The post-transcriptional steps of eukaryotic ribosome biogenesis

Cellular and Molecular Life Sciences

Volumn 65, Issue 15, 2008, Pages 2334-2359

  Henras, A K ^a   Soudet, J ^a   Gerus M ^a   Lebaron, S ^a   Caizergues Ferrer, M ^a   Mougin, A ^a   Henry, Y ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Nuclear export; Pre ribosomal particle; Pre rRNA processing; Quality control; snoRNP

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CELL NUCLEUS RECEPTOR; GUANOSINE TRIPHOSPHATASE; NUCLEOPORIN; PROTEIN ARX1P; PROTEIN TIF6P; RECEPTOR PROTEIN; RIBOSOME PROTEIN; RIBOSOME RNA; SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG;

BIOGENESIS; CELL FUNCTION; CYTOPLASM; EUKARYOTE; GENETIC TRANSCRIPTION; HUMAN; HYDROLYSIS; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; QUALITY CONTROL; REVIEW; RIBOSOME; RIBOSOME SUBUNIT; RNA METHYLATION; RNA PROCESSING; RNA STRUCTURE; RNA SYNTHESIS;

ANIMALS; EUKARYOTIC CELLS; HUMANS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA PRECURSORS; RNA, RIBOSOMAL; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 49249139050     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8027-0     Document Type: Review

References (241)

1. Warner, J. R. (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437-440.
2. Warner, J. R., Vilardell, J. and Sohn, J. H. (2001) Economics of ribosome biosynthesis. Cold Spring Harb. Symp. Quant. Biol. 66, 567-574.
3. Venema, J. and Tollervey, D. (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33, 261-311.
4. Harnpicharnchai, P., Jakovljevic, J., Horsey, E., Miles, T., Roman, J., Rout, M., Meagher, D., Imai, B., Guo, Y., Brame, C. J., Shabanowitz, J., Hunt, D. F. and Woolford, J. L., Jr. (2001) Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol. Cell 8, 505-515.
5. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Séraphin, B. (1999)Ageneric protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032.
6. Warner, J. R. (2001) Nascent ribosomes. Cell 107, 133-136.
7. de la Cruz, J., Kressler, D. and Linder, P. (2004) Ribosomal subunit assembly. In: The Nucleolus, pp. 258-285, Olson, M. O. (ed.), Kluwer Academic/Plenum, New York.
8. Fromont-Racine, M., Senger, B., Saveanu, C. and Fasiolo, F. (2003) Ribosome assembly in eukaryotes. Gene 313, 17-42.
9. Gerbi, S. A. and Borovjagin, A. V. (2004) Pre-ribosomal RNA processing in multicellular organisms. In: The Nucleolus, pp. 170-198, Olson, M. O. (ed.), Kluwer Academic/Plenum, New York.
10. Granneman, S. and Baserga, S. J. (2004) Ribosome biogenesis: of knobs and RNA processing. Exp. Cell Res. 296, 43-50.
11. Johnson, A. W. (2004) Nuclear export of ribosomal subunits. In: The Nucleolus, pp. 286-301, Olson, M. O. (ed.), Kluwer Academic/Plenum, New York.
12. Lafontaine, D. L. J. (2004) Eukaryotic ribosome synthesis. In: Protein Synthesis and Ribosome Structure, pp. 107-143, Nierhaus, K. (ed.), Wiley-InterScience, Weinheim.
13. Raué, H. A. (2004) Pre-ribosomal RNA processing and assembly in Saccharomyces cerevisiae: the Machine that makes the machine. In: The Nucleolus, pp. 199-222, Olson, M. O., (ed.), Kluwer Academic/Plenum, New York.
14. Zemp, I. and Kutay, U. (2007) Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 581, 2783-2793.
15. Andersen, J. S., Lam, Y. W., Leung, A. K., Ong, S. E., Lyon, C. E., Lamond, A. I. and Mann, M. (2005) Nucleolar proteome dynamics. Nature 433, 77 -83.
16. Thiry, M. and Lafontaine, D. L. (2005) Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 15, 194-199.
17. Raška, I., Shaw, P. J. and Cmarko, D. (2006) Structure and function of the nucleolus in the spotlight. Curr. Opin. Cell Biol. 18, 325-334.
18. Schneider, D. A., Michel, A., Sikes, M. L., Vu, L., Dodd, J. A., Salgia, S., Osheim, Y. N., Beyer, A. L. and Nomura, M. (2007) Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly. Mol. Cell 26, 217-229.
19. Mougey, E. B., O'Reilly, M., Osheim, Y., Miller, O. L., Jr., Beyer, A. and Sollner-Webb, B. (1993) The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. Genes Dev. 7, 1609-1619.
20. Henras, A. K., Bertrand, E. and Chanfreau, G. (2004) A cotranscriptional model for 3′-end processing of the Saccharomyces cerevisiae pre-ribosomal RNA precursor. RNA 10, 1572-1585.
21. Kufel, J., Dichtl, B. and Tollervey, D. (1999) Yeast Rnt1p is required for cleavage of the pre-ribosomal RNA in the 3′ ETS but not the 5′ ETS. RNA 5, 909-917.
22. Osheim, Y. N., French, S. L., Keck, K. M., Champion, E. A., Spasov, K., Dragon, F., Baserga, S. J. and Beyer, A. L. (2004) Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol. Cell 16, 943-954.
23. Grandi, P., Rybin, V., Bassler, J., Petfalski, E., Strauss, D., Marzioch, M., Schäfer, T., Kuster, B., Tschochner, H., Tollervey, D., Gavin, A. C. and Hurt, E. (2002) 90S preribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 10, 105-115.
24. Dragon, F., Gallagher, J. E., Compagnone-Post, P. A., Mitchell, B. M., Porwancher, K. A., Wehner, K. A., Wormsley, S., Settlage, R. E., Shabanowitz, J., Osheim, Y., Beyer, A. L., Hunt, D. F. and Baserga, S. J. (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417, 967-970.
25. Krogan, N. J., Peng, W. T., Cagney, G., Robinson, M. D., Haw, R., Zhong, G., Guo, X., Zhang, X., Canadien, V., Richards, D. P., Beattie, B. K., Lalev, A., Zhang, W., Davierwala, A. P., Mnaimneh, S., Starostine, A., Tikuisis, A. P., Grigull, J., Datta, N., Bray, J. E., Hughes, T. R., Emili, A. and Greenblatt, J. F. (2004) High-definition macromolecular composition of yeast RNA-processing complexes. Mol. Cell 13, 225-239.
26. Perez-Fernandez, J., Roman, A., De Las Rivas, J., Bustelo, X. R. and Dosil, M. (2007) The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol. 27, 5414-5429.
