Structural characterization of a eukaryotic chaperone-the ribosome-associated complex

Nature Structural and Molecular Biology

Volumn 20, Issue 1, 2013, Pages 23-28

  Leidig, Christoph ^a   Bange, Gert ^b   Kopp, Jürgen ^b   Amlacher, Stefan ^b   Aravind, Ajay ^b   Wickles, Stephan ^a   Witte, Gregor ^a   Hurt, Ed ^b   Beckmann, Roland ^a   Sinning, Irmgard ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ARGININE; ASPARAGINE; ERJ1 PROTEIN; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; MAGNESIUM ION; PROTEIN; RIBOSOME PROTEIN; SSZ1 PROTEIN; THREONINE; UNCLASSIFIED DRUG; ZUO1 PROTEIN;

ALPHA HELIX; ARTICLE; CATALYSIS; CHAETOMIUM THERMOPHILUM; ENDOPLASMIC RETICULUM; FUNGUS; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RIBOSOME ASSOCIATED COMPLEX; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CHAETOMIUM; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; FUNGAL PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RIBOSOMAL PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

CHAETOMIUM THERMOPHILUM; EUKARYOTA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84872010820     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2447     Document Type: Article

References (53)

1. Preissler, S. & Deuerling, E. Ribosome-associated chaperones as key players in proteostasis. Trends Biochem. Sci. 37, 274-283 (2012).
2. Kramer, G., Boehringer, D., Ban, N. & Bukau, B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589-597 (2009).
3. Lowther, W. T. & Matthews, B. W. Structure and function of the methionine aminopeptidases. Biochim. Biophys. Acta 1477, 157-167 (2000).
4. Polevoda, B. & Sherman, F. Composition and function of the eukaryotic N-terminal acetyltransferase subunits. Biochem. Biophys. Res. Commun. 308, 1-11 (2003).
5. Grudnik, P., Bange, G. & Sinning, I. Protein targeting by the signal recognition particle. Biol. Chem. 390, 775-782 (2009).
6. Cross, B. C., Sinning, I., Luirink, J. & High, S. Delivering proteins for export from the cytosol. Nat. Rev. Mol. Cell Biol. 10, 255-264 (2009).
7. Gautschi, M. et al. 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 (2001).
8. Hartl, F. U. & Hayer-Hartl, M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16, 574-581 (2009).
9. Bukau, B., Weissman, J. & Horwich, A. Molecular chaperones and protein quality control. Cell 125, 443-451 (2006).
10. Kampinga, H. H. & Craig, E. A. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 11, 579-592 (2010).
11. Gautschi, M., Mun, A., Ross, S. & Rospert, S. A functional chaperone triad on the yeast ribosome. Proc. Natl. Acad. Sci. USA 99, 4209-4214 (2002).
12. Otto, H. et al. The chaperones MPP11 and Hsp70L1 form the mammalian ribosome-associated complex. Proc. Natl. Acad. Sci. USA 102, 10064-10069 (2005).
13. Huang, P., Gautschi, M., Walter, W., Rospert, S. & Craig, E. A. The Hsp70 Ssz1 modulates the function of the ribosome-associated J-protein Zuo1. Nat. Struct. Mol. Biol. 12, 497-504 (2005).
14. Yan, W. et al. Zuotin, a ribosome-associated DnaJ molecular chaperone. EMBO J. 17, 4809-4817 (1998).
15. Koplin, A. et al. A dual function for chaperones SSB-RAC and the NAC nascent polypeptide-associated complex on ribosomes. J. Cell Biol. 189, 57-68 (2010).
16. Albanèse, V., Reissmann, S. & Frydman, J. A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis. J. Cell Biol. 189, 69-81 (2010).
17. Karbstein, K. Chaperoning ribosome assembly. J. Cell Biol. 189, 11-12 (2010).
18. Amlacher, S. et al. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146, 277-289 (2011).
19. Fiaux, J. et al. Structural analysis of the ribosome-associated complex (RAC) reveals an unusual Hsp70/Hsp40 interaction. J. Biol. Chem. 285, 3227-3234 (2010).
20. Holm, L. & Sander, C. Dali: a network tool for protein structure comparison. Trends Biochem. Sci. 20, 478-480 (1995).
21. Mourão, A., Varrot, A., Mackereth, C. D., Cusack, S. & Sattler, M. Structure and RNA recognition by the snRNA and snoRNA transport factor PHAX. RNA 16, 1205-1216 (2010).
22. Peisker, K. et al. Ribosome-associated complex binds to ribosomes in close proximity of Rpl31 at the exit of the polypeptide tunnel in yeast. Mol. Biol. Cell 19, 5279-5288 (2008).
23. O'Brien, M. C., Flaherty, K. M. & McKay, D. B. Lysine 71 of the chaperone protein Hsc70 Is essential for ATP hydrolysis. J. Biol. Chem. 271, 15874-15878 (1996).
