The Geometry of the Ribosomal Polypeptide Exit Tunnel

Journal of Molecular Biology

Volumn 360, Issue 4, 2006, Pages 893-906

  Voss, N R ^a   Gerstein, M ^a   Steitz, T A ^a,b   Moore, P B ^a  

^a YALE UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

exit tunnel; geometry; ribosome; solvent content

Indexed keywords

PEPTIDYLTRANSFERASE; POLYPEPTIDE; TRANSLOCON; WATER;

ALPHA HELIX; ARTICLE; GEOMETRY; HALOARCULA MARISMORTUI; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RIBOSOME SUBUNIT;

HALOARCULA MARISMORTUI;

EID: 33745628037     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.05.023     Document Type: Article

References (56)

1. Frank J., Zhu J., Penczek P., Li Y., Srivastava S., Verschoor A., et al. A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature 376 (1995) 441-444
2. Bernabeu C., and Lake J.A. Nascent polypeptide chains emerge from the exit domain of the large ribosomal subunit: immune mapping of the nascent chain. Proc. Natl Acad. Sci. USA 79 (1982) 3111-3115
3. Ban N., Nissen P., Hansen J., Moore P.B., and Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289 (2000) 905-920
4. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., et al. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107 (2001) 679-688
5. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H. Structures of the bacterial ribosome at 3.5 A resolution. Science 310 (2005) 827-834
6. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H., and Noller H.F. Crystal structure of the ribosome at 5.5 A resolution. Science 292 (2001) 883-896
7. Ban N., Nissen P., Hansen J., Capel M., Moore P.B., and Steitz T.A. Placement of protein and RNA structures into a 5 A-resolution map of the 50S ribosomal subunit. Nature 400 (1999) 841-847
8. Nakatogawa H., and Ito K. The ribosomal exit tunnel functions as a discriminating gate. Cell 108 (2002) 629-636
9. Nakatogawa H., Murakami A., and Ito K. Control of SecA and SecM translation by protein secretion. Curr. Opin. Microbiol. 7 (2004) 145-150
10. Tenson T., and Ehrenberg M. Regulatory nascent peptides in the ribosomal tunnel. Cell 108 (2002) 591-594
11. Gong F., and Yanofsky C. Instruction of translating ribosome by nascent peptide. Science 297 (2002) 1864-1867
12. Hansen J.L., Moore P.B., and Steitz T.A. Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J. Mol. Biol. 330 (2003) 1061-1075
13. Agmon I., Auerbach T., Baram D., Bartels H., Bashan A., Berisio R., et al. On peptide bond formation, translocation, nascent protein progression and the regulatory properties of ribosomes. Derived on 20 October 2002 at the 28th FEBS Meeting in Istanbul. Eur. J. Biochem. 270 (2003) 2543-2556
14. Nissen P., Hansen J., Ban N., Moore P.B., and Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science 289 (2000) 920-930
15. Baram D., Pyetan E., Sittner A., Auerbach-Nevo T., Bashan A., and Yonath A. Structure of trigger factor binding domain in biologically homologous complex with eubacterial ribosome reveals its chaperone action. Proc. Natl Acad. Sci. USA 102 (2005) 12017-12022
16. Mitra K., Schaffitzel C., Shaikh T., Tama F., Jenni S., Brooks III C.L., et al. Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438 (2005) 318-324
17. Zengel J.M., Jerauld A., Walker A., Wahl M.C., and Lindahl L. The extended loops of ribosomal proteins L4 and L22 are not required for ribosome assembly or L4-mediated autogenous control. RNA 9 (2003) 1188-1197
18. Gabashvili I.S., Gregory S.T., Valle M., Grassucci R., Worbs M., Wahl M.C., et al. The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol. Cell. 8 (2001) 181-188
19. Gilbert R.J., Fucini P., Connell S., Fuller S.D., Nierhaus K.H., Robinson C.V., et al. Three-dimensional structures of translating ribosomes by Cryo-EM. Mol. Cell. 14 (2004) 57-66
20. Pal S., Chandra S., Chowdhury S., Sarkar D., Ghosh A.N., and Gupta C.D. Complementary role of two fragments of domain V of 23 S ribosomal RNA in protein folding. J. Biol. Chem. 274 (1999) 32771-32777
21. Liao S., Lin J., Do H., and Johnson A.E. Both lumenal and cytosolic gating of the aqueous ER translocon pore are regulated from inside the ribosome during membrane protein integration. Cell 90 (1997) 31-41
22. Kleywegt, G. J., Zou, J. Y., Kjeldgaard, M. & Jones, T.A. (2001). Around O. In International Tables for Crystallography, Vol. F. Crystallography of Biological Macromolecules (Rossman, M. G. E. A., ed), pp. 353-356, 366-367. Kluwer Academic Publishers, The Netherlands (2001).
23. Kleywegt G.J., and Jones T.A. Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallog. sect. D 50 (1994) 178-185
24. Laskowski R.A. SurfNET - a program for visualizing molecular-surfaces, cavities, and intermolecular interactions. J. Mol. Graph. 13 (1995) 323-330
25. Bakowies D., and van Gunsteren W.F. Water in protein cavities: a procedure to identify internal water and exchange pathways and application to fatty acid-binding protein. Proteins: Struct. Funct. Genet. 47 (2002) 534-545
