Eukaryotic Ribosome Assembly and Nuclear Export

International Review of Cell and Molecular Biology

Volumn 319, Issue , 2015, Pages 107-140

  Nerurkar, Purnima ^a,b   Altvater, Martin ^a,b   Gerhardy, Stefan ^a,c   Schütz, Sabina ^a,b   Fischer, Ute ^a   Weirich, Christine ^a   Panse, Vikram Govind ^a  

^a ETH ZURICH   (Switzerland)

^b Molecular Life Sciences Graduate School   (Switzerland)

^c Biomolecular Structure and Mechanism (BSM) Graduate School   (Switzerland)

Author keywords

40S subunits; 60S subunits; Biogenesis; Eukaryotic cells; Nuclear transport; Ribosome

Indexed keywords

BIOGENESIS; CELL MATURATION; CYTOPLASM; EUKARYOTE; NONHUMAN; NUCLEAR EXPORT SIGNAL; RIBOSOME; RIBOSOME SUBUNIT; ACTIVE TRANSPORT; ANIMAL; CELL NUCLEUS; EUKARYOTIC CELL; HUMAN; METABOLISM; NUCLEOLUS;

RIBOSOME PROTEIN;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEOLUS; CELL NUCLEUS; EUKARYOTIC CELLS; HUMANS; RIBOSOMAL PROTEINS; RIBOSOMES;

EID: 84938631140     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ircmb.2015.07.002     Document Type: Article

References (153)

1. Altvater M., Chang Y., Melnik A., Occhipinti L., Schütz S., Rothenbusch U., Picotti P., Panse V.G. Targeted proteomics reveals compositional dynamics of 60S pre-ribosomes after nuclear export. Mol. Syst. Biol. 2012, 8:628.
2. Armache J.P., Jarasch A., Anger A.M., Villa E., Becker T., Bhushan S., Jossinet F., Habeck M., Dindar G., Franckenberg S., Marquez V., Mielke T., Thomm M., Berninghausen O., Beatrix B., Soding J., Westhof E., Wilson D.N., Beckmann R. Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:19748-19753.
3. Askjaer P., Bachi A., Wilm M., Bischoff F.R., Weeks D.L., Ogniewski V., Ohno M., Niehrs C., Kjems J., Mattaj I.W., Fornerod M. RanGTP-regulated interactions of CRM1 with nucleoporins and a shuttling DEAD-box helicase. Mol. Cell Biol. 1999, 19:6276-6285.
4. Ball S. Diamond Blackfan anemia. Hematol. Am. Soc. Hematol. Educ. Program 2011, 2011:487-491.
5. Ballesta J.P., Remacha M. The large ribosomal subunit stalk as a regulatory element of the eukaryotic translational machinery. Prog. Nucleic Acid. Res. Mol. Biol. 1996, 55:157-193.
6. Ban N., Beckmann R., Cate J.H., Dinman J.D., Dragon F., Ellis S.R., Lafontaine D.L., Lindahl L., Liljas A., Lipton J.M., Mcalear M.A., Moore P.B., Noller H.F., Ortega J., Panse V.G., Ramakrishnan V., Spahn C.M., Steitz T.A., Tchorzewski M., Tollervey D., Warren A.J., Williamson J.R., Wilson D., Yonath A., Yusupov M. A new system for naming ribosomal proteins. Curr. Opin. Struct. Biol. 2014 Feb, 24:165-169.
7. Bassler J., Grandi P., Gadal O., Lessmann T., Petfalski E., Tollervey D., Lechner J., Hurt E. Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol. Cell 2001, 8:517-529.
8. Bassler J., Kallas M., Pertschy B., Ulbrich C., Thoms M., Hurt E. The AAA-ATPase Rea1 drives removal of biogenesis factors during multiple stages of 60S ribosome assembly. Mol. Cell 2010, 38:712-721.
9. Bassler J., Klein I., Schmidt C., Kallas M., Thomson E., Wagner M.A., Bradatsch B., Rechberger G., Strohmaier H., Hurt E., Bergler H. The conserved Bud20 zinc finger protein is a new component of the ribosomal 60S subunit export machinery. Mol. Cell Biol. 2012, 32:4898-4912.
