A nine-residue synthetic propeptide enhances secretion efficiency of heterologous proteins in Lactococcus lactis

Journal of Bacteriology

Volumn 180, Issue 7, 1998, Pages 1895-1903

  Le Loir, Y ^a   Gruss, A ^a   Ehrlich, S D ^a   Langella, P ^a  

^a CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ENZYME ACTIVITY; GEOBACILLUS STEAROTHERMOPHILUS; GRAM POSITIVE BACTERIUM; LACTOCOCCUS LACTIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; REPORTER GENE; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); GEOBACILLUS STEAROTHERMOPHILUS; LACTOCOCCUS LACTIS; NEGIBACTERIA; POSIBACTERIA; PROKARYOTA; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS;

EID: 0031944982     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.7.1895-1903.1998     Document Type: Article

References (61)

1. Baneyx, F., and G. Georgiou. 1990. In vivo degradation of secreted fusion proteins by the Escherichia coli outer membrane protease OmpT. J. Bacteriol. 172:491-494.
2. Barkocy-Gallagher, G. A., and P. J. Bassford, Jr. 1992. Synthesis of precursor maltose-binding protein with proline in the +1 position of the cleavage site interferes with the activity of Escherichia coli signal peptidase I in vivo. J. Biol. Chem. 267:1231-1238.
3. Bieker, K. L., and T. J. Silhavy. 1990. The genetics of protein secretion in E. coli. Trends Genet. 6:329-334.
4. Birnboim, H., and J. Doly. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7:1513-1523.
5. Braun, P., J. Tommassen, and A. Filloux. 1996. Role of the propeptide in folding and secretion of elastase of Pseudomonas aeruginosa. Mol. Microbiol. 19:297-306.
6. Chen, M. W., and V. Nagarajan. 1993. A cytoplasmic protein is incompatible for export of chloramphenicol acetyltransferase from Bacillus subtilis. J. Bacteriol. 175:5697-5700.
7. Davis, A., I. B. Moore, D. S. Parker, and H. Taniuchi. 1977. Nuclease B: a possible precursor of nuclease A, an extracellular nuclease of Staphylococcus aureus. J. Biol. Chem. 252:6544-6553.
8. de Vos, W. M., and G. F. M. Simons. 1994. Gene cloning and expression in lactococci, p. 52-105. In M. J. Gasson and W. M. de Vos (ed.), Genetics and biotechnology of lactic acid bacteria. Chapman and Hall, London, England.
9. Duffaud, G., and M. Inouye. 1988. Signal peptidases recognize a structure feature at the cleavage site of secretory proteins. J. Biol. Chem. 263:10224-10228.
10. Gasson, M. J. 1983. Plasmid complements of Streptococcus lactis NCDO 712 and other lactic acid streptococci after protoplast-induced curing. J. Bacteriol. 154:1-9.
11. Gibson, T. J. 1984. Ph.D. thesis. University of Cambridge, Cambridge, England.
12. Gottesman, S. 1987. Regulation by proteolysis, p. 1308-1312. In F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 2. American Society for Microbiology, Washington, D.C.
13. Ikemura, H., and M. Inouye. 1988. In vitro processing of prosubtilisin produced in Escherichia coli. J. Biol. Chem. 263:12959-12963.
14. Itoh, Y., K. Kanoh, K. Nakamura, K. Takase, and K. Yamane. 1990. Artificial insertion of peptides between signal peptide and mature protein: effect on secretion and processing of hybrid thermostable α-amylases in Bacillus subtilis and Escherichia coli cells. J. Gen. Microbiol. 136:1551-1558.
15. Kovacevic, S., L. E. Veal, H. M. Hsiung, and J. R. Miller. 1985. Secretion of staphylococcal nuclease by Bacillus subtilis. J. Bacteriol. 162:521-528.
16. Langella, P., Y. Le Loir, S. D. Ehrlich, and A. Gruss. 1993. Efficient plasmid mobilization by pIP501 in Lactococcus lactis subsp. lactis. J. Bacteriol. 175: 5806-5813.
17. Le Loir, Y., A. Gruss, S. D. Ehrlich, and P. Langella. 1994. Direct screening of recombinants in gram-positive bacteria using the secreted staphylococcal nuclease as a reporter. J. Bacteriol. 176:5135-5139.
