A cradle for new proteins: Trigger factor at the ribosome

Current Opinion in Structural Biology

Volumn 15, Issue 2, 2005, Pages 204-212

  Maier, Timm ^a   Ferbitz, Lars ^a   Deuerling, Elke ^b   Ban, Nenad ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; PROTEIN; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ESCHERICHIA COLI; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; RIBOSOME;

EID: 17044363522     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2005.03.005     Document Type: Review

References (51)

1. C.A. Woolhead, P.J. McCormick, and A.E. Johnson Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins Cell 116 2004 725 736 This work demonstrates helix-like protein folding inside the ribosomal exit tunnel, observed only for membrane proteins. This early compaction may play a decisive role regarding the fate of the protein, and its future interactions with TF and SRP.
2. R.J. Gilbert, P. Fucini, S. Connell, S.D. Fuller, K.H. Nierhaus, C.V. Robinson, C.M. Dobson, and D.I. Stuart Three-dimensional structures of translating ribosomes by cryo-EM Mol Cell 14 2004 57 66
3. B. Bukau, E. Deuerling, C. Pfund, and E.A. Craig Getting newly synthesized proteins into shape Cell 101 2000 119 122
4. F.U. Hartl, and M. Hayer-Hartl Molecular chaperones in the cytosol: from nascent chain to folded protein Science 295 2002 1852 1858
5. E. Deuerling, A. Schulze-Specking, T. Tomoyasu, A. Mogk, and B. Bukau Trigger factor and DnaK cooperate in folding of newly synthesized proteins Nature 400 1999 693 696
6. S.A. Teter, W.A. Houry, D. Ang, T. Tradler, D. Rockabrand, G. Fischer, P. Blum, C. Georgopoulos, and F.U. Hartl Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains Cell 97 1999 755 765
7. B. Bukau, and A.L. Horwich The Hsp70 and Hsp60 chaperone machines Cell 92 1998 351 366
8. M. Muller, H.G. Koch, K. Beck, and U. Schafer Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane Prog Nucleic Acid Res Mol Biol 66 2001 107 157
9. K. Beck, L.F. Wu, J. Brunner, and M. Muller 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
10. G. Kramer, A. Rutkowska, R.D. Wegrzyn, H. Patzelt, T.A. Kurz, F. Merz, T. Rauch, S. Vorderwulbecke, E. Deuerling, and B. Bukau Functional dissection of Escherichia coli trigger factor: unraveling the function of individual domains J Bacteriol 186 2004 3777 3784
11. T. Hesterkamp, S. Hauser, H. Lutcke, and B. Bukau Escherichia coli trigger factor is a prolyl isomerase that associates with nascent polypeptide chains Proc Natl Acad Sci USA 93 1996 4437 4441
12. T. Hesterkamp, E. Deuerling, and B. Bukau 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
13. G. Kramer, T. Rauch, W. Rist, S. Vorderwulbecke, H. Patzelt, A. Schulze-Specking, N. Ban, E. Deuerling, and B. Bukau L23 protein functions as a chaperone docking site on the ribosome Nature 419 2002 171 174
14. L. Ferbitz, T. Maier, H. Patzelt, B. Bukau, E. Deuerling, and N. Ban Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins Nature 431 2004 590 596 This article describes X-ray crystal structures of full-length TF at 2.7 Å resolution and of the RB domain of TF in complex with the 50S ribosomal subunit at 3.5 Å resolution. It also provides a structure-based model of TF action.
15. ••], demonstrating the rigidity of the overall TF fold.
16. O. Kristensen, and M. Gajhede Chaperone binding at the ribosomal exit tunnel Structure 11 2003 1547 1556
17. M. Vogtherr, D.M. Jacobs, T.N. Parac, M. Maurer, A. Pahl, K. Saxena, H. Ruterjans, C. Griesinger, and K.M. Fiebig NMR solution structure and dynamics of the peptidyl-prolyl cis-trans isomerase domain of the trigger factor from Mycoplasma genitalium compared to FK506-binding protein J Mol Biol 318 2002 1097 1115
