Carboxy terminal modifications of the P0 protein reveal alternative mechanisms of nuclear ribosomal stalk assembly

Nucleic Acids Research

Volumn 41, Issue 18, 2013, Pages 8628-8636

  Francisco Velilla, Rosario ^a   Remacha, Miguel ^a   Ballesta, Juan P G ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; LEPTOMYCIN B; PROTEIN L 12; PROTEIN MRT4; PROTEIN P0; PROTEIN P1; PROTEIN P2; RIBOSOME PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; LARGE RIBOSOMAL SUBUNIT; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; RIBOSOMAL STALK ASSEMBLY;

CELL NUCLEUS; FLUORESCENT DYES; GENE DELETION; GREEN FLUORESCENT PROTEINS; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84885927049     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt637     Document Type: Article

References (41)

1. Gonzalo, P. and Reboud, J.P. (2003) The puzzling lateral flexible stalk of the ribosome. Biol. Cell, 95, 179-193.
2. Ben-Shem, A., Jenner, L., Yusupova, G. and Yusupov, M. (2010) Crystal structure of the eukaryotic ribosome. Science, 330, 1203-1209.
3. Lee, K.M., Yu, C.W., Chiu, T.Y., Sze, K.H., Shaw, P.C. and Wong, K.B. (2012) Solution structure of the dimerization domain of the eukaryotic stalk P1/P2 complex reveals the structural organization of eukaryotic stalk complex. Nucleic Acids Res., 40, 3172-3182.
4. Naganuma, T., Nomura, N., Yao, M., Mochizuki, M., Uchiumi, T. and Tanaka, I. (2010) Structural basis for translation factor recruitment to the eukaryotic/archaeal ribosomes. J. Biol. Chem., 285, 4747-4756.
5. Zinker, S. and Warner, J.R. (1976) The ribosomal proteins of Saccharomyces cerevisiae. Phosphorylated and exchangeable proteins. J. Biol. Chem., 251, 1799-1807.
6. Tsurugi, K. and Ogata, K. (1985) Evidence for the exchangeability of acidic ribosomal proteins on cytoplasmic ribosomes in regenerating rat liver. J. Biochem., 98, 1427-1431.
7. Scharf, K.D. and Nover, L. (1987) Control of ribosome biosynthesis in plant cell cultures under heat shock conditions. II. Ribosomal proteins. Biochim. Biophys. Acta, 909, 44-57.
8. Ballesta, J.P.G. and Remacha, M. (1996) The large ribosomal subunit stalk as a regulatory element of the eukaryotic translational machinery. Progr. Nucl. Acid. Res. Mol. Biol., 55, 157-193.
9. Lo, K.Y., Li, Z., Bussiere, C., Bresson, S., Marcotte, E.M. and Johnson, A.W. (2010) Defining the Pathway of Cytoplasmic Maturation of the 60S Ribosomal Subunit. Mol. Cell, 39, 196-208.
10. Lo, K.Y., Li, Z., Wang, F., Marcotte, E.M. and Johnson, A.W. (2009) Ribosome stalk assembly requires the dual-specificity phosphatase C for the exchange of Mrt4 with P0. J. Cell Biol., 186, 849-862.
11. Kemmler, S., Occhipinti, L., Veisu, M. and Panse, V.G. (2009) Yvh1 is required for a late maturation step in the 60S biogenesis pathway. J. Cell Biol., 186, 863-880.
12. Rodriguez-Mateos, M., Garcia-Gomez, J.J., Francisco-Velilla, R., Remacha, M., de la Cruz, J. and Ballesta, J.P. (2009) Role and dynamics of the ribosomal protein P0 and its related trans-acting factor Mrt4 during ribosome assembly in Saccharomyces cerevisiae. Nucleic Acids Res., 37, 7519-7532.
13. Rodriguez-Mateos, M., Abia, D., Garcia-Gomez, J.J., Morreale, A., de la Cruz, J., Santos, C., Remacha, M. and Ballesta, J.P. (2009) The amino terminal domain from Mrt4 protein can functionally replace the RNA binding domain of the ribosomal P0 protein. Nucleic Acids Res., 37, 3514-3521.
14. Santos, C. and Ballesta, J.P. (2005) Characterization of the 26S rRNA-binding domain in Saccharomyces cerevisiae ribosomal stalk phosphoprotein P0. Mol. Microbiol., 58, 217-226.
15. Harnpicharnchai, P., Jakovljevic, J., Horsey, E., Miles, T., Roman, J., Rout, M., Meagher, D., Imai, B., Guo, Y., Brame, C.J. et al. (2001) Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol. Cell, 8, 505-515.
16. Santos, C. and Ballesta, J.P.G. (1995) The highly conserved protein P0 carboxyl end is essential for ribosome activity only in the absence of proteins P1 and P2. J. Biol. Chem., 270, 20608-20614.
17. Mochizuki, M., Kitamyo, M., Miyoshi, T., Ito, K. and Uchiumi, T. (2012) Analysis of chimeric ribosomal stalk complexes from eukaryotic and bacterial sources: structural features responsible for specificity of translation factors. Genes Cells, 17, 273-284.
18. Janke, C., Magiera, M.M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E. et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast, 21, 947-962.
