Use of synthetic genes for cloning, production and functional expression of the bacteriocins enterocin A and bacteriocin E 50-52 by Pichia pastoris and Kluyveromyces lactis

Molecular Biotechnology

Volumn 56, Issue 6, 2014, Pages 571-583

  Jiménez, Juan J ^a   Borrero, Juan ^a   Gútiez, Loreto ^a   Arbulu, Sara ^a   Herranz, Carmen ^a   Cintas, Luis M ^a   Hernández, Pablo E ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Bacteriocin E 50 52; Bacteriocins; Enterocin A; Heterologous production; Kluyveromyces lactis; Pichia pastoris; Synthetic genes

Indexed keywords

AMINO ACIDS; BACTERIA; CLONING; PURIFICATION; YEAST;

BACTERIOCINS; ENTEROCIN; HETEROLOGOUS PRODUCTION; KLUYVEROMYCES LACTIS; PICHIA PASTORIS; SYNTHETIC GENES;

GENE EXPRESSION;

BACTERIOCIN; BACTERIOCIN E 50 52; ENTEROCIN A; SYNTHETIC DNA; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIOCIN E 50-52, ENTEROCOCCUS FAECIUM;

AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIUM TRANSFORMATION; CLONING; CODON USAGE; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; FUNGAL GENE; FUNGAL STRAIN; GENE EXPRESSION; INCUBATION TIME; KLUYVEROMYCES LACTIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PICHIA PASTORIS; PROTEIN EXPRESSION; RECOMBINANT PLASMID; SUPERNATANT; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GRAM POSITIVE BACTERIUM; KLUYVEROMYCES; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR CLONING; PICHIA;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; ENTEROCOCCUS FAECIUM; KLUYVEROMYCES LACTIS; LISTERIA MONOCYTOGENES; NEGIBACTERIA; PICHIA PASTORIS; POSIBACTERIA;

ANTI-BACTERIAL AGENTS; BACTERIOCINS; CLONING, MOLECULAR; ENTEROCOCCUS FAECIUM; GENE EXPRESSION REGULATION, BACTERIAL; GENES, SYNTHETIC; GRAM-POSITIVE BACTERIA; KLUYVEROMYCES; MICROBIAL SENSITIVITY TESTS; PICHIA;

EID: 84900811958     PISSN: 10736085     EISSN: 15590305     Source Type: Journal    
DOI: 10.1007/s12033-014-9731-7     Document Type: Article

References (49)

