Structure of the signal recognition particle interacting with the elongation-arrested ribosome

Nature

Volumn 427, Issue 6977, 2004, Pages 808-814

  Halic, Mario ^a   Becker, Thomas ^a   Pool, Martin R ^b   Spahn, Christian M T ^a   Grassucci, Robert A ^c,d   Frank, Joachim ^c,d   Beckmann, Roland ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; ELECTRON MICROSCOPY; MOLECULAR DYNAMICS; SIGNAL DETECTION;

RIBOSOMES; SIGNAL RECOGNITION PARTICLES (SRP);

PROTEINS;

RIBONUCLEOPROTEIN; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE;

BIOLOGY;

ANIMAL; ARTICLE; BINDING SITE; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CRYOELECTRON MICROSCOPY; GENETICS; MAMMAL; MEMBRANE TRANSPORT; METABOLISM; MOLECULAR GENETICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; RIBOSOME; RNA TRANSLATION; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

ANIMALS; BASE SEQUENCE; BINDING SITES; CRYOELECTRON MICROSCOPY; MAMMALS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RIBOSOMES; SIGNAL RECOGNITION PARTICLE; STRUCTURE-ACTIVITY RELATIONSHIP;

ANIMALIA; MAMMALIA;

EID: 1542319100     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature02342     Document Type: Article

References (50)

