1887

Abstract

Summary: Protein secretion in Gram-negative bacteria is often dependent on the general secretory pathway (GSP). In , this system requires at least 12 Xcp (Gsp) proteins, which are proposed to constitute a multiprotein complex localized in the bacterial envelope. Hitherto, little was known about the mutual interactions between Xcp proteins. In this study, mutants affected in the gene encoding a bitopic inner-membrane protein were analysed to investigate the role of this protein in the architecture of the secretory machinery. The absence of XcpZ resulted in a decreased amount of XcpY. Reciprocally, XcpZ was not detectable in a mutant demonstrating a mutual stabilization of these two proteins. These results strongly suggest that XcpZ and XcpY interact within the functional secretory apparatus.

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/content/journal/micro/10.1099/00221287-144-12-3379
1998-12-01
2021-10-28
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References

  1. Akrim M., Bally M., Ball G., Tommassen J., Teerink H., Filloux A., Lazdunski A. 1993; Xcp -mediated protein secretion in Pseudomonas aeruginosa: identification of two additional genes and evidence for regulation of xcp gene expression.. Mol Microbiol 10:431–443
    [Google Scholar]
  2. Bally M., Filloux A., Akrim M., Ball G., Lazdunski A., Tommassen J. 1992; Protein secretion in Pseudomonas aeruginosa: characterization of seven xcp genes and processing of secretory apparatus components by prepilin peptidase.. Mol Microbiol 6:1121–1131
    [Google Scholar]
  3. Bitter W., Koster M., Latijnhouwers M., de Cock H., Tommassen J. 1998; Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. . Mol Microbiol 27:209–219
    [Google Scholar]
  4. Bleves S., Lazdunski A., Filloux A. 1996; Membrane topology of three Xcp proteins involved in exoprotein transport by Pseudomonas aeruginosa. . J Bacteriol 178:4297–4300
    [Google Scholar]
  5. Bleves S., Voulhoux R., Michel G., Lazdunski A., Tommassen J., Filloux A. 1998; The secretion apparatus of Pseudomonas aeruginosa-, identification of a fifth pseudopilin, XcpX (GspK family).. Mol Microbiol 27:159–170
    [Google Scholar]
  6. Chapon-Hervé V., Akrim M., Latifi A., Williams P., Lazdunski A., Bally M. 1997; Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. . Mol Microbiol 24:1169–1178
    [Google Scholar]
  7. Fellay R., Frey J., Krisch H. 1987; Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria.. Gene 52:147–154
    [Google Scholar]
  8. Fernandez D., Spudich G.M., Zhou X.-R., Christie P.J. 1996; The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus.. J Bacteriol 178:3168–3176
    [Google Scholar]
  9. Filloux A., Bally M., Ball G., Akrim M., Tommassen J., Lazdunski A. 1990; Protein secretion in gram-negative bacteria: transport across the outer membrane involves common mechanisms in different bacteria.. EMBO J 9:4323–4329
    [Google Scholar]
  10. Francetic O., Pugsley A.P. 1996; The cryptic general secretory pathway {gsp) operon of Escherichia coli K-12 encodes functional proteins.. J Bacteriol 178:3544–3549
    [Google Scholar]
  11. Friedman A.M., Long S.R., Brown S.E., Buikema W.J., Ausubel F.M. 1982; Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants.. Gene 18:289–296
    [Google Scholar]
  12. Fürste J.P., Pansegrau W., Frank R., Blöcker H., Scholz P., Bagdasarian M., Lanka E. 1986; Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector.. Gene 48:119–131
    [Google Scholar]
  13. de Groot A., Filloux A., Tommassen J. 1991; Conservation of xcp genes, involved in the two-step secretion process, in different Pseudomonas species and other Gram-negative bacteria.. Mol Gen Genet 229:278–284
    [Google Scholar]
  14. Guruprasad K., Reddy B.V., Pandit M.W. 1990; Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence.. Protein Eng 4:155–161
    [Google Scholar]
  15. Gutierrez C., Devedjian J.C. 1989; A plasmid facilitating in vitro construction of phoA gene fusions in Escherichia coli. . Nucleic Acids Res 17:3999
    [Google Scholar]
  16. Hardie K.R., Lory S., Pugsley A.P. 1996; Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein.. EMBO J 15:978–988
    [Google Scholar]
  17. Howard S.P., Meiklejohn H.G., Shivak D., Jahagirdar R. 1996; A TonB-like protein and a novel membrane protein containing an ATP-binding cassette function together in exotoxin secretion.. Mol Microbiol 22:595–604
