller L.M., Chatterjee C., van der Donk W.A., and Kelleher N.L. The dehydratase activity of lacticin 481 synthetase is highly processive. J. Am. Chem. Soc. 128 (2005) 1420-1421
51. Schmid D.G., Majer F., Kupke T., and Jung G. Electrospray ionization fourier transform ion cyclotron resonance mass spectrometry to reveal the substrate specificity of the peptidyl-cysteine decarboxylase EpiD. Rapid Commun. Mass Spectrom. 16 (2002) 1779-1784
52. Majer F., Schmid D.G., Altena K., Bierbaum G., and Kupke T. The flavoprotein MrsD catalyzes the oxidative decarboxylation reaction involved in formation of the peptidoglycan biosynthesis inhibitor mersacidin. J. Bacteriol. 184 (2002) 1234-1243
53. Blaesse M., Kupke T., Huber R., and Steinbacher S. Crystal structure of the peptidyl-cysteine decarboxylase EpiD complexed with a pentapeptide substrate. EMBO J. 19 (2000) 6299-6310
54. Blaesse M., Kupke T., Huber R., and Steinbacher S. Structure of MrsD, an FAD-binding protein of the HFCD family. Acta Crystallogr. D Biol. Crystallogr. 59 (2003) 1414-1421
55. Cotter P.D., O'Connor P.M., Draper L.A., Lawton E.M., Deegan L.H., Hill C., and Ross R.P. Posttranslational conversion of l-serines to d-alanines is vital for optimal production and activity of the lactibiotic lacticin 3147. Proc. Natl. Acad. Sci. USA 102 (2005) 18584-18589
56. van der Meer J.R., Polman J., Beerthuyzen M.M., Siezen R.J., Kuipers O.P., and de Vos W.M. Characterization of the Lactococcus lactis nisin A operon genes nisP, encoding a subtilisin-like serine protease involved in precursor processing, and nisR, encoding a regulatory protein involved in nisin biosynthesis. J. Bacteriol. 175 (1993) 2578-2588
57. Geissler S., Götz F., and Kupke T. Serine protease EpiP from Staphylococcus epidermidis catalyzes the processing of the epidermin precursor peptide. J. Bacteriol. 178 (1996) 284-288
58. Håvarstein L.S., Diep D.B., and Nes I.F. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol. Microbiol. 16 (1995) 229-240
59. Franke C.M., Tiemersma J., Venema G., and Kok J. Membrane topology of the lactococcal bacteriocin ATP-binding cassette transporter protein LcnC. Involvement of LcnC in lactococcin a maturation. J. Biol. Chem. 274 (1999) 8484-8490
60. Uguen P., Hindré T., Didelot S., Marty C., Haras D., Le Pennec J.-P., Vallée-Réhel K., and Dufour A. Maturation by LctT is required for biosynthesis of full-length lantibiotic lacticin 481. Appl. Environ. Microbiol. 71 (2005) 562-565
61. Covey C., Stein T., Düsterhus S., Karas M., and Entian K.-D. Activation of subtilin precursors by Bacillus subtilis extracellular serine protease subtilisin (AprE), WprA, and Vpr. Biochem. Biophys. Res. Commun. 304 (2003) 48-54
62. van Kraaij C., Breukink E., Rollema H.S., Bongers R.S., Kosters H.A., de Kruijff B., and Kuipers O.P. Engineering a disulfide bond and free thiols in the lantibiotic nisin Z. Eur. J. Biochem. 230 (1995) 827-853
63. Bierbaum G., Szekat C., Josten M., Heidrich C., Kempter C., Jung G., and Sahl H.-G. Engineering of a novel thioether bridge and role of modified residues in the lantibiotic Pep5. Appl. Environ. Microbiol. 62 (1996) 385-392
64. Breukink E., Ganz P., de Kruijff B., and Seelig J. Binding of nisin Z to bilayer vesicles as determined with isothermal titration calorimetry. Biochemistry 39 (2000) 10247-10254
65. Giffard C.J., Dodd H.M., Horn N., Ladha S., Machie A.R., Parr A., Gasson M.J., and Sanders D. Structure-function relations of variant and fragments nisin studied with model membrane systems. Biochemistry 36 (1997) 3802-3810
66. Winkowski K., Ludescher R.D., and Montville T. Physicochemical characterization of the nisin-membrane interaction with liposome derived from Listeria monocytogenes. Appl. Environ. Microbiol. 62 (1996) 323-327
67. van Heusden H., de Kruijff B., and Breukink E. Lipid II induces an overall transmembrane orientation of the pore-forming peptide lantibiotic nisin. Biochemistry 41 (2002) 12171-12178
68. Turner D.L., Brennan L., Meyer H.E., Lohaus C., Siethoff C., Costa H.S., Gonzalez B., Santos H., and Suarez J.E. Solution structure of plantaricin C, a novel lantibiotic. Eur. J. Biochem. 264 (1999) 833-839
