Immunochemical characterization of temperature-regulated production of enterocin L50 (EntL50A and EntL50B), enterocin P, and enterocin Q by Enterococcus faecium L50

Applied and Environmental Microbiology

Volumn 72, Issue 12, 2006, Pages 7634-7643

  Criado, Raquel ^a   Gutiérrez, Jorge ^a   Martín, María ^a   Herranz, Carmen ^a   Hernández, Pablo E ^a   Cintas, Luis M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; ANTIBODIES; BIOASSAY; IMMUNIZATION; PROTEINS; SYNTHESIS (CHEMICAL);

ENTEROCIN; ENTEROCOCCUS FAECIUM; ENZYME-LINKED IMMUNOSORBENT ASSAY (ELISA); IMMUNOCHEMICAL CHARACTERIZATION;

MICROBIOLOGY;

ANTIBODY; BACTERIOCIN; CARRIER PROTEIN; ENTEROCIN L50A; ENTEROCIN L50A ANTIBODY; ENTEROCIN L50B; ENTEROCIN L50B ANTIBODY; ENTEROCIN P; ENTEROCIN Q; ENTEROCIN Q ANTIBODY; KEYHOLE LIMPET HEMOCYANIN; POLYCLONAL ANTIBODY;

ANTIBODY; BACTERIUM; ENZYME; IMMUNIZATION; IMMUNOASSAY; PEPTIDE; SMALL MAMMAL;

ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; CARBOXY TERMINAL SEQUENCE; COMPETITIVE INDIRECT ENZYME LINKED IMMUNOSORBENT ASSAY; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS FAECIUM L50; ENZYME LINKED IMMUNOSORBENT ASSAY; EVALUATION; IMMUNIZATION; IMMUNOCHEMISTRY; NON COMPETITIVE INDIRECT ENZYME LINKED IMMUNOSORBENT ASSAY; NONHUMAN; PLASMID; PROTEIN ANALYSIS; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEOMICS; QUANTITATIVE ANALYSIS; RABBIT; SENSITIVITY AND SPECIFICITY; SERUM; SYNTHESIS; TEMPERATURE SENSITIVITY;

ANIMALS; ANTIBODIES; ANTIBODY SPECIFICITY; BACTERIOCINS; ENTEROCOCCUS FAECIUM; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; MEAT PRODUCTS; RABBITS; TEMPERATURE;

ANIMALIA; ENTEROCOCCUS FAECIUM; ORYCTOLAGUS CUNICULUS;

EID: 33845523513     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00983-06     Document Type: Article

References (66)

