Home LiteratureArticle Details
PMID: 17660303 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Dissection and modulation of the four distinct activities of nisin by mutagenesis of rings A and B and by C-terminal truncation.

Applied and environmental microbiology ·Vol. 73 ·No. 18 ·2007-09-00 ·Pages 5809-16

Rink R, Wierenga J, Kuipers A, Kluskens LD, Driessen AJ, Kuipers OP, Moll GN

Abstract

Nisin A is a pentacyclic antibiotic peptide produced by various Lactococcus lactis strains. Nisin displays four different activities: (i) it autoinduces its own synthesis; (ii) it inhibits the growth of target bacteria by membrane pore formation; (iii) it inhibits bacterial growth by interfering with cell wall synthesis; and, in addition, (iv) it inhibits the outgrowth of spores. Here we investigate the structural requirements and relevance of the N-terminal thioether rings of nisin by randomization of the ring A and B positions. The data demonstrate that: (i) mutation of ring A results in variants with enhanced activity and a modulated spectrum of target cells; (ii) for the cell growth-inhibiting activity of nisin, ring A is rather promiscuous with respect to its amino acid composition, whereas the bulky amino acid residues in ring B abolish antimicrobial activity; (iii) C-terminally truncated nisin A mutants lacking rings D and E retain significant antimicrobial activity but are unable to permeabilize the target membrane; (iv) the dehydroalanine in ring A is not essential for the inhibition of the outgrowth of Bacillus cells; (v) some ring A mutants have significant antimicrobial activities but have decreased autoinducing activities; (vi) the opening of ring B eliminates antimicrobial activity while retaining autoinducing activity; and (vii) some ring A mutants escape the nisin immune system(s) and are toxic to the nisin-producing strain NZ9700. These data demonstrate that the various activities of nisin can be engineered independently and provide a basis for the design and synthesis of tailor-made analogs with desired activities.

