Eukaryotic ribosome biogenesis at a glance

Journal of Cell Science

Volumn 126, Issue 21, 2013, Pages 4815-4821

  Thomson, Emma ^a   Ferreira Cerca, Sébastien ^a,b   Hurt, Ed ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA DIRECTED RNA POLYMERASE; ENDONUCLEASE; EXONUCLEASE; EXPORTIN 1; GUANOSINE TRIPHOSPHATASE; HELICASE; INITIATION FACTOR; INTERNAL TRANSCRIBED SPACER; PEPTIDYLTRANSFERASE; RIBOSOME PROTEIN; RIBOSOME RNA; RNA 18S; RNA 5.8S; RNA POLYMERASE; TATA BINDING PROTEIN; TRANSLATION TERMINATION FACTOR;

ARTICLE; BINDING SITE; BIOGENESIS; CELL DIVISION; CELL MATURATION; CYTOPLASM; DISSOCIATION; ELECTRON MICROSCOPY; EUKARYOTE; EUKARYOTIC CELL; EXOSOME; GENETIC DISORDER; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR PORE COMPLEX; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; RIBOSOME; RIBOSOME SUBUNIT; RNA DEGRADATION; X RAY CRYSTALLOGRAPHY;

ANIMALS; EUKARYOTA; HUMANS; RIBOSOMAL PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE;

EID: 84887591511     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.111948     Document Type: Article

References (125)

1. Allmang, C., Mitchell, P., Petfalski, E. and Tollervey, D. (2000). Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res., 28, 1684-1691.
2. Bassler, J., Kallas, M., Pertschy, B., Ulbrich, C., Thoms, M. and Hurt, E. (2010). The AAA-ATPase Rea1 drives removal of biogenesis factors during multiple stages of 60S ribosome assembly. Mol. Cell, 38, 712-721.
3. Bassler, J., Klein, I., Schmidt, C., Kallas, M., Thomson, E., Wagner, M. A., Bradatsch, B., Rechberger, G., Strohmaier, H., Hurt, E. et al. (2012). The conserved Bud20 zinc finger protein is a new component of the ribosomal 60S subunit export machinery. Mol. Cell. Biol., 32, 4898-4912.
4. Beltrame, M. and Tollervey, D. (1992). Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J., 11, 1531-1542.
5. 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.
6. Beltrame, M., Henry, Y. and Tollervey, D. (1994). Mutational analysis of an essential binding site for the U3 snoRNA in the 59 external transcribed spacer of yeast pre-rRNA. Nucleic Acids Res., 22, 4057-4065.
7. Bernstein, K. A., Gallagher, J. E., Mitchell, B. M., Granneman, S. and Baserga, S. J. (2004). The smallsubunit processome is a ribosome assembly intermediate. Eukaryot. Cell, 3, 1619-1626.
8. Bolze, A., Mahlaoui, N., Byun, M., Turner, B., Trede, N., Ellis, S. R., Abhyankar, A., Itan, Y., Patin, E., Brebner, S. et al. (2013). Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia. Science, 340, 976-978.
9. Bradatsch, B., Katahira, J., Kowalinski, E., Bange, G., Yao, W., Sekimoto, T., Baumgärtel, V., Boese, G., Bassler, J., Wild, K. et al. (2007). Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit. Mol. Cell, 27, 767-779.
10. Bradatsch, B., Leidig, C., Granneman, S., Gnädig, M., Tollervey, D., Böttcher, B., Beckmann, R. and Hurt, E. (2012). Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel. Nat. Struct. Mol. Biol., 19, 1234-1241.
11. Burger, K., Mühl, B., Rohrmoser, M., Coordes, B., Heidemann, M., Kellner, M., Gruber-Eber, A., Heissmeyer, V., Strässer, K. and Eick, D. (2013). Cyclin-dependent kinase 9 links RNA Polymerase II transcription to processing of ribosomal RNA. J. Biol. Chem., 288, 21173-21183.
12. Carron, C., O'Donohue, M. F., Choesmel, V., Faubladier, M. and Gleizes, P. E. (2011). Analysis of two human pre-ribosomal factors, bystin and hTsr1, highlights differences in evolution of ribosome biogenesis between yeast and mammals. Nucleic Acids Res., 39, 280-291.
