Article thumbnail
Location of Repository

Protein quality control in the bacterial periplasm

By Marika Miot and Jean-Michel Betton


The proper functioning of extracytoplasmic proteins requires their export to, and productive folding in, the correct cellular compartment. All proteins in Escherichia coli are initially synthesized in the cytoplasm, then follow a pathway that depends upon their ultimate cellular destination. Many proteins destined for the periplasm are synthesized as precursors carrying an N-terminal signal sequence that directs them to the general secretion machinery at the inner membrane. After translocation and signal sequence cleavage, the newly exported mature proteins are folded and assembled in the periplasm. Maintaining quality control over these processes depends on chaperones, folding catalysts, and proteases. This article summarizes the general principles which control protein folding in the bacterial periplasm by focusing on the periplasmic maltose-binding protein

Topics: Review
Publisher: BioMed Central
Year: 2004
DOI identifier: 10.1186/1475-2859-3-4
OAI identifier:
Provided by: PubMed Central

Suggested articles


  1. (1998). A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli.
  2. (1999). A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell
  3. (2002). A: Construction and deconstruction of bacterial inclusion bodies.
  4. (1999). A: Proteolytic digestion of bacterial inclusion body proteins during dynamic transition between soluble and insoluble forms. Biochim Biophys Acta
  5. (1982). Active transport of maltose in Escherichia coli K12.
  6. An in vivo pathway for disulfide bond isomerization in Escherichia coli.
  7. (2002). CA: DegS and Yael participate sequentially in the cleavage of RseA to activate the σE-dependent extracytoplasmic stress response. Gene Dev
  8. (1992). CA: DnaK and DnaJ heat-shock proteins participate in protein export in Escherichia coli. Gene Dev
  9. (1995). CA: rpoE, the gene encoding the secon heat-shock sigma factor, σE, in Escherichia coli.
  10. (1996). CA: SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev
  11. (1999). CA: The Escherichia coli σE-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Gene Dev
  12. (2001). CA: The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity.
  13. (1997). CA: The σE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σE. Mol Microbiol
  14. (1997). Caldas TD: Chaperone properties of the bacterial periplasmic substrate-binding proteins.
  15. (1999). CC: Chaperone activity of DsbC.
  16. (1989). Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature.
  17. (2001). Characterization of the Escherichia coli sigma E regulon.
  18. (1999). Chung CH: Selective degradation of unfolded proteins by the self-compartmentalizing HtrA protease, a periplasmic heat shock protein in Escherichia coli.
  19. (1990). CT: Peptidyl-prolyl cis-trans isomerase from Escherichia coli: a periplasmic homolog of cyclophilin that is not inhibited by cyclosporin A. P r o c N a t l A c a d S c i U S A
  20. (1998). Degradation versus aggregation of misfolded maltose-binding protein in the periplasm of Escherichia coli.
  21. (1997). Dowhan W: The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine.
  22. (2000). DsbG, a protein disulfide isomerase with chaperone activity.
  23. (1995). Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides.
  24. (1993). ECC: The deduced aminoacid sequence of the cloned cpxR gene suggests the protein is the cognate regulator for the membrane sensor, CpxA, in a two-component signal transduction system of Escherichia coli. Gene
  25. (2001). EcfE, a new essential inner membrane protease: its role in the regulation of heat shock response in Escherichia coli.
  26. (1998). ES: Environmental regulation of Salmonella typhi invasion-defective mutants. Infect Immun
  27. (1996). Escherichia coli trigger factor is a prolyl isomerase that associates with nascent polypeptide chains.
  28. (1990). Export of the periplasmic maltose-binding protein of Escherichia coli.
  29. (2002). Folding and aggregation of export-defective mutants of the maltose-binding protein. Res Microbiol
  30. (2003). Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci USA
  31. (1998). FX: Prolyl isomerase do not catalyse isomerization of non-prolyl peptide bonds. Biol Chem
  32. (2004). GA: Structural and functional studies of FkpA from Escherichia coli, a cis/trans peptidyl-prolyl isomerase with chaperone activity.
  33. (1990). Genetic analysis of protein export in Escherichia coli. Ann Rev Genet
  34. (1985). Goldberg AL: Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes. Cell
  35. (1989). Gross CA: Identification of the σE subunit of Escherichia coli RNA polymerase: a second alternate σ factor involved in high-temperature gene expression. Genes Dev
  36. (1996). Hofnung M: Folding of a mutant maltose binding protein of E. coli which forms inclusion bodies.
  37. (1980). Hofnung M: Mutations which alter the function of the signal sequence of the maltose binding protein of Escherichia coli.
  38. (1988). Hofnung M: Two regions of mature periplasmic maltose-binding protein of Escherichia coli involved in secretion.
  39. (1985). Host cell-plasmid interactions in the expression of DNA donor activity by F+ strains of Escherichia coli K-12. Bioessays
  40. (1995). Involvement of cpxA, a sensor of a two-component regulatory system, in the pH-dependent regulation of expression of Shigella sonnei virF gene.
  41. (1999). Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation.
  42. (1989). Ito Y: Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli.
  43. (2001). J-M: Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol Microbiol
  44. (2003). J-M: Crystal structure of a defective folding protein. Protein Sci