27. Gallagher, J. E., Dunbar, D. A., Granneman, S., Mitchell, B. M., Osheim, Y., Beyer, A. L. and Baserga, S. J. (2004) RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev. 18, 2506-2517.
28. Vos, H. R., Bax, R., Faber, A. W., Vos, J. C. and Raué, H. A. (2004) U3 snoRNP and Rrp5p associate independently with Saccharomyces cerevisiae 35S pre-rRNA, but Rrp5p is essential for association of Rok1p. Nucleic Acids Res. 32, 5827-533.
29. Dunbar, D. A., Wormsley, S., Agentis, T. M. and Baserga, S. J. (1997) Mpp10p, a U3 small nucleolar ribonucleoprotein component required for pre-18S rRNA processing in yeast. Mol. Cell. Biol. 17, 5803-5812.
30. Granneman, S., Gallagher, J. E., Vogelzangs, J., Horstman, W., van Venrooij, W. J., Baserga, S. J. and Pruijn, G. J. (2003) The human Imp3 and Imp4 proteins form a ternary complex with hMpp10, which only interacts with the U3 snoRNA in 60-80S ribonucleoprotein complexes. Nucleic Acids Res. 31, 1877-1887.
31. Lee, S. J. and Baserga, S. J. (1999) Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing. Mol. Cell. Biol. 19, 5441-5452.
32. Wehner, K. A., Gallagher, J. E. and Baserga, S. J. (2002) Components of an interdependent unit within the SSU processome regulate and mediate its activity. Mol. Cell. Biol. 22, 7258-7267.
33. Deshmukh, M., Tsay, Y. F., Paulovich, A. G. and Woolford, J. L., Jr. (1993) Yeast ribosomal protein L1 is required for the stability of newly synthesized 5S rRNA and the assembly of 60S ribosomal subunits. Mol. Cell. Biol. 13, 2835-2845.
34. Steitz, J. A., Berg, C., Hendrick, J. P., LaBranche-Chabot, H., Metspalu, A., Rinke, J. and Yario, T. (1988) A 5S rRNA/L5 complex is a precursor to ribosome assembly in mammalian cells. J. Cell Biol. 106, 545-556.
35. Miyoshi, K., Tsujii, R., Yoshida, H., Maki, Y., Wada, A., Matsui, Y., Toh, E. A. and Mizuta, K. (2002) Normal assembly of 60 S ribosomal subunits is required for the signaling in response to a secretory defect in Saccharomyces cerevisiae. J. Biol. Chem. 277, 18334-18339.
36. Morita, D., Miyoshi, K., Matsui, Y., Toh, E. A., Shinkawa, H., Miyakawa, T. and Mizuta, K. (2002) Rpf2p, an evolutionarily conserved protein, interacts with ribosomal protein L11 and is essential for the processing of 27 SB Pre-rRNA to 25 S rRNA and the 60 S ribosomal subunit assembly in Saccharomyces cerevisiae. J. Biol. Chem. 277, 28780-28786.
37. Zhang, J., Harnpicharnchai, P., Jakovljevic, J., Tang, L., Guo, Y., Oeffinger, M., Rout, M. P., Hiley, S. L., Hughes, T. and Woolford, J. L., Jr. (2007) Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 21, 2580-2592.
38. Ferreira-Cerca, S., Poll, G., Kuhn, H., Neueder, A., Jakob, S., Tschochner, H. and Milkereit, P. (2007) Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol. Cell 28, 446-457.
39. Ferreira-Cerca, S., Poll, G., Gleizes, P. E., Tschochner, H. and Milkereit, P. (2005) Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol. Cell 20, 263-275.
40. Held, W. A., Ballou, B., Mizushima, S. and Nomura, M. (1974) Assembly mapping of 30 S ribosomal proteins from Escherichia coli: further studies. J. Biol. Chem. 249, 3103-3111.
41. Hughes, J. M. and Ares, M., Jr. (1991) Depletion of U3 small nucleolar RNA inhibits cleavage in the 5′ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 10, 4231-4239.
42. Kass, S., Tyc, K., Steitz, J. A. and Sollner-Webb, B. (1990) The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell 60, 897-908.
43. Borovjagin, A. V. and Gerbi, S. A. (1999) U3 small nucleolar RNA is essential for cleavage at sites 1, 2 and 3 in pre-rRNA and determines which rRNA processing pathway is taken in Xenopus oocytes. J. Mol. Biol. 286, 1347-1363.
44. Borovjagin, A. V. and Gerbi, S. A. (2001) Xenopus U3 snoRNA GAC-Box A′ and Box A sequences play distinct functional roles in rRNA processing. Mol. Cell. Biol. 21, 6210-6221.
45. Borovjagin, A. V. and Gerbi, S. A. (2005) An evolutionary intra-molecular shift in the preferred U3 snoRNA binding site on pre-ribosomal RNA. Nucleic Acids Res. 33, 4995-5005.
46. Savino, R. and Gerbi, S. A. (1990) In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J. 9, 2299-2308.
47. Borovjagin, A. V. and Gerbi, S. A. (2000) The spacing between functional cis-elements of U3 snoRNA is critical for rRNA processing. J. Mol. Biol. 300, 57-74.
48. Beltrame, M. and Tollervey, D. (1995) Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J. 14, 4350-4356.
49. Borovjagin, A. V. and Gerbi, S. A. (2004) Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction. RNA 10, 942-953.
50. Hughes, J. M. (1996) Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA. J. Mol. Biol. 259, 645-654.
51. Méreau, A., Fournier, R., Grégoire, A., Mougin, A., Fabrizio, P., Lührmann, R. and Branlant, C. (1997) An in vivo and in vitro structure-function analysis of the Saccharomyces cerevisiae U3A snoRNP: protein-RNA contacts and base-pair interaction with the pre-ribosomal RNA. J. Mol. Biol. 273, 552-571.
52. Sharma, K. and Tollervey, D. (1999) Base pairing between U3 small nucleolar RNA and the 5′ end of 18S rRNA is required for pre-rRNA processing. Mol. Cell. Biol. 19, 6012-6019.
53. Billy, E., Wegierski, T., Nasr, F. and Filipowicz, W. (2000) Rcl1p, the yeast protein similar to the RNA 3′-phosphate cyclase, associates with U3 snoRNP and is required for 18S rRNA biogenesis. EMBO J. 19, 2115-2126.
54. Gelperin, D., Horton, L., Beckman, J., Hensold, J. and Lemmon, S. K. (2001) Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA 7, 1268-1283.
55. Karbstein, K. and Doudna, J. A. (2006) GTP-dependent formation of a ribonucleoprotein subcomplex required for ribosome biogenesis. J. Mol. Biol. 356, 432-443.