1. Aasen, I. M., T. Møretro, T. Katla, L. Axelsson, and I. Storrø. 2000. Influence of complex nutrients, temperature and pH on bacteriocin production by Lactobacillus sakei CCUG 42687. Appl. Microbiol. Biotechnol. 53:159-166.
2. Abriouel, H., E. Valdivia, M. Martinez-Bueno, M. Maqueda, and A. Gálvez. 2003. A simple method for semi-preparative-scale production and recovery of enterocin AS-48 derived from Enterococcus faecalis subsp. liquefaciens A-48-32. J. Microbiol. Methods 55:599-605.
3. Audisio, M. C., H. R. Terxolo, and M. C. Apella. 2005. Bacteriocin from honeybee beebread Enterococcus avium, active against Listeria monocytogenes. Appl. Environ. Microbiol. 71:3373-3375.
4. Avrameas, S., and T. Termync. 1969. The cross-linking of proteins with glutaraldehyde and its use for the preparation of immunoadsorbents. Immunochemistry 6:53-56.
5. Benech, R. O., E. E. Kheadr, C. Lacroix, and I. Fliss. 2002. Antibacterial activities of nisin Z encapsulated in liposomes or produced in situ by mixed culture during Cheddar cheese ripening. Appl. Environ. Microbiol. 68:5607-5619.
6. Bouksaim, M., C. Lacroix, R. Bazin, and R. E. Simard. 1999. Production and utilization of polyclonal antibodies against nisin in an ELISA and for immuno-location of nisin in producing and sensitive bacterial strains. J. Appl. Microbiol. 87:500-510.
7. Bouksaim, M., C. Lacroix, P. Audet, and R. E. Simard. 2000. Effects of mixed starter composition on nisin Z production by Lactococcus lactis subsp. lactis biovar diacelylactis UL 719 during production and ripening of Gouda cheese. Int. J. Food Microbiol. 59:141-156.
8. Casaus, P., T. Nilsen, L. M. Cintas, I. F. Nes, P. E. Hernández, and H. Holo. 1997. Enterocin B, a new bacteriocin from Enterococcus faecium T136 which can act synergistically with enterocin A. Microbiology 143:2287-2294.
9. Cintas, L. M., J. M. Rodríguez, M. F. Fernández, K. Sletten, I. F. Nes, P. E. Hernández, and H. Holo. 1995. Isolation and characterization of pcdiocin L50, a new bacteriocin from Pediococcus acidilactici with a broad inhibitory spectrum. Appl. Environ. Microbiol. 61:2643-2648.
10. Cintas, L. M., P. Casaus, M. F. Fernández, and P. E. Hernández. 1998. Comparative antimicrobial activity of enterocin L50, pediocin PA-1, nisin A and lactocin S against spoilage and foodborne pathogenic bacteria. Food Microbiol. 15:289-298.
11. Cintas, L. M., P. Casaus, H. Holo, P. E. Hernández, I. F. Nes, and L. S. Håvarstein. 1998. Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins. J. Bacteriol. 180:1988-1994.
12. Cintas, L. M., P. Casaus, C. Herranz, L. S. Håvarstein, H. Holo, P. E. Hernández, and I. F. Nes. 2000. Biochemical and genetic evidence that Enterococcus faecium L50 produces enterocins L50A and L50B, the sec-dependent enterocin P, and a novel bacteriocin secreted without an N-terminal extension termed enterocin Q. J. Bacteriol. 182:6806-6814.
13. Cintas, L. M., P. Casaus, C. Herranz, I. F. Nes, and P. E. Hernández. 2001. Bacteriocins of lactic acid bacteria. Food Sci. Tech. Int. 7:281-305.
14. 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.
15. Criado, R., D. B. Diep, Å. Aakra, J. Gutiérrez, I. F. Nes, P. E. Hernández, and L. M. Cintas. 2006. Complete sequence of the enterocin Q-encoding plasmid pCIZ2 from the multiple bacteriocin producer Enterococcus faecium L50 and genetic characterization of enterocin Q production and immunity. Appl. Environ. Microbiol. 72:6653-6666.
16. Daoudi, L., C. Turcotte, C. Lacroix, and I. Fliss. 2001. Production and characterization of anti-nisin Z monoclonal antibodies: suitability for distinguishing active from inactive forms through a competitive enzyme immunoassay. Appl. Microbiol. Biotechnol. 56:114-119.
17. Delgado, A., D. Brito, C. Peres, F. Noé,-Arroyo, and A. Garrido-Fernández. 2005. Bacteriocin production by Lactobacillus pentosus B96 can be expressed as a function of temperature and NaCl concentration. Food Microbiol. 22:521-528.
18. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
19. de Vuyst, L., R. Callewaert, and K. Crabbe. 1996. Primary metabolite kinetics of bacteriocin biosynthesis by Lactobacillus amylovorus and evidence for stimulation of bacteriocin production under unfavourable growth conditions. Microbiology 142:817-827.
20. Diep, D. B., L. Axelsson, C. Grefsli, and I. F. Nes. 2000. The synthesis of the bacteriocin sakacin A is a temperature-sensitive process regulated by a pheromone peptide through a three-component regulatory system. Microbiology 146:2155-2160.
