New Insights into Nisin's Antibacterial Mechanism Revealed by Binding Studies with Synthetic Lipid II Analogues

Biochemistry

Volumn 55, Issue 1, 2016, Pages 232-237

  'T Hart, Peter ^a   Oppedijk, Sabine F ^b   Breukink, Eefjan ^b   Martin, Nathaniel I ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BINS;

ANTIBACTERIAL MECHANISMS; BINDING STUDIES; HIGH AFFINITY; ISOTHERMAL TITRATION CALORIMETRY; MODE OF ACTION; STRONG BINDING; SYNTHETIC LIPID; THERMODYNAMIC PARAMETER;

ANTIBIOTICS;

LIPID; LIPID II ANALOGUE; NISIN; PENTAPEPTIDE; PYROPHOSPHATE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; MURAMYL-NAC-(PENTAPEPTIDE)PYROPHOSPHORYL-UNDECAPRENOL; URIDINE DIPHOSPHATE N ACETYLMURAMIC ACID;

ARTICLE; BINDING AFFINITY; CHANNEL GATING; DRUG BINDING; DRUG MECHANISM; ENTROPY; ISOTHERMAL TITRATION CALORIMETRY; LIPOGENESIS; PRECURSOR; PRIORITY JOURNAL; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; BACTERIUM; CHEMISTRY; LACTOCOCCUS LACTIS; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIA; LACTOCOCCUS LACTIS; MOLECULAR SEQUENCE DATA; NISIN; URIDINE DIPHOSPHATE N-ACETYLMURAMIC ACID;

EID: 84954407099     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b01173     Document Type: Article

References (22)

