5wyj

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Cryo-EM structure of the 90S small subunit pre-ribosome (Dhr1-depleted, Enp1-TAP, state 1)

Structural highlights

5wyj is a 64 chain structure with sequence from Baker's yeast and Saccharomyces cerevisiae (strain atcc 204508 / s288c). Full crystallographic information is available from OCA. For a guided tour on the structure components use FirstGlance.
Activity:rRNA small subunit pseudouridine methyltransferase Nep1, with EC number 2.1.1.260
Experimental data:Check to display Experimental Data
Resources:FirstGlance, OCA, PDBe, RCSB, PDBsum, ProSAT

Function

[RRP5_YEAST] Involved in the biogenesis of rRNA. Required for the formation of 18S and 5.8S rRNA.[1] [RRP7_YEAST] Plays an important role in the synthesis of 18S rRNA but is not required for the 5.8S and 25S pathway. Is necessary for the cleavage at site A2. Is required for efficient association of RPS27 with the pre-ribosomal particle. [KRR1_YEAST] Required for 40S ribosome biogenesis. Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly. Essential for vegetative growth.[2] [3] [4] [5] [FBRL_YEAST] S-adenosyl-L-methionine-dependent methyltransferase that has the ability to methylate both RNAs and proteins. Involved in pre-rRNA processing by catalyzing the site-specific 2'-hydroxyl methylation of ribose moieties in pre-ribosomal RNA (PubMed:1825809). Site specificity is provided by a guide RNA that base pairs with the substrate. Methylation occurs at a characteristic distance from the sequence involved in base pairing with the guide RNA. Involved in the biogenesis of the 18S rRNA. Also acts as a protein methyltransferase by mediating methylation of 'Gln-105' of histone H2A (H2AQ105me), a modification that impairs binding of the FACT complex and is specifically present at 35S ribosomal DNA locus (PubMed:24352239).[6] [7] [8] [UTP12_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA.[9] [UTP13_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA.[10] [PNO1_YEAST] Required for small ribosomal subunit (SSU) synthesis. Has a role in the processing of early nucleolar and late cytoplasmic pre-RNA species. Recruits DIM1 to nucleolar pre-RNAs. Indirectly required for cleavage at the A2 site of the 20S pre-rRNA, forming 18S rRNA, and at A1 and A2 sites of other pre-rRNAs.[11] [12] [13] [PWP2_YEAST] Required for bud-site selection and cell separation. Also involved in nucleolar processing of pre-18S ribosomal RNA.[14] [15] [IMP3_YEAST] Required for the early cleavages at sites A0, A1 and A2 during 18S ribosomal pre-RNA processing.[16] [17] [IMP4_YEAST] Required for the early cleavages at sites A0, A1 and A2 during 18S ribosomal pre-RNA processing.[18] [19] [FCF1_YEAST] Essential protein involved in pre-rRNA processing and 40S ribosomal subunit assembly. Required for the early cleavage steps of 35S rRNA at the A(0), A(1), and A(2) sites.[20] [UTP21_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly.[21] [ENP1_YEAST] Required for normal export of the pre-40S particles from the nucleus to the cytoplasm. Its subcellular location and association with pre-40S subunit shifts from mixed cytoplasm/nucleus to all nuclear in RPS19 disruptions, suggesting it acts after the ribosomal protein.[22] [23] [RCL1_YEAST] Does not have cyclase activity. Plays a role in 40S-ribosomal-subunit biogenesis in the early pre-rRNA processing steps at sites A0, A1 and A2 that are required for proper maturation of the 18S RNA. Essential for viability. [RS27A_YEAST] Ubiquitin exists either covalently attached to another protein, or free (unanchored). When covalently bound, it is conjugated to target proteins via an isopeptide bond either as a monomer (monoubiquitin), a polymer linked via different Lys residues of the ubiquitin (polyubiquitin chains) or a linear polymer linked via the initiator Met of the ubiquitin (linear polyubiquitin chains). Polyubiquitin chains, when attached to a target protein, have different functions depending on the Lys residue of the ubiquitin that is linked: Lys-6-linked may be involved in DNA repair; Lys-11-linked is involved in ERAD (endoplasmic reticulum-associated degradation) and in cell-cycle regulation; Lys-29-linked is involved in lysosomal degradation; Lys-33-linked is involved in kinase modification; Lys-48-linked is involved in protein degradation via the proteasome; Lys-63-linked is involved in endocytosis, and DNA-damage responses. Linear polymer chains formed via attachment by the initiator Met lead to cell signaling. Ubiquitin is usually conjugated to Lys residues of target proteins, however, in rare cases, conjugation to Cys or Ser residues has been observed. When polyubiquitin is free (unanchored-polyubiquitin), it also has distinct roles, such as in activation of protein kinases, and in signaling (By similarity). 40S ribosomal protein S31 is a component of the 40S subunit of the ribosome (By similarity). [UTP22_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly.[24] [NEP1_YEAST] S-adenosyl-L-methionine-dependent pseudouridine N(1)-methyltransferase that methylates pseudouridine at position 1189 (Psi1189) in 18S rRNA. Involved the biosynthesis of the hypermodified N1-methyl-N3-(3-amino-3-carboxypropyl) pseudouridine (m1acp3-Psi) conserved in eukaryotic 18S rRNA. N1-methylation is independent on acp-modification at the N3-position of U1191. Has also an essential role in 40S ribosomal subunit biogenesis independent on its methyltransferase activity, facilitating the incorporation of ribosomal protein S19 (RPS19A/RPS19B) during the formation of pre-ribosomes.[25] [26] [27] [28] [29] [SNU13_YEAST] Common component of the spliceosome and rRNA processing machinery. In association with the spliceosomal U4/U6.U5 tri-snRNP particle, required for splicing of pre-mRNA. In association with box C/D snoRNPs, required for processing of pre-ribosomal RNA (rRNA) and site-specific 2'-O-methylation of substrate RNAs. Essential for the accumulation and stability of U4 snRNA, U6 snRNA, and box C/D snoRNAs.[30] [31] [32] [RS7A_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly.[33] [NOP56_YEAST] Required for 60S ribosomal subunit synthesis.[34] [RL1D1_YEAST] Involved in rRNA-processing and ribosome biosynthesis.[35] [RS9A_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly.[36] [UTP10_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA. Required for optimal pre-ribosomal RNA transcription by RNA polymerase I together with a subset of U3 proteins required for transcription (t-UTPs). Involved in ribosome biosynthesis.[37] [38] [39] [40] [BMS1_YEAST] May act as a molecular switch during maturation of the 40S ribosomal subunit in the nucleolus. The depletion of BMS1 interferes with processing of the 35S pre-rRNA at sites A0, A1, and A2, and the formation of 40S subunits.[41] [42] [RS6A_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly.[43] [NOP58_YEAST] Required for pre-18S rRNA processing. May bind microtubules.[44] [45] [RS14A_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly.[46] [UTP18_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA and ribosome assembly.[47] [RRP9_YEAST] Involved in nucleolar processing of pre-18S ribosomal RNA. Required for efficient pre-rRNA cleavage at sites A0, A1 and A2, and biosynthesis of 18S rRNA.[48]