24. Sousa, M. C. & McKay, D. B. The hydroxyl of threonine 13 of the bovine 70-kDa heat shock cognate protein is essential for transducing the ATP-induced conformational change. Biochemistry 37, 15392-15399 (1998).
25. Johnson, E. R. & McKay, D. B. Mapping the role of active site residues for transducing an ATP-induced conformational change in the bovine 70-kDa heat shock cognate protein. Biochemistry 38, 10823-10830 (1999).
26. Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372 (2001).
27. Nilsson, J., Sengupta, J., Gursky, R., Nissen, P. & Frank, J. Comparison of fungal 80S ribosomes by cryo-EM reveals diversity in structure and conformation of rRNA expansion segments. J. Mol. Biol. 369, 429-438 (2007).
28. Armache, J. P. et al. Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5. 5-Å resolution. Proc. Natl. Acad. Sci. USA 107, 19748-19753 (2010).
29. Melnikov, S. et al. One core, two shells: bacterial and eukaryotic ribosomes. Nat. Struct. Mol. Biol. 19, 560-567 (2012).
30. Blau, M. et al. ERj1p uses a universal ribosomal adaptor site to coordinate the 80S ribosome at the membrane. Nat. Struct. Mol. Biol. 12, 1015-1016 (2005).
31. Preissler, S. & Deuerling, E. Ribosome-associated chaperones as key players in proteostasis. Trends Biochem. Sci. 37, 274-283 (2012).
32. Schlenker, O., Hendricks, A., Sinning, I. & Wild, K. The structure of the mammalian signal recognition particle (SRP) receptor as prototype for the interaction of small GTPases with Longin domains. J. Biol. Chem. 281, 8898-8906 (2006).
33. Rakwalska, M. & Rospert, S. The ribosome-bound chaperones RAC and Ssb1/2p are required for accurate translation in Saccharomyces cerevisiae. Mol. Cell Biol. 24, 9186-9197 (2004).
34. Rospert, S., Rakwalska, M. & Dubaquie, Y. Polypeptide chain termination and stop codon readthrough on eukaryotic ribosomes. Rev. Physiol. Biochem. Pharmacol. 155, 1-30 (2005).
35. Halic, M. et al. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427, 808-814 (2004).
36. Amlacher, S. et al. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146, 277-289 (2011).
37. Collaborative Computational Project, No. 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
38. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
39. Jia-Xing, Y., Woolfson, M. M., Wilson, K. S. & Dodson, E. J. A modified ACORN to solve protein structures at resolutions of 1. 7 Å or better. Acta Crystallogr. D Biol. Crystallogr. 61, 1465-1475 (2005).
40. Langer, G., Cohen, S. X., Lamzin, V. S. & Perrakis, A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179 (2008).
41. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
42. Girish, V. & Vijayalakshmi, A. Affordable image analysis using NIH Image/ImageJ. Indian J. Cancer 41, 47 (2004).
43. Wagenknecht, T., Grassucci, R. & Frank, J. Electron microscopy and computer image averaging of ice-embedded large ribosomal subunits from Escherichia coli. J. Mol. Biol. 199, 137-147 (1988).
44. Shaikh, T. R. et al. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc. 3, 1941-1974 (2008).
45. Norousi, R. et al. Automatic post-picking improves particle image detection from cryo-EM micrographs. Preprint at http://arxiv. org/abs/1112. 3173v2 (2011).
46. Penczek, P. A., Frank, J. & Spahn, C. M. A method of focused classification, based on the bootstrap 3D variance analysis, and its application to EF-G-dependent translocation. J. Struct. Biol. 154, 184-194 (2006).
47. Becker, T. et al. Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326, 1369-1373 (2009).
48. Putnam, C. D., Hammel, M., Hura, G. L. & Tainer, J. A. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q. Rev. Biophys. 40, 191-285 (2007).
49. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. & Svergun, D. I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282 (2003).
50. Svergun, D. I., Petoukhov, M. V. & Koch, M. H. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80, 2946-2953 (2001).
51. Volkov, V. V. & Svergun, D. I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864 (2003).
52. Wriggers, W. Using Situs for the integration of multi-resolution structures. Biophys. Rev. 2, 21-27 (2010).
53. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).