6g51 Citations

Visualizing late states of human 40S ribosomal subunit maturation.

Nature 558 249-253 (2018)
Related entries: 6g18, 6g4s, 6g4w, 6g53, 6g5h, 6g5i

Cited: 72 times
EuropePMC logo PMID: 29875412

Abstract

The formation of eukaryotic ribosomal subunits extends from the nucleolus to the cytoplasm and entails hundreds of assembly factors. Despite differences in the pathways of ribosome formation, high-resolution structural information has been available only from fungi. Here we present cryo-electron microscopy structures of late-stage human 40S assembly intermediates, representing one state reconstituted in vitro and five native states that range from nuclear to late cytoplasmic. The earliest particles reveal the position of the biogenesis factor RRP12 and distinct immature rRNA conformations that accompany the formation of the 40S subunit head. Molecular models of the late-acting assembly factors TSR1, RIOK1, RIOK2, ENP1, LTV1, PNO1 and NOB1 provide mechanistic details that underlie their contribution to a sequential 40S subunit assembly. The NOB1 architecture displays an inactive nuclease conformation that requires rearrangement of the PNO1-bound 3' rRNA, thereby coordinating the final rRNA folding steps with site 3 cleavage.

Articles - 6g51 mentioned but not cited (4)

  1. Measurement of atom resolvability in cryo-EM maps with Q-scores. Pintilie G, Zhang K, Su Z, Li S, Schmid MF, Chiu W. Nat Methods 17 328-334 (2020)
  2. The final step of 40S ribosomal subunit maturation is controlled by a dual key lock. Plassart L, Shayan R, Montellese C, Rinaldi D, Larburu N, Pichereaux C, Froment C, Lebaron S, O'Donohue MF, Kutay U, Marcoux J, Gleizes PE, Plisson-Chastang C. Elife 10 e61254 (2021)
  3. Crystal structure of human RIOK2 bound to a specific inhibitor. Wang J, Varin T, Vieth M, Elkins JM. Open Biol 9 190037 (2019)
  4. The nucleoplasmic phase of pre-40S formation prior to nuclear export. Cheng J, Lau B, Thoms M, Ameismeier M, Berninghausen O, Hurt E, Beckmann R. Nucleic Acids Res 50 11924-11937 (2022)


Reviews citing this publication (12)

  1. Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors. Sáez-Vásquez J, Delseny M. Plant Cell 31 1945-1967 (2019)
  2. Eukaryotic Ribosome Assembly. Baßler J, Hurt E. Annu Rev Biochem 88 281-306 (2019)
  3. The World of Stable Ribonucleoproteins and Its Mapping With Grad-Seq and Related Approaches. Gerovac M, Vogel J, Smirnov A. Front Mol Biosci 8 661448 (2021)
  4. Maturation of pre-40S particles in yeast and humans. Cerezo E, Plisson-Chastang C, Henras AK, Lebaron S, Gleizes PE, O'Donohue MF, Romeo Y, Henry Y. Wiley Interdiscip Rev RNA 10 e1516 (2019)
  5. Pre-Ribosomal RNA Processing in Human Cells: From Mechanisms to Congenital Diseases. Aubert M, O'Donohue MF, Lebaron S, Gleizes PE. Biomolecules 8 (2018)
  6. RNA folding and functions of RNA helicases in ribosome biogenesis. Mitterer V, Pertschy B. RNA Biol 19 781-810 (2022)
  7. Ribosome biogenesis factors-from names to functions. Dörner K, Ruggeri C, Zemp I, Kutay U. EMBO J 42 e112699 (2023)
  8. The Rio1 protein kinases/ATPases: conserved regulators of growth, division, and genomic stability. Berto G, Ferreira-Cerca S, De Wulf P. Curr Genet 65 457-466 (2019)
  9. Uncovering the assembly pathway of human ribosomes and its emerging links to disease. Bohnsack KE, Bohnsack MT. EMBO J. 38 e100278 (2019)
  10. Genetics animates structure: leveraging genetic interactions to study the dynamics of ribosome biogenesis. Black JJ, Johnson AW. Curr Genet 67 729-738 (2021)
  11. A Comparative Perspective on Ribosome Biogenesis: Unity and Diversity Across the Tree of Life. Jüttner M, Ferreira-Cerca S. Methods Mol Biol 2533 3-22 (2022)
  12. Quality control ensures fidelity in ribosome assembly and cellular health. Parker MD, Karbstein K. J Cell Biol 222 e202209115 (2023)

