Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 26, Issue 10, 2006, Pages 3718-3727

  Hung, Nai Jung ^a   Johnson, Arlen W ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARX1 PROTEIN; DNA DIRECTED RNA POLYMERASE; ENHANCED GREEN FLUORESCENT PROTEIN; FUNGAL DNA; GENOMIC DNA; METHIONYL AMINOPEPTIDASE; REI1 PROTEIN; RIBOSOME RNA; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; FUNGUS GROWTH; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RIBOSOME; RIBOSOME SUBUNIT; RNA BINDING; SACCHAROMYCES CEREVISIAE; YEAST;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; BLOTTING, WESTERN; CELL FRACTIONATION; CELL NUCLEUS; CENTRIFUGATION, DENSITY GRADIENT; CYCLOHEXIMIDE; CYTOPLASM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; GENE DELETION; GENES, FUNGAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PRECIPITIN TESTS; PROTEIN SYNTHESIS INHIBITORS; RECOMBINANT FUSION PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

SACCHAROMYCES CEREVISIAE;

EID: 33646582609     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.10.3718-3727.2006     Document Type: Article

References (54)

1. Bassler, J., P. Grandi, O. Gadal, T. Lessmann, E. Petfalski, D. Tollervey, J. Lechner, and E. Hurt. 2001. Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol. Cell 8:517-529.
2. Basu, U., K. Si, J. R. Warner, and U. Maitra. 2001. The Saccharomyces cerevisiae T1F6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis. Mol. Cell. Biol. 21:1453-1462.
3. Beckmann, R., C. M. Spahn, N. Eswar, J. Helmers, P. A. Penczek, A. Sali, J. Frank, and G. Blobel. 2001. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107:361-372.
4. Ceci, M., C. Gaviraghi, C. Gorrini, L. A. Sala, N. Offenhauser, P. C. Marchisio, and S. Biffo. 2003. Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426:579-584.
5. Ciufo, L. F., and J. D. Brown. 2000. Nuclear export of yeast signal recognition particle lacking Srp54p by the Xpo1p/Crm1p NES-dependent pathway. Curr. Biol. 10:1256-1264.
6. Dragon, F., J. E. Gallagher, P. A. Compagnone-Post, B. M. Mitchell, K. A. Porwancher, K. A. Wehner, S. Wormsley, R. E. Settlage, J. Shabanowitz, Y. Osheim, A. L. Beyer, D. F. Hunt, and S. J. Baserga. 2002. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967-970.
7. Franke, J., B. Reimann, E. Hartmann, M. Kohlerl, and B. Wiedmann. 2001. Evidence for a nuclear passage of nascent polypeptide-associated complex subunits in yeast. J. Cell Sci. 114:2641-2648.
8. Fromont-Racine, M., B. Senger, C. Saveanu, and F. Fasiolo. 2003. Ribosome assembly in eukaryotes. Gene 313:17-42.
9. Gautschi, M., H. Lilie, U. Funfschilling, A. Mun, S. Ross, T. Lithgow, P. Rucknagel, and S. Rospert. 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., A. Mun, S. Ross, and S. Rospert. 2002. A functional chaperone triad on the yeast ribosome. Proc. Natl. Acad. Sci. USA 99:4209-4214.
11. Gavin, A. C., M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J. M. Rick, A. M. Michon, C. M. Cruciat, M. Remor, C. Hofert, M. Schelder, M. Brajenovic, H. Ruffner, A. Merino, K. Klein, M. Hudak, D. Dickson, T. Rudi, V. Gnau, A. Bauch, S. Bastuck, B. Huhse, C. Leutwein, M. A. Heurtier, R. R. Copley, A. Edelmann, E. Querfurth, V. Rybin, G. Drewes, M. Raida, T. Bouwmeester, P. Bork, B. Seraphin, B. Kuster, G. Neubauer, and G. Superti-Furga. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
12. Grandi, P., V. Rybin, J. Bassler, E. Petfalski, D. Strauss, M. Marzioch, T. Schafer, B. Kuster, H. Tschochner, D. Tollervey, A. C. Gavin, and E. Hurt. 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.
13. Granneman, S., and S. J. Baserga. 2004. Ribosome biogenesis: of knobs and RNA processing. Exp. Cell Res. 296:43-50.
