The extracytoplasmic folding factor PrsA is required for protein secretion only in the presence of the cell wall in Bacillus subtilis

References

1. Archibald A. R, Hancock I. C., Harwood C. R. 1993; Cell wall structure, synthesis and turnover. In Bacillus subtilis and Other Gram-positive Bacteria pp  381–410 Edited by Sonenshein A.L., Hoch J.A., Losick R. Washington, DC: American Society for Microbiology;
   [Google Scholar]
2. Arié J. P, Sassoon N., Betton J. M. 2001; Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli . Mol Microbiol 39:199–210
   [Google Scholar]
3. Behrens S, Maier R, de Cock H, Schmid F. X., Gross C. A. 2001; The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 20:285–294
   [Google Scholar]
4. Beveridge T. J., Murray R. G. 1980; Sites of metal deposition in the cell wall of Bacillus subtilis . J Bacteriol 141:876–887
   [Google Scholar]
5. Bolhuis A, Tjalsma H, Smith H. E, de Jong A, Meima R, Venema G, Bron S., van Dijl J. M. 1999; Evaluation of bottlenecks in the late stages of protein secretion in Bacillus subtilis . Appl Environ Microbiol 65:2934–2941
   [Google Scholar]
6. Bose S, Weikl T, Bugl H., Buchner J. 1996; Chaperone function of Hsp90-associated proteins. Science 274:1715–1717
   [Google Scholar]
7. Demchick P., Koch A. L. 1996; The permeability of the wall fabric of Escherichia coli and Bacillus subtilis . J Bacteriol 178:768–773
   [Google Scholar]
8. Freeman B. C, Toft D. O., Morimoto R. I. 1996; Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274:1718–1720
   [Google Scholar]
9. Freskgard P. O, Bergenhem N, Jonsson B. H, Svensson M., Carlsson U. 1992; Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258:466–468
   [Google Scholar]
10. Haddaoui E. A, Leloup L, Petit-Glatron M. F., Chambert R. 1997; Characterization of a stable intermediate trapped during reversible refolding of Bacillus subtilis α -amylase. Eur J Biochem 249:505–509
    [Google Scholar]
11. Harwood C. R., Cutting S. M. 1990 Molecular Biological Methods for Bacillus New York: Wiley;
    [Google Scholar]
12. Hyyryläinen H.-L, Vitikainen M, Thwaite J, Wu H, Sarvas M, Harwood C, Kontinen V., Spehenson K. 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
    [Google Scholar]
13. Hyyryläinen H. L, Bolhuis A, Darmon E. 8 other authors 2001; A novel two-component regulatory system in Bacillus subtilis for the survival of severe secretion stress. Mol Microbiol 41:1159–1172
    [Google Scholar]
14. Jacobs M, Andersen J. B, Kontinen V., Sarvas M. 1993; Bacillus subtilis PrsA is required in vivo as an extracytoplasmic chaperone for secretion of active enzymes synthesized either with or without pro-sequences. Mol Microbiol 8:957–966
    [Google Scholar]
15. Kontinen V., Sarvas M. 1993; The PrsA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion. Mol Microbiol 8:727–737
    [Google Scholar]
16. Kontinen V. P, Saris P., Sarvas M. 1991; A gene ( prsA ) of Bacillus subtilis involved in a novel, late stage of protein export. Mol Microbiol 5:1273–1283
    [Google Scholar]
17. Leloup L, el Haddaoui A, Chambert R., Petit-Glatron M. F. 1997; Characterization of the rate-limiting step of the secretion of Bacillus subtilis α -amylase overproduced during the exponential phase of growth. Microbiology 143:3295–3303
    [Google Scholar]
18. Leloup L, Le Saux J, Petit-Glatron M.-F., Chambert R. 1999; Kinetics of the secretion of Bacillus subtilis levanase overproduced during the exponential phase of growth. Microbiology 145:613–619
    [Google Scholar]
19. Leskelä S, Wahlström E, Hyyryläinen H. L, Jacobs M, Palva A, Sarvas M., Kontinen V. P. 1999a; Ecs, an ABC transporter of Bacillus subtilis : dual signal transduction functions affecting expression of secreted proteins as well as their secretion. Mol Microbiol 31:533–543
    [Google Scholar]
20. Leskelä S, Wahlström E, Kontinen V. P., Sarvas M. 1999b; Lipid modification of prelipoproteins is dispensable for growth but essential for efficient protein secretion in Bacillus subtilis : characterization of the lgt gene. Mol Microbiol 31:1075–1085
    [Google Scholar]
21. Lounatmaa K. 1985; Electron microscopic methods for the study of bacterial surface structures. In Enterobacterial Surface Antigens. Methods for Molecular Characterisation pp  243–261 Edited by Korhonen T. K., Dawes E. A., Mäkelä P. H. Amsterdam: Elsevier;
