The PIN domain endonuclease Utp24 cleaves pre-ribosomal RNA at two coupled sites in yeast and humans

Nucleic Acids Research

Volumn 44, Issue 11, 2016, Pages 5399-5409

  Wells, Graeme R ^a   Weichmann, Franziska ^a,d   Colvin, David ^a   Sloan, Katherine E ^a,e   Kudla, Grzegorz ^b,c   Tollervey, David ^b   Watkins, Nicholas J ^a   Schneider, Claudia ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; PRERIBOSOME RNA; RCL1 PROTEIN; RIBOSOME RNA; RNA 18S; SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG; UTP24 PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BASE PAIRING; CONTROLLED STUDY; CROSS LINKING; EMBRYO; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; IN VIVO STUDY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN RNA BINDING; RNA CLEAVAGE; RNA STRUCTURE; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE;

EID: 84976428149     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw213     Document Type: Article

References (37)

1. Henras A.K, Plisson-Chastang C, ODonohue M.F, Chakraborty A, and Gleizes P.E. (2015). An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip. Rev. RNA, 6, 225-242.
2. Phipps K.R, Charette J, and Baserga S.J. (2011). The small subunit processome in ribosome biogenesis-progress and prospects. Wiley Interdiscip. Rev. RNA, 2, 1-21.
3. Watkins N.J, and Bohnsack M.T. (2012). The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip. Rev. RNA, 3, 397-414.
4. Bleichert F, Granneman S, Osheim Y.N, Beyer A.L, and Baserga S.J. (2006). The PINc domain protein Utp24, a putative nuclease, is required for the early cleavage steps in 18S rRNA maturation. Proc. Natl. Acad. Sci. U.S.A, 103, 9464-9469.
5. Billy E, Wegierski T, Nasr F, and Filipowicz W. (2000). Rcl1p, the yeast protein similar to the RNA 3-phosphate cyclase, associates with U3 snoRNP and is required for 18S rRNA biogenesis. EMBO J, 19, 2115-2126.
6. Fatica A, Oeffinger M, Dlakic M, and Tollervey D. (2003). Nob1p is required for cleavage of the 3 end of 18S rRNA. Mol. Cell. Biol, 23, 1798-1807.
7. Pertschy B, Schneider C, Gnadig M, Schafer T, Tollervey D, and Hurt E. (2009). RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem, 284, 35079-35091.
8. Lebaron S, Schneider C, van Nues R.W, Swiatkowska A, Walsh D, Bottcher B, Granneman S, Watkins N.J, and Tollervey D. (2012). Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol, 19, 744-753.
9. Horn D.M, Mason S.L, and Karbstein K. (2011). Rcl1 protein, a novel nuclease for 18 S ribosomal RNA production. J. Biol. Chem, 286, 34082-34087.
10. Delprato A, Al Kadri Y, Perebaskine N, Monfoulet C, Henry Y, Henras A.K, and Fribourg S. (2014). Crucial role of the Rcl1p-Bms1p interaction for yeast pre-ribosomal RNA processing. Nucleic Acids Res, 42, 10161-10172.
11. Sloan K.E, Mattijssen S, Lebaron S, Tollervey D, Pruijn G.J, and Watkins N.J. (2013). Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J. Cell Biol, 200, 577-588.
12. Tafforeau L, Zorbas C, Langhendries J.L, Mullineux S.T, Stamatopoulou V, Mullier R, Wacheul L, and Lafontaine D.L. (2013). The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol. Cell, 51, 539-551.
13. Sloan K.E, Bohnsack M.T, Schneider C, and Watkins N.J. (2014). The roles of SSU processome components and surveillance factors in the initial processing of human ribosomal RNA. RNA, 20, 540-550.
14. Wang M, Anikin L, and Pestov D.G. (2014). Two orthogonal cleavages separate subunit RNAs in mouse ribosome biogenesis. Nucleic Acids Res, 42, 11180-11191.
15. Tomecki R, Labno A, Drazkowska K, Cysewski D, and Dziembowski A. (2015). hUTP24 is essential for processing of the human rRNA precursor at site A1, but not at site A0. RNA Biol, 12, 1010-1029.
