Periplasmic quality control in biogenesis of outer membrane proteins

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 133-138

  Lyu, Zhi Xin ^a   Zhao, Xin Sheng ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

Chaperone; FRET; Outermembrane protein; Periplasm; Protease; Singlemolecule detection

Indexed keywords

DEGP PROTEIN; OUTER MEMBRANE PROTEIN; PERIPLASMIC PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN; SURA PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHAPERONE; DEGP PROTEASE; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; HEAT SHOCK PROTEIN; PEPTIDYLPROLYL ISOMERASE; SERINE PROTEINASE; SKP PROTEIN, E COLI; SURA PROTEIN, E COLI;

ARTICLE; BIOGENESIS; CYTOPLASM; ESCHERICHIA COLI; INNER MEMBRANE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; QUALITY CONTROL; BIOPHYSICS; BIOSYNTHESIS; CHEMISTRY; GENETICS; METABOLISM; PROTEIN FOLDING;

ESCHERICHIA COLI; NEGIBACTERIA;

BACTERIAL OUTER MEMBRANE PROTEINS; BIOPHYSICAL PROCESSES; CARRIER PROTEINS; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; PEPTIDYLPROLYL ISOMERASE; PERIPLASM; PERIPLASMIC PROTEINS; PROTEIN FOLDING; SERINE ENDOPEPTIDASES;

EID: 84934932603     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140217     Document Type: Article

References (37)

1. Fairman, J. W., Noinaj, N. and Buchanan, S. K. (2011) The structural biology of beta-barrel membrane proteins: a summary of recent reports. Curr. Opin. Struct. Biol. 21, 523-531
2. Driessen, A. J. and Nouwen, N. (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 77, 643-667
3. Ruiz, N., Kahne, D. and Silhavy, T. J. (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4, 57-66
4. Mogensen, J. E. and Otzen, D. E. (2005) Interactions between folding factors and bacterial outer membrane proteins. Mol. Microbiol. 57, 326-346
5. Chen, R. and Henning, U. (1996) A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol. Microbiol. 19, 1287-1294
6. Qu, J., Mayer, C., Behrens, S., Holst, O. and Kleinschmidt, J. H. (2007) The trimeric periplasmic chaperone Skp of Escherichia coli forms 1:1 complexes with outer membrane proteins via hydrophobic and electrostatic interactions. J. Mol. Biol. 374, 91-105
7. Korndorfer, I. P., Dommel, M. K. and Skerra, A. (2004) Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture. Nat. Struct. Mol. Biol. 11, 1015-1020
8. Walton, T. A., Sandoval, C. M., Fowler, C. A., Pardi, A. and Sousa, M. C. (2009) The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains. Proc. Nat. Acad. Sci. U. S. A. 106, 1772-1777
9. Harms, N., Koningstein, G., Dontje, W., Muller, M., Oudega, B., Luirink, J. and de Cock, H. (2001) The early interaction of the outer membrane protein PhoE with the periplasmic chaperone Skp occurs at the cytoplasmic membrane. J. Biol. Chem. 276, 18804-18811
10. Lyu, Z. X., Shao, Q., Gao, Y. Q. and Zhao, X. S. (2012) Direct observation of the uptake of outer membrane proteins by the periplasmic chaperone Skp. Plos ONE 7, e46068
11. Burmann, B. M., Wang, C. and Hiller, S. (2013) Conformation and dynamics of the periplasmic membrane-protein-chaperone complexes OmpX-Skp and tOmpA-Skp. Nat. Struct. Mol. Biol. 20, 1265-1272
12. Moon, C. P., Zaccai, N. R., Fleming, P. J., Gessmann, D. and Fleming, K. G. (2013) Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm. Proc. Nat. Acad. Sci. U. S. A. 110, 4285-4290
13. Sklar, J. G., Wu, T., Kahne, D. and Silhavy, T. J. (2007) Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Gene Dev. 21, 2473-2484
14. Rouviere, P. E. and Gross, C. A. (1996) SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Gene Dev. 10, 3170-3182
15. Behrens, S., Maier, R., de Cock, H., Schmid, F. X. and Gross, C. A. (2001) The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J. 20, 285-294
16. Bitto, E. and McKay, D. B. (2002) Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure 10, 1489-1498
17. Chai, Q., Ferrell, B., Zhong, M., Zhang, X., Ye, C. and Wei, Y. (2014) Diverse sequences are functional at the C-terminus of the E. coli periplasmic chaperone SurA. Protein Eng. Des. Sel. 27, 111-116
18. Bitto, E. and McKay, D. B. (2003) The periplasmic molecular chaperone protein SurA binds a peptide motif that is characteristic of integral outer membrane proteins. J. Biol. Chem. 278, 49316-49322
19. Xu, X., Wang, S., Hu, Y. X. and McKay, D. B. (2007) The periplasmic bacterial molecular chaperone SurA adapts its structure to bind peptides in different conformations to assert a sequence preference for aromatic residues. J. Mol. Biol. 373, 367-381
20. Ureta, A. R., Endres, R. G., Wingreen, N. S. and Silhavy, T. J. (2007) Kinetic analysis of the assembly of the outer membrane protein LamB in Escherichia coli mutants each lacking a secretion or targeting factor in a different cellular compartment. J. Bacteriol. 189, 446-454
21. Spiess, C., Beil, A. and Ehrmann, M. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97, 339-347
22. Clausen, T., Southan, C. and Ehrmann, M. (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol. Cell 10, 443-455
23. Clausen, T., Kaiser, M., Huber, R. and Ehrmann, M. (2011) HTRA proteases: regulated proteolysis in protein quality control. Nat. Rev. Mol. Cell Biol. 12, 152-162
24. Ge, X., Wang, R., Ma, J., Liu, Y., Ezemaduka, A. N., Chen, P. R., Fu, X. and Chang, Z. (2014) DegP primarily functions as a protease for the biogenesis of beta-barrel outer membrane proteins in the Gram-negative bacterium Escherichia coli. FEBS J. 281, 1226-1240
25. Rizzitello, A. E., Harper, J. R. and Silhavy, T. J. (2001) Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J. Bacteriol. 183, 6794-6800
26. Jiang, J., Zhang, X., Chen, Y., Wu, Y., Zhou, Z. H., Chang, Z. and Sui, S. F. (2008) Activation of DegP chaperone-protease via formation of large cage-like oligomers upon binding to substrate proteins. Proc. Nat. Acad. Sci. U. S. A. 105, 11939-11944
27. Krojer, T., Garrido-Franco, M., Huber, R., Ehrmann, M. and Clausen, T. (2002) Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416, 455-459
28. Shen, Q. T., Bai, X. C., Chang, L. F., Wu, Y., Wang, H. W. and Sui, S. F. (2009) Bowl-shaped oligomeric structures on membranes as DegP's new functional forms in protein quality control. Proc. Nat. Acad. Sci. U. S. A. 106, 4858-4863
29. Thompson, N. J., Merdanovic, M., Ehrmann, M., van Duijn, E. and Heck, A. J. (2014) Substrate occupancy at the onset of oligomeric transitions of DegP. Structure 22, 281-290
30. Kim, S. and Sauer, R. T. (2012) Cage assembly of DegP protease is not required for substrate-dependent regulation of proteolytic activity or high-temperature cell survival. Proc. Nat. Acad. Sci. U. S. A. 109, 7263-7268
31. Kim, S. and Sauer, R. T. (2014) Distinct regulatory mechanisms balance DegP proteolysis to maintain cellular fitness during heat stress. Gene Dev. 28, 902-911
32. Krojer, T., Sawa, J., Schafer, E., Saibil, H. R., Ehrmann, M. and Clausen, T. (2008) Structural basis for the regulated protease and chaperone function of DegP. Nature 453, 885-890
33. Wu, S., Ge, X., Lv, Z., Zhi, Z., Chang, Z. and Zhao, X. S. (2011) Interaction between bacterial outer membrane proteins and periplasmic quality control factors: a kinetic partitioning mechanism. Biochem. J. 438, 505-511
34. Strauch, K. L., Johnson, K. and Beckwith, J. (1989) Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J. Bacteriol. 171, 2689-2696 PubMed
35. Walther, D. M., Rapaport, D. and Tommassen, J. (2009) Biogenesis of beta-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell. Mol. Life Sci. 66, 2789-2804
36. Pavlova, O., Peterson, J. H., Ieva, R. and Bernstein, H. D. (2013) Mechanistic link between beta barrel assembly and the initiation of autotransporter secretion. Proc. Nat. Acad. Sci. U. S. A. 110, 938-947
37. Merdanovic, M., Clausen, T., Kaiser, M., Huber, R. and Ehrmann, M. (2011) Protein quality control in the bacterial periplasm. Annu. Rev. Microbiol. 65, 149-168