10. Bayliss R., Leung S.W., Baker R.P., Quimby B.B., Corbett A.H., Stewart M. Structural basis for the interaction between NTF2 and nucleoporin FxFG repeats. EMBO J. 2002, 21:2843-2853.
11. Becam A.M., Nasr F., Racki W.J., Zagulski M., Herbert C.J. Ria1p (Ynl163c), a protein similar to elongation factors 2, is involved in the biogenesis of the 60S subunit of the ribosome in Saccharomyces cerevisiae. Mol. Genet. Genomics 2001, 266:454-462.
12. Becker T., Franckenberg S., Wickles S., Shoemaker C.J., Anger A.M., Armache J.P., Sieber H., Ungewickell C., Berninghausen O., Daberkow I., Karcher A., Thomm M., Hopfner K.P., Green R., Beckmann R. Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature 2012, 482:501-506.
13. Belk J.P., He F., Jacobson A. Overexpression of truncated Nmd3p inhibits protein synthesis in yeast. RNA 1999, 5:1055-1070.
14. Ben-Shem A., Garreau De Loubresse N., Melnikov S., Jenner L., Yusupova G., Yusupov M. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 2011, 334:1524-1529.
15. Berk V., Cate J.H. Insights into protein biosynthesis from structures of bacterial ribosomes. Curr. Opin. Struct. Biol. 2007, 17:302-309.
16. Bohnsack M.T., Martin R., Granneman S., Ruprecht M., Schleiff E., Tollervey D. Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol. Cell 2009, 36:583-592.
17. Bonner W.M. Protein migration into nuclei. I. Frog oocyte nuclei in vivo accumulate microinjected histones, allow entry to small proteins, and exclude large proteins. J. Cell Biol. 1975, 64:421-430.
18. 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., Hurt E. Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit. Mol. Cell 2007, 27:767-779.
19. Bradatsch B., Leidig C., Granneman S., Gnädig M., Tollervey D., Böttcher B., Beckmann R., Hurt E. Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel. Nat. Struct. Mol. Biol. 2012, 19:1234-1241.
20. Campbell M.G., Karbstein K. Protein-protein interactions within late pre-40S ribosomes. PLoS One 2011, 6:e16194.
21. Ciganda M., Williams N. Eukaryotic 5S rRNA biogenesis. Wiley Interdiscip. Rev. RNA 2011, 2:523-533.
22. Cole C.N., Scarcelli J.J. Transport of messenger RNA from the nucleus to the cytoplasm. Curr. Opin. Cell Biol. 2006, 18:299-306.
23. Conti E., Izaurralde E. Nucleocytoplasmic transport enters the atomic age. Curr. Opin. Cell Biol. 2001, 13:310-319.
24. Cook A., Bono F., Jinek M., Conti E. Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 2007, 76:647-671.
25. Dalley J.A., Selkirk A., Pool M.R. Access to ribosomal protein Rpl25p by the signal recognition particle is required for efficient cotranslational translocation. Mol. Biol. Cell 2008, 19:2876-2884.
26. De Keersmaecker K., Atak Z.K., Li N., Vicente C., Patchett S., Girardi T., Gianfelici V., Geerdens E., Clappier E., Porcu M., Lahortiga I., Luca R., Yan J., Hulselmans G., Vranckx H., Vandepoel R., Sweron B., Jacobs K., Mentens N., Wlodarska I., Cauwelier B., Cloos J., Soulier J., Uyttebroeck A., Bagni C., Hassan B.A., Vandenberghe P., Johnson A.W., Aerts S., Cools J. Exome sequencing identifies mutation in CNOT3 and ribosomal genes RPL5 and RPL10 in T-cell acute lymphoblastic leukemia. Nat. Genet. 2013, 45:186-190.
27. Demoinet E., Jacquier A., Lutfalla G., Fromont-Racine M. The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae. RNA 2007, 13:1570-1581.
28. Ellis S.R., Gleizes P.E. Diamond Blackfan anemia: ribosomal proteins going rogue. Semin. Hematol. 2011, 48:89-96.
29. Ellis S.R., Lipton J.M. Diamond Blackfan anemia: a disorder of red blood cell development. Curr. Top. Dev. Biol. 2008, 82:217-241.
30. Englmeier L., Fornerod M., Bischoff F.R., Petosa C., Mattaj I.W., Kutay U. RanBP3 influences interactions between CRM1 and its nuclear protein export substrates. EMBO Rep. 2001, 2:926-932.