Publication Abstract from PubMed

Eukaryotic small ribosomal subunits are first assembled into 90S pre-ribosomes. The complete 90S is a gigantic complex with a molecular mass of approximately five megadaltons. Here, we report the nearly complete architecture of Saccharomyces cerevisiae 90S determined from three cryo-electron microscopy single particle reconstructions at 4.5 to 8.7 angstrom resolution. The majority of the density maps were modeled and assigned to specific RNA and protein components. The nascent ribosome is assembled into isolated native-like substructures that are stabilized by abundant assembly factors. The 5' external transcribed spacer and U3 snoRNA nucleate a large subcomplex that scaffolds the nascent ribosome. U3 binds four sites of pre-rRNA, including a novel site on helix 27 but not the 3' side of the central pseudoknot, and crucially organizes the 90S structure. The 90S model provides significant insight into the principle of small subunit assembly and the function of assembly factors.

Molecular architecture of the 90S small subunit pre-ribosome.,Sun Q, Zhu X, Qi J, An W, Lan P, Tan D, Chen R, Wang B, Zheng S, Zhang C, Chen X, Zhang W, Chen J, Dong MQ, Ye K Elife. 2017 Feb 28;6. pii: e22086. doi: 10.7554/eLife.22086. PMID:28244370[49]

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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See Also