13. Cavaillé, J. and Bachellerie, J. P. (1998). SnoRNAguided ribose methylation of rRNA: structural features of the guide RNA duplex influencing the extent of the reaction. Nucleic Acids Res., 26, 1576-1587.
14. 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.
15. Cole, S. E., LaRiviere, F. J., Merrikh, C. N. and Moore, M. J. (2009). A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol. Cell, 34, 440-450.
16. Decatur, W. A. and Fournier, M. J. (2002). rRNA modifications and ribosome function. Trends Biochem. Sci., 27, 344-351.
17. 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.
18. 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.
19. Donati, G., Peddigari, S., Mercer, C. A. and Thomas, G. (2013). 5S ribosomal RNA is an essential component of a nascent ribosomal precursor complex that regulates the Hdm2-p53 checkpoint. Cell Rep., 4, 87-98.
20. 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. et al. (2002). A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature, 417, 967-970.
21. Drygin, D., Rice, W. G. and Grummt, I. (2010). The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu. Rev. Pharmacol. Toxicol., 50, 131-156.
22. Dunbar, D. A., Dragon, F., Lee, S. J. and Baserga, S. J. (2000). A nucleolar protein related to ribosomal protein L7 is required for an early step in large ribosomal subunit biogenesis. Proc. Natl. Acad. Sci. USA, 97, 13027-13032.
23. Fatica, A., Oeffinger, M., Tollervey, D. and Bozzoni, I. (2003). Cic1p/Nsa3p is required for synthesis and nuclear export of 60S ribosomal subunits. RNA, 9, 1431-1436.
24. Faza, M. B., Chang, Y., Occhipinti, L., Kemmler, S. and Panse, V. G. (2012). Role of Mex67-Mtr2 in the nuclear export of 40S pre-ribosomes. PLoS Genet. 8, e1002915.
25. Ferreira-Cerca, S., Pöll, 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.
26. Ferreira-Cerca, S., Pöll, G., Kühn, 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.
27. Filipovska, A. and Rackham, O. (2013). Specialization from synthesis: how ribosome diversity can customize protein function. FEBS Lett., 587, 1189-1197.
28. Finch, A. J., Hilcenko, C., Basse, N., Drynan, L. F., Goyenechea, B., Menne, T. F., González Fernández, A., Simpson, P., D'Santos, C. S., Arends, M. J. et al. (2011). Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome. Genes Dev., 25, 917-929.
29. Freed, E. F., Bleichert, F., Dutca, L. M. and Baserga, S. J. (2010). When ribosomes go bad: diseases of ribosome biogenesis. Mol. Biosyst., 6, 481-493.
30. Fromont-Racine, M., Senger, B., Saveanu, C. and Fasiolo, F. (2003). Ribosome assembly in eukaryotes. Gene, 313, 17-42.
31. Gadal, O., Strauss, D., Kessl, J., Trumpower, B., Tollervey, D. and Hurt, E. (2001). Nuclear export of 60s 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.
32. 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, 941-952.
33. 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.
34. Ganot, P., Bortolin, M. L. and Kiss, T. (1997a). Sitespecific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell, 89, 799-809.
35. Ganot, P., Caizergues-Ferrer, M. and Kiss, T. (1997b). The family of box ACA small nucleolar RNAs is defined by an evolutionarily conserved secondary structure and ubiquitous sequence elements essential for RNA accumulation. Genes Dev., 11, 941-956.
36. Grandi, P., Rybin, V., Bassler, J., Petfalski, E., Strauss, D., Marzioch, M., Schäfer, 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.
37. Granneman, S. and Baserga, S. J. (2005). Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing. Curr. Opin. Cell Biol., 17, 281-286.
38. Granneman, S., Petfalski, E., Swiatkowska, A. and Tollervey, D. (2010). Cracking pre-40S ribosomal subunit structure by systematic analyses of RNAprotein cross-linking. EMBO J., 29, 2026-2036.
39. Granneman, S., Petfalski, E. and Tollervey, D. (2011). A cluster of ribosome synthesis factors regulate prerRNA folding and 5.8S rRNA maturation by the Rat1 exonuclease. EMBO J., 30, 4006-4019.
40. Greber, B. J., Boehringer, D., Montellese, C. and Ban, N. (2012). Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. Nat. Struct. Mol. Biol., 19, 1228-1233.
