1932

Abstract

Ribosomes, which synthesize the proteins of a cell, comprise ribosomal RNA and ribosomal proteins, which coassemble hierarchically during a process termed ribosome biogenesis. Historically, biochemical and molecular biology approaches have revealed how preribosomal particles form and mature in consecutive steps, starting in the nucleolus and terminating after nuclear export into the cytoplasm. However, only recently, due to the revolution in cryo–electron microscopy, could pseudoatomic structures of different preribosomal particles be obtained. Together with in vitro maturation assays, these findings shed light on how nascent ribosomes progress stepwise along a dynamic biogenesis pathway. Preribosomes assemble gradually, chaperoned by a myriad of assembly factors and small nucleolar RNAs, before they reach maturity and enter translation. This information will lead to a better understanding of how ribosome synthesis is linked to other cellular pathways in humans and how it can cause diseases, including cancer, if disturbed.

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2019-06-20
2024-03-29
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Literature Cited

  1. 1. 
    Ban N, Beckmann R, Cate JH, Dinman JD, Dragon F et al. 2014. A new system for naming ribosomal proteins. Curr. Opin. Struct. Biol. 24:165–69
    [Google Scholar]
  2. 2. 
    Melnikov S, Ben-Shem A, Garreau de Loubresse N, Jenner L, Yusupova G, Yusupov M 2012. One core, two shells: bacterial and eukaryotic ribosomes. Nat. Struct. Mol. Biol. 19:560–67
    [Google Scholar]
  3. 3. 
    Scherrer K, Latham H, Darnell JE 1963. Demonstration of an unstable RNA and of a precursor to ribosomal RNA in HeLa cells. PNAS 49:240–48
    [Google Scholar]
  4. 4. 
    Scherrer K, Darnell JE. 1962. Sedimentation characteristics of rapidly labelled RNA from HeLa cells. Biochem. Biophys. Res. Commun. 7:486–90
    [Google Scholar]
  5. 5. 
    Tamaoki T. 1966. The particulate fraction containing 45 s RNA in L cell nuclei. J. Mol. Biol. 15:624–39
    [Google Scholar]
  6. 6. 
    Warner JR, Soeiro R. 1967. Nascent ribosomes from HeLa cells. PNAS 58:1984–90
    [Google Scholar]
  7. 7. 
    Trapman J, Retèl J, Planta RJ 1975. Ribosomal precursor particles from yeast. Exp. Cell Res. 90:95–104
    [Google Scholar]
  8. 8. 
    Miller OL, Beatty BR. 1969. Visualization of nucleolar genes. Science 164:955–57
    [Google Scholar]
  9. 9. 
    Scheer U, Rose KM. 1984. Localization of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. PNAS 81:1431–35
    [Google Scholar]
  10. 10. 
    Spector DL, Ochs RL, Busch H 1984. Silver staining, immunofluorescence, and immunoelectron microscopic localization of nucleolar phosphoproteins B23 and C23. Chromosoma 90:139–48
    [Google Scholar]
  11. 11. 
    Hügle B, Hazan R, Scheer U, Franke WW 1985. Localization of ribosomal protein S1 in the granular component of the interphase nucleolus and its distribution during mitosis. J. Cell Biol. 100:873–86
    [Google Scholar]
  12. 12. 
    Udem SA, Warner JR. 1973. The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast. J. Biol. Chem. 248:1412–16
    [Google Scholar]
  13. 13. 
    Udem SA, Warner JR. 1972. Ribosomal RNA synthesis in Saccharomyces cerevisiae. J. Mol. Biol 65:227–42
    [Google Scholar]
  14. 14. 
    Warner JR. 1989. Synthesis of ribosomes in Saccharomyces cerevisiae.Microbiol. . Rev 53:256–71
    [Google Scholar]
  15. 15. 
    Wool IG. 1979. The structure and function of eukaryotic ribosomes. Annu. Rev. Biochem. 48:719–54
    [Google Scholar]
  16. 16. 
    Kressler D, Linder P, De La Cruz J 1999. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae.Mol. Cell. . Biol 19:7897–912
    [Google Scholar]
  17. 17. 
    Venema J, Tollervey D. 1999. Ribosome synthesis in Saccharomyces cerevisiae.Annu.Rev. . Genet 33:261–311
    [Google Scholar]
  18. 18. 
    Watkins NJ, Bohnsack MT. 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
    [Google Scholar]
  19. 19. 
    Prestayko AW, Tonato M, Busch H 1970. Low molecular weight RNA associated with 28 s nucleolar RNA. J. Mol. Biol. 47:505–15
    [Google Scholar]
  20. 20. 
    Calvet JP, Pederson T. 1981. Base-pairing interactions between small nuclear RNAs and nuclear RNA precursors as revealed by psoralen cross-linking in vivo. Cell 26:363–70
    [Google Scholar]
  21. 21. 
    Watkins NJ, Segault V, Charpentier B, Nottrott S, Fabrizio P et al. 2000. A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell 103:457–66
    [Google Scholar]
  22. 22. 
    Beltrame M, Tollervey D. 1992. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J 11:1531–42
    [Google Scholar]
  23. 23. 
    Tyc K, Steitz JA. 1992. A new interaction between the mouse 5′ external transcribed spacer of pre-rRNA and U3 snRNA detected by psoralen crosslinking. Nucleic Acids Res 20:5375–82
    [Google Scholar]
  24. 24. 