18. Li, P. J., J. Beckwith, and H. Inouye. 1988. Alteration of the amino terminus of the mature sequence of a periplasmic protein can severely affect protein export in Escherichia coli. Proc. Natl. Acad. Sci. USA 85:7685-7689.
19. Liebl, W., A. J. Sinskey, and K. H. Schleifer. 1992. Expression, secretion, and processing of staphylococcal nuclease by Corynebacterium glutamicum. J. Bacteriol. 174:1854-1861.
20. Liu, G., T. B. Topping, and L. L. Randall. 1989. Physiological role during export for the retardation of folding by the leader peptide of maltose-binding protein. Proc. Natl. Acad. Sci. USA 86:9213-9217.
21. MacIntyre, S., M. L. Eschbach, and B. Mutschler. 1990. Export incompatibility of N-terminal basic residues in a mature polypeptide of Escherichia coli can be alleviated by optimising the signal peptide. Mol. Gen. Genet. 221:466-474.
22. Mézes, P. S. F., Y. Q. Yang, M. Hussain, and J. O. Lampen. 1983. Bacillus cereus 569/H β-lactamase I: cloning in Escherichia coli and signal sequence determination. FEBS Lett. 161:195-200.
23. Miller, J. R., S. Kovacevic, and L. E. Veal. 1987. Secretion and processing of staphylococcal nuclease by Bacillus subtilis. J. Bacteriol. 169:3508-3514.
24. Miller, J. R., L. E. Veal, and S. Kovacevic. 1988. Human growth hormone-nuclease fusion proteins: Bacillus subtilis mutants with altered growth hormone production and secretion, p. 377-382. In A. T. Ganesan and J. A. Hoch (ed.), Genetics and biotechnology of bacilli, vol. 2. Academic Press, Inc., San Diego, Calif.
25. Morel, F. 1997. Personal communication.
26. Nagarajan, V. 1993. Protein secretion, p. 713-726. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria. American Society for Microbiology, Washington, D.C.
27. Nakajima, R., T. Imanaka, and S. Aiba. 1985. Nucleotide sequence of the Bacillus stearothermophilus α-amylase gene. J. Bacteriol. 163:401-406.
28. Neuberger, M. S., G. T. Williams, and R. O. Fox. 1984. Recombinant antibodies possessing novel effector functions. Nature 312:604-608.
29. Norton, P. M., H. W. Brown, J. M. Wells, A. M. MacPherson, P. W. Wilson, and R. W. Le Page. 1996. Factors affecting the immunogenicity of tetanus toxin fragment C expressed in Lactococcus lactis. FEMS Immunol. Med. Microbiol. 14(2-3):167-177.
30. Norton, P. M., J. M. Wells, H. W. Brown, A. M. MacPherson, and R. W. Le Page. 1997. Protection against tetanus toxin in mice nasally immunized with recombinant Lactococcus lactis expressing tetanus toxin fragment C. Vaccine 15:616-619.
31. Perez-Martinez, G., J. Kok, G. Venema, J. M. van Dijl, H. Smith, and S. Bron. 1992. Protein export elements from Lactococcus lactis. Mol. Gen. Genet. 234:401-411.
32. Píard, J. C., R. Jimenez-Diaz, S. D. Ehrlich, V. A. Fischetti, and A. Gruss. 1997. The M6 protein of Streptococcus pyogenes and its potential as a tool to anchor biologically active molecules at the surface of lactic acid bacteria, p. 545-550. In T. Horaud (ed.), Streptococci and the host. Plenum Press, New York, N.Y.
33. Poquet, I., S. D. Ehrlich, and A. Gruss. 1998. An export-specific reporter designed for gram-positive bacteria: application to Lactococcus lactis. J. Bacteriol. 180:1904-1912.
34. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
35. Puohiniemi, R., M. Simonen, S. Muttilainen, J. P. Himanen, and M. Sarvas. 1992. Secretion of Escherichia coli outer membrane proteins OmpA and OmpF in Bacillus subtilis is blocked at an early intracellular step. Mol. Microbiol. 6:981-990.
36. Raya, R. 1997. Personal communication.
37. Recsei, P. Personal communication.
38. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
