Function of trigger factor and DnaK in multidomain protein folding: Increase in yield at the expense of folding speed

Cell

Volumn 117, Issue 2, 2004, Pages 199-209

  Agashe, Vishwas R ^a   Guha, Suranjana ^a   Chang, Hung Chun ^a   Genevaux, Pierre ^b   Hayer Hartl, Manajit ^a   Stemp, Markus ^a   Georgopoulos, Costa ^b   Hartl, F Ulrich ^a   Barral, José M ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CHAPERONE; LUCIFERASE; PROTEIN; PROTEIN DNAK; TRIGGER FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; EUKARYOTIC CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; RIBOSOME; RNA TRANSLATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 1942421714     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(04)00299-5     Document Type: Article

References (38)

1. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. Current Protocols in Molecular Biology. 2003;John Wiley & Sons, Inc, New York.
2. Ayling A., Baneyx F. Influence of the GroE molecular chaperone machine on the in vitro refolding of Escherichia coli beta-galactosidase. Protein Sci. 5:1996;478-487.
3. Baneyx F. Recombinant protein expression in Escherichia coli. Curr. Opin. Biotechnol. 10:1999;411-421.
4. Beck K., Wu L.F., Brunner J., Muller M. Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J. 19:2000;134-143.
5. Bremer H., Dennis P.P. Modulation of chemical composition and other parameters of the cell by growth rate. Neidhardt F.C. Escherichia Coli and Salmonella. Cellular and Molecular Biology:1996;1553-1569 ASM Press, Washington, D.C.
6. Buchberger A., Schroder H., Hesterkamp T., Schonfeld H.J., Bukau B. Substrate shuttling between the DnaK and GroEL systems indicates a chaperone network promoting protein folding. J. Mol. Biol. 261:1996;328-333.
7. Bukau B., Horwich A.L. The Hsp70 and Hsp60 chaperone machines. Cell. 92:1998;351-366.
8. Bukau B., Deuerling E., Pfund C., Craig E.A. Getting newly synthesized proteins into shape. Cell. 101:2000;119-122.
9. Castanié H.P., Berges H., Oreglia J., Prère M.F., 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.
10. Conti E., Franks N.P., Brick P. Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure. 4:1996;287-298.
11. Deuerling E., Schulze-Specking A., Tomoyasu T., Mogk A., Bukau B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature. 400:1999;693-696.
12. Frydman J. Folding of newly translated proteins in vivo. the role of molecular chaperones Annu. Rev. Biochem. 70:2001;603-647.
13. Frydman J., Nimmesgern E., Ohtsuka K., Hartl F.U. Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature. 370:1994;111-117.
14. Frydman J., Erdjument-Bromage H., Tempst P., Hartl F.U. Co-translational domain folding as the structural basis for the rapid de novo folding of firefly luciferase. Nat. Struct. Biol. 6:1999;697-705.
15. Genevaux P., Keppel F., Schwager F., Langendijk-Genevaux P.S., Hartl F.U., Georgopoulos C. In vivo analysis of the overlapping functions of DnaK and trigger factor. EMBO Rep. 5:2004;195-200.
16. Greer L.F. III, Szalay A.A. Imaging of light emission from the expression of luciferases in living cells and organisms. a review Luminescence. 17:2002;43-74.
17. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol. from nascent chain to folded protein Science. 295:2002;1852-1858.
18. Herbst R., Schafer U., Seckler R. Equilibrium intermediates in the reversible unfolding of firefly (Photinus pyralis) luciferase. J. Biol. Chem. 272:1997;7099-7105.