    Henras AK, Soudet J, Gerus M, Lebaron S, Caizergues-Ferrer M et al. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65:2334–59
    [Google Scholar]
  25. 25. 
    Bally M, Hughes J, Cesareni G 1988. SnR30: a new, essential small nuclear RNA from Saccharomyces cerevisiae. . Nucleic Acids Res 16:5291–303
    [Google Scholar]
  26. 26. 
    Jarmolowski A, Zagorski J, Li HV, Fournier MJ 1990. Identification of essential elements in U14 RNA of Saccharomyces cerevisiae. . EMBO J 9:4503–9
    [Google Scholar]
  27. 27. 
    Tollervey D, Kiss T. 1997. Function and synthesis of small nucleolar RNAs. Curr. Opin. Cell Biol. 9:337–42
    [Google Scholar]
  28. 28. 
    Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D 1997. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 91:457–66
    [Google Scholar]
  29. 29. 
    Henry Y, Wood H, Morrissey JP, Petfalski E, Kearsey S, Tollervey D 1994. The 5′ end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site. EMBO J 13:2452–63
    [Google Scholar]
  30. 30. 
    Filipowicz W, Kiss T. 1993. Structure and function of nucleolar snRNPs. Mol. Biol. Rep. 18:149–56
    [Google Scholar]
  31. 31. 
    Balakin AG, Smith L, Fournier MJ 1996. The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell 86:823–34
    [Google Scholar]
  32. 32. 
    Sharma S, Yang J, Watzinger P, Kotter P, Entian KD 2013. Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res 41:9062–76
    [Google Scholar]
  33. 33. 
    Lafontaine D, Delcour J, Glasser AL, Desgres J, Vandenhaute J 1994. The DIM1 gene responsible for the conserved m62Am62A dimethylation in the 3′-terminal loop of 18 S rRNA is essential in yeast. J. Mol. Biol. 241:492–97
    [Google Scholar]
  34. 34. 
    Meyer B, Wurm JP, Kotter P, Leisegang MS, Schilling V et al. 2011. The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of Psi1191 in yeast 18S rRNA. Nucleic Acids Res 39:1526–37
    [Google Scholar]
  35. 35. 
    Sharma S, Langhendries JL, Watzinger P, Kotter P, Entian KD, Lafontaine DL 2015. Yeast Kre33 and human NAT10 are conserved 18S rRNA cytosine acetyltransferases that modify tRNAs assisted by the adaptor Tan1/THUMPD1. Nucleic Acids Res 43:2242–58
    [Google Scholar]
  36. 36. 
    Natchiar SK, Myasnikov AG, Kratzat H, Hazemann I, Klaholz BP 2017. Visualization of chemical modifications in the human 80S ribosome structure. Nature 551:472–77
    [Google Scholar]
  37. 37. 
    Rocak S, Linder P. 2004. DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol. 5:232–41
    [Google Scholar]
  38. 38. 
    Hurt E, Hannus S, Schmelzl B, Lau D, Tollervey D, 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
    [Google Scholar]
  39. 39. 
    Moy TI, Silver PA. 1999. Nuclear export of the small ribosomal subunit requires the Ran-GTPase cycle and certain nucleoporins. Genes Dev 13:2118–33
    [Google Scholar]
  40. 40. 
    Pillet B, Mitterer V, Kressler D, Pertschy B 2017. Hold on to your friends: dedicated chaperones of ribosomal proteins. BioEssays 39:1–12
    [Google Scholar]
  41. 41. 
    Pausch P, Singh U, Ahmed YL, Pillet B, Murat G et al. 2015. Co-translational capturing of nascent ribosomal proteins by their dedicated chaperones. Nat. Commun. 6:7494
    [Google Scholar]
  42. 42. 
    Gadal O, Strauss D, Kessl J, Trumpower B, Tollervey D, Hurt E 2001. Nuclear export of 60S ribosomal subunits depends on Xpo1p and requires a NES-containing factor Nmd3p that associates with the large subunit protein Rpl10p. Mol. Cell. Biol. 21:3405–15
    [Google Scholar]
  43. 43. 
    Thomas F, Kutay U. 2003. Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J. Cell Sci. 116:2409–19
    [Google Scholar]
  44. 44. 
    Trotta CR, Lund E, Kahan L, Johnson AW, Dahlberg JE 2003. Coordinated nuclear export of 60S ribosomal subunits and NMD3 in vertebrates. EMBO J 22:2841–51
    [Google Scholar]
  45. 45. 
    Ho JHN, Kallstrom G, Johnson AW 2000. Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit. J. Cell Biol. 151:1057–66
    [Google Scholar]
  46. 46. 
    Nerurkar P, Altvater M, Gerhardy S, Schutz S, Fischer U et al. 2015. Eukaryotic ribosome assembly and nuclear export. Int. Rev. Cell Mol. Biol. 319:107–40
    [Google Scholar]
  47. 47. 
    Merwin JR, Bogar LB, Poggi SB, Fitch RM, Johnson AW, Lycan DE 2014. Genetic analysis of the ribosome biogenesis factor Ltv1 of Saccharomyces cerevisiae. . Genetics 198:1071–85
    [Google Scholar]
  48. 48. 
