NSR from Streptococcus agalactiae confers resistance against nisin and is encoded by a conserved nsr operon

Biological Chemistry

Volumn 394, Issue 11, 2013, Pages 1543-1549

  Khosa, Sakshi ^a   AlKhatib, Zainab ^a   Smits, Sander H J ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

ABC transporter; Immunity; Lantibiotic; Lipoprotein; Nisin resistance protein; Regulation

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; LIPOPROTEIN; NISIN; NISIN RESISTANCE PROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; CHEMICAL STRUCTURE; LACTOCOCCUS LACTIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STREPTOCOCCUS AGALACTIAE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CONSERVED SEQUENCE; DRUG RESISTANCE, BACTERIAL; LACTOCOCCUS LACTIS; MEMBRANE TRANSPORT PROTEINS; OPERON; STREPTOCOCCUS AGALACTIAE;

EID: 84888124851     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2013-0167     Document Type: Article

References (44)

1. Abts, A., Mavaro, A., Stindt, J., Bakkes, P.J., Metzger, S., Driessen, A.J., Smits, S.H., and Schmitt, L. (2011). Easy and rapid purification of highly active nisin. Int. J. Pept. 2011, 175145.
2. Alkhatib, Z., Abts, A., Mavaro, A., Schmitt, L., and Smits, S.H. (2012). Lantibiotics: how do producers become self-protected? J. Biotechnol. 159, 145-154.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
4. Bernsel, A., Viklund, H., Hennerdal, A., and Elofsson, A. (2009). TOPCONS: consensus prediction of membrane protein topology. Nucl. Acids Res. 37, W465-W468.
5. Bierbaum, G., Szekat, C., Josten, M., Heidrich, C., Kempter, C., Jung, G., and Sahl, H.-G. (1996). Engineering of a novel thioether bridge and role of modified residues in the lantibiotic Pep5. Appl. Environ. Microbiol. 62, 385-392. (Pubitemid 26051563)
6. Carlson, S. and Bauer, H. (1957). A study of problems associated with resistance to nisin. Arch. Hyg. Bakteriol. 141, 445-460.
7. Chatterjee, C., Miller, L.M., Leung, Y.L., Xie, L., Yi, M., Kelleher, N.L., and van der Donk, W.A. (2005a). Lacticin 481 synthetase phosphorylates its substrate during lantibiotic production. J. Am. Chem. Soc. 127, 15332-15333. (Pubitemid 41572483)
8. Chatterjee, C., Paul, M., Xie, L., and van der Donk, W.A. (2005b). Biosynthesis and mode of action of lantibiotics. Chem. Rev. 105, 633-684.
9. Davidson, A.L., Dassa, E., Orelle, C., and Chen, J. (2008). Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364. (Pubitemid 351822295)
10. Froseth, B.R. and McKay, L.L. (1991). Molecular characterization of the nisin resistance region of Lactococcus lactis subsp. lactis biovar diacetylactis DRC3. Appl. Environ. Microbiol. 57, 804-811.
11. Harris, L.J., Fleming, H.P., and Klaenhammer, T.R. (1992). Developments in nisin research. Food Res. Int. 25, 57-66.
12. Hasper, H.E., Kramer, N.E., Smith, J.L., Hillman, J., Zachariah, C., Kuipers, O.P., De Kruijff, B., and Breukink, E. (2006). An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science 313, 1636-1637. (Pubitemid 44414037)
13. Higgins, C.F. and Linton, K.J. (2004). The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11, 918-926. (Pubitemid 39315294)
14. Hirsch, A. (1950). The assay of the antibiotic nisin. J. Gen. Microbiol. 4, 70-83.
15. Holland, I.B., Cole, S.P., Kuchler, K., and Higgins, C.F. (2003). ABC Proteins: From Bacteria to Man (Academic Press) Access Online via Elsevier.
16. Ingram, L.C. (1969). Synthesis of the antibiotic nisin: formation of lanthionine and beta-methyl-lanthionine. Biochim. Biophys. Acta 184, 216-219.
17. Kawada-Matsuo, M., Oogai, Y., Zendo, T., Nagao, J., Shibata, Y., Yamashita, Y., Ogura, Y., Hayashi, T., Sonomoto, K., and Komatsuzawa, H. (2013). Involvement of the novel two-component NsrRS and LcrRS systems in distinct resistance pathways against nisin A and nukacin ISK-1 in Streptococcus mutans. Appl. Environ. Microbiol. 79, 4751-4755.
18. Keiler, K.C., and Sauer, R.T. (1995). Identification of active site residues of the Tsp protease. J. Biol. Chem. 270, 28864-28868.
19. Kleerebezem, M. (2004). Quorum sensing control of lantibiotic production; nisin and subtilin autoregulate their own biosynthesis. Peptides 25, 1405-1414. (Pubitemid 39221524)
20. Kuipers, O.P., Beerthuyzen, M.M., de Ruyter, P.G., Luesink, E.J., and de Vos, W.M. (1995). Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J. Biol. Chem. 270, 27299-27304.