1. Denis-Quanquin, S., Lamouroux, L., Lougarre, A., Mahéo, S., Saves, I., Paquereau, L., et al. (2007). Protein expression from synthetic genes: Selection of clones using GFP. Journal of Biotechnology, 131, 223-230. (Pubitemid 47362428)
2. Gao, Z., Li, Z., Zhang, Y., Huang, H., Li, M., Zhou, L., et al. (2012). High-level expression of the Penicillum notatum glucose oxidase gene in Pichia pastoris using codon usage optimization. Biotechnology Letters, 34, 507-514.
3. Öberg, F., Sjöhman, J., Conner, M. T., Bill, R. M., & Hedfalk, K. (2011). Improving recombinant eukaryotic membrane protein yields in Pichia pastoris: The importance of codon optimization and clone selection. Molecular Membrane Biology, 28, 398-411.
4. Ward, N. J., Buckley, S. M., Waddington, S. N., Van den Driesche, T., Chuah, M. K., Nathwani, A. C., et al. (2011). Codon optimization of human factor VIII cDNAs leads to high level expression. Blood, 117, 798.
5. Borrero, J., Jiménez, J. J., Gútiez, L., Herranz, C., Cintas, L. M., & Hernández, P. E. (2011). Protein expression vector and secretion signal peptide optimization to drive the production, secretion, and functional expression of the bacteriocin enterocin A in lactic acid bacteria. Journal of Biotechnology, 156, 76-86.
6. Montalbán-López, M., Sánchez-Hidalgo, M., Valdivia, E., Martínez-Bueno, M., & Maqueda, M. (2011). Are bacteriocins underexploited? Novel applications for old antimicrobials. Current Pharmaceutical Biotechnology, 12, 1205-1220.
7. Franz, C. M., van Belkum, M. J., Holzapfel, W. H., Abriouel, H., & Gálvez, A. (2007). Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiology Reviews, 31, 293-310. (Pubitemid 46525308)
8. Cotter, P. D., Hill, C., & Ross, R. P. (2005). Bacteriocins: developing innate immunity for food. Nature Reviews Microbiology, 3, 777-788. (Pubitemid 41518738)
9. Drider, D., Fimland, G., Héchard, Y., McMullen, L. M., & Prévost, H. (2006). The continuing story of class IIa bacteriocins. Microbiology and Molecular Biology Reviews, 70, 564-582. (Pubitemid 43895038)
10. Nes, I. F., Yoon, S. S., & Diep, D. B. (2007). Ribosomally synthesized antimicrobial peptides (bacteriocins) in lactic acid bacteria: A review. Food Science and Biotechnology, 16, 675-690.
11. Kjos, M., Borrero, J., Opsata, M., Birri, D. J., Holo, H., Cintas, L. M., et al. (2011). Target recognition, resistance, immunity and genome mining of class II bacteriocins from gram-positive bacteria. Microbiology, 157, 3256-3267.
12. Gutiérrez, J., Larsen, R., Cintas, L. M., Kok, J., & Hernández, P. E. (2006). High-level heterologous production and functional expression of the sec-dependent enterocin P from Enterococcus faecium P13 in Lactococcus lactis. Applied Microbiology and Biotechnology, 72, 41-51.
13. Nilsen, T., Nes, I. F., & Holo, H. (1998). An exported inducer regulates bacteriocin production in Enterococcus faecium CTC492. Journal of Bacteriology, 180, 1848-1854. (Pubitemid 28173066)
14. O'Keefee, T., Hill, C., & Ross, R. P. (1999). Characterization and heterologous expression of the genes encoding enterocin A production, immunity and regulation in Enterococcus faecium DPC1146. Applied and Environment Microbiology, 65, 1506-1515. (Pubitemid 29173678)
15. Borrero, J., Kunze, G., Jiménez, J. J., Böer, E., Gútiez, L., Herranz, C., et al. (2012). Cloning, production and functional expression of the bacteriocin enterocin A, produced by Enterococcus faecium T136, by the yeasts Pichia pastoris, Kluyveromyces lactis, Hansenula polymorpha and Arxula adeninivorans. Applied and Environment Microbiology, 78, 5956-5961.
16. Hoang, K. V., Stern, N. J., & Lin, J. (2011). Development and stability of bacteriocin resistance in Campylobacter spp. Journal of Applied Microbiology, 111, 1544-1550.
17. Messaoudi, S., Kergourlay, G., Dalgarrondo, M., Choiset, Y., Ferchichi, M., Prevost, H., et al. (2012). Purification and characterization of a new bacteriocin active against Campylobacter produced by Lactobacillus salivarius SMXD51. Food Microbiology, 32, 129-134.
