Sec-mediated transport of posttranslationally dehydrated peptides in Lactococcus lactis

Applied and Environmental Microbiology

Volumn 72, Issue 12, 2006, Pages 7626-7633

  Kuipers, Anneke ^a   Wierenga, Jenny ^a   Rink, Rick ^a   Kluskens, Leon D ^a   Driessen, Arnold J M ^b   Kuipers, Oscar P ^b   Moll, Gert N ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIBIOTICS; BACTERIA; DEHYDRATION; ENZYMES; SUBSTRATES;

LACTOCOCCUS LACTIS; LANTHIONINES; POSTTRANSLATIONAL MODIFICATIONS; THERAPEUTIC PEPTIDES;

POLYPEPTIDES;

ABC TRANSPORTER; BACTERIAL PROTEIN; HYDROLYASE; LANTHIONINE; LANTIBIOTIC; NISIN; PEPTIDASE; PEPTIDE; POLYPEPTIDE; PROTEIN NISB; PROTEIN NISC; PROTEIN NISP; PROTEIN NIST; PROTEIN PRECURSOR; PROTEIN SECA; SERINE; SIGNAL PEPTIDE; THREONINE; TRANSACTIVATOR PROTEIN;

AMINO ACID; BACTERIUM; DEHYDRATION; GENE EXPRESSION; PEPTIDE;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DEHYDRATION; ENZYME ACTIVITY; ENZYME MODIFICATION; GENE EXPRESSION; LACTOCOCCUS LACTIS; NISBTC GENE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TRANSPORT; PROTEIN VARIANT; REGULATORY MECHANISM; SEQUENCE ANALYSIS;

ADENOSINE TRIPHOSPHATASES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOTECHNOLOGY; LACTOCOCCUS LACTIS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; NISIN; PEPTIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SORTING SIGNALS;

LACTOCOCCUS LACTIS;

EID: 33845526596     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01802-06     Document Type: Article

References (53)