31. Fassio C.A., Schofield B.J., Seiser R.M., Johnson A.W., Lycan D.E. Dominant mutations in the late 40S biogenesis factor Ltv1 affect cytoplasmic maturation of the small ribosomal subunit in Saccharomyces cerevisiae. Genetics 2010, 185:199-209.
32. Faza M.B., Chang Y., Occhipinti L., Kemmler S., Panse V.G. Role of Mex67-Mtr2 in the nuclear export of 40S pre-ribosomes. PLoS Genet. 2012, 8:e1002915.
33. Ferreira-Cerca S., Sagar V., Schafer T., Diop M., Wesseling A.M., Lu H., Chai E., Hurt E., Laronde-Leblanc N. ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit. Nat. Struct. Mol. Biol. 2012, 19:1316-1323.
34. Finch A.J., Hilcenko C., Basse N., Drynan L.F., Goyenechea B., Menne T.F., Gonzalez Fernandez A., Simpson P., D'Santos C.S., Arends M.J., Donadieu J., Bellanne-Chantelot C., Costanzo M., Boone C., Mckenzie A.N., Freund S.M., Warren A.J. Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome. Genes Dev. 2011, 25:917-929.
35. Fischer U., Schauble N., Schütz S., Altvater M., Chang Y., Boulos Faza M., Panse V.G. A non-canonical mechanism for Crm1-export cargo complex assembly. eLife 2015, 4.
36. Fornerod M., Ohno M., Yoshida M., Mattaj I.W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90:1051-1060.
37. Freed E.F., Prieto J.L., Mccann K.L., Mcstay B., Baserga S.J. NOL11, implicated in the pathogenesis of North American Indian childhood cirrhosis, is required for pre-rRNA transcription and processing. PLoS Genet. 2012, 8:e1002892.
38. Frey S., Gorlich D. A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 2007, 130:512-523.
39. Fribourg S., Conti E. Structural similarity in the absence of sequence homology of the messenger RNA export factors Mtr2 and p15. EMBO Rep. 2003, 4:699-703.
40. Gadal O., Strauss D., Braspenning J., Hoepfner D., Petfalski E., Philippsen P., Tollervey D., Hurt E. A nuclear AAA-type ATPase (Rix7p) is required for biogenesis and nuclear export of 60S ribosomal subunits. EMBO J. 2001, 20:3695-3704.
41. Gadal O., Strauss D., Kessl J., Trumpower B., Tollervey D., Hurt E. 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. 2001, 21:3405-3415.
42. Garcia-Gomez J.J., Fernandez-Pevida A., Lebaron S., Rosado I.V., Tollervey D., Kressler D., De La Cruz J. Final Pre-40S maturation depends on the functional integrity of the 60S subunit ribosomal protein L3. PLoS Genet. 2014, 10:e1004205.
43. Geerlings T.H., Faber A.W., Bister M.D., Vos J.C., Raue H.A. Rio2p, an evolutionarily conserved, low abundant protein kinase essential for processing of 20 S Pre-rRNA in Saccharomyces cerevisiae. J. Biol. Chem. 2003, 278:22537-22545.
44. Gerhardy S., Menet A.M., Pena C., Petkowski J.J., Panse V.G. Assembly and nuclear export of pre-ribosomal particles in budding yeast. Chromosoma 2014, 123:327-344.
45. Ghalei H., Schaub F.X., Doherty J.R., Noguchi Y., Roush W.R., Cleveland J.L., Stroupe M.E., Karbstein K. Hrr25/CK1delta-directed release of Ltv1 from pre-40S ribosomes is necessary for ribosome assembly and cell growth. J. Cell Biol. 2015, 208:745-759.
46. Gilbert W., Guthrie C. The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol. Cell 2004, 13:201-212.
47. Gonzalo P., Reboud J.P. The puzzling lateral flexible stalk of the ribosome. Biol. Cell 2003, 95:179-193.
48. Grandi P., Rybin V., Bassler J., Petfalski E., Strauss D., Marzioch M., Schafer T., Kuster B., Tschochner H., Tollervey D., Gavin A.C., Hurt E. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 2002, 10:105-115.
49. Greber B.J., Boehringer D., Montellese C., Ban N. Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. Nat. Struct. Mol. Biol. 2012, 19:1228-1233.