18. Svetoch, E. A., Eruslanov, B. V., Perelygin, V. V., Mitsevich, E. V., Mitsevich, I. P., Borzenkov, V. N., et al. (2008). Diverse antimicrobial killing by Enterococcus faecium E 50-52 bacteriocin. Journal of Agricultural and Food Chemistry, 56, 1942-1948. (Pubitemid 351497850)
19. Svetoch, E. A., Levchuk, V. P., Pokhilenko, V. D., Eruslanov, B. V., Mitsevich, E. V., Mitsevich, I. P., et al. (2008). Inactivating methicillin-resistant Staphylococcus aureus and other pathogens by use of bacteriocins OR-7 and E 50-52. Journal of Clinical Microbiology, 46, 3863-3865.
20. Svetoch, E. A., Eruslanov, B. V., Kovalev, Y. N., Mitsevich, E. V., Mitsevich, I. P., Levchuck, V. P., et al. (2009). Antimicrobial activities of bacteriocins E 50-52 and B 602 against antibioticresistant strains involved in nosocomial infections. Probiotics and Antimicrobial Proteins, 1, 136-142.
21. Svetoch, E. A., & Stern, N. J. (2010). Bacteriocins to control Campylobacter spp. in poultry - A review. Poultry Science, 89, 1763-1768.
22. Casaus, P., Nilsen, T., Cintas, L. M., Nes, I. F., Hernández, P. E., & Holo, H. (1997). Enterocin B, a new bacteriocin from Enterococcus faecium T136 which can act synergistically with enterocin A. Microbiology, 143, 2287-2294. (Pubitemid 27356762)
23. Aymerich, T., Holo, H., Håvarstein, L. S., Hugas, M., Garriga, M., & Nes, I. F. (1996). Biochemical and genetic characterization of enterocin A from Enterococcus faecium, a new antilisterial bacteriocin in the pediocin-family of bacteriocins. Applied and Environment Microbiology, 62, 1676-1682. (Pubitemid 26143442)
24. Gutiérrez, J., Criado, R., Martín, M., Herranz, C., Cintas, L. M., & Hernández, P. E. (2005). Production of enterocin P, an antilisterial pediocin-like bacteriocin from Enterococcus faecium P13, in Pichia pastoris . Antimicrobial Agents and Chemotherapy, 49, 3004-3008.
25. Sánchez, J., Diep, D. B., Herranz, C., Nes, I. F., Cintas, L. M., & Hernández, P. E. (2007). Amino acid and nucleotide sequence, adjacent genes, and heterologous expression of hiracin JM79, a Sec-dependent bacteriocin produced by Enterococcus hirae DCH5, isolated from Mallard ducks (Anas platyrhynchos). FEMS Microbiology Letters, 270, 227-236.
26. van Ooyen, A. J. J., Dekker, P., Huang, M., Olsthoorn, M. M. A., Jacobs, D. I., Colussi, P. A., et al. (2006). Heterologous protein production in the yeast Kluyveromyces lactis . FEMS Yeast Research, 6, 381-392.
27. Böer, E., Steinborn, G., Kunze, G., & Gellissen, G. (2007). Yeast expression platforms. Applied Microbiology and Biotechnology, 77, 513-523. (Pubitemid 350125520)
28. Richard, C., Drider, D., Elmorjani, K., Marion, D., & Prevost, H. (2004). Heterologous expression and purification of active divercin V41, a class IIa bacteriocin encoded by a synthetic gene in Escherichia coli. Journal of Bacteriology, 186, 4276-4284. (Pubitemid 38802576)
29. Acuña, L., Picariello, G., Sesma, F., Morero, R. D., & Bellomio, A. (2012). A new hybrid bacteriocin, Ent35-MccV, displays antimicrobial activity against pathogenic Gram-positive and Gram-negative bacteria. FEBS Open Bio, 2, 12-19.
30. Cregg, J. M., Cereghino, J. L., Shi, J., & Higins, D. R. (2000). Recombinant protein expression in Pichia pastoris . Molecular Biotechnology, 16, 23-52.
31. Colussi, P. A., & Taron, C. H. (2005). Kluyveromyces lactis LAC4 promoter variants that lack function in bacteria but retain full function in K. lactis. Applied and Environment Microbiology, 71, 7092-7098. (Pubitemid 43194199)
32. Le Loir, Y., Gruss, A., Ehrlich, D., & Langella, P. (1998). A nine-residue synthetic propeptide enhances secretion efficiency of heterologous proteins in Lactococcus lactis. Journal of Bacteriology, 180, 1895-1903. (Pubitemid 28173072)
33. Schoeman, H., Vivier, M. A., du Toit, M., Dicks, L. M. T., & Pretorius, I. S. (1999). The development of bactericidal yeast strains by expressing the Pediococcus acidilactici pediocin gene (pedA) in Saccharomyces cerevisiae. Yeast, 15, 647-656. (Pubitemid 29286545)
34. van Reenen, C. A., Chikindas, M. L., van Zyl, W. H., & Dicks, L. M. T. (2002). Characterization and heterologous expression of a class IIa bacteriocin, plantaricin 423 from Lactobacillus plantarum 423, in Saccharomyces cerevisiae . International Journal of Food Microbiology, 81, 29-40. (Pubitemid 35335391)