56. Karbstein, K., Jonas, S. and Doudna, J. A. (2005) An essential GTPase promotes assembly of preribosomal RNA processing complexes. Mol. Cell 20, 633-643.
57. Wegierski, T., Billy, E., Nasr, F. and Filipowicz, W. (2001) Bms1p, a G-domain-containing protein, associates with Rcl1p and is required for 18S rRNA biogenesis in yeast. RNA 7, 1254-1267.
58. Gerczei, T. and Correll, C. C. (2004) Imp3p and Imp4p mediate formation of essential U3-precursor rRNA (prerRNA) duplexes, possibly to recruit the small subunit processome to the pre-rRNA. Proc. Natl Acad. Sci. U. S. A. 101, 15301-15306.
59. Colley, A., Beggs, J. D., Tollervey, D. and Lafontaine, D. L. (2000) Dhr1p, a putative DEAH-box RNA helicase, is associated with the box C+D snoRNP U3. Mol. Cell. Biol. 20, 7238-7246.
60. Liang, X. H. and Fournier, M. J. (2006) The helicase Has1p is required for snoRNA release from pre-rRNA. Mol. Cell. Biol. 26, 7437-7450.
61. Tycowski, K. T., Shu, M. D. and Steitz, J. A. (1994) Requirement for intron-encoded U22 small nucleolar RNA in 18S ribosomal RNA maturation. Science 266, 1558-1561.
62. Li, H. D., Zagorski, J. and Fournier, M. J. (1990) Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 1145-1152.
63. Morrissey, J. P. and Tollervey, D. (1993) Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis. Mol. Cell. Biol. 13, 2469-2477.
64. Tollervey, D. (1987) A yeast small nuclear RNAis required for normal processing of pre-ribosomal RNA. EMBO J. 6, 4169-4175.
65. 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.
66. Morrissey, J. P. and Tollervey, D. (1997) U14 small nucleolar RNA makes multiple contacts with the pre-ribosomal RNA. Chromosoma 105, 515-522.
67. Jarmolowski, A., Zagorski, J., Li, H. V. and Fournier, M. J. (1990) Identification of essential elements in U14 RNA of Saccharomyces cerevisiae. EMBO J. 9, 4503-4509.
68. Liang, W. Q. and Fournier, M. J. (1995) U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev. 9, 2433-2443.
69. Atzorn, V., Fragapane, P. and Kiss, T. (2004) U17/snR30 is a ubiquitous snoRNA with two conserved sequence motifs essential for 18S rRNA production. Mol. Cell. Biol. 24, 1769-1778.
70. Bousquet-Antonelli, C., Henry, Y., Gélugne J. P., Caizergues-Ferrer, M. and Kiss, T. (1997) A small nucleolar RNP protein is required for pseudouridylation of eukaryotic ribosomal RNAs. EMBO J. 16, 4770-4776.
71. Brand, R. C., Klootwijk, J., Van Steenbergen, T. J., De Kok, A. J. and Planta, R. J. (1977) Secondary methylation of yeast ribosomal precursor RNA. Eur. J. Biochem. 75, 311-318.
72. Lapeyre, B. and Purushothaman, S. K. (2004) Spb1p-directed formation of Gm2922 in the ribosome catalytic center occurs at a late processing stage. Mol. Cell 16, 663-669.
73. Retel, J., van den Bos, R. C. and Planta, R. J. (1969) Characteristics of the methylation in vivo of ribosomal RNA in yeast. Biochim. Biophys. Acta 195, 370-380.
74. Cavaillé, J., Nicoloso, M. and Bachellerie, J. P. (1996) Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature 383, 732-735.
75. Kiss-László, Z., Henry, Y., Bachellerie, J. P., Caizergues-Ferrer, M. and Kiss, T. (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 85, 1077-1088.
76. Tycowski, K. T., Smith, C. M., Shu, M. D. and Steitz, J. A. (1996) A small nucleolar RNA requirement for site-specific ribose methylation of rRNAinXenopus. Proc. Natl Acad. Sci. U. S. A. 93, 14480-14485.
77. Ganot, P., Bortolin, M. L. and Kiss, T. (1997) Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89, 799-809.
78. Ni, J., Tien, A. L. and Fournier, M. J. (1997) Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell 89, 565-573.
79. Hoareau-Aveilla, C. and Henry, Y. (2007) BoxH/ACARNPs: from ribosomal formation to telomere maintenance. In:RNA Binding Proteins in Development and Disease, Denman, R. (ed.), Research SignPost, Kerala.
80. Kiss, T., Fayet, E., Jády, B. E., Richard, P. and Weber, M. (2006) Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold. Spring Harb. Symp. Quant. Biol. 71, 407-417.
81. Reichow, S. L., Hamma, T., Ferré-D'Amaré, A. R. and Varani, G. (2007) The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res. 35, 1452-1464.
82. Peculis, B. A. and Steitz, J. A. (1993) Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73, 1233-1245.
83. Dunbar, D. A. and Baserga, S. J. (1998) The U14 snoRNA is required for 2′-O-methylation of the pre-18S rRNA in Xenopus oocytes. RNA 4, 195-204.
84. King, T. H., Liu, B., McCully, R. R. and Fournier, M. J. (2003) Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol. Cell 11, 425-435.
85. Decatur, W. A., Liang, X. H., Piekna-Przybylska, D. and Fournier, M. J. (2007) Identifying effects of snoRNA-guided modifications on the synthesis and function of the yeast ribosome. Methods Enzymol. 425, 283-316.
86. Tollervey, D., Lehtonen, H., Jansen, R., Kern, H. and Hurt, E. C. (1993) Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly. Cell 72, 443-457.
87. Zebarjadian, Y., King, T., Fournier, M. J., Clarke, L. and Carbon, J. (1999) Point mutations in yeast CBF5can abolish in vivo pseudouridylation of rRNA. Mol. Cell. Biol. 19, 7461-7472.
88. Liang, X. H., Liu, Q. and Fournier, M. J. (2007) rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol. Cell 28, 965-977.
89. Kos, M. and Tollervey, D. (2005) The putative RNA helicase Dbp4p is required for release of the U14 snoRNA from preribosomes in Saccharomyces cerevisiae. Mol. Cell 20, 53-64.
90. Venema, J. and Tollervey, D. (1996) RRP5 is required for formation of both 18S and 5.8S rRNA in yeast. EMBO J. 15, 5701-5714.
91. Oeffinger, M., Wei, K. E., Rogers, R., Degrasse, J. A., Chait, B. T., Aitchison, J. D. and Rout, M. P. (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 4, 951-956.
92. Chu, S., Archer, R. H., Zengel, J. M. and Lindahl, L. (1994) The RNA of RNase MRP is required for normal processing of ribosomal RNA. Proc. Natl Acad. Sci. U. S. A. 91, 659-663.
