Mutational analysis of the class IIa bacteriocin curvacin A and its orientation in target cell membranes

Applied and Environmental Microbiology

Volumn 74, Issue 21, 2008, Pages 6766-6773

  Haugen, Helén Sophie ^a   Kristiansen, Per Eugen ^a   Fimland, Gunnar ^a,b   Nissen Meyer, Jon ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CELLS; CYTOLOGY; HYDROPHOBICITY; INTERNET; MEMBRANES; POLYPEPTIDES; TARGETS;

ANTIMICROBIAL PEPTIDES; BACTERIOCIN; GLYCINE RESIDUES; HYDROPHILIC; HYDROPHOBIC; HYDROPHOBIC CORES; HYDROPHOBIC REGIONS; INTERFACE REGIONS; MUTATIONAL ANALYSIS; PEDIOCIN; RECEPTOR PROTEINS; TARGET CELLS;

CELL MEMBRANES;

BACTERIOCIN; CURVACIN A; UNCLASSIFIED DRUG;

AMINO ACID; ANTIMICROBIAL ACTIVITY; HYDROPHOBICITY; MUTATION; PEPTIDE; PROTEIN; REPLACEMENT;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANTIMICROBIAL ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; HYDROPHILICITY; HYDROPHOBICITY; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

ANTI-BACTERIAL AGENTS; BACTERIOCINS; CELL MEMBRANE; DNA MUTATIONAL ANALYSIS; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 55049088136     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01068-08     Document Type: Article

References (62)