26. Liang J., Edelsbrunner H., and Woodward C. Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design. Protein Sci. 7 (1998) 1884-1897
27. Laskowski R.A., Luscombe N.M., Swindells M.B., and Thornton J.M. Protein clefts in molecular recognition and function. Protein Sci. 5 (1996) 2438-2452
28. Smart O.S., Goodfellow J.M., and Wallace B.A. The pore dimensions of gramicidin A. Biophys. J. 65 (1993) 2455-2460
29. Richards F.M. Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6 (1977) 151-176
30. Taylor T.C., and Andersson I. The structure of the complex between rubisco and its natural substrate ribulose 1,5-bisphosphate. J. Mol. Biol. 265 (1997) 432-444
31. Richards F.M. The interpretation of protein structures: total volume, group volume distributions and packing density. J. Mol. Biol. 82 (1974) 1-14
32. Malkin L.I., and Rich A. Partial resistance of nascent polypeptide chains to proteolytic digestion due to ribosomal shielding. J. Mol. Biol. 26 (1967) 329-346
33. Hardesty B., and Kramer G. Folding of a nascent peptide on the ribosome. Prog Nucl. Acid Res. Mol. Biol. 66 (2001) 41-66
34. Lu J., and Deutsch C. Folding zones inside the ribosomal exit tunnel. Nature Struct. Mol. Biol. 12 (2005) 1123-1129
35. Woolhead C.A., McCormick P.J., and Johnson A.E. 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
36. Ziv G., Haran G., and Thirumalai D. Ribosome exit tunnel can entropically stabilize alpha-helices. Proc. Natl Acad. Sci. USA 102 (2005) 18956-18961
37. Wei Z.Y., Dickman M.H., and Pope M.T. New routes for multiple derivatization of polyoxometalates, bis(acetato)dirhodium-11-tungstophosphate, [(PO4)W11O35{Rh-2(OAc)(2)}](5-). Inorg. Chem. 36 (1997) 130-131
38. Ban N., Freeborn B., Nissen P., Penczek P., Grassucci R.A., Sweet R., et al. A 9 A resolution X-ray crystallographic map of the large ribosomal subunit. Cell 93 (1998) 1105-1115
39. Ditzel L., Lowe J., Stock D., Stetter K.O., Huber H., Huber R., and Steinbacher S. Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93 (1998) 125-138
40. Van Coppenolle F., Vanden Abeele F., Slomianny C., Flourakis M., Hesketh J., Dewailly E., and Prevarskaya N. Ribosome-translocon complex mediates calcium leakage from endoplasmic reticulum stores. J. Cell Sci. 117 (2004) 4135-4142
41. Marcus Y. Ion solvation (1985), Wiley, Chichester, New York
42. Menetret J.F., Hegde R.S., Heinrich S.U., Chandramouli P., Ludtke S.J., Rapoport T.A., and Akey C.W. Architecture of the ribosome-channel complex derived from native membranes. J. Mol. Biol. 348 (2005) 445-457
43. Adams P.L., Stahley M.R., Kosek A.B., Wang J., and Strobel S.A. Crystal structure of a self-splicing group I intron with both exons. Nature 430 (2004) 45-50
44. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The protein data bank. Nucl. Acids Res. 28 (2000) 235-242
45. Klein D.J., Schmeing T.M., Moore P.B., and Steitz T.A. The kink-turn: a new RNA secondary structure motif. EMBO J. 20 (2001) 4214-4221
46. Ogle J.M., Murphy F.V., Tarry M.J., and Ramakrishnan V. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111 (2002) 721-732
47. Edayathumangalam R.S., Weyermann P., Gottesfeld J.M., Dervan P.B., and Luger K. Molecular recognition of the nucleosomal "supergroove". Proc. Natl Acad. Sci. USA 101 (2004) 6864-6869
48. Ellenberger T.E., Brandl C.J., Struhl K., and Harrison S.C. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein-DNA complex. Cell 71 (1992) 1223-1237
49. Soroka V., Kolkova K., Kastrup J.S., Diederichs K., Breed J., Kiselyov V.V., et al. Structure and interactions of NCAM Ig1-2-3 suggest a novel zipper mechanism for homophilic adhesion. Structure 11 (2003) 1291-1301
50. Word J.M., Lovell S.C., Richardson J.S., and Richardson D.C. Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation. J. Mol. Biol. 285 (1999) 1735-1747
51. Sanner M.F., Olson A.J., and Spehner J.C. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38 (1996) 305-320
52. Gerstein M., and Richards F.M. Protein geometry: distances, areas, and volumes. In: Rossmann M., and Arnold E. (Eds). International Tables for Crystallography. Crystallography of Biological Macromolecules vol. F (2001), Springer, Dordrecht 531-539
53. Sanner M., Olson A.J., and Spehner J.C. Fast and robust computation of molecular surfaces. Proc. 11th ACM Symp. Comp. Geom. (1995) C1-C7
54. Kleywegt G.J., and Jones T.A. xdlMAPMAN and xdlDATAMAN-Programs for reformatting, analysis and manipulation of biomacromolecular electron-density maps and reflection data sets. Acta Crystallogr. Sect. D 52 (1996) 826-828
55. DeLano W.L. The PyMOL Molecular Graphics System 0.95 edit (2002), DeLano Scientific, San Carlos, CA, USA. http://www.pymol.org http://www.pymol.org
56. Thoden J.B., Miran S.G., Phillips J.C., Howard A.J., Raushel F.M., and Holden H.M. Carbamoyl phosphate synthetase: caught in the act of glutamine hydrolysis. Biochemistry 37 (1998) 8825-8831