Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis

Molecular Microbiology

Volumn 77, Issue 1, 2010, Pages 108-127

  Hyyryläinen, Hanne Leena ^a   Marciniak, Bogumila C ^b   Dahncke, Kathleen ^c,e   Pietiäinen, Milla ^a   Courtin, Pascal ^d   Vitikainen, Marika ^a,f   Seppala, Raili ^a   Otto, Andreas ^c   Becher, Dörte ^c   Chapot Chartier, Marie Pierre ^d   Kuipers, Oscar P ^b   Kontinen, Vesa P ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d CEMAGREF   (France)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

^f VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CIS TRANS ISOMERASE; MAGNESIUM; PENICILLIN BINDING PROTEIN; PROTEIN PRSA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; LIPOPROTEIN; MEMBRANE PROTEIN; PEPTIDOGLYCAN; PEPTIDYLPROLYL ISOMERASE; PRSA PROTEIN, BACTERIA;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; CELL STRUCTURE; ENZYME ACTIVITY; ENZYME MECHANISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; BACTERIAL GENE; CELL MEMBRANE; CELL WALL; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; ESSENTIAL GENE; GENE DELETION; GENETICS; METABOLISM; PROTEIN MULTIMERIZATION;

BACILLUS SUBTILIS; POSIBACTERIA;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL MEMBRANE; CELL WALL; GENE DELETION; GENES, BACTERIAL; GENES, ESSENTIAL; LIPOPROTEINS; MAGNESIUM; MEMBRANE PROTEINS; PENICILLIN-BINDING PROTEINS; PEPTIDOGLYCAN; PEPTIDYLPROLYL ISOMERASE; PROTEIN FOLDING; PROTEIN MULTIMERIZATION;

EID: 77953985332     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07188.x     Document Type: Article

References (86)

