Mrd1p is required for release of base-paired U3 snoRNA within the preribosomal complex

Molecular and Cellular Biology

Volumn 29, Issue 21, 2009, Pages 5763-5774

  Lundkvist, Pär ^a   Jupiter, Sara ^a   Segerstolpe, Åsa ^a   Osheim, Yvonne N ^b   Beyer, Ann L ^b   Wieslander, Lars ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MULTIDRUG RESISTANCE PROTEIN 1; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SMALL NUCLEOLAR RNA;

ARTICLE; BASE PAIRING; GENE MUTATION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN FUNCTION; SMALL RIBOSOMAL SUBUNIT;

ALLELES; AMINO ACID SEQUENCE; BASE PAIRING; FLUOROURACIL; GENE EXPRESSION REGULATION, FUNGAL; GENES, DOMINANT; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; OROTIC ACID; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS; RIBOSOMES; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL NUCLEOLAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 70350542597     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00428-09     Document Type: Article

References (54)

1. Allain, F. H., D. E. Gilbert, P. Bouvet, and J. Feigon. 2000. Solution structure of the two N-terminal RNA-binding domains of nucleolin and NMR study of the interaction with its RNA target. J. Mol. Biol. 303:227-241.
2. Beltrame, M., Y. Henry, and D. Tollervey. 1994. Mutational analysis of an essential binding site for U3 snoRNA in the 5′ external transcribed spacer of yeast pre-rRNA. Nucleic Acids Res. 22:5139-5147.
3. Beltrame, M., and D. Tollervey. 1995. Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J. 14:4350-4356.
4. Bleichert, F., and S. J. Baserga. 2007. The long unwinding road of RNA helicases. Mol. Cell 27:339-352. (Pubitemid 47126943)
5. Bohnsack, M. T., K. Kos, and D. Tollervey. 2008. Quantitative analysis of snoRNA association with pre-ribosomes and release of snR30 by Rok1 helicase. EMBO Rep. 9:1-7.
6. Burke, D., D. Dawson, and T. Stearns. 2000. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
7. Chu, V. B., and D. Herschlag. 2008. Unwinding RNA's secrets: advances in the biology, physics, and modeling of complex RNAs. Curr. Opin. Struct. Biol. 18:305-314.
8. Colley, A., J. D. Beggs, D. Tollervey, and D. L. J. Lafontaine. 2000. Dhr1p, a putative DEAH-box RNA helicase, is associated with the box C+D snoRNP U3. Mol. Biol. Cell 20:7238-7246.
9. Dammel, C. S., and H. F. Noller. 1993. A cold-sensitive mutation in 16S rRNA provides evidence for helical switching in ribosome assembly. Genes Dev. 7:660-670. (Pubitemid 23125265)
10. De Gaudenzi, J., A. C. Frasch, and C. Clayton. 2005. RNA-binding domain proteins in kinetoplasids: a comparative analysis. Eukaryot. Cell 4:2106-2114. (Pubitemid 41798316)
11. Dennis, P. P., A. G. Russell, and M. Moniz De Sá. 1997. Formation of the 5′ end pseudoknot in small subunit ribosomal RNA: involvement of U3-like sequences. RNA 3:337-343.
12. Dosil, M., and X. R. Bustelo. 2004. Functional characterization of Pwp2p, a WD family protein essential for the assembly of the 90S pre-ribosomal particle. J. Biol. Chem. 279:37385-37397.
13. Fang, F., J. Hoskins, and J. S. Butler. 2004. 5-Fluorouracil enhances exosome-dependent accumulation of polyadenylated rRNAs. Mol. Cell. Biol. 24:10766-10776.
14. Ferreira-Cerca, S., G. Pöll, P. E. Gleizes, H. Tschochner, and P. Milkereit. 2005. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol. Cell 20:263-275. (Pubitemid 41484171)
15. Ferreira-Cerca, S., G. Pöll, H. Kühn, A. Neueder, S. Jakob, H. Tschochner, and P. Milkereit. 2007. Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol. Cell 28:446-457. (Pubitemid 350030572)
