Influence of Lipoteichoic Acid D-Alanylation on Protein Secretion in Lactococcus lactis as Revealed by Random Mutagenesis

Applied and Environmental Microbiology

Volumn 70, Issue 3, 2004, Pages 1600-1607

  Nouaille, S ^a   Commissaire, J ^a   Gratadoux, J J ^a   Ravn, P ^b   Bolotin, A ^a   Gruss, A ^a   Le Loir, Y ^a   Langella, P ^a  

^a CEMAGREF   (France)

^b Biotechnological Institute Denmark   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMES; DRUG THERAPY; ENZYMES; GENES; MUTAGENESIS; PATHOLOGY; PROTEINS;

HETEROLOGOUS PROTEINS; MUTANT PHENOTYPES;

MICROBIOLOGY;

DEXTRO ALANINE; HYBRID PROTEIN; LIPOTEICHOIC ACID; NUCLEASE; PEPTIDE; PROTEIN;

BACTERIUM;

ARTICLE; CELL SURFACE; CHROMOSOME; GENE CASSETTE; LACTOCOCCUS LACTIS; MUTAGENESIS; PHENOTYPE; PROTEIN SECRETION;

ALANINE; BACTERIAL PROTEINS; GENES, BACTERIAL; LACTOCOCCUS LACTIS; LIPOPOLYSACCHARIDES; MICROCOCCAL NUCLEASE; MUTAGENESIS, INSERTIONAL; PEPTIDOGLYCAN; RECOMBINANT FUSION PROTEINS; TEICHOIC ACIDS;

BACTERIA (MICROORGANISMS); LACTOCOCCUS LACTIS; POSIBACTERIA; STREPTOCOCCUS;

EID: 1642312955     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.3.1600-1607.2004     Document Type: Article

References (49)