1. Alonzo, F. 3rd., Port, G.C., Cao, M. Freitag, N.E. (2009) The posttranslocation chaperone PrsA2 contributes to multiple facets of Listeria monocytogenes pathogenesis. Infect Immun 77 : 2612 2623.
2. Antelmann, H., Darmon, E., Noone, D., Veening, J.W., Westers, H., Bron, S., et al. (2003) The extracellular proteome of Bacillus subtilis under secretion stress conditions. Mol Microbiol 49 : 143 156.
3. Atrih, A., Bacher, G., Allmaier, G., Williamson, M.P. Foster, S.J. (1999) Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J Bacteriol 181 : 3956 3966.
4. 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.
5. Bramkamp, M., Weston, L., Daniel, R.A. Errington, J. (2006) Regulated intramembrane proteolysis of FtsL protein and the control of cell division in Bacillus subtilis. Mol Microbiol 62 : 580 591.
6. Carballido-Lopez, R. Errington, J. (2003) The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev Cell 4 : 19 28.
7. Carballido-Lopez, R., Formstone, A., Li, Y., Ehrlich, S.D., Noirot, P. Errington, J. (2006) Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 11 : 399 409.
8. Claessen, D., Emmins, R., Hamoen, L.W., Daniel, R.A., Errington, J. Edwards, D.H. (2008) Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Mol Microbiol 68 : 1029 1046.
9. Courtin, P., Miranda, G., Guillot, A., Wessner, F., Mezange, C., Domakova, E., et al. (2006) Peptidoglycan structure analysis of Lactococcus lactis reveals the presence of an L,d-carboxypeptidase involved in peptidoglycan maturation. J Bacteriol 188 : 5293 5298.
10. Daniel, R.A. Errington, J. (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113 : 767 776.
11. Daniel, R.A., Harry, E.J., Katis, V.L., Wake, R.G. Errington, J. (1998) Characterization of the essential cell division gene ftsL(yIID) of Bacillus subtilis and its role in the assembly of the division apparatus. Mol Microbiol 29 : 593 604.
12. Daniel, R.A., Noirot-Gros, M.F., Noirot, P. Errington, J. (2006) Multiple interactions between the transmembrane division proteins of Bacillus subtilis and the role of FtsL instability in divisome assembly. J Bacteriol 188 : 7396 7404.
13. Darmon, E., Noone, D., Masson, A., Bron, S., Kuipers, O.P., Devine, K.M. van Dijl, J.M. (2002) A novel class of heat and secretion stress-responsive genes is controlled by the autoregulated CssRS two-component system of Bacillus subtilis. J Bacteriol 184 : 5661 5671.
14. Defeu Soufo, H.J. Graumann, P.L. (2004) Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep 5 : 789 794.
15. Defeu Soufo, H.J. Graumann, P.L. (2006) Dynamic localization and interaction with other Bacillus subtilis actin-like proteins are important for the function of MreB. Mol Microbiol 62 : 1340 1356.
16. Divakaruni, A.V., Loo, R.R., Xie, Y., Loo, J.A. Gober, J.W. (2005) The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc Natl Acad Sci USA 102 : 18602 18607.
17. Divakaruni, A.V., Baida, C., White, C.L. Gober, J.W. (2007) The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol Microbiol 66 : 174 188.
18. Drouault, S., Anba, J., Bonneau, S., Bolotin, A., Ehrlich, S.D. Renault, P. (2002) The peptidyl-prolyl isomerase motif is lacking in PmpA, the PrsA-like protein involved in the secretion machinery of Lactococcus lactis. Appl Environ Microbiol 68 : 3932 3942.
19. Ellermeier, C.D. Losick, R. (2006) Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis. Genes Dev 20 : 1911 1922.
20. van den Ent, F., Leaver, M., Bendezu, F., Errington, J., de Boer, P. Lowe, J. (2006) Dimeric structure of the cell shape protein MreC and its functional implications. Mol Microbiol 62 : 1631 1642.
21. Eymann, C., Dreisbach, A., Albrecht, D., Bernhardt, J., Becher, D., Gentner, S., et al. (2004) A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4 : 2849 2876.
22. Figge, R.M., Divakaruni, A.V. Gober, J.W. (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51 : 1321 1332.
23. Formstone, A. Errington, J. (2005) A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis. Mol Microbiol 55 : 1646 1657.
24. Glauner, B. (1988) Separation and quantification of muropeptides with high-performance liquid chromatography. Anal Biochem 172 : 451 464.
25. Glauner, B., Holtje, J.V. Schwarz, U. (1988) The composition of the murein of Escherichia coli. J Biol Chem 263 : 10088 10095.
26. Hani, J., Schelbert, B., Bernhardt, A., Domdey, H., Fischer, G., Wiebauer, K. Rahfeld, J.U. (1999) Mutations in a peptidylprolyl-cis/trans- isomerase gene lead to a defect in 3′-end formation of a pre-mRNA in Saccharomyces cerevisiae. J Biol Chem 274 : 108 116.
27. Harry, E.J., Pogliano, K. Losick, R. (1995) Use of immunofluorescence to visualize cell-specific gene expression during sporulation in Bacillus subtilis. J Bacteriol 177 : 3386 3393.
28. Healy, J., Weir, J., Smith, I. Losick, R. (1991) Post-transcriptional control of a sporulation regulatory gene encoding transcription factor sigma H in Bacillus subtilis. Mol Microbiol 5 : 477 487. (Pubitemid 21896068)
