An Essential Role for the DnaK Molecular Chaperone in Stabilizing Over-expressed Substrate Proteins of the Bacterial Twin-arginine Translocation Pathway

Journal of Molecular Biology

Volumn 367, Issue 3, 2007, Pages 715-730

  Pérez Rodríguez, Ritsdeliz ^a   Fisher, Adam C ^a   Perlmutter, Jason D ^a   Hicks, Matthew G ^b   Chanal, Angélique ^c   Santini, Claire Lise ^c   Wu, Long Fei ^c   Palmer, Tracy ^b   DeLisa, Matthew P ^a  

^a Cornell University   (United States)

^b JOHN INNES CENTRE   (United Kingdom)

^c CNRS   (France)

Author keywords

heat shock protein; inner membrane transport; molecular chaperone machinery; periplasm; protein secretion

Indexed keywords

ARGININE; BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; PROTEIN DNAK; TRANSACTIVATOR PROTEIN; TRIMETHYLAMINE OXIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOTECHNOLOGY; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN TRANSPORT; SCREENING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33847396185     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.01.027     Document Type: Article

References (88)

1. Van den Berg B., Clemons Jr. W.M., Collinson I., Modis Y., Hartmann E., Harrison S.C., and Rapoport T.A. X-ray structure of a protein-conducting channel. Nature 427 (2004) 36-44
2. Driessen A.J., Manting E.H., and van der Does C. The structural basis of protein targeting and translocation in bacteria. Natue Struct. Biol. 8 (2001) 492-498
3. Lecker S.H., Driessen A.J., and Wickner W. ProOmpA contains secondary and tertiary structure prior to translocation and is shielded from aggregation by association with SecB protein. EMBO J. 9 (1990) 2309-2314
4. Liu G., Topping T.B., and Randall L.L. Physiological role during export for the retardation of folding by the leader peptide of maltose-binding protein. Proc. Natl Acad. Sci. USA 86 (1989) 9213-9217
5. Collier D.N., Bankaitis V.A., Weiss J.B., and Bassford Jr. P.J. The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell 53 (1988) 273-283
6. Kumamoto C.A. Escherichia coli SecB protein associates with exported protein precursors in vivo. Proc. Natl Acad. Sci. USA 86 (1989) 5320-5324
7. Watanabe M., and Blobel G. 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 (1989) 2728-2732
8. Kumamoto C.A., and Beckwith J. Mutations in a new gene, secB, cause defective protein localization in Escherichia coli. J. Bacteriol. 154 (1983) 253-260
9. Knoblauch N.T., Rudiger S., Schonfeld H.J., Driessen A.J., Schneider-Mergener J., and Bukau B. Substrate specificity of the SecB chaperone. J. Biol. Chem. 274 (1999) 34219-34225
10. Phillips G.J., and Silhavy T.J. Heat-shock proteins DnaK and GroEL facilitate export of LacZ hybrid proteins in E. coli. Nature 344 (1990) 882-884
11. Wild J., Altman E., Yura T., and Gross C.A. DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev. 6 (1992) 1165-1172
12. Wild J., Rossmeissl P., Walter W.A., and Gross C.A. Involvement of the DnaK-DnaJ-GrpE chaperone team in protein secretion in Escherichia coli. J. Bacteriol. 178 (1996) 3608-3613
13. Berks B.C., Sargent F., and Palmer T. The Tat protein export pathway. Mol. Microbiol. 35 (2000) 260-274
14. Robinson C., and Bolhuis A. Protein targeting by the twin-arginine translocation pathway. Nature Rev. Mol. Cell Biol. 2 (2001) 350-356
15. DeLisa M.P., Tullman D., and Georgiou G. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc. Natl Acad. Sci. USA 100 (2003) 6115-6120
16. Fisher A.C., Kim W., and DeLisa M.P. Genetic selection for protein solubility enabled by the folding quality control feature of the twin-arginine translocation pathway. Protein Sci. 15 (2006) 449-458
17. Kim J.-Y., Fogarty E.A., Lu F.J., Zhu H., Henderson L.A., and DeLisa M.P. Twin-arginine translocation of active human tissue plasminogen activator in Escherichia coli. Appl. Environ. Microbiol. 71 (2005) 8451-8459
18. Rodrigue A., Chanal A., Beck K., Muller M., and Wu L.F. Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J. Biol. Chem. 274 (1999) 13223-13228
19. Sanders C., Wethkamp N., and Lill H. Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol. Microbiol. 41 (2001) 241-246
