Structural and functional diversity of lantibiotic immunity proteins

Current Pharmaceutical Biotechnology

Volumn 12, Issue 8, 2011, Pages 1231-1239

  Okuda, Ken ichi ^a   Sonomoto, Kenji ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Abc transporter; Immunity; Lantibiotic; Membrane protein; Self protection

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; EPICIDIN 280; EPIDERMIN; LACTICIN 481; LANTIBIOTIC; LIPOPROTEIN; MEMBRANE PROTEIN; NISIN A; NUKACIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN; PROTEIN SUBUNIT; SUBLANCIN 168; SUBTILIN; UNCLASSIFIED DRUG;

CELL PROTECTION; EXTRACELLULAR SPACE; GRAM POSITIVE BACTERIUM; HYDROLYSIS; IMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BACTERIOCINS; GRAM-POSITIVE BACTERIA; LIPOPROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA;

POSIBACTERIA;

EID: 79959956372     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920111796117274     Document Type: Review

References (79)

1. Nagao, J.; Asaduzzaman, S.M.; Aso, Y.; Okuda, K.; Nakayama, J.; Sonomoto, K. Lantibiotics: insight and foresight for new paradigm. J. Biosci. Bioeng., 2006, 102(3), 139-149.
2. Chatterjee, C.; Paul, M.; Xie, L.; van der Donk, W.A. Biosynthesis and mode of action of lantibiotics. Chem. Rev., 2005, 105(2), 633-684.
3. Rogers, L.A. The inhibiting effect of Streptococcus lactis on Lactobacillus bulgaricus. J. Bacteriol., 1928, 16(5), 321-325.
4. Delves-Broughton, J.; Blackburn, P.; Evans, R.J.; Hugenholtz, J. Applications of the bacteriocin, nisin. Antonie van Leeuwenhoek, 1996, 69(2), 193-202.
5. Rayman, M.K.; Aris, B.; Hurst, A. Nisin: a possible alternative or adjunct to nitrite in the preservation of meats. Appl. Environ. Microbiol., 1981, 41(2), 375-380.
6. Xie, L.; Miller, L.M.; Chatterjee, C.; Averin, O.; Kelleher, N.L.; van der Donk, W.A. Lacticin 481: in vitro reconstitution of lantibiotic synthetase activity. Science, 2004, 303(5658), 679-681.
7. Kuipers, A.; de Boef, E.; Rink, R.; Fekken, S.; Kluskens, L.D.; Driessen, A.J.; Leenhouts, K.; Kuipers, O.P.; 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., 2004, 279(21), 22176-22182.
8. Rink, R.; Kuipers, A.; de Boef, E.; Leenhouts, K.J.; Driessen, A.J.; Moll, G.N.; Kuipers, O.P. Lantibiotic structures as guidelines for the design of peptides that can be modified by lantibiotic enzymes. Biochemistry, 2005, 44(24), 8873-8882.
9. Kluskens, L.D.; Kuipers, A.; Rink, R.; de Boef, E.; Fekken, S.; Driessen, A.J.; Kuipers, O.P.; Moll, G.N. Post-translational modification of therapeutic peptides by NisB, the dehydratase of the lantibiotic nisin. Biochemistry, 2005, 44(38), 12827-12834.
10. Rink, R.; Wierenga, J.; Kuipers, A.; Kluskens, L.D.; Driessen, A.J.; Kuipers, O.P.; Moll, G.N. Production of dehydroamino acidcontaining peptides by Lactococcus lactis. Appl. Environ. Microbiol., 2007, 73(6), 1792-1796.
11. Peschel, A.; Götz, F. Analysis of the Staphylococcus epidermidis genes epiF, -E, and -G involved in epidermin immunity. J. Bacteriol., 1996, 178(2), 531-536.
12. Rince, A.; Dufour, A.; Uguen, P.; Le Pennec, J.P.; Haras, D. Characterization of the lacticin 481 operon: the Lactococcus lactis genes lctF, lctE, and lctG encode a putative ABC transporter involved in bacteriocin immunity. Appl. Environ. Microbiol., 1997, 63(11), 4252-4260.
13. Otto, M.; Peschel, A.; Götz, F. Producer self-protection against the lantibiotic epidermin by the ABC transporter EpiFEG of Staphylococcus epidermidis Tü3298. FEMS Microbiol. Lett., 1998, 166(2), 203-211.
