A little help from my friends: Quality control of presecretory proteins in bacteria

Journal of Bacteriology

Volumn 186, Issue 22, 2004, Pages 7467-7473

  Fisher, Adam C ^a   Delisa, Matthew P ^a,b  

^a Cornell University ^*  (United States)

^b School of Operations Research and Industrial Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BACTERIAL PROTEIN; CHAPERONE; PORTEIN TAT; PROTEIN SEC; SECRETORY PROTEIN; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

CELL MEMBRANE; CROSS LINKING; CYTOSOL; EXTRACELLULAR SPACE; HYDROPHOBICITY; LIPID MEMBRANE; MEMBRANE TRANSPORT; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; QUALITY CONTROL; SHORT SURVEY; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATASES; BACTERIA; BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; INTRACELLULAR MEMBRANES; MEMBRANE TRANSPORT PROTEINS; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS);

EID: 7744227965     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.22.7467-7473.2004     Document Type: Short Survey

References (82)

1. Alami, M., I. Luke, S. Deitermann, G. Eisner, H. G. Koch, J. Brunner, and M. Muller. 2003. Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell 12:937-946.
2. Arkowitz, R. A., J. C. Joly, and W. Wickner. 1993. Translocation can drive the unfolding of a preprotein domain. EMBO J. 12:243-253.
3. Berks, B. C. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22:393-404.
4. Berks, B. C., F. Sargent, and T. Palmer. 2000. The Tat protein export pathway. Mol. Microbiol. 35:260-274.
5. Blaudeck, N., P. Kreutzenbeck, R. Freudl, and G. A. Sprenger. 2003. Genetic analysis of pathway specificity during posttranslational protein translocation across the Escherichia coli plasma membrane. J. Bacteriol. 185:2811-2819.
6. Bochkareva, E. S., M. E. Solovieva, and A. S. Girshovich. 1998. Targeting of GroEL to SecA on the cytoplasmic membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA 95:478-483.
7. Brundage, L., J. P. Hendrick, E. Schiebel, A. J. Driessen, and W. Wickner. 1990. The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 62:649-657.
8. Bruser, T., and C. Sanders. 2003. An alternative model of the twin arginine translocation system, Microbiol. Res. 158:7-17.
9. Bruser, T., H. G. Truper, and C. Dahl. 1997. Cloning and sequencing of the gene encoding the high potential iron-sulfur protein (HiPIP) from the purple sulfur bacterium Chromatium vinosum. Biochim. Biophys. Acta 1352:18-22.
10. Buskiewicz, I., E. Deuerling, S. Q. Gu, J. Jockel, M. V. Rodnina, B. Bukau, and W. Wintermeyer. 2004. Trigger factor binds to ribosome-signal- recognition particle (SRP) complexes and is excluded by binding of the SRP receptor. Proc. Natl. Acad. Sci. USA 101:7902-7906.
11. Chanal, A., C. Santini, and L. Wu. 1998. Potential receptor function of three homologous components, TatA, TatB and TatE, of the twin-arginine signal sequence-dependent metalloenzyme translocation pathway in Escherichia coli. Mol. Microbiol. 30:674-676.
12. 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.
13. Clark, S. A., and S. M. Theg. 1997. A folded protein can be transported across the chloroplast envelope and thylakoid membranes. Mol. Biol. Cell 8:923-934.
14. Collier, D. N., V. A. Bankaitis, J. B. Weiss, and P. J. Bassford, Jr. 1988. The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell 53:273-283.
15. Cristobal, S., J. W. de Gier, H. Nielsen, and G. von Heijne. 1999. Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J. 18:2982-2990.
16. Crooke, E., L. Brundage, M. Rice, and W. Wickner. 1988. ProOmpA spontaneously folds in a membrane assembly competent state which trigger factor stabilizes. EMBO J. 7:1831-1835.
17. Crooke, E., B. Guthrie, S. Lecker, R. Lill, and W. Wickner. 1988. ProOmpA is stabilized for membrane translocation by either purified E. coli trigger factor or canine signal recognition particle. Cell 54:1003-1011.