14. Grosshans, H., K. Deinert, E. Hurt, and G. Simos. 2001. Biogenesis of the signal recognition particle (SRP) involves import of SRP proteins into the nucleolus, assembly with the SRP-RNA, and Xpo1p-mediated export. J. Cell Biol. 153:745-762.
15. Halic, M., T. Becker, M. R. Pool, C. M. Spahn, R. A. Grassucci, J. Frank, and R. Beckmann. 2004. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427:808-814.
16. Harnpicharnchai, P., J. Jakovljevic, E. Horsey, T. Miles, J. Roman, M. Rout, D. Meagher, B. Imai, Y. Guo, C. J. Brame, J. Shabanowitz, D. F. Hunt, and J. L. Woolford, Jr. 2001. Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol. Cell 8:505-515.
17. Hedges, J., M. West, and A. W. Johnson. 2005. Release of the export adapter, Nmd3, from the 60S ribosomal subunit requires Rp110p and the cytoplasmic GTPase Lsg1. EMBO J. 24:567-579.
18. Ho, J. H., G. Kallstrom, and A. W. Johnson. 2000. md3 is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit. J. Cell Biol. 151:1057-1066.
19. Huang, S., R. C. Elliott, P. S. Liu, R. K. Koduri, J. L. Weickmann, J. H. Lee, L. C. Blair, P. Ghosh-Dastidar, R. A. Bradshaw, K. M. Bryan, et al. 1987. Specificity of cotranslational amino-terminal processing of proteins in yeast. Biochemistry 26:8242-8246.
20. Huh, W. K., J. V. Falvo, L. C. Gerke, A. S. Carroll, R. W. Howson, J. S. Weissman, and E. K. O'Shea. 2003. Global analysis of protein localization in budding yeast. Nature 425:686-691.
21. Iwase, M., and A. Toh-e. 2001. Nis1 encoded by YNL078W: a new neck protein of Saccharomyces cerevisiae. Genes Genet. Syst. 76:335-343.
22. Iwase, M., and A. Toh-e. 2004. Ybr267w is a new cytoplasmic protein belonging to the mitotic signaling network of Saccharomyces cerevisiae. Cell Struct. Funct. 29:1-15.
23. Johnson, A. 2004. Nuclear export of ribosomal subunits, p. 286-301. In M. O. J. Olson (ed.), The nucleolus. Georgetown, Kluwer Academic/Plenum Publisher, New York, N.Y.
24. Johnson, A. W., J. H. Ho, G. Kallstrom, C. Trotta, E. Lund, L. Kahan, J. Dahlberg, and J. Hedges. 2001. Nuclear export of the large ribosomal subunit. Cold Spring Harb. Symp. Quant. Biol. 66:599-605.
25. Kaiser, C. M. S., and A. Mitchell. 1994. Methods in yeast genetics, p. 207-217. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
26. Kallstrom, G., J. Hedges, and A. Johnson. 2003. The putative GTPases Nog1p and Lsg1 are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol. Cell. Biol. 23: 4344-4355.
27. Kressler, D., P. Linder, and J. de La Cruz. 1999. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:7897-7912.
28. Kudo, N., B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. 1998. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:540-547.
29. Lessor, T. J., J. Y. Yoo, X. Xia, N. Woodford, and A. W. Hamburger. 2000. Ectopic expression of the ErbB-3 binding protein ebp1 inhibits growth and induces differentiation of human breast cancer cell lines. J. Cell Physiol. 183:321-329.
30. Li, X., and Y. H. Chang. 1995. Amino-terminal protein processing in Saccharomyces cerevisiae is an essential function that requires two distinct methionine aminopeptidases. Proc. Natl. Acad. Sci. USA 92:12357-12361.
31. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
32. Lopez, N., J. Halladay, W. Walter, and E. A. Craig. 1999. SSB, encoding a ribosome-associated chaperone, is coordinately regulated with ribosomal protein genes. J. Bacteriol. 181:3136-3143.
33. Milkereit, P., O. Gadal, A. Podtelejnikov, S. Trumtel, N. Gas, E. Petfalski, D. Tollervey, M. Mann, E. Hurt, and H. Tschochner. 2001. Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 105:499-509.
34. Moy, T. I., and P. A. Silver. 2002. Requirements for the nuclear export of the small ribosomal subunit. J. Cell Sci. 115:2985-2995.