14. Chen, P.; Qi, F.; Novak, J.; Caufield, P.W. The specific genes for lantibiotic mutacin II biosynthesis in Streptococcus mutans T8 are clustered and can be transferred en bloc. Appl. Environ. Microbiol., 1999, 65(3), 1356-1360.
15. Altena, K.; Guder, A.; Cramer, C.; Bierbaum, G. Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster. Appl. Environ. Microbiol., 2000, 66(6), 2565-2571.
16. Guder, A.; Schmitter, T.; Wiedemann, I.; Sahl, H.-G.; Bierbaum, G. Role of the single regulator MrsR1 and the two-component system MrsR2/K2 in the regulation of mersacidin production and immunity. Appl. Environ. Microbiol., 2002, 68(1), 106-113.
17. Stein, T.; Heinzmann, S.; Solovieva, I.; 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., 2003, 278(1), 89-94.
18. Stein, T.; Heinzmann, S.; Dusterhus, S.; Borchert, S.; Entian, K.D. Expression and functional analysis of the subtilin immunity genes spaIFEG in the subtilin-sensitive host Bacillus subtilis, MO1099. J. Bacteriol., 2005, 187(3), 822-828.
19. Aso, Y.; Okuda, K.; Nagao, J.; Kanemasa, Y.; Thi Bich Phuong, N.; Koga, H.; Shioya, K.; Sashihara, T.; Nakayama, J.; Sonomoto, K. A novel type of immunity protein, NukH, for the lantibiotic nukacin ISK-1 produced by Staphylococcus warneri ISK-1. Biosci. Biotechnol. Biochem., 2005, 69(7), 1403-1410.
20. Fath, M.J.; Kolter, R. ABC transporters: bacterial exporters. Microbiol. Rev., 1993, 57(4), 995-1017.
21. Rees, D.C.; Johnson, E.; Lewinson, O. ABC transporters: the power to change. Nat. Rev. Mol. Cell. Biol., 2009, 10(3), 218-227.
22. Klein, C.; Entian, K.D. Genes involved in self-protection against the lantibiotic subtilin produced by Bacillus subtilis ATCC 6633. Appl. Environ. Microbiol., 1994, 60(8), 2793-2801.
23. Siegers, K.; Entian, K.D. Genes involved in immunity to the lantibiotic nisin produced by Lactococcus lactis 6F3. Appl. Environ. Microbiol., 1995, 61(3), 1082-1089.
24. Okuda, K.; Aso, Y.; Nakayama, J.; Sonomoto, K. Cooperative transport between NukFEG and NukH in immunity against the lantibiotic nukacin ISK-1 produced by Staphylococcus warneri ISK-1. J. Bacteriol., 2008, 190(1), 356-362.
25. Okuda, K.; Yanagihara, S.; Sugayama, T.; Zendo, T.; Nakayama, J.; Sonomoto, K. Functional significance of the E loop, a novel motif conserved in the lantibiotic immunity ATP-binding cassette transport systems. J. Bacteriol., 2010, 192(11), 2801-2808.
26. Jones, P.M.; George, A.M. Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotidebinding subunit. Proc. Natl. Acad. Sci. USA, 2002, 99(20), 12639-12644.
27. Rao, D.K.; Kaur, P. The Q-loop of DrrA is involved in producing the closed conformation of the nucleotide binding domains and in transduction of conformational changes between DrrA and DrrB. Biochemistry, 2008, 47(9), 3038-3050.
28. Oldham, M.L.; Khare, D.; Quiocho, F.A.; Davidson, A.L.; Chen, J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature, 2007, 450(7169), 515-521.
29. Locher, K.P.; Lee, A.T.; Rees, D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science, 2002, 296(5570), 1091-1098.
30. Chen, J.; Lu, G.; Lin, J.; Davidson, A.L.; Quiocho, F.A. A tweezers- like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell, 2003, 12(3), 651-661.
31. Kobayashi, N.; Takenouchi, T.; Endo, S.; Munekata, E. 1H NMR study on the conformation of bacitracin A in aqueous solution. FEBS Lett., 1992, 305(2), 105-109.
32. Stone, K.J.; Strominger, J.L. Mechanism of action of bacitracin: complexation with metal ion and C55-isoprenyl pyrophosphate. Proc. Natl. Acad. Sci. USA, 1971, 68 (12), 3223-3227.
