Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM

Nature Structural and Molecular Biology

Volumn 11, Issue 10, 2004, Pages 957-962

  Sengupta, Jayati ^a   Nilsson, Jakob ^d   Gursky, Richard ^b   Spahn, Christian M T ^e   Nissen, Poul ^d   Frank, Joachim ^b,c  

^a WADSWORTH CENTER   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d AARHUS UNIVERSITY   (Denmark)

^e HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MEMBRANE RECEPTOR; MESSENGER RNA; PROTEIN KINASE; PROTEIN KINASE C; PROTEIN RACK1; UNCLASSIFIED DRUG;

ARTICLE; CRYOELECTRON MICROSCOPY; EUKARYOTE; MASS SPECTROMETRY; MEMBRANE BINDING; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN LOCALIZATION; RECEPTOR BINDING; RIBOSOME; THERMOACTINOMYCES; THERMOMYCES LANUGINOSUS;

CRYOELECTRON MICROSCOPY; GTP-BINDING PROTEINS; MODELS, MOLECULAR; NEOPLASM PROTEINS; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RIBOSOMES;

EUKARYOTA; THERMOACTINOMYCES; THERMOMYCES; THERMOMYCES LANUGINOSUS;

EID: 4744350970     PISSN: 15459993     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsmb822     Document Type: Article

References (44)

