Export of the pseudopilin XcpT of the Pseudomonas aeruginosa type II secretion system via the signal recognition particle-Sec pathway

Journal of Bacteriology

Volumn 189, Issue 5, 2007, Pages 2069-2076

  Arts, Jorik ^a   Van Boxtel, Ria ^a   Filloux, Alain ^b   Tommassen, Jan ^a   Koster, Margot ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALKALINE PHOSPHATASE; AMPICILLIN; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; GENTAMICIN; HYBRID PROTEIN; KANAMYCIN; PEPTIDASE; PHOA PROTEIN; PILIN; PSEUDOPILIN; SECRETORY PROTEIN; SIGNAL RECOGNITION PARTICLE; UNCLASSIFIED DRUG; XCPT PROTEIN;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIUM PILUS; ENZYME ACTIVITY; ESCHERICHIA COLI; IMMUNOBLOTTING; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; ESCHERICHIA COLI; MEMBRANE TRANSPORT PROTEINS; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; SIGNAL RECOGNITION PARTICLE;

ARCHAEA; ESCHERICHIA COLI; NEGIBACTERIA; POSIBACTERIA; PROKARYOTA; PSEUDOMONAS AERUGINOSA;

EID: 33947360771     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01236-06     Document Type: Article

References (55)

1. Adams, H., P. A. Scotti, H. De Cock, J. Luirink, and J. Tommassen. 2002. The presence of a helix breaker in the hydrophobia core of signal sequences of secretory proteins prevents recognition by the signal-recognition particle in Escherichia coli. Eur. J. Biochem. 269:5564-5571.
2. Ball, G., V. Chapon-Hervé, S. Bleves, G. Michel, and M. Bally. 1999. Assembly of XcpR in the cytoplasmic membrane is required for extracellular protein secretion in Pseudomonas aeruginosa. J. Bacteriol. 181:382-388.
3. Ball, G., E. Durand, A. Lazdunski, and A. Filloux. 2002. A novel type II secretion system in Pseudomonas aeruginosa. Mol. Microbiol. 43:475-485.
4. Bally, M., G. Ball, A. Badere, and A. Lazdunski. 1991. Protein secretion in Pseudomonas aeruginosa: the xcpA gene encodes an integral inner membrane protein homologous to Klebsiella pneumoniae secretion function protein PulO. J. Bacteriol. 173:479-486.
5. Bowers, C. W., F. Lau, and T. J. Silhavy. 2003. Secretion of LamB-LacZ by the signal recognition particle pathway of Escherichia coli. J. Bacteriol. 185:5697-5705.
6. Casadaban, M. J. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555.
7. Casadaban, M. J., and S. N. Cohen. 1980. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138:179-207.
8. China, B., T. Michiels, and G. R. Cornelis. 1990. The pYV plasmid of Yersinia encodes a lipoprotein, YlpA, related to TraT. Mol. Microbiol. 4:1585-1593.
9. Chung, Y. S., and D. Dubnau. 1995. ComC is required for the processing and translocation of ComGC, a pilin-like competence protein of Bacillus subtilis. Mol. Microbiol. 15:543-551.
10. Dalbey, R. E., and W. Wickner. 1985. Leader peptidase catalyzes the release of exported proteins from the outer surface of the Escherichia coli plasma membrane. J. Biol. Chem. 260:15925-15931.
11. de Gier, J. W., Q. A. Valent, G. Von Heijne, and J. Luirink. 1997. The E. coli SRP: preferences of a targeting factor. FEBS Lett. 408:1-4.
12. de Groot, A., I. Heijnen, H. de Cock, A. Filloux, and J. Tommassen. 1994. Characterization of type IV pilus genes in plant growth-promoting Pseudomonas putida WCS358. J. Bacteriol. 176:642-650.
13. de Keyzer, J., C. van der Does, and A. J. M. Driessen. 2003. The bacterial translocase: a dynamic protein channel complex. Cell. Mol. Life Sci. 60:2034-2052.
14. Dupuy, B., M. K. Taba, A. P. Pugsley, and C. Marchal. 1991. Neisseria gonorrhoeae prepilin export studied in Escherichia coli. J. Bacteriol. 173:7589-7598.
15. Durand, E., A. Bernadac, G. Ball, A. Lazdunski, J. N. Sturgis, and A. Filloux. 2003. Type 11 protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J. Bacteriol. 185:2749-2758.
16. Durand, E., G. Michel, R. Voulhoux, J. Kurner, A. Bernadac, and A. Filloux. 2005. XcpX controls biogenesis of the Pseudomonas aeruginosa XcpT-containing pseudopilus. J. Biol. Chem. 280:31378-31389.
17. Enderle, P. J., and M. A. Farwell. 1998. Electroporation of freshly plated Escherichia coli and Pseudomonas aeruginosa cells. BioTechniques 25:954-958.
18. Filloux, A. 2004. The underlying mechanisms of type II protein secretion. Biochim. Biophys. Acta 1694:163-179.
19. Filloux, A., M. Bally, M. Murgier, B. Wretlind, and A. Lazdunski. 1989. Cloning of xcp genes located at the 55 min region of the chromosome and involved in protein secretion in Pseudomonas aeruginosa. Mol. Microbiol. 3:261-265.
20. Filloux, A., G. Michel, and M. Bally. 1998. GSP-dependent protein secretion in gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa. FEMS Microbiol. Rev. 22:177-198.
21. Francetic, O., N. Buddelmeijer, S. Lewenza, C. A. Kumamoto, and A. P. Pugsley. 2007. Signal recognition particle-dependent inner membrane targeting of the PuIG pseudopilin component of a type II secretion system. J. Bacteriol. 189:1780-1793.
22. Francetic, O., S. Lory, and A. P. Pugsley. 1998. A second prepilin peptidase gene in Escherichia coli K-12. Mol. Microbiol. 27:763-775.
