Lipoprotein signal peptides are processed by Lsp and Eep of Streptococcus uberis

Journal of Bacteriology

Volumn 190, Issue 13, 2008, Pages 4641-4647

  Denham, E L ^a   Ward, P N ^b   Leigh, J A ^c  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEIN; LIPOPROTEIN MTUA; LIPOPROTEIN SIGNAL PEPTIDASE; PEPTIDASE; PHEROMONE; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; ENHANCED EXPRESSION OF PHEROMONE GENE; ENTEROCOCCUS FAECALIS; GENE; GENE EXPRESSION; MASTITIS; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; STREPTOCOCCUS UBERIS; WESTERN BLOTTING;

BACTERIAL PROTEINS; BLOTTING, SOUTHERN; BLOTTING, WESTERN; COMPUTATIONAL BIOLOGY; GENOME, BACTERIAL; LIPOPROTEINS; MUTATION; PROTEIN SORTING SIGNALS; STREPTOCOCCUS;

BOVINAE; ENTEROCOCCUS FAECALIS; POSIBACTERIA; STREPTOCOCCUS UBERIS;

EID: 46049119823     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00287-08     Document Type: Article

References (50)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Meyers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. An, F. Y., and D. B. Clewell. 2002. Identification of the cAD1 sex pheromone precursor in Enterococcus faecalis. J. Bacteriol. 184:1880-1887.
3. An, F. Y., M. C. Sulavik, and D. B. Clewell. 1999. Identification and characterization of a determinant (eep) on the Enterococcus faecalis chromosome that is involved in production of the peptide sex pheromone cAD1. J. Bacteriol. 181:5915-5921.
4. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
5. Berg, T., N. Firth, and R. A. Skurray. 1997. Enterococcal pheromone-like activity derived from a lipoprotein signal peptide encoded by a Staphylococcus aureus plasmid. Adv. Exp. Med. Biol. 418:1041-1044.
6. 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.
7. Brown, M. S., J. Ye, R. B. Rawson, and J. L. Goldstein. 2000. Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100:391-398.
8. Chandler, J. R., and G. M. Dunny. 2004. Enterococcal peptide sex pheromones: synthesis and control of biological activity. Peptides 25:1377-1388.
9. Clewell, D. B., F. Y. An, S. E. Flannagan, M. Antiporta, and G. M. Dunny. 2000. Enterococcal sex pheromone precursors are part of signal sequences for surface lipoproteins. Mol. Microbiol. 35:246-247.
10. De Greeff, A., A. Hamilton, I. C. Sutcliffe, H. Buys, L. Van Alphen, and H. E. Smith. 2003. Lipoprotein signal peptidase of Streptococcus suis serotype 2. Microbiology 149:1399-1407.
11. Dev, I. K., R. J. Harvey, and P. H. Ray. 1985. Inhibition of prolipoprotein signal peptidase by globomycin. J. Biol. Chem. 260:5891-5894.
12. Dev, I. K., and P. H. Ray. 1984. Rapid assay and purification of a unique signal peptidase that processes the prolipoprotein from Escherichia coli B. J. Biol. Chem. 259:11114-11120.
13. Firth, N., P. D. Fink, L. Johnson, and R. A. Skurray. 1994. A lipoprotein signal peptide encoded by the staphylococcal conjugative plasmid pSK41 exhibits an activity resembling that of Enterococcus faecalis pheromone cAD1. J. Bacteriol. 176:5871-5873.
14. Flannagan, S. E., and D. B. Clewell. 2002. Identification and characterization of genes encoding sex pheromone cAM373 activity in Enterococcus faecalis and Staphylococcus aureus. Mol. Microbiol. 44:803-817.
15. Frishman, D., K. Albermann, J. Hani, K. Heumann, A. Metanomski, A. Zollner, and H. W. Mewes. 2001. Functional and structural genomics using PEDANT. Bioinformatics 17:44-57.