1. Arnau, J., E. Hjerl-Hansen, and H. Israelsen. 1997. Heterologous gene expression of bovine plasmin in Lactococcus lactis. Appl. Microbiol. Biotechnol. 48:331-338.
2. Bhunia, A. K., M. C. Johnson, and B. Ray. 1987. Direct detection of an antimicrobial peptide of Pediococcus acidilactici in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J. Ind. Microbiol. 2:319-322.
3. Bolotin, A., P. Wincker, S. Mauger, O. Jaillon, K. Malarme, J. Weissenbach, S. D. Ehrlich, and A. Sorokin. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11:731-753.
4. Breukink, E., H. E. van Heusden, P. J. Vollmerhaus, E. Swiezewska, L. Brunner, S. Walker, A. J. Heck, and B. de Kruijff. 2003. Lipid II is an intrinsic component of the pore induced by nisin in bacterial membranes. J. Biol. Chem. 278:19898-19903.
5. Chakicherla, A., and J. N. Hansen. 1995. Role of the leader and structural regions of prelantibiotic peptides as assessed by expressing nisin-subtilin chimeras in Bacillus subtilis 168, and characterization of their physical, chemical, and antimicrobial properties. J. Biol. Chem. 270:23533-23539.
6. De Lisa, M. P., D. Tullman, and G. Georgiou. 2003. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc. Natl. Acad. Sci. USA 100:6115-6120.
7. de Ruyter, P. G., O. P. Kuipers, and W. M. de Vos. 1996. Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl. Environ. Microbiol. 62:3662-3667.
8. de Vos, W. M., O. P. Kuipers, J. R. van der Meer, and R. J. Siezen. 1995. Maturation pathway of nisin and other lantibiotics: post-translationally modified antimicrobial peptides exported by gram-positive bacteria. Mol. Microbiol. 17:427-437.
9. Fekkes, P., and A. J. Driessen. 1999. Protein targeting to the bacterial cytoplasmic membrane. Microbiol. Mol. Biol. Rev. 63:161-173.
10. Herranz, C., and A. J. Driessen. 2005. Sec-mediated secretion of bacteriocin enterocin P by Lactococcus lactis. Appl. Environ. Microbiol. 71:1959-1963.
11. Holo, H., and I. F. Nes. 1995. Transformation of Lactococcus by electroporation. Methods Mol. Biol. 47:195-199.
12. Jensen, P. R., and K. Hammer. 1993. Minimal requirements for exponential growth of Lactococcus lactis. Appl. Environ. Microbiol. 59:4363-4366.
13. Jongbloed, J. D., U. Grieger, H. Antelmann, M. Hecker, R. Nijland, S. Bron, and J. M. van Dijl. 2004. Two minimal Tat translocases in Bacillus. Mol. Microbiol. 54:1319-1325.
14. Karakas Sen, A., A. Narbad, N. Horn, H. M. Dodd, A. J. Parr, I. Colquhoun, and M. J. Gasson. 1999. Post-translational modification of nisin. The involvement of NisB in the dehydration process. Eur. J. Biochem. 261:524-532.
15. Kiesau, P., U. Eikmanns, Z. Gutowski-Eckel, S. Weber, M. Hammelmann, and K. D. Entian. 1997. Evidence for a multimeric subtilin synthetase complex. J. Bacteriol. 179:1475-1481.
16. Kluskens, L. D., A. Kuipers, R. Rink, E. de Boef, S. Fekken, A. J. Driessen, O. P. Kuipers, and G. N. Moll. 2005. Post-translational modification of therapeutic peptides by NisB, the dehydratase of the lantibiotic nisin. Biochemistry 44:12827-12834.
17. Koivula, T., I. Palva, and H. Hemila. 1991. Nucleotide sequence of the secY gene from Lactococcus lactis and identification of conserved regions by comparison of four SecY proteins. FEBS Lett. 288:114-118.
18. Koponen, O., M. Tolonen, M. Qiao, G. Wahlstrom, J. Helin, and P. E. Saris. 2002. NisB is required for the dehydration and NisC for the lanthionine formation in the post-translational modification of nisin. Microbiology 148:3561-3568.
19. Kuipers, A., E. de Boef, R. Rink, S. Fekken, L. D. Kluskens, A. J. Driessen, K. Leenhouts, O. P. Kuipers, and G. N. Moll. 2004. 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. 279:22176-22182.
20. Kuipers, O. P., M. M. Beerthuyzen, R. J. Siezen, and W. M. de Vos. 1993. 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. 216:281-291.
21. Kuipers, O. P., M. M. Beerthuyzen, P. G. de Ruyter, E. J. Luesink, and W. M. de Vos. 1995. Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J. Biol. Chem. 270:27299-27304.
22. Kuipers, O. P., P. G. de Ruyter, M. Kleerebezem, and W. M. de Vos. 1997. Controlled overproduction of proteins by lactic acid bacteria. Trends Biotechnol. 15:135-140.
23. Kuipers, O. P., P. G. de Ruyter, M. Kleerebezem, and W. M. de Vos. 1998 Quorum sensing-controlled gene expression in lactic acid bacteria. J. Biotechnol. 64:15-21.
24. Kunst, F., N. Ogasawara, I. Moszer, A. M. Albertini, G. Alloni, V. Azevedo, M. G. Bertero, P. Bessieres, A. Bolotin, S. Borchert, R. Borriss, L. Boursier, A. Brans, M. Braun, S. C. Brignell, S. Bron, S. Brouillet, C. V. Bruschi, B. Caldwell, V. Capuano, N. M. Carter, S. K. Choi, J. J. Codani, I. F. Connerton, and A. Danchin. 1997. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249-256.
25. Leenhouts, K., A. Bolhuis, G. Venema, and J. Kok. 1998. Construction of a food-grade multiple-copy integration system for Lactococcus lactis. Appl. Microbiol. Biotechnol. 49:417-423.
26. Le Loir, Y., V. Azevedo, S. C. Oliveira, D. A. Freitas, A. Miyoshi, L. G. Bermudez-Humaran, S. Nouaille, L. A. Ribeiro, S. Leclercq, J. E. Gabriel, V. D. Guimaraes, M. N. Oliveira, C. Charlier, M. Gautier, and P. Langella. 2005. Protein secretion in Lactococcus lactis: an efficient way to increase the overall heterologous protein production. Microb. Cell Fact. 4:2.
