Optimization of the inefficient translation initiation region of the cpxP gene from Escherichia coli

Protein Science

Volumn 16, Issue 11, 2007, Pages 2445-2453

  Miot, Marika ^a   Betton, Jean Michel ^a  

^a CNRS   (France)

Author keywords

Periplasm; Protein production; Signal sequence; Stress response; Synonymous codon

Indexed keywords

MESSENGER RNA;

ARTICLE; BACTERIAL GENE; CPXP GENE; CYTOPLASM; ESCHERICHIA COLI; GENE MUTATION; GENE SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; SIGNAL TRANSDUCTION; STRESS;

BASE SEQUENCE; CODON; CYTOPLASM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDES; PERIPLASM; PERIPLASMIC BINDING PROTEINS; PROTEIN DISULFIDE-ISOMERASE; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI;

EID: 35648955713     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.073047807     Document Type: Article

References (38)

1. Alba, B.M. and Gross, C.A. 2004. Regulation of the Escherichia coli δ-dependent envelope stress response. Mol. Microbiol. 52: 613-619.
2. Betton, J.M. 2004. High-throughput cloning and expression strategies for protein production. Biochimie 86: 601-605.
3. Betton, J.M., Boscus, D., Missiakas, D., Raina, S., and Hofnung, M. 1996. Probing the structural role of an ab 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. Buelow, D.R. and Raivio, T.L. 2005. Cpx signal transduction is influenced by a conserved N-terminal domain in the novel inhibitor CpxP and the periplasmic protease DegP. J. Bacteriol. 187: 6622-6630.
5. Burns, D.M. and Beacham, I.R. 1985. Rare codons in E. coli and S. typhimurium signal sequences. FEBS Lett. 189: 318-324.
6. Danese, P.N. and Silhavy, T.J. 1997. The δ(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes & Dev. 11: 1183-1193.
7. Danese, P.N. and Silhavy, T.J. 1998. CpxP, a stress-combative member of the Cpx regulon. J. Bacteriol. 180: 831-839.
8. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J., and Silhavy, T.J. 1995. The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes & Dev. 9: 387-398.
9. Danese, P.N., Oliver, G.R., Barr, K., Bowman, G.D., Rick, P.D., and Silhavy, T.J. 1998. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J. Bacteriol. 180: 5875-5884.
10. Dartigalongue, C. and Raina, S. 1998. A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 17: 3968-3980.
11. de Smit, M.H. and van Duin, J. 1990. Control of prokaryotic translational initiation by mRNA secondary structure. Prog. Nucleic Acid Res. Mol. Biol. 38: 1-35.
12. De Wulf, P., McGuire, A.M., Liu, X., and Lin, E.C. 2002. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J. Biol. Chem. 277: 26652-26661.
13. DiGiuseppe, P.A. and Silhavy, T.J. 2003. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185: 2432-2440.
14. Dong, J., Iuchi, S., Kwan, H.S., Lu, Z., and Lin, E.C. 1993. The deduced amino-acid 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 136: 227-230.
15. Duguay, A.R. and Silhavy, T.J. 2004. Quality control in the bacterial periplasm. Biochim. Biophys. Acta 1694: 121-134.
16. Fleischer, R., Heermann, R., Jung, K., and Hunke, S. 2007. Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J. Biol. Chem. 282: 8583-8593.
17. Hung, D.L., Raivio, T.L., Jones, C.H., Silhavy, T.J., and Hultgren, S.J. 2001. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20: 1508-1518.
18. Hunke, S. and Betton, J.M. 2003. Temperature effect on inclusion body formation and stress response in the periplasm of Escherichia coli. Mol. Microbiol. 50: 1579-1589.
19. Isaac, D.D., Pinkner, J.S., Hultgren, S.J., and Silhavy, T.J. 2005. The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. Proc. Natl. Acad. Sci. 102: 17775-17779.
20. Kuipers, O.P., Beerthuyzen, M.M., Siezen, R.J., and De Vos, W.M. 1993. Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Requirement of expression of the nisA and nisI genes for development of immunity. Eur. J. Biochem. 216: 281-291.
21. Livak, K.J. and Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25: 402-408.
22. Miller, J. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
23. Missiakas, D. and Raina, S. 1997. Protein folding in the bacterial periplasm. J. Bacteriol. 179: 2465-2471.
24. Mogensen, J.E. and Otzen, D.E. 2005. Interactions between folding factors and bacterial outer membrane proteins. Mol. Microbiol. 57: 326-346.
25. Morita, M.T., Tanaka, Y., Kodama, T.S., Kyogoku, Y., Yanagi, H., and Yura, T. 1999. Translational induction of heat shock transcription factor s32: Evidence for a built-in RNA thermosensor. Genes & Dev. 13: 655-665.
26. Nakayama, S. and Watanabe, H. 1995. Involvement of cpxA, a sensor of a two-component regulatory system, in the pH-dependent regulation of expression of Shigella sonnei virF gene. J. Bacteriol. 177: 5062-5069.
27. Pogliano, J., Lynch, A.S., Belin, D., Lin, E.C., and Beckwith, J. 1997. Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes & Dev. 11: 1169-1182.
28. Raivio, T.L. and Silhavy, T.J. 1999. The sE and Cpx regulatory pathways: Overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2: 159-165.
29. Raivio, T.L. and Silhavy, T.J. 2001. Periplasmic stress and ECF δ factors. Annu. Rev. Microbiol. 55: 591-624.
30. Schierle, C.F., Berkmen, M., Huber, D., Kumamoto, C., Boyd, D., and Beckwith, J. 2003. The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway. J. Bacteriol. 185: 5706-5713.
31. Serruto, D. and Galeotti, C.L. 2004. The signal peptide sequence of a lytic transglycosylase of Neisseria meningitidis is involved in regulation of gene expression. Microbiol. 150: 1427-1437.
32. Sharp, P.M. and Li, W.H. 1987. The codon Adaptation Index - A measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15: 1281-1295.
33. Snyder, W.B., Davis, L.J., Danese, P.N., Cosma, C.L., and Silhavy, T.J. 1995. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J. Bacteriol. 177: 4216-4223.
34. Voges, D., Watzele, M., Nemetz, C., Wizemann, S., and Buchberger, B. 2004. Analyzing and enhancing mRNA translational efficiency in an Escherichia coli in vitro expression system. Biochem. Biophys. Res. Commun. 318: 601-614.
35. Walsh, N.P., Alba, B.M., Bose, B., Gross, C.A., and Sauer, R.T. 2003. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113: 61-71.
36. Weber, R.F. and Silverman, P.M. 1988. The cpx proteins of Escherichia coli K12. Structure of the cpxA polypeptide as an inner membrane component. J. Mol. Biol. 203: 467-478.
37. Zalucki, Y.M. and Jennings, M.P. 2007. Experimental confirmation of a key role for nonoptimal codons in protein export. Biochem. Biophys. Res. Commun. 355: 143-148.
38. Zuker, M. 1989. On finding all suboptimal foldings of an RNA molecule. Science 244: 48-52.