69. Jack R., Benz R., Tagg J., and Sahl H.-G. The mode of action of SA-FF, a lantibiotic isolated from Streptococcus pyrogenes strain FF22. Eur. J. Biochem. 219 (1994) 699-705
70. Chikindas M.L., Novak J., Driessen A.J., Konings W.N., Schilling K.M., and Caufield P.W. Mutacin II, a bacteriocidal lantibiotic from Streptococcus mutans, Antimicrob. Agents Chemother. 39 (1995) 2656-2660
71. Asaduzzaman S.M., Nagao J., Aso Y., Nakayama J., and Sonomoto K. Lysine-oriented charges trigger the membrane binding and activity of nukacin ISK-1. Appl. Environ. Microbiol. 72 (2006) 6012-6017
72. Bierbaum G., Reis M., Szekat C., and Sahl H.-G. Construction of an expression system for engineering of the lantibiotic Pep5. Appl. Environ. Microbiol. 60 (1994) 4332-4338
73. Kuipers O.P., Rollema H.S., Yap W.M.G.J., Boot H.J., Siezen R.J., and de Vos W.M. Engineering dehydrated amino acid residues in the antimicrobial peptide nisin. J. Biol. Chem. 267 (1992) 24340-24346
74. Szekat C., Jack R.W., Skutlarek D., Färber H., and Bierbaum G. Construction of an expression system for site-directed mutagenesis of the lantibiotic mersacidin. Appl. Environ. Microbiol. 69 (2003) 3777-3783
75. Chen P., Novak J., Kirk M., Barnes S., Qi F., and Caufield P.W. Structure-activity study of the lantibiotic mutacin II from Streptococcus mutans T8 by a gene replacement strategy. Appl. Environ. Microbiol. 64 (1998) 2335-2340
76. Chakicherla A., and Hansen J.N. Role of the leader and structural region of prelantibiotic peptides as assessed by expressing nisin-subtilin chimeras in Bacillus subtilis 168, and characterization of their physical, chemical, and antimicrobial properties. J. Biol. Chem. 270 (1995) 23533-23539
77. Liu W., and Hansen J.N. Enhancement of the chemical and antimicrobial properties of subtilin by site-directed mutagenesis. J. Biol. Chem. 267 (1992) 25078-25085
78. Yuan J., Zhang Z.-Z., Chen X.-Z., Yang W., and Huan L.-D. Site-directed mutagenesis of the hinge region of nisinZ and properties of nisinZ mutants. Appl. Microbiol. Biotechnol. 64 (2004) 806-815
79. Osapay G., Prokai L., Kim H.-S., Medzihradszky K.F., Coy D.H., Liapakins G., Reisine T., Melacini G., Zhu Q., Wang S.H.-H., Mattern R.-H., and Goodman M. Lanthionine-somatostatin analogs: synthesis, characterization, biological activity, and enzymatic stability studies. J. Med. Chem. 40 (1997) 2241-2251
80. Rew Y., Malkmus S., Svensson C., Yaksh T.L., Chung N.N., Schiller P.W., Cassel J.A., DeHaven R.N., and Goodman M. Synthesis and biological activities of cyclic lanthionine enkephalin analogues: δ-opioid receptor selective ligands. J. Med. Chem. 45 (2002) 3746-3754
81. Rink R., Kuipers A., de Boef E., Leenhouts K.J., Driessen A.J., Moll G.N., and Kuipers O.P. Lantibiotic structures as guidelines for the design of peptides that can be modified by lantibiotic enzymes. Biochemistry 44 (2005) 8873-8882
82. Stein T., Heinzmann S., Solovieva I., and Entian K.-D. Function of Lactococcus lactis nisin immunity genes nisI and nisFEG after coordinated expression in the surrogate host Bacillus subtilis. J. Biol. Chem. 278 (2003) 89-94
83. Stein T., Heinzmann S., Dusterhus S., Borchert S., and Entian K.-D. Expression and functional analysis of the subtilin immunity genes spaIFEG in the subtilin-sensitive host Bacillus subtilis MO1099. J. Bacteriol. 187 (2005) 822-828
84. Aso Y., Okuda K., Nagao J., Kanemasa Y., Phuogh N.T.B., Shioya K., Sashihara T., Nakayama J., and Sonomoto K. A novel type of immunity protein, NukH, for the lantibiotic nukacin ISK-1 produced by Staphylococcus warneri ISK-1. Biosci. Biotechnol. Biochem. 69 (2005) 1403-1410
85. Okuda K., Aso Y., Nagao J., Shioya K., Kanemasa Y., Nakayama J., and Sonomoto K. Characterization of functional domains of lantibiotic-binding immunity protein, NukH, from Staphylococcus warneri ISK-1. FEMS Microbiol. Lett. 250 (2005) 19-25
86. Lee K.H. Development of short antimicrobial peptides derived from host defense peptide or by combinatorial libraries. Curr. Pharm. 8 (2002) 795-813