A local role for the small ribosomal subunit primary binder rpS5 in final 18S rRNA processing in yeast

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Neueder, Andreas ^a   Jakob, Steffen ^a   Pöll, Gisela ^a   Linnemann, Jan ^a   Deutzmann, Rainer ^a   Tschochner, Herbert ^a   Milkereit, Philipp ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; NOB1P PROTEIN; RIBOSOME PROTEIN; RNA; RNA 18S; RNA 40S; SMALL RIBOSOMAL SUBUNIT PROTEIN S14; SMALL RIBOSOMAL SUBUNIT PROTEIN S5; UNCLASSIFIED DRUG; RIBOSOMAL PROTEIN S5; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; CHEMICAL STRUCTURE; CHEMISTRY; GENE DELETION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SMALL RIBOSOMAL SUBUNIT;

EUKARYOTA;

MODELS, MOLECULAR; PROTEIN TRANSPORT; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL; RNA, RIBOSOMAL, 18S; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION;

EID: 77956336157     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010194     Document Type: Article

References (53)

1. Wimberly BT, Brodersen DE, Clemons WM, Morgan-Warren RJ, Carter AP, et al. (2000) Structure of the 30S ribosomal subunit. Nature 407: 327-339. doi:10.1038/35030006.
2. Spahn CMT, Gomez-Lorenzo MG, Grassucci RA, Jørgensen R, Andersen GR, et al. (2004) Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J 23: 1008-1019. doi:10.1038/sj.emboj.7600102.
3. Chandramouli P, Topf M, Ménétret J, Eswar N, Cannone JJ, et al. (2008) Structure of the mammalian 80S ribosome at 8.7 A resolution. Structure 16: 535-548. doi:10.1016/j.str.2008.01.007.
4. Sykes MT, Williamson JR (2009) A complex assembly landscape for the 30S ribosomal subunit. Annu Rev Biophys 38: 197-215. doi:10.1146/annurev. biophys.050708.133615.
5. Weitzmann CJ, Cunningham PR, Nurse K, Ofengand J (1993) Chemical evidence for domain assembly of the Escherichia coli 30S ribosome. FASEB J 7: 177-180.
6. Agalarov SC, Zheleznyakova EN, Selivanova OM, Zheleznaya LA, Matvienko NI, et al. (1998) In vitro assembly of a ribonucleoprotein particle corresponding to the platform domain of the 30S ribosomal subunit. Proc Natl Acad Sci USA 95: 999-1003.
7. Samaha RR, O'Brien B, O'Brien TW, Noller HF (1994) Independent in vitro assembly of a ribonucleoprotein particle containing the 39 domain of 16S rRNA. Proc Natl Acad Sci USA 91: 7884-7888.
8. Agalarov SC, Selivanova OM, Zheleznyakova EN, Zheleznaya LA, Matvienko NI, et al. (1999) Independent in vitro assembly of all three major morphological parts of the 30S ribosomal subunit of Thermus thermophilus. Eur J Biochem 266: 533-537.
9. Henras AK, Soudet J, Gérus M, Lebaron S, Caizergues-Ferrer M, et al. (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65: 2334-2359. doi:10.1007/s00018-008-8027-0.
10. Fang F, Hoskins J, Butler JS (2004) 5-fluorouracil enhances exosome-dependent accumulation of polyadenylated rRNAs. Mol Cell Biol 24: 10766-10776. doi:10.1128/MCB.24.24.10766-10776.2004.
11. Kuai L, Fang F, Butler JS, Sherman F (2004) Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 101: 8581-8586. doi:10.1073/pnas.0402888101.
12. Houseley J, Tollervey D (2008) The nuclear RNA surveillance machinery: The link between ncRNAs and genome structure in budding yeast? Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1779: 239-246. doi:10.1016/j.bbagrm.2007.12.008.
13. Cole SE, LaRiviere FJ, Merrikh CN, Moore MJ (2009) A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol Cell 34: 440-450. doi:10.1016/j.molcel.2009.04.017.
14. Ferreira-Cerca S, Pöll G, Gleizes P, Tschochner H, Milkereit P (2005) Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol Cell 20: 263-275. doi:10.1016/j.molcel.2005.09.005.
15. Pöll G, Braun T, Jakovljevic J, Neueder A, Jakob S, et al. (2009) rRNA maturation in yeast cells depleted of large ribosomal subunit proteins. PLoS ONE 4: e8249. doi:10.1371/journal.pone.0008249.