1. Atrih, A., N. Rekhif, A. J. Moir, A. Lebrihi, and G. Lefebvre. 2001. Mode of action, purification and amino acid sequence of plantaricin C19, an anti-Listeria bacteriocin produced by Lactobacillus plantarum C19. Int. J. Food Microbiol. 68:93-104.
2. Aukrust, T. W., M. B. Brurberg, and I. F. Nes. 1995. Transformation of Lactobacillus by electroporation. Methods Mol. Biol. 47:201-208.
3. Axelsson, L., and A. Holck. 1995. The genes involved in production of and immunity to sakacin A, a bacteriocin from Lactobacillus sake Lb706. J. Bacteriol. 177:2125-2137.
4. Atrih, A., N. Rekhif, A. J. Moir, A. Lebrihi, and G. Lefebvre. 2001. Mode of action, purification and amino acid sequence of plantaricin C19, an anti-Listeria bacteriocin produced by Lactobacillus plantarum C19. Int. J. Food Microbiol. 68:93-104.
5. Aukrust, T. W., M. B. Brurberg, and I. F. Nes. 1995. Transformation of Lactobacillus by electroporation. Methods Mol. Biol. 47:201-208.
6. Axelsson, L., and A. Holck. 1995. The genes involved in production of and immunity to sakacin A, a bacteriocin from Lactobacillus sake Lb706. J. Bacteriol. 177:2125-2137.
7. Axelsson, L., T. Katla, M. Bjornslett, V. G. Eijsink, and A. Holck. 1998. A system for heterologous expression of bacteriocins in Lactobacillus sake. FEMS Microbiol. Lett. 168:137-143.
8. Aymerich, T., H. Holo, L. S. Havarstein, M. Hugas, M. Garriga, and I. F. Nes. 1996. Biochemical and genetic characterization of enterocin A from Enterococcus faecium, a new antilisterial bacteriocin in the pediocin family of bacteriocins. Appl. Environ. Microbiol. 62:1676-1682.
9. Bennik, M. H. J., B. Vanloo, R. Brasseur, L. G. M. Gorris, and E. J. Smid. 1998. A novel bacteriocin with a YGNGV motif from vegetable-associated Enterococcus mundtii; full characterization and interaction with target organisms. Biochim. Biophys. Acta 1373:47-58.
10. Bhugaloo-Vial, P., X. Dousset, A. Métivier, O. Sorokine, P. Anglade, P. Boyaval, and D. Marion. 1996. Purification and amino acid sequence of piscicocins V1a and V1b that display significantly different levels of specific inhibitory activity. Appl. Environ. Microbiol. 62:4410-4416.
11. Chen, Y., R. D. Ludescher, and T. J. Montville. 1997. Electrostatic interactions, but not the YNGNV consensus motif, govern the binding of pediocin PA-1 and its fragments of phospholipid vesicles. Appl. Environ. Microbiol. 63:4770-4777.
12. Cintas, L. M., P. Casaus, L. S. Havarstein, P. E. Hernandez, and I. F. Nes. 1997. Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum. Appl. Environ. Microbiol. 63:4321-4330.
13. Cleveland, J., T. J. Montville, I. F. Nes, and M. L. Chikindas. 2001. Bacteriocins: safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 71:1-20.
14. Corr, S. C., Y. Li, C. U. Riedel, P. W. O'Toole, C. Hill, and C. G. Gahan. 2007. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc. Natl. Acad. Sci. USA 104:7617-7621.
15. Cotter, P. D., C. Hill, and R. P. Ross. 2005. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3:777-788.
16. De Kwaadsteniet, M., T. Fraser, C. A. Van Reenen, and L. M. Dicks. 2006. Bacteriocin T8, a novel class IIa sec-dependent bacteriocin produced by Enterococcus faecium T8, isolated from vaginal secretions of children infected with human immunodeficiency virus. Appl. Environ. Microbiol. 72:4761-4766.
17. Del Campo, R., C. Tenorio, R. Jimenez-Diaz, C. Rubio, R. Gomez-Lus, F. Baquero, and C. Torres. 2001. Bacteriocin production in vancomycin-resistant and vancomycin-susceptible Enterococcus isolates of different origins. Antimicrob. Agents Chemother. 45:905-912.
18. Diep, D. B., L. Godager, D. Brede, and I. F. Nes. 2006. Data mining and characterization of a novel pediocin-like bacteriocin system from the genome of Pediococcus pentosaceus ATCC 25745. Microbiology 152:1649-1659.
19. Diep, D. B., M. Skaugen, Z. Salehian, H. Holo, and I. F. Nes. 2007. Common mechanisms of target cell recognition and immunity for class II bacteriocins. Proc. Natl. Acad. Sci. USA 104:2384-2389.
20. Eguchi, T., K. Kaminaka, J. Shima, S. Kawamoto, K. Mori, S. H. Choi, K. Doi, S. Ohmomo, and S. Ogata. 2001. Isolation and characterization of enterocin SE-K4 produced by thermophilic enterococci, Enterococcus faecalis K-4. Biosci. Biotechnol. Biochem. 65:247-253.
21. Ferchichi, M., J. Frere, K. Mabrouk, and M. Manai. 2001. Lactococcin MMFII, a novel class IIa bacteriocin produced by Lactococcus lactis MMFII, isolated from a Tunisian dairy product. FEMS Microbiol. Lett. 205:49-55.
22. Fimland, G., V. Eijsink, and J. Nissen-Meyer. 2002. Mutational analysis of the role of tryptophan residues in an antimicrobial peptide. Biochemistry 41:9508-9515.
23. Fimland, G., R. Jack, G. Jung, I. F. Nes, and J. Nissen-Meyer. 1998. The bactericidal activity of pediocin PA-1 is specifically inhibited by a 15-mer fragment that spans the bacteriocin from the center toward the C terminus. Appl. Environ. Microbiol. 64:5057-5060.