    Fischer U, Schauble N, Schutz S, Altvater M, Chang Y et al. 2015. A non-canonical mechanism for Crm1-export cargo complex assembly. eLife 4:e05745
    [Google Scholar]
  49. 49. 
    Zemp I, Wild T, O'Donohue MF, Wandrey F, Widmann B et al. 2009. Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 185:1167–80
    [Google Scholar]
  50. 50. 
    Baßler J, Grandi P, Gadal O, Leßmann T, Tollervey D et al. 2001. Identification of a 60S pre-ribosomal particle that is closely linked to nuclear export. Mol. Cell 8:517–29
    [Google Scholar]
  51. 51. 
    Harnpicharnchai P, Jakovljevic J, Horsey E, Miles T, Roman J et al. 2001. Composition and functional characterization of yeast 66s ribosome assembly intermediates. Mol. Cell 8:505–15
    [Google Scholar]
  52. 52. 
    Saveanu C, Bienvenu D, Namane A, Gleizes PE, Gas N et al. 2001. Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J 20:6475–84
    [Google Scholar]
  53. 53. 
    Fatica A, Cronshaw AD, Dlakić M, Tollervey D 2002. Ssf1p prevents premature processing of an early pre-60S ribosomal particle. Mol. Cell 9:341–51
    [Google Scholar]
  54. 54. 
    Tschochner H, Hurt E. 2003. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 13:255–63
    [Google Scholar]
  55. 55. 
    Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA et al. 2002. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967–70
    [Google Scholar]
  56. 56. 
    Grandi P, Rybin V, Baßler J, Petfalski E, Strauss 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 10:105–15
    [Google Scholar]
  57. 57. 
    Milkereit P, Gadal O, Podtelejnikov A, Trumtel S, Gas N et al. 2001. Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 105:499–509
    [Google Scholar]
  58. 58. 
    Perez-Fernandez J, Roman A, De Las Rivas J, Bustelo XR, Dosil M 2007. The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol. 27:5414–29
    [Google Scholar]
  59. 59. 
    Granneman S, Gallagher JE, Vogelzangs J, Horstman W, van Venrooij WJ et al. 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 31:1877–87
    [Google Scholar]
  60. 60. 
    Hierlmeier T, Merl J, Sauert M, Perez-Fernandez J, Schultz P et al. 2013. Rrp5p, Noc1p and Noc2p form a protein module which is part of early large ribosomal subunit precursors in S. cerevisiae. . Nucleic Acids Res 41:1191–210
    [Google Scholar]
  61. 61. 
    de la Cruz J, Karbstein K, Woolford JL 2015. Functions of ribosomal proteins in assembly of eukaryotic ribosomes in vivo. Annu. Rev. Biochem. 84:93–129
    [Google Scholar]
  62. 62. 
    Ferreira-Cerca S, Poll G, Gleizes PE, Tschochner H, Milkereit P 2005. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol. Cell 20:263–75
    [Google Scholar]
  63. 63. 
    Krogan NJ, Peng WT, Cagney G, Robinson MD, Haw R et al. 2004. High-definition macromolecular composition of yeast RNA-processing complexes. Mol. Cell 13:225–39
    [Google Scholar]
  64. 64. 
    McCann KL, Charette JM, Vincent NG, Baserga SJ 2015. A protein interaction map of the LSU processome. Genes Dev 29:862–75
    [Google Scholar]
  65. 65. 
    Vincent NG, Charette JM, Baserga SJ 2018. The SSU processome interactome in Saccharomyces cerevisiae reveals novel protein subcomplexes. RNA 24:77–89
    [Google Scholar]
  66. 66. 
    Baßler J, Ahmed YL, Kallas M, Kornprobst M, Calvino FR et al. 2017. Interaction network of the ribosome assembly machinery from a eukaryotic thermophile. Protein Sci 26:327–42
    [Google Scholar]
  67. 67. 
    Jakob S, Ohmayer U, Neueder A, Hierlmeier T, Perez-Fernandez J et al. 2012. Interrelationships between yeast ribosomal protein assembly events and transient ribosome biogenesis factors interactions in early pre-ribosomes. PLOS ONE 7:e32552
    [Google Scholar]
  68. 68. 
    Hunziker M, Barandun J, Petfalski E, Tan D, Delan-Forino C et al. 2016. UtpA and UtpB chaperone nascent pre-ribosomal RNA and U3 snoRNA to initiate eukaryotic ribosome assembly. Nat. Commun. 7:12090
    [Google Scholar]
  69. 69. 
    Zhang C, Sun Q, Chen R, Chen X, Lin J, Ye K 2016. Integrative structural analysis of the UTPB complex, an early assembly factor for eukaryotic small ribosomal subunits. Nucleic Acids Res 44:7475–86
    [Google Scholar]
  70. 70. 
    Granneman S, Kudla G, Petfalski E, Tollervey D 2009. Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. PNAS 106:9613–18
    [Google Scholar]
  71. 71. 
    Zhang L, Wu C, Cai G, Chen S, Ye K 2016. Stepwise and dynamic assembly of the earliest precursors of small ribosomal subunits in yeast. Genes Dev 30:718–32
    [Google Scholar]
  72. 72. 
    Chen W, Xie Z, Yang F, Ye K 2017. Stepwise assembly of the earliest precursors of large ribosomal subunits in yeast. Nucleic Acids Res 45:6837–47
    [Google Scholar]
  73. 73. 