21. Magrane, M. (2011). UniProt Knowledgebase: a hub of integrated protein data. Database: (Oxford) 2011, bar009.
22. Matos, R., Pinto, V.V., Ruivo, M., and Lopes, M.D.F.S. (2009). Study on the dissemination of the bcrABDR cluster in Enterococcus spp. reveals that the BcrAB transporter is sufficient to confer high-level bacitracin resistance. Int. J. Antimicrob. Agents 34, 142-147.
23. Nishie, M., Sasaki, M., Nagao, J., Zendo, T., Nakayama, J., and Sonomoto, K. (2011). Lantibiotic transporter requires cooperative functioning of the peptidase domain and the ATP binding domain. J. Biol. Chem. 286, 11163-11169.
24. Oldham, M.L., Khare, D., Quiocho, F.A., Davidson, A.L., and Chen, J. (2007). Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450, 515-521. (Pubitemid 350190241)
25. Oman, T.J. and van der Donk, W.A. (2009). Insights into the mode of action of the two-peptide lantibiotic haloduracin. ACS Chem. Biol. 4, 865-874.
26. Ra, R., Beerthuyzen, M.M., de Vos, W.M., Saris, P.E., and Kuipers, O.P. (1999). Effects of gene disruptions in the nisin gene cluster of Lactococcus lactis on nisin production and producer immunity. Microbiology 145, 1227-1233. (Pubitemid 29231827)
27. Rawlings, N.D., Barrett, A.J., and Bateman, A. (2012). MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucl. Acid Res. 40, D343-D350.
28. Reisinger, P., Seidel, H., Tschesche, H., and Hammes, W.P. (1980). The effect of nisin on murein synthesis. Arch. Microbiol. 127, 187-193. (Pubitemid 11208251)
29. Rogers, L. (1928). The inhibiting effect of Streptococcus lactis on Lactobacillus bulgaricus. J. Bacteriol. 16, 321-325.
30. Sahl, H.-G. and Bierbaum, G. (1998). Lantibiotics: biosynthesis and biological activities of uniquely modified peptides from Gram-positive bacteria. Annu. Rev. Microbiol. 52, 41-79. (Pubitemid 28481187)
31. Sayers, E.W., Barrett, T., Benson, D.A., Bolton, E., Bryant, S.H., Canese, K., Chetvernin, V., Church, D.M., DiCuccio, M., and Federhen, S. (2010). Database resources of the National Center for Biotechnology Information. Nucl. Acids Res. 38, D5-D16.
32. Schmitt, L. and Tampé, R. (2002). Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 12, 754-760. (Pubitemid 36009492)
33. Siegers, K. and Entian, K. (1995). Genes involved in immunity to the lantibiotic nisin produced by Lactococcus lactis 6F3. Appl. Environ. Microbiol. 61, 1082-1089.
34. Silber, K.R., Keiler, K.C., and Sauer, R.T. (1992). Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini. Proc. Natl. Acad. Sci. USA 89, 295-299.
35. Söding, J. (2005). Protein homology detection by HMM-HMM comparison. Bioinformatics 21, 951-960. (Pubitemid 40467915)
36. Stein, T., Heinzmann, S., Solovieva, I., and Entian, K.D. (2003). Function of Lactococcus lactis nisin immunity genes nisI and nisFEG after coordinated expression in the surrogate host Bacillus subtilis. J. Biol. Chem. 278, 89-94. (Pubitemid 36043548)
37. Stein, T., Heinzmann, S., Düsterhus, S., Borchert, S., and Entian, K.-D. (2005). Expression and functional analysis of the subtilin immunity genes spaIFEG in the subtilin-sensitive host Bacillus subtilis MO1099. J. Bacteriol. 187, 822-828. (Pubitemid 40189755)
38. Sun, Z., Zhong, J., Liang, X., Liu, J., Chen, X., and Huan, L. (2009). Novel mechanism for nisin resistance via proteolytic degradation of nisin by the nisin resistance protein NSR. Antimicrob. Agents Chemother. 53, 1964-1973.
39. Van Der Does, C. and Tampe, R. (2004). How do ABC transporters drive transport? Biol. Chem. 385, 927-933. (Pubitemid 39481140)
40. van der Heide, T. and Poolman, B. (2002). ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep. 3, 938-943. (Pubitemid 35256467)
41. van Heusden, H.E., de Kruijff, B., and Breukink, E. (2002). Lipid II induces a transmembrane orientation of the pore-forming peptide lantibiotic nisin. Biochemistry 41, 12171-12178.
42. 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. (Pubitemid 32109649)
43. Willey, J.M. and van der Donk, W.A. (2007). Lantibiotics: peptides of diverse structure and function. Annu. Rev. Microbiol. 61, 477-501. (Pubitemid 350058218)
44. Zaitseva, J., Oswald, C., Jumpertz, T., Jenewein, S., Wiedenmann, A., Holland, I.B., and Schmitt, L. (2006). A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. EMBO J. 25, 3432-3443. (Pubitemid 44141799)