23. Garen, A., and H. Echols. 1962. Genetic control of induction of alkaline phosphatase synthesis in E. coli. Proc. Natl. Acad. Sci. USA 48:1398-1402.
24. Gutierrez, C., and J. C. Devedjian. 1989. A plasmid facilitating in vitro construction of phoA gene fusions in Escherichia coli. Nucleic Acids Res. 17:3999.
25. Haas, D., and B. W. Holloway. 1976. R factor variants with enhanced sex factor activity in Pseudomonas aeruginosa. Mol. Gen. Genet. 144:243-251.
26. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plas-mids. J. Mol. Biol. 166:557-580.
27. Kagami, Y., M. Ratliff, M. Surber, A. Martinez, and D. N. Nunn. 1998. Type 11 protein secretion by Pseudomonas aeruginosa: genetic suppression of a conditional mutation in the pilin-like component XcpT by the cytoplasmic component XcpR. Mol. Microbiol. 27:221-233.
28. Koch, H. G., T. Hengelage, C. Neumann-Haefelin, J. MacFarlane, H. K. Hoffschulte, K. L. Schimz, B. Mechler, and M. Müller. 1999. In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/ SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol. Biol. Cell 10:2163-2173.
29. Köhler, R., K. Schäfer, S. Müller, G. Vignon, K. Diederichs, A. Philippsen, P. Ringler, A. P. Pugsley, A. Engel, and W. Welte. 2004. Structure and assembly of the pseudopilin PulG. Mol. Microbiol. 54:647-664.
30. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
31. Langley, K. E., M. R. Villarejo, A. V. Fowler, P. J. Zamenhof, and I. Zabin. 1975. Molecular basis of beta-galactosidase alpha-complementation. Proc. Natl. Acad. Sci. USA 72:1254-1257.
32. LaPointe, C. F., and R. K. Taylor. 2000. The type 4 prepilin peptidases comprise a novel family of aspartic acid proteases. J. Biol. Chem. 275:1502-1510.
33. Lee, H. C., and H. D. Bernstein. 2001. The targeting pathway of Escherichia coli presecretory and integral membrane proteins is specified by the hydrophobicity of the targeting signal. Proc. Natl. Acad. Sci. USA 98:3471-3476.
34. Mayer, M. P. 1995. A new set of useful cloning and expression vectors derived from pBlueScript. Gene 163:41-46.
35. Nunn, D. 1999. Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol. 9:402-408.
36. Nunn, D. N., and S. Lory. 1991. Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc. Natl. Acad. Sci. USA 88:3281-3285.
37. Oliver, D. B., and J. Beckwith. 1981. E. coli mutant pleiotropically defective in the export of secreted proteins. Cell 25:765-772.
38. Osborn, M. J., J. E. Gander, and E. Parisi. 1972. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Site of synthesis of lipopolysaccharide. J. Biol. Chem. 247:3973-3986.
39. Peabody, C. R., Y. J. Chung, M. R. Yen, D. Vidal-Ingigliardi, A. P. Pugsley, and M. H. Saier, Jr. 2003. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051-3072.
40. Pugsley, A. P. 1996. Multimers of the precursor of a type IV pilin-like component of the general secretory pathway are unrelated to pili. Mol. Microbiol. 20:1235-1245.
41. Rather, U., and B. Müller-Hill. 1983. Easy identification of cDNA clones. EMBO J. 2:1791-1794.
42. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Samuelson, J. C., M. Chen, F. Jiang, I. Moller, M. Wiedmann, A. Kuhn, G. J. Phillips, and R. E. Dalbey. 2000. YidC mediates membrane protein insertion in bacteria. Nature 406:637-641.
44. Sauvonnet, N., G. Vignon, A. P. Pugsley, and P. Gounon. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:2221-2228.
45. Shiba, K., K. Ito, T. Yura, and D. P. Cerretti. 1984. A defined mutation in the protein export gene within the spc ribosomal protein operon of Escherichia coli: isolation and characterization of a new temperature-sensitive secY mutant. EMBO J. 3:631-635.
46. Strom, M. S., and S. Lory. 1987. Mapping of export signals of Pseudomonas aeruginosa pilin with alkaline phosphatase fusions. J. Bacteriol. 169:3181-3188.
47. Strom, M. S., and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
48. Strom, M. S., D. N. Nunn, and S. Lory. 1993. A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc. Natl. Acad. Sci. USA 90:2404-2408.
49. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 82:1074-1078.
50. Tian, H., and J. Beckwith. 2002. Genetic screen yields mutations in genes encoding all known components of the Escherichia coli signal recognition particle pathway. J. Bacteriol. 184:111-118.
51. Tian, H., D. Boyd, and J. Beckwith. 2000. A mutant hunt for defects in membrane protein assembly yields mutations affecting the bacterial signal recognition particle and Sec machinery. Proc. Natl. Acad. Sci. USA 97:4730-4735.
52. Tommassen, J., H. van Tol, and B. Lugtenberg. 1983. The ultimate localization of an outer membrane protein of Escherichia coli K-12 is not determined by the signal sequence. EMBO J. 2:1275-1279.
53. von Heijne, G. 1985. Signal sequences. The limits of variation. J. Mol. Biol. 184:99-105.
54. Whitchnrch, C. B., and J. S. Mattick. 1994. Escherichia coli contains a set of genes homologous to those involved in protein secretion, DNA uptake and the assembly of type-4 fimbriae in other bacteria. Gene 150:9-15.
55. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors. Gene 33:103-119.