50. Hackmann A., Gross T., Baierlein C., Krebber H. The mRNA export factor Npl3 mediates the nuclear export of large ribosomal subunits. EMBO Rep. 2011, 12:1024-1031.
51. Hasgall P.A., Hoogewijs D., Faza M.B., Panse V.G., Wenger R.H., Camenisch G. The putative RNA helicase HELZ promotes cell proliferation, translation initiation and ribosomal protein S6 phosphorylation. PLoS One 2011, 6:e22107.
52. Hedges J., West M., Johnson A.W. Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J. 2005, 24:567-579.
53. Herold A., Suyama M., Rodrigues J.P., Braun I.C., Kutay U., Carmo-Fonseca M., Bork P., Izaurralde E. TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol. Cell Biol. 2000, 20:8996-9008.
54. Ho J.H., Kallstrom G., Johnson A.W. Nascent 60S ribosomal subunits enter the free pool bound by Nmd3p. RNA 2000, 6:1625-1634.
55. Hung N.J., Johnson A.W. Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae. Mol. Cell Biol. 2006, 26:3718-3727.
56. Hung N.J., Lo K.Y., Patel S.S., Helmke K., Johnson A.W. Arx1 is a nuclear export receptor for the 60S ribosomal subunit in yeast. Mol. Biol. Cell 2008, 19:735-744.
57. Hurt E., Hannus S., Schmelzl B., Lau D., Tollervey D., Simos G. A novel in vivo assay reveals inhibition of ribosomal nuclear export in ran-cycle and nucleoporin mutants. J. Cell Biol. 1999, 144:389-401.
58. van Hoof A., Lennertz P., Parker R. 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 P RNAs in yeast. EMBO J. 2000, 19:1357-1365.
59. Ito T., Chiba T., Ozawa R., Yoshida M., Hattori M., Sakaki Y. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:4569-4574.
60. Jakel S., Gorlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 1998, 17:4491-4502.
61. Jakel S., Mingot J.M., Schwarzmaier P., Hartmann E., Gorlich D. Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J. 2002, 21:377-386.
62. Jakovljevic J., De Mayolo P.A., Miles T.D., Nguyen T.M., Leger-Silvestre I., Gas N., Woolford J.L. The carboxy-terminal extension of yeast ribosomal protein S14 is necessary for maturation of 43S preribosomes. Mol. Cell 2004, 14:331-342.
63. Kappel L., Loibl M., Zisser G., Klein I., Fruhmann G., Gruber C., Unterweger S., Rechberger G., Pertschy B., Bergler H. Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation. J. Cell Biol. 2012, 199:771-782.
64. Karl T., Onder K., Kodzius R., Pichova A., Wimmer H., Th R.,A., Hundsberger H., Loffler M., Klade T., Beyer A., Breitenbach M., Koller L. GRC5 and NMD3 function in translational control of gene expression and interact genetically. Curr. Genet. 1999, 34:419-429.
65. Kemmler S., Occhipinti L., Veisu M., Panse V.G. Yvh1 is required for a late maturation step in the 60S biogenesis pathway. J. Cell Biol. 2009, 186:863-880.
66. Klinge S., Voigts-Hoffmann F., Leibundgut M., Arpagaus S., Ban N. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 2011, 334:941-948.
67. Kressler D., Bange G., Ogawa Y., Stjepanovic G., Bradatsch B., Pratte D., Amlacher S., Strauss D., Yoneda Y., Katahira J., Sinning I., Hurt E. Synchronizing nuclear import of ribosomal proteins with ribosome assembly. Science 2012, 338:666-671.
68. Kressler D., Hurt E., Bergler H., Bassler J. The power of AAA-ATPases on the road of pre-60S ribosome maturation-molecular machines that strip pre-ribosomal particles. Biochim. Biophys. Acta 2012, 1823:92-100.
69. Kressler D., Linder P., De La Cruz J. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol. Cell Biol. 1999, 19:7897-7912.
70. Kressler D., Roser D., Pertschy B., Hurt E. The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles. J. Cell Biol. 2008, 181:935-944.
71. Lafontaine D., Vandenhaute J., Tollervey D. The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev. 1995, 9:2470-2481.
72. Lafontaine D.L., Preiss T., Tollervey D. Yeast 18S rRNA dimethylase Dim1p: a quality control mechanism in ribosome synthesis?. Mol. Cell Biol. 1998, 18:2360-2370.