Articles citing this publication (56)

  1. Structural basis for translational shutdown and immune evasion by the Nsp1 protein of SARS-CoV-2. Thoms M, Buschauer R, Ameismeier M, Koepke L, Denk T, Hirschenberger M, Kratzat H, Hayn M, Mackens-Kiani T, Cheng J, Straub JH, Stürzel CM, Fröhlich T, Berninghausen O, Becker T, Kirchhoff F, Sparrer KMJ, Beckmann R. Science 369 1249-1255 (2020)
  2. Structural basis for the final steps of human 40S ribosome maturation. Ameismeier M, Zemp I, van den Heuvel J, Thoms M, Berninghausen O, Kutay U, Beckmann R. Nature 587 683-687 (2020)
  3. Quality control of 40S ribosome head assembly ensures scanning competence. Huang H, Ghalei H, Karbstein K. J Cell Biol 219 e202004161 (2020)
  4. A conserved rRNA switch is central to decoding site maturation on the small ribosomal subunit. Schedlbauer A, Iturrioz I, Ochoa-Lizarralde B, Diercks T, López-Alonso JP, Lavin JL, Kaminishi T, Çapuni R, Dhimole N, de Astigarraga E, Gil-Carton D, Fucini P, Connell SR. Sci Adv 7 eabf7547 (2021)
  5. Phosphoproteomic Analysis Reveals Rio1-Related Protein Phosphorylation Changes in Response to UV Irradiation in Sulfolobus islandicus REY15A. Huang Q, Lin Z, Wu P, Ni J, Shen Y. Front Microbiol 11 586025 (2020)
  6. Insights into synthesis and function of KsgA/Dim1-dependent rRNA modifications in archaea. Knüppel R, Trahan C, Kern M, Wagner A, Grünberger F, Hausner W, Quax TEF, Albers SV, Oeffinger M, Ferreira-Cerca S. Nucleic Acids Res 49 1662-1687 (2021)
  7. SARS-CoV-2 Disrupts Splicing, Translation, and Protein Trafficking to Suppress Host Defenses. Banerjee AK, Blanco MR, Bruce EA, Honson DD, Chen LM, Chow A, Bhat P, Ollikainen N, Quinodoz SA, Loney C, Thai J, Miller ZD, Lin AE, Schmidt MM, Stewart DG, Goldfarb D, De Lorenzo G, Rihn SJ, Voorhees RM, Botten JW, Majumdar D, Guttman M. Cell 183 1325-1339.e21 (2020)
  8. The human RNA helicase DHX37 is required for release of the U3 snoRNP from pre-ribosomal particles. Choudhury P, Hackert P, Memet I, Sloan KE, Bohnsack MT. RNA Biol 16 54-68 (2019)
  9. USP16 counteracts mono-ubiquitination of RPS27a and promotes maturation of the 40S ribosomal subunit. Montellese C, van den Heuvel J, Ashiono C, Dörner K, Melnik A, Jonas S, Zemp I, Picotti P, Gillet LC, Kutay U. Elife 9 (2020)
  10. Good Vibrations: Structural Remodeling of Maturing Yeast Pre-40S Ribosomal Particles Followed by Cryo-Electron Microscopy. Shayan R, Rinaldi D, Larburu N, Plassart L, Balor S, Bouyssié D, Lebaron S, Marcoux J, Gleizes PE, Plisson-Chastang C. Molecules 25 (2020)
  11. Impact of two neighbouring ribosomal protein clusters on biogenesis factor binding and assembly of yeast late small ribosomal subunit precursors. Linnemann J, Pöll G, Jakob S, Ferreira-Cerca S, Griesenbeck J, Tschochner H, Milkereit P. PLoS ONE 14 e0203415 (2019)
  12. Interactions and activities of factors involved in the late stages of human 18S rRNA maturation. Sloan KE, Knox AA, Wells GR, Schneider C, Watkins NJ. RNA Biol 16 196-210 (2019)