References

  1. ↑ Venema J, Tollervey D. RRP5 is required for formation of both 18S and 5.8S rRNA in yeast. EMBO J. 1996 Oct 15;15(20):5701-14. PMID:8896463
  2. ↑ Gromadka R, Rytka J. The KRR1 gene encodes a protein required for 18S rRNA synthesis and 40S ribosomal subunit assembly in Saccharomyces cerevisiae. Acta Biochim Pol. 2000;47(4):993-1005. PMID:11996121
  3. ↑ Sasaki T, Toh-E A, Kikuchi Y. Yeast Krr1p physically and functionally interacts with a novel essential Kri1p, and both proteins are required for 40S ribosome biogenesis in the nucleolus. Mol Cell Biol. 2000 Nov;20(21):7971-9. PMID:11027267
  4. ↑ Gromadka R, Karkusiewicz I, Rempola B, Rytka J. Functional and physical interactions of Krr1p, a Saccharomyces cerevisiae nucleolar protein. Acta Biochim Pol. 2004;51(1):173-87. PMID:15094838 doi:http://dx.doi.org/045101173
  5. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  6. ↑ Tollervey D, Lehtonen H, Carmo-Fonseca M, Hurt EC. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 1991 Mar;10(3):573-83. PMID:1825809
  7. ↑ Tessarz P, Santos-Rosa H, Robson SC, Sylvestersen KB, Nelson CJ, Nielsen ML, Kouzarides T. Glutamine methylation in histone H2A is an RNA-polymerase-I-dedicated modification. Nature. 2014 Jan 23;505(7484):564-8. doi: 10.1038/nature12819. Epub 2013 Dec 18. PMID:24352239 doi:http://dx.doi.org/10.1038/nature12819
  8. ↑ Schimmang T, Tollervey D, Kern H, Frank R, Hurt EC. A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 1989 Dec 20;8(13):4015-24. PMID:2686980
  9. ↑ Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature. 2002 Jun 27;417(6892):967-70. Epub 2002 Jun 9. PMID:12068309 doi:http://dx.doi.org/10.1038/nature00769
  10. ↑ Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature. 2002 Jun 27;417(6892):967-70. Epub 2002 Jun 9. PMID:12068309 doi:http://dx.doi.org/10.1038/nature00769
  11. ↑ Tone Y, Toh-E A. Nob1p is required for biogenesis of the 26S proteasome and degraded upon its maturation in Saccharomyces cerevisiae. Genes Dev. 2002 Dec 15;16(24):3142-57. PMID:12502737 doi:http://dx.doi.org/10.1101/gad.1025602
  12. ↑ Senapin S, Clark-Walker GD, Chen XJ, Seraphin B, Daugeron MC. RRP20, a component of the 90S preribosome, is required for pre-18S rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res. 2003 May 15;31(10):2524-33. PMID:12736301
  13. ↑ Vanrobays E, Gelugne JP, Caizergues-Ferrer M, Lafontaine DL. Dim2p, a KH-domain protein required for small ribosomal subunit synthesis. RNA. 2004 Apr;10(4):645-56. PMID:15037774
  14. ↑ Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature. 2002 Jun 27;417(6892):967-70. Epub 2002 Jun 9. PMID:12068309 doi:http://dx.doi.org/10.1038/nature00769
  15. ↑ Shafaatian R, Payton MA, Reid JD. PWP2, a member of the WD-repeat family of proteins, is an essential Saccharomyces cerevisiae gene involved in cell separation. Mol Gen Genet. 1996 Aug 27;252(1-2):101-14. PMID:8804409
  16. ↑ Lee SJ, Baserga SJ. Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing. Mol Cell Biol. 1999 Aug;19(8):5441-52. PMID:10409734