73. Lamanna A.C., Karbstein K. Nob1 binds the single-stranded cleavage site D at the 3'-end of 18S rRNA with its PIN domain. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14259-14264.
74. Lebaron S., Schneider C., Van Nues R.W., Swiatkowska A., Walsh D., Bottcher B., Granneman S., Watkins N.J., Tollervey D. Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol. 2012, 19:744-753.
75. Lebreton A., Saveanu C., Decourty L., Rain J.C., Jacquier A., Fromont-Racine M. A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J. Cell Biol. 2006, 173:349-360.
76. Leger-Silvestre I., Milkereit P., Ferreira-Cerca S., Saveanu C., Rousselle J.C., Choesmel V., Guinefoleau C., Gas N., Gleizes P.E. The ribosomal protein Rps15p is required for nuclear exit of the 40S subunit precursors in yeast. EMBO J. 2004, 23:2336-2347.
77. Li Z., Lee I., Moradi E., Hung N.J., Johnson A.W., Marcotte E.M. Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS Biol. 2009, 7:e1000213.
78. Lindsay M.E., Holaska J.M., Welch K., Paschal B.M., Macara I.G. Ran-binding protein 3 is a cofactor for Crm1-mediated nuclear protein export. J. Cell Biol. 2001, 153:1391-1402.
79. Lo K.Y., Li Z., Bussiere C., Bresson S., Marcotte E.M., Johnson A.W. Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit. Mol. Cell 2010, 39:196-208.
80. Lo K.Y., Li Z., Wang F., Marcotte E.M., Johnson A.W. Ribosome stalk assembly requires the dual-specificity phosphatase Yvh1 for the exchange of Mrt4 with P0. J. Cell Biol. 2009, 186:849-862.
81. Matsuo Y., Granneman S., Thoms M., Manikas R.G., Tollervey D., Hurt E. Coupled GTPase and remodelling ATPase activities form a checkpoint for ribosome export. Nature 2014, 505:112-116.
82. Maurer P., Redd M., Solsbacher J., Bischoff F.R., Greiner M., Podtelejnikov A.V., Mann M., Stade K., Weis K., Schlenstedt G. The nuclear export receptor Xpo1p forms distinct complexes with NES transport substrates and the yeast Ran binding protein 1 (Yrb1p). Mol. Biol. Cell 2001, 12:539-549.
83. Melnikov S., Ben-Shem A., Garreau De Loubresse N., Jenner L., Yusupova G., Yusupov M. One core, two shells: bacterial and eukaryotic ribosomes. Nat. Struct. Mol. Biol. 2012, 19:560-567.
84. Menne T.F., Goyenechea B., Sanchez-Puig N., Wong C.C., Tonkin L.M., Ancliff P.J., Brost R.L., Costanzo M., Boone C., Warren A.J. The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nat. Genet. 2007, 39:486-495.
85. Merwin J.R., Bogar L.B., Poggi S.B., Fitch R.M., Johnson A.W., Lycan D.E. Genetic analysis of the ribosome biogenesis factor Ltv1 of Saccharomyces cerevisiae. Genetics 2014, 198:1071-1085.
86. Meyer A.E., Hoover L.A., Craig E.A. The cytosolic J-protein, Jjj1, and Rei1 function in the removal of the pre-60 S subunit factor Arx1. J. Biol. Chem. 2010, 285:961-968.
87. Meyer A.E., Hung N.J., Yang P., Johnson A.W., Craig E.A. The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunit biogenesis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1558-1563.
88. Milkereit P., Strauss D., Bassler J., Gadal O., Kuhn H., Schutz S., Gas N., Lechner J., Hurt E., Tschochner H. A Noc complex specifically involved in the formation and nuclear export of ribosomal 40 S subunits. J. Biol. Chem. 2003, 278:4072-4081.
89. Moritz M., Paulovich A.G., Tsay Y.F., Woolford J.L. Depletion of yeast ribosomal proteins L16 or rp59 disrupts ribosome assembly. J. Cell Biol. 1990, 111:2261-2274.
90. Moy T.I., Silver P.A. Requirements for the nuclear export of the small ribosomal subunit. J. Cell Sci. 2002, 115:2985-2995.