93. Lygerou, Z., Allmang, C., Tollervey, D. and Séraphin, B. (1996) Accurate processing of a eukaryotic precursor ribosomal RNA by ribonuclease MRP in vitro. Science 272, 268-270.
94. Schmitt, M. E. and Clayton, D. A. (1993) Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 7935-7941.
95. Zhu, Y., Stribinskis, V., Ramos, K. S. and Li, Y. (2006) Sequence analysis of RNase MRPRNA reveals its origination from eukaryotic RNase P RNA. RNA 12, 699-706.
96. Altman, S. (1990) Enzymatic cleavage of RNA by RNA. Biosci. Rep. 10, 317-337.
97. Henry, Y., Wood, H., Morrissey, J. P., Petfalski, E., Kearsey, S. and Tollervey, D. (1994) The 5′ end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site. EMBO J. 13, 2452-2463.
98. Liu, Q., Greimann, J. C. and Lima, C. D. (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127, 1223-1237.
99. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M. and Tollervey, D. (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91, 457-466.
100. Mitchell, P., Petfalski, E. and Tollervey, D. (1996) The 3′ end of yeast 5.8S rRNAis generated by an exonuclease processing mechanism. Genes Dev. 10, 502-513.
101. Allmang, C., Kufel, J., Chanfreau, G., Mitchell, P., Petfalski, E. and Tollervey, D. (1999) Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 18, 5399-5410.
102. Briggs, M. W., Burkard, K. T. and Butler, J. S. (1998) Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J. Biol. Chem. 273, 13255-13263.
103. de la Cruz, J., Kressler, D., Tollervey, D. and Linder, P. (1998) Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J. 17, 1128-1140.
104. van Hoof, A., Lennertz, P. and Parker, R. (2000) Three conserved members of the RNase D family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase PRNAs in yeast. EMBO J. 19, 1357-1365.
105. Faber, A. W., Van Dijk, M., Raué, H. A. and Vos, J. C. (2002) Ngl2p is aCcr4p-like RNA nuclease essential for the final step in 3′-end processing of 5.8S rRNA in Saccharomyces cerevisiae. RNA 8, 1095-1101.
106. Geerlings, T. H., Vos, J. C. and Raué, H. A. (2000) The final step in the formation of 25S rRNA in Saccharomyces cerevisiae is performed by 5′→3′ exonucleases. RNA 6, 1698-1703.
107. Schilders, G., Raijmakers, R., Raats, J. M. and Pruijn, G. J. (2005) MPP6 is an exosome-associated RNA-binding protein involved in 5.8S rRNA maturation. Nucleic Acids Res. 33, 6795-6804.
108. Schilders, G., van Dijk, E. and Pruijn, G. J. (2007) C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res. 35, 2564-2572.
109. Michot, B., Joseph, N., Mazan, S. and Bachellerie, J. P. (1999) Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences. Nucleic Acids Res. 27, 2271-2282.
110. Peculis, B. A. (1997) The sequence of the 5′ end of the U8 small nucleolar RNA is critical for 5.8S and 28S rRNA maturation. Mol. Cell. Biol. 17, 3702-3713.
111. Okuwaki, M. (in press) The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J. Biochem.
112. Savkur, R. S. and Olson, M. O. (1998) Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res. 26, 4508-4515.
113. Bassler, J., Grandi, P., Gadal, O., Lessmann, T., Petfalski, E., Tollervey, D., Lechner, J. and Hurt, E. (2001) Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol. Cell 8, 517-529.
114. Fatica, A., Cronshaw, A. D., Dlakic, M. and Tollervey, D. (2002) Ssf1p prevents premature processing of an early pre-60S ribosomal particle. Mol. Cell 9, 341-351.
115. 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.
116. Saveanu, C., Bienvenu, D., Namane, A., Gleizes, P. E., Gas, N., Jacquier, A. and Fromont-Racine, M. (2001) Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J. 20, 6475-6484.
117. Saveanu, C., Namane, A., Gleizes, P. E., Lebreton, A., Rousselle, J. C., Noaillac-Depeyre, J., Gas, N., Jacquier, A. and Fromont-Racine, M. (2003) Sequential protein association with nascent 60S ribosomal particles. Mol. Cell. Biol. 23, 4449-4460.
118. Zagulski, M., Kressler, D., Becam, A. M., Rytka, J. and Herbert, C. J. (2003) Mak5p, which is required for the maintenance of the M1 dsRNA virus, is encoded by the yeast ORF YBR142w and is involved in the biogenesis of the 60S subunit of the ribosome. Mol. Genet. Genomics 270, 216-224.
119. Bond, A. T., Mangus, D. A., He, F. and Jacobson, A. (2001) Absence of Dbp2p alters both nonsense-mediated mRNA decay and rRNA processing. Mol. Cell. Biol. 21, 7366-7379.
120. Jalal, C., Uhlmann-Schiffler, H. and Stahl, H. (2007) Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res. 35, 3590-3601.
121. Weaver, P. L., Sun, C. and Chang, T. H. (1997) Dbp3p, a putative RNA helicase in Saccharomyces cerevisiae, is required for efficient pre-rRNA processing predominantly at site A3. Mol. Cell. Biol. 17, 1354-1365.
122. Kressler, D., de la Cruz, J., Rojo, M. and Linder, P. (1998) Dbp6p is an essential putative ATP-dependent RNA helicase required for 60S-ribosomal-subunit assembly in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 1855-1865.
123. Daugeron, M. C. and Linder, P. (1998) Dbp7p, a putative ATP-dependent RNA helicase from Saccharomyces cerevisiae, is required for 60S ribosomal subunit assembly. RNA 4, 566-581.
124. Daugeron, M. C., Kressler, D. and Linder, P. (2001) Dbp9p, a putative ATP-dependent RNA helicase involved in 60S-ribosomal-subunit biogenesis, functionally interacts with Dbp6p. RNA 7, 1317-1334.
125. Burger, F., Daugeron, M. C. and Linder, P. (2000) Dbp10p, a putative RNA helicase from Saccharomyces cerevisiae, is required for ribosome biogenesis. Nucleic Acids Res. 28, 2315-223.
126. Ripmaster, T. L., Vaughn, G. P. and Woolford, J. L., Jr. (1992) A putative ATP-dependent RNA helicase involved in Saccharomyces cerevisiae ribosome assembly. Proc. Natl Acad. Sci. U. S. A. 89, 11131-11135.
127. de la Cruz, J., Kressler, D., Rojo, M., Tollervey, D. and Linder, P. (1998) Spb4p, an essential putative RNA helicase, is required for a late step in the assembly of 60S ribosomal subunits in Saccharomyces cerevisiae. RNA 4, 1268-1281.
