Access to ribosomal protein Rpl25p by the signal recognition particle is required for efficient cotranslational translocation

Molecular Biology of the Cell

Volumn 19, Issue 7, 2008, Pages 2876-2884

  Dalley, Jane A ^a,b   Selkirk, Alexander ^a   Pool, Martin R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY HOSPITAL OF NORTH STAFFORDSHIRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MUTANT PROTEIN; PROTEIN RP125P; RIBOSOME PROTEIN; SIGNAL RECOGNITION PARTICLE; TRANSLOCON; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL FRACTIONATION; CELL GROWTH; CELL STRESS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE OVEREXPRESSION; GENE TRANSLOCATION; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TARGETING; RIBOSOME; RNA TRANSLATION; UPREGULATION;

ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, FUNGAL; GENES, DOMINANT; GREEN FLUORESCENT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; MUTATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RIBOSOMAL PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SIGNAL RECOGNITION PARTICLE; SUBCELLULAR FRACTIONS;

EID: 51349087640     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-10-1074     Document Type: Article

References (57)

1. Albanèse, V., Yam, A. Y., Baughman, J., Parnot, C., and Frydman, J. (2006). Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 124, 75-88.
2. Arnold, C. E., and Wittrup, K. D. (1994). The stress response to loss of signal recognition particle function in Saccharomyces cerevisiae. J. Biol. Chem. 269, 30412-30418.
3. Bacher, G., Lütcke, H., Jungnickel, B., Rapoport, T. A., and Dobberstein, B. (1996). Regulation by the ribosome of the GTPase of the signal recognition particle during protein targeting. Nature 381, 248-251.
4. Beckmann, R., Spahn, C.M.T., Eswar, N., Helmers, J., Penczek, P. A., Sall, A., Frank, J., and Blobel, G. (2001). Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372.
5. Buskiewicz, I., Deuerling, E., Gu, S. Q., Jockel, J., Rodnina, M. V., Bukau, B., and Wintermeyer, W. (2004). 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, 7902-7906.
6. Chapman, R. E., and Munro, S. (1994). The functioning of the yeast Golgi apparatus requires an ER protein encoded by ANP1, a member of a new family of genes affecting the secretory pathway. EMBO J. 13, 4896-4907.
7. Deshaies, R. J., and Schekman, R. (1989). SEC62 encodes a putative membrane protein required for protein translocation into the yeast endoplasmic reticulum. J. Cell Biol. 109, 2653-2664.
8. Frey, S., Pool, M., and Seedorf, M. (2001). Scp160p, an RNA-binding, polysome-associated protein, localizes to the endoplasmic reticulum of Saccharomyces cerevisiae in a microtubule-dependent manner. J. Biol. Chem. 276, 15905-15912.
9. Gautschi, M., Lilie, H., Funfschilling, U., Mun, A., Ross, S., Lithgow, T., Rucknagel, P., and Rospert, S. (2001). RAC, a stable ribosome-associated complex in yeast formed by the DnaK-DnaJ homologs Ssz1p and zuotin. Proc. Natl. Acad. Sci. USA 98, 3762-3767.
10. Gautschi, M., Mun, A., Ross, S., and Rospert, S. (2002). A functional chaperone triad on the yeast ribosome. Proc. Natl. Acad. Sci. USA 99, 4209-4214.
11. Gilmore, R., Walter, P., and Blobel, G. (1982). Protein translocation across the endoplasmic reticulum. II. Isolation and characterization of the signal recognition particle receptor. J. Cell Biol. 95, 470-477.
12. Gu, S. Q., Peske, F., Wieden, H. J., Rodnina, M. V., and Wintermeyer, W. (2003). The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome. RNA 9, 566-573.
13. Halic, M., Becker, T., Pool, M. R., Spahn, C. M., Grassucci, R. A., Frank, J., and Beckmann, R. (2004). Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427, 808-814.
14. Halic, M., Blau, M., Becker, T., Mielke, T., Pool, M. R., Wild, K., Sinning, I., and Beckmann, R. (2006a). Following the signal sequence from ribosomal tunnel exit to signal recognition particle. Nature 444, 507-511.