  17. ↑ Gerczei T, Correll CC. Imp3p and Imp4p mediate formation of essential U3-precursor rRNA (pre-rRNA) duplexes, possibly to recruit the small subunit processome to the pre-rRNA. Proc Natl Acad Sci U S A. 2004 Oct 26;101(43):15301-6. Epub 2004 Oct 15. PMID:15489263 doi:http://dx.doi.org/10.1073/pnas.0406819101
  18. ↑ Lee SJ, Baserga SJ. Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing. Mol Cell Biol. 1999 Aug;19(8):5441-52. PMID:10409734
  19. ↑ Gerczei T, Correll CC. Imp3p and Imp4p mediate formation of essential U3-precursor rRNA (pre-rRNA) duplexes, possibly to recruit the small subunit processome to the pre-rRNA. Proc Natl Acad Sci U S A. 2004 Oct 26;101(43):15301-6. Epub 2004 Oct 15. PMID:15489263 doi:http://dx.doi.org/10.1073/pnas.0406819101
  20. ↑ Rempola B, Karkusiewicz I, Piekarska I, Rytka J. Fcf1p and Fcf2p are novel nucleolar Saccharomyces cerevisiae proteins involved in pre-rRNA processing. Biochem Biophys Res Commun. 2006 Jul 28;346(2):546-54. Epub 2006 Jun 2. PMID:16762320 doi:http://dx.doi.org/S0006-291X(06)01217-4
  21. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  22. ↑ Schafer T, Strauss D, Petfalski E, Tollervey D, Hurt E. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 2003 Mar 17;22(6):1370-80. PMID:12628929 doi:http://dx.doi.org/10.1093/emboj/cdg121
  23. ↑ Leger-Silvestre I, Caffrey JM, Dawaliby R, Alvarez-Arias DA, Gas N, Bertolone SJ, Gleizes PE, Ellis SR. Specific Role for Yeast Homologs of the Diamond Blackfan Anemia-associated Rps19 Protein in Ribosome Synthesis. J Biol Chem. 2005 Nov 18;280(46):38177-85. Epub 2005 Sep 12. PMID:16159874 doi:http://dx.doi.org/10.1074/jbc.M506916200
  24. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  25. ↑ Liu PC, Thiele DJ. Novel stress-responsive genes EMG1 and NOP14 encode conserved, interacting proteins required for 40S ribosome biogenesis. Mol Biol Cell. 2001 Nov;12(11):3644-57. PMID:11694595
  26. ↑ Eschrich D, Buchhaupt M, Kotter P, Entian KD. Nep1p (Emg1p), a novel protein conserved in eukaryotes and archaea, is involved in ribosome biogenesis. Curr Genet. 2002 Feb;40(5):326-38. Epub 2002 Feb 6. PMID:11935223 doi:http://dx.doi.org/10.1007/s00294-001-0269-4
  27. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  28. ↑ Meyer B, Wurm JP, Kotter P, Leisegang MS, Schilling V, Buchhaupt M, Held M, Bahr U, Karas M, Heckel A, Bohnsack MT, Wohnert J, Entian KD. 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. 2011 Mar;39(4):1526-37. doi: 10.1093/nar/gkq931. Epub 2010 Oct, 23. PMID:20972225 doi:http://dx.doi.org/10.1093/nar/gkq931
  29. ↑ Thomas SR, Keller CA, Szyk A, Cannon JR, Laronde-Leblanc NA. Structural insight into the functional mechanism of Nep1/Emg1 N1-specific pseudouridine methyltransferase in ribosome biogenesis. Nucleic Acids Res. 2010 Nov 17. PMID:21087996 doi:10.1093/nar/gkq1131
  30. ↑ Watkins NJ, Segault V, Charpentier B, Nottrott S, Fabrizio P, Bachi A, Wilm M, Rosbash M, Branlant C, Luhrmann R. A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell. 2000 Oct 27;103(3):457-66. PMID:11081632
  31. ↑ Galardi S, Fatica A, Bachi A, Scaloni A, Presutti C, Bozzoni I. Purified box C/D snoRNPs are able to reproduce site-specific 2'-O-methylation of target RNA in vitro. Mol Cell Biol. 2002 Oct;22(19):6663-8. PMID:12215523