128. Bernstein, K. A., Granneman, S., Lee, A. V., Manickam, S. and Baserga, S. J. (2006) Comprehensive mutational analysis of yeast DEXD/H box RNA helicases involved in large ribosomal subunit biogenesis. Mol. Cell. Biol. 26, 1195-1208.
129. Emery, B., de la Cruz, J., Rocak, S., Deloche, O. and Linder, P. (2004) Has1p, a member of the DEAD-box family, is required for 40S ribosomal subunit biogenesis in Saccharomyces cerevisiae. Mol. Microbiol. 52, 141-158.
130. Combs, D. J., Nagel, R. J., Ares, M., Jr. and Stevens, S. W. (2006) Prp43p is a DEAH-box spliceosome disassembly factor essential for ribosome biogenesis. Mol. Cell. Biol. 26, 523-534.
131. Lebaron, S., Froment, C., Fromont-Racine, M., Rain, J. C., Monsarrat, B., Caizergues-Ferrer, M. and Henry, Y. (2005) The splicing ATPase prp43p is a component of multiple preribosomal particles. Mol. Cell. Biol. 25, 9269-9282.
132. Leeds, N. B., Small, E. C., Hiley, S. L., Hughes, T. R. and Staley, J. P. (2006) The splicing factor Prp43p, a DEAH box ATPase, functions in ribosome biogenesis. Mol. Cell. Biol. 26, 513-522.
133. Gadal, O., Strauss, D., Braspenning, J., Hoepfner, D., Petfalski, E., Philippsen, P., Tollervey, D. and Hurt, E. (2001) A nuclear AAA-type ATPase (Rix7p) is required for biogenesis and nuclear export of 60S ribosomal subunits. EMBO J. 20, 3695-3704.
134. Galani, K., Nissan, T. A., Petfalski, E., Tollervey, D. and Hurt, E. (2004) Rea1, a dynein-related nuclear AAA-ATPase, is involved in late rRNA processing and nuclear export of 60 S subunits. J. Biol. Chem. 279, 55411-55448.
135. Jensen, B. C., Wang, Q., Kifer, C. T. and Parsons, M. (2003) The NOG1 GTP-binding protein is required for biogenesis of the 60 S ribosomal subunit. J. Biol. Chem. 278, 32204-3211.
136. Kressler, D., Rojo, M., Linder, P. and Cruz, J. (1999) Spb1p is a putative methyltransferase required for 60S ribosomal subunit biogenesis in Saccharomyces cerevisiae. Nucleic Acids Res. 27, 4598-4608.
137. Pintard, L., Kressler, D. and Lapeyre, B. (2000) Spb1p is a yeast nucleolar protein associated with Nop1p and Nop58p that is able to bind S-adenosyl-L-methionine in vitro. Mol. Cell. Biol. 20, 1370-1381.
138. de Beus, E., Brockenbrough, J. S., Hong, B. and Aris, J. P. (1994) Yeast NOP2 encodes an essential nucleolar protein with homology to a human proliferation marker. J. Cell Biol. 127, 1799-1813.
139. Hong, B., Brockenbrough, J. S., Wu, P. and Aris, J. P. (1997) Nop2p is required for pre-rRNAprocessing and 60S ribosome subunit synthesis in yeast. Mol. Cell. Biol. 17, 378-388.
140. Shan, X., Xue, Z. and Mélèse, T. (1994) Yeast NPI46 encodes a novel prolyl cis-trans isomerase that is located in the nucleolus. J. Cell Biol. 126, 853-862.
141. Gadal, O., Strauss, D., Petfalski, E., Gleizes, P. E., Gas, N., Tollervey, D. and Hurt, E. (2002) Rlp7p is associated with 60S preribosomes, restricted to the granular component of the nucleolus, and required for pre-rRNA processing. J. Cell Biol. 157, 941-951.
142. Milkereit, P., Gadal, O., Podtelejnikov, A., Trumtel, S., Gas, N., Petfalski, E., Tollervey, D., Mann, M., Hurt, E. and Tschochner, H. (2001) Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 105, 499-509.
143. Dlakic, M. and Tollervey, D. (2004) The Noc proteins involved in ribosome synthesis and export contain divergent HEAT repeats. RNA 10, 351-354.
144. Adams, C. C., Jakovljevic, J., Roman, J., Harnpicharnchai, P. and Woolford, J. L., Jr. (2002) Saccharomyces cerevisiae nucleolar protein Nop7p is necessary for biogenesis of 60S ribosomal subunits. RNA 8, 150-165.
145. Du, Y. C. and Stillman, B. (2002) Yph1p, an ORC-interacting protein: potential links between cell proliferation control, DNA replication, and ribosome biogenesis. Cell 109, 835-848.
146. Holzel, M., Rohrmoser, M., Schlee, M., Grimm, T., Harasim, T., Malamoussi, A., Gruber-Eber, A., Kremmer, E., Hiddemann, W., Bornkamm, G. W. and Eick, D. (2005) Mammalian WDR12 is a novel member of the Pes1-Bop1 complex and is required for ribosome biogenesis and cell proliferation. J. Cell Biol. 170, 367-378.
147. Lapik, Y. R., Fernandes, C. J., Lau, L. F. and Pestov, D. G. (2004) Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol. Cell 15, 17-29.
148. Lerch-Gaggl, A., Haque, J., Li, J., Ning, G., Traktman, P. and Duncan, S. A. (2002) Pescadillo is essential for nucleolar assembly, ribosome biogenesis, and mammalian cell proliferation. J. Biol. Chem. 277, 45347-45355.
149. Oeffinger, M., Leung, A., Lamond, A. and Tollervey, D. (2002) Yeast Pescadillo is required for multiple activities during 60S ribosomal subunit synthesis. RNA 8, 626-636.
150. Pestov, D. G., Stockelman, M. G., Strezoska, Z. and Lau, L. F. (2001) ERB1, the yeast homolog of mammalian Bop1, is an essential gene required for maturation of the 25S and 5.8S ribosomal RNAs. Nucleic Acids Res. 29, 3621-3630.
151. Strezoska, Z., Pestov, D. G. and Lau, L. F. (2000) Bop1 is a mouse WD40 repeat nucleolar protein involved in 28S and 5. 8S RRNA processing and 60S ribosome biogenesis. Mol. Cell. Biol. 20, 5516-5528.
152. Strezoska, Z., Pestov, D. G. and Lau, L. F. (2002) Functional inactivation of the mouse nucleolar protein Bop1 inhibits multiple steps in pre-rRNA processing and blocks cell cycle progression. J. Biol. Chem. 277, 29617-29625.
