1887

Abstract

The growth and protein export defects (Ts) strains can be suppressed by the CsaA protein of . The present studies indicate that this effect can be attributed to chaperone-like activities of CsaA. First, CsaA stimulated protein export in , and mutant strains of . Second, CsaA suppressed the growth defects of , and mutants of . Third, and most importantly, CsaA exhibited chaperone-like properties by stimulating the reactivation of heat-denatured firefly luciferase in , , and mutant strains of , and by preventing the aggregation of heat-denatured luciferase . Thus, it seems that CsaA suppresses the growth and secretion defects of (Ts) strains either by improving the translocation competence of exported pre-proteins, thereby making them better substrates for mutant SecA proteins, or by stimulating the translocation activity of mutant SecA proteins.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-146-1-77
2000-01-01
2020-04-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/146/1/1460077a.html?itemId=/content/journal/micro/10.1099/00221287-146-1-77&mimeType=html&fmt=ahah

References

  1. Altman E., Kumamoto C. A., Emr S. D.. 1991; Heat-shock proteins can substitute for SecB function during protein export in Escherichia coli. EMBO J10:239–245
    [Google Scholar]
  2. Ang D., Chandrasekhar G. N., Zylicz M., Georgopoulos C.. 1986; Escherichia coli grpE gene codes for heat shock protein B25.3, essential for both lambda DNA replication at all temperatures and host growth at high temperature. J Bacteriol167:25–29
    [Google Scholar]
  3. den Blaauwen T., Driessen A. J. M.. 1996; Sec-dependent preprotein translocation in bacteria. Arch Microbiol165:1–8[CrossRef]
    [Google Scholar]
  4. Bolhuis A., Sorokin A., Azevedo V., Ehrlich S. D., Braun P. G., de Jong A., Venema G., Bron S., van Dijl J. M.. 1996; Bacillus subtilis can modulate its capacity and specificity for protein secretion through temporally controlled expression of the sipS gene for signal peptidase I. Mol Microbiol22:605–618[CrossRef]
    [Google Scholar]
  5. Bolhuis A., Broekhuizen C. P., Sorokin A., van Roosmalen M. L., Venema G., Bron S., Quax W. J., van Dijl J. M.. 1998; SecDF of Bacillus subtilis, a molecular Siamese twin required for the efficient secretion of proteins. J Biol Chem273:21217–21224[CrossRef]
    [Google Scholar]
  6. Bolivar F., Rodriguez R. L., Betlach M. C., Boyer H. W.. 1977; Construction and characterization of new cloning vehicles. I Ampicillin-resistant derivatives of the plasmid pMB9. Gene2:75–93[CrossRef]
    [Google Scholar]
  7. Brickman E. R., Oliver D. B., Garwin J. L., Kumamoto C. A., Beckwith J.. 1984; The use of extragenic suppressors to define genes involved in protein export in Escherichia coli. Mol Gen Genet196:24–27[CrossRef]
    [Google Scholar]
  8. de Cock H., Randall L. L.. 1998; Correlation between requirement for SecA during export and folding properties of precursor polypeptides. Mol Microbiol27:469–476[CrossRef]
    [Google Scholar]
  9. Dalbey R. E., Lively M. O., Bron S., van Dijl J. M.. 1997; The chemistry and enzymology of the type I signal peptidases. Protein Science6:1129–1138[CrossRef]
    [Google Scholar]
  10. Danese P. N., Murphy C. K., Silhavy T. J.. 1995; Multicopy suppression of cold-sensitive sec mutations in Escherichia coli. J Bacteriol177:4969–4973
    [Google Scholar]
  11. De Gier J. W., Valent Q. A., von Heijne G., Luirink J.. 1997; The E. coli SRP: preferences of a targeting factor. FEBS Lett408:1–4[CrossRef]
    [Google Scholar]
  12. van der Does C., Manting E. H., Kaufmann A., Lutz M., Driessen A. J. M.. 1998; Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state. Biochemistry37:201–210[CrossRef]
    [Google Scholar]
  13. van Dijl J. M., de Jong A., Smith H., Bron S., Venema G.. 1991; Signal peptidase I overproduction results in increased efficiencies of export and maturation of hybrid secretory proteins in Escherichia coli. Mol Gen Genet227:40–48[CrossRef]