27. Le Loir, Y., S. Nouaille, J. Commissaire, L. Bretigny, A. Gruss, and P. Langella. 2001. Signal peptide and propeptide optimization for heterologous protein secretion in Lactococcus lactis. Appl. Environ. Microbiol. 67:4119-4127.
28. Li, B., J. P. Yu, J. S. Brunzelle, G. N. Moll, W. A. van der Donk, and S. K. Nair. 2006. Structure and mechanism of the lantibiotic cyclase involved in nisin biosynthesis. Science 311:1464-1467.
29. Lombardi, A., B. D'Agostino, F. Nastri, L. D. D'Andrea, A. Filippelli, M. Falciani, F. Rossi, and V. Pavone. 1998. A novel super-potent neurokinin A receptor antagonist containing dehydroalanine. Bioorg. Med. Chem. Lett. 8:1153-1156.
30. Meens, J, E. Frings, M. Klose, and R. Freudl. 1993. An outer membrane protein (OmpA) of Escherichia coli can be translocated across the cytoplasmic membrane of Bacillus subtilis. Mol. Microbiol. 9:847-855.
31. Morris, S. L., R. C. Walsh, and J. N. Hansen. 1984. Identification and characterization of some bacterial membrane sulfhydryl groups which are targets of bacteriostatic and antibiotic action. J. Biol. Chem. 259:13590-13594.
32. Murkin, A. S., and M. E. Tanner. 2002. Dehydroalanine-based inhibition of a peptide epimerase from spider venom. J. Org. Chem. 67:8389-8394.
33. Oliver, D. B., R. J. Cabelli, K. M. Dolan, and G. P. Jarosik. 1990. Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl. Acad. Sci. USA 87:8227-8231.
34. Pag, U., C. Heidrich, G. Bierbaum, and H. G. Sahl. 1999. Molecular analysis of expression of the lantibiotic pep5 immunity phenotype. Appl. Environ. Microbiol. 65:591-598.
35. Palmer, D. E., C. Pattaroni, K. Nunami, R. K. Chadha, M. Goodman, T. Wakamiya, K. Fukase, S. Horimoto, M. Kitazawa, H. Fujita, A. Kubo, and T. Shiba. 1992. Effects of dehydroalanine on peptide conformations. J. Am. Chem. Soc. 114:5634-5642.
36. Pohlschröder, M., M. I. Gimenez, and K. F. Jarrell. 2005. Protein transport in Archaea: Sec and twin arginine translocation pathways. Curr. Opin. Microbiol. 8:713-719.
37. Qiao, M., and P. E. Saris. 1996. Evidence for a role of NisT in transport of the lantibiotic nisin produced by Lactococcus lactis N8. FEMS Microbiol. Lett. 144:89-93.
38. Rew, Y., S. Malkmus, C. Svensson, T. L. Yaksh, N. N. Chung, P. W. Schiller, J. A. Cassel, R. N. DeHaven, J. P. Taulane, and M. Goodman. 2002. Synthesis and biological activities of cyclic lanthionine enkephalin analogues: delta-opioid receptor selective ligands. J. Med. Chem. 45:3746-3754.
39. Rink, R., A. Kuipers, E. de Boef, K. J. Leenhouts, A. J. Driessen, G. N. Moll, and O. P. Kuipers. 2005. Lantibiotic structures as guidelines for the design of peptides that can be modified by lantibiotic enzymes. Biochemistry 44:8873-8882.
40. Sanders, C., N. Wethkamp, and H. Lill. 2001. Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol. Microbiol. 41:241-246.
41. Schagger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
42. Siegers, K., S. Heinzmann, and K. D. Entian. 1996. Biosynthesis of lantibiotic nisin. Posttranslational modification of its prepeptide occurs at a multimeric membrane-associated lanthionine synthetase complex. J. Biol. Chem. 271:12294-12301.
43. Simon, D., and A. Chopin. 1988. Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis. Biochimie 70:559-566.
44. Stein, T., and K. D. Entian. 2002. Maturation of the lantibiotic subtilin: matrix-assisted laser desorption/ionization time-of-flight mass spectrometry to monitor precursors and their proteolytic processing in crude bacterial cultures. Rapid Commun. Mass Spectrom. 16:103-110.
45. Svensson, C. I., Y. Rew, S. Malkmus, P. W. Schiller, J. P. Taulane, M. Goodman, and T. L. Yaksh. 2003. Systemic and spinal analgesic activity of a delta-opioid-selective lanthionine enkephalin analog. J. Pharmacol. Exp. Ther. 304:827-832.
46. Terzaghi, B. E., and W. E. Sandine. 1975. Improved medium for lactic streptococci and their bacteriophages. Appl. Microbiol. 29:807-813.
47. Tian, P., and I. Andricioaei. 2006. Size, motion, and function of the SecY translocon revealed by molecular dynamics simulations with virtual probes. Biophys. J. 90:2718-2730.
48. Tjalsma, H., A. Bolhuis, J. D. Jongbloed, S. Bron, and J. M. van Dijl. 2000. Signal pcptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol. Mol. Biol. Rev. 64:515-547.
49. van Asseldonk, M., W. M. de Vos, and G. Simons. 1993. Functional analysis of the Lactococcus lactis usp45 secretion signal in the secretion of a homologous proteinase and a heterologous alpha-amylase. Mol. Gen. Genet. 240:428-434.
50. van Wely, K. H., J. Swaving, R. Freudl, and A. J. Driessen. 2001. Translocation of proteins across the cell envelope of Gram-positive bacteria. FEMS Microbiol. Rev. 25:437-454.
51. von Heijne, G. 1985. Signal sequences. The limits of variation. J. Mol. Biol. 184:99-105.
52. Xie, L., L. M. Miller, C. Chatterjee, O. Averin, N. L. Kelleher, and W. A. van der Donk. 2004. Lacticin 481: in vitro reconstitution of lantibiotic synthetase activity. Science 303:679-681.
53. Ye, S. Y., O. Koponen, M. Qiao, T. Immonen, and P. E. Saris. 1995. NisP is related to nisin precursor processing and possibly to immunity in Lactococcus lactis. J. Tongji Med. Univ. 15:193-197.