18. H. Patzelt, G. Kramer, T. Rauch, H.J. Schonfeld, B. Bukau, and E. Deuerling Three-state equilibrium of Escherichia coli trigger factor Biol Chem 383 2002 1611 1619
19. G. Kramer, H. Patzelt, T. Rauch, T.A. Kurz, S. Vorderwulbecke, B. Bukau, and E. Deuerling Trigger factor peptidyl-prolyl cis/trans isomerase activity is not essential for the folding of cytosolic proteins in Escherichia coli J Biol Chem 279 2004 14165 14170
20. P. Genevaux, F. Keppel, F. Schwager, P.S. Langendijk-Genevaux, F.U. Hartl, and C. Georgopoulos In vivo analysis of the overlapping functions of DnaK and trigger factor EMBO Rep 5 2004 195 200
21. W.R. Lyon, and M.G. Caparon Trigger factor-mediated prolyl isomerization influences maturation of the Streptococcus pyogenes cysteine protease J Bacteriol 185 2003 3661 3667
22. E. Bitto, and D.B. McKay Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins Structure 10 2002 1489 1498
23. S. Behrens, R. Maier, H. de Cock, F.X. Schmid, and C.A. Gross The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity EMBO J 20 2001 285 294
24. E. Bitto, and D.B. McKay Binding of phage-display-selected peptides to the periplasmic chaperone protein SurA mimics binding of unfolded outer membrane proteins FEBS Lett 568 2004 94 98
25. T. Krojer, M. Garrido-Franco, R. Huber, M. Ehrmann, and T. Clausen Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine Nature 416 2002 455 459
26. A.E. Rizzitello, J.R. Harper, and T.J. Silhavy Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli J Bacteriol 183 2001 6794 6800
27. A.V. Nicola, W. Chen, and A. Helenius Co-translational folding of an alphavirus capsid protein in the cytosol of living cells Nat Cell Biol 1 1999 341 345
28. W.J. Netzer, and F.U. Hartl Recombination of protein domains facilitated by co-translational folding in eukaryotes Nature 388 1997 343 349
29. V.R. Agashe, S. Guha, H.C. Chang, P. Genevaux, M. Hayer-Hartl, M. Stemp, C. Georgopoulos, F.U. Hartl, and J.M. Barral Function of trigger factor and DnaK in multidomain protein folding: increase in yield at the expense of folding speed Cell 117 2004 199 209 The authors provide a detailed analysis of the influence of DnaK and TF on the folding kinetics of two model proteins, β-galactosidase and firefly luciferase, during in vitro translation.
30. R. Maier, B. Eckert, C. Scholz, H. Lilie, and F.X. Schmid Interaction of trigger factor with the ribosome J Mol Biol 326 2003 585 592 A detailed investigation of the dynamics of the TF-ribosome interaction, using a TF variant with a fluorescent label attached to its N-terminal RB domain. It revealed that the TF-ribosome complex has much longer life-times than complexes between TF and artificial unfolded protein substrates without the context of the ribosome.
31. Q.A. Valent, J.W. de Gier, G. von Heijne, D.A. Kendall, C.M. ten Hagen-Jongman, B. Oudega, and J. Luirink Nascent membrane and presecretory proteins synthesized in Escherichia coli associate with signal recognition particle and trigger factor Mol Microbiol 25 1997 53 64
32. H. Patzelt, S. Rudiger, D. Brehmer, G. Kramer, S. Vorderwulbecke, E. Schaffitzel, A. Waitz, T. Hesterkamp, L. Dong, and J. Schneider-Mergener Binding specificity of Escherichia coli trigger factor Proc Natl Acad Sci USA 98 2001 14244 14249
33. R. Maier, C. Scholz, and F.X. Schmid Dynamic association of trigger factor with protein substrates J Mol Biol 314 2001 1181 1190
34. S. Rudiger, L. Germeroth, J. Schneider-Mergener, and B. Bukau Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries EMBO J 16 1997 1501 1507
35. S. Rudiger, J. Schneider-Mergener, and B. Bukau Its substrate specificity characterizes the DnaJ co-chaperone as a scanning factor for the DnaK chaperone EMBO J 20 2001 1042 1050