16. Frishman, D., M. Mokrejs, D. Kosykh, G. Kastenmuller, G. Kolesov, I. Zubrzycki, C. Gruber, B. Geier, A. Kaps, K. Albermann, A. Volz, C. Wagner, M. Fellenberg, K. Heumann, and H. W. Mewes. 2003. The PEDANT genome database. Nucleic Acids Res. 31:207-211.
17. Fukuda, A., S. Matsuyama, T. Hara, J. Nakayama, H. Nagasawa, and H. Tokuda. 2002. Aminoacylation of the N-terminal cysteine is essential for Lol-dependent release of lipoproteins from membranes but does not depend on lipoprotein sorting signals. J. Biol. Chem. 277:43512-43518.
18. Hill, A. W., and J. A. Leigh. 1989. DNA fingerprinting of Streptococcus uberis: a useful tool for epidemiology of bovine mastitis. Epidemiol. Infect. 103:165-171.
19. Hillerton, J. E., and E. A. Berry. 2005. Treating mastitis in the cow - a tradition or an archaism. J. Appl. Microbiol. 98:1250-1255.
20. Innis, M. A., M. Tokunaga, M. E. Williams, J. M. Loranger, S. Y. Chang, S. Chang, and H. C. Wu. 1984. Nucleotide sequence of the Escherichia coli prolipoprotein signal peptidase (lsp) gene. Proc. Natl. Acad. Sci. USA 81:3708-3712.
21. Inukai, M., M. Takeuchi, K. Shimizu, and M. Arai. 1978. Mechanism of action of globomycin. J. Antibiot. (Tokyo) 31:1203-1205.
22. Isaki, L., M. Kawakami, R. Beers, R. Hom, and H. C. Wu. 1990. Cloning and nucleotide sequence of the Enterobacter aerogenes signal peptidase II (lsp) gene. J. Bacteriol. 172:469-472.
23. Jones, C. L. 2006. Ph.D. thesis. University of Sussex, Brighton, United Kingdom.
24. Jones, C. L., P. Monaghan, T. R. Field, A. J. Smith, P. N. Ward, and J. A. Leigh. 2004. Localization of MtuA, an LraI homologue in Streptococcus uberis. J. Appl. Microbiol. 97:149-157.
25. Jones, D. T. 2007. Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 23:538-544.
26. Jongeneel, C. V., J. Bouvier, and A. Bairoch. 1989. A unique signature identifies a family of zinc-dependent metallopeptidases. FEBS Lett. 242:211-214.
27. Kall, L., A. Krogh, and E. L. Sonnhammer. 2004. A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 338:1027-1036.
28. Khandavilli, S., K. A. Homer, J. Yuste, S. Basavanna, T. Mitchell, and J. S. Brown. 2008. Maturation of Streptococcus pneumoniae lipoproteins by a type II signal peptidase is required for ABC transporter function and full virulence. Mol. Microbiol. 67:541-557.
29. Lalioui, L., E. Pellegrini, S. Dramsi, M. Baptista, N. Bourgeois, F. Doucet-Populaire, C. Rusniok, M. Zouine, P. Glaser, F. Kunst, C. Poyart, and P. Trieu-Cuot. 2005. The SrtA sortase of Streptococcus agalactiae is required for cell wall anchoring of proteins containing the LPXTG motif, for adhesion to epithelial cells, and for colonization of the mouse intestine. Infect. Immun. 73:3342-3350.
30. Maguin, E., H. Prevost, S. D. Ehrlich, and A. Gruss. 1996. Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J. Bacteriol. 178:931-935.
31. Munoa, F. J., K. W. Miller, R. Beers, M. Graham, and H. C. Wu. 1991. Membrane topology of Escherichia coli prolipoprotein signal peptidase (signal peptidase II). J. Biol. Chem. 266:17667-17672.
32. Reglier-Poupet, H., C. Frehel, I. Dubail, J. L. Beretti, P. Berche, A. Charbit, and C. Raynaud. 2003. Maturation of lipoproteins by type II signal peptidase is required for phagosomal escape of Listeria monocytogenes. J. Biol. Chem. 278:49469-49477.
33. Regue, M., J. Remenick, M. Tokunaga, G. A. Mackie, and H. C. Wu. 1984. Mapping of the lipoprotein signal peptidase gene (lsp). J. Bacteriol. 158:632-635.
34. Sander, P., M. Rezwan, B. Walker, S. K. Rampini, R. M. Kroppenstedt, S. Ehlers, C. Keller, J. R. Keeble, M. Hagemeier, M. J. Colston, B. Springer, and E. C. Bottger. 2004. Lipoprotein processing is required for virulence of Mycobacterium tuberculosis. Mol. Microbiol. 52:1543-1552.