24. Fimland, G., L. Johnsen, L. Axelsson, M. B. Brurberg, I. F. Nes, V. Eijsink, and J. Nissen-Meyer. 2000. A C-terminal disulfide bridge in pediocin-like bacteriocins renders bacteriocin activity less temperature dependent and is a major determinant of the antimicrobial spectrum. J. Bacteriol. 182:2643-2648.
25. Fimland, G., L. Johnsen, B. Dalhus, and J. Nissen-Meyer. 2005. Pediocin-like antimicrobial peptides (class IIa bacteriocins) and their immunity proteins: biosynthesis, structure, and mode of action. J. Pept. Sci. 11:688-696.
26. Fimland, G., J. Pirneskoski, J. Kaewsrichan, A. Jutila, P. E. Kristiansen, P. K. Kinnunen, and J. Nissen-Meyer. 2006. Mutational analysis and membrane interactions of the beta-sheet-like N-terminal domain of the pediocin-like antimicrobial peptide sakacin P. Biochim. Biophys. Acta 1764:1132-1140.
27. Fimland, G., K. Sletten, and J. Nissen-Meyer. 2002. The complete amino acid sequence of the pediocin-like antimicrobial peptide leucocin C. Biochem. Biophys. Res. Commun. 295:826-827.
28. Fleury, Y., M. Abdel Dayem, J. J. Montagne, E. Chaboisseau, J. P. Le Caer, P. Nicolas, and A. Delfour. 1996. Covalent structure, synthesis, and structure-function studies of mesentericin Y 10537, a defensive peptide from Gram-positive bacteria Leconostoc mesenteroides. J. Biol. Chem. 271:14421-14429.
29. Fregeau Gallagher, N. L., M. Sailer, W. P. Niemczura, T. T. Nakashima, M. E. Stiles, and J. C. Vederas. 1997. Three-dimensional structure of leucocin A in trifluoroethanol and dodecylphosphocholine micelles: spatial location of residues critical for biological activity in type IIa bacteriocins from lactic acid bacteria. Biochemistry 36:15062-15072.
30. Hastings, J. W., M. Sailer, K. Johnson, K. L. Roy, J. C. Vederas, and M. E. Stiles. 1991. Characterization of leucocin A-UAL 187 and cloning of the bacteriocin gene from Leuconostoc gelidum. J. Bacteriol. 173:7491-7500.
31. Haugen, H. S., G. Fimland, J. Nissen-Meyer, and P. E. Kristiansen. 2005. Three-dimensional structure in lipid micelles of the pediocin-like antimicrobial peptide curvacin A. Biochemistry 44:16149-16157.
32. Henderson, J. T., A. L. Chopko, and P. D. van Wassenaar. 1992. Purification and primary structure of pediocin PA-1 produced by Pediococcus acidilactici PAC-1.0. Arch. Biochem. Biophys. 295:5-12.
33. Holck, A., L. Axelsson, S. E. Birkeland, T. Aukrust, and H. Blom. 1992. Purification and amino acid sequence of sakacin A, a bacteriocin from Lactobacillus sake Lb706. J. Gen. Microbiol. 138:2715-2720.
34. Jack, R. W., J. Wan, J. Gordon, K. Harmark, B. E. Davidson, A. J. Hillier, R. E. Wettenhall, M. W. Hickey, and M. J. Coventry. 1996. Characterization of the chemical and antimicrobial properties of piscicolin 126, a bacteriocin produced by Carnobacterium piscicola JG126. Appl. Environ. Microbiol. 62:2897-2903.
35. Johnsen, L., G. Fimland, D. Mantzilas, and J. Nissen-Meyer. 2004. Structure-function analysis of immunity proteins of pediocin-like bacteriocins: C-terminal parts of immunity proteins are involved in specific recognition of cognate bacteriocins. Appl. Environ. Microbiol. 70:2647-2652.
36. Johnsen, L., G. Fimland, and J. Nissen-Meyer. 2005. The C-terminal domain of pediocin-like antimicrobial peptides (class IIa bacteriocins) is involved in specific recognition of the C-terminal part of cognate immunity proteins and in determining the antimicrobial spectrum. J. Biol. Chem. 280:9243-9250.
37. Kalmokoff, M. L., S. K. Banerjee, T. Cyr, M. A. Hefford, and T. Gleeson. 2001. Identification of a new plasmid-encoded sec-dependent bacteriocin produced by Listeria innocua 743. Appl. Environ. Microbiol. 67:4041-4047.
38. Kawamoto, S., J. Shima, R. Sato, T. Eguchi, S. Ohmomo, J. Shibato, N. Horikoshi, K. Takeshita, and T. Sameshima. 2002. Biochemical and genetic characterization of mundticin KS, an antilisterial peptide produced by Enterococcus mundtii NFRI 7393. Appl. Environ. Microbiol. 68:3830-3840.
39. Kazazic, M., J. Nissen-Meyer, and G. Fimland. 2002. Mutational analysis of the role of charged residues in target-cell binding, potency and specificity of the pediocin-like bacteriocin sakacin P. Microbiology 148:2019-2027.
40. Killian, J. A., and G. von Heijne. 2000. How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 25:429-434.
41. Le Marrec, C., B. Hyronimus, P. Bressollier, B. Verneuil, and M. C. Urdaci. 2000. Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I(4). Appl. Environ. Microbiol. 66:5213-5220.
42. Marugg, J. D., C. F. Gonzalez, B. S. Kunka, A. M. Ledeboer, M. J. Pucci, M. Y. Toonen, S. A. Walker, L. C. Zoetmulder, and P. A. Vandenbergh. 1992. Cloning, expression, and nucleotide sequence of genes involved in production of pediocin PA-1, and bacteriocin from Pediococcus acidilactici PAC1.0. Appl. Environ. Microbiol. 58:2360-2367.