1. McCahill, A., Warwicker, J., Bolger, G.B., Houslay, M.D. & Yarwood, S.J. The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol. Pharmacol. 62, 1261-1273(2002).
2. Ron, D. et al. Cloning of an intracellular receptor for protein kinase C: a homolog of the β subunit of G proteins. Proc. Natl. Acad. Sci. USA 91, 839-843 (1994).
3. Rodriguez, M.M., Ron, D., Touhara, K., Chen, C.H. & Mochly-Rosen, D. RACK1, a protein kinase C anchoring protein, coordinates the binding of activated protein kinase C and select pleckstrin homology domains in vitro. Biochemistry 38, 13787-13794 (1999).
4. Chang, B.Y., Conroy, K.B., Machleder, E.M. & Cartwright, C.A. RACK1, a receptor for activated C kinase and a homolog of the β subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol. Cell. Biol. 18, 3245-3256 (1998).
5. Chang, B.Y., Harte, R.A. & Cartwright, C.A. RACK1: a novel substrate for the Src protein-tyrosine kinase. Oncogene 21, 7619-7629 (2002).
6. Liliental, J. & Chang, D. D. Rack1, a receptor for activated protein kinase C, interacts with integrin β subunit. J. Biol. Chem. 273, 2379-2383 (1998).
7. Yaka, R. et al. NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc. Natl. Acad. Sci. USA 99, 5710-5715 (2002).
8. Sondek, J. & Siderovski, D.P. Gγ-like (GGL) domains: new frontiers in G-protein signaling and β-propeller scaffolding. Biochem. Pharmacol. 61, 1329-1337 (2001).
9. Steele, M.R. et al. Identification of a surface on the β-propeller protein RACK1 that interacts with the cAMP-specific phosphodiesterase PDE4D5. Cell Signal. 13, 507-513 (2001).
10. Link, A.J. et al. Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17, 676-682 (1999).
11. Ceci, M. et al. Release of elF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426, 579-584(2003).
12. Chantrel, Y., Gaisne, M., Lions, C. & Verdiere, J. The transcriptional regulator Hap1p (Cyp1p) is essential for anaerobic or heme-deficient growth of Saccharomyces cerevisiae: genetic and molecular characterization of an extragenic suppressor that encodes a WD repeat protein. Genetics 148, 559-569 (1998).
13. Shor, B., Calaycay, J., Rushbrook, J. & McLeod, M. Cpc2/RACK1 is a ribosome-associated protein that promotes efficient translation in Schizosaccharomyces pombe. J. Biol. Chem. 278, 49119-49128 (2003).
14. Inada, T. et al. One-step affinity purification of the yeast ribosome and its associated proteins and mRNAs. RNA 8, 948-958 (2002).
15. Baum, S., Bittins, M., Frey, S. & Seedorf, M. Asc1p, a WD40-domain containing adaptor protein, is required for the interaction of the RNA-binding protein Scp160p with polysomes. Biochem. J. 380, 823-830 (2004).
16. Angenstein, F. et al. A receptor for activated C kinase is part of messenger ribonucleoprotein complexes associated with polyA-mRNAs in neurons. J. Neurosci. 22, 8827-8837 (2002).
17. Li, A.M., Watson, A. & Fridovich-Keil, J.L. Scp160p associates with specific mRNAs in yeast. Nucleic Acids Res. 31, 1830-1837 (2003).
18. Gavin, A.C. et al. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147 (2002).
19. Spahn, C.M. et al. Structure of the 80S ribosome from Saccharomyces cerevisiae - tRNA-ribosome and subunit-subunit interactions. Cell 107, 373-386 (2001).
20. Wimberly, B.T. et al. Structure of the 30S ribosomal subunit. Nature 407, 327-339 (2000).
21. Brodersen, D.E., Clemons, W.M. Jr., Carter, A.P., Wimberly, B.T. & Ramakrishnan, V. Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16S RNA. J. Mol. Biol. 316, 725-768 (2002).
22. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996).
23. Spann, C.M. et al. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 23, 1008-1019 (2004).
24. Spann, C.M. et al. Cryo-EM visualization of a viral internal ribosome entry site (IRES) bound to human 40S and 80S ribosomes: the IRES functions as an RNA-based translation factor. Cell 118, 465-475 (2004).
25. 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).
26. Halic, M. et al. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427, 808-814 (2004).
27. Dube, P. et al. Correlation of the expansion segments in mammalian rRNA with the fine structure of the 80 S ribosome; a cryoelectron microscopic reconstruction of the rabbit reticulocyte ribosome at 21 A resolution. J. Mol. Biol. 279, 403-421 (1998).
28. Bates, P.A., Kelley, L.A., MacCallum, R.M. & Sternberg, M.J. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins 5 (suppl.), 39-46 (2001).
29. Lambright, D.G. et al. The 2.0 Å crystal structure of a heterotrimeric G protein. Nature 379, 311-319 (1996).
30. Rath, B.K. et al. Fast 3D motif search of EM density maps using a locally normalized cross-correlation function. J. Struct. Biol. 144, 95-103 (2003).
31. Bates, P.A. & Sternberg, M.J. Model building by comparison at CASP3: using expert knowledge and computer automation. Proteins 3 (suppl.), 47-54 (1999).
32. Chang, B.Y., Chiang, M. & Cartwright, C.A. The interaction of Src and RACK1 is enhanced by activation of protein kinase C and tyrosine phosphorylation of RACK1. J. Biol. Chem. 276, 20346-20356 (2001).
33. Chicurel, M.E., Singer, R.H., Meyer, C.J. & Ingber, D.E. Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 392, 730-733 (1998).
34. Steward, O. & Schuman, E.M. Compartmentalized synthesis and degradation of proteins in neurons. Neuron 40, 347-359 (2003).
35. Shevchenko, A., Matthias, W., Ole, V. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996).
36. Keough, T., Lacey, M.P. & Youngquist, R.S. Derivatization procedures to facilitate de novo sequencing of lysine-terminated tryptic peptides using postsource decay matrix-assisted laser desorption/ionization mass spectrometry. Rapid Commun. Mass Spectrom. 14, 2348-2356 (2000).
37. Sottrup-Jensen, L. A low-pH reverse-phase high-performance liquid chromatography system for analysis of the phenylthiohydantoins of S-carboxymethylcysteine and S-carboxyamidomethylcysteine. Anal. Biochem. 225, 187-188 (1995).
38. 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).
39. Frank, J., Penczek, P., Agrawal, R.K., Grassucci, R. & Heagle, A. Three-dimensional cryoelectron microscopy of ribosomes. Methods Enzymol. 317, 276-291 (2000).
40. Zhu, J., Penczek, P.A., Schröder, R. & Frank, J. Three-dimensional reconstruction with contrast transfer function correction from energy-filtered cryoelectron micrographs: procedure and application to the 70S Escherichia coli ribosome. J. Struct. Biol. 118, 197-219 (1997).
41. Malhotra, A. et al. Escherichia coli 70 S ribosome at 15 Å resolution by cryo-electron microscopy: localization of fMet-tRNAfMet and fitting of L1 protein. J. Mol. Biol. 280, 103-116(1998).
42. Gabashvili, I. et al. Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100, 537-549 (2000).
43. Chothia, C. & Lesk, A.M. The relation between the divergence of sequence and structure in proteins. EMBO J. 5, 823-826 (1986).
44. Carson, M. Ribbons 2.0. J. Appl. Crystallog. 24, 958-961 (1991).