  13. The human 18S rRNA m6A methyltransferase METTL5 is stabilized by TRMT112. van Tran N, Ernst FGM, Hawley BR, Zorbas C, Ulryck N, Hackert P, Bohnsack KE, Bohnsack MT, Jaffrey SR, Graille M, Lafontaine DLJ. Nucleic Acids Res. 47 7719-7733 (2019)
  14. A structural inventory of native ribosomal ABCE1-43S pre-initiation complexes. Kratzat H, Mackens-Kiani T, Ameismeier M, Potocnjak M, Cheng J, Dacheux E, Namane A, Berninghausen O, Herzog F, Fromont-Racine M, Becker T, Beckmann R. EMBO J 40 e105179 (2021)
  15. Cryo-EM reconstruction of the human 40S ribosomal subunit at 2.15 Å resolution. Pellegrino S, Dent KC, Spikes T, Warren AJ. Nucleic Acids Res 51 4043-4054 (2023)
  16. Domain definition and interaction mapping for the endonuclease complex hNob1/hPno1. Raoelijaona F, Thore S, Fribourg S. RNA Biol 15 1174-1180 (2018)
  17. Kaposi's sarcoma-associated herpesvirus induces specialised ribosomes to efficiently translate viral lytic mRNAs. Murphy JC, Harrington EM, Schumann S, Vasconcelos EJR, Mottram TJ, Harper KL, Aspden JL, Whitehouse A. Nat Commun 14 300 (2023)
  18. New Selective Inhibitors of ERG Positive Prostate Cancer: ERGi-USU-6 Salt Derivatives. Eldhose B, Pandrala M, Xavier C, Mohamed AA, Srivastava S, Sunkara AD, Dobi A, Malhotra SV. ACS Med Chem Lett 12 1703-1709 (2021)
  19. Nucleolar maturation of the human small subunit processome. Singh S, Vanden Broeck A, Miller L, Chaker-Margot M, Klinge S. Science 373 eabj5338 (2021)
  20. RIOK2 phosphorylation by RSK promotes synthesis of the human small ribosomal subunit. Cerezo EL, Houles T, Lié O, Sarthou MK, Audoynaud C, Lavoie G, Halladjian M, Cantaloube S, Froment C, Burlet-Schiltz O, Henry Y, Roux PP, Henras AK, Romeo Y. PLoS Genet 17 e1009583 (2021)
  21. Ratchet, swivel, tilt and roll: a complete description of subunit rotation in the ribosome. Hassan A, Byju S, Freitas FC, Roc C, Pender N, Nguyen K, Kimbrough EM, Mattingly JM, Gonzalez RL, de Oliveira RJ, Dunham CM, Whitford PC. Nucleic Acids Res 51 919-934 (2023)
  22. A kinase-dependent checkpoint prevents escape of immature ribosomes into the translating pool. Parker MD, Collins JC, Korona B, Ghalei H, Karbstein K. PLoS Biol. 17 e3000329 (2019)
  23. A ribosomal gene panel predicting a novel synthetic lethality in non-BRCAness tumors. Zhang C, Guo Q, Chen L, Wu Z, Yan XJ, Zou C, Zhang Q, Tan J, Fang T, Rao Q, Li Y, Shen S, Deng M, Wang L, Gao H, Yu J, Li H, Zhang C, Nowsheen S, Kloeber J, Zhao F, Yin P, Teng C, Lin Z, Song K, Yao S, Yao L, Wu L, Zhang Y, Cheng X, Gao Q, Yuan J, Lou Z, Zhang JS. Signal Transduct Target Ther 8 183 (2023)
  24. Bud23 promotes the final disassembly of the small subunit Processome in Saccharomyces cerevisiae. Black JJ, Sardana R, Elmir EW, Johnson AW. PLoS Genet 16 e1009215 (2020)
  25. Cms1 coordinates stepwise local 90S pre-ribosome assembly with timely snR83 release. Lau B, Beine-Golovchuk O, Kornprobst M, Cheng J, Kressler D, Jády B, Kiss T, Beckmann R, Hurt E. Cell Rep 41 111684 (2022)
  26. Computational Studies of the Structural Basis of Human RPS19 Mutations Associated With Diamond-Blackfan Anemia. An K, Zhou JB, Xiong Y, Han W, Wang T, Ye ZQ, Wu YD. Front Genet 12 650897 (2021)