35. Nishi, K., M. Yoshida, D. Fujiwara, M. Nishikawa, S. Horinouchi, and T. Beppu. 1994. Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J. Biol. Chem. 269:6320-6324.
36. Nissan, T. A., J. Bassler, E. Petfalski, D. Tollervey, and E. Hurt. 2002. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J. 21:5539-5547.
37. Nissan, T. A., K. Galani, B. Maco, D. Tollervey, U. Aebi, and E. Hurt. 2004. A pre-ribosome with a tadpole-like structure functions in ATP-dependent maturation of 60S subunits. Mol. Cell 15:295-301.
38. Pool, M. R., J. Stumm, T. A. Fulga, I. Sinning, and B. Dobberstein. 2002. Distinct modes of signal recognition particle interaction with the ribosome. Science 297:1345-1348.
39. Rospert, S., Y. Dubaquie, and M. Gautschi. 2002. Nascent-polypeptide- associated complex. Cell Mol. Life Sci. 59:1632-1639.
40. Rout, M. P., and G. Blobel. 1993. Isolation of the yeast nuclear pore complex. J. Cell Biol. 123:771-783.
41. Saveanu, C., D. Bienvenu, A. Namane, P. E. Gleizes, N. Gas, A. Jacquier, and M. Fromont-Racine. 2001. Nog2, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J. 20:6475-6484.
42. Senger, B., D. L. Lafontaine, J. S. Graindorge, O. Gadal, A. Camasses, A. Sanni, J. M. Garnier, M. Breitenbach, E. Hurt, and F. Fasiolo. 2001. The nucle(ol)ar Tif6 and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 8:1363-1373.
43. Si, K., and U. Maitra. 1999. The Saccharomyces cerevisiae homologue of mammalian translation initiation factor 6 does not function as a translation initiation factor. Mol. Cell. Biol. 19:1416-1426.
44. Spahn, C. M., R. Beckmann, N. Eswar, P. A. Penczek, A. Sali, G. Blobel, and J. Frank. 2001. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA-ribosome and subunit-subunit interactions. Cell 107:373-386.
45. Spahn, C. M., M. G. Gomez-Lorenzo, R. A. Grassucci, R. Jorgensen, G. R. Andersen, R. Beckmann, P. A. Penczek, J. P. Ballesta, and J. Frank. 2004. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 23:1008-1019.
46. Squatrito, M., M. Mancino, M. Donzelli, L. B. Areces, and G. F. Draetta. 2004. EBP1 is a nucleolar growth-regulating protein that is part of pre-ribosomal ribonucleoprotein complexes. Oncogene 23:4454-4465.
47. Thomas, F., and U. Kutay. 2003. Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J. Cell Sci. 116:2409-2419.
48. Trotta, C. R., E. Lund, L. Kahan, A. W. Johnson, and J. E. Dahlberg. 2003. Coordinated nuclear export of 60S ribosomal subunits and NMD3 in vertebrates. EMBO J. 22:2841-2851.
49. Tschochner, H., and E. Hurt. 2003. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13:255-263.
50. West, M., H. Hedges, A. Chen, and A. W. Johnson. 2005. Defining the order in which Nmd3 and Rpl10p load onto nascent 60S ribosomal subunits. Mol. Cell. Biol. 25:3802-3813.
51. Xia, X., A. Cheng, T. Lessor, Y. Zhang, and A. W. Hamburger. 2001. Ebp1, an ErbB-3 binding protein, interacts with Rb and affects Rb transcriptional regulation. J. Cell Physiol. 187:209-217.
52. Yoo, J. Y., X. W. Wang, A. K. Rishi, T. Lessor, X. M. Xia, T. A. Gustafson, and A. W. Hamburger. 2000. Interaction of the PA2G4 (EBP1) protein with ErbB-3 and regulation of this binding by heregulin. Br. J. Cancer 82:683-690.
53. Zavanelli, M. I., J. S. Britton, A. H. Igel, and M. Ares, Jr. 1994. Mutations in an essential U2 small nuclear RNA structure cause cold-sensitive U2 small nuclear ribonucleoprotein function by favoring competing alternative U2 RNA structures. Mol. Cell. Biol. 14:1689-1697.
54. Zhang, Y., N. Woodford, X. Xia, and A. W. Hamburger. 2003. Repression of E2F1-mediated transcription by the ErbB3 binding protein Ebp1 involves histone deacetylases. Nucleic Acids Res. 31:2168-2177.