91. Neuber A., Franke J., Wittstruck A., Schlenstedt G., Sommer T., Stade K. Nuclear export receptor Xpo1/Crm1 is physically and functionally linked to the spindle pole body in budding yeast. Mol. Cell Biol. 2008, 28:5348-5358.
92. Neueder A., Jakob S., Poll G., Linnemann J., Deutzmann R., Tschochner H., Milkereit P. A local role for the small ribosomal subunit primary binder rpS5 in final 18S rRNA processing in yeast. PLoS One 2010, 5:e10194.
93. Nissan T.A., Bassler J., Petfalski E., Tollervey D., Hurt E. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J. 2002, 21:5539-5547.
94. Occhipinti L., Chang Y., Altvater M., Menet A.M., Kemmler S., Panse V.G. Non-FG mediated transport of the large pre-ribosomal subunit through the nuclear pore complex by the mRNA export factor Gle2. Nucleic Acids Res. 2013, 41:8266-8279.
95. Oeffinger M., Dlakic M., Tollervey D. A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev. 2004, 18:196-209.
96. Oeffinger M., Zenklusen D., Ferguson A., Wei K.E., El Hage A., Tollervey D., Chait B.T., Singer R.H., Rout M.P. Rrp17p is a eukaryotic exonuclease required for 5' end processing of Pre-60S ribosomal RNA. Mol. Cell 2009, 36:768-781.
97. Paine P.L., Moore L.C., Horowitz S.B. Nuclear envelope permeability. Nature 1975, 254:109-114.
98. Panse V.G., Kressler D., Pauli A., Petfalski E., Gnadig M., Tollervey D., Hurt E. Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 2006, 7:1311-1321.
99. Peng W.T., Robinson M.D., Mnaimneh S., Krogan N.J., Cagney G., Morris Q., Davierwala A.P., Grigull J., Yang X., Zhang W., Mitsakakis N., Ryan O.W., Datta N., Jojic V., Pal C., Canadien V., Richards D., Beattie B., Wu L.F., Altschuler S.J., Roweis S., Frey B.J., Emili A., Greenblatt J.F., Hughes T.R. A panoramic view of yeast noncoding RNA processing. Cell 2003, 113:919-933.
100. 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., Bergler H. Cytoplasmic recycling of 60S preribosomal factors depends on the AAA protein Drg1. Mol. Cell Biol. 2007, 27:6581-6592.
101. Pertschy B., Schneider C., Gnadig M., Schafer T., Tollervey D., Hurt E. RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem. 2009, 284:35079-35091.
102. Rabl J., Leibundgut M., Ataide S.F., Haag A., Ban N. Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 2011, 331:730-736.
103. Ribbeck K., Lipowsky G., Kent H.M., Stewart M., Gorlich D. NTF2 mediates nuclear import of Ran. EMBO J. 1998, 17:6587-6598.
104. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Seraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17:1030-1032.
105. Rout M.P., Blobel G., Aitchison J.D. A distinct nuclear import pathway used by ribosomal proteins. Cell 1997, 89:715-725.
106. Russell D.W., Spremulli L.L. Purification and characterization of a ribosome dissociation factor (eukaryotic initiation factor 6) from wheat germ. J. Biol. Chem. 1979, 254:8796-8800.
107. Santos-Rosa H., Moreno H., Simos G., Segref A., Fahrenkrog B., Pante N., Hurt E. Nuclear mRNA export requires complex formation between Mex67p and Mtr2p at the nuclear pores. Mol. Cell Biol. 1998, 18:6826-6838.
108. Saveanu C., Namane A., Gleizes P.E., Lebreton A., Rousselle J.C., Noaillac-Depeyre J., Gas N., Jacquier A., Fromont-Racine M. Sequential protein association with nascent 60S ribosomal particles. Mol. Cell Biol. 2003, 23:4449-4460.
109. Schafer T., Maco B., Petfalski E., Tollervey D., Bottcher B., Aebi U., Hurt E. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 2006, 441:651-655.
110. Schafer T., Strauss D., Petfalski E., Tollervey D., Hurt E. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 2003, 22:1370-1380.
111. Schlenstedt G., Smirnova E., Deane R., Solsbacher J., Kutay U., Gorlich D., Ponstingl H., Bischoff F.R. Yrb4p, a yeast ran-GTP-binding protein involved in import of ribosomal protein L25 into the nucleus. EMBO J. 1997, 16:6237-6249.