21. 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.
22. Ennahar, S., T. Sashihara, K. Sonomoto, and A. Ishizaki. 2000. Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24:85-106.
23. Falahee, M. B., M. R. Adams, J. W. Dale, and B. A. Morris. 1990. An enzyme immunoassay for nisin. Int. J. Food Sci. Technol. 25:590-595.
24. Foulquié-Moreno, M. R., P. Sarantinopoulos, E. Tsakalidou, and L. de Vuyst. 2006. The role and application of enterococci in food and health. Int. J. Food Microbiol. 106:1-24.
25. Franz, C. M. A., U. Schillinger, and W. H. Holzapfel. 1996. Production and characterization of enterocin 900, a bacteriocin produced by Enterococcus faecium BFE 900 from black olives. Int. J. Food Microbiol. 29:255-270.
26. Garneau, S., N. I. Martin, and J. C. Vederas. 2002. Two-peptide bacteriocins produced by lactic acid bacteria. Biochimie 84:577-592.
27. Giraffa, G. 1995. Enterococcal bacteriocins: their potential as anti-Listeria factors in the dairy technology. Food Microbiol. 12:291-299.
28. Grome, N. P. 1994. Immunoassays of proteins and anti-peptide antibodies, p. 139-179. In G. R. Wisdom (ed.), Peptide antigens: a practical approach. IRL Press, Oxford, United Kingdom.
29. Gutiérrez, J., R. Criado, R. Citti, M. Martin, C. Herranz, M. F. Fernández, L. M. Cintas, and P. E. Hernández. 2004. Performance and applications of polyclonal antipeptide antibodies specific for the enterococcal bacteriocin enterocin P. J. Agric. Food Chem. 52:2247-2255.
30. Gutiérrez, J. 2005. Ph.D thesis. Universidad Complutense de Madrid, Madrid, Spain.
31. Harlander, S. K. 1994. Regulatory aspects of bacteriocin use, p. 233-248. In D. G. Hoover (ed.), Bacteriocins of lactic acid bacteria. Academic Press, Inc., New York, N.Y.
32. Herranz, C., J. M. Martínez, J. M. Rodríguez, P. E. Hernández, and L. M. Cintas. 2001. Optimization of enterocin P production by batch fermentation of Enterococcus faecium P13 at constant pH. Appl. Microbiol. Biotechnol. 56:378-383.
33. Horn, N., M. I. Martínez, J. M. Martínez, P. E. Hernández, M. H. Gasson, J. M. Rodríguez, and H. M. Dood. 1998. Enhanced production of pediocin PA-1 and coproduction of nisin and pedrocin PA-J by Lactococcus lactis. Appl. Environ. Microbiol. 65:4443-4450.
34. Horn, N., M. I. Martínez, J. M. Martínez, P. E. Hernández, M. H. Gasson, J. M. Rodríguez, and H. M. Dodd. 1998. Production of pedrocin PA-1 by Lactococcus lactis using lactococcin A secretory apparatus. Appl. Environ. Microbiol. 64:818-823.
35. Huot, E., C. Barena-González, and H. Petitdemange. 1996. Tween 80 effect on bacteriocin synthesis by Lactococcus lactis subsp. cremoris J46. Lett. Appl. Microbiol. 22:307-310.
36. Kang, J. H., and M. S. Lee. 2005. Characterization of a bacteriocin produced by Enterococcus faecium GM-1 isolated from an infant. J. Appl. Microbiol. 98:1169-1176.
37. Kawamoto, S., J. Shima, R. Sato, T. Eguchi, S. Ohniomo, 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.
38. Keren, T., M. Yarmus, G. Halevy, and R. Shapira. 2004. Immunodetection of the bacteriocin lacticin RM: analysis of the influence of temperature and Tween 80 on its expression and activity. Appl. Environ. Microbiol. 70:2098-2104.
39. Klaenhammer, T. R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39-86.
40. Krier, F., A. M. Revol-Junelles, and P. Germain. 1998. Influence of temperature and pH on production of two bacteriocins by Leuconostoc mesenteroides subsp. mesenteroides FR52 during batch fermentation. Appl. Microbiol. Biotechnol. 50:359-363.
41. Lejeune, R., R. Callewaert, K. Crabbé, and L. de Vuyst. 1998. Modelling the growth and bacteriocin production by Lactobacillus amylovorus DCE 471 in batch cultivation. J. Appl. Bacteriol. 84:159-168.
42. Leroy, F., and L. de Vuyst. 1999. Temperature and pH conditions that prevail during fermentation of sausages are optimal for production of the antilisterial bacteriocin sakacin K. Appl. Environ. Microbiol. 65:974-981.
43. Leroy, F., and L. de Vuyst. 2002. Bacteriocin production by Enterococcus faecium RZS C5 is cell density limited and occurs in the very early growth phase. Int. J. Food Microbiol. 72:155-164.
44. Leroy, F., and L. de Vuyst. 2005. Simulation of the effect of sausage ingredients and technology on the functionality of the bacteriocin-producing Lactobacillus sakei CTC 494 strain. Int. J. Food Microbiol. 100:141-152.
45. Leung, P. P., M. Khadre, T. H. Shellhammer, and A. E. Yousef. 2002. Immunoassay method for quantitative determination of nisin in solution and on polymeric films. Lett. Appl. Microbiol. 34:199-204.