15. Halic, M., Gartmann, M., Schlenker, O., Mielke, T., Pool, M. R., Sinning, I., and Beckmann, R. (2006b). Signal recognition particle receptor exposes the ribosomal translocon binding site. Science 312, 745-747.
16. Hurt, E., Hannus, S., Schmelzl, B., Lau, D., Tollervey, D., and Simos, G. (1999). A novel in vivo assay reveals inhibition of ribosomal nuclear export in Ran-cycle and nuceleoporin mutants. J. Cell Biol. 144, 389-401.
17. Inada, T., Winstall, E., Tarun, S. Z., Yates, J. R., Schieltz, D., and Sachs, A. B. (2002). One-step affinity purification of the yeast ribosome and its associated proteins and mRNAs. RNA 8, 948-958.
18. Jermy, A. J., Willer, M., Davis, E., Wilkinson, B. M., and Stirling, C. J. (2006). The Brl domain in Sec63p is required for assembly of functional endoplasmic reticulum translocons. J. Biol. Chem. 281, 7899-7906.
19. Jungnickel, B., and Rapoport, T. A. (1995). A posttargeting signal sequence recognition event in the endoplasmic reticulum membrane. Cell 82, 261-270.
20. Kalies, K.-U., Görlich, D., and Rapoport, T. A. (1994). Binding of ribosomes to the rough endoplasmic reticulum mediated by the Sec61p-complex. J. Cell Biol. 126, 925-934.
21. Keenan, R. J., Freymann, D. M., Stroud, R. M., and Walter, P. (2001). The signal recognition particle. Annu. Rev. Biochem. 70, 755-775.
22. Kooi, E. A., Rutgers, C. A., Kleijmer, M. J., van't Riet, J., and Raué, H.A. (1994). Mutational analysis of the C-terminal region of Saccharomyces cerevisiae ribosomal protein L25 in vivo and in vitro demonstrates the presence of two distinct functional elements. J. Mol. Biol. 240, 243-255.
23. Kramer, G., Rauch, T., Rist, W., Vorderwulbecke, S., Patzelt, H., Schulze-Specking, A., Ban, N., Deuerling, E., and Bukau, B. (2002). L23 protein functions as a chaperone docking site on the ribosome. Nature 419, 171-174.
24. Mason, N., Ciufo, L. F., and Brown, J. D. (2000). Elongation arrest is a physiologically important function of the signal recognition particle. EMBO J. 19, 4164-4174.
25. Menetret, J. F., Hegde, R. S., Heinrich, S. U., Chandramouli, P., Ludtke, S. J., Rapoport, T. A., and Akey, C. W. (2005). Architecture of the ribosome-channel complex derived from native membranes. J. Mol. Biol. 348, 445-457.
26. Meyer, D. I., Louvard, D., and Dobberstein, B. (1982). Characterization of molecules involved in protein translocation using a specific antibody. J. Cell Biol. 92, 579-583.
27. Mitra, K., Schaffitzel, C., Shaikh, T., Tama, F., Jenni, S., Brooks, C. L., 3rd, Ban, N., and Frank, J. (2005). Structure of the E. coli protein-conducting channel bound to a translating ribosome. Nature 438, 318-324.
28. Mutka, S. C., and Walter, P. (2001). Multifaceted physiological response allows yeast to adapt to the loss of the signal recognition particle-dependent protein-targeting pathway. Mol. Biol. Cell 12, 577-588.
29. Ng, D. T., Brown, J. D., and Walter, P. (1996). Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134, 269-278.
30. Nissen, P., Hansen, J., Ban, N., Moore, P. B., and Steitz, T. A. (2000). The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920-930.
31. Ogg, S. C., Barz, W. P., and Walter, P. (1998). A functional GTPase domain, but not its transmembrane domain, is required for function of the SRP receptor beta-subunit. J. Cell Biol. 142, 341-354.
32. Osborne, A. R., Rapoport, T. A., and van den Berg, B. (2005). Protein translocation by the Sec61/SecY channel. Annu. Rev. Cell Dev. Biol. 21, 529-550.
33. Panzner, S., Dreier, L., Hartmann, E., Kostka, S., and Rapoport, T. A. (1995). Posttranslational protein translocation in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 81, 561-570.
34. Pfund, C., Lopez-Hoyo, N., Ziegelhoffer, T., Schilke, B. A., Lopez-Buesa, P., Walter, W. A., Wiedmann, M., and Craig, E. A. (1998). The molecular chaperone Ssb from Saccharomyces cerevisiae is a component of the ribosomenascent chain complex. EMBO J. 17, 3981-3989.
35. Pool, M. R. (2005). Signal recognition particles in chloroplasts, bacteria, yeast and mammals (review). Mol. Membr. Biol. 22, 3-15.