  27. Conformational proofreading of distant 40S ribosomal subunit maturation events by a long-range communication mechanism. Mitterer V, Shayan R, Ferreira-Cerca S, Murat G, Enne T, Rinaldi D, Weigl S, Omanic H, Gleizes PE, Kressler D, Plisson-Chastang C, Pertschy B. Nat Commun 10 2754 (2019)
  28. Dynamics of nuclear export of pre-ribosomal subunits revealed by high-speed single-molecule microscopy in live cells. Junod SL, Tingey M, Kelich JM, Goryaynov A, Herbine K, Yang W. iScience 26 107445 (2023)
  29. Efficient fractionation and analysis of ribosome assembly intermediates in human cells. Nieto B, Gaspar SG, Sapio RT, Clavaín L, Bustelo XR, Pestov DG, Dosil M. RNA Biol 18 182-197 (2021)
  30. Eukaryotic Ribosome Biogenesis: The 60S Subunit. Moraleva AA, Deryabin AS, Rubtsov YP, Rubtsova MP, Dontsova OA. Acta Naturae 14 39-49 (2022)
  31. Exploration of tricyclic heterocycles as core structures for RIOK2 inhibitors. Xiong H, Yu Q, Ma H, Yu X, Ouyang Y, Zhang ZM, Zhou W, Zhang Z, Cai Q. RSC Med Chem 14 2007-2011 (2023)
  32. Identification of RIOK2 as a master regulator of human blood cell development. Ghosh S, Raundhal M, Myers SA, Carr SA, Chen X, Petsko GA, Glimcher LH. Nat Immunol 23 109-121 (2022)
  33. Identification of distinct maturation steps involved in human 40S ribosomal subunit biosynthesis. Nieto B, Gaspar SG, Moriggi G, Pestov DG, Bustelo XR, Dosil M. Nat Commun 11 156 (2020)
  34. Impact of the yeast S0/uS2-cluster ribosomal protein rpS21/eS21 on rRNA folding and the architecture of small ribosomal subunit precursors. Pöll G, Griesenbeck J, Tschochner H, Milkereit P. PLoS One 18 e0283698 (2023)
  35. In vitro dimerization of human RIO2 kinase. Maurice F, Pérébaskine N, Thore S, Fribourg S. RNA Biol 16 1633-1642 (2019)
  36. Inhibiting eukaryotic ribosome biogenesis. Awad D, Prattes M, Kofler L, Rössler I, Loibl M, Pertl M, Zisser G, Wolinski H, Pertschy B, Bergler H. BMC Biol. 17 46 (2019)
  37. Molecular basis for recognition and deubiquitination of 40S ribosomes by Otu2. Ikeuchi K, Ivic N, Buschauer R, Cheng J, Fröhlich T, Matsuo Y, Berninghausen O, Inada T, Becker T, Beckmann R. Nat Commun 14 2730 (2023)
  38. Mutations in RPS19 may affect ribosome function and biogenesis in Diamond Blackfan anemia. Hiregange DG, Rivalta A, Yonath A, Zimmerman E, Bashan A, Yonath H. FEBS Open Bio 12 1419-1434 (2022)
  39. Mutations in the ribosome biogenesis factor gene LTV1 are linked to LIPHAK syndrome, a novel poikiloderma-like disorder. Han JH, Ryan G, Guy A, Liu L, Quinodoz M, Helbling I, Lai-Cheong JE, Genomics England Research Consortium, Barwell J, Folcher M, McGrath JA, Moss C, Rivolta C. Hum Mol Genet 31 1970-1978 (2022)
  40. Nop9 recognizes structured and single-stranded RNA elements of preribosomal RNA. Zhang J, Teramoto T, Qiu C, Wine RN, Gonzalez LE, Baserga SJ, Tanaka Hall TM. RNA 26 1049-1059 (2020)
  41. PDCD2 functions as an evolutionarily conserved chaperone dedicated for the 40S ribosomal protein uS5 (RPS2). Landry-Voyer AM, Bergeron D, Yague-Sanz C, Baker B, Bachand F. Nucleic Acids Res 48 12900-12916 (2020)