33. Storm, D.R.; Strominger, J.L. Complex formation between bacitracin peptides and isoprenyl pyrophosphates. The specificity of lipid-peptide interactions. J. Biol. Chem., 1973, 248(11), 3940-3945.
34. Putman, M.; van Veen, H.W.; Konings, W.N. Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev., 2000, 64(4), 672-693.
35. Eckford, P.D.; Sharom, F.J. ABC efflux pump-based resistance to chemotherapy drugs. Chem. Rev.,2009, 109(7), 2989-3011.
36. Bolhuis, H.; van Veen, H.W.; Brands, J.R.; Putman, M.; Poolman, B.; Driessen, A.J.; Konings, W.N. Energetics and mechanism of drug transport mediated by the lactococcal multidrug transporter LmrP. J. Biol. Chem., 1996, 271(39), 24123-24128.
37. Bolhuis, H.; van Veen, H.W.; Molenaar, D.; Poolman, B.; Driessen, A.J.; Konings, W.N. Multidrug resistance in Lactococcus lactis: evidence for ATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane. EMBO J., 1996, 15(16), 4239-42345.
38. Shapiro, A.B.; Ling, V. Extraction of Hoechst 33342 from the cytoplasmic leaflet of the plasma membrane by P-glycoprotein. Eur. J. Biochem., 1997, 250(1), 122-129.
39. Shapiro, A.B.; Corder, A.B.; Ling, V. P-glycoprotein-mediated Hoechst 33342 transport out of the lipid bilayer. Eur. J. Biochem., 1997, 250(1), 115-121.
40. van Veen, H.W.; Callaghan, R.; Soceneantu, L.; Sardini, A.; Konings, W.N.; Higgins, C.F. A bacterial antibiotic-resistance gene that complements the human multidrug-resistance P-glycoprotein gene. Nature, 1998, 391(6664), 291-295.
41. van Veen, H.W.; Venema, K.; Bolhuis, H.; Oussenko, I.; Kok, J.; Poolman, B.; Driessen, A.J.; Konings, W.N. Multidrug resistance mediated by a bacterial homolog of the human multidrug transporter MDR1. Proc. Natl. Acad. Sci. USA, 1996, 93(20), 10668-10672.
42. Alqawi, O.; Poelarends, G.; Konings, W.N.; Georges, E. Photoaffinity labeling under non-energized conditions of a specific drugbinding site of the ABC multidrug transporter LmrA from Lactococcus lactis. Biochem. Biophys. Res. Commun., 2003, 311(3), 696-701.
43. Ecker, G.F.; Pleban, K.; Kopp, S.; Csaszar, E.; Poelarends, G.J.; Putman, M.; Kaiser, D.; Konings, W.N.; Chiba, P. A threedimensional model for the substrate binding domain of the multidrug ATP binding cassette transporter LmrA. Mol. Pharmacol., 2004, 66(5), 1169-1179.
44. Aller, S.G.; Yu, J.; Ward, A.; Weng, Y.; Chittaboina, S.; Zhuo, R.; Harrell, P.M.; Trinh, Y.T.; Zhang, Q.; Urbatsch, I.L.; Chang, G. Structure of P-glycoprotein reveals a molecular basis for polyspecific drug binding. Science, 2009, 323(5922), 1718-1722.
45. Engelke, G.; Gutowski-Eckel, Z.; Kiesau, P.; Siegers, K.; Hammelmann, M.; Entian, K.D. Regulation of nisin biosynthesis and immunity in Lactococcus lactis 6F3. Appl. Environ. Microbiol., 1994, 60(3), 814-825.
46. Kuipers, O.P.; Beerthuyzen, M.M.; Siezen, R.J.; de Vos, W.M. 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, 216(1), 281-291.
47. Qiao, M.; Immonen, T.; Koponen, O.; Saris, P.E. The cellular location and effect on nisin immunity of the NisI protein from Lactococcus lactis N8 expressed in Escherichia coli and L. lactis. FEMS Microbiol. Lett., 1995, 131(1), 75-80.
48. Duan, K.; Harvey, M.L.; Liu, C.Q.; Dunn, N.W. Identification and characterization of a mobilizing plasmid, pND300, in Lactococcus lactis M189 and its encoded nisin resistance determinant. J. Appl. Bacteriol., 1996, 81(5), 493-500.
49. Ra, R.; Beerthuyzen, M.M.; de Vos, W.M.; Saris, P.E.; Kuipers, O.P. Effects of gene disruptions in the nisin gene cluster of Lactococcus lactis on nisin production and producer immunity. Microbiology, 1999, 145(5), 1227-1233.