    [Google Scholar]
22. Manting E. H., Driessen A. J. M. 2000; Escherichia coli translocase: the unravelling of a molecular machine. Mol Microbiol 37:226–238
    [Google Scholar]
23. Margot P., Karamata D. 1996; The wprA gene of Bacillus subtilis 168, expressed during exponential growth, encodes a cell-wall-associated protease. Microbiology 142:3437–3444
    [Google Scholar]
24. Meens J, Frings E, Klose M., Freudl R. 1993; An outer membrane protein (OmpA) of Escherichia coli can be translocated across the cytoplasmic membrane of Bacillus subtilis . Mol Microbiol 9:847–855
    [Google Scholar]
25. Merchante R, Pooley H. M., Karamata D. 1995; A periplasm in Bacillus subtilis . J Bacteriol 177:6176–6183
    [Google Scholar]
26. Palva I. 1982; Molecular cloning of α -amylase gene from Bacillus amyloliquefaciens and its expression in B. subtilis . Gene 19:81–87
    [Google Scholar]
27. Perego M, Glaser P, Minutello A, Strauch M. A, Leopold K., Fischer W. 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
    [Google Scholar]
28. Peschel A, Otto M, Jack R. W, Kalbacher H, Jung G., Götz F. 1999; Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins and other antimicrobial peptides. J Biol Chem 274:8405–8410
    [Google Scholar]
29. Petit-Glatron M.-F, Grajcar L, Munz A., Chambert R. 1993; The contribution of the cell wall to a transmembrane calcium gradient could play a key role in Bacillus subtilis protein secretion. Mol Microbiol 9:1097–1106
    [Google Scholar]
30. Pummi T, Leskelä S, Wahlström E, Gerth U, Tjalsma H, Hecker M, Sarvas M., Kontinen V. P. 2002; ClpXP protease regulates the signal peptide cleavage of secretory preproteins in Bacillus subtilis with a mechanism distinct from that of the Ecs ABC transporter. J Bacteriol 184:1010–1018
    [Google Scholar]
31. Puohiniemi R, Simonen M, Muttilainen S, Himanen J. P., Sarvas M. 1992; Secretion of the Escherichia coli outer membrane proteins OmpA and OmpF in Bacillus subtilis is blocked at an early intracellular step. Mol Microbiol 6:981–990
    [Google Scholar]
32. Rahfeld J.-U, Rücknagel K. P, Schelbert B, Ludvig B, Hacker J, Mann K., Fischer G. 1994; Confirmation of the existence of a third family among peptidyl-prolyl cis / trans isomerases. Amino acid sequence and recombinant production of parvulin. FEBS Lett 352:180–184
    [Google Scholar]
33. Ramm K., Plückthun A. 2000; The periplasmic Escherichia coli peptidyl-prolyl cis / trans -isomerase FkpA. II. Isomerase-independent chaperone activity in vitro . J Biol Chem 275:17106–17113
    [Google Scholar]
34. Ramm K., Plückthun A. 2001; High enzymatic activity and chaperone function are mechanistically related features of the dimeric E. coli peptidyl-prolyl-isomerase FkpA. J Mol Biol 310:485–498
    [Google Scholar]
35. Sanders R. L., May B. K. 1975; Evidence for extrusion of unfolded extracellular enzyme polypeptide chains through membranes of Bacillus amyloliquefaciens . J Bacteriol 123:806–814
    [Google Scholar]
36. Scholz C, Stoller G, Zarnt T, Fischer G., Schmid F. X. 1997; Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J 16:54–58
    [Google Scholar]
37. Smith T. J, Blackman S. A., Foster S. J. 2000; Autolysins of Bacillus subtilis : multiple enzymes with multiple functions. Microbiology 146:249–262
    [Google Scholar]
38. Stephenson K, Carter N. M, Harwood C. R, Petit-Glatron M. F., Chambert R. 1998; The influence of protein folding on late stages of the secretion of α -amylases from Bacillus subtilis . FEBS Lett 430:385–389
    [Google Scholar]
39. Tjalsma H, Bolhuis A, Jongbloed J. D, Bron S., van Dijl J. M. 2000; Signal peptide-dependent protein transport in Bacillus subtilis : a genome-based survey of the secretome. Microbiol Mol Biol Rev 64:515–547
    [Google Scholar]
40. Vitikainen M, Pummi T, Airaksinen U, Wu H, Sarvas M., Kontinen V. P. 2001; Quantitation of the capacity of the secretion apparatus and requirement for PrsA in growth and secretion of α -amylase in Bacillus subtilis . J Bacteriol 183:1881–1890
    [Google Scholar]
41. Yoshida K, Sano H, Seki S, Oda M, Fujimura M., Fujita Y. 1995; Cloning and sequencing of a 29 kb region of the Bacillus subtilis genome containing the hut and wapA loci. Microbiology 141:337–343
    [Google Scholar]