19. Bonneaud, N., Ozier-Kalogeropoulos, O., Li, G., Labouesse, M., Minvielle-Sebastia, L. and Lacroute, F. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast, 7, 609-615.
20. Rodriguez-Gabriel, M.A., Remacha, M. and 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.
21. Kressler, D., de la Cruz, J., Rojo, M. and Linder, P. (1997) Fal1p is an essential DEAD-box protein involved in 40S-ribosomal-subunit biogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol., 17, 7283-7294.
22. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol., 17, 1030-1032.
23. Krokowski, D., Boguszewska, A., Abramczyk, D., Liljas, A., Tchorzewski, M. and Grankowski, N. (2006) Yeast ribosomal P0 protein has two separate binding sites for P1/P2 proteins. Mol. Microbiol., 60, 386-400.
24. Cá rdenas, D., Revuelta-Cervantes, J., Jiménez-D́az, A., Camargo, H., Remacha, M. and Ballesta, J.P.G. (2012) P1 and P2 protein heterodimer binding to the p0 protein of Saccharomyces cerevisiae is relatively non-specific and a source of ribosomal heterogeneity. Nucleic Acids Res., 40, 4520-4529.
25. Remacha, M., Santos, C., Bermejo, B., Naranda, T. and Ballesta, J.P.G. (1992) Stable binding of the eukaryotic acidic phosphoproteins to the ribosome is not an absolute requirement for in vivo protein synthesis. J. Biol. Chem., 267, 12061-12067.
26. Nusspaumer, G., Remacha, M. and Ballesta, J.P. (2000) Phosphorylation and N-terminal region of yeast ribosomal protein P1 mediate its degradation, which is prevented by protein P2. EMBO J., 19, 6075-6084.
27. Briceno, V., Camargo, H., Remacha, M., Santos, C. and Ballesta, J.P. (2008) Structural and functional characterization of the amino terminal domain of the yeast ribosomal stalk P1 and P2 proteins. Int. J. Biochem. Cell Biol., 41, 1315-1322.
28. Santos, C. and Ballesta, J.P. (1994) Ribosomal protein P0, contrary to phosphoproteins P1 and P2, is required for ribosome activity and Saccharomyces cerevisiae viability. J. Biol. Chem., 269, 15689-15696.
29. Neville, M. and Rosbash, M. (1999) The NES-Crm1p export pathway is not a major mRNA export route in Saccharomyces cerevisiae. EMBO J., 18, 3746-3756.
30. Kudo, N., Matsumori, N., Taoka, H., Fujiwara, D., Schreiner, E.P., Wolff, B., Yoshida, M. and Horinouchi, S. (1999) Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl Acad. Sci. USA, 96, 9112-9117.
31. Ho, J.H., Kallstrom, G. and Johnson, A.W. (2000) Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit. J. Cell Biol., 151, 1057-1066.
32. Sengupta, J., Bussiere, C., Pallesen, J., West, M., Johnson, A.W. and Frank, J. (2010) Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J. Cell Biol., 189, 1079-1086.
33. Kressler, D., Hurt, E. and Babetaler, J. (2010) Driving ribosome assembly. Biochim. Biophys. Acta, 1803, 673-683.
34. Remacha, M., Jimenez-Diaz, A., Bermejo, B., Rodriguez-Gabriel, M.A., Guarinos, E. and Ballesta, J.P.G. (1995) Ribosomal acidic phosphoproteins P1 and P2 are not required for cell viability but regulate the pattern of protein expression in Saccharomyces cerevisiae. Mol. Cell. Biol., 15, 4754-4762.
35. Shajani, Z., Sykes, M.T. and Williamson, J.R. (2011) Assembly of bacterial ribosomes. Annu. Rev. Biochem., 80, 501-526.
36. Nissan, T.A., Bassler, J., Petfalski, E., Tollervey, D. and Hurt, E. (2002) 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J., 21, 5539-5547.
37. Grandi, P., Rybin, V., Bassler, J., Petfalski, E., Strauss, D., Marzioch, M., Schafer, T., Kuster, B., Tschochner, H., Tollervey, D. et al. (2002) 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell, 10, 105-115.
38. Dez, C., Froment, C., Noaillac-Depeyre, J., Monsarrat, B., Caizergues-Ferrer, M. and Henry, Y. (2004) Npa1p, a component of very early pre-60S ribosomal particles, associates with a subset of small nucleolar RNPs required for peptidyl transferase center modification. Mol. Cell. Biol., 24, 6324-6337.
39. Thomas, T.J. and Rothstein, R. (1989) Elevated recombination rates in transcriptionally active DNA. Cell, 56, 619-630.
40. Hedges, J., West, M. and Johnson, A.W. (2005) Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J., 24, 567-579.
41. Zambrano, R., Briones, E., Remacha, M. and Ballesta, J.P.G. (1997) Phosphorylation of the acidic ribosomal P proteins in Saccharomyces cerevisiae. A reappraisal. Biochemistry, 36, 14439-14446.