  45. (1998). J-M: Tertiary structuredependence of misfolding substitutions in loops of the maltose-binding protein. Protein Sci
  46. (1995). KD: Escherichia coli and other species of the Enterobacteriaceae encode a protein similar to the Mip-like FK506-binding protein. Arch Microbiol
  47. (2003). Ligand crowding at a nascent signal sequence.
  48. (1993). LL: Folding of maltosebinding protein.
  49. (1998). Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev
  50. (1994). Mammalian and Escherichia coli signal recognition particles. Mol Microbiol
  51. (2002). McKay DB: Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure
  52. (1997). Modular structure of the trigger factor required for high activity in ptotein folding.
  53. (1997). Modulation of the Escherichia coli σE(RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol Microbiol
  54. (1999). Oxidative protein folding is driven by the electron transport system. Cell
  55. (2000). P: Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nature Struct Biol
  56. (1988). PM: The Cpx proteins of Escherichia coli K 12: structure of the CpxA polypeptide as an inner membrane component.
  57. (1999). Posttranslational quality control: folding, refolding, and degrading proteins. Science
  58. (1996). Probing the structural role of an αβ loop of maltose-binding protein by mutagenesis: heat-shock induction by loop variants of the maltose-binding protein that form periplasmic inclusion bodies.
  59. (2003). Protein disulfide bond formation in prokaryotes. Annu Rev Biochem
  60. (2001). Protein solubility and folding monitored in vivo by structural complementation of a genetic marker protein. Nat Biotechnol
  61. (1991). Quiocho FA: The 2.3-Å resolution structure of the maltose-or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis.
  62. (1997). Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev
  63. (1993). Regulation of the Escherichia coli heat-shock response. Mol Microbiol
  64. (2000). RseB binding to the periplasmic domain of RseA modulates the RseA: sigmaE interaction in the cytoplasm and the availability of sigmaE.RNA polymerase.
  65. (2003). RT: OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell
  66. (1996). S: New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol
  67. (1998). Satoh T: Isolation of a periplasmic molecular chaperone-like protein of Rhodobacter sphaeroides f. sp. denitrificans that is homologous to the dipeptide transport protein DppA of Escherichia coli.
  68. (1990). SecB protein: a cytosolic export factor that associates with nascent exported proteins.
  69. (2003). Signal recognition particule (SRP)-mediated targeting and Sec-dependent translocation of extracellular Escherichia coli protein.
  70. (1987). Silent and functional changes in the periplasmic maltose-binding protein of Escherichia coli K12.
  71. (1995). Silhavy TJ: Overproduction of NlpE, a new membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway.
  72. (2001). Silhavy TJ: Periplasmic stress and ECF sigma factors. Annu Rev Microbiol
  73. (2002). Silhavy TJ: Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway.
  74. (1998). Silhavy TJ: Targeting and assembly of periplasmic and outer-membrane proteins in Escherichia coli. Annu Rev Genet
  75. (2000). Silhavy TJ: Tethering of CpxP to the inner membrane prevents spheroplast induction of the Cpx envelope stress response. Mol Microbiol
  76. (1999). Silhavy TJ: The Cpx envelope stress response is controlled by amplification and feedback inhibition.
  77. (1995). Silhavy TJ: The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stressinducible periplasmic protease, DegP. Genes Dev
  78. (1999). Silhavy TJ: The sigmaE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr Opin Microbiol
  79. (1997). Silhavy TJ: The σE and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev
  80. (1986). SJ: Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose-binding protein in E. coli. Cell
  81. (2001). SJ: Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili.
  82. (1995). SJ: High selectivity with low specificity: how SecB has solved the paradox of chaperone binding. Trends Biochem Sci
  83. (2000). SJ: PapD-like chaperones provide the missing information for folding of pilin proteins. Proc Natl Acad Sci USA
  84. (1997). SJ: The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems.
  85. (1999). Skp, a molecular chaperone of gram-negative bacteria is required for the formation of soluble periplasmic intermediates of outer membrane proteins.
  86. (2004). Snapshots of DsbA in action: detection of proteins in the process of oxidative folding. Science
  87. (1998). Strynadka NCJ: Crystal structure of a bacterial signal peptidase in complex with a β-lactam inhibitor. Nature
  88. (2002). T: Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature
  89. (2004). TA: X-ray structure of a protein-conducting channel. Nature
  90. (1995). Tanfani F: Comparaison of the structure of wild-type HtrA heat shock protease and mutant HtrA proteins.
  91. (1996). Targeting of signal sequenceless proteins for export in Escherichia coli with altered protein translocase.
  92. (2003). Temperature effect on inclusion body formation and stress response in the periplasm of Escherichia coli. Mol Microbiol
  93. (1993). The complete general secretory pathway in Gram-Negative bacteria. Microbiol Rev
  94. (2003). The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway.
  95. (1990). The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an endopeptidase.
  96. (2002). The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell
  97. (1995). The rpoE gene encoding the σE (σ24) heat shock sigma factor of Escherichia coli.
  98. (1994). Wickner W: SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.