18. Crooke, E., and W. Wickner. 1987. Trigger factor: a soluble protein that folds pro-OmpA into a membrane-assembly-competent form. Proc. Natl. Acad. Sci. USA 84:5216-5220.
19. Danese, P. N., and T. J. Silhavy. 1998. Targeting and assembly of periplasmic and outer-membrane proteins in Escherichia coli. Annu. Rev. Genet. 32:59-94.
20. Delepelaire, P., and C. Wandersman. 1998. The SecB chaperone is involved in the secretion of the Serratia marcescens HasA protein through an ABC transporter. EMBO J. 17:936-944.
21. DeLisa, M. P., P. Lee, T. Palmer, and G. Georgiou. 2004. Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J. Bacteriol. 186:366-373.
22. DeLisa, M. P., D. Tullman, and G. Georgiou. 2003. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc. Natl. Acad. Sci. USA 100:6115-6120.
23. Derman, A. I., J. W. Puziss, P. J. Bassford, Jr., and J. Beckwith. 1993. A signal sequence is not required for protein export in prlA mutants of Escherichia coli. EMBO J. 12:879-888.
24. Dilks, K., R. W. Rose, E. Hartmann, and M. Pohlschroder. 2003. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J. Bacteriol. 185:1478-1483.
25. Duong, F., and W. Wickner. 1999. The PrlA and PrlG phenotypes are caused by a loosened association among the translocase SecYEG subunits. EMBO J. 18:3263-3270.
26. Economou, A., and W. Wickner. 1994. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78:835-843.
27. Eser, M., and M. Ehrmann. 2003. SecA-dependent quality control of intracellular protein localization. Proc. Natl. Acad. Sci. USA 100:13231-13234.
28. Fekkes, P., and A. J. Driessen. 1999. Protein targeting to the bacterial cytoplasmic membrane. Microbiol. Mol. Biol. Rev. 63:161-173.
29. Fekkes, P., C. van der Does, and A. J. Driessen. 1997. The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J. 16:6105-6113.
30. Flower, A. M., R. C. Doebele, and T. J. Silhavy. 1994. PrlA and PrlG suppressors reduce the requirement for signal sequence recognition. J. Bacteriol. 176:5607-5614.
31. Galan, J. E., and A. Collmer. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322-1328.
32. Guthrie, B., and W. Wickner. 1990. Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J. Bacteriol. 172:5555-5562.
33. Halbig, D., T. Wiegert, N. Blaudeck, R. Freudl, and G. A. Sprenger. 1999. The efficient export of NADP-containing glucose-fructose oxidoreductase to the periplasm of Zymomonas mobilis depends both on an intact twin-arginine motif in the signal peptide and on the generation of a structural export signal induced by cofactor binding. Eur. J. Biochem. 263:543-551.
34. Henry, R., M. Carrigan, M. McCaffrey, X. Ma, and K. Cline. 1997. Targeting determinants and proposed evolutionary basis for the Sec and the Delta pH protein transport systems in chloroplast thylakoid membranes. J. Cell Biol. 136:823-832.
35. Hynds, P. J., D. Robinson, and C. Robinson. 1998. The sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane. J. Biol. Chem. 273:34868-34874.
36. Jormakka, M., S. Tornroth, B. Byrne, and S. Iwata. 2002. Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295:1863-1868.
37. Kebir, M. O., and D. A. Kendall. 2002. SecA specificity for different signal peptides. Biochemistry 41:5573-5580.
38. Kipping, M., H. Lilie, U. Lindenstrauss, J. R. Andreesen, C. Griesinger, T. Carlomagno, and T. Bruser. 2003. Structural studies on a twin-arginine signal sequence. FEBS Lett. 550:18-22.
39. Knoblauch, N. T., S. Rudiger, H. J. Schonfeld, A. J. Driessen, J. Schneider-Mergener, and B. Bukau. 1999. Substrate specificity of the SecB chaperone. J. Biol. Chem. 274:34219-34225.
40. Kowarik, M., S. Kung, B. Martoglio, and A. Helenius. 2002. Protein folding during cotranslational translocation in the endoplasmic reticulum. Mol. Cell 10:769-778.
