The evolutionarily conserved protein las1 is required for pre-rRNA processing at both ends of ITS2

Molecular and Cellular Biology

Volumn 32, Issue 2, 2012, Pages 430-444

  Schillewaert, Stéphanie ^a   Wacheul, Ludivine ^a   Lhomme, Frédéric ^b   Lafontaine, Denis L J ^a,b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b Academie Wallonie Bruxelles   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN LAS1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DIVISION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PURIFICATION; RNA PROCESSING; YEAST;

ALLELES; BASE SEQUENCE; CELL CYCLE; DNA, RIBOSOMAL SPACER; EXORIBONUCLEASES; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; RIBOSOME SUBUNITS, LARGE; RNA PRECURSORS; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES;

EID: 84856807167     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06019-11     Document Type: Article

References (51)

1. Ansel KM, et al. 2008. Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Nat. Struct. Mol. Biol. 15:523-530.
2. Bassler J, et al. 2010. The AAA-ATPase Rea1 drives removal of biogenesis factors during multiple stages of 60S ribosome assembly. Mol. Cell 38: 712-721.
3. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. 2007. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 8:574-585.
4. Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. 2010. The nucleolus under stress. Mol. Cell 40:216-227.
5. Breslow DK, et al. 2008. A comprehensive strategy enabling highresolution functional analysis of the yeast genome. Nat. Methods 5:711-718.
6. Briggs MW, Burkard KT, Butler JS. 1998. Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3' end formation. J. Biol. Chem. 273:13255-13263.
7. Castle CD, Cassimere EK, Lee J, Denicourt C. 2010. Las1L is a nucleolar protein required for cell proliferation and ribosome biogenesis. Mol. Cell. Biol. 30:4404-4414.
8. Colau G, Thiry M, Leduc V, Bordonné R, Lafontaine DLJ. 2004. The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol. Cell. Biol. 24: 7976-7986.
9. Cote CA, Greer CL, Peculis BA. 2002. Dynamic conformational model for the role of ITS2 in pre-rRNA processing in yeast. RNA 8:786-797.
10. Coute Y, et al. 2008. ISG20L2, a novel vertebrate nucleolar exoribonuclease involved in ribosome biogenesis. Mol. Cell Proteomics 7:546-559.
11. de la Cruz J, Kressler D, Tollervey D, Linder P. 1998. Dob1p (Mtr4p) is a putative ATP-dependentRNAhelicase required for the 3' end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J. 17:1128-1140.
12. Deutscher MP. 2009. Maturation and degradation of ribosomal RNA in bacteria. Prog. Mol. Biol. Transl. Sci. 85:369-391.
13. Dez C, Tollervey D. 2004. Ribosome synthesis meets the cell cycle. Curr. Opin. Microbiol. 7:631-637.
14. Doseff AI, Arndt KT. 1995. LAS1 is an essential nuclear protein involved in cell morphogenesis and cell surface growth. Genetics 141:857-871.
15. El Hage A, Koper M, Kufel J, Tollervey D. 2008. Efficient termination of transcription by RNA polymerase I requires the 5' exonuclease Rat1 in yeast. Genes Dev. 22:1069-1081.
16. Faber AW, Van Dijk M, Raue HA, Vos JC. 2002. Ngl2p is a Ccr4p-like RNAnuclease essential for the final step in 3'-end processing of 5.8S rRNA in Saccharomyces cerevisiae. RNA 8:1095-1101.
17. Fang F, Phillips S, Butler JS. 2005. Rat1p and Rai1p function with the nuclear exosome in the processing and degradation of rRNA precursors. RNA 11:1571-1578.
18. Fatica A, Tollervey D. 2002. Making ribosomes. Curr. Opin. Cell Biol. 14:313-318.
19. Finkbeiner E, Haindl M, Muller S. 2011. The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J. 30:1067-1078.
20. Geerlings TH, Vos JC, Raue HA. 2000. The final step in the formation of 25S rRNA in Saccharomyces cerevisiae is performed by 5'→3' exonucleases. RNA 6:1698-1703.
21. Gérus M, Caizergues-Ferrer M, Henry Y, Henras AK. 2011. Crosstalk between ribosome synthesis and cell cycle and its potential implications in human diseases, p. 157-184. In Olson MO (ed.), Protein reviews, vol. 15. The nucleolus. Springer, New York, NY.