    Chaker-Margot M, Hunziker M, Barandun J, Dill BD, Klinge S 2015. Stage-specific assembly events of the 6-MDa small-subunit processome initiate eukaryotic ribosome biogenesis. Nat. Struct. Mol. Biol. 22:920–23
    [Google Scholar]
  74. 74. 
    Nissan TA, Galani K, Maco B, Tollervey D, Aebi U, Hurt E 2004. A pre-ribosome with a tadpole-like structure functions in ATP-dependent maturation of 60S subunits. Mol. Cell 15:295–301
    [Google Scholar]
  75. 75. 
    Ulbrich C, Diepholz M, Baßler J, Kressler D, Pertschy B et al. 2009. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunit. Cell 138:911–22
    [Google Scholar]
  76. 76. 
    Schäfer T, Maco B, Petfalski E, Tollervey D, Bottcher B et al. 2006. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441:651–55
    [Google Scholar]
  77. 77. 
    Strunk B, Loucks C, Su M, Vashisth H, Cheng S et al. 2011. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333:1449–502
    [Google Scholar]
  78. 78. 
    Bradatsch B, Leidig C, Granneman S, Gnadig M, Tollervey D et al. 2012. Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel. Nat. Struct. Mol. Biol. 19:1234–41
    [Google Scholar]
  79. 79. 
    Larburu N, Montellese C, O'Donohue MF, Kutay U, Gleizes PE, Plisson-Chastang C 2016. Structure of a human pre-40S particle points to a role for RACK1 in the final steps of 18S rRNA processing. Nucleic Acids Res 44:8465–78
    [Google Scholar]
  80. 80. 
    Greber BJ, Boehringer D, Montellese C, Ban N 2012. Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. Nat. Struct. Mol. Biol. 19:1228–33
    [Google Scholar]
  81. 81. 
    Sengupta J, Bussiere C, Pallesen J, West M, Johnson AW, Frank J 2010. Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J. Cell Biol. 189:1079–86
    [Google Scholar]
  82. 82. 
    Malyutin AG, Musalgaonkar S, Patchett S, Frank J, Johnson AW 2017. Nmd3 is a structural mimic of eIF5A, and activates the cpGTPase Lsg1 during 60S ribosome biogenesis. EMBO J 36:854–68
    [Google Scholar]
  83. 83. 
    Ma C, Yan K, Tan D, Li N, Zhang Y et al. 2016. Structural dynamics of the yeast Shwachman-Diamond syndrome protein (Sdo1) on the ribosome and its implication in the 60S subunit maturation. Protein Cell 7:187–200
    [Google Scholar]
  84. 84. 
    Greber BJ, Gerhardy S, Leitner A, Leibundgut M, Salem M et al. 2016. Insertion of the biogenesis factor Rei1 probes the ribosomal tunnel during 60S maturation. Cell 164:91–102
    [Google Scholar]
  85. 85. 
    Kornprobst M, Turk M, Kellner N, Cheng J, Flemming D et al. 2016. Architecture of the 90S pre-ribosome: a structural view on the birth of the eukaryotic ribosome. Cell 166:380–93
    [Google Scholar]
  86. 86. 
    Chaker-Margot M, Barandun J, Hunziker M, Klinge S 2017. Architecture of the yeast small subunit processome. Science 355:aal1880
    [Google Scholar]
  87. 87. 
    Johnson MC, Ghalei H, Doxtader KA, Karbstein K, Stroupe ME 2017. Structural heterogeneity in pre-40S ribosomes. Structure 25:329–40
    [Google Scholar]
  88. 88. 
    Wu S, Tutuncuoglu B, Yan K, Brown H, Zhang Y et al. 2016. Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. Nature 534:133–37
    [Google Scholar]
  89. 89. 
    Leidig C, Thoms M, Holdermann I, Bradatsch B, Berninghausen O et al. 2014. 60S ribosome biogenesis requires rotation of the 5S ribonucleoprotein particle. Nat. Commun. 5:3491
    [Google Scholar]
  90. 90. 
    Baßler J, Paternoga H, Holdermann I, Thoms M, Granneman S et al. 2014. A network of assembly factors is involved in remodeling rRNA elements during preribosome maturation. J. Cell Biol. 207:481–98
    [Google Scholar]
  91. 91. 
    Shu S, Ye K. 2018. Structural and functional analysis of ribosome assembly factor Efg1. Nucleic Acids Res 46:2096–106
    [Google Scholar]
  92. 92. 
    Kressler D, Hurt E, Baßler J 2017. A puzzle of life: crafting ribosomal subunits. Trends Biochem. Sci. 42:640–54
    [Google Scholar]
  93. 93. 
    Greber BJ. 2016. Mechanistic insight into eukaryotic 60S ribosomal subunit biogenesis by cryo-electron microscopy. RNA 22:1643–62
    [Google Scholar]
  94. 94. 
    Barandun J, Hunziker M, Klinge S 2018. Assembly and structure of the SSU processome—a nucleolar precursor of the small ribosomal subunit. Curr. Opin. Struct. Biol. 49:85–93
    [Google Scholar]
  95. 95. 