50. Takala, T.M.; Saris, P.E. C terminus of NisI provides specificity to nisin. Microbiology, 2006, 152(12), 3543-3549.
51. Reis, M.; Eschbach-Bludau, M.; Iglesias-Wind, M.I.; Kupke, T.; Sahl, H.-G. Producer immunity towards the lantibiotic Pep5: identification of the immunity gene pepI and localization and functional analysis of its gene product. Appl. Environ. Microbiol., 1994, 60(8), 2876-2883.
52. Hoffmann, A.; Schneider, T.; Pag, U.; Sahl, H.-G. Localization and functional analysis of PepI, the immunity peptide of Pep5- producing Staphylococcus epidermidis strain 5. Appl. Environ. Microbiol., 2004, 70(6), 3263-3271.
53. Heidrich, C.; Pag, U.; Josten, M.; Metzger, J.; Jack, R.W.; Bierbaum, G.; Jung, G.; Sahl, H.-G. Isolation, characterization, and heterologous expression of the novel lantibiotic epicidin 280 and analysis of its biosynthetic gene cluster. Appl. Environ. Microbiol., 1998, 64(9), 3140-3146.
54. Pag, U.; Heidrich, C.; Bierbaum, G.; Sahl, H.-G. Molecular analysis of expression of the lantibiotic Pep5 immunity phenotype. Appl. Environ. Microbiol., 1999, 65(2), 591-598.
55. McAuliffe, O.; Hill, C.; Ross, R.P. Identification and overexpression of ltnl, a novel gene which confers immunity to the twocomponent lantibiotic lacticin 3147. Microbiology, 2000, 146(1), 129-138.
56. Morgan, S.M.; O'Connor P.M.; Cotter, P.D.; Ross, R.P.; Hill, C. Sequential actions of the two component peptides of the lantibiotic lacticin 3147 explain its antimicrobial activity at nanomolar concentrations. Antimicrob. Agents Chemother., 2005, 49(7), 2606-2611.
57. Ryan, M.P.; Rea, M.C.; Hill, C.; Ross, R.P. An application in cheddar cheese manufacture for a strain of Lactococcus lactis producing a novel broad-spectrum bacteriocin, lacticin 3147. Appl. Environ. Microbiol., 1996, 62(2), 612-619.
58. Draper, L.A.; Grainger, K.; Deegan, L.H.; Cotter, P.D.; Hill, C.; Ross, R.P. Cross-immunity and immune mimicry as mechanisms of resistance to the lantibiotic lacticin 3147. Mol. Microbiol., 2009, 71(4), 1043-1054.
59. Coburn, P.S.; Hancock, L.E.; Booth, M.C.; Gilmore, M.S. A novel means of self-protection, unrelated to toxin activation, confers immunity to the bactericidal effects of the Enterococcus faecalis cytolysin. Infect. Immun., 1999, 67(7), 3339-3347.
60. Ike, Y.; Hashimoto, H.; Clewell, D.B. High incidence of hemolysin production by Enterococcus (Streptococcus) faecalis strains associated with human parenteral infections. J. Clin. Microbiol., 1987, 25(8), 1524-1528.
61. Booth, M.C.; Bogie, C.P.; Sahl, H.-G.; Siezen, R.J.; Hatter, K.L.; Gilmore, M.S. Structural analysis and proteolytic activation of Enterococcus faecalis cytolysin, a novel lantibiotic. Mol. Microbiol., 1996, 21(6), 1175-1184.
62. Gilmore, M.S.; Segarra, R.A.; Booth, M.C.; Bogie, C.P.; Hall, L.R.; Clewell, D.B. Genetic structure of the Enterococcus faecalis plasmid pAD1-encoded cytolytic toxin system and its relationship to lantibiotic determinants. J. Bacteriol., 1994, 176(23), 7335-7344.
63. Dubois, J.Y.; Kouwen, T.R.; Schurich, A.K.; Reis, C.R.; Ensing, H.T.; Trip, E.N.; Zweers, J.C.; van Dijl, J.M. Immunity to the bacteriocin sublancin 168 is determined by the SunI (YolF) protein of Bacillus subtilis. Antimicrob. Agents Chemother., 2009, 53(2), 651-661.
64. Okuda, K.; Aso, Y.; Nagao, J.; Shioya, K.; Kanemasa, Y.; Nakayama, J.; Sonomoto, K. Characterization of functional domains of lantibiotic-binding immunity protein, NukH, from Staphylococcus warneri ISK-1. FEMS Microbiol. Lett., 2005, 250(1), 19-25.