153. Miles, T. D., Jakovljevic, J., Horsey, E. W., Harnpicharnchai, P., Tang, L. and Woolford, J. L., Jr. (2005) Ytm1, Nop7, and Erb1 form a complex necessary for maturation of yeast 66S preribosomes. Mol. Cell. Biol. 25, 10419-10432.
154. Rohrmoser, M., Holzel, M., Grimm, T., Malamoussi, A., Harasim, T., Orban, M., Pfisterer, I., Gruber-Eber, A., Kremmer, E. and Eick, D. (2007) Interdependence of Pes1, Bop1, and WDR12 controls nucleolar localization and assembly of the PeBoW complex required for maturation of the 60S ribosomal subunit. Mol. Cell. Biol. 27, 3682-3694.
155. Saveanu, C., Rousselle, J. C., Lenormand, P., Namane, A., Jacquier, A. and Fromont-Racine, M. (2007) The p21-activated protein kinase inhibitor Skb15 and its budding yeast homologue are 60S ribosome assembly factors. Mol. Cell. Biol. 27, 2897-2909.
156. Rosado, I. V., Dez, C., Lebaron, S., Caizergues-Ferrer, M., Henry, Y. and de la Cruz, J. (2007) Characterization of Saccharomyces cerevisiae Npa2p (Urb2p) reveals a low-molecular-mass complex containing Dbp6p, Npa1p (Urb1p), Nop8p, and Rsa3p involved in early steps of 60S ribosomal subunit biogenesis. Mol. Cell. Biol. 27, 1207-1221.
157. Nissan, T. A., Galani, K., Maco, B., Tollervey, D., Aebi, U. and Hurt, E. (2004) A pre-ribosome with a tadpole-like structure functions in ATP-dependent maturation of 60S subunits. Mol. Cell 15, 295-301.
158. Schäfer, T., Strauss, D., Petfalski, E., Tollervey, D. and Hurt, E. (2003) The path from nucleolar 90S to cytoplasmic 40S preribosomes. EMBO J. 22, 1370-1380.
159. Chen, W., Bucaria, J., Band, D. A., Sutton, A. and Sternglanz, R. (2003) Enp1, a yeast protein associated with U3 and U14 snoRNAs, is required for pre-rRNA processing and 40S subunit synthesis. Nucleic Acids Res. 31, 690-699.
160. Fatica, A., Oeffinger, M., Dlakic, M. and Tollervey, D. (2003) Nob1p is required for cleavage of the 3′ end of 18S rRNA. Mol. Cell. Biol. 23, 1798-1807.
161. Oeffinger, M., Dlakic, M. and Tollervey, D. (2004) A preribosome- associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev. 18, 196-209.
162. Vanrobays, E., Gélugne, J. P., Caizergues-Ferrer, M. and Lafontaine, D. L. (2004) Dim2p, a KH-domain protein required for small ribosomal subunit synthesis. RNA 10, 645-656.
163. Loar, J. W., Seiser, R. M., Sundberg, A. E., Sagerson, H. J., Ilias, N., Zobel-Thropp, P., Craig, E. A. and Lycan, D. E. (2004) Genetic and biochemical interactions among Yar1, Ltv1 and Rps3 define novel links between environmental stress and ribosome biogenesis in Saccharomyces cerevisiae. Genetics 168, 1877-1889.
164. Vanrobays, E., Gélugne, J. P., Gleizes, P. E. and Caizergues-Ferrer, M. (2003) Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 23, 2083-2095.
165. Vanrobays, E., Gleizes, P. E., Bousquet-Antonelli, C., Noaillac-Depeyre, J., Caizergues-Ferrer, M. and Gélugne, J. P. (2001) Processing of 20S pre-rRNA to 18S ribosomal RNA in yeast requires Rrp10p, an essential non-ribosomal cytoplasmic protein. EMBO J. 20, 4204-4213.
166. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S. and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-6891.
167. Seiser, R. M., Sundberg, A. E., Wollam, B. J., Zobel-Thropp, P., Baldwin, K., Spector, M. D. and Lycan, D. E. (2006) Ltv1 is required for efficient nuclear export of the ribosomal small subunit in Saccharomyces cerevisiae. Genetics 174, 679-691.
168. Léger-Silvestre, I., Caffrey, J. M., Dawaliby, R., Alvarez-Arias, D. A., Gas, N., Bertolone, S. J., Gleizes, P. E. and Ellis, S. R. (2005) Specific Role forYeast homologs of the Diamond Blackfan anemia-associated Rps19 Pprotein in Rribosome synthesis. J. Biol. Chem. 280, 38177-38185.
169. Schäfer, T., Maco, B., Petfalski, E., Tollervey, D., Bottcher, B., Aebi, U. and Hurt, E. (2006) Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441, 651-655.
170. Bataille, N., Helser, T. and Fried, H. M. (1990) Cytoplasmic transport of ribosomal subunits microinjected into the Xenopus laevis oocyte nucleus: a generalized, facilitated process. J. Cell Biol. 111, 1571-1582.
171. Khanna-Gupta, A. and Ware, V. C. (1989) Nucleocytoplasmic transport of ribosomes in a eukaryotic system: is there a facilitated transport process? Proc. Natl Acad. Sci. U. S. A. 86, 1791-1795.
172. Pemberton, L. F. and Paschal, B. M. (2005) Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6, 187-198.
173. Gleizes, P. E., Noaillac-Depeyre, J., Léger-Silvestre, I., Teulières, F., Dauxois, J. Y., Pommet, D., Azum-Gélade, M. C. and Gas, N. (2001) Ultrastructural localization of rRNA shows defective nuclear export of preribosomes in mutants of the Nup82p complex. J. Cell Biol. 155, 923-936.
174. Hurt, E., Hannus, S., Schmelzl, B., Lau, D., Tollervey, D. and Simos, G. (1999) A novel in vivo assay reveals inhibition of ribosomal nuclear export in ran-cycle and nucleoporin mutants. J. Cell Biol. 144, 389-401.
175. Stage-Zimmermann, T., Schmidt, U. and Silver, P. A. (2000) Factors affecting nuclear export of the 60S ribosomal subunit in vivo. Mol. Biol. Cell 11, 3777-3789.
176. Moy, T. I. and Silver, P. A. (1999) Nuclear export of the small ribosomal subunit requires the ran-GTPase cycle and certain nucleoporins. Genes Dev. 13, 2118-2133.
177. Moy, T. I. and Silver, P. A. (2002) Requirements for the nuclear export of the small ribosomal subunit. J. Cell Sci. 115, 2985-2995.
178. Trotta, C. R., Lund, E., Kahan, L., Johnson, A. W. and Dahlberg, J. E. (2003) Coordinated nuclear export of 60S ribosomal subunits and NMD3 in vertebrates. EMBO J. 22, 2841-2851.