36. Pool, M. R., Stumm, J., Fulga, T. A., Sinning, I., and Dobberstein, B. (2002). Distinct modes of signal recognition particle interaction with the ribosome. Science 297, 1345-1348.
37. Prinz, A., Behrens, C., Rapoport, T. A., Hartmann, E., and Kalies, K. U. (2000). Evolutionarily conserved binding of ribosomes to the translocation channel via the large ribosomal RNA. EMBO J. 19, 1900-1906.
38. Reimann, B., Bradsher, J., Franke, J., Hartmann, E., Wiedmann, M., Prehn, S., and Wiedmann, B. (1999). Initial characterization of the nascent polypeptide-associated complex in yeast. Yeast 15, 397-407.
39. Rothblatt, J. A., Deshaies, R. J., Sanders, S. L., Daum, G., and Schekman, R. (1989). Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum in yeast. J. Cell Biol. 109, 2641-2652.
40. Ruegsegger, U., Leber, J. H., and Walter, P. (2001). Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107, 103-114.
41. Sachs, A. B., and Davis, R. W. (1989). The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell 58, 857-867.
42. Sachs, A. B., and Davis, R. W. (1990). Translation initiation and ribosomal biogenesis: involvement of a putative rRNA helicase and RPL46. Science 247, 1077-1079.
43. Schaffitzel, C., Oswald, M., Berger, I., Ishikawa, T., Abrahams, J. P., Koerten, H. K., Koning, R. I., and Ban, N. (2006). Structure of the E. coli signal recognition particle bound to a translating ribosome. Nature 444, 503-506.
44. Segref, A., Sharma, K., Doye, V., Hellwig, A., Huber, J., Luhrmann, R., and Hurt, E. (1997). Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J. 16, 3256-3271.
45. Siegel, V., and Walter, P. (1985). Elongation arrest is not a prerequisite for secretory protein translocation across the microsomal membrane. J. Cell Biol. 100, 1913-1921.
46. Song, W., Raden, D., Mandon, E. C., and Gilmore, R. (2000). Role of Sec61a in the regulated transfer of the ribosome-nascent chain complex from the signal recognition particle to the translocation channel. Cell 100, 333-343.
47. Sorger, P. K. (1991). Heat shock factor and the heat shock response. Cell 65, 363-366.
48. Stirling, C. J., Rothblatt, J., Hosobuchi, M., Deshaies, R., and Schekman, R. (1992). Protein translocation mutants defective in the insertion of integral membrane proteins into the endoplasmic reticulum. Mol. Biol. Cell 3, 129-142.
49. Terzi, L., Pool, M. R., Dobberstein, B., and Strub, K. (2004). Signal recognition particle Alu domain occupies a defined site at the ribosomal subunit interface upon signal sequence recognition. Biochemistry 43, 107-117.
50. Wegrzyn, R. D., Hofmann, D., Merz, F., Nikolay, R., Rauch, T., Graf, C., and Deuerling, E. (2006). A conserved motif is prerequisite for the interaction of NAC with ribosomal protein L23 and nascent chains. J. Biol. Chem. 281, 2847-2857.
51. Wiedmann, B., Sakai, H., Davis, T. A., and Wiedmann, M. (1994). A protein complex required for signal-sequence-specific sorting and translocation. Nature 370, 434-440.
52. Wild, K., Halic, M., Sinning, I., and Beckmann, R. (2004). SRP meets the ribosome. Nat. Struct. Mol. Biol. 11, 1049-1053.
53. Wilkinson, B. M., Purswani, J., and Stirling, C. J. (2006). Yeast GTB1 encodes a subunit of glucosidase II required for glycoprotein processing in the endoplasmic reticulum. J. Biol. Chem. 281, 6325-6333.
54. Wilkinson, B. M., Regnacq, M., and Stirling, C. J. (1997). Protein translocation across the membrane of the endoplasmic reticulum. J. Membr. Biol. 155, 189-197.
55. Willer, M., Jermy, A. J., Steel, G. J., Garside, H. J., Carter, S., and Stirling, C. J. (2003). An in vitro assay using overexpressed yeast SRP demonstrates that cotranslational translocation is dependent upon the J-domain of Sec63p. Biochemistry 42, 7171-7177.
56. Winzeler, E. A. et al. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
57. Woolhead, C. A., McCormick, P. J., and Johnson, A. E. (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.