    [Google Scholar]
  14. van Dijl J. M., de Jong A., Vehmaanperä J., Venema G., Bron S.. 1992; Signal peptidase I of Bacillus subtilis: patterns of conserved amino acids in prokaryotic and eukaryotic type I signal peptidases. EMBO J11:2819–2828
    [Google Scholar]
  15. Duong F., Eichler J., Price A., Leonard M. R., Wickner W.. 1997; Biogenesis of the Gram-negative bacterial envelope. Cell91:567–573[CrossRef]
    [Google Scholar]
  16. Economou A., Wickner W.. 1994; SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell78:835–843[CrossRef]
    [Google Scholar]
  17. Economou A., Pogliano J. A., Beckwith J., Oliver D. B., Wickner W.. 1995; SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell83:1171–1181[CrossRef]
    [Google Scholar]
  18. Fekkes P., Driessen A. J. M.. 1999; Protein targeting to the bacterial cytoplasmic membrane. Microbiol Mol Biol Rev63:161–173
    [Google Scholar]
  19. Fekkes P., van der Does C., Driessen A. J. M.. 1997; The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of the precursor protein translocation. EMBO J16:6105–6113[CrossRef]
    [Google Scholar]
  20. Georgopoulos C. P.. 1977; A new bacterial gene (groPC) which affects lambda DNA replication. Mol Gen Genet151:35–39[CrossRef]
    [Google Scholar]
  21. Gräfe S., Ellinger T., Malke H.. 1996; Structural dissection and functional analysis of the complex promoter of the streptokinase gene from Streptococcus equisimilis H46A. Med Microbiol Immunol185:11–17[CrossRef]
    [Google Scholar]
  22. Hartl F.-U., Lecker S., Schiebel E., Hendrick J. P., Wickner W.. 1990; The binding cascade of SecB to SecA to SecY/E mediates pre-protein targeting to the Escherichia coli plasma membrane. Cell63:269–279[CrossRef]
    [Google Scholar]
  23. von Heijne G.. 1990; The signal peptide. J Membrane Biol115:195–201[CrossRef]
    [Google Scholar]
  24. Hendrick J. P., Hartl F.-U.. 1993; Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem62:349–384[CrossRef]
    [Google Scholar]
  25. Hesterkamp T., Bukau B.. 1998; Role of the DnaK and HscA homologs of Hsp70 chaperones in protein folding in E. coli. EMBO J17:4818–4828[CrossRef]
    [Google Scholar]
  26. Honda K., Nakamura K., Nishiguchi M., Yamane K.. 1993; Cloning and characterization of a Bacillus subtilis gene encoding a homolog of the 54-kilodalton subunit of mammalian signal recognition particle and Escherichia coli Ffh. J Bacteriol17:4885–4894
    [Google Scholar]
  27. Ito K., Bassford P. Jr, Beckwith J.. 1981; Protein localization in E. coli: is there a common step in the secretion of periplasmic and outer membrane proteins?. Cell24:707–714[CrossRef]
    [Google Scholar]
  28. Jeong S. M., Yoshikawa H., Takahashi H.. 1993; Isolation and characterization of the secE homologue gene of Bacillus subtilis. Mol Microbiol10:133–142[CrossRef]
    [Google Scholar]
  29. Kim Y. J., Oliver D. B.. 1994; Escherichia coli SecY and SecE protein appear insufficient to constitute the SecA receptor. FEBS Lett339:175–180[CrossRef]
    [Google Scholar]
  30. Kumamoto C. A.. 1989; Escherichia coli SecB protein associates with exported protein precursors in vivo. Proc Natl Acad Sci USA86:5320–5324[CrossRef]
    [Google Scholar]
  31. Kumamoto C. A., Beckwith J.. 1985; Evidence for specificity at an early step in protein export in Escherichia coli. J Bacteriol163:267–274
    [Google Scholar]
  32. Kunst F., Ogasawara N., Moszer I..148 other authors 1997; The complete genome sequence of the Gram-positive bacterium. Bacillus subtilis. Nature390:249–256[CrossRef]
    [Google Scholar]
  33. Kusukawa N., Yura T., Ueguchi C., Akiyama Y., Ito K.. 1989; Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J8:3517–3521
    [Google Scholar]
  34. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685[CrossRef]
    [Google Scholar]
  35. Lee C. A., Beckwith J.. 1986; Suppression of growth and protein secretion defects in Escherichia coli secA mutants by decreasing protein synthesis. J Bacteriol166:878–883