46. Leversee, J. A., and B. A. Glatz. 2001. Detection of the bacteriocin propionicin PLG-I with polyvalent anti-PLG-1 antiserum. Appl. Environ. Microbiol. 67:2235-2239.
47. Martínez, J. M., M. I. Martínez, A. M. Suárez, C. Herranz, P. Casaus, L. M. Cintas, J. M. Rodríguez, and P. E. Hernández. 1998. Generation of polyclonal antibodies of predetermined specificity against pediocin PA-1. Appl. Environ. Microbiol. 64:4536-4545.
48. Martínez, J. M., M. I. Martínez, C. Herranz, A. M. Suárez, M. F. Fernández, J. M. Rodríguez, and P. E. Hernández. 1999. Antibodies to a synthetic 1-9-N-terminal amino acid fragment of mature pediocin PA-1: sensitivity and specificity for pediocin PA-1 and cross-reactivity against class IIa bacteriocins. Microbiology 145:2777-2787.
49. Martínez, J. M., J. Kok, J. W. Sanders, and P. E. Hernández. 2000. Heterologous coproduction of enterocin A and pediocin PA-1 by Lactococcus lactis: detection by specific peptide-directed antibodies. Appl. Environ. Microbiol. 66:3543-3549.
50. Martínez, J. M., M. I. Martínez, C. Herranz, A. M. Suárez, L. M. Cintas, M. F. Fernández, J. M. Rodríguez, and P. E. Hernández. 2000. Use of genetic and immunological probes for pediocin PA-1 gene detection and quantification of bacteriocin production in Pediococcus acidilactici strains of meat origin. Food Agric. Immunol. 12:299-310.
51. Martínez, M. I., J. M. Rodríguez, A. M. Suárez, J. M. Martínez, J. I. Azcona, and P. E. Hernández. 1997. Generation of polyclonal antibodies against a chemically synthesized N-terminal fragment of the bacteriocin pediocin PA-1. Lett. Appl. Microbiol. 24:488-492.
52. Messens, W., J. Verluyten, F. Leroy, and L. de Vuyst. 2003. Modelling growth and bacteriocin production by Lactobacillus curvatus LTH 1174 in response to temperature and pH values used for European sausage fermentation processes. Int. J. Food Microbiol. 81:41-52.
53. Møretro, T., I. M. Aasen, I. Storrø, and L. Axelsson. 2000. Production of sakacin P by Lactobacillus sakei in a completely defined medium. J. Appl. Microbiol. 88:536-545.
54. Nes, I. F., D. B. Diep, L. S. Håvarstein, and M. B. Brurberg. 1996. Biosynthesis of bacteriocins in lactic acid bacteria. Antonie Leeuwenhoek 70:113-128.
55. Neysens, P., W. Messens, D. Gevers, J. Swings, and L. de Vuyst. 2003. Biphasic kinetics of growth and bacteriocin production with Lactobacillus amylovorus DCE 471 occur under stress conditions. Microbiology 149:1073-1082.
56. 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.
57. Parente, E., and C. Hill. 1992. Characterization of enterocin 1146, a bacteriocin from Enterococcus faecium inhibitory to Listeria monocytogenes. J. Food Prot. 55:497-502.
58. Parente, E., and A. Ricciardi. 1999. Production, recovery and purification of bacteriocins from lactic acid bacteria. Appl. Microbiol. Biotechnol. 52:628-638.
59. Prioult, G., C. Turcotte, L. Labarre, C. Lacroix, and I. Fliss. 2000. Rapid purification of nisin A using specific monoclonal antibody-coated magnetic beads. Int. Dairy J. 10:627-633.
60. Richard, C., D. Drider, I. Fliss, S. Denry, and H. Prevost. 2004. Generation and utilization of polyclonal antibodies to a synthetic C-terminal amino acid fragment of divercin V41, a class IIa bacteriocin. Appl. Environ. Microbiol. 70:248-254.
61. Rose, N. L., P. Sporns, and L. M. McMullen. 2001. Production of antibodies against enterocin B for immunological detection and purification purposes. Food Agric. Immunol. 13:225-239.
62. Skaugen, M., L. M. Cintas, and I. F. Nes. 2003. Genetics of bacteriocin production in lactic acid bacteria, p. 225-260. In B. J. B. Wood (ed.), The lactic acid bacteria. Genetics of lactic acid bacteria, vol. 3. Kluwer Academic/Plenum Publisher, New York, N.Y.
63. Suárez, A. M., J. M. Rodriguez, P. E. Hernández, and J. I. Azcona-Olivera. 1996. Generation of polyclonal antibodies against nisin: immunization strategies and immunoassay development. Appl. Environ. Microbiol. 62:2117-2121.
64. Torri Tarelli, G., D. Carminati, and G. Giraffa. 1994. Production of bacteriocins active against Listeria monocytogenes and Listeria innocua from dairy enterococci. Food Microbiol. 11:243-252.
65. Vogel, R. F., B. S. Pohle, P. S. Tichaczek, and W. P. Hammes. 1993. The competitive advantage of Lactobacillus curvatus LTH 1174 in sausage fermentations is caused by formation of curvacin A. Syst. Appl. Microbiol. 16:457-462.
66. Yang, R., and B. Ray. 1994. Factors influencing production of bacteriocins by lactic acid bacteria. Food Microbiol. 11:281-291.