1. Blobel, G. & Sabatini, D. in Biomembranes (ed. Manson, L. A.) 193-195 (Plenum, New York, 1971).
2. Walter, P., Ibrahimi, I. & Blobel, G. Translocation of proteins across the endoplasmic reticulum. 1. Signal recognition protein (SRP) binds to in-vitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91, 545-550 (1981).
3. Koch, H. G., Moser, M. & Muller, M. Signal recognition particle-dependent protein targeting, universal to all kingdoms of life. Rev. Physiol. Biochem. Pharmacol. 146, 55-94 (2003).
4. Gundelfinger, E. D., Krause, E., Melli, M. & Dobberstein, B. The organization of the 7SL RNA in the signal recognition particle. Nucleic Acids Res. 11, 7363-7374 (1983).
5. Siegel, V. & Walter, P. Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: analysis of biochemical mutants of SRP. Cell 52, 39-49 (1988).
6. Walter, P. & Blobel, G. Disassembly and reconstitution of signal recognition particle. Cell 34, 525-533 (1983).
7. Connolly, T. & Gilmore, R. The signal recognition particle receptor mediates the GTP-dependent displacement of SRP from the signal sequence of the nascent polypeptide. Cell 57, 599-610 (1989).
8. Bernstein, H. D. et al. Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle. Nature 340, 482-486 (1989).
9. Romisch, K., Webb, J., Lingelbach, K., Gausepohl, H. & Dobberstein, B. The 54-kD protein of signal recognition particle contains a methionine-rich RNA binding domain. J. Cell Biol. 111, 1793-1802 (1990).
10. Batey, R. T., Rambo, R. P., Lucast, L., Rha, B. & Doudna, J. A. Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science 287, 1232-1239 (2000).
11. Zopf, D., Bernstein, H. D., Johnson, A. E. & Walter, P. The methionine-rich domain of the 54 kD protein subunit of the signal recognition particle contains an RNA binding site and can be crosslinked to a signal sequence. EMBO 1. 9, 4511-4517 (1990).
12. Pool, M. R., Stumm, J., Fulga, T. A., Sinning, I. & Dobberstein, B. Distinct modes of signal recognition particle interaction with the ribosome. Science 297, 1345-1348 (2002).
13. Siegel, V. & Walter, P. Removal of the Alu structural domain from signal recognition particle leaves its protein translocation activity intact. Nature 320, 81-34 (1986).
14. Walter, P. & Blobel, G. Translocation of proteins across the endoplasmic reticulum. III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol. 91, 557-561 (1981).
15. Wolin, S. L. & Walter, P. Signal recognition particle mediates a transient elongation arrest of preprolactin in reticulocyte lysate. J. Cell Biol. 109, 2617-2622 (1989).
16. Mason, N., Ciufo, L. F. & Brown, J. D. Elongation arrest is a physiologically important function of signal recognition particle. EMBO J. 19, 4164-4174 (2000).
17. Siegel, V. & Walter, P. Elongation arrest is not a prerequisite for secretory protein translocation across the microsomal membrane. J. Cell Biol. 100, 1913-1921 (1985).
18. Andrews, D. W., Walter, P. & Ottensmeyer, F. P. Evidence for an extended 7SL RNA structure in the signal recognition particle. EMBO J. 6, 3471-3477 (1987).
19. Nagai, K. et al. Structure, function and evolution of the signal recognition particle. EMBO J. 22, 3479-3485 (2003).
20. Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372 (2001).
21. Walter, P. & Blobel, G. Subcellular distribution of signal recognition particle and 7SL-RNA determined with polypeptide-specific antibodies and complementary DNA probe. J. Cell Biol. 97, 1693-1699 (1983).
22. Spahn, C. M. et al. Structure of the 80S ribosome from Saccharomyces cerevisiae tRNA-ribosome and subunit-subunit interactions. Cell 107, 373-386 (2001).
23. Kuglstatter, A., Oubridge, C. & Nagai, K. Induced structural changes of 7SL RNA during the assembly of human signal recognition particle. Nature Struct. Biol. 9, 740-744 (2002).
24. Huang, Q., Abdulrahman, S., Yin, J. & Zwieb, C. Systematic site-directed mutagenesis of human protein SRP54: interactions with signal recognition particle RNA and modes of signal peptide recognition. Biochemistry 41, 11362-11371 (2002).
25. Padmanabhan, S. & Freymann, D. M. The conformation of bound GMPPNP suggests a mechanism for gating the active site of the SRP GTPase. Struct. Fold. Des. 9, 859-867 (2001).
26. Rosendal, K. R., Wild, K., Montoya, G. & Sinning, I. Crystal structure of the complete core of archaeal signal recognition particle and implications for interdomain communication. Proc. Natl. Acad. Sci. USA 100, 14701-14706 (2003).
27. Siegel, V. & Walter, P. Binding sites of the 19-kDa and 68/72-kDa signal recognition particle (SRP) proteins on SRP RNA as determined in protein-RNA 'footprinting'. Proc. Natl. Acad. Sci. USA 85, 1801-1805 (1988).
28. Ban, N., Nissen, P., Hansen, I., Moore, P. B. & Steitz, T. A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905-920 (2000).
29. Weichenrieder, O., Wild, K., Strub, K. & Cusack, S. Structure and assembly of the Alu domain of the mammalian signal recognition particle. Nature 408, 167-173 (2000).
30. Rosenblad, M. A., Gorodkin, J., Knudsen, B., Zwieb, C. & Samuelsson, T. SRPDB: signal recognition particle database. Nucleic Acids Res. 31, 363-364 (2003).
31. Gu, S. Q., Peske, F., Wieden, H. J., Rodnina, M. V. & Wintermeyer, W. The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome. RNA 9, 566-573 (2003).
32. Eisner, G., Koch, H. G., Beck, K., Brunner, J. & Muller, M. Ligand crowding at a nascent signal sequence. J. Cell Biol. 163, 35-44 (2003).
33. Kramer, G. et al. L23 protein functions as a chaperone docking site on the ribosome. Nature 419, 171-174 (2002).
34. Ullers, R. S. et al. 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, 679-684 (2003).
35. Rinke-Appel, J. et al. Crosslinking of 4.5S RNA to the Escherichia coli ribosome in the presence or absence of the protein Ffh. RNA 8, 612-625 (2002).
36. Morgan, D. G., Menetret, J. F., Neuhof, A., Rapoport, T. A. & Akey, C. W. Structure of the mammalian ribosome-channel complex at 17 Å resolution. J. Mol. Biol. 324, 871-886 (2002).
37. Moller, I. et al. A general mechanism for regulation of access to the translocon: competition for a membrane attachment site on ribosomes. Proc. Natl. Acad. Sci. USA 95, 13425-13430 (1998).
38. Thomas, Y., Bui, N. & Strub, K. A truncation in the 14kDa protein of the signal recognition particle leads to tertiary structure changes in the RNA and abolishes the elongation arrest activity of the particle. Nucleic Acids Res. 25, 1920-1929 (1997).
39. Wilson, D. N. et al. Protein synthesis at atomic resolution: mechanistics of translation in the light of highly resolved structures for the ribosome. Curr. Protein Peptide Sci. 3, 1-53 (2002).
40. Gomez-Lorenzo, M. G. et al. Three-dimensional cryo-electron microscopy localization of EF2 in the Saccharomyces cerevisiae 80S ribosome at 17.5 Å resolution. EMBO J. 19, 2710-2718 (2000).
41. Spahn, C. et al. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. (in the press).
42. Valle, M. et al. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nature Struct. Biol. 10, 899-906 (2003).
43. Wolin, S. L. & Walter, P. Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J. 7, 3559-3569 (1988).
44. Ogg, S. C. & Walter, P. SRP samples nascent chains for the presence of signal sequences by interacting with ribosomes at a discrete step during translation elongation. Cell 81, 1075-1084 (1995).
45. Andreazzoli, M. & Gerbi, S. A. Changes in 7SL RNA conformation during the signal recognition particle cycle. EMBO J. 10, 767-777 (1991).
46. Martoglio, B., Hauser, S. & Dobberstein, B. in Cell Biology: A Laboratory Handbook (ed. Celis, J. C.) 265-273 (Academic, San Diego, 1997).
47. Walter, P. & Blobel, G. Signal recognition particle: a ribonucleoprotein required for cotranslational translocation of proteins, isolation and properties. Methods Enzymol. 96, 682-691 (1983).
48. Wagenknecht, T., Grassucci, R. & Frank, I. Electron microscopy and computer image averaging of ice-embedded large ribosomal subunits from Escherichia coli. J. Mol. Biol. 199, 137-147 (1988).
49. Jones, T. A., Zhou, J. Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
50. Carson, M. Ribbons 2.0. Appl. Crystallogr. 24, 103-106 (1991).