    Biedka S, Wu S, LaPeruta AJ, Gao N, Woolford JL 2017. Insights into remodeling events during eukaryotic large ribosomal subunit assembly provided by high resolution cryo-EM structures. RNA Biol 14:1306–13
    [Google Scholar]
  96. 96. 
    Sun Q, Zhu X, Qi J, An W, Lan P et al. 2017. Molecular architecture of the 90S small subunit pre-ribosome. eLife 6:e22086
    [Google Scholar]
  97. 97. 
    Cheng J, Kellner N, Berninghausen O, Hurt E, Beckmann R 2017. 3.2-Å-resolution structure of the 90S preribosome before A1 pre-rRNA cleavage. Nat. Struct. Mol. Biol. 24:954–64
    [Google Scholar]
  98. 98. 
    Barandun J, Chaker-Margot M, Hunziker M, Molloy KR, Chait BT, Klinge S 2017. The complete structure of the small-subunit processome. Nat. Struct. Mol. Biol. 24:944–53
    [Google Scholar]
  99. 99. 
    Rout MP, Field MC. 2017. The evolution of organellar coat complexes and organization of the eukaryotic cell. Annu. Rev. Biochem. 86:637–57
    [Google Scholar]
  100. 100. 
    Fernandez-Pevida A, Kressler D, de la Cruz J 2015. Processing of preribosomal RNA in Saccharomyces cerevisiae.Wiley Interdiscip.Rev. . RNA 6:191–209
    [Google Scholar]
  101. 101. 
    Phipps KR, Charette J, Baserga SJ 2011. The small subunit processome in ribosome biogenesis—progress and prospects. Wiley Interdiscip. Rev. RNA 2:1–21
    [Google Scholar]
  102. 102. 
    Tomecki R, Labno A, Drazkowska K, Cysewski D, Dziembowski A 2015. hUTP24 is essential for processing of the human rRNA precursor at site A1, but not at site A0. RNA Biol 12:1010–29
    [Google Scholar]
  103. 103. 
    Bleichert F, Granneman S, Osheim YN, Beyer AL, Baserga SJ 2006. The PINc domain protein Utp24, a putative nuclease, is required for the early cleavage steps in 18S rRNA maturation. PNAS 103:9464–69
    [Google Scholar]
  104. 104. 
    Wells GR, Weichmann F, Colvin D, Sloan KE, Kudla G et al. 2016. The PIN domain endonuclease Utp24 cleaves pre-ribosomal RNA at two coupled sites in yeast and humans. Nucleic Acids Res 44:5399–409
    [Google Scholar]
  105. 105. 
    Horn DM, Mason SL, Karbstein K 2011. Rcl1 protein, a novel nuclease for 18 S ribosomal RNA production. J. Biol. Chem. 286:34082–87
    [Google Scholar]
  106. 106. 
    Zhu J, Liu X, Anjos M, Correll CC, Johnson AW 2016. Utp14 recruits and activates the RNA helicase Dhr1 to undock U3 snoRNA from the preribosome. Mol. Cell. Biol. 36:965–78
    [Google Scholar]
  107. 107. 
    Sardana R, Liu X, Granneman S, Zhu J, Gill M et al. 2015. The DEAH-box helicase Dhr1 dissociates U3 from the pre-rRNA to promote formation of the central pseudoknot. PLOS Biol 13:e1002083
    [Google Scholar]
  108. 108. 
    Scaiola A, Pena C, Weisser M, Bohringer D, Leibundgut M et al. 2018. Structure of a eukaryotic cytoplasmic pre-40S ribosomal subunit. EMBO J 37:e98499
    [Google Scholar]
  109. 109. 
    Heuer A, Thomson E, Schmidt C, Berninghausen O, Becker T et al. 2017. Cryo-EM structure of a late pre-40S ribosomal subunit from Saccharomyces cerevisiae. eLife 6:e30189
    [Google Scholar]
  110. 110. 
    Ghalei H, Schaub FX, Doherty JR, Noguchi Y, Roush WR et al. 2015. Hrr25/CK1δ-directed release of Ltv1 from pre-40S ribosomes is necessary for ribosome assembly and cell growth. J. Cell Biol. 208:745–59
    [Google Scholar]
  111. 111. 
    Mitterer V, Gantenbein N, Birner-Gruenberger R, Murat G, Bergler H et al. 2016. Nuclear import of dimerized ribosomal protein Rps3 in complex with its chaperone Yar1. Sci. Rep. 6:36714
    [Google Scholar]
  112. 112. 
    Turowski TW, Lebaron S, Zhang E, Peil L, Dudnakova T et al. 2014. Rio1 mediates ATP-dependent final maturation of 40S ribosomal subunits. Nucleic Acids Res 42:12189–99
    [Google Scholar]
  113. 113. 
    Strunk BS, Novak MN, Young CL, Karbstein K 2012. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150:111–21
    [Google Scholar]
  114. 114. 
    Ferreira-Cerca S, Kiburu I, Thomson E, LaRonde N, Hurt E 2014. Dominant Rio1 kinase/ATPase catalytic mutant induces trapping of late pre-40S biogenesis factors in 80S-like ribosomes. Nucleic Acids Res 42:8635–47
    [Google Scholar]
  115. 115. 
    Belhabich-Baumas K, Joret C, Jady BE, Plisson-Chastang C, Shayan R et al. 2017. The Rio1p ATPase hinders premature entry into translation of late pre-40S pre-ribosomal particles. Nucleic Acids Res 45:10824–36
    [Google Scholar]
  116. 116. 