22. Henras AK, et al. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65:2334-2359.
23. Henry Y, et al. 1994. The 5' end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site. EMBO J. 13:2452-2463.
24. Hernandez-Verdun D, Roussel P, Thiry M, Sirri V, Lafontaine DLJ. 2010. The nucleolus: structure/function in RNA metabolism. RNA 1:415-431.
25. Houseley J, LaCava J, Tollervey D. 2006. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 7:529-539.
26. Johnson AW. 1997. Rat1p and Xrn1p are functionally interchangeable exoribonucleases that are restricted to and required in the nucleus and cytoplasm, respectively. Mol. Cell. Biol. 17:6122-6130.
27. Jorgensen P, Tyers M, Warner JR. 2004. Forging the factory: ribosome synthesis and growth control in budding yeast, p 329-370. In Hall M, Raff M, Thomas G (ed), Cell growth: control of cell size. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Kitano E, Hayashi A, Kanai D, Shinmyozu K, Nakayama JI. 2011.Roles of fission yeast Grc3 in ribosomal RNA processing and heterochromatic gene silencing. J. Biol. Chem.
29. Kos M, Tollervey D. 2010. Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell 37:809-820.
30. Kressler D, Hurt E, Bassler J. 2010. Driving ribosome assembly. Biochim. Biophys. Acta 1803:673-683.
31. Lafontaine DLJ. 2010. A 'garbage can' for ribosomes: how eukaryotes degrade their ribosomes? Trends Biochem. Sci. 35:267-277.
32. Lafontaine DLJ, Tollervey D. 2001. The function and synthesis of ribosomes. Nat. Rev. Mol. Cell Biol. 2:514-520.
33. Lebreton A, Tomecki R, Dziembowski A, Seraphin B. 2008. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456:993-996.
34. O'Donohue MF, Choesmel V, Faubladier M, Fichant G, Gleizes PE. 2010. Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J. Cell Biol. 190:853-866.
35. Oeffinger M, et al. 2007. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 4:951-956.
36. Oeffinger M, et al. 2009. Rrp17p is a eukaryotic exonuclease required for 5' end processing of pre-60S ribosomal RNA. Mol. Cell 36:768 -781.
37. Osheim YN, et al. 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.
38. Peng WT, et al. 2003. A panoramic view of yeast noncoding RNA processing. Cell 113:919-933.
39. Schaeffer D, et al. 2009. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat. Struct. Mol. Biol. 16:56-62.
40. Schilders G, van Dijk E, Pruijn GJ. 2007. C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res. 35:2564-2572.
41. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101-1108.
42. Schneider C, Leung E, Brown J, Tollervey D. 2009. The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res. 37:1127-1140.
43. Strunk BS, Karbstein K. 2009. Powering through ribosome assembly. RNA 15:2083-2104.
44. Sydorskyy Y, et al. 2003. Intersection of the Kap123p-mediated nuclear import and ribosome export pathways. Mol. Cell. Biol. 23:2042-2054.
45. Thomson E, Tollervey D. 2010. The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol. Cell. Biol. 30:976-984.
46. Ulbrich C, et al. 2009. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 138:911-922.
47. van Hoof A, Lennertz P, Parker R. 2000. Three conserved members of the RNaseDfamily have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. EMBO J. 19:1357-1365.
48. Wery M, Ruidant S, Schillewaert S, Lepore N, Lafontaine DL. 2009. The nuclear poly(A) polymerase and exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 15:406-419.
49. Xue Y, et al. 2000. Saccharomyces cerevisiae RAI1 (YGL246c) is homologous to human DOM3Z and encodes a protein that binds the nuclear exoribonuclease Rat1p. Mol. Cell. Biol. 20:4006-4015.
50. Yeh LC, Lee JC. 1990. Structural analysis of the internal transcribed spacer 2 of the precursor ribosomal RNA from Saccharomyces cerevisiae. J. Mol. Biol. 211:699-712.
51. Zhang J, Jr, et al. 2007. Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 21:2580-2592.