  32. ↑ Dobbyn HC, O'Keefe RT. Analysis of Snu13p mutations reveals differential interactions with the U4 snRNA and U3 snoRNA. RNA. 2004 Feb;10(2):308-20. PMID:14730029
  33. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  34. ↑ Gautier T, Berges T, Tollervey D, Hurt E. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol Cell Biol. 1997 Dec;17(12):7088-98. PMID:9372940
  35. ↑ Wade CH, Umbarger MA, McAlear MA. The budding yeast rRNA and ribosome biosynthesis (RRB) regulon contains over 200 genes. Yeast. 2006 Mar;23(4):293-306. PMID:16544271 doi:http://dx.doi.org/10.1002/yea.1353
  36. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  37. ↑ Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature. 2002 Jun 27;417(6892):967-70. Epub 2002 Jun 9. PMID:12068309 doi:http://dx.doi.org/10.1038/nature00769
  38. ↑ Gallagher JE, Dunbar DA, Granneman S, Mitchell BM, Osheim Y, Beyer AL, Baserga SJ. RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev. 2004 Oct 15;18(20):2506-17. PMID:15489292 doi:http://dx.doi.org/18/20/2506
  39. ↑ Wade CH, Umbarger MA, McAlear MA. The budding yeast rRNA and ribosome biosynthesis (RRB) regulon contains over 200 genes. Yeast. 2006 Mar;23(4):293-306. PMID:16544271 doi:http://dx.doi.org/10.1002/yea.1353
  40. ↑ Dez C, Dlakic M, Tollervey D. Roles of the HEAT repeat proteins Utp10 and Utp20 in 40S ribosome maturation. RNA. 2007 Sep;13(9):1516-27. Epub 2007 Jul 24. PMID:17652137 doi:http://dx.doi.org/rna.609807
  41. ↑ Wegierski T, Billy E, Nasr F, Filipowicz W. Bms1p, a G-domain-containing protein, associates with Rcl1p and is required for 18S rRNA biogenesis in yeast. RNA. 2001 Sep;7(9):1254-67. PMID:11565748
  42. ↑ Gelperin D, Horton L, Beckman J, Hensold J, Lemmon SK. Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA. 2001 Sep;7(9):1268-83. PMID:11565749
  43. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  44. ↑ Gautier T, Berges T, Tollervey D, Hurt E. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol Cell Biol. 1997 Dec;17(12):7088-98. PMID:9372940
  45. ↑ Wu P, Brockenbrough JS, Metcalfe AC, Chen S, Aris JP. Nop5p is a small nucleolar ribonucleoprotein component required for pre-18 S rRNA processing in yeast. J Biol Chem. 1998 Jun 26;273(26):16453-63. PMID:9632712
  46. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  47. ↑ Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell. 2004 Dec;3(6):1619-26. PMID:15590835 doi:http://dx.doi.org/10.1128/EC.3.6.1619-1626.2004
  48. ↑ Venema J, Vos HR, Faber AW, van Venrooij WJ, Raue HA. Yeast Rrp9p is an evolutionarily conserved U3 snoRNP protein essential for early pre-rRNA processing cleavages and requires box C for its association. RNA. 2000 Nov;6(11):1660-71. PMID:11105764
  49. ↑ Sun Q, Zhu X, Qi J, An W, Lan P, Tan D, Chen R, Wang B, Zheng S, Zhang C, Chen X, Zhang W, Chen J, Dong MQ, Ye K. Molecular architecture of the 90S small subunit pre-ribosome. Elife. 2017 Feb 28;6. pii: e22086. doi: 10.7554/eLife.22086. PMID:28244370 doi:http://dx.doi.org/10.7554/eLife.22086

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