    Ghalei H, Trepreau J, Collins JC, Bhaskaran H, Strunk BS, Karbstein K 2017. The ATPase Fap7 tests the ability to carry out translocation-like conformational changes and releases Dim1 during 40S ribosome maturation. Mol. Cell 67:990–1000
    [Google Scholar]
  117. 117. 
    Lebaron S, Schneider C, van Nues RW, Swiatkowska A, Walsh D et al. 2012. Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol. 19:744–53
    [Google Scholar]
  118. 118. 
    Ameismeier M, Cheng J, Berninghausen O, Beckmann R 2018. Visualizing late states of human 40S ribosomal subunit maturation. Nature 558:249–53
    [Google Scholar]
  119. 119. 
    Matsuo Y, Granneman S, Thoms M, Manikas RG, Tollervey D, Hurt E 2014. Coupled GTPase and remodelling ATPase activities form a checkpoint for ribosome export. Nature 505:112–16
    [Google Scholar]
  120. 120. 
    Sarkar A, Thoms M, Barrio-Garcia C, Thomson E, Flemming D et al. 2017. Preribosomes escaping from the nucleus are caught during translation by cytoplasmic quality control. Nat. Struct. Mol. Biol. 24:1107–15
    [Google Scholar]
  121. 121. 
    Rodriguez-Galan O, Garcia-Gomez JJ, Kressler D, de la Cruz J 2015. Immature large ribosomal subunits containing the 7S pre-rRNA can engage in translation in Saccharomyces cerevisiae. . RNA Biol 12:838–46
    [Google Scholar]
  122. 122. 
    Biedka S, Micic J, Wilson D, Brown H, Diorio-Toth L, Woolford JL 2018. Hierarchical recruitment of ribosomal proteins and assembly factors remodels nucleolar pre-60S ribosomes. J. Cell Biol. 217:2503–18
    [Google Scholar]
  123. 123. 
    Lebreton A, Rousselle JC, Lenormand P, Namane A, Jacquier A et al. 2008. 60S ribosomal subunit assembly dynamics defined by semi-quantitative mass spectrometry of purified complexes. Nucleic Acids Res 36:4988–99
    [Google Scholar]
  124. 124. 
    Ma C, Wu S, Li N, Chen Y, Yan K et al. 2017. Structural snapshot of cytoplasmic pre-60S ribosomal particles bound by Nmd3, Lsg1, Tif6 and Reh1. Nat. Struct. Mol. Biol. 24:214–20
    [Google Scholar]
  125. 125. 
    Weis F, Giudice E, Churcher M, Jin L, Hilcenko C et al. 2015. Mechanism of eIF6 release from the nascent 60S ribosomal subunit. Nat. Struct. Mol. Biol. 22:914–19
    [Google Scholar]
  126. 126. 
    Kater L, Thoms M, Barrio-Garcia C, Cheng J, Ismail S et al. 2017. Visualizing the assembly pathway of nucleolar pre-60S ribosomes. Cell 171:1599–610
    [Google Scholar]
  127. 127. 
    Sanghai ZA, Miller L, Molloy KR, Barandun J, Hunziker M et al. 2018. Modular assembly of the nucleolar pre-60S ribosomal subunit. Nature 556:126–29
    [Google Scholar]
  128. 128. 
    Zhou D, Zhu X, Zheng S, Tan D, Dong MQ, Ye K 2018. Cryo-EM structure of an early precursor of large ribosomal subunit reveals a half-assembled intermediate. Protein Cell https://doi.org/10.1007/s13238-018-0526-7
    [Crossref] [Google Scholar]
  129. 129. 
    van Nues RW, Rientjes JM, Morre SA, Mollee E, Planta RJ et al. 1995. Evolutionarily conserved structural elements are critical for processing of Internal Transcribed Spacer 2 from Saccharomyces cerevisiae precursor ribosomal RNA. J. Mol. Biol. 250:24–36
    [Google Scholar]
  130. 130. 
    van der Sande CA, Kwa M, van Nues RW, van Heerikhuizen H, Raue HA, Planta RJ 1992. Functional analysis of internal transcribed spacer 2 of Saccharomyces cerevisiae ribosomal DNA. J. Mol. Biol. 223:899–910
    [Google Scholar]
  131. 131. 
    Gadal O, Strauss D, Petfalski E, Gleizes PE, Gas N et al. 2002. Rlp7p is associated with 60S preribosomes, restricted to the granular component of the nucleolus, and required for pre-rRNA processing. J. Cell Biol. 157:941–51
    [Google Scholar]
  132. 132. 
    Adams CC, Jakovljevic J, Roman J, Harnpicharnchai P, Woolford JL Jr 2002. Saccharomyces cerevisiae nucleolar protein Nop7p is necessary for biogenesis of 60S ribosomal subunits. RNA 8:150–65
    [Google Scholar]
  133. 133. 
    Madru C, Lebaron S, Blaud M, Delbos L, Pipoli J et al. 2015. Chaperoning 5S RNA assembly. Genes Dev 29:1432–46
    [Google Scholar]
  134. 134. 
    Asano N, Kato K, Nakamura A, Komoda K, Tanaka I, Yao M 2015. Structural and functional analysis of the Rpf2–Rrs1 complex in ribosome biogenesis. Nucleic Acids Res 43:4746–57
    [Google Scholar]
  135. 135. 
