Probing ribosome-nascent chain complexes produced in vivo by NMR spectroscopy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 52, 2009, Pages 22239-22244

  Cabrita, Lisa D ^a,b   Hsu, Shang Te Danny ^a   Launay, Helene ^b   Dobson, Christopher M ^a   Christodoulou, John ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cotranslational folding; Ribosome; SecM

Indexed keywords

IMMUNOGLOBULIN; POLYPEPTIDE;

ARTICLE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SYNTHESIS; RIBOSOME;

CARRIER PROTEINS; ESCHERICHIA COLI; GENETIC VECTORS; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PEPTIDES; PLASMIDS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RIBOSOMES;

EID: 76049097596     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0903750106     Document Type: Article

References (44)

1. Steitz TA (2008) A structural understanding of the dynamic ribosome machine. Nat Rev Mol Cell Biol 9:242-253.
2. Bashan A, Yonath A(2008) Correlating ribosome function with high-resolution structures. Trends Microbiol 16:326-335.
3. Korostelev A, Trakhanov S, Laurberg M, Noller HF (2006) Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126:1065-1077.
4. Mitra K, Frank J (2006) Ribosome dynamics: Insights from atomic structure modeling into cryo-electron microscopy maps. Ann Rev Biophys Biomol Struc 35:299-317.
5. Evans MS, Sander IM, Clark PL (2008) Cotranslational folding promotes beta-helix formation and avoids aggregation in vivo. J Mol Biol 383:683-692.
6. Clark PL, King J (2001) A newly synthesized, ribosome-bound polypeptide chain adopts conformations dissimilar from early in vitro refolding intermediates. J Biol Chem 276:25411-25420.
7. Fedorov AN, et al. (1992) Folding on the ribosome of Escherichia coli tryptophan synthase beta subunit nascent chains probed with a conformation-dependent monoclonal antibody. J Mol Biol 228:351-358.
8. Netzer WJ, Hartl FU (1997) Recombination of protein domains facilitated by cotranslational folding in eukaryotes. Nature 388:343-349.
9. Nicola AV, Chen W, Helenius A (1999) Co-translational folding of an alphavirus capsid protein in the cytosol of living cells. Nat Cell Biol 1:341-345.
10. Ellis JP, et al. (2008) Chain dynamics of nascent polypeptides emerging from the ribosome. ACS Chem Biol 3:555-566.
11. Alekhina OM, Vassilenko KS, Spirin AS (2007) Translation of non-capped mRNAs in a eukaryotic cell-free system: Acceleration of initiation rate in the course of polysome formation. Nucleic Acids Res 35:6547-6559.
12. Fedorov AN, Baldwin TO (1995) Contribution of cotranslational folding to the rate of formation of native protein structure. Proc Natl Acad Sci USA 92:1227-1231.
13. Hartl FU, Hayer-Hartl M(2002) Molecular chaperones in the cytosol: From nascent chain to folded protein. Science 295:1852-1858.
14. Evans MS, Clarke TF, 4th, Clark PL (2005) Conformations of co-translational folding intermediates. Protein Pept Lett 12:189-195.
15. Woolhead CA, McCormick PJ, Johnson AE (2004) Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116:725-736.
16. Voss NR, Gerstein M, Steitz TA, Moore PB (2006) The geometry of the ribosomal polypeptide exit tunnel. J Mol Biol 360:893-906.
17. Kosolapov A, Deutsch C (2009) Tertiary interactions within the ribosomal exit tunnel. Nat Struct Mol Biol 16:405-411.
18. Gilbert RJC, et al. (2004) 3D structures of translating ribosomes by cryo-EM. Mol Cell 14:57-66.
19. Lu J, Deutsch C (2005) Folding zones inside the ribosomal exit tunnel. Nat Struct Mol Biol 12:1123-1129.
20. Ban N, et al. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 angstrom resolution. Science 289:905-920.