    [Google Scholar]
  36. Luirink J., High S., Wood H., Giner A., Tollervey D., Dobberstein B.. 1992; Signal sequence recognition by an Escherichia coli ribonucleoprotein complex. Nature359:741–743[CrossRef]
    [Google Scholar]
  37. Mead D. A., Szczesna-Skorupa E., Kemper B.. 1986; Single-stranded DNA ‘blue’ T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Engng1:67–74[CrossRef]
    [Google Scholar]
  38. Meijer W. J., de Jong A., Bea G., Wisman A., Tjalsma H., Venema G., Bron S., van Dijl J. M.. 1995; The endogenous Bacillus subtilis (natto) plasmids pTA1015 and pTA1040 contain signal peptidase-encoding genes: identification of a new structural module on cryptic plasmids. Mol Microbiol17:621–631[CrossRef]
    [Google Scholar]
  39. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  40. Müller J.. 1996; Influence of impaired chaperone or secretion function on SecB production in Escherichia coli. J Bacteriol178:6097–6104
    [Google Scholar]
  41. Müller J., Walter F., van Dijl J. M., Behnke D.. 1992; Suppression of the growth and export defects of an Escherichia coli secA(Ts) mutant by a gene cloned from Bacillus subtilis. Mol Gen Genet235:89–96[CrossRef]
    [Google Scholar]
  42. Nakamura K., Nakamura A., Takamatsu H., Yoshikawa H., Yamane K.. 1990; Cloning and characterization of a Bacillus subtilis gene homologous to Escherichia coli secY. J Biochem107:603–607
    [Google Scholar]
  43. Närvänen A.. 1990; Synthetic peptides as probes for protein interactions and as antigenic epitopes PhD thesis University of Jyväskylä; Finland:
    [Google Scholar]
  44. Oliver D. B.. 1985; Identification of five new essential genes involved in the synthesis of a secreted protein in Escherichia coli. J Bacteriol161:285–291
    [Google Scholar]
  45. Oliver D. B., Beckwith J.. 1981; Escherichia coli mutant pleiotropically defective in the export of secreted proteins. Cell25:765–772[CrossRef]
    [Google Scholar]
  46. Oliver D. B., Beckwith J.. 1982; Regulation of a membrane component required for protein secretion in Escherichia coli. Cell330:311–319
    [Google Scholar]
  47. Overhoff B., Klein M., Spies M., Freudl R.. 1991; Identification of a gene fragment which codes for the amino-terminal 364 amino acid residues of a SecA homologue from Bacillus subtilis: further evidence for the conservation of the protein export apparatus in Gram-positive and Gram-negative bacteria. Mol Gen Genet228:417–423
    [Google Scholar]
  48. Overhoff-Freundlieb B., Freudl R.. 1991; Suppression of an Escherichia coli secAts mutant by a gene cloned from Staphylococcus carnosus. FEMS Microbiol Lett84:1143–1150
    [Google Scholar]
  49. Phillips G. J., Silhavy T. J.. 1992; The Escherichia coli ffh gene is necessary for viability and efficient protein export. Nature359:744–746[CrossRef]
    [Google Scholar]
  50. Pohlschröder M., Prinz W. A., Hartmann E., Beckwith J.. 1997; Protein translocation in the three domains of life: variations on a theme. Cell91:563–566[CrossRef]
    [Google Scholar]
  51. Polissi A., Goffin L., Georgopoulos C.. 1995; The Escherichia coli heat shock response and bacteriophage lambda development. FEMS Microbiol Rev17:159–169
    [Google Scholar]
  52. Pugsley A. P.. 1993; The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev57:50–108
    [Google Scholar]
  53. Sadaie Y., Takamatsu H., Nakamura K., Yamane K.. 1991; Sequencing reveals similarity of the wild-type div + gene of Bacillus subtilis to the Escherichia coli secA gene. Gene98:101–105[CrossRef]
    [Google Scholar]
  54. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  55. Schmidt A. M., Schiesswohl M., Völker U., Hecker M., Schumann W.. 1992; Cloning, sequencing, mapping, and transcriptional analysis of the groESL operon of Bacillus subtilis. J Bacteriol174:3993–3999
    [Google Scholar]
  56. Schmidt M. G., Oliver D. B.. 1989; SecA protein autogenously represses its own translation during normal protein secretion in Escherichia coli. J Bacteriol171:643–649