    Kharde S, Calvino FR, Gumiero A, Wild K, Sinning I 2015. The structure of Rpf2–Rrs1 explains its role in ribosome biogenesis. Nucleic Acids Res 43:7083–95
    [Google Scholar]
  136. 136. 
    Baßler J, Kallas M, Ulbrich C, Thoms M, Pertschy B, Hurt E 2010. The AAA-ATPase Rea1 drives removal of biogenesis factors during multiple stages of 60S ribosome assembly. Mol. Cell 38:712–21
    [Google Scholar]
  137. 137. 
    Hiraishi N, Ishida YI, Sudo H, Nagahama M 2018. WDR74 participates in an early cleavage of the pre-rRNA processing pathway in cooperation with the nucleolar AAA-ATPase NVL2. Biochem. Biophys. Res. Commun. 495:116–23
    [Google Scholar]
  138. 138. 
    Kappel L, Loibl M, Zisser G, Klein I, Fruhmann G et al. 2012. Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation. J. Cell Biol. 199:771–82
    [Google Scholar]
  139. 139. 
    Traub P, Nomura M. 1968. Structure and function of E. coli ribosomes, V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. PNAS 59:777–84
    [Google Scholar]
  140. 140. 
    Granneman S, Lin C, Champion EA, Nandineni MR, Zorca C, Baserga SJ 2006. The nucleolar protein Esf2 interacts directly with the DExD/H box RNA helicase, Dbp8, to stimulate ATP hydrolysis. Nucleic Acids Res 34:3189–99
    [Google Scholar]
  141. 141. 
    Lebaron S, Papin C, Capeyrou R, Chen YL, Froment C et al. 2009. The ATPase and helicase activities of Prp43p are stimulated by the G-patch protein Pfa1p during yeast ribosome biogenesis. EMBO J 28:3808–19
    [Google Scholar]
  142. 142. 
    Khoshnevis S, Askenasy I, Johnson MC, Dattolo MD, Young-Erdos CL et al. 2016. The DEAD-box protein Rok1 orchestrates 40S and 60S ribosome assembly by promoting the release of Rrp5 from pre-40S ribosomes to allow for 60S maturation. PLOS Biol 14:e1002480
    [Google Scholar]
  143. 143. 
    Manikas RG, Thomson E, Thoms M, Hurt E 2016. The K+-dependent GTPase Nug1 is implicated in the association of the helicase Dbp10 to the immature peptidyl transferase centre during ribosome maturation. Nucleic Acids Res 44:1800–12
    [Google Scholar]
  144. 144. 
    Galardi S, Fatica A, Bachi A, Scaloni A, Presutti C, Bozzoni I 2002. Purified box C/D snoRNPs are able to reproduce site-specific 2′-O-methylation of target RNA in vitro. Mol. Cell. Biol. 22:6663–68
    [Google Scholar]
  145. 145. 
    Gasse L, Flemming D, Hurt E 2015. Coordinated ribosomal ITS2 RNA processing by the Las1 complex integrating endonuclease, polynucleotide kinase, and exonuclease activities. Mol. Cell 60:808–15
    [Google Scholar]
  146. 146. 
    Fromm L, Falk S, Flemming D, Schuller JM, Thoms M et al. 2017. Reconstitution of the complete pathway of ITS2 processing at the pre-ribosome. Nat. Commun. 8:1787
    [Google Scholar]
  147. 147. 
    Pillon MC, Sobhany M, Stanley RE 2018. Characterization of the molecular crosstalk within the essential Grc3/Las1 pre-rRNA processing complex. RNA 24:721–38
    [Google Scholar]
  148. 148. 
    Pillon MC, Sobhany M, Borgnia MJ, Williams JG, Stanley RE 2017. Grc3 programs the essential endoribonuclease Las1 for specific RNA cleavage. PNAS 114:E5530–38
    [Google Scholar]
  149. 149. 
    Schuller JM, Falk S, Fromm L, Hurt E, Conti E 2018. Structure of the nuclear exosome captured on a maturing preribosome. Science 360:219–22
    [Google Scholar]
  150. 150. 
    Thoms M, Thomson E, Baßler J, Gnadig M, Griesel S, Hurt E 2015. The exosome is recruited to RNA substrates through specific adaptor proteins. Cell 162:1029–38
    [Google Scholar]
  151. 151. 
    Narla A, Ebert BL. 2010. Ribosomopathies: human disorders of ribosome dysfunction. Blood 115:3196–205
    [Google Scholar]
  152. 152. 
    Danilova N, Gazda HT. 2015. Ribosomopathies: how a common root can cause a tree of pathologies. Dis. Models Mech. 8:1013–26
    [Google Scholar]
  153. 153. 
    Yelick PC, Trainor PA. 2015. Ribosomopathies: global process, tissue specific defects. Rare Dis 3:e1025185
    [Google Scholar]
  154. 154. 
    Pelava A, Schneider C, Watkins NJ 2016. The importance of ribosome production, and the 5S RNP-MDM2 pathway, in health and disease. Biochem. Soc. Trans. 44:1086–90
    [Google Scholar]
  155. 155. 