20. Turner R.J., Papish A.L., and Sargent F. Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can. J. Microbiol. 50 (2004) 225-238
21. Berks B.C. A common export pathway for proteins binding complex redox cofactors?. Mol. Microbiol. 22 (1996) 393-404
22. Dubini A., and Sargent F. Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Letters 549 (2003) 141-146
23. Jack R.L., Buchanan G., Dubini A., Hatzixanthis K., Palmer T., and Sargent F. Coordinating assembly and export of complex bacterial proteins. EMBO J. 23 (2004) 3962-3972
24. Ray N., Oates J., Turner R.J., and Robinson C. 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 Letters 534 (2003) 156-160
25. Oresnik I.J., Ladner C.L., and Turner R.J. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 40 (2001) 323-331
26. Berks B.C., Palmer T., and Sargent F. The Tat protein translocation pathway and its role in microbial physiology. Advan. Microbiol. Physiol. 47 (2003) 187-254
27. Palmer T., Sargent F., and Berks B.C. Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol. 13 (2005) 175-180
28. Berks B.C., Palmer T., and Sargent F. Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr. Opin. Microbiol. 8 (2005) 174-181
29. Tullman-Ercek D., DeLisa M.P., Kawarasaki Y., Iranpour P., Ribnicky B., Palmer T., and Georgiou G. Export pathway selectivity of Escherichia coli twin-arginine translocation signal peptides. J. Biol. Chem (2007) 10.1074/jbc.M610507200
30. DeLisa M.P., Samuelson P., Palmer T., and Georgiou G. Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J. Biol. Chem. 277 (2002) 29825-29831
31. Santini C.L., Bernadac A., Zhang M., Chanal A., Ize B., Blanco C., and Wu L.F. Translocation of jellyfish green fluorescent protein via the Tat system of Escherichia coli and change of its periplasmic localization in response to osmotic up-shock. J. Biol. Chem. 276 (2001) 8159-8164
32. Thomas J.D., Daniel R.A., Errington J., and Robinson C. Export of active green fluorescent protein to the periplasm by the twin-arginine translocase (Tat) pathway in Escherichia coli. Mol. Microbiol. 39 (2001) 47-53
33. Blaudeck N., Kreutzenbeck P., Freudl R., and Sprenger G.A. Genetic analysis of pathway specificity during posttranslational protein translocation across the Escherichia coli plasma membrane. J. Bacteriol. 185 (2003) 2811-2819
34. Fisher A.C., and DeLisa M.P. A little help from my friends: quality control of presecretory proteins in bacteria. J. Bacteriol. 186 (2004) 7467-7473
35. Jong W.S., ten Hagen-Jongman C.M., Genevaux P., Brunner J., Oudega B., and Luirink J. Trigger factor interacts with the signal peptide of nascent Tat substrates but does not play a critical role in Tat-mediated export. Eur. J. Biochem. 271 (2004) 4779-4787
36. Rodrigue A., Batia N., Muller M., Fayet O., Bohm R., Mandrand-Berthelot M.A., and Wu L.F. Involvement of the GroE chaperonins in the nickel-dependent anaerobic biosynthesis of NiFe-hydrogenases of Escherichia coli. J. Bacteriol. 178 (1996) 4453-4460
37. Kerner M.J., Naylor D.J., Ishihama Y., Maier T., Chang H.C., Stines A.P., et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122 (2005) 209-220
38. Howell, J. M. & Turner, R. J. (2007). Identification of an interactome for DmsD, a chaperone for DmsA and the Tat system. (submitted).
39. Xu Y., Weng C.L., Narayanan N., Hsieh M.Y., Anderson W.A., Scharer J.M., et al. Chaperone-mediated folding and maturation of the penicillin acylase precursor in the cytoplasm of Escherichia coli. Appl. Environ. Microbiol. 71 (2005) 6247-6253
40. Yahr T.L., and Wickner W.T. Functional reconstitution of bacterial Tat translocation in vitro. EMBO J. 20 (2001) 2472-2479
41. Alami M., Trescher D., Wu L.F., and Muller M. Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli. J. Biol. Chem. 277 (2002) 20499-20503
42. Chanal A., Santini C.L., and Wu L.F. Specific inhibition of the translocation of a subset of Escherichia coli TAT substrates by the TorA signal peptide. J. Mol. Biol. 327 (2003) 563-570