41. Green, R. and Noller, H. F. (1997). Ribosomes and translation. Annu. Rev. Biochem., 66, 679-716.
42. Hackmann, A., Gross, T., Baierlein, C. and Krebber, H. (2011). The mRNA export factor Npl3 mediates the nuclear export of large ribosomal subunits. EMBO Rep., 12, 1024-1031.
43. 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.
44. 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.
45. Henras, A. K., Soudet, J., Gérus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A. and Henry, Y. (2008). The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci., 65, 2334-2359.
46. 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.
47. Horn, H. F. and Vousden, K. H. (2008). Cooperation between the ribosomal proteins L5 and L11 in the p53 pathway. Oncogene, 27, 5774-5784.
48. Kappel, L., Loibl, M., Zisser, G., Klein, I., Fruhmann, G., Gruber, C., Unterweger, S., Rechberger, G., Pertschy, B. and Bergler, H. (2012). Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation. J. Cell Biol., 199, 771-782.
49. 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.
50. 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.
51. Kiss-László, Z., Henry, Y., Bachellerie, J.-P., Caizergues-Ferrer, M. and Kiss, T. (1996). Sitespecific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell, 85, 1077-1088.
52. Kiss-László, Z., Henry, Y. and Kiss, T. (1998). Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO J., 17, 797-807.
53. 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.
54. Kondrashov, N., Pusic, A., Stumpf, C. R., Shimizu, K., Hsieh, A. C., Xue, S., Ishijima, J., Shiroishi, T. and Barna, M. (2011). Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell, 145, 383-397.
55. Koš, M. and Tollervey, D. (2010). Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell, 37, 809-820.
56. Kressler, D., Roser, D., Pertschy, B. and Hurt, E. (2008). The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles. J. Cell Biol., 181, 935-944.
57. Kressler, D., Hurt, E. and Bassler, J. (2010). Driving ribosome assembly. Biochim. Biophys. Acta, 1803, 673-683.
58. Kressler, D., Hurt, E., Bergler, H. and Bassler, J. (2012). The power of AAA-ATPases on the road of pre-60S ribosome maturation - molecular machines that strip pre-ribosomal particles. Biochim. Biophys. Acta, 1823, 92-100.
59. Lamanna, A. C. and Karbstein, K. (2009). Nob1 binds the single-stranded cleavage site D at the 39-end of 18S rRNA with its PIN domain. Proc. Natl. Acad. Sci. USA, 106, 14259-14264.
60. Landowski, M., O'Donohue, M. F., Buros, C., Ghazvinian, R., Montel-Lehry, N., Vlachos, A., Sieff, C. A., Newburger, P. E., Niewiadomska, E., Matysiak, M. et al. (2013). Novel deletion of RPL15 identified by array-comparative genomic hybridization in Diamond-Blackfan anemia. Hum. Genet. [Epub ahead of print] doi:10.1007/s00439-013-1326-z%T.
61. LaRiviere, 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.
62. Lebaron, S., Schneider, C., van Nues, R. W., Swiatkowska, A., Walsh, D., Böttcher, B., Granneman, S., Watkins, N. J. and Tollervey, D. (2012). Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol., 19, 744-753.
63. 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.
64. 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.
65. Littlefield, J. W. and Dunn, D. B. (1958a). Natural occurrence of thymine and three methylated adenine bases in several ribonucleic acids. Nature, 181, 254-255.
66. Littlefield, J. W. and Dunn, D. B. (1958b). The occurrence and distribution of thymine and three methylated-adenine bases in ribonucleic acids from several sources. Biochem. J., 70, 642-651.
67. Lo, K. Y., Li, Z., Wang, F., Marcotte, E. M. and Johnson, A. W. (2009). Ribosome stalk assembly requires the dual-specificity phosphatase Yvh1 for the exchange of Mrt4 with P0. J. Cell Biol., 186, 849-862.
68. 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.
69. Marneros, A. G. (2013). BMS1 is mutated in aplasia cutis congenita. PLoS Genet. 9, e1003573.
70. Mauro, V. P. and Edelman, G. M. (2002). The ribosome filter hypothesis. Proc. Natl. Acad. Sci. USA, 99, 12031-12036.
71. Mauro, V. P. and Edelman, G. M. (2007). The ribosome filter redux. Cell Cycle, 6, 2246-2251.
72. McIntosh, K. B. and Warner, J. R. (2007). Yeast ribosomes: variety is the spice of life. Cell, 131, 450-451.
73. Menne, T. F., Goyenechea, B., Sánchez-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.
74. Meyer, A. E., Hoover, L. A. and Craig, E. A. (2010). The cytosolic J-protein, Jjj1, and Rei1 function in the removal of the pre-60 S subunit factor Arx1. J. Biol. Chem., 285, 961-968.