    Bursac S, Brdovcak MC, Donati G, Volarevic S 2014. Activation of the tumor suppressor p53 upon impairment of ribosome biogenesis. Biochim. Biophys. Acta 1842:817–30
    [Google Scholar]
  156. 156. 
    Holmberg Olausson K, Nister M, Lindstrom MS 2012. p53-dependent and -independent nucleolar stress responses. Cells 1:774–98
    [Google Scholar]
  157. 157. 
    Pelletier J, Thomas G, Volarevic S 2018. Ribosome biogenesis in cancer: new players and therapeutic avenues. Nat. Rev. Cancer 18:51–63
    [Google Scholar]
  158. 158. 
    Onofrillo C, Galbiati A, Montanaro L, Derenzini M 2017. The pre-existing population of 5S rRNA effects p53 stabilization during ribosome biogenesis inhibition. Oncotarget 8:4257–67
    [Google Scholar]
  159. 159. 
    Bursac S, Brdovcak MC, Pfannkuchen M, Orsolic I, Golomb L et al. 2012. Mutual protection of ribosomal proteins L5 and L11 from degradation is essential for p53 activation upon ribosomal biogenesis stress. PNAS 109:20467–72
    [Google Scholar]
  160. 160. 
    Zheng J, Lang Y, Zhang Q, Cui D, Sun H et al. 2015. Structure of human MDM2 complexed with RPL11 reveals the molecular basis of p53 activation. Genes Dev 29:1524–34
    [Google Scholar]
  161. 161. 
    Jaako P, Debnath S, Olsson K, Zhang Y, Flygare J et al. 2015. Disruption of the 5S RNP-Mdm2 interaction significantly improves the erythroid defect in a mouse model for Diamond-Blackfan anemia. Leukemia 29:2221–29
    [Google Scholar]
  162. 162. 
    Barlow JL, Drynan LF, Hewett DR, Holmes LR, Lorenzo-Abalde S et al. 2010. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat. Med. 16:59–66
    [Google Scholar]
  163. 163. 
    Jones NC, Lynn ML, Gaudenz K, Sakai D, Aoto K et al. 2008. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med. 14:125–33
    [Google Scholar]
  164. 164. 
    Macias E, Jin A, Deisenroth C, Bhat K, Mao H et al. 2010. An ARF-independent c-MYC-activated tumor suppression pathway mediated by ribosomal protein-Mdm2 interaction. Cancer Cell 18:231–43
    [Google Scholar]
  165. 165. 
    Kamio T, Gu BW, Olson TS, Zhang Y, Mason PJ, Bessler M 2016. Mice with a mutation in the Mdm2 gene that interferes with MDM2/ribosomal protein binding develop a defect in erythropoiesis. PLOS ONE 11:e0152263
    [Google Scholar]
  166. 166. 
    MacInnes AW, Amsterdam A, Whittaker CA, Hopkins N, Lees JA 2008. Loss of p53 synthesis in zebrafish tumors with ribosomal protein gene mutations. PNAS 105:10408–13
    [Google Scholar]
  167. 167. 
    Brighenti E, Trere D, Derenzini M 2015. Targeted cancer therapy with ribosome biogenesis inhibitors: a real possibility?. Oncotarget 6:38617–27
    [Google Scholar]
  168. 168. 
    Quin JE, Devlin JR, Cameron D, Hannan KM, Pearson RB, Hannan RD 2014. Targeting the nucleolus for cancer intervention. Biochim. Biophys. Acta 1842:802–16
    [Google Scholar]
  169. 169. 
    Derenzini E, Rossi A, Trere D 2018. Treating hematological malignancies with drugs inhibiting ribosome biogenesis: when and why. J. Hematol. Oncol. 11:75
    [Google Scholar]
  170. 170. 
    Burger K, Muhl B, Harasim T, Rohrmoser M, Malamoussi A et al. 2010. Chemotherapeutic drugs inhibit ribosome biogenesis at various levels. J. Biol. Chem. 285:12416–25
    [Google Scholar]
  171. 171. 
    Bruno PM, Liu Y, Park GY, Murai J, Koch CE et al. 2017. A subset of platinum-containing chemotherapeutic agents kills cells by inducing ribosome biogenesis stress. Nat. Med. 23:461–71
    [Google Scholar]
  172. 172. 
    Sapio RT, Nezdyur AN, Krevetski M, Anikin L, Manna VJ et al. 2017. Inhibition of post-transcriptional steps in ribosome biogenesis confers cytoprotection against chemotherapeutic agents in a p53-dependent manner. Sci. Rep. 7:9041
    [Google Scholar]
  173. 173. 
    Loibl M, Klein I, Prattes M, Schmidt C, Kappel L et al. 2014. The drug diazaborine blocks ribosome biogenesis by inhibiting the AAA-ATPase Drg1. J. Biol. Chem. 289:3913–22
    [Google Scholar]
  174. 174. 
    Kawashima SA, Chen Z, Aoi Y, Patgiri A, Kobayashi Y et al. 2016. Potent, reversible, and specific chemical inhibitors of eukaryotic ribosome biogenesis. Cell 167:512–24
    [Google Scholar]
  175. 175. 
    Neyer S, Kunz M, Geiss C, Hantsche M, Hodirnau VV et al. 2016. Structure of RNA polymerase I transcribing ribosomal DNA genes. Nature 540:607–10
    [Google Scholar]
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