1. Abachin, E., C. Poyart, E. Pellegrini, F. Milohanic, F. Fiedler, P. Berche, and P. Trieu-Cuot. 2002. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43:1-14.
2. Bermudez-Humaran, L. G., P. Langella, N. G. Cortes-Perez, A. Gruss, R. S. Tamez-Guerra, S. C. Oliveira, C. O. S., R. Montes de Oca-Luna, and Y. Le Loir. 2003. Intranasal immunization with recombinant Lactococcus lactis secreting murine interleukin-12 enhances antigen-specific Th1 cytokine production. Infect. Immun. 71:1887-1896.
3. Bermudez-Humaran, L. G., P. Langella, A. Miyoshi, A. Gruss, R. T. Guerra, R. Montes de Oca-Luna, and Y. Le Loir. 2002. Production of human papillomavirus type 16 E7 protein in Lactococcus lactis. Appl. Environ. Microbiol. 68:917-922.
4. Birnboim, H. C., and J. Doly. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res, 7:1513-1523.
5. Biswas, I., A. Gruss, S. D. Ehrlich, and E. Maguin. 1993. High-efficiency gene inactivation and replacement system for gram-positive bacteria. J. Bacteriol. 175:3628-3635.
6. Bolhuis, A., H. Tjalsma, H. E. Smith, A. de Jong, R. Meima, G. Venema, S. Bron, and J. M. van Dijl. 1999. Evaluation of bottlenecks in the late stages of protein secretion in Bacillus subtilis. Appl. Environ. Microbiol. 65:2934-2941.
7. 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.
8. Boyd, D. A., D. G. Cvitkovitch, A. S. Bleiweis, M. Y. Kiriukhin, D. V. Debabov, F. C. Neuhaus, and I. R. Hamilton. 2000. Defects in D-alanyllipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity. J. Bacteriol. 182:6055-6065.
9. Buist, G., J. Kok, K. J. Leenhouts, M. Dabrowska, G. Venema, and A. J. Haandrikman. 1995. Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation. J. Bacteriol. 177:1554-1563.
10. a. Chopin, A., A. Bolotin, A. Sorokin, S. D. Ehrlich, and M. C. Chopin. 2001. Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations. Nucleic Acids Res. 29:644-651.
11. Clemans, D. L., P. E. Kolenbrander, D. V. Debabov, Q. Zhang, R. D. Lunsford, H. Sakone, C. J. Whittaker, M. P. Heaton, and F. C. Neuhaus. 1999. Insertional inactivation of genes responsible for the D-alanylation of lipoteichoic acid in Streptococcus gordonü DL1 (Challis) affects intrageneric coaggregations. Infect. Immun. 67:2464-2474.
12. Debabov, D. V., M. Y. Kiriukhin, and F. C. Neuhaus. 2000. Biosynthesis of lipoteichoic acid in Lactobacillus rhamnosus: role of DltD in D-alanylation. J. Bacteriol. 182:2855-2864.
13. Delorme, C., J. J. Godon, S. D. Ehrlich, and P. Renault. 1993. Gene inactivation in Lactococcus lactis: histidine biosynthesis. J. Bacteriol. 175:4391-4399.
14. Delorme, C., J. J. Godon, S. D. Ehrlich, and P. Renault. 1994. Mosaic structure of large regions of the Lactococcus lactis subsp. cremoris chromosome. Microbiology 140:3053-3060.
15. de Vos, W. M. 1999. Gene expression systems for lactic acid bacteria. Curr. Opin. Microbiol. 2:289-295.
16. Dieye, Y., S. Usai, F. Clier, A. Gruss, and J. C. Piard. 2001. Design of a protein-targeting system for lactic acid bacteria. J. Bacteriol. 183:4157-4166.
17. Duwat, P., A. Cochu, S. D. Ehrlich, and A. Gruss. 1997. Characterization of Lactococcus lactis UV-sensitive mutants obtained by ISS1 transposition. J. Bacteriol. 179:4473-4479.
18. Gasson, M. J. 1983. Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J. Bacteriol. 154:1-9.
19. Gibson, T. J. 1984. Ph.D. thesis. University of Cambridge, Cambridge, England.
20. Glenting, J., S. M. Madsen, A. Vrang, A. Fomsgaard, and H. Israelsen. 2002. A plasmid selection system in Lactococcus lactis and its use for gene expression in L. lactis and human kidney fibroblasts. Appl. Environ. Microbiol. 68:5051-5056.
21. Gross, M., S. E. Cramton, F. Gotz, and A. Peschel. 2001. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun. 69:3423-3426.
22. Hyyrylainen, H. L., M. Vitikainen, J. Thwaite, H. Wu, M. Sarvas, C. R. Harwood, V. P. Kontinen, and K. Stephenson. 2000. D-Alanine substitution of teichoic acids as a modulator of protein folding and stability at the cytoplasmic membrane/cell wall interface of Bacillus subtilis. J. Biol. Chem. 275:26696-26703.
23. Jacobs, M. F., J. B. Andersen, T. V. Borchert, and V. P. Kontinen. 1995. Identification of a Bacillus subtilis secretion mutant using a beta-galactosidase screening procedure. Microbiology 141:1771-1779.
24. Kleerebezem, M., M. M. Beerthuyzen, E. E. Vaughan, W. M. de Vos, and O. P. Kuipers. 1997. Controlled gene expression systems for lactic acid bacteria: transferable nisin-inducible expression cassettes for Lactococcus, Leuconostoc, and Lactobacillus spp. Appl. Environ. Microbiol. 63:4581-4584.
