Gradual processing of the ITS1 from the nucleolus to the cytoplasm during synthesis of the human 18S rRNA

Nucleic Acids Research

Volumn 41, Issue 8, 2013, Pages 4709-4723

  Preti, Milena ^a,b   O'Donohue, Marie Françoise ^a,b   Montel Lehry, Nathalie ^a,b   Bortolin Cavaillé, Marie Line ^a,b   Choesmel, Valérie ^a,b   Gleizes, Pierre Emmanuel ^a,b  

^a Université Paul Sabatier   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

18S E PRECURSOR; EXONUCLEASE; INTERNAL TRANSCRIBED SPACER 1; PROTEIN RPL26; PROTEIN XRN2; RIBOSOME PROTEIN; RNA 18S; RNA PRECURSOR; UNCLASSIFIED DRUG;

ARTICLE; BLACKFAN DIAMOND ANEMIA; CELL DIVISION; CONTROLLED STUDY; CYTOPLASM; DNA DEGRADATION; DNA DETERMINATION; DNA MODIFICATION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MOLECULAR MECHANICS; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA PROCESSING; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; YEAST;

BASE SEQUENCE; CELL NUCLEOLUS; CONSERVED SEQUENCE; CYTOPLASM; EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; HELA CELLS; HUMANS; RIBOSOMAL PROTEINS; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL, 18S;

EID: 84877269808     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt160     Document Type: Article

References (52)

1. Fumagalli, S. and Thomas, G. (2011) The role of p53 in ribosomopathies. Semin. Hematol., 48, 97-105.
2. Donati, G., Montanaro, L. and Derenzini, M. (2012) Ribosome biogenesis and control of cell proliferation: p53 is not alone. Cancer Res., 72, 1602-1607.
3. Chakraborty, A., Uechi, T. and Kenmochi, N. (2011) Guarding the 'translation apparatus': defective ribosome biogenesis and the p53 signaling pathway. WIRE RNA, 2, 507-522.
4. Ellis, S.R. and Gleizes, P.-E. (2011) Diamond Blackfan anemia: ribosomal proteins going rogue. Semin. Hematol., 48, 89-96.
5. Boria, I., Garelli, E., Gazda, H.T., Aspesi, A., Quarello, P., Pavesi, E., Ferrante, D., Meerpohl, J.J., Kartal, M., Da Costa, L. et al. (2010) The ribosomal basis of Diamond-Blackfan Anemia: mutation and database update. Hum. Mutat., 31, 1269-1279.
6. Dutt, S., Narla, A., Lin, K., Mullally, A., Abayasekara, N., Megerdichian, C., Wilson, F.H., Currie, T., Khanna-Gupta, A., Berliner, N. et al. (2011) Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood, 117, 2567-2576.
7. Narla, A. and Ebert, B.L. (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood, 115, 3196-3205.
8. Burwick, N., Shimamura, A. and Liu, J.M. (2011) Non-Diamond Blackfan anemia disorders of ribosome function: Shwachman Diamond syndrome and 5q-syndrome. Semin. Hematol., 48, 136-143.
9. Fatica, A. and Tollervey, D. (2002) Making ribosomes. Curr. Opin. Cell Biol., 14, 313-318.
10. Fromont-Racine, M., Senger, B., Saveanu, C. and Fasiolo, F. (2003) Ribosome assembly in eukaryotes. Gene, 313, 17-42.
11. Henras, A.K., Soudet, J., Gérus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A. and Henry, Y. (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci., 65, 2334-2359.
12. Granneman, S. and Baserga, S.J. (2004) Ribosome biogenesis: of knobs and RNA processing. Exp. Cell Res., 296, 43-50.
13. Rouquette, J., Choesmel, V. and Gleizes, P.-E. (2005) Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J., 24, 2862-2872.
14. Carron, C., O'Donohue, M.-F., Choesmel, V., Faubladier, M. and Gleizes, P.-E. (2011) Analysis of two human pre-ribosomal factors, bystin and hTsr1, highlights differences in evolution of ribosome biogenesis between yeast and mammals. Nucleic Acids Res., 39, 280-291.
15. Hadