Roles of DegP in prevention of protein misfolding in the periplasm upon overexpression of penicillin acylase in Escherichia coli

Journal of Bacteriology

Volumn 185, Issue 10, 2003, Pages 3020-3030

  Pan, Kao Lu ^a   Hsiao, Hsu Chou ^a   Weng, Chiao Ling ^a   Wu, Ming Sheng ^a   Chou, C Perry ^a  

^a FENG CHIA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; PENICILLIN AMIDASE; PROTEIN DEGP; PROTEIN DEGQ; PROTEIN DEGS; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CELL DENSITY; CELL FUNCTION; CELL INCLUSION; CYTOPLASM; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE EXPRESSION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; TOXICITY;

ENZYME PRECURSORS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK PROTEINS; INCLUSION BODIES; PENICILLIN AMIDASE; PERIPLASM; PERIPLASMIC PROTEINS; PROTEIN FOLDING; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0038643369     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.10.3020-3030.2003     Document Type: Article

References (48)

1. E activity. Mol. Microbiol. 40:1323-1333.
2. Arie, J. P., N. Sassoon, and J. M. Betton. 2001. Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol. Microbiol. 39:199-210.
3. Betton, J. M., D. Boscus, D. Missiakas, S. Raina, and M. Hofnung. 1996. Probing the structural role of an alpha beta loop of maltose-binding protein by mutagenesis: heat shock induction by loop variants of the maltose-binding protein that form periplasmic inclusion bodies. J. Mol. Biol. 262:140-150.
4. Bowden, G. A., A. M. Paredes, and G. Georgiou. 1991. Structure and morphology of protein inclusion bodies in Escherichia coli. Bio/Technology 9:725-730.
5. Boyer, H. W., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
6. Chou, C. P., J.-H. Tseng, B.-Y. Kuo, K.-M. Lai, M.-I. Lin, and H.-K. Lin. 1999. Effect of SecB chaperone on production of periplasmic penicillin acylase in Escherichia coli. Biotechnol. Prog. 15:439-445.
7. Chou, C. P., C.-C. Yu, W.-J. Lin, B.-Y. Kuo, and W.-C. Wang. 1999. Novel strategy for efficient screening and construction of host/vector systems to overproduce penicillin acylase in Escherichia coli. Biotechnol. Bioeng. 65:219-226.
8. Chou, C. P., C.-C. Yu, J.-H. Tseng, M.-I. Lin, and H.-K. Lin. 1999. Genetic manipulation to identify limiting steps and develop strategies for high-level expression of penicillin acylase in Escherichia coli. Biotechnol. Bioeng. 63:263-272.
9. Connolly, L., A. De Las Penas, B. M. Alba, and C. A. Gross. 1997. The response to extracytoplasmic stress in Escherichia coli is controlled by partially overlapping pathways. Genes Dev. 11:2012-2021.
10. Guigueno, A., P. Belin, and P. Boquet. 1997. Defective export in Escherichia coli caused by DsbA′-PhoA hybrid proteins whose DsbA′ domain cannot fold into a conformation resistant to periplasmic proteases. J. Bacteriol. 179:3260-3269.
11. Hayhurst, A., and W. J. Harris. 1999. Escherichia coli Skp chaperone coexpression improves solubility and phage display of single-chain antibody fragments. Protein Express. Purif. 15:336-343.
12. E, is essential for bacterial growth at high temperature. J. Bacteriol. 177:2918-2922.
13. Kadokura, H., H. Kawasaki, K. Yoda, M. Yamasaki, and K. Kitamoto. 2001. Efficient export of alkaline phosphatase overexpressed from a multicopy plasmid requires degP, a gene encoding a periplasmic protease of Escherichia coli. J. Gen. Appl. Microbiol. 47:133-141.
14. Kane, J. F., and D. L. Hartley. 1988. Formation of recombinant protein inclusion bodies in Escherichia coli. Trends Biotechnol. 6:95-101.
15. Kasche, V., K. Lummer, A. Nurk, E. Piotraschke, A. Rieks, S. Stoeva, and W. Voelter. 1999. Intramolecular autoproteolysis initiates the maturation of penicillin amidase from Escherichia coli. Biochim. Biophys. Acta 1433:76-86.
16. Kim, K. I., S. C. Park, S. H. Kang, G. W. Cheong, and C. H. Chung. 1999. Selective degradation of unfolded proteins by the self-compartmentalizing HtrA protease, a periplasmic heat shock protein in Escherichia coli. J. Mol. Biol. 294:1363-1374.
17. Kolmar, H., P. R. Waller, and R. T. Sauer. 1996. The DegP and DegQ periplasmic endoproteases of Escherichia coli: specificity for cleavage sites and substrate conformation. J. Bacteriol. 178:5925-5929.
18. Krojer, T., M. Garrido-Franco, R. Huber, M. Ehrmann, and T. Clausen. 2002. Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416:455-459.
19. Laskowska, E., D. Kuczynska-Wisnik, J. Skorko-Glonek, and A. Taylor. 1996. Degradation by proteases Lon, Clp and HtrA, of Escherichia coli proteins aggregated in vivo by heat shock; HtrA protease action in vivo and in vitro. Mol. Microbiol. 22:555-571.
20. Lazar, S. W., and R. Kolter. 1996. SurA assists the folding of Escherichia coli outer membrane proteins. J. Bacteriol. 178:1770-1773.
21. Lin, W.-J., S.-W. Huang, and C. P. Chou. 2001. DegP coexpression minimizes inclusion body formation upon overproduction of recombinant penicillin acylase in Escherichia coli. Biotechnol. Bioeng. 73:484-492.
22. Lindsay, C. D., and R. H. Pain. 1990. The folding and solution conformation of penicillin G acylase. Eur. J. Biochem. 192:133-141.
23. Lindsay, C. D., and R. H. Pain. 1991. Refolding and assembly of penicillin acylase, an enzyme composed of two polypeptide chains that result from proteolytic activation. Biochemistry USA 30:9034-9040.
24. Makrides, S. C. 1996. Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol. Rev. 60:512-538.
25. Miller, C. G. 1996. Protein degradation and proteolytic modification, p. 938-954. In F. C. Neidhardt, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
26. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
27. S120A rescues the lethal phenotype of Escherichia coli OmpF assembly mutants in a degP background. J. Bacteriol. 182:4882-4888.
28. Missiakas, D., J.-M. Betton, and S. Raina. 1996. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol. Microbiol. 21:871-884.
29. Missiakas, D., and S. Raina. 1997. Protein misfolding in the cell envelope of Escherichia coli: new signaling pathways. Trends Biochem. Sci. 22:59-63.
30. Pallen, M. J., and B. W. Wren. 1997. The HtrA family of serine proteases. Mol. Microbiol. 26:209-221.
31. Perez-Perez, J., and J. Gutierrez. 1995. An arabinose-inducible expression vector, pAR3, compatible with ColE1-derived plasmids. Gene 158:141-142.
32. E and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2:159-165.
33. Rawlings, N., and A. Barrett. 1994. Families of serine peptidases. Methods Enzymol. 244:19-61.
34. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
35. Sawers, G., and M. Jarsch. 1996. Alternative regulation principles for the production of recombinant proteins in Escherichia coli. Appl. Microbiol. Biotechnol. 46:1-9.
36. Scherrer, S., N. Robas, H. Zouheiry, G. Branlant, and C. Branlant. 1994. Periplasmic aggregation limits the proteolytic maturation of the Escherichia coli penicillin G amidase precursor polypeptide. Appl. Microbiol. Biotechnol. 42:85-91.
37. Shewale, J. G., and H. Sivaraman. 1989. Penicillin acylase: enzyme production and its application in the manufacture of 6-APA. Process Biochem. 24:146-154.
38. Sizmann, D., C. Keilmann, and A. Bock. 1990. Primary structure requirements for the maturation in vivo of penicillin acylase from Escherichia coli ATCC 11105. Eur. J. Biochem. 192:143-151.
39. Skorko-Glonek, J., K. Krzewski, B. Lipinska, E. Bertoli, and F. Tanfani. 1995. Comparison of the structure of wild-type HtrA heat shock protease and mutant HtrA proteins. A Fourier transform infrared spectroscopic study J. Biol. Chem. 270:11140-11146. (Erratum, J. Biol. Chem. 270:31413.)
40. Skorko-Glonek, J., K. Krzewski, G. Zolese, E. Bertoli, and F. Tanfani. 1997. HtrA heat shock protease interacts with phospholipid membranes and undergoes conformational changes. J. Biol. Chem. 272:8974-8982.
41. Skorko-Glonek J., A. Wawrzynow, K. Krzewski, K. Kurpierz, and B. Lipinska. 1995. Site-directed mutagenesis of the HtrA (DegP) serine protease, whose proteolytic activity is indispensable for Escherichia coli survival at elevated temperatures. Gene 163:47-52.
42. Spiess, C., A. Beil, and M. Ehrmann. 1999. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339-347.
43. Sriubolmas, N., W. Panbangred, S. Sriurairatana, and V. Meevootisom. 1997. Localization and characterization of inclusion bodies in recombinant Escherichia coli cells overproducing penicillin G acylase. Appl. Microbiol. Biotechnol. 47:373-378.
44. Strandberg, L., and S.-O. Enfors. 1991. Factors influencing inclusion body formation in the production of a fused protein in Escherichia coli. Appl. Environ. Microbiol. 57:1669-1674.
45. Strauch, K. L., K. Johnson, and J. Beckwith. 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.
46. Thomas, J. G., A. Ayling, and F. Baneyx. 1997. Molecular chaperones, folding catalysts, and the recovery of active recombinant proteins from E. coli. Appl. Biochem. Biotechnol. 66:197-238.
47. Waller, P. R., and R. T. Sauer. 1996. Characterization of degQ and degS, Escherichia coli genes encoding homologs of the DegP protease. J. Bacteriol. 178:1146-1153.
48. Yee, L., and H. W. Blanch. 1992. Recombinant protein expression in high cell density fed-batch cultures of Escherichia coli. Bio/Technology 10:1550-1556.