35. Schobel, S., S. Zellmeier, W. Schumann, and T. Wiegert. 2004. The Bacillus subtilis sigmaW anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol. Microbiol. 52:1091-1105.
36. Smith, A. J., P. N. Ward, T. R. Field, C. L. Jones, R. A. Lincoln, and J. A. Leigh. 2003. MtuA, a lipoprotein receptor antigen from Streptococcus uberis, is responsible for acquisition of manganese during growth in milk and is essential for infection of the lactating bovine mammary gland. Infect. Immun. 71:4842-4849.
37. Sutcliffe, I. C., and D. J. Harrington. 2002. Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes. Microbiology 148:2065-2077.
38. Sutcliffe, I. C., and D. J. Harrington. 2004. Putative lipoproteins of Streptococcus agalactiae identified by bioinformatic genome analysis. Antonie van Leeuwenhoek 85:305-315.
39. Taylor, D. L., P. N. Ward, C. D. Rapier, J. A. Leigh, and L. D. Bowler. 2003. Identification of a differentially expressed oligopeptide binding protein (OppA2) in Streptococcus uberis by representational difference analysis of cDNA. J. Bacteriol. 185:5210-5219.
40. Tjalsma, H., A. Bolhuis, J. D. Jongbloed, S. Bron, and J. M. van Dijl. 2000. Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol. Mol. Biol. Rev. 64:515-547.
41. Tjalsma, H., V. P. Kontinen, Z. Pragai, H. Wu, R. Meima, G. Venema, S. Bron, M. Sarvas, and J. M. van Dijl. 1999. The role of lipoprotein processing by signal peptidase II in the Gram-positive eubacterium Bacillus subtilis. Signal peptidase II is required for the efficient secretion of alpha-amylase, a non-lipoprotein. J. Biol. Chem. 274:1698-1707.
42. Tjalsma, H., G. Zanen, G. Venema, S. Bron, and J. M. van Dijl. 1999. The potential active site of the lipoprotein-specific (type II) signal peptidase of Bacillus subtilis. J. Biol. Chem. 274:28191-28197.
43. Tokunaga, M., J. M. Loranger, S. Y. Chang, M. Regue, S. Chang, and H. C. Wu. 1985. Identification of prolipoprotein signal peptidase and genomic organization of the lsp gene in Escherichia coli. J. Biol. Chem. 260:5610-5615.
44. Tokunaga, M., H. Tokunaga, and H. C. Wu. 1982. Post-translational modification and processing of Escherichia coli prolipoprotein in vitro. Proc. Natl. Acad. Sci. USA 79:2255-2259.
45. van Roosmalen, M. L., N. Geukens, J. D. Jongbloed, H. Tjalsma, J. Y. Dubois, S. Bron, J. M. van Dijl, and J. Anne. 2004. Type I signal peptidases of Gram-positive bacteria. Biochim. Biophys. Acta 1694:279-297.
46. Venema, R., H. Tjalsma, J. M. van Dijl, A. de Jong, K. Leenhouts, G. Buist, and G. Venema. 2003. Active lipoprotein precursors in the Gram-positive eubacterium Lactococcus lactis. J. Biol. Chem. 278:14739-14746.
47. von Heijne, G. 1989. The structure of signal peptides from bacterial lipoproteins. Protein Eng. 2:531-534.
48. Ward, P. N., T. R. Field, W. G. Ditcham, E. Maguin, and J. A. Leigh. 2001. Identification and disruption of two discrete loci encoding hyaluronic acid capsule biosynthesis genes hasA, hasB, and hasC in Streptococcus uberis. Infect. Immun. 69:392-399.
49. Yamagata, H. 1983. Temperature-sensitive prolipoprotein signal peptidase in an Escherichia coli mutant: use of the mutant for an efficient and convenient assay system. J. Biochem. (Tokyo) 93:1509-1515.
50. Zhao, X. J., and H. C. Wu. 1992. Nucleotide sequence of the Staphylococcus aureus signal peptidase II (lsp) gene. FEBS Lett. 299:80-84.