36. E. Deuerling, H. Patzelt, S. Vorderwulbecke, T. Rauch, G. Kramer, E. Schaffitzel, A. Mogk, A. Schulze-Specking, H. Langen, and B. Bukau Trigger factor and DnaK possess overlapping substrate pools and binding specificities Mol Microbiol 47 2003 1317 1328
37. G. Kramer, V. Ramachandiran, P.M. Horowitz, and B. Hardesty The molecular chaperone DnaK is not recruited to translating ribosomes that lack trigger factor Arch Biochem Biophys 403 2002 63 70
38. W.S. Jong, C.M. Ten Hagen-Jongman, P. Genevaux, J. Brunner, B. Oudega, and J. Luirink 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
39. R.S. Ullers, E.N. Houben, A. Raine, C.M. ten Hagen-Jongman, M. Ehrenberg, J. Brunner, B. Oudega, N. Harms, and J. Luirink 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 2003 679 684
40. M. Halic, T. Becker, M.R. Pool, C.M. Spahn, R.A. Grassucci, J. Frank, and R. Beckmann Structure of the signal recognition particle interacting with the elongation-arrested ribosome Nature 427 2004 808 814 Cryo-EM reconstruction of the eukaryotic ribosome-SRP complex and model building of the complex based on existing crystal structures provide a comprehensive view of ribosome-SRP and SRP-nascent chain interactions.
41. R. Beckmann, C.M. Spahn, N. Eswar, J. Helmers, P.A. Penczek, A. Sali, J. Frank, and G. Blobel Architecture of the protein-conducting channel associated with the translating 80S ribosome Cell 107 2001 361 372
42. M.R. Sharma, E.C. Koc, P.P. Datta, T.M. Booth, L.L. Spremulli, and R.K. Agrawal Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins Cell 115 2003 97 108
43. L. Jia, M. Dienhart, M. Schramp, M. McCauley, K. Hell, and R.A. Stuart Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1 EMBO J 22 2003 6438 6447
44. A. Raine, N. Ivanova, J.E. Wikberg, and M. Ehrenberg Simultaneous binding of trigger factor and signal recognition particle to the E. coli ribosome Biochimie 86 2004 495 500
45. I. Buskiewicz, E. Deuerling, S.Q. Gu, J. Jockel, M.V. Rodnina, B. Bukau, and W. Wintermeyer 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 2004 7902 7906 The authors present an analysis of the interactions between SRP, SRP receptor and TF based on cross-linking patterns and spectroscopical measurements. Unexpectedly, SRP and TF bind to the ribosome simultaneously, and TF dissociates from the complex only after formation of the TF-SRP-SRP receptor-ribosome quaternary complex.
46. H.C. Lee, and H.D. Bernstein 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 2001 3471 3476
47. H.C. Lee, and H.D. Bernstein Trigger factor retards protein export in Escherichia coli J Biol Chem 277 2002 43527 43535
48. S.C. Ha, T.H. Lee, S.S. Cha, and K.K. Kim Functional identification of the SecB homologue in Methanococcus jannaschii and direct interaction of SecB with trigger factor Biochem Biophys Res Commun 315 2004 1039 1044
49. R.S. Ullers, J. Luirink, N. Harms, F. Schwager, C. Georgopoulos, and P. Genevaux SecB is a bona fide generalized chaperone in Escherichia coli Proc Natl Acad Sci USA 101 2004 7583 7588 This study demonstrates that SecB overexpression efficiently suppresses the synthetic lethality of an E. coli strain lacking both TF and DnaK, and that SecB interacts with nascent chains of secreted and also non-secreted proteins in the absence of TF. Based on these observations, the authors suggest a generalized role for SecB in protein folding.
50. A.C. Fisher, and M.P. DeLisa A little help from my friends: quality control of presecretory proteins in bacteria J Bacteriol 186 2004 7467 7473
51. E. Or, D. Boyd, S. Gon, J. Beckwith, and T. Rapoport The bacterial ATPase SecA functions as a monomer in protein translocation J Biol Chem 280 2005 9097 9105