25. Kontinen, V. P., and M. Sarvas. 1988. Mutants of Bacillus subtilis defective in protein export. J. Gen. Microbiol. 134:2333-2344.
26. 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.
27. 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.
28. Le Loir, Y., A. Gruss, S. D. Ehrlich, and P. Langella. 1998. A nine-residue synthetic propeptide enhances secretion efficiency of heterologous proteins in Lactococcus lactis. J. Bacteriol. 180:1895-1903.
29. 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.
30. Leloup, L., A. Haddaoui el, R. Chambert, and M. F. Petit-Glatron. 1997. Characterization of the rate-limiting step of the secretion of Bacillus subtilis alpha-amylase overproduced during the exponential phase of growth. Microbiology 143:3295-3303.
31. 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.
32. Miyoshi, A., I. Poquet, V. Azevedo, J. Commissaire, L. Bermudez-Humaran, E. Domakova, Y. Le Loir, S. C. Oliveira, A. Gruss, and P. Langella. 2002. Controlled production of stable heterologous proteins in Lactococcus lactis. Appl. Environ. Microbiol. 68:3141-3146.
33. Neuhaus, F. C., M. P. Heaton, D. V. Debabov, and Q. Zhang. 1996. The dlt operon in the biosynthesis of D-alanyl-lipoteichoic acid in Lactobacillus casei. Microb. Drug Resist. 2:77-84.
34. Ntamere, A. S., D. J. Taron, and F. C. Neuhaus. 1987. Assembly of D-alanyllipoteichoic acid in Lactobacillus casei: mutants deficient in the D-alanyl ester content of this amphiphile. J. Bacteriol. 169:1702-1711.
35. Perego, M., P. Glaser, A. Minutello, M. A. Strauch, K. Leopold, and W. Fischer. 1995. Incorporation of D-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J. Biol. Chem. 270:15598-15606.
36. Peschel, A., M. Otto, R. W. Jack, H. Kalbacher, G. Jung, and F. Gotz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405-8410.
37. Poquet, I., V. Saint, E. Seznec, N. Simoes, A. Bolotin, and A. Gruss. 2000. HtrA is the unique surface housekeeping protease in Lactococcus lactis and is required for natural protein processing. Mol. Microbiol. 35:1042-1051.
38. Poyart, C., M. C. Lamy, C. Boumaila, F. Fiedler, and P. Trieu-Cuot. 2001. Regulation of D-alanyl-lipoteichoic acid biosynthesis in Streptococcus agalactiae involves a novel two-component regulatory system. J. Bacteriol. 183:6324-6334.
39. Poyart, C., E. Pellegrini, M. Marceau, M. Baptista, F. Jaubert, M. C. Lamy, and P. Trieu-Cuot. 2003. Attenuated virulence of Streptococcus agalactiae deficient in D-alanyl-lipoteichoic acid is due to an increased susceptibility to defensins and phagocytic cells. Mol. Microbiol. 49:1615-1625.
40. Ribeiro, L. A., V. Azevedo, Y. Le Loir, S. C. Oliveira, Y. Dieye, J. C. Piard, A. Gruss, and P. Langella. 2002. Production and targeting of the Brucella abortus antigen L7/L12 in Lactococcus lactis: a first step towards food-grade live vaccines against brucellosis. Appl. Environ. Microbiol. 68:910-916.
41. 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.
42. Shortle, D. 1983. A genetic system for analysis of staphylococcal nuclease. Gene 22:181-189.
43. Sorensen, K. I., R. Larsen, A. Kibenich, M. P. Junge, and E. Johansen. 2000. A food-grade cloning system for industrial strains of Lactococcus lactis. Appl. Environ. Microbiol. 66:1253-1258.
44. Steidler, L., W. Hans, L. Schotte, S.; Neirynck, F. Obermeier, W. Falk, W. Fiers, and E. Remaut. 2000. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289:1352-1355.
45. Terzaghi, B., and W. E. Sandine. 1975. Improved medium for lactic acid streptococci and their bacteriophages. Appl. Microbiol. 29:807-813.
46. Thwaite, J. E., L. W. Baillie, N. M. Carter, K. Stephenson, M. Rees, C. R. Harwood, and P. T. Emmerson. 2002. Optimization of the cell wall microenvironment allows increased production of recombinant Bacillus anthracis protective antigen from B. subtilis. Appl. Environ. Microbiol. 68:227-234.
47. 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.
48. Wecke, J., M. Perego, and W. Fischer. 1996. D-Alanine deprivation of Bacillus subtilis teichoic acids is without effect on cell growth and morphology but affects the autolytic activity. Microb. Drug Resist. 2:123-129.
49. Wells, J. M., P. W. Wilson, P. M. Norton, M. J. Gasson, and R. W. Le Page. 1993. Lactococcus lactis: high-level expression of tetanus toxin fragment C and protection against lethal challenge. Mol. Microbiol. 8:1155-1162.