112. Schütz S., Fischer U., Altvater M., Nerurkar P., Pena C., Gerber M., Chang Y., Caesar S., Schubert O.T., Schlenstedt G., Panse V.G. A RanGTP-independent mechanism allows ribosomal protein nuclear import for ribosome assembly. eLife 2014, 3:e03473.
113. Segref A., Sharma K., Doye V., Hellwig A., Huber J., Luhrmann R., Hurt E. Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J. 1997, 16:3256-3271.
114. Seiser R.M., Sundberg A.E., Wollam B.J., Zobel-Thropp P., Baldwin K., Spector M.D., Lycan D.E. Ltv1 is required for efficient nuclear export of the ribosomal small subunit in Saccharomyces cerevisiae. Genetics 2006, 174:679-691.
115. Senapin S., Clark-Walker G.D., Chen X.J., Seraphin B., Daugeron M.C. RRP20, a component of the 90S preribosome, is required for pre-18S rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res. 2003, 31:2524-2533.
116. Senay C., Ferrari P., Rocher C., Rieger K.J., Winter J., Platel D., Bourne Y. The Mtr2-Mex67 NTF2-like domain complex. Structural insights into a dual role of Mtr2 for yeast nuclear export. J. Biol. Chem. 2003, 278:48395-48403.
117. Senger B., Lafontaine D.L., Graindorge J.S., Gadal O., Camasses A., Sanni A., Garnier J.M., Breitenbach M., Hurt E., Fasiolo F. The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 2001, 8:1363-1373.
118. Sengupta J., Bussiere C., Pallesen J., West M., Johnson A.W., Frank J. Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J. Cell Biol. 2010, 189:1079-1086.
119. Stade K., Ford C.S., Guthrie C., Weis K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 1997, 90:1041-1050.
120. Stage-Zimmermann T., Schmidt U., Silver P.A. Factors affecting nuclear export of the 60S ribosomal subunit in vivo. Mol. Biol. Cell 2000, 11:3777-3789.
121. Strasser K., Bassler J., Hurt E. Binding of the Mex67p/Mtr2p heterodimer to FXFG, GLFG, and FG repeat nucleoporins is essential for nuclear mRNA export. J. Cell Biol. 2000, 150:695-706.
122. Strawn L.A., Shen T., Wente S.R. The GLFG regions of Nup116p and Nup100p serve as binding sites for both Kap95p and Mex67p at the nuclear pore complex. J. Biol. Chem. 2001, 276:6445-6452.
123. Strunk B.S., Loucks C.R., Su M., Vashisth H., Cheng S., Schilling J., Brooks C.L., Karbstein K., Skiniotis G. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 2011, 333:1449-1453.
124. Strunk B.S., Novak M.N., Young C.L., Karbstein K. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 2012, 150:111-121.
125. Stutz F., Bachi A., Doerks T., Braun I.C., Seraphin B., Wilm M., Bork P., Izaurralde E. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 2000, 6:638-650.
126. Sydorskyy Y., Dilworth D.J., Yi E.C., Goodlett D.R., Wozniak R.W., Aitchison J.D. Intersection of the Kap123p-mediated nuclear import and ribosome export pathways. Mol. Cell Biol. 2003, 23:2042-2054.
127. Taura T., Krebber H., Silver P.A. A member of the Ran-binding protein family, Yrb2p, is involved in nuclear protein export. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:7427-7432.
128. Thorsness P.E., White K.H., Ong W.C. AFG2, an essential gene in yeast, encodes a new member of the Sec18p, Pas1p, Cdc48p, TBP-1 family of putative ATPases. Yeast 1993, 9:1267-1271.
129. Trapman J., Retel J., Planta R.J. Ribosomal precursor particles from yeast. Exp. Cell Res. 1975, 90:95-104.
130. Tuck A.C., Tollervey D. A transcriptome-wide atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 2013, 154:996-1009.
131. Turowski T.W., Lebaron S., Zhang E., Peil L., Dudnakova T., Petfalski E., Granneman S., Rappsilber J., Tollervey D. Rio1 mediates ATP-dependent final maturation of 40S ribosomal subunits. Nucleic Acids Res. 2014, 42:12189-12199.