16. Liang X, Liu Q, Fournier MJ (2007) rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol Cell 28: 965-977. doi:10.1016/j.molcel.2007.10.012.
17. Liang X, Liu Q, Fournier MJ (2009) Loss of rRNA modifications in the decoding center of the ribosome impairs translation and strongly delays pre-rRNA processing. RNA 15: 1716-1728. doi:10.1261/rna.1724409.
18. Ferreira-Cerca S, Pöll G, Kühn H, Neueder A, Jakob S, et al. (2007) Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol Cell 28: 446-457. doi:10.1016/j.molcel.2007.09.029.
19. Tabb-Massey A, Caffrey JM, Logsden P, Taylor S, Trent JO, et al. (2003) Ribosomal proteins Rps0 and Rps21 of Saccharomyces cerevisiae have overlapping functions in the maturation of the 39 end of 18S rRNA. Nucleic Acids Res 31: 6798-6805.
20. Léger-Silvestre I, Milkereit P, Ferreira-Cerca S, Saveanu C, Rousselle J, et al. (2004) The ribosomal protein Rps15p is required for nuclear exit of the 40S subunit precursors in yeast. EMBO J 23: 2336-2347. doi:10.1038/sj. emboj.7600252.
21. Ford CL, Randal-Whitis L, Ellis SR (1999) Yeast proteins related to the p40/ laminin receptor precursor are required for 20S ribosomal RNA processing and the maturation of 40S ribosomal subunits. Cancer Res 59: 704-710.
22. Fatica A, Oeffinger M, Dlakic M, Tollervey D (2003) Nob1p Is Required for Cleavage of the 39 End of 18S rRNA. Mol Cell Biol 23: 1798-1807. doi:10.1128/MCB.23.5.1798-1807.2003.
23. Pertschy B, Schneider C, Gnadig M, Schafer T, Tollervey D, et al. (2009) RNA helicase Prp43 and its co-factor Pfa1 promote 20S to 18S rRNA processing catalyzed by the endonuclease Nob1. Journal of Biological Chemistry. Available: http://www.jbc.org/content/early/2009/09/29/jbc.M109.040774.abstract. Accessed 8 Oct 2009.
24. Lamanna AC, Karbstein K (2009) Nob1 binds the single-stranded cleavage site D at the 39-end of 18S rRNA with its PIN domain. Proc Natl Acad Sci USA 106: 14259-14264. doi:10.1073/pnas.0905403106.
25. Gelperin D, Horton L, Beckman J, Hensold J, Lemmon SK (2001) Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA 7: 1268-1283.
26. Vanrobays E, Gelugne J, Gleizes P, Caizergues-Ferrer M (2003) Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol Cell Biol 23: 2083-2095.
27. Udem SA, Warner JR (1973) The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast. J Biol Chem 248: 1412-1416.
28. Trapman J, Planta RJ (1976) Maturation of ribosomes in yeast. I Kinetic analysis by labelling of high molecular weight rRNA species. Biochim Biophys Acta 442: 265-274.
29. Jakovljevic J, de Mayolo PA, Miles TD, Nguyen TM, Léger-Silvestre I, et al. (2004) The carboxy-terminal extension of yeast ribosomal protein S14 is necessary for maturation of 43S preribosomes. Mol Cell 14: 331-342.
30. Lacombe T, Garci{dotless}́a-Gómez JJ, de la Cruz J, Roser D, Hurt E, et al. (2009) Linear ubiquitin fusion to Rps31 and its subsequent cleavage are required for the efficient production and functional integrity of 40S ribosomal subunits. Mol Microbiol 72: 69-84. doi:10.1111/j.1365-2958.2009.06622.x.
31. Robert F, Brakier-Gingras L (2001) Ribosomal protein S7 from Escherichia coli uses the same determinants to bind 16S ribosomal RNA and its messenger RNA. Nucleic Acids Res 29: 677-682.
32. Schäfer T, Maco B, Petfalski E, Tollervey D, Böttcher B, et al. (2006) Hrr25- dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441: 651-655. doi:10.1038/nature04840.
33. Brodersen DE, Clemons WM, Carter AP, Wimberly BT, Ramakrishnan V (2002) Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16 S RNA. J Mol Biol 316: 725-768. doi:10.1006/jmbi.2001.5359.
34. Vanrobays E, Gélugne J, Caizergues-Ferrer M, Lafontaine DLJ (2004) Dim2p, a KH-domain protein required for small ribosomal subunit synthesis. RNA 10: 645-656.
35. Tone Y, Toh-E A (2002) Nob1p is required for biogenesis of the 26S proteasome and degraded upon its maturation in Saccharomyces cerevisiae. Genes Dev 16: 3142-3157. doi:10.1101/gad.1025602.