43. Gon S., Patte J.C., Mejean V., and Iobbi-Nivol C. The torYZ (yecK bisZ) operon encodes a third respiratory trimethylamine N-oxide reductase in Escherichia coli. J. Bacteriol. 182 (2000) 5779-5786
44. Mikhaleva N.I., Santini C.L., Giordano G., Nesmeyanova M.A., and Wu L.F. Requirement for phospholipids of the translocation of the trimethylamine N-oxide reductase through the Tat pathway in Escherichia coli. FEBS Letters 463 (1999) 331-335
45. DeLisa M.P., Lee P., Palmer T., and Georgiou G. Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J. Bacteriol. 186 (2004) 366-373
46. Farrell C.M., Grossman A.D., and Sauer R.T. Cytoplasmic degradation of ssrA-tagged proteins. Mol. Microbiol. 57 (2005) 1750-1761
47. Bronstein P.A., Marrichi M., Cartinhour S., Schneider D.J., and DeLisa M.P. Identification of a twin-arginine translocation system in Pseudomonas syringae pv. tomato DC3000 and its contribution to pathogenicity and fitness. J. Bacteriol. 187 (2005) 8450-8461
48. Barrett C.M., Ray N., Thomas J.D., Robinson C., and Bolhuis A. Quantitative export of a reporter protein, GFP, by the twin-arginine translocation pathway in Escherichia coli. Biochem. Biophys. Res. Commun. 304 (2003) 279-284
49. Cristobal S., de Gier J.W., Nielsen H., and von Heijne G. Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J. 18 (1999) 2982-2990
50. Angelini S., Moreno R., Gouffi K., Santini C., Yamagishi A., Berenguer J., and Wu L. Export of Thermus thermophilus alkaline phosphatase via the twin-arginine translocation pathway in Escherichia coli. FEBS Letters 506 (2001) 103-107
51. Rudiger S., Germeroth L., Schneider-Mergener J., and Bukau B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16 (1997) 1501-1507
52. Deuerling E., Schulze-Specking A., Tomoyasu T., Mogk A., and Bukau B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400 (1999) 693-696
53. Tomoyasu T., Ogura T., Tatsuta T., and Bukau B. Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli. Mol. Microbiol. 30 (1998) 567-581
54. Castanie M.P., Berges H., Oreglia J., Prere M.F., and Fayet O. A set of pBR322-compatible plasmids allowing the testing of chaperone-assisted folding of proteins overexpressed in Escherichia coli. Anal. Biochem. 254 (1997) 150-152
55. Dionisi H.M., Checa S.K., Krapp A.R., Arakaki A.K., Ceccarelli E.A., Carrillo N., and Viale A.M. Cooperation of the DnaK and GroE chaperone systems in the folding pathway of plant ferredoxin-NADP+ reductase expressed in Escherichia coli. Eur. J. Biochem. 251 (1998) 724-728
56. Leheny E.A., Teter S.A., and Theg S.M. 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 (1998) 805-814
57. Madueno F., Napier J.A., and Gray J.C. Newly imported Rieske iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 5 (1993) 1865-1876
58. Molik S., Karnauchov I., Weidlich C., Herrmann R.G., and Klosgen R.B. 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 (2001) 42761-42766
59. Gur E., Biran D., Shechter N., Genevaux P., Georgopoulos C., and Ron E.Z. The Escherichia coli DjlA and CbpA proteins can substitute for DnaJ in DnaK-mediated protein disaggregation. J. Bacteriol. 186 (2004) 7236-7242
60. Erbse A., Dougan D.A., and Bukau B. A folding machine for many but a master of none. Nature Struct. Biol. 10 (2003) 84-86
61. Houry W.A., Frishman D., Eckerskorn C., Lottspeich F., and Hartl F.U. Identification of in vivo substrates of the chaperonin GroEL. Nature 402 (1999) 147-154
62. Chanal A., Santini C., and Wu L. 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 (1998) 674-676
63. Mogk A., Deuerling E., Vorderwulbecke S., Vierling E., and Bukau B. Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 50 (2003) 585-595
64. Butland G., Peregrin-Alvarez J.M., Li J., Yang W., Yang X., Canadien V., et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433 (2005) 531-537
65. Li S.Y., Chang B.Y., and Lin S.C. Coexpression of TorD enhances the transport of GFP via the TAT pathway. J. Biotechnol. 122 (2006) 412-421
66. Guzman L.M., Belin D., Carson M.J., and Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177 (1995) 4121-4130
67. Sargent F., Bogsch E.G., Stanley N.R., Wexler M., Robinson C., Berks B.C., and Palmer T. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17 (1998) 3640-3650