    [Google Scholar]
  18. Kagami Y., Ratliff M., Surber M., Martinez A., Nunn D.N. 1998; Type II 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
    [Google Scholar]
  19. Laemmli U.K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4.. Nature 227:680–685
    [Google Scholar]
  20. Lazdunski A., Filloux A., Michel G., Foglino M., Murgier M., Latifi A., Chapon V., Bleves S. 1996; The general secretion pathway in Pseudomonas aeruginosa: molecular mechanisms and regulation.. In Proceedings of the Fifth International Symposium on Pseudomonads: Molecular Biology and Biotechnology pp. 427–437 Edited by Nakazawa T., Furukawa K., Haas D., Silver S. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  21. Lindeberg M., Salmond G.P.C., Collmer A. 1996; Complementation of deletion mutations in a cloned functional cluster of Erwinia chrysanthemi out genes with Erwinia carotovora out homologues reveals OutC and OutD as candidate gatekeepers of species-specific secretion of proteins via the type II pathway.. Mol Microbiol 20:175–190
    [Google Scholar]
  22. Lu H.-M., Motley S.T., Lory S. 1997; Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion.. Mol Microbiol 25:247–259
    [Google Scholar]
  23. Marmur J. 1961; A procedure for the isolation of deoxyribonucleic acid from micro-organisms.. J Mol Biol 3:208–218
    [Google Scholar]
  24. Morales V.M., Böckman A., Bagdasarian M. 1991; A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants.. Gene 97:39–47
    [Google Scholar]
  25. Nishiyama K., Mizushima S., Tokuda H. 1992; The carboxyl- terminal region of SecE interacts with SecY and is functional in the reconstitution of protein translocation activity in Escherichia coli. . J Biol Chem 267:7170–7176
    [Google Scholar]
  26. Nunn D.N., Lory S. 1991; Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase.. Proc Natl Acad Sci USA 883281–3285
    [Google Scholar]
  27. Nunn D.N., Lory S. 1993; Cleavage, methylation, and localization of the Pseudomonas aeruginosa export proteins XcpT, -U, -V, and -W.. J Bacteriol 175:4375–4382
    [Google Scholar]
  28. Pugsley A.P. 1993; The complete general secretion pathway in Gram-negative bacteria.. Microbiol Rev 57:50–108
    [Google Scholar]
  29. 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
    [Google Scholar]
  30. Pugsley A.P., Possot O. 1993; The general secretory pathway of Klebsiella oxytoca: no evidence for relocalization or assembly of pilin-like PulG protein into a multiprotein complex.. Mol Microbiol 10:665–674
    [Google Scholar]
  31. Reeves P.J., Douglas P., Salmond P.C. 1994; Beta-lactamase topology probe analysis of the OutO NMePhe peptidase, and six other Out protein components of the Erwinia carotovora general secretion pathway apparatus.. Mol Microbiol 12:445–4157
    [Google Scholar]
  32. Sandkvist M., Bagdasarian M., Howard S.P., DiRita V.J. 1995; Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. . EMBO J 14:1664–1673
    [Google Scholar]
  33. Skare J.T., Postle K. 1991; Evidence for a TonB-dependent energy transduction complex in Escherichia coli. . Mol Microbiol 5:2883–2890
    [Google Scholar]
  34. Smith A.W., Iglewski B.H. 1989; Transformation of Pseudomonas aeruginosa by electroporation.. Nucleic Acids Res 17:10509
    [Google Scholar]
  35. Strom M.S., Nunn D.N., Lory S. 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 902404–2408
    [Google Scholar]
  36. Thomas J.D., Reeves P.J., Salmond G.P.C. 1997; The general secretion pathway of Erwinia carotovora subsp.carotovora: analysis of the membrane topology of OutC and OutF.. Microbiology 143:713–720
    [Google Scholar]
  37. Tommassen J., Filloux A., Bally M., Murgier M., Lazdunski A.?. 1992; Protein secretion in Pseudomonas aeruginosa. . FEMS Microbiol Rev 103:73–90
    [Google Scholar]
  38. Wretlind B., Pavlovskis O.R. 1984; Genetic mapping and characterization of Pseudomonas aeruginosa mutants defective in the formation of extracellular proteins.. J Bacteriol 158:801–808
    [Google Scholar]
  39. Zhang Y.B., Broome-Smith J.K. 1990; Correct insertion of a simple eukaryotic plasma-membrane protein into the cytoplasmic membrane of Escherichia coli. . Gene 96:51–57
    [Google Scholar]
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