21. Fulle S, Gohlke H (2009) Statics of the ribosomal exit tunnel: Implications for cotranslational peptide folding, elongation regulation, and antibiotics binding. J Mol Biol 387:502-517.
22. Elcock (2006) A Molecular simulations of cotranslational protein folding: Fragment stabilities, folding cooperativity and trapping in the ribosome tunnel. PLoS Comput Biol 2:e98.
23. Dobson CM (2003) Protein folding and misfolding. Nature 426:884-890.
24. Hsu ST, et al. (2007) Structure and dynamics of a ribosome-bound nascent chain by NMR spectroscopy. Proc Natl Acad Sci USA 104:16516-16521.
25. Evans MS, Ugrinov KG, Frese MA, Clark PL (2005) Homogeneous stalled ribosome nascent chain complexes produced in vivo or in vitro. Nat Methods 2:757-762.
26. Schaffitzel C, Ban N(2007) Generation of ribosome nascent chain complexes for structural and functional studies. J Struct Biol 159:302-310.
27. Rutkowska A, et al. (2008) Dynamics of trigger factor interaction with translating ribosomes. J Biol Chem 283:4124-4132.
28. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207-234.
29. Nakatogawa H, Ito K (2002) The ribosomal exit tunnel functions as a discriminating gate. Cell 108:629-636.
30. Ou J, et al. (2004) Stationary phase protein overproduction is a fundamental capability of Escherichia coli. Biochem Biophys Res Commun 314:174-180.
31. Yoshida H, Yamamoto H, Uchiumi T, Wada A (2004) RMF inactivates ribosomes by covering the peptidyl transferase centre and entrance of peptide exit tunnel. Genes Cells 9:271-278.
32. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645.
33. Schanda P, Kupce E, Brutscher B (2005) SOFAST-HMQC experiments for recording twodimensional heteronuclear correlation spectra of proteins within a few seconds. J Biomol NMR 33:199-211.
34. Hsu ST, et al. (2009) Probing side-chain dynamics of a ribosome-bound nascent chain using methyl NMR spectroscopy. J Am Chem Soc 131:8366-8367.
35. Christodoulou J, et al. (2004) Heteronuclear NMR investigations of dynamic regions of intact E. coli ribosomes. Proc Natl Acad Sci USA 101:10949-10954.
36. Mulder FA, et al. (2004) Conformation and dynamics of ribosomal stalk protein L12 in solution and on the ribosome. Biochemistry 43:5930-5936.
37. McCoy AJ, Fucini P, Noegel AA, Stewart M(1999) Structural basis for dimerization of the Dictyostelium gelation factor (ABP120) rod. Nat Struct Biol 6:836-841.
38. Harpaz Y, Chothia C (1994) Many of the immunoglobulin superfamily domains in cell adhesion molecules and surface receptors belong to a new structural set which is close to that containing variable domains. J Mol Biol 238:528-539.
39. Fowler SB, et al. (2002) Mechanical unfolding of a titin Ig domain: Structure of unfolding intermediate revealed by combining AFM, molecular dynamics simulations, NMR and protein engineering. J Mol Biol 322:841-849.
40. Sauer FG, et al. (1999) Structural basis of chaperone function and pilus biogenesis. Science 285:1058-1061.
41. Cavalli A, Salvatella X, Dobson CM, Vendruscolo M(2007) Protein structure determination from NMR chemical shifts. Proc Natl Acad Sci USA 104:9615-9620.
42. Shen Y, et al. (2008) Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci USA 105:4685-4690.
43. Ferrage F, et al. (2003) Slow diffusion of macromolecular assemblies by a new pulsed field gradient NMR method. J Am Chem Soc 125:2541-2545.
44. Hsu S-TD, et al. (2009) Structure, dynamics and folding of an immunoglobulin domain of the gelation factor (ABP-120) from Dictyostelium discoideum. J Mol Biol 388:865-879.