68. Stanley N.R., Findlay K., Berks B.C., and Palmer T. Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotropic defects in the cell envelope. J. Bacteriol. 183 (2001) 139-144
69. Chen G., Hayhurst A., Thomas J.G., Harvey B.R., Iverson B.L., and Georgiou G. Isolation of high-affinity ligand-binding proteins by periplasmic expression with cytometric screening (PECS). Nature Biotechnol. 19 (2001) 537-542
70. De Leeuw E., Porcelli I., Sargent F., Palmer T., and Berks B.C. Membrane interactions and self-association of the TatA and TatB components of the twin-arginine translocation pathway. FEBS Letters 506 (2001) 143-148
71. Derman A.I., Prinz W.A., Belin D., and Beckwith J. Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli. Science 262 (1993) 1744-1747
72. Silvestro A., Pommier J., and Giordano G. The inducible trimethylamine-N-oxide reductase of Escherichia coli K12: biochemical and immunological studies. Biochim. Biophys. Acta 954 (1988) 1-13
73. Enoch H.G., and Lester R.L. The purification and properties of formate dehydrogenase and nitrate reductase from Escherichia coli. J. Biol. Chem. 250 (1975) 6693-6705
74. Tian H., and Beckwith J. Genetic screen yields mutations in genes encoding all known components of the Escherichia coli signal recognition particle pathway. J. Bacteriol. 184 (2002) 111-118
75. Strauch K.L., and Beckwith J. An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc. Natl Acad. Sci. USA 85 (1988) 1576-1580
76. Tatsuta T., Tomoyasu T., Bukau B., Kitagawa M., Mori H., Karata K., and Ogura T. Heat shock regulation in the ftsH null mutant of Escherichia coli: dissection of stability and activity control mechanisms of sigma32 in vivo. Mol. Microbiol. 30 (1998) 583-593
77. Tilly K., Murialdo H., and Georgopoulos C. Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis. Proc. Natl Acad. Sci. USA 78 (1981) 1629-1633
78. Yochem J., Uchida H., Sunshine M., Saito H., Georgopoulos C.P., and Feiss M. Genetic analysis of two genes, dnaJ and dnaK, necessary for Escherichia coli and bacteriophage lambda DNA replication. Mol. Gen. Genet. 164 (1978) 9-14
79. Bogsch E.G., Sargent F., Stanley N.R., Berks B.C., Robinson C., and Palmer T. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273 (1998) 18003-18006
80. Wexler M., Sargent F., Jack R.L., Stanley N.R., Bogsch E.G., Robinson C., et al. TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in sec-independent protein export. J. Biol. Chem. 275 (2000) 16717-16722
81. Thomas J.G., and Baneyx F. Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J. Bacteriol. 180 (1998) 5165-5172
82. Zylicz M., Ang D., and Georgopoulos C. The grpE protein of Escherichia coli. Purification and properties. J. Biol. Chem. 262 (1987) 17437-17442
83. Liberek K., Marszalek J., Ang D., Georgopoulos C., and Zylicz M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl Acad. Sci. USA 88 (1991) 2874-2878
84. Teter S.A., Houry W.A., Ang D., Tradler T., Rockabrand D., Fischer G., et al. Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97 (1999) 755-765
85. Ogura T., Inoue K., Tatsuta T., Suzaki T., Karata K., Young K., et al. Balanced biosynthesis of major membrane components through regulated degradation of the committed enzyme of lipid A biosynthesis by the AAA protease FtsH (HflB) in Escherichia coli. Mol. Microbiol. 31 (1999) 833-844
86. Zeilstra-Ryalls J., Fayet O., Baird L., and Georgopoulos C. Sequence analysis and phenotypic characterization of groEL mutations that block lambda and T4 bacteriophage growth. J. Bacteriol. 175 (1993) 1134-1143
87. Weiss J.B., Ray P.H., and Bassford Jr. P.J. Purified SecB protein of Escherichia coli retards folding and promotes membrane translocation of the maltose-binding protein in vitro. Proc. Natl Acad. Sci. USA 85 (1988) 8978-8982
88. Diao J., Young L., Kim S., Fogarty E.A., Heilman S.M., Zhou P., et al. A three-channel microfluidic device for generating static linear gradients and its application to the quantitative analysis of bacterial chemotaxis. Lab. Chip. 6 (2006) 381-388