39. Sasamoto, H., K. Nakasawa, K. Tsutsumi, K. Takase, and K. Yamane. 1988. Signal peptide of Bacillus subtilis α-amylase. J. Biochem. 106:376-382.
40. Savijoki, K., M. Kahala, and A. Palva. 1997. High-level heterologous protein production in Lactococcus and Lactobacillus using a new secretion system based on the Lactobacillus brevis S-layer signals. Gene 186:255-262.
41. Schatz, G., and B. Dobberstein. 1996. Common principles of protein translocation across membranes. Science 271:1519-1526.
42. Shortle, D. 1983. A genetic system for analysis of staphylococcal nuclease. Gene 22:181-189.
43. Sibakov, M., T. Koivula, A. von Wright, and I. Palva. 1991. Secretion of TEM β-lactamase with signal sequences isolated from the chromosome of Lactococcus lactis subsp. lactis. Appl. Environ. Microbiol. 57:341-348.
44. Silen, J. L., and D. A. Agard. 1989. The α-lytic protease pro-region does not require a physical linkage to activate the protease domain in vivo. Nature 341:462-464.
45. 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.
46. Simonen, M., and I. Palva. 1993. Protein secretion in Bacillus species. Microbiol. Rev. 57:109-137.
47. Simons, G., G. Rutten, G. Rutten, M. Nijhuis, and M. van Asseldonk. 1992. Production of prochymosin in lactococci. Adv. Exp. Med. Biol. 306:115-120.
48. Steidler, L., J. M. Wells, A. Raeymaekers, J. Vandekerckhove, W. Fiers, and E. Remaut. 1995. Secretion of biologically active murine interleukin-2 by Lactococcus lactis subsp. lactis. Appl. Environ. Microbiol. 61:1627-1629.
49. Suciu, D., and M. Inouye. 1996. The 19-residue pro-peptide of staphylococcal nuclease has a profound secretion-enhancing ability in Escherichia coli. Mol. Microbiol. 21:181-195.
50. Summers, R. G., and J. R. Knowles. 1989. Illicit secretion of a cytoplasmic protein into the periplasm of Escherichia coli requires a signal peptide plus a portion of the cognate secreted protein. Demarcation of the critical region of the mature protein. J. Biol. Chem. 264:20074-20081.
51. Takase, K., H. Mizuno, and K. Yamane. 1988. NH2-terminal processing of Bacillus subtilis α-amylase. J. Biol. Chem. 263:11548-11553.
52. Terzaghi, B. E., and W. E. Sandine. 1975. Improved medium for lactic streptococci and their bacteriophages. Appl. Environ. Microbiol. 29:807-813.
53. van Asseldonk, M., G. Rutten, M. Oteman, R. J. Siezen, W. M. de Vos, and G. Simons. 1990. Cloning of usp45, a gene encoding a secreted protein from Lactococcus lactis subsp. lactis MG1363. Gene 95:155-160.
54. 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 α-amylasc. Mol. Gen. Genet. 240:428-434.
55. van der Vossen, J. M. B. M., D. van der Lelie, and G. Venema. 1987. Isolation and characterization of Streptococcus cremoris Wg2-specific promoters. Appl. Environ. Microbiol. 53:2452-2457.
56. von Heijne, G. 1984. How signal sequences maintain cleavage specificity. J. Mol. Biol. 173:243-251.
57. von Heijne, G. 1986. Net N-C charge imbalance may be important for signal sequence function in bacteria. J. Mol. Biol. 192:287-290.
58. von Heijne, G. 1990. The signal peptide. J. Membr. Biol. 115:195-201.
59. Yamane, K., and S. Mizushima. 1988. Introduction of basic amino acid residue after the signal peptide inhibits protein translocation across the cell membrane of Escherichia coli. 3. Biol. Chem. 263:19690-19696.
60. Zagorec, M., and M. Steinmetz. 1990. Expression of levansucrase-β-galactosidase hybrids inhibits secretion and is lethal in Bacillus subtilis. J. Gen. Microbiol. 136:1137-1143.
61. Zhu, X., Y. Ohta, F. Jordan, and M. Inouye. 1989. Pro-sequence of subtilisin can guide the refolding of denatured subtilisin in an intermolecular process. Nature 339:483-484.