75. 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.
76. Miller, O. L., Jr and Beatty, B. R. (1969). Visualization of nucleolar genes. Science, 164, 955-957.
77. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M. and Tollervey, D. (1997). The exosome: a conserved eukaryotic RNA processing complex containing multiple 39-.59 exoribonucleases. Cell, 91, 457-466.
78. Moss, T., Langlois, F., Gagnon-Kugler, T. and Stefanovsky, V. (2007). A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci., 64, 29-49.
79. Moy, T. I. and Silver, P. A. (2002). Requirements for the nuclear export of the small ribosomal subunit. J. Cell Sci., 115, 2985-2995.
80. Mullineux, S. T. and Lafontaine, D. L. (2012). Mapping the cleavage sites on mammalian pre-rRNAs:where do we stand? Biochimie 94, 1521-1532.
81. Narla, A. and Ebert, B. L. (2010). Ribosomopathies:human disorders of ribosome dysfunction. Blood, 115, 3196-3205.
82. Németh, A., Perez-Fernandez, J., Merkl, P., Hamperl, S., Gerber, J., Griesenbeck, J. and Tschochner, H. (2013). RNA polymerase I termination: Where is the end? Biochim. Biophys. Acta, 1829, 306-317.
83. 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.
84. 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.
85. 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.
86. Oeffinger, M. and Tollervey, D. (2003). Yeast Nop15p is an RNA-binding protein required for pre-rRNA processing and cytokinesis. EMBO J., 22, 6573-6583.
87. 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.
88. Oeffinger, M., Dlakic, M. and Tollervey, D. (2004). A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev., 18, 196-209.
89. Ofengand, J. (2002). Ribosomal RNA pseudouridines and pseudouridine synthases. FEBS Lett., 514, 17-25.
90. 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.
91. 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.
92. Peculis, B. A. and Steitz, J. A. (1994). Sequence and structural elements critical for U8 snRNP function in Xenopus oocytes are evolutionarily conserved. Genes Dev., 8, 2241-2255.
93. Pérez-Fernández, J., Román, 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.
94. Pérez-Fernández, J., Martín-Marcos, P. and Dosil, M. (2011). Elucidation of the assembly events required for the recruitment of Utp20, Imp4 and Bms1 onto nascent pre-ribosomes. Nucleic Acids Res., 39, 8105-8121.
95. Pertschy, B., Saveanu, C., Zisser, G., Lebreton, A., Tengg, M., Jacquier, A., Liebminger, E., Nobis, B., Kappel, L., van der Klei, I. et al. (2007). Cytoplasmic recycling of 60S preribosomal factors depends on the AAA protein Drg1. Mol. Cell. Biol., 27, 6581-6592.
96. Pertschy, B., Schneider, C., Gnädig, M., Schäfer, T., Tollervey, D. and Hurt, E. (2009). RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem., 284, 35079-35091.
97. 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.
98. Preti, M., O'Donohue, M. F., Montel-Lehry, N., Bortolin-Cavaillé, M. L., Choesmel, V. and Gleizes, P. E. (2013). Gradual processing of the ITS1 from the nucleolus to the cytoplasm during synthesis of the human 18S rRNA. Nucleic Acids Res., 41, 4709-4723.
99. Raychaudhuri, P., Stringer, E. A., Valenzuela, D. M. and Maitra, U. (1984). Ribosomal subunit antiassociation activity in rabbit reticulocyte lysates. Evidence for a low molecular weight ribosomal subunit antiassociation protein factor (Mr 5 25,000). J. Biol. Chem., 259, 11930-11935.
100. Rodríguez-Mateos, M., Abia, D., García-Gómez, J. J., Morreale, A., de la Cruz, J., Santos, C., Remacha, M. and Ballesta, J. P. (2009a). 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.
101. Rodríguez-Mateos, M., García-Gómez, J. J., Francisco-Velilla, R., Remacha, M., de la Cruz, J. and Ballesta, J. P. (2009b). 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.