43. Metivier, A., M. F. Pilet, X. Dousset, O. Sorokine, P. Anglade, M. Zagorec, J. C. Piard, D. Marion, Y. Cenatiempo, and C. Fremaux. 1998. Divercin V41, a new bacteriocin with two disulphide bonds produced by Carnobacterium divergens V41: primary structure and genomic organization. Microbiology 144:2837-2844.
44. Morisset, D., J. M. Berjeaud, D. Marion, C. Lacombe, and J. Frere. 2004. Mutational analysis of mesentericin Y105, an anti-Listeria bacteriocin, for determination of impact on bactericidal activity, in vitro secondary structure, and membrane interaction. Appl. Environ. Microbiol. 70:4672-4680.
45. Nes, I. F., H. Holo, G. Fimland, H. H. Hauge, and J. Nissen-Meyer. 2001. Unmodified peptide-bactericins (class II) produced by lactic acid bacteria, p. 81-116. In H. Dutton, M. Haxwell, H. McArthur, and R. G. Wax (ed.), Peptide antibiotics: discovery, modes of action and application. Marcel Decker, New York, NY.
46. Nissen-Meyer, J., H. Holo, L. S. Håvarstein, K. Sletten, and I. F. Nes. 1992. A novel lactococcal bacteriocin whose activity depends on the complementary action of two peptides. J. Bacteriol. 174:5686-5692.
47. Nissen-Meyer, J., and I. F. Nes. 1997. Ribosomally synthesized antimicrobial peptides: their function, structure, biogenesis, and mechanism of action. Arch. Microbiol. 167:67-77.
48. Quadri, L. E., M. Sailer, K. L. Roy, J. C. Vederas, and M. E. Stiles. 1994. Chemical and genetic characterization of bacteriocins produced by Carnobacterium piscicola LV17B. J. Biol. Chem. 269:12204- 12211.
49. Saavedra, L., C. Minahk, A. P. D. Holgado, and F. Sesma. 2004. Enhancement of the enterocin CRL35 activity by a synthetic peptide derived from the NH2-terminal sequence. Antimicrob. Agents Chemother. 48:2778-2781.
50. Senes, A., D. E. Engel, and W. F. DeGrado. 2004. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14:465-479.
51. Simon, L., C. Fremaux, Y. Cenatiempo, and J. M. Berjeaud. 2002. Sakacin G, a new type of antilisterial bacteriocin. Appl. Environ. Microbiol. 68:6416-6420.
52. Tahiri, I., M. Desbiens, R. Benech, E. Kheadr, C. Lacroix, S. Thibault, D. Ouellet, and I. Fliss. 2004. Purification, characterization and amino acid sequencing of divergicin M35: a novel class IIa bacteriocin produced by Carnobacterium divergens M35. Int. J. Food Microbiol. 97:123-136.
53. Tichaczek, P. S., J. Nissen-Meyer, I. F. Nes, R. F. Vogel, and W. P. Hammes. 1992. Characterization of the bacteriocins curvacin A and sakacin P produced by Lactobacillus curvatus LTH 1174 and L. sake LTH673. Syst. Appl. Microbiol. 15:460-468.
54. Tomita, H., S. Fujimoto, K. Tanimoto, and Y. Ike. 1996. Cloning and genetic organization of the bacteriocin 31 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pYI17. J. Bacteriol. 178:3585-3593.
55. Uteng, M., H. H. Hauge, I. Brondz, J. Nissen-Meyer, and G. Fimland. 2002. Rapid two-step procedure for large-scale purification of pediocin-like bacteriocins and other cationic antimicrobial peptides from complex culture medium. Appl. Environ. Microbiol. 68:952-956.
56. Uteng, M., H. H. Hauge, P. R. L. Markciwck, G. Fimland, D. Mantzilas, J. Nissen-Meyer, and C. Muhle-Goll. 2003. Three-dimensional structure in lipid micelles of the pediocin-like antimicrobial peptide sakacin P and a sakacin P variant that is structurally stabilized by an inserted C-terminal disulfide bridge. Biochemistry 42:11417-11426.
57. Van Reenen, C. A., M. L. Chikindas, W. H. Van Zyl, and L. M. Dicks. 2003. Characterization and heterologous expression of a class IIa bacteriocin, plantaricin 423 from Lactobacillus plantarum 423, in Saccharomyces cerevisiae. Int. J. Food Microbiol. 81:29-40.
58. Vaughan, A., V. G. Eijsink, T. F. O'Sullivan, K. O'Hanlon, and D. van Sinderen. 2001. An analysis of bacteriocins produced by lactic acid bacteria isolated from malted barley. J. Appl. Microbiol. 91:131-138.
59. von Wright, A., S. Tynkkynen, and M. Suominen. 1987. Cloning of a Streptococcus lactis subsp. lactis chromosomal fragment associated with the ability to grow in milk. Appl. Environ. Microbiol. 53:1584-1588.
60. Wang, Y., M. E. Henz, N. L. Fregeau Gallagher, S. Chai, A. C. Gibbs, L. Z. Yan, M. E. Stiles, D. S. Wishart, and J. C. Vederas. 1999. Solution structure of carnobacteriocin B2 and implications for structure-activity relationships among type IIa bacteriocins from lactic acid bacteria. Biochemistry 38:15438-15447.
61. Yamazaki, K., M. Suzuki, Y. Kawai, N. Inoue, and T. J. Montville. 2005. Purification and characterization of a novel class IIa bacteriocin, piscicocin CS526, from surimi-associated Carnobacterium piscicola CS526. Appl. Environ. Microbiol. 71:554-557.
62. Yan, L. Z., A. C. Gibbs, M. E. Stiles, D. S. Wishart, and J. C. Vederas. 2000. Analogues of bacteriocins: antimicrobial specificity and interactions of leucocin A with its enantiomer, carnobacteriocin B2, and truncated derivatives. J. Med. Chem. 43:4579-4581.