1. Breukink, E. and de Kruijff, B. (2006) Lipid II as a target for antibiotics Nat. Rev. Drug Discovery 5, 321-332 10.1038/nrd2004
2. Bierbaum, G. and Sahl, H.-G. (2009) Lantibiotics: mode of action, biosynthesis and bioengineering Curr. Pharm. Biotechnol. 10, 2-18 10.2174/138920109787048616
3. Breukink, E., van Heusden, H. E., Vollmerhaus, P. J., Swiezewska, E., Brunner, L., Walker, S., Heck, A. J. R., and de Kruijff, B. (2003) Lipid II is an intrinsic component of the pore induced by nisin in bacterial membranes J. Biol. Chem. 278, 19898-19903 10.1074/jbc.M301463200
4. Breukink, E., Wiedemann, I., Van Kraaij, C., Kuipers, O. P., Sahl, H.-G., and de Kruijff, B. (1999) Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic Science 286, 2361-2364 10.1126/science.286.5448.2361
5. Hsu, S.-T. D., Breukink, E., Tischenko, E., Lutters, M. A. G., de Kruijff, B., Kaptein, R., Bonvin, A. M. J. J., and van Nuland, N. A. J. (2004) The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics Nat. Struct. Mol. Biol. 11, 963-967 10.1038/nsmb830
6. Breukink, E., Van Kraaij, C., Demel, R. A., Siezen, R. J., Kuipers, O. P., and de Kruijff, B. (1997) The C-terminal region of nisin is responsible for the initial interaction of nisin with the target membrane Biochemistry 36, 6968-6976 10.1021/bi970008u
7. Brötz, H., Josten, M., Wiedemann, I., Schneider, U., Götz, F., Bierbaum, G., and Sahl, H.-G. (1998) Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics Mol. Microbiol. 30, 317-327 10.1046/j.1365-2958.1998.01065.x
8. Willey, J. M. and van der Donk, W. A. (2007) Lantibiotics: peptides of diverse structure and function Annu. Rev. Microbiol. 61, 477-501 10.1146/annurev.micro.61.080706.093501
9. Zhou, H., Fang, J., Tian, Y., and Lu, X. Y. (2014) Mechanisms of nisin resistance in Gram-positive bacteria Ann. Microbiol. 64, 413-420 10.1007/s13213-013-0679-9
10. Bonev, B. B., Breukink, E., Swiezewska, E., de Kruijff, B., and Watts, A. (2004) Targeting extracellular pyrophosphates underpins the high selectivity of nisin FASEB J. 18, 1862-1869 10.1096/fj.04-2358com
11. Christ, K., Wiedemann, I., Bakowsky, U., Sahl, H.-G., and Bendas, G. (2007) The role of lipid II in membrane binding of and pore formation by nisin analyzed by two combined biosensor techniques Biochim. Biophys. Acta, Biomembr. 1768, 694-704 10.1016/j.bbamem.2006.12.003
12. Müller, A., Ulm, H., Reder-Christ, K., Sahl, H.-G., and Schneider, T. (2012) Interaction of type A lantibiotics with undecaprenol-bound cell envelope precursors Microb. Drug Resist. 18, 261-270 10.1089/mdr.2011.0242
13. VanNieuwenhze, M. S., Mauldin, S. C., Zia-Ebrahimi, M. S., Aikins, J. A., and Blaszczak, L. C. (2001) The total synthesis of lipid I J. Am. Chem. Soc. 123, 6983-6988 10.1021/ja016082o
14. Danilov, L. L., Druzhinina, T. N., Kalinchuk, N. A., Maltsev, S. D., and Shibaev, V. N. (1989) Polyprenyl phosphates: synthesis and structure-activity relationship for a biosynthetic system of Salmonella anatum O-specific polysaccharide Chem. Phys. Lipids 51, 191-203 10.1016/0009-3084(89)90006-6
15. El Ghachi, M., Bouhss, A., Blanot, D., and Mengin-Lecreulx, D. (2004) The bacA gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity J. Biol. Chem. 279, 30106-30113 10.1074/jbc.M401701200
16. 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 10.1074/jbc.M006770200
17. Al-Kaddah, S., Reder-Christ, K., Klocek, G., Wiedemann, I., Brunschweiger, M., and Bendas, G. (2010) Analysis of membrane interactions of antibiotic peptides using ITC and biosensor measurements Biophys. Chem. 152, 145-152 10.1016/j.bpc.2010.09.002
18. Paiva, A. D., Breukink, E., and Mantovani, H. C. (2011) Role of lipid II and membrane thickness in the mechanism of action of the lantibiotic bovicin HC5 Antimicrob. Agents Chemother. 55, 5284-5293 10.1128/AAC.00638-11
19. Islam, M. R., Nishie, M., Nagao, J., Zendo, T., Keller, S., Nakayama, J., Kohda, D., Sahl, H.-G., and Sonomoto, K. (2012) Ring A of Nukacin ISK-1: A lipid II-binding motif for type-A(II) lantibiotic J. Am. Chem. Soc. 134, 3687-3690 10.1021/ja300007h
20. Yin, N., Marshall, R. L., Matheson, S., and Savage, P. B. (2003) Synthesis of lipid A derivatives and their interactions with polymyxin B and polymyxin B nonapeptide J. Am. Chem. Soc. 125, 2426-2435 10.1021/ja0284456
21. Martin, N. I., Hu, H., Moake, M. M., Churey, J. J., Whittal, R., Worobo, R. W., and Vederas, J. C. (2003) Isolation, structural characterization, and properties of mattacin (polymyxin M), a cyclic peptide antibiotic produced by Paenibacillus kobensis M J. Biol. Chem. 278, 13124-13132 10.1074/jbc.M212364200
22. Velkov, T., Soon, R. L., Chong, P. L., Huang, J. X., Cooper, M. A., Azad, M. A., Baker, M. A., Thompson, P. E., Roberts, K., Nation, R. L., Clements, A., Strugnell, R. A., and Li, J. (2013) Molecular basis for the increased polymyxin susceptibility of Klebsiella pneumoniae strains with under-acylated lipid A Innate Immun. 19, 265-277 10.1177/1753425912459092