Analysis of chimeric ribosomal stalk complexes from eukaryotic and bacterial sources: Structural features responsible for specificity of translation factors

Genes to Cells

Volumn 17, Issue 4, 2012, Pages 273-284

  Mochizuki, Masahiro ^a   Kitamyo, Masumi ^a   Miyoshi, Tomohiro ^a   Ito, Kosuke ^a   Uchiumi, Toshio ^a  

^a NIIGATA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 1ALPHA; ELONGATION FACTOR 2; HETERODIMER; HOMODIMER; RIBOSOME PROTEIN;

ARTICLE; BACTERIUM; CARBOXY TERMINAL SEQUENCE; CHIMERA; ESCHERICHIA COLI; EUKARYOTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RIBOSOME; SILKWORM;

ANIMALS; BOMBYX; ESCHERICHIA COLI; PEPTIDE ELONGATION FACTORS; RIBOSOMAL PROTEINS; RIBOSOMES; SWINE;

BACTERIA (MICROORGANISMS); BOMBYX MORI; ESCHERICHIA COLI; EUKARYOTA;

EID: 84858341033     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2012.01586.x     Document Type: Article

References (35)

1. Dabbs, E.R. (1979) Selection for Escherichia coli mutation with proteins missing from the ribosome. J. Bacteriol. 140, 734-737.
2. Diaconu, M., Kothe, U., Schlünzen, F., Fischer, N., Harms, J.M., Tonevitsky, A.G., Stark, H., Rodnina, M.V. & Wahl, M.C. (2005) Structural Basis for the Function of the Ribosomal L7/L12 Stalk in Factor Binding and GTPase Activation. Cell 121, 991-1004.
3. Domínguez, J.M., Gómez-Lorenzo, M.G. & Martin, J.J. (1999) Sordarin inhibits fungal protein synthesis by blocking translocation differently to fusidic acid. J. Biol. Chem. 274, 22423-22427.
4. Gao, Y.-G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C. & Ramakrishnan, V. (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694-699.
5. Gómez-Lorenzo, M.G. & García-Bustos, J.F. (1998) Ribosomal P-protein stalk function is targeted by sordarin antifungals. J. Biol. Chem. 273, 25041-25044.
6. Grela, P., Helgstrand, M., Krokowski, D., Boguszewska, A., Svergun, D., Liljas, A., Bernadó, P., Grankowski, N., Akke, M. & Tchórzewski, M. (2007) Structual characterization of the ribosomal P1A-P2B protein dimer by small-angle X-ray scattering and NMR spectroscopy. Biochemistry 46, 1988-1998.
7. Griaznova, O. & Traut, R.R. (2000) Deletion of C-terminal residues of Escherichia coli ribosomal protein L10 causes the loss of binding of one L7/L12 dimer: ribosome with one L7/L12 dimer. Biochemistry 39, 4075-4081.
8. Hagiya, A., Naganuma, T., Maki, Y., Ohta, J., Tohkairin, Y., Shimizu, T., Nomura, T., Hachimori, A. & Uchiumi, T. (2005) A mode ofe assembly of P0, P1, and P2 Proteins at the GTPase-associated center in animal ribosome: in vitro analyses with P0 truncation mutants. J. Biol. Chem. 280, 39193-39199.
9. Harms, J.M., Wilson, D.N., Schuenzen, F., Connell, S.R., Stachelhaus, T., Zaborowska, Z., Spahn, C.M.T. & Fucini, P. (2008) Translation regulation via L11: molecular switches on the ribosomes turned on and off by thiostrepton and micrococcin. Mol. Cell 30, 36-38.
10. Helgstrand, M., Mandava, C.S., Mulder, F.A.A., Liljas, A., Sanyal, S. & Akke, M. (2007) The ribosomal stalk binds to translation factor IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain. J. Mol. Biol. 365, 468-479.
11. Iwasaki, K. & Kaziro, Y. (1979) Polypeptide chain elongation factors from pig liver. Methods Enzymol. 60, 657-676.
12. Justice, M.C., Ku, T., Hsu, M.J., Carniol, K., Schmatz, D. & Nielsen, J. (1999) Mutations in ribosomal protein L10e confer resistance to the fungal-specific eukaryotic elongation factor 2 inhibitor sordarin. J. Biol. Chem. 274, 4869-4875.
13. Kravchenko, O., Mitroshin, I., Nikonov, S., Piendl, W. & Garber, M. (2010) Structure of a two-domain N-terminal fragment of ribosomal protein L10 from Methanococcus jannaschii ribosomal stalk. J. Mol. Biol. 399, 214-220.
14. Krokowski, D., Boguszewska, A., Abramczyk, D., Liljas, A., Tchórzewski, M. & Nikodem, F. (2006) Yeast ribosomal P0 protein has two binding sites for P1/P2 proteins. Mol. Microbiol. 60, 386-400.
15. Maki, Y., Hashimoto, T., Zhou, M., Naganuma, T., Ohta, J., Nomura, T., Robinson, C.V. & Uchiumi, T. (2007) Three binding sites for stalk protein dimers are generally present in ribosomes from archaeal organism. J. Biol. Chem. 282, 32827-32833.