19. Hesterkamp T., Bukau B. Role of the DnaK and HscA homologs of Hsp70 chaperones in protein folding in E. coli. EMBO J. 17:1998;4818-4828.
20. Hesterkamp T., Hauser S., Lutcke H., Bukau B. Escherichia coli trigger factor is a prolyl isomerase that associates with nascent polypeptide chains. Proc. Natl. Acad. Sci. USA. 93:1996;4437-4441.
21. Hesterkamp T., Deuerling E., Bukau B. The amino-terminal 118 amino acids of Escherichia coli trigger factor constitute a domain that is necessary and sufficient for binding to ribosomes. J. Biol. Chem. 272:1997;21865-21871.
22. Jacobson R.H., Zhang X.J., DuBose R.F., Matthews B.W. Three-dimensional structure of beta-galactosidase from E. coli. Nature. 369:1994;761-766.
23. Kolb V.A., Makeyev E.V., Spirin A.S. Folding of firefly luciferase during translation in a cell-free system. EMBO J. 13:1994;3631-3637.
24. Kramer G., Rauch T., Rist W., Vorderwulbecke S., Patzelt H., Schulze-Specking A., Ban N., Deuerling E., Bukau B. L23 protein functions as a chaperone docking site on the ribosome. Nature. 419:2002;171-174.
25. Lill R., Crooke E., Guthrie B., Wickner W. The "trigger factor cycle" includes ribosomes, presecretory proteins, and the plasma membrane. Cell. 54:1988;1013-1018.
26. Maier R., Eckert B., Scholz C., Lilie H., Schmid F.X. Interaction of trigger factor with the ribosome. J. Mol. Biol. 326:2003;585-592.
27. Netzer W.J., Hartl F.U. Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature. 388:1997;343-349.
28. Nichtl A., Buchner J., Jaenicke R., Rudolph R., Scheibel T. Folding and association of beta-galactosidase. J. Mol. Biol. 282:1998;1083-1091.
29. Nicola A.V., Chen W., Helenius A. Co-translational folding of an alphavirus capsid protein in the cytosol of living cells. Nat. Cell Biol. 1:1999;341-345.
30. Patzelt H., Rudiger S., Brehmer D., Kramer G., Vorderwulbecke S., Schaffitzel E., Waitz A., Hesterkamp T., Dong L., Schneider-Mergener J.et al. Binding specificity of Escherichia coli trigger factor. Proc. Natl. Acad. Sci. USA. 98:2001;14244-14249.
31. Spedding G. Isolation and analysis of ribosomes from prokaryotes, eukaryotes, and organelles. Spedding G. Ribosomes and Protein Synthesis. A Practical Approach:1990;1-29 Oxford University Press, Oxford.
32. Pierpaoli E.V., Sandmeier E., Baici Antonio, Schönfeld H.-J., Gisler S., Christen P. The power stroke of the DnaK/DnaJ/GrpE molecular chaperone system. J. Mol. Biol. 269:1997;757-768.
33. Rüdiger S., Germeroth L., Schneider-Mergener J., Bukau B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide. EMBO J. 16:1997;1501-1507.
34. Sánchez I.E., Morillas M., Zobley E., Kiefhaber T., Glockshuber R. Fast folding of the two-domain Semliki Forest virus capsid protein explains co-translational proteolytic activity. J. Mol. Biol. in press:2004.
35. Stoller G., Rucknagel K.P., Nierhaus K.H., Schmid F.X., Fischer G., Rahfeld J.U. A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J. 14:1995;4939-4948.
36. Szabo A., Langer T., Schroder H., Flanagan J., Bukau B., Hartl F.U. The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl. Acad. Sci. USA. 91:1994;10345-10349.
37. Teter S.A., Houry W.A., Ang D., Tradler T., Rockabrand D., Fischer G., Blum P., Georgopoulos C., Hartl F.U. Polypeptide flux through bacterial Hsp70. DnaK cooperates with trigger factor in chaperoning nascent chains Cell. 97:1999;755-765.
38. Valent Q.A., Kendall D.A., High S., Kusters R., Oudega B., Luirink J. Early events in preprotein recognition in E. coli. interaction of SRP and trigger factor with nascent polypeptides EMBO J. 14:1995;5494-5505.