16. Fromont-Racine, M., B. Senger, C. Saveanu, and F. Fasiolo. 2003. Ribosome assembly in eukaryotes. Gene 313:17-42.
17. Ginisty, H., F. Amalric, and P. Bouvet. 2001. Two different combinations of RNA-binding domains determine the RNA binding specificity of nucleolin. J. Biol. Chem. 276:14338-14343.
18. Grandi, P., V. Rybin, J. Bassler, E. Petfalski, D. Strauss, M. Marzioch, T. Schafer, B. Kuster, H. Tschochner, D. Tollervey, A. C. Gavin, and E. Hurt. 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 10:105-115. (Pubitemid 34879149)
19. Granneman, S., J. Vogelzangs, R. Lührmann, W. J. van Venrooij, G. J. M. Pruijn, and N. J. Watkins. 2004. Role of pre-rRNA base pairing and 80S complex formation in subnucleolar localization of U3 snoRNP. Mol. Cell. Biol. 24:8600-8610.
20. Granneman, S., C. Lin, E. A. Champion, M. R. Nandineni, C. Zorca, and S. J. Baserga. 2006. The nucleolar protein Esf2 interacts directly with the DexD/H box RNA helicase Dbp8 to stimulate ATP hydrolysis. Nucleic Acids Res. 34:3189-3199. (Pubitemid 44540444)
21. Gutell, R. R., N. Larsen, and C. R. Woese. 1994. Lessons from an evolving ribosomal RNA: 16S and 23S ribosomal RNA structures from a comparative perspecitive. Microbiol. Rev. 58:10-26.
22. Herschlag, D. 1995. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270:20871-20874.
23. Hoang, T., W.-T. Peng, E. Vanrobays, N. Krogan, S. Hiley, A. L. Beyer, Y. N. Osheim, J. Greenblatt, T. R. Hughes, and D. L. J. Lafontaine. 2005. Esf2p, a U3-associated factor required for small-subunit processome assembly and compaction. Mol. Cell. Biol. 25:5523-5534.
24. Hoskins, J., and J. S. Butler. 2008. RNA-based 5-fluorouracil toxicity requires the pseudouridylation activity of Cbf5p. Genetics 179:323-330.
25. Hughes, J. M. 1996. Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA. J. Mol. Biol. 259:645-654.
26. Jin, S.-B., J. Zhao, P. Björk, K. Schmekel, P. O. Ljungdahl, and L. Wieslander. 2002. Mrd1p is required for processing of pre-rRNA and for maintenance of steady-state levels of 40S ribosomal subunits in yeast. J. Biol. Chem. 277:18431-18439.
27. Kielkopf, C. L., S. Lücke, and M. R. Green. 2004. U2AF homology motifs: protein recognition in the RRM world. Genes Dev. 18:1513-1526.
28. Kiss, T. 2002. Small nucleolar RNAs: an abundant group of non-coding RNAs with diverse cellular function. Cell 109:145-148. (Pubitemid 34518252)
29. Kos, M., and D. Tollervey. 2005. The putative RNA helicase Dbp4p is required for release of the U14 snoRNA from preribosomes in Saccharomyces cerevisiae. Mol. Cell 20:53-64.
30. Kressler, D., D. Roser, B. Pertschy, and E. Hurt. 2008. The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles. J. Cell Biol. 181:935-944. (Pubitemid 351846827)
31. Krogan, N. J., W.-T. Peng, G. Cagney, M. D. Robinson, R. Haw, G. Zhong, X. Guo, X. Zhang, V. Canadien, D. P. Richards, B. K. Beattle, A. Lalev, W. Zhang, A. P. Davierwala, S. Mnaimneh, A. Starostine, A. P. Tikuisis, J. Grigull, N. Datta, J. E. Hughes, A. Emili, and J. F. Greenblatt. 2004. High-definition macromolecular composition of yeast RNA-processing complexes. Mol. Cell 13:225-239.
32. Lee, S. J., and S. J. Baserga. 1999. Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing. Mol. Cell. Biol. 19:5441-5452.
33. Liang, X. H., and M. J. Fournier. 2006. The helicase Has1p is required for snoRNA release from pre4-rRNA. Mol. Cell. Biol. 26:7437-7450.