16. Miyoshi, T., Nomura, T. & Uchiumi, T. (2009) Engineering and characterization of the ribosomal L10•L12 stalk complex: a structural element responsible for high turnover of the elongation factor G-dependent GTPase. J. Biol. Chem. 284, 85-92.
17. Mohr, D., Wintermeyer, W. & Rodnina, M.V. (2002) GTPase activation of elongation factors Tu and G on the ribosome. Biochemistry 41, 12520-12528.
18. Naganuma, T., Nomura, N., Yao, M., Mochizuki, M., Uchiumi, T. & Tanaka, I. (2010) Structual basis for translation factor recruitment to the eukaryotic/archaeal ribosomes. J. Biol. Chem. 285, 4747-4756.
19. Nomura, T., Mochizuki, R., Dabbs, E.R., Shimizu, Y., Ueda, T., Hachimori, A. & Uchiumi, T. (2003) A point mutation in ribosomal protein L7/L12 reduces its ability to form a compact dimer structure and to assemble into the GTPase center. Biochemistry 42, 4691-4698.
20. Nomura, T., Nakao, K., Maki, Y., Naganuma, T., Takashima, T., Tanaka, I., Kimura, M., Hachimori, A. & Uchiumi, T. (2006) In vitro reconstitution of the GTPase-associated centre of the archaebacterial ribosome: the functional features observed in a hybrid form with Escherichia coli 50S subunits. Biochem. J. 396, 565-571.
21. Parisi, B., Milanesi, G., Van Etten, J.L., Perani, A. & Ciferri, O. (1967) Species specificity in protein synthesis. J. Mol. Biol. 274, 259-309.
22. Pérez-Fernández, J., Remacha, M. & Ballesta, J.P.G. (2005) The acidic proteins binding site is partially hidden in the free Saccharomyces cerevisiae ribosomal stalk protein P0. Biochemistry 44, 5532-5540.
23. Rendi, R. & Ochoa, S. (1962) Species specificity in activation and transfer of leusine from carrier ribonucleic acid to ribosomes. J. Biol. Chem. 237, 3707-3710.
24. Rich, B.E. & Steitz, J.A. (1978) Human acidic ribosomal phosphoproteins P0, P1, P2: analysis of cDNA clones, In vitro synthesis, and Assembly. Mol. Cell. Biol. 7, 4065-4074.
25. Rondríguez-Gabriel, M.A., Remacha, M. & Ballesta, J.P.G. (2000) The RNA interacting domain but not the protein interacting domain is highly conserved in ribosomal protein P0. J. Biol. Chem. 275, 2130-2136.
26. Santos, C. & Ballesta, J.P.G. (2002) Role of the ribosomal stalk components in the resistance of Aspergillus fumigatus to the sordarin antifungals. Mol. Microbiol. 43, 227-237.
27. Santos, C. & Ballesta, J.P.G. (2005) Characterization of the 26S rRNA-binding domain in Saccharomyces cerevisiae ribosomal stalk phosphoprotein P0. Mol. Microbiol. 58, 217-226.
28. Shimizu, T., Nakagaki, M., Nishi, Y., Kobayashi, Y., Hachimori, A. & Uchiumi, T. (2002) Interaction among silkworm ribosomal proteins P1, P2 and P0 required for functional protein binding to the GTPase-associated domain of 28S rRNA. Nucleic Acid Res. 30, 2620-2627.
29. Shimmin, L.C., Ramirez, C., Matheson, A.T. & Dennis, P.P. (1989) Sequence alignment and evolutionary comparison of the L10 equivalent and L12 equivalent ribosomal proteins from archaebacteria, eubacteria, and eucaryotes. J. Mol. Evol. 29, 448-462.
30. Tokimatsu, H., Strycharz, W.A. & Dahlberg, A.E. (1981) Gel electrophoretic studies on ribosomal proteins L7/L12 and the Escherichia coli 50 S subunit. J. Mol. Biol. 152, 397-412.
31. Uchiumi, T., Honma, S., Endo, Y. & Hachimori, A. (2002a) Ribosomal proteins at the stalk region modulate functional rRNA structures in the GTPase center. J. Biol. Chem. 277, 41401-41409.
32. Uchiumi, T., Honma, S., Nomura, T., Dabbs, E.R. & Hachimori, A. (2002b) Translation elongation by a hybrid ribosome in which proteins at the GTPase center of the Escherichia coli ribosome are replaced with rat counterparts. J. Biol. Chem. 277, 3857-3862.
33. Uchiumi, T., Hori, K., Nomura, T. & Hachimori, A. (1999) Replacement of L7/L12.L10 protein complex in Escherichia coli ribosomes with the eukaryotic counterpart changes the specificity of elongation factor binding. J. Biol. Chem. 274, 27578-27582.
34. Wahl, M.C. & Möller, W. (2002) Structure and function of the Acidic ribosomal stalk proteins. Curr. Protein Pept. Sci. 3, 93-106.
35. Wilson, D.N. & Nierhaus, K.H. (2005) Ribosome proteins in the spotlight. Crit. Rev. Biochem. Mol. Biol. 40, 243-267.