MeSH Terms
Anti-Bacterial Agents/biosynthesis,chemistry Bacteria/drug effects,growth & development Bacterial Proteins Mutagenesis Mutagenesis, Site-Directed Nisin/biosynthesis,chemistry,genetics,pharmacology Protein Conformation Protein Engineering/methods Recombinant Proteins/chemistry,pharmacology Structure-Activity Relationship
Chemicals
Anti-Bacterial Agents Bacterial Proteins Recombinant Proteins Nisin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Rink Rick
BiOMaDe Technology Foundation, Nijenborgh 4, 9747 AG Groningen, The Netherlands.
Wierenga Jenny
Kuipers Anneke
Kluskens Leon D
Driessen Arnold J M
Kuipers Oscar P
Moll Gert N
References (41)
41 references, click to expand
  1. Regulation of bacterial sugar-H+ symport by phosphoenolpyruvate-dependent enzyme I/HPr-mediated phosphorylation.
    Proc Natl Acad Sci U S A. 1995 Jan 31;92(3):778-82 PMID: 7846050
  2. An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II.
    Science. 2006 Sep 15;313(5793):1636-7 PMID: 16973881
  3. Engineering a disulfide bond and free thiols in the lantibiotic nisin Z.
    Eur J Biochem. 2000 Feb;267(3):901-9 PMID: 10651829
  4. Lantibiotic structures as guidelines for the design of peptides that can be modified by lantibiotic enzymes.
    Biochemistry. 2005 Jun 21;44(24):8873-82 PMID: 15952794
  5. Plantaricin A is an amphiphilic alpha-helical bacteriocin-like pheromone which exerts antimicrobial and pheromone activities through different mechanisms.
    Biochemistry. 1998 Nov 17;37(46):16026-32 PMID: 9819195
  6. Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction.
    J Biol Chem. 1995 Nov 10;270(45):27299-304 PMID: 7592991
  7. Identification and characterization of some bacterial membrane sulfhydryl groups which are targets of bacteriostatic and antibiotic action.
    J Biol Chem. 1984 Nov 10;259(21):13590-4 PMID: 6436249
  8. Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Requirement of expression of the nisA and nisI genes for development of immunity.
    Eur J Biochem. 1993 Aug 15;216(1):281-91 PMID: 7689965
  9. Novel surface display system for proteins on non-genetically modified gram-positive bacteria.
    Appl Environ Microbiol. 2006 Jan;72(1):880-9 PMID: 16391130
  10. The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics.
    Nat Struct Mol Biol. 2004 Oct;11(10):963-7 PMID: 15361862
  11. Molecular and genetic characterization of a novel nisin variant produced by Streptococcus uberis.
    Appl Environ Microbiol. 2006 Feb;72(2):1148-56 PMID: 16461661
  12. 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. 2001 Jan 19;276(3):1772-9 PMID: 11038353
  13. Structure-activity relationships in the peptide antibiotic nisin: role of dehydroalanine 5.
    Appl Environ Microbiol. 1996 Aug;62(8):2966-9 PMID: 8702290
  14. Elucidation of the primary structure of the lantibiotic epilancin K7 from Staphylococcus epidermidis K7. Cloning and characterisation of the epilancin-K7-encoding gene and NMR analysis of mature epilancin K7.
    Eur J Biochem. 1995 Jun 1;230(2):587-600 PMID: 7607233
  15. Engineering dehydrated amino acid residues in the antimicrobial peptide nisin.
    J Biol Chem. 1992 Dec 5;267(34):24340-6 PMID: 1447185
  16. Improved medium for lactic streptococci and their bacteriophages.
    Appl Microbiol. 1975 Jun;29(6):807-13 PMID: 16350018
  17. Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis.
    Biochimie. 1988 Apr;70(4):559-66 PMID: 2844302
  18. Controlled overproduction of proteins by lactic acid bacteria.
    Trends Biotechnol. 1997 Apr;15(4):135-40 PMID: 9131833
  19. Catabolic repression of bacterial sporulation.
    Proc Natl Acad Sci U S A. 1965 Sep;54(3):704-11 PMID: 4956288
  20. Construction of a food-grade multiple-copy integration system for Lactococcus lactis.
    Appl Microbiol Biotechnol. 1998 Apr;49(4):417-23 PMID: 9615484
  21. Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics.
    Mol Microbiol. 1998 Oct;30(2):317-27 PMID: 9791177
  22. Lipid II is an intrinsic component of the pore induced by nisin in bacterial membranes.
    J Biol Chem. 2003 May 30;278(22):19898-903 PMID: 12663672
  23. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic.
    Science. 1999 Dec 17;286(5448):2361-4 PMID: 10600751
  24. Molecular analysis of the regulation of nisin immunity.
    Microbiology. 1996 Sep;142 ( Pt 9):2385-92 PMID: 8828206
  25. Post-translational modification of therapeutic peptides by NisB, the dehydratase of the lantibiotic nisin.
    Biochemistry. 2005 Sep 27;44(38):12827-34 PMID: 16171398
  26. The complete genome sequence of the gram-positive bacterium Bacillus subtilis.
    Nature. 1997 Nov 20;390(6657):249-56 PMID: 9384377
  27. Transformation of Lactococcus by electroporation.
    Methods Mol Biol. 1995;47:195-9 PMID: 7550735
  28. Protein engineering of lantibiotics.
    Antonie Van Leeuwenhoek. 1996 Feb;69(2):161-69 PMID: 8775976
  29. Assembly and stability of nisin-lipid II pores.
    Biochemistry. 2004 Sep 14;43(36):11567-75 PMID: 15350143
  30. Enhancement of the chemical and antimicrobial properties of subtilin by site-directed mutagenesis.
    J Biol Chem. 1992 Dec 15;267(35):25078-85 PMID: 1460009
  31. Resistance of Gram-positive bacteria to nisin is not determined by lipid II levels.
    FEMS Microbiol Lett. 2004 Oct 1;239(1):157-61 PMID: 15451114
  32. Role of transmembrane pH gradient and membrane binding in nisin pore formation.
    J Bacteriol. 1997 Jan;179(1):135-40 PMID: 8981990
  33. Influence of charge differences in the C-terminal part of nisin on antimicrobial activity and signaling capacity.
    Eur J Biochem. 1997 Jul 1;247(1):114-20 PMID: 9249016
  34. Structure-activity relationships in the peptide antibiotic nisin: antibacterial activity of fragments of nisin.
    FEBS Lett. 1996 Jul 22;390(2):129-32 PMID: 8706842
  35. Biosynthesis and mode of action of lantibiotics.
    Chem Rev. 2005 Feb;105(2):633-84 PMID: 15700960
  36. Lipid II induces a transmembrane orientation of the pore-forming peptide lantibiotic nisin.
    Biochemistry. 2002 Oct 8;41(40):12171-8 PMID: 12356318
  37. 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. 2004 May 21;279(21):22176-82 PMID: 15044440
  38. Insights into in vivo activities of lantibiotics from gallidermin and epidermin mode-of-action studies.
    Antimicrob Agents Chemother. 2006 Apr;50(4):1449-57 PMID: 16569864
  39. Structure and biological activity of chemically modified nisin A species.
    Eur J Biochem. 1996 Nov 1;241(3):716-22 PMID: 8944757
  40. Site-directed mutagenesis of the hinge region of nisinZ and properties of nisinZ mutants.
    Appl Microbiol Biotechnol. 2004 Jun;64(6):806-15 PMID: 15048591
  41. Inhibition of virulence factor expression in Staphylococcus aureus by the Staphylococcus epidermidis agr pheromone and derivatives.
    FEBS Lett. 1999 May 7;450(3):257-62 PMID: 10359085
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
0099-2240
Published
2007-09-00
Epub
2007-00-27
Pages
5809-16
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC2074915
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com