179. Cheng, Y., Dahlberg, J. E. and Lund, E. (1995) Diverse effects of the guanine nucleotide exchange factor RCC1 on RNA transport. Science 267, 1807-1810.
180. Bernad, R., Engelsma, D., Sanderson, H., Pickersgill, H. and Fornerod, M. (2006) Nup214-Nup88 nucleoporin subcomplex is required for CRM1-mediated 60 S preribosomal nuclear export. J. Biol. Chem. 281, 19378-19386.
181. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I. W. (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060.
182. Stade, K., Ford, C. S., Guthrie, C. and Weis, K. (1997) Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90, 1041-1050.
183. Gadal, O., Strauss, D., Kessl, J., Trumpower, B., Tollervey, D. and Hurt, E. (2001) Nuclear export of 60 s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol. Cell. Biol. 21, 3405-3415.
184. 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.
185. Ho, J. H. and Johnson, A. W. (1999) NMD3 encodes an essential cytoplasmic protein required for stable 60S ribosomal subunits in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 2389-2399.
186. Kallstrom, G., Hedges, J. and Johnson, A. (2003) The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol. Cell. Biol. 23, 4344-4355.
187. Belk, J. P., He, F. and Jacobson, A. (1999) Overexpression of truncated Nmd3p inhibits protein synthesis in yeast. RNA 5, 1055-1070.
188. Thomas, F. and Kutay, U. (2003) Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J. Cell Sci. 116, 2409-2419.
189. Santos-Rosa, H., Moreno, H., Simos, G., Segref, A., Fahrenkrog, B., Pante, N. and Hurt, E. (1998) Nuclear mRNA export requires complex formation between Mex67p and Mtr2p at the nuclear pores. Mol. Cell. Biol. 18, 6826-6838.
190. Strasser, K., Bassler, J. and Hurt, E. (2000) Binding of the Mex67p/Mtr2p heterodimer to FXFG, GLFG, and FG repeat nucleoporins is essential for nuclear mRNA export. J. Cell Biol. 150, 695-706.
191. Yao, W., Roser, D., Kohler, A., Bradatsch, B., Bassler, J. and Hurt, E. (2007) Nuclear export of ribosomal 60S subunits by the general mRNA export receptor Mex67-Mtr2. Mol. Cell 26, 51-62.
192. Yao, W., Lutzmann, M. and Hurt, E. (2008) A versatile interaction platform on the Mex67-Mtr2 receptor creates an overlap between mRNA and ribosome export. EMBO J. 27, 6-16.
193. Bradatsch, B., Katahira, J., Kowalinski, E., Bange, G., Yao, W., Sekimoto, T., Baumgartel, V., Boese, G., Bassler, J., Wild, K., Peters, R., Yoneda, Y., Sinning, I. and Hurt, E. (2007) Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit. Mol. Cell 27, 767-779.
194. Hung, N. J. and Johnson, A. W. (2006) Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae. Mol. Cell. Biol. 26, 3718-3727.
195. Rouquette, J., Choesmel, V. and Gleizes, P. E. (2005) Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J. 24, 2862-2872.
196. Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M. and Sakaki, Y. (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl Acad. Sci. U. S. A. 98, 4569-4574.
197. Noguchi, E., Hayashi, N., Nakashima, N. and Nishimoto, T. (1997) Yrb2p, a Nup2p-related yeast protein, has a functional overlap with Rna1p, a yeast Ran-GTPase-activating protein. Mol. Cell. Biol. 17, 2235-2246.
198. Taura, T., Schlenstedt, G. and Silver, P. A. (1997) Yrb2p is a nuclear protein that interacts with Prp20p, a yeast Rcc1 homologue. J. Biol. Chem. 272, 31877-31884.
199. Taura, T., Krebber, H. and Silver, P. A. (1998) A member of the Ran-binding protein family, Yrb2p, is involved in nuclear protein export. Proc. Natl Acad. Sci. U. S. A. 95, 7427-732.
200. Léger-Silvestre, I., Milkereit, P., Ferreira-Cerca, S., Saveanu, C., Rousselle, J. C., Choesmel, V., Guinefoleau, C., Gas, N. and Gleizes, P. E. (2004) The ribosomal protein Rps15p is required for nuclear exit of the 40S subunit precursors in yeast. EMBO J. 23, 2336-2347.
201. Warner, J. R. (1971) The assembly of ribosomes in yeast. J. Biol. Chem. 246, 447-454.
202. 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.
203. West, M., Hedges, J. B., Chen, A. and Johnson, A. W. (2005) Defining the order in which Nmd3p and Rpl10p load onto nascent 60S ribosomal subunits. Mol. Cell. Biol. 25, 3802-3813.
204. Hofer, A., Bussiere, C. and Johnson, A. W. (2007) Mutational analysis of the ribosomal protein Rpl10 from yeast. J. Biol. Chem. 282, 32630-32639.
205. Pertschy, B., Saveanu, C., Zisser, G., Lebreton, A., Tengg, M., Jacquier, A., Liebminger, E., Nobis, B., Kappel, L., van der Klei, I., Hogenauer, G., Fromont-Racine, M. and Bergler, H. (2007) Cytoplasmic recycling of 60S preribosomal factors depends on the AAA protein Drg1. Mol. Cell. Biol. 27, 6581-6592.
206. Zakalskiy, A., Hogenauer, G., Ishikawa, T., Wehrschutz-Sigl, E., Wendler, F., Teis, D., Zisser, G., Steven, A. C. and Bergler, H. (2002) Structural and enzymatic properties of the AAA protein Drg1p from Saccharomyces cerevisiae: decoupling of intracellular function from ATPase activity and hexamerization. J. Biol. Chem. 277, 26788-26795.
207. Lebreton, A., Saveanu, C., Decourty, L., Rain, J. C., Jacquier, A. and Fromont-Racine, M. (2006) A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J. Cell Biol. 173, 349-360.
208. Demoinet, E., Jacquier, A., Lutfalla, G. and Fromont-Racine, M. (2007) The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae. RNA 13, 1570-1581.
209. Meyer, A. E., Hung, N. J., Yang, P., Johnson, A. W. and Craig, E. A. (2007) The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunit biogenesis. Proc. Natl Acad. Sci. U. S. A. 104, 1558-1563.
210. Menne, T. F., Goyenechea, B., Sanchez-Puig, N., Wong, C. C., Tonkin, L. M., Ancliff, P. J., Brost, R. L., Costanzo, M., Boone, C. and Warren, A. J. (2007) The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nat. Genet. 39, 486-495.
211. Senger, B., Lafontaine, D. L., Graindorge, J. S., Gadal, O., Camasses, A., Sanni, A., Garnier, J. M., Breitenbach, M., Hurt, E. and Fasiolo, F. (2001) The nucle(ol)arTif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 8, 1363-1373.