41. Kumamoto, C. A. 1989. Escherichia coli SecB protein associates with exported protein precursors in vivo. Proc. Natl. Acad. Sci. USA 86:5320-5324.
42. Kumamoto, C. A., and J. Beckwith. 1983. Mutations in a new gene, secB, cause defective protein localization in Escherichia coli. J. Bacteriol. 154:253-260.
43. Kusukawa, N., T. Yura, C. Ueguchi, Y. Akiyama, and K. Ito. 1989. Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J. 8:3517-3521.
44. Lecker, S., R. Lill, T. Ziegelhoffer, C. Georgopoulos, P. J. Bassford, Jr., C. A. Kumamoto, and W. Wickner. 1989. Three pure chaperone proteins of Escherichia coli - SecB, trigger factor and GroEL - form soluble complexes with precursor proteins in vitro. EMBO J. 8:2703-2709.
45. Lee, H. C., and H. D. Bernstein. 2001. The targeting pathway of Escherichia coli presecretory and integral membrane proteins is specified by the hydrophobicity of the targeting signal. Proc. Natl. Acad. Sci. USA 98:3471-3476.
46. Lee, H. C., and H. D. Bernstein. 2002. Trigger factor retards protein export in Escherichia coli. J. Biol. Chem. 277:43527-43535.
47. Lee, P. A., G. Buchanan, N. R. Stanley, B. C. Berks, and T. Palmer. 2002. Truncation analysis of TatA and TatB defines the minimal functional units required for protein translocation. J. Bacteriol. 184:5871-5879.
48. Leheny, E. A., S. A. Teter, and S. M. Theg. 1998. Identification of a role for an azide-sensitive factor in the thylakoid transport of the 17-kilodalton subunit of the photosynthetic oxygen-evolving complex. Plant Physiol. 116:805-814.
49. Liu, G., T. B. Topping, and L. L. Randall. 1989. Physiological role during export for the retardation of folding by the leader peptide of maltose-binding protein. Proc. Natl. Acad. Sci. USA 86:9213-9217.
50. Madueno, F., J. A. Napier, and J. C. Gray. 1993. Newly imported Rieske iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 5:1865-1876.
51. Mallik, I., M. A. Smith, and A. M. Flower. 2002. Recognition of secretory proteins in Escherichia coli requires signals in addition to the signal sequence and slow folding. BMC Microbiol. 2:32.
52. Mingarro, I., I. Nilsson, P. Whitley, and G. von Heijne. 2000. Different conformations of nascent polypeptides during translocation across the ER membrane. BMC Cell Biol. 1:3.
53. Molik, S., I. Karnauchov, C. Weidlich, R. G. Herrmann, and R. B. Klosgen. 2001. The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J. Biol. Chem. 276:42761-42766.
54. Mori, H., and K. Cline. 2002. A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid [Delta]pH/Tat translocase. J. Cell Biol. 157:205-210.
55. Nouwen, N., B. de Kruijff, and J. Tommassen. 1996. prlA suppressors in Escherichia coli relieve the proton electrochemical gradient dependency of translocation of wild-type precursors. Proc. Natl. Acad. Sci. USA 93:5953-5957.
56. Oresnik, I. J., C. L. Ladner, and R. J. Turner. 2001. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 40:323-331.
57. Osborne, R. S., and T. J. Silhavy. 1993. PrlA suppressor mutations cluster in regions corresponding to three distinct topological domains. EMBO J. 12:3391-3398.
58. Patzelt, H., S. Rudiger, D. Brehmer, G. Kramer, S. Vorderwulbecke, E. Schaffitzel, A. Waitz, T. Hesterkamp, L. Dong, J. Schneider-Mergener, B. Bukau, and E. Deuerling. 2001. Binding specificity of Escherichia coli trigger factor. Proc. Natl. Acad. Sci. USA 98:14244-14249.
59. Phillips, G. J., and T. J. Silhavy. 1990. Heat-shock proteins DnaK and GroEL facilitate export of LacZ hybrid proteins in E. coli. Nature 344:882-884.
60. Pop, O. I., M. Westermann, R. Volkmer-Engert, D. Schulz, C. Lemke, S. Schreiber, R. Gerlach, R. Wetzker, and J. P. Muller. 2003. Sequence-specific binding of prePhoD to soluble TatAd indicates protein-mediated targeting of the Tat export in Bacillus subtilis. J. Biol. Chem. 278:38428-38436.