36. Granneman S, Nandineni MR, Baserga SJ (2005) The putative NTPase Fap7 mediates cytoplasmic 20S pre-rRNA processing through a direct interaction with Rps14. Mol Cell Biol 25: 10352-10364. doi:10.1128/MCB.25.23. 10352-10364.2005.
37. Lafontaine D, Delcour J, Glasser AL, Desgrès J, Vandenhaute J (1994) The DIM1 gene responsible for the conserved m6(2)Am6(2)A dimethylation in the 39-terminal loop of 18 S rRNA is essential in yeast. J Mol Biol 241: 492-497. doi:10.1006/jmbi.1994.1525.
38. Xu Z, O'Farrell HC, Rife JP, Culver GM (2008) A conserved rRNA methyltransferase regulates ribosome biogenesis. Nat Struct Mol Biol 15: 534-536. doi:10.1038/nsmb.1408.
39. BohnsackMT,Martin R, Granneman S,RuprechtM, Schleiff E, et al. (2009) Prp43 Bound atDifferent Sites on the Pre-rRNA Performs Distinct Functions in Ribosome Synthesis. Molecular Cell 36: 583-592. doi:10.1016/j.molcel.2009.09.039.
40. Sharma MR, Barat C, Wilson DN, Booth TM, Kawazoe M, et al. (2005) Interaction of Era with the 30S Ribosomal Subunit: Implications for 30S Subunit Assembly. Molecular Cell 18: 319-329. doi:10.1016/j.molcel.2005.03.028.
41. Pisarev AV, Kolupaeva VG, Yusupov MM, Hellen CUT, Pestova TV (2008) Ribosomal position and contacts of mRNA in eukaryotic translation initiation complexes. EMBO J 27: 1609-1621. doi:10.1038/emboj.2008.90.
42. Lomakin IB, Kolupaeva VG, Marintchev A, Wagner G, Pestova TV (2003) Position of eukaryotic initiation factor eIF1 on the 40S ribosomal subunit determined by directed hydroxyl radical probing. Genes Dev 17: 2786-2797. doi:10.1101/gad.1141803.
43. Yu Y, Marintchev A, Kolupaeva VG, Unbehaun A, Veryasova T, et al. (2009) Position of eukaryotic translation initiation factor eIF1A on the 40S ribosomal subunit mapped by directed hydroxyl radical probing. Nucleic Acids Res 37: 5167-5182. doi:10.1093/nar/gkp519.
44. Passmore LA, Schmeing TM, Maag D, Applefield DJ, Acker MG, et al. (2007) The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol Cell 26: 41-50. doi:10.1016/ j.molcel.2007.03.018.
45. Devaraj A, Shoji S, Holbrook ED, Fredrick K (2009) A role for the 30S subunit E site in maintenance of the translational reading frame. RNA 15: 255-265. doi:10.1261/rna.1320109.
46. Robert F, Brakier-Gingras L (2003) A functional interaction between ribosomal proteins S7 and S11 within the bacterial ribosome. J Biol Chem 278: 44913-44920. doi:10.1074/jbc.M306534200.
47. Lumsden T, Bentley AA, Beutler W, Ghosh A, Galkin O, et al. (2010) Yeast strains with N-terminally truncated ribosomal protein S5: implications for the evolution, structure and function of the Rps5/Rps7 proteins. Nucleic Acids Res 38: 1261-1272. doi:10.1093/nar/gkp1113.
48. Soudet J, Gélugne J, Belhabich-Baumas K, Caizergues-Ferrer M, Mougin A Immature small ribosomal subunits can engage in translation initiation in Saccharomyces cerevisiae. EMBO J. Available: http://www.ncbi.nlm.nih.gov/pubmed/19893492. Accessed 24 Nov 2009.
49. Sambrook J, Fritsch E, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. 2. ed. Cold Spring Harbor Laboratory Press.
50. Burke D, Dawson D, Stearns T (2000) Methods in Yeast Genetics, 2000 Edition: A Cold Spring Harbor Laboratory Course Manual. 1. ed. Cold Spring Harbor Laboratory Press.
51. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961. doi:10.1002/ (SICI)1097-0061(199807)14:10,953::AID-YEA293.3.0.CO;2-U.
52. Léger-Silvestre I, Milkereit P, Ferreira-Cerca S, Saveanu C, Rousselle J, et al. (2004) The ribosomal protein Rps15p is required for nuclear exit of the 40S subunit precursors in yeast. EMBO J 23: 2336-2347. doi:10.1038/sj.emboj.7600252.
53. Oeffinger M, Wei KE, Rogers R, DeGrasse JA, Chait BT, et al. (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat Methods 4: 951-956. doi:10.1038/nmeth1101.