102. 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.
103. Sahasranaman, A., Dembowski, J., Strahler, J., Andrews, P., Maddock, J. and Woolford, J. L., Jr (2011). Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: role of factors required for 27S prerRNA processing. EMBO J., 30, 4020-4032.
104. Schäfer, T., Strauss, D., Petfalski, E., Tollervey, D. and Hurt, E. (2003). The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J., 22, 1370-1380.
105. Schäfer, T., Maco, B., Petfalski, E., Tollervey, D., Böttcher, B., Aebi, U. and Hurt, E. (2006). Hrr25- dependent phosphorylation state regulates organization of the pre-40S subunit. Nature, 441, 651-655.
106. Schneider, D. A. (2012). RNA polymerase I activity is regulated at multiple steps in the transcription cycle:recent insights into factors that influence transcription elongation. Gene, 493, 176-184.
107. 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.
108. Sloan, K. E., Bohnsack, M. T. and Watkins, N. J. (2013a). The 5S RNP couples p53 homeostasis to ribosome biogenesis and nucleolar stress. Cell Rep., 5, 237-247.
109. Sloan, K. E., Mattijssen, S., Lebaron, S., Tollervey, D., Pruijn, G. J. and Watkins, N. J. (2013b). Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J. Cell Biol., 200, 577-588.
110. Smith, J. E., Cooperman, B. S. and Mitchell, P. (1992). Methylation sites in Escherichia coli ribosomal RNA: localization and identification of four new sites of methylation in 23S rRNA. Biochemistry, 31, 10825-10834.
111. Strunk, B. S., Loucks, C. R., Su, M., Vashisth, H., Cheng, S., Schilling, J., Brooks, C. L., III, Karbstein, K. and Skiniotis, G. (2011). Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science, 333, 1449-1453.
112. Strunk, B. S., Novak, M. N., Young, C. L. and Karbstein, K. (2012). A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell, 150, 111-121.
113. Tafforeau, L., Zorbas, C., Langhendries, J. L., Mullineux, S. T., Stamatopoulou, V., Mullier, R., Wacheul, L. and Lafontaine, D. L. (2013). The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of pre-rRNA processing factors. Mol. Cell., 51, 539-551.
114. Tang, L., Sahasranaman, A., Jakovljevic, J., Schleifman, E. and Woolford, J. L., Jr (2008). Interactions among Ytm1, Erb1, and Nop7 required for assembly of the Nop7-subcomplex in yeast preribosomes. Mol. Biol. Cell, 19, 2844-2856.
115. Teng, T., Thomas, G. and Mercer, C. A. (2013). Growth control and ribosomopathies. Curr. Opin. Genet. Dev., 23, 63-71.
116. Udem, S. A. and Warner, J. R. (1973). The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast. J. Biol. Chem., 248, 1412-1416.
117. Ulbrich, C., Diepholz, M., Bassler, J., Kressler, D., Pertschy, B., Galani, K., Böttcher, B. and Hurt, E. (2009). Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell, 138, 911-922.
118. Warner, J. R. (1999). The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci., 24, 437-440.
119. Watkins, N. J. and Bohnsack, M. T. (2012). The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip Rev. RNA, 3, 397-414.
120. Widmann, B., Wandrey, F., Badertscher, L., Wyler, E., Pfannstiel, J., Zemp, I. and Kutay, U. (2012). The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits. Mol. Biol. Cell, 23, 22-35.
121. Wild, T., Horvath, P., Wyler, E., Widmann, B., Badertscher, L., Zemp, I., Kozak, K., Csucs, G., Lund, E. and Kutay, U. (2010). A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export. PLoS Biol. 8, e1000522.
122. Yao, W., Roser, D., Köhler, 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.
123. Yao, Y., Demoinet, E., Saveanu, C., Lenormand, P., Jacquier, A. and Fromont-Racine, M. (2010). Ecm1 is a new pre-ribosomal factor involved in pre-60S particle export. RNA, 16, 1007-1017.
124. Yoon, A., Peng, G., Brandenburger, Y., Zollo, O., Xu, W., Rego, E. and Ruggero, D. (2006). Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science, 312, 902-906.
125. Zemp, I., Wild, T., O'Donohue, M. F., Wandrey, F., Widmann, B., Gleizes, P. E. and Kutay, U. (2009). Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol., 185, 1167-1180.