    [Google Scholar]
  57. Schröder H., Langer T., Hartl F.-U., Bukau B.. 1993; DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J12:4137–4144
    [Google Scholar]
  58. Seoh H. K., Tai P. C.. 1997; Carbon source-dependent synthesis of SecB, a cytosolic chaperone involved in protein translocation across Escherichia coli membranes. J Bacteriol179:1077–1081
    [Google Scholar]
  59. Seoh H. K., Tai P. C.. 1999; Catabolic repression of secB expression is positively controlled by cyclic AMP (cAMP) receptor protein-cAMP complexes at the transcriptional level. J Bacteriol181:1892–1899
    [Google Scholar]
  60. Skinner M. K., Griswold M. D.. 1983; Fluorographic detection of radioactivity in polyacrylamide gels with 2,5-diphenyloxazole in acetic acid and its comparison with existing procedures. Biochem J209:281–284
    [Google Scholar]
  61. Struck J. C. R., Vogel D. W., Ulbrich N., Erdmann V. A.. 1988; The Bacillus subtilis scRNA is related to the 4.5S RNA from Escherichia coli. Nucleic Acids Res16:2719[CrossRef]
    [Google Scholar]
  62. Suh J.-W., Boylan S. A., Thomas S. M., Dolan K. M., Oliver D. B., Price C. W.. 1990; Isolation of a secY homologue from Bacillus subtilis: evidence for a common protein export pathway in eubacteria. Mol Microbiol4:305–314[CrossRef]
    [Google Scholar]
  63. Sunshine M., Feiss M., Stuart J., Yochem J.. 1977; A new host gene (groPC) necessary for lambda DNA replication. Mol Gen Genet151:27–34[CrossRef]
    [Google Scholar]
  64. Tjalsma H., Noback M. A., Bron S., Venema G., Yamane K., van Dijl J. M.. 1997; Bacillus subtilis contains four closely related type I signal peptidases with overlapping substrate specificities. Constitutive and temporally controlled expression of different sip genes. J Biol Chem272:25983–25992[CrossRef]
    [Google Scholar]
  65. Tjalsma H., Bolhuis A., van Roosmalen M. L., Wiegert T., Schumann W., Broekhuizen C. P., Quax W. J., Venema G., Bron S., van Dijl J. M.. 1998; Functional analysis of the secretory precursor processing machinery of Bacillus subtilis: identification of a eubacterial homolog of archaeal and eukaryotic signal peptidases. Genes Dev12:2318–2331[CrossRef]
    [Google Scholar]
  66. Topping T. B., Randall L. L.. 1997; Chaperone SecB from Escherichia coli mediates kinetic partitioning via a dynamic equilibrium with its ligands. J Biol Chem272:19314–19318[CrossRef]
    [Google Scholar]
  67. Towbin H., Staehelin T., Gordon J.. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA76:4350–4354[CrossRef]
    [Google Scholar]
  68. Van Dyk T. K., Gatenby A. A., LaRossa R. A.. 1989; Demonstration by genetic suppression of interaction of GroE products with many proteins. Nature342:451–453[CrossRef]
    [Google Scholar]
  69. Wetzstein J., Völker U., Dedio J., Löbau S., Zuber U., Schiesswohl M., Herget C., Hecker M., Schumann W.. 1992; Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis. J Bacteriol174:3300–3310
    [Google Scholar]
  70. Wickner W., Driessen A. J. M., Hartl F.-U.. 1991; The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu Rev Biochem60:101–124[CrossRef]
    [Google Scholar]
  71. Wild J., Altman E., Yura T., Gross C. A.. 1992; DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev6:1165–1172[CrossRef]
    [Google Scholar]
  72. Wild J., Walter W. A., Gross C. A., Altman E.. 1993; Accumulation of secretory protein precursors in Escherichia coli induces the heat shock response. J Bacteriol175:3992–3997
    [Google Scholar]
  73. Wild J., Rossmeissl P., Walter W. A., Gross C. A.. 1996; Involvement of the DnaK-DnaJ-GrpE chaperone team in protein secretion in Escherichia coli. J Bacteriol178:3608–3616
    [Google Scholar]
  74. Wolin S. L.. 1994; From elephant to E. coli: SRP-dependent protein targeting. Cell77:787–790[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-146-1-77
Loading
/content/journal/micro/10.1099/00221287-146-1-77
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error