29. Heikkinen, O., Seppala, R., Tossavainen, H., Heikkinen, S., Koskela, H., Permi, P. Kilpelainen, I. (2009) Solution structure of the parvulin-type PPIase domain of Staphylococcus aureus PrsA - implications for the catalytic mechanism of parvulins. BMC Struct Biol 9 : 17.
30. Heinrich, J., Lunden, T., Kontinen, V.P. Wiegert, T. (2008) The Bacillus subtilis ABC transporter EcsAB influences intramembrane proteolysis through RasP. Microbiology 154 : 1989 1997.
31. Hennecke, G., Nolte, J., Volkmer-Engert, R., Schneider-Mergener, J. Behrens, S. (2005) The periplasmic chaperone SurA exploits two features characteristic of integral outer membrane proteins for selective substrate recognition. J Biol Chem 280 : 23540 23548.
32. Hyyryläinen, H.-L., Vitikainen, M., Thwaite, J., Wu, H., Sarvas, M., Harwood, C., et al. (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.
33. Hyyryläinen, H.L., Bolhuis, A., Darmon, E., Muukkonen, L., Koski, P., Vitikainen, M., et al. (2001) A novel two-component regulatory system in Bacillus subtilis for the survival of severe secretion stress. Mol Microbiol 41 : 1159 1172.
34. Hyyrylainen, H.L., Sarvas, M. Kontinen, V.P. (2005) Transcriptome analysis of the secretion stress response of Bacillus subtilis. Appl Microbiol Biotechnol 67 : 389 396.
35. 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.
36. Jensen, S.O., Thompson, L.S. Harry, E.J. (2005) Cell division in Bacillus subtilis: FtsZ and FtsA association is Z-ring independent, and FtsA is required for efficient midcell Z-Ring assembly. J Bacteriol 187 : 6536 6544.
37. Jones, L.J., Carballido-Lopez, R. Errington, J. (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104 : 913 922.
38. Kalinowski, J., Bathe, B., Bartels, D., Bischoff, N., Bott, M., Burkovski, A., et al. (2003) The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol 104 : 5 25.
39. Kaltwasser, M., Wiegert, T. Schumann, W. (2002) Construction and application of epitope- and green fluorescent protein-tagging integration vectors for Bacillus subtilis. Appl Environ Microbiol 68 : 2624 2628.
40. Katis, V.L. Wake, R.G. (1999) Membrane-bound division proteins DivIB and DivIC of Bacillus subtilis function solely through their external domains in both vegetative and sporulation division. J Bacteriol 181 : 2710 2718.
41. Kawai, Y., Daniel, R.A. Errington, J. (2009) Regulation of cell wall morphogenesis in Bacillus subtilis by recruitment of PBP1 to the MreB helix. Mol Microbiol 71 : 1131 1144.
42. 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.
43. Kühlewein, A., Voll, G., Hernandez Alvarez, B., Kessler, H., Fischer, G., Rahfeld, J.U. Gemmecker, G. (2004) Solution structure of Escherichia coli Par10: The prototypic member of the Parvulin family of peptidyl-prolyl cis/trans isomerases. Protein Sci 13 : 2378 2387.
44. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390 : 249 256. (Pubitemid 27513299)
45. Leaver, M. Errington, J. (2005) Roles for MreC and MreD proteins in helical growth of the cylindrical cell wall in Bacillus subtilis. Mol Microbiol 57 : 1196 1209.
46. Letek, M., Ordonez, E., Vaquera, J., Margolin, W., Flardh, K., Mateos, L.M. Gil, J.A. (2008) DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J Bacteriol 190 : 3283 3292.
47. Lindholm, A., Ellmen, U., Tolonen-Martikainen, M. Palva, A. (2006) Heterologous protein secretion in Lactococcus lactis is enhanced by the Bacillus subtilis chaperone-like protein PrsA. Appl Microbiol Biotechnol 73 : 904 914.
48. Lu, K.P. Zhou, X.Z. (2007) The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 8 : 904 916.
49. Lu, K.P., Hanes, S.D. Hunter, T. (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380 : 544 547.
50. Lu, P.J., Zhou, X.Z., Shen, M. Lu, K.P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283 : 1325 1328.
51. Ma, Y., Bryant, A.E., Salmi, D.B., Hayes-Schroer, S.M., McIndoo, E., Aldape, M.J. Stevens, D.L. (2006) Identification and characterization of bicistronic speB and prsA gene expression in the group A Streptococcus. J Bacteriol 188 : 7626 7634.
52. McPherson, D.C., Driks, A. Popham, D.L. (2001) Two class A high-molecular-weight penicillin-binding proteins of Bacillus subtilis play redundant roles in sporulation. J Bacteriol 183 : 6046 6053.
53. Margot, P. Karamata, D. (1996) The wprA gene of Bacillus subtilis 168, expressed during exponential growth, encodes a cell-wall-assosciated protease. Microbiology 142 : 3437 3444.
54. Pedersen, L.B., Angert, E.R. Setlow, P. (1999) Septal localization of penicillin-binding protein 1 in Bacillus subtilis. J Bacteriol 181 : 3201 3211.
55. Pinho, M.G. Errington, J. (2003) Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol Microbiol 50 : 871 881.
56. Popham, D.L. Setlow, P. (1995) Cloning, nucleotide sequence, and mutagenesis of the Bacillus subtilis ponA operon, which codes for penicillin-binding protein (PBP) 1 and a PBP-related factor. J Bacteriol 177 : 326 335.