34. Linder, P. 2006. Dead-box proteins: a family affair - active and passive players in RNP-remodelling. Nucleic Acids Res. 34:4168-4180. (Pubitemid 44542196)
35. Longtine, M. S., A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
36. Maris, C., C. Dominique, and F. H.-T. Allain. 2005. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J. 272:2118-2131. (Pubitemid 40655326)
37. Mereau, A., R. Fournier, A. Gregoire, A. Mougin, P. Fabrizio, R. Lührmann, and C. Branlant. 1997. An in vivo and in vitro structure-function analysis of the Saccharomyces cerevisiae U3A snoRNOP: protein-RNA contacts and base-pair interaction with the precursor rRNA. J. Mol. Biol. 273:552-571.
38. Mougey, E. B., M. O'Reilley, Y. N. Osheim, O. L. Miller Jr., A. L. Beyer, and B. Sollner-Webb. 1993. The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. Genes Dev. 7:1609-1619. (Pubitemid 23234353)
39. Nissan, T. A., K. Galani, B. Maco, D. Tollervey, U. Aebi, and E. Hurt. 2004. A pre-ribosome with a tadpole-like structure functions in ATP-dependent maturation of 60S subunits. Mol. Cell 15:295-301.
40. Osheim, Y. N., S. L. French, K. M. Keck, E. A. Champion, K. Spasov, F. Dragon, S. J. Baserga, and A. L. Beyer. 2004. Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol. Cell 16:943-954.
41. Peng, W.-T., N. J. Krogan, D. P. Richards, J. F. Greenblatt, and T. R. Hughes. 2004. ESF1 is required for 18S rRNA synthesis in Saccharomyces cerevisiae. Nuclic Acids Res. 32:1993-1999.
42. Pérez-Canadillas, J.-M., and G. Varani. 2001. Recent advances in RNA-protein recognition. Curr. Opin. Struct. Biol. 11:53-58.
43. Pérez-Fernández, J., A. Román, J. De Las Rivas, X. R. Bustelo, and M. Dosil. 2007. The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol. 27:5414-5429.
44. Rajkowitsch, L., D. Chen, S. Stampfl, K. Semrad, C. Waldsich, O. Mayer, M. F. Jantsch, R. Konrat, U. Bläsi, and R. Schröder. 2007. RNA chaperones, RNA annealers and RNA helicases. RNA Biol. 4:118-130.
45. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
46. Schäfer, T., B. Maco, E. Petfalski, D. Tollervey, B. Böttcher, U. Aebi, and E. Hurt. 2006. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441:651-655. (Pubitemid 43927298)
47. Segerstolpe, Å., P. Lundkvist, Y. N. Osheim, A. L. Beyer, and L. Wieslander. 2008. Mrd1p binds to pre-rRNA early during transcription independent of U3 snoRNA and is required for compaction of the pre-rRNA into small subunit processomes. Nucleic Acids Res. 36:4364-4380.
48. Shamoo, Y., N. Abdul-Manan, and K. R. Williams. 1995. Multiple RNA binding domains (RBDs) just don't add up. Nucleic Acids Res. 23:725-728.
49. Sharma, K., and D. Tollervey. 1999. Base pairing between U3 small nucleolar RNA and the 5′ end of 18S rRNA is required for pre-rRNA processing. Mol. Cell. Biol. 19:6012-6019.
50. Storici, F., L. K. Lewis, and M. A. Resnick. 2001. In vivo site-directed mutagenesis using oligonucleotides. Nat. Biotechnol. 8:773-776.
51. Toyn, J. H., P. L. Gunyuzlu, W. Hunter White, L. A. Thompson, and G. F. Hollis. 2000. A counterselection for the tryptophan pathway in yeast: 5-fluoroanthranilic acid resistance. Yeast 16:553-560.
52. Venema, J., and D. Tollervey. 1999. Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33:261-311.
53. 70-like motif: a eukaryotic RNA binding domain unique to a superfamily of proteins required for ribosome biogenesis. Mol. Cell 9:329-339.
54. Young, R. A., and J. A. Steitz. 1978. Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc. Natl. Acad. Sci. USA 75:3593-3597.