212. Ceci, M., Gaviraghi, C., Gorrini, C., Sala, L. A., Offenhauser, N., Marchisio, P. C. and Biffo, S. (2003) Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426, 579-584.
213. Si, K. and Maitra, U. (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.
214. Lafontaine, D., Delcour, J., Glasser, A. L., Desgres, J. and Vandenhaute, J. (1994) The DIM1 gene responsible for the conserved m6(2)Am6(2)A dimethylation in the 3′-terminal loop of 18 S rRNA is essential in yeast. J. Mol. Biol. 241, 492-497.
215. Lafontaine, D., Vandenhaute, J. and Tollervey, D. (1995) The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev. 9, 2470-2481.
216. Lafontaine, D. L., Preiss, T. and Tollervey, D. (1998) Yeast 18S rRNA dimethylase Dim1p: a quality control mechanism in ribosome synthesis? Mol. Cell. Biol. 18, 2360-2370.
217. Arcus, V. L., Backbro, K., Roos, A., Daniel, E. L. and Baker, E. N. (2004) Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J. Biol. Chem. 279, 16471-16478.
218. Fatica, A., Tollervey, D. and Dlakic, M. (2004) PIN domain of Nob1p is required for D-site cleavage in 20S pre-rRNA. RNA 10, 1698-1701.
219. Granneman, S., Nandineni, M. R. and Baserga, S. J. (2005) The putative NTPase Fap7 mediates cytoplasmic 20S prer-RNA processing through a direct interaction with Rps14. Mol. Cell. Biol. 25, 10352-10364.
220. Angermayr, M. and Bandlow, W. (2002) RIO1, an extraordinary novel protein kinase. FEBS Lett. 524, 31-36.
221. Angermayr, M., Roidl, A. and Bandlow, W. (2002) Yeast Rio1p is the founding member of a novel subfamily of protein serine kinases involved in the control of cell cycle progression. Mol. Microbiol. 44, 309-324.
222. Geerlings, T. H., Faber, A. W., Bister, M. D., Vos, J. C. and Raué, H. A. (2003) Rio2p, an evolutionarily conserved, low abundant protein kinase essential for processing of 20 S PrerRNA in Saccharomyces cerevisiae. J. Biol. Chem. 278, 22537-22545.
223. Laronde-Leblanc, N., Guszczynski, T., Copeland, T. and Wlodawer, A. (2005) Structure and activity of the atypical serine kinase Rio1. FEBS J. 272, 3698-3713.
224. LaRonde-LeBlanc, N., Guszczynski, T., Copeland, T. and Wlodawer, A. (2005)Autophosphorylation of Archaeoglobus fulgidus Rio2 and crystal structures of its nucleotide-metal ion complexes. FEBS J. 272, 2800-2810.
225. LaRonde-LeBlanc, N. and Wlodawer, A. (2005) A family portrait of the RIO kinases. J. Biol. Chem. 280, 37297-37300.
226. LaRonde-LeBlanc, N. and Wlodawer, A. (2005) The RIO kinases: an atypical protein kinase family required for ribosome biogenesis and cell cycle progression. Biochim. Biophys. Acta 1754, 14-24.
227. Gavin, A. C., Bosche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J. M., Michon, A. M., Cruciat, C. M., Remor, M., Hofert, C., Schelder, M., Brajenovic, M., Ruffner, H., Merino, A., Klein, K., Hudak, M., Dickson, D., Rudi, T., Gnau, V., Bauch, A., Bastuck, S., Huhse, B., Leutwein, C., Heurtier, M. A., Copley, R. R., Edelmann, A., Querfurth, E., Rybin, V., Drewes, G., Raida, M., Bouwmeester, T., Bork, P., Séraphin, B., Kuster, B., Neubauer, G. and Superti-Furga, G. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147.
228. Ford, C. L., Randal-Whitis, L. and Ellis, S. R. (1999) Yeast proteins related to the p40/laminin receptor precursor are required for 20S ribosomal RNA processing and the maturation of 40S ribosomal subunits. Cancer Res. 59, 704-710.
229. Tabb-Massey, A., Caffrey, J. M., Logsden, P., Taylor, S., Trent, J. O. and Ellis, S. R. (2003) Ribosomal proteins Rps0 and Rps21 of Saccharomyces cerevisiae have overlapping functions in the maturation of the 3′ end of 18S rRNA. Nucleic Acids Res. 31, 6798-6805.
230. Jakovljevic, J., de Mayolo, P. A., Miles, T. D., Nguyen, T. M., Léger-Silvestre, I., Gas, N. and Woolford, J. L., Jr. (2004) The carboxy-terminal extension of yeast ribosomal protein S14 is necessary for maturation of 43S preribosomes. Mol. Cell 14, 331-342.
231. Spahn, C. M., Beckmann, R., Eswar, N., Penczek, P. A., Sali, A., Blobel, G. and Frank, J. (2001) Structure of the 80S ribosome from Saccharomyces cerevisiae -tRNA-ribosome and subunit-subunit interactions. Cell 107, 373-386.
232. Hage, A. E. and Tollervey, D. (2004) A surfeit of factors: why is ribosome assembly so much more complicated in eukaryotes than bacteria? RNA Biol. 1, 10-15.
233. Dez, C., Houseley, J. and Tollervey, D. (2006) Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 25, 1534-1546.
234. Kadaba, S., Krueger, A., Trice, T., Krecic, A. M., Hinnebusch, A. G. and Anderson, J. (2004) Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 18, 1227-1240.
235. LaCava, J., Houseley, J., Saveanu, C., Petfalski, E., Thompson, E., Jacquier, A. and Tollervey, D. (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121, 713-724.
236. Vanacova, S., Wolf, J., Martin, G., Blank, D., Dettwiler, S., Friedlein, A., Langen, H., Keith, G. and Keller, W. (2005) A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3, e189.
237. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J. C., Dufour, M. E., Boulay, J., Regnault, B., Devaux, F., Namane, A., Séraphin, B., Libri, D. and Jacquier, A. (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121, 725-737.
238. Houseley, J., LaCava, J. and Tollervey, D. (2006)RNA-quality control by the exosome. Nat. Rev. Mol. Cell. Biol. 7, 529-539.
239. LaRivière, F. J., Cole, S. E., Ferullo, D. J. and Moore, M. J. (2006) A late-acting quality control process for mature eukaryotic rRNAs. Mol. Cell 24, 619-626.
240. Selker, E. U., Stevens, J. N. and Metzenberg, R. L. (1985) Heterogeneity of 5S RNA in fungal ribosomes. Science 227, 1340-1343.
241. Komili, S., Farny, N. G., Roth, F. P. and Silver, P. A. (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131, 557-571.