35. Basanta, A., Herranz, C., Gutiérrez, J., Criado, R., Hernández, P. E., & Cintas, L. M. (2009). Development of bacteriocinogenic strains of Saccharomyces cerevisiae heterologously expressing and secreting the leaderless enterocin L50 peptides L50A and L50B from Enterococcus faecium L50. Applied and Environment Microbiology, 75, 2382-2392.
36. Beaulieu, L., Groleau, D., Míguez, C. B., Jetté, J. F., Aomari, H., & Subirade, M. (2005). Production of pediocin PA-1 in the methylotrophic yeast Pichia pastoris reveals unexpected inhibition of its biological activity due to the presence of collagen-like material. Protein Expression and Purification, 43, 111-125.
37. Sánchez, J., Borrero, J., Gómez-Sala, B., Basanta, A., Herranz, C., Cintas, L. M., et al. (2008). Cloning and heterologous production of hiracin JM79, a sec-dependent bacteriocin produced by Enterococcus hirae, in lactic acid bacteria and Pichia pastoris. Applied and Environment Microbiology, 74, 2471-2479. (Pubitemid 351555460)
38. Basanta, A., Gómez-Sala, B., Sánchez, J., Dzung, B. D., Herranz, C., Hernández, P. E., et al. (2010). Use of the yeast Pichia pastoris as an expression host for secretion of enterocin L50, a leaderless two-peptide (L50A and L50B) bacteriocin from Enterococcus faecium L50. Applied and Environment Microbiology, 76, 3314-3324.
39. Martín, M., Gutiérrez, J., Criado, R., Herranz, C., Cintas, L. M., & Hernández, P. E. (2007). Chimeras of mature pediocin PA-1 fused to the signal peptide of enterocin P permits the cloning, production, and expression of pediocin PA-1 in Lactococcus lactis. Journal of Food Protection, 70, 2792-2798.
40. Martín, M., Gutiérrez, J., Criado, R., Herranz, C., Cintas, L. M., & Hernández, P. E. (2007). Cloning, production and expression of the bacteriocin enterocin A produced by Enterococcus faecium PLBC21 in Lactococcus lactis. Applied Microbiology and Biotechnology, 76, 667-675.
41. Borrero, J., Jiménez, J. J., Gútiez, L., Herranz, C., Cintas, L. M., & Hernández, P. E. (2011). Use of the usp45 lactococcal secretion sequence signal sequence to drive the secretion and functional expression of enterococcal bacteriocins in Lactococcus lactis. Applied Microbiology and Biotechnology, 89, 131-143.
42. Borrero, J., Brede, D. A., Skaugen, M., Diep, D. B., Herranz, C., Nes, I. F., et al. (2011). Characterization of garvicin ML, a novel circular bacteriocin produced by Lactococcus garvieae DCC43, isolated from mallard ducks (Anas platyrhynchos). Applied and Environment Microbiology, 77, 369-373.
43. Gasser, B., Saloheimo, M., Rinas, U., Dragosits, M., Rodríguez- Carmona, E., Baumann, K., et al. (2008). Protein folding and conformational stress in microbial cells producing recombinant proteins: A host comparative overview. Microbial Cell Factories, 4, 7-11.
44. Zhao, Y., & Jensen, O. N. (2009). Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques. Proteomics, 9, 4362-4641.
45. Eijsink, V. G. H., Skeie, M., Middelhoven, P. H., Brurberg, M. B., & Nes, I. F. (1998). Comparative studies of class II bacteriocins of lactic acid bacteria. Applied and Environment Microbiology, 64, 3275-3281. (Pubitemid 28411447)
46. Zerbs, S., Frank, A. M., & Collart, F. R. (2009). Bacterial systems for production of heterologous proteins. Methods in Enzymology, 463, 149-168.
47. Katla, T., Naterstad, K., Vancanneyt, M., Swings, J., & Axelsson, L. (2003). Differences in susceptibility of Listeria monocytogenes strains to sakacin P, sakacin A, pediocin PA-1, and nisin. Applied and Environment Microbiology, 69, 4431-4437. (Pubitemid 36992897)
48. Diep, D. B., Skaugen, M., Salehian, Z., Holo, H., & Nes, I. F. (2007). Common mechanisms of target cell recognition and immunity for class II bacteriocins. Proceedings of the National Academy of Sciences of the United States of America, 104, 2384-2389. (Pubitemid 46391406)
49. Cintas, L. M., Casaus, P., Håvarstein, L. S., Hernández, P. E., & Nes, I. F. (1997). Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum. Applied and Environment Microbiology, 63, 4321-4330. (Pubitemid 27485757)