57. Popham, D.L. Setlow, P. (1996) Phenotypes of Bacillus subtilis mutants lacking multiple class a high-molecular-weight penicillin-binding proteins. J Bacteriol 178 : 2079 2085.
58. Popham, D.L. Young, K.D. (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr Opin Microbiol 6 : 594 599.
59. Popham, D.L., Helin, J., Costello, C.E. Setlow, P. (1996) Analysis of the peptidoglycan structure of Bacillus subtilis endospores. J Bacteriol 178 : 6451 6458.
60. 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.
61. Robson, S.A. King, G.F. (2006) Domain architecture and structure of the bacterial cell division protein DivIB. Proc Natl Acad Sci USA 103 : 6700 6705.
62. Rodgers, K.K., Bu, Z., Fleming, K.G., Schatz, D.G., Engelman, D.M. Coleman, J.E. (1996) A zinc-binding domain involved in the dimerization of RAG1. J Mol Biol 260 : 70 84.
63. Sauvage, E., Kerff, F., Terrak, M., Ayala, J.A. Charlier, P. (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32 : 234 258.
64. Scheffers, D.J., Jones, L.J. Errington, J. (2004) Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol Microbiol 51 : 749 764.
65. Schiene, C. Fischer, G. (2000) Enzymes that catalyse the restructuring of proteins. Curr Opin Struct Biol 10 : 40 45.
66. Soufo, H.J. Graumann, P.L. (2003) Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr Biol 13 : 1916 1920.
67. Spiess, C., Beil, A. Ehrmann, M. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97 : 339 347.
68. Stephenson, K. Harwood, C.R. (1998) Influence of a cell-wall-associated protease on production of α-amylase by Bacillus subtilis. Appl Environ Microbiol 64 : 2875 2881.
69. Stewart, G.C. (2005) Taking shape: control of bacterial cell wall biosynthesis. Mol Microbiol 57 : 1177 1181.
70. Stulke, J., Hanschke, R. Hecker, M. (1993) Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J Gen Microbiol 139 : 2041 2045.
71. Stymest, K.H. Klappa, P. (2008) The periplasmic peptidyl prolyl cis-trans isomerases PpiD and SurA have partially overlapping substrate specificities. FEBS J 275 : 3470 3479.
72. Tiyanont, K., Doan, T., Lazarus, M.B., Fang, X., Rudner, D.Z. Walker, S. (2006) Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. Proc Natl Acad Sci USA 103 : 11033 11038.
73. Uchida, T., Fujimori, F., Tradler, T., Fischer, G. Rahfeld, J.-U. (1999) Identification and characterization of a 14 kDa human protein as a novel parvulin like peptidyl-prolyl cis/trans isomerase. FEBS Lett 446 : 278 282.
74. 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.
75. Vitikainen, M., Lappalainen, I., Seppala, R., Antelmann, H., Boer, H., Taira, S., et al. (2004) Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J Biol Chem 279 : 19302 19314.
76. Vitikainen, M., Hyyrylainen, H.L., Kivimaki, A., Kontinen, V.P. Sarvas, M. (2005) Secretion of heterologous proteins in Bacillus subtilis can be improved by engineering cell components affecting post-translocational protein folding and degradation. J Appl Microbiol 99 : 363 375.
77. Wahlstrom, E., Vitikainen, M., Kontinen, V.P. Sarvas, M. (2003) The extracytoplasmic folding factor PrsA is required for protein secretion only in the presence of the cell wall in Bacillus subtilis. Microbiology 149 : 569 577.
78. Wang, P. Heitman, J. (2005) The cyclophilins. Genome Biol 6 : 226.
79. Wei, Y., Havasy, T., McPherson, D.C. Popham, D.L. (2003) Rod shape determination by the Bacillus subtilis class B penicillin-binding proteins encoded by pbpA and pbpH. J Bacteriol 185 : 4717 4726.
80. Williams, R.C., Rees, M.L., Jacobs, M.F., Pragai, Z., Thwaite, J.E., Baillie, L.W., et al. (2003) Production of Bacillus anthracis protective antigen is dependent on the extracellular chaperone, PrsA. J Biol Chem 278 : 18056 18062.
81. Wu, S.C., Ye, R., Wu, X.C., Ng, S.C. Wong, S.L. (1998) Enhanced secretory production of a single-chain antibody fragment from Bacillus subtilis by coproduction of molecular chaperones. J Bacteriol 180 : 2830 2835.
82. Wu, X., Wilcox, C.B., Devasahayam, G., Hackett, R.L., Arevalo-Rodriguez, M., Cardenas, M.E., et al. (2000) The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J 19 : 3727 3738.
83. Yaffe, M.B., Schutkowski, M., Shen, M., Zhou, X.Z., Stukenberg, P.T., Rahfeld, J.U., et al. (1997) Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278 : 1957 1960.
84. Yao, J.L., Kops, O., Lu, P.J. Lu, K.P. (2001) Functional conservation of phosphorylation-specific prolyl isomerases in plants. J Biol Chem 276 : 13517 13523.
85. Zemansky, J., Kline, B.C., Woodward, J.J., Leber, J.H., Marquis, H. Portnoy, D.A. (2009) Development of a mariner-based transposon and identification of Listeria monocytogenes determinants, including the peptidyl-prolyl isomerase PrsA2, that contribute to its hemolytic phenotype. J Bacteriol 191 : 3950 3964.
86. Zhao, G., Meier, T.I., Kahl, S.D., Gee, K.R. Blaszczak, L.C. (1999) BOCILLIN FL, a sensitive and commercially available reagent for detection of penicillin-binding proteins. Antimicrob Agents Chemother 43 : 1124 1128.