16. Sharma K, and Tollervey D. (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.
17. Kos M, and Tollervey D. (2010). Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell, 37, 809-820.
18. Lazdins I.B, Delannoy M, and Sollner-Webb B. (1997). Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridization. Chromosoma, 105, 481-495.
19. Preti M, ODonohue M.F, Montel-Lehry N, Bortolin-Cavaille M.L, Choesmel V, and Gleizes P.E. (2013). Gradual processing of the ITS1 from the nucleolus to the cytoplasm during synthesis of the human 18S rRNA. Nucleic Acids Res, 41, 4709-4723.
20. Gietz D, St Jean A, Woods R.A, and Schiestl R.H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res, 20, 1425.
21. Granneman S, Kudla G, Petfalski E, and Tollervey D. (2009). Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-Throughput analysis of cDNAs. Proc. Natl. Acad. Sci. U.S.A, 106, 9613-9618.
22. Granneman S, Petfalski E, and Tollervey D. (2011). A cluster of ribosome synthesis factors regulate pre-rRNA folding and 5.8S rRNA maturation by the Rat1 exonuclease. EMBO J, 30, 4006-4019.
23. Wlotzka W, Kudla G, Granneman S, and Tollervey D. (2011). The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J, 30, 1790-1803.
24. Schneider C, Anderson J.T, and Tollervey D. (2007). The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol. Cell, 27, 324-331.
25. Schneider C, Leung E, Brown J, and 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.
26. Schneider C, Kudla G, Wlotzka W, Tuck A, and Tollervey D. (2012). Transcriptome-wide analysis of exosome targets. Mol. Cell, 48, 422-433.
27. Fayet-Lebaron E, Atzorn V, Henry Y, and Kiss T. (2009). 18S rRNA processing requires base pairings of snR30 H/ACA snoRNA to eukaryote-specific 18S sequences. EMBO J, 28, 1260-1270.
28. Venema J, Henry Y, and Tollervey D. (1995). Two distinct recognition signals define the site of endonucleolytic cleavage at the 5-end of yeast 18S rRNA. EMBO J, 14, 4883-4892.
29. Rempola B, Karkusiewicz I, Piekarska I, and Rytka J. (2006). Fcf1p and Fcf2p are novel nucleolar Saccharomyces cerevisiae proteins involved in pre-rRNA processing. Biochem. Biophys. Res. Commun, 346, 546-554.
30. Skruzny M, Schneider C, Racz A, Weng J, Tollervey D, and Hurt E. (2009). An endoribonuclease functionally linked to perinuclear mRNP quality control associates with the nuclear pore complexes. PLoS Biol, 7, e8.
31. Allmang C, Henry Y, Wood H, Morrissey J.P, Petfalski E, and Tollervey D. (1996). Recognition of cleavage site A(2) in the yeast pre-rRNA. RNA, 2, 51-62.
32. Elbashir S.M, Harborth J, Weber K, and Tuschl T. (2002). Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods, 26, 199-213.
33. Wang M, and Pestov D.G. (2011). 5-end surveillance by Xrn2 acts as a shared mechanism for mammalian pre-rRNA maturation and decay. Nucleic Acids Res, 39, 1811-1822.
34. Karbstein K, Jonas S, and Doudna J.A. (2005). An essential GTPase promotes assembly of preribosomal RNA processing complexes. Mol. Cell, 20, 633-643.
35. Sardana R, Liu X, Granneman S, Zhu J, Gill M, Papoulas O, Marcotte E.M, Tollervey D, Correll C.C, and Johnson A.W. (2015). The DEAH-box helicase Dhr1 dissociates U3 from the pre-rRNA to promote formation of the central pseudoknot. PLoS Biol, 13, e1002083.
36. Turner A.J, Knox A.A, Prieto J.L, McStay B, and Watkins N.J. (2009). A novel small-subunit processome assembly intermediate that contains the U3 snoRNP, nucleolin, RRP5, and DBP4. Mol. Cell. Biol, 29, 3007-3017.
37. Turner A.J, Knox A.A, and Watkins N.J. (2012). Nucleolar disruption leads to the spatial separation of key 18S rRNA processing factors. RNA Biol, 9, 175-186.