65. Okuda, K.; Yanagihara, S.; Shioya, K.; Harada, Y.; Nagao, J.; Aso, Y.; Zendo, T.; Nakayama, J.; Sonomoto, K. Binding specificity of the lantibiotic-binding immunity protein NukH. Appl. Environ. Microbiol., 2008, 74(24), 7613-7619.
66. Kalmokoff, M.L.; Lu, D.; Whitford, M.F.; Teather, R.M. Evidence for production of a new lantibiotic (butyrivibriocin OR79A) by the ruminal anaerobe Butyrivibrio fibrisolvens OR79: characterization of the structural gene encoding butyrivibriocin OR79A. Appl. Environ. Microbiol., 1999, 65(5), 2128-21235.
67. Gomez, A.; Ladire, M.; Marcille, F.; Fons, M. Trypsin mediates growth phase-dependent transcriptional regulation of genes involved in biosynthesis of ruminococcin A, a lantibiotic produced by a Ruminococcus gnavus strain from a human intestinal microbiota. J. Bacteriol., 2002, 184(1), 18-28.
68. Peschel, A.; Schnell, N.; Hille, M.; Entian, K.D.; Götz, F. Secretion of the lantibiotics epidermin and gallidermin: sequence analysis of the genes gdmT and gdmH, their influence on epidermin production and their regulation by EpiQ. Mol. Gen. Genet., 1997, 254(3), 312-318.
69. Hille, M.; Kies, S.; Götz, F.; Peschel, A. Dual role of GdmH in producer immunity and secretion of the Staphylococcal lantibiotics gallidermin and epidermin. Appl. Environ. Microbiol., 2001, 67(3), 1380-1383.
70. Kellner, R.; Jung, G.; Horner, T.; Zahner, H.; Schnell, N.; Entian, K.D.; Götz, F. Gallidermin: a new lanthionine-containing polypeptide antibiotic. Eur. J. Biochem., 1988, 177(1), 53-59.
71. Ottenwalder, B.; Kupke, T.; Brecht, S.; Gnau, V.; Metzger, J.; Jung, G.; Götz, F. Isolation and characterization of genetically engineered gallidermin and epidermin analogs. Appl. Environ. Microbiol., 1995, 61(11), 3894-3903.
72. Hsu, S.T.; Breukink, E.; Tischenko, E.; Lutters, M.A.; de Kruijff, B.; Kaptein, R.; Bonvin, A.M.; van Nuland, N.A. The nisin-lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat. Struct. Mol. Biol., 2004, 11(10), 963-967.
73. Hasper, H.E.; Kramer, N.E.; Smith, J.L.; Hillman, J.D.; Zachariah, C.; Kuipers, O.P.; de Kruijff, B.; Breukink, E. An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science, 2006, 313(5793), 1636-1637.
74. Wiedemann, I.; Bottiger, T.; Bonelli, R.R.; Wiese, A.; Hagge, S.O.; Gutsmann, T.; Seydel, U.; Deegan, L.; Hill, C.; Ross, P.; Sahl, H.- G. 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., 2006, 61(2), 285-296.
75. Hsu, S.T.; Breukink, E.; Bierbaum, G.; Sahl, H.-G.; de Kruijff, B.; Kaptein, R.; van Nuland, N.A.; Bonvin, A.M. NMR study of mersacidin and lipid II interaction in dodecylphosphocholine micelles. Conformational changes are a key to antimicrobial activity. J. Biol. Chem., 2003, 278(15), 13110-13117.
76. Brötz, H.; Bierbaum, G.; Leopold, K.; Reynolds, P.E.; Sahl, H.-G. The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob. Agents Chemother., 1998, 42(1), 154-160.
77. Dufour, A.; Hindre, T.; Haras, D.; Le Pennec, J.P. The biology of lantibiotics from the lacticin 481 group is coming of age. FEMS Microbiol. Rev., 2007, 31(2), 134-167.
78. Islam, M.R.; Shioya, K.; Nagao, J.; Nishie, M.; Jikuya, H.; Zendo, T.; Nakayama, J.; Sonomoto, K. Evaluation of essential and variable residues of nukacin ISK-1 by NNK scanning. Mol. Microbiol., 2009, 72(6), 1438-1447.
79. Higgins, C.F. ABC transporters: physiology, structure and mechanism - an overview. Res. Microbiol., 2001, 152(3-4), 205-210.