132. Udem S.A., Warner J.R. Ribosomal RNA synthesis in Saccharomyces cerevisiae. J. Mol. Biol. 1972, 65:227-242.
133. Ulbrich C., Diepholz M., Bassler J., Kressler D., Pertschy B., Galani K., Bottcher B., Hurt E. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 2009, 138:911-922.
134. Valenzuela D.M., Chaudhuri A., Maitra U. Eukaryotic ribosomal subunit anti-association activity of calf liver is contained in a single polypeptide chain protein of Mr = 25,500 (eukaryotic initiation factor 6). J. Biol. Chem. 1982, 257:7712-7719.
135. Vanrobays E., Gelugne J.P., Caizergues-Ferrer M., Lafontaine D.L. Dim2p, a KH-domain protein required for small ribosomal subunit synthesis. RNA 2004, 10:645-656.
136. Vanrobays E., Gelugne J.P., Gleizes P.E., Caizergues-Ferrer M. Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol. Cell Biol. 2003, 23:2083-2095.
137. Venema J., Tollervey D. Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast 1995, 11:1629-1650.
138. Warner J.R. The assembly of ribosomes in yeast. J. Biol. Chem. 1971, 246:447-454.
139. Warner J.R. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 1999, 24:437-440.
140. Weis K. Nucleocytoplasmic transport: cargo trafficking across the border. Curr. Opin. Cell Biol. 2002, 14:328-335.
141. Wendler F., Bergler H., Prutej K., Jungwirth H., Zisser G., Kuchler K., Hogenauer G. Diazaborine resistance in the yeast Saccharomyces cerevisiae reveals a link between YAP1 and the pleiotropic drug resistance genes PDR1 and PDR3. J. Biol. Chem. 1997, 272:27091-27098.
142. West M., Hedges J.B., Chen A., Johnson A.W. Defining the order in which Nmd3p and Rpl10p load onto nascent 60S ribosomal subunits. Mol. Cell Biol. 2005, 25:3802-3813.
143. Windgassen M., Sturm D., Cajigas I.J., Gonzalez C.I., Seedorf M., Bastians H., Krebber H. Yeast shuttling SR proteins Npl3p, Gbp2p, and Hrb1p are part of the translating mRNPs, and Npl3p can function as a translational repressor. Mol. Cell Biol. 2004, 24:10479-10491.
144. Wong C.C., Traynor D., Basse N., Kay R.R., Warren A.J. Defective ribosome assembly in Shwachman-Diamond syndrome. Blood 2011, 118:4305-4312.
145. Woolford J.L., Baserga S.J. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 2013, 195:643-681.
146. Yao W., Lutzmann M., Hurt E. A versatile interaction platform on the Mex67-Mtr2 receptor creates an overlap between mRNA and ribosome export. EMBO J. 2008, 27:6-16.
147. Yao W., Roser D., Kohler A., Bradatsch B., Bassler J., Hurt E. Nuclear export of ribosomal 60S subunits by the general mRNA export receptor Mex67-Mtr2. Mol. Cell 2007, 26:51-62.
148. Yao Y., Demoinet E., Saveanu C., Lenormand P., Jacquier A., Fromont-Racine M. Ecm1 is a new pre-ribosomal factor involved in pre-60S particle export. RNA 2010, 16:1007-1017.
149. Zakalskiy A., Hogenauer G., Ishikawa T., Wehrschutz-Sigl E., Wendler F., Teis D., Zisser G., Steven A.C., Bergler H. Structural and enzymatic properties of the AAA protein Drg1p from Saccharomyces cerevisiae. Decoupling of intracellular function from ATPase activity and hexamerization. J. Biol. Chem. 2002, 277:26788-26795.
150. Zemp I., Kutay U. Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 2007, 581:2783-2793.
151. Zemp I., Wandrey F., Rao S., Ashiono C., Wyler E., Montellese C., Kutay U. CK1delta and CK1epsilon are components of human 40S subunit precursors required for cytoplasmic 40S maturation. J. Cell Sci. 2014, 127:1242-1253.
152. Zemp I., Wild T., O'Donohue M.F., Wandrey F., Widmann B., Gleizes P.E., Kutay U. Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 2009, 185:1167-1180.
153. Zhang J., Harnpicharnchai P., Jakovljevic J., Tang L., Guo Y., Oeffinger M., Rout M.P., Hiley S.L., Hughes T., Woolford J.L. Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 2007, 21:2580-2592.