  42. PNO1 promotes the progression of osteosarcoma via TGF-β and YAP/TAZ pathway. Fang L, Wang B, Yang Z, Zhao T, Hao W. Sci Rep 13 21827 (2023)
  43. Processing of the ribosomal ubiquitin-like fusion protein FUBI-eS30/FAU is required for 40S maturation and depends on USP36. van den Heuvel J, Ashiono C, Gillet LC, Dörner K, Wyler E, Zemp I, Kutay U. Elife 10 e70560 (2021)
  44. Prp43/DHX15 exemplify RNA helicase multifunctionality in the gene expression network. Bohnsack KE, Kanwal N, Bohnsack MT. Nucleic Acids Res 50 9012-9022 (2022)
  45. RIOK2 Contributes to Cell Growth and Protein Synthesis in Human Oral Squamous Cell Carcinoma. Matsuzaki Y, Naito Y, Miura N, Mori T, Watabe Y, Yoshimoto S, Shibahara T, Takano M, Honda K. Curr Oncol 30 381-391 (2022)
  46. RPS15 interacted with IGF2BP1 to promote esophageal squamous cell carcinoma development via recognizing m6A modification. Zhao Y, Li Y, Zhu R, Feng R, Cui H, Yu X, Huang F, Zhang R, Chen X, Li L, Chen Y, Liu Y, Wang J, Du G, Liu Z. Signal Transduct Target Ther 8 224 (2023)
  47. Release of the ribosome biogenesis factor Bud23 from small subunit precursors in yeast. Black JJ, Johnson AW. RNA 28 371-389 (2022)
  48. Structural snapshots of human pre-60S ribosomal particles before and after nuclear export. Liang X, Zuo MQ, Zhang Y, Li N, Ma C, Dong MQ, Gao N. Nat Commun 11 3542 (2020)
  49. The C-terminal tail of ribosomal protein Rps15 is engaged in cytoplasmic pre-40S maturation. Rössler I, Weigl S, Fernández-Fernández J, Martín-Villanueva S, Strauss D, Hurt E, de la Cruz J, Pertschy B. RNA Biol 19 560-574 (2022)
  50. The DEAH-box RNA helicase Dhr1 contains a remarkable carboxyl terminal domain essential for small ribosomal subunit biogenesis. Roychowdhury A, Joret C, Bourgeois G, Heurgué-Hamard V, Lafontaine DLJ, Graille M. Nucleic Acids Res. 47 7548-7563 (2019)
  51. The METTL5-TRMT112 N6-methyladenosine methyltransferase complex regulates mRNA translation via 18S rRNA methylation. Sepich-Poore C, Zheng Z, Schmitt E, Wen K, Zhang ZS, Cui XL, Dai Q, Zhu AC, Zhang L, Sanchez Castillo A, Tan H, Peng J, Zhuang X, He C, Nachtergaele S. J Biol Chem 298 101590 (2022)
  52. The Ribosome Biogenesis Factor Ltv1 Is Essential for Digestive Organ Development and Definitive Hematopoiesis in Zebrafish. Zhang C, Huang R, Ma X, Chen J, Han X, Li L, Luo L, Ruan H, Huang H. Front Cell Dev Biol 9 704730 (2021)
  53. The dark side of the ribosome life cycle. Ferreira-Cerca S. RNA Biol 19 1045-1049 (2022)
  54. The modifying enzyme Tsr3 establishes the hierarchy of Rio kinase binding in 40S ribosome assembly. Huang H, Parker M, Karbstein K. RNA 28 568-582 (2022)
  55. The path of pre-ribosomes through the nuclear pore complex revealed by electron tomography. Delavoie F, Soldan V, Rinaldi D, Dauxois JY, Gleizes PE. Nat Commun 10 497 (2019)
  56. Visualizing the nucleoplasmic maturation of human pre-60S ribosomal particles. Zhang Y, Liang X, Luo S, Chen Y, Li Y, Ma C, Li N, Gao N. Cell Res (2023)