61. Powers, T., and P. Walter. 1997. Co-translational protein targeting catalyzed by the Escherichia coli signal recognition particle and its receptor. EMBO J. 16:4880-4886.
62. Pradel, N., C. L. Santini, C. Y. Ye, L. Fevat, F. Gerard, M. Alami, and L. F. Wu. 2003. Influence of tat mutations on the ribose-binding protein translocation in Escherichia coli. Biochem. Biophys. Res. Commun. 306:786-791.
63. Prinz, W. A., C. Spiess, M. Ehrmann, C. Schierle, and J. Beckwith. 1996. Targeting of signal sequenceless proteins for export in Escherichia coli with altered protein translocase. EMBO J. 15:5209-5217.
64. Ray, N., J. Oates, R. J. Turner, and C. Robinson. 2003. DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus. FEBS Lett. 534:156-160.
65. Rodrigue, A., N. Batia, M. Muller, O. Fayet, R. Bohm, M. A. Mandrand-Berthelot, and L. F. Wu. 1996. Involvement of the GroE chaperonins in the nickel-dependent anaerobic biosynthesis of NiFe-hydrogenases of Escherichia coli. J. Bacteriol. 178:4453-4460.
66. Rodrigue, A., A. Chanal, K. Beck, M. Muller, and L. F. Wu. 1999. Cotranslocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J. Biol. Chem. 274:13223-13228.
67. Roffey, R. A., and S. M. Theg. 1996. Analysis of the import of carboxyl-terminal truncations of the 23-kilodalton subunit of the oxygen-evolving complex suggests that its structure is an important determinant for thylakoid transport. Plant Physiol. 111:1329-1338.
68. Rose, R. W., T. Bruser, J. C. Kissinger, and M. Pohlschroder. 2002. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol. Microbiol. 45:943-950.
69. Rudiger, S., L. Germeroth, J. Schneider-Mergener, and B. Bukau. 1997. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16:1501-1507.
70. Sanders, C., N. Wethkamp, and H. Lill. 2001. Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol. Microbiol. 41:241-246.
71. Sandkvist, M. 2001. Biology of type II secretion. Mol. Microbiol. 40:271-283.
72. Santini, C. L., B. Ize, A. Chanal, M. Muller, G. Giordano, and L. F. Wu. 1998. A novel sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17:101-112.
73. Sargent, F., U. Gohlke, E. De Leeuw, N. R. Stanley, T. Palmer, H. R. Saibil, and B. C. Berks. 2001. Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268:3361-3367.
74. Schierle, C. F., M. Berkmen, D. Huber, C. Kumamoto, D. Boyd, and J. Beckwith. 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.
75. Settles, A. M., A. Yonetani, A. Baron, D. R. Bush, K. Cline, and R. Martienssen. 1997. Sec-independent protein translocation by the maize Hcf106 protein. Science 278:1467-1470.
76. Turner, R. J., A. L. Papish, and F. Sargent. 2004. Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can. J. Microbiol. 50:225-238.
77. Ullers, R. S., E. N. Houben, A. Raine, C. M. ten Hagen-Jongman, M. Ehrenberg, J. Brunner, B. Oudega, N. Harms, and J. Luirink. 2003. Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome. J. Cell Biol. 161:679-684.
78. Ullers, R. S., J. Luirink, N. Harms, F. Schwager, C. Georgopoulos, and P. Genevaux. 2004. SecB is a bona fide generalized chaperone in Escherichia coli. Proc. Natl. Acad. Sci. USA 101:7853-7858.
79. Van den Berg, B., W. M. Clemons, Jr., I. Collinson, Y. Modis, E. Hartmann, S. C. Harrison, and T. A. Rapoport. 2004. X-ray structure of a protein-conducting channel. Nature 427:36-44.
80. Watanabe, M., and G. Blobel. 1989. Cytosolic factor purified from Escherichia coli is necessary and sufficient for the export of a preprotein and is a homotetramer of SecB. Proc. Natl. Acad. Sci. USA 86:2728-2732.
81. Weiner, J. H., P. T. Bilous, G. M. Shaw, S. P. Lubitz, L. Frost, G. H. Thomas, J. A. Cole, and R. J. Turner. 1998. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93:93-101.
82. Xu, Z., J. D. Knafels, and K. Yoshino. 2000. Crystal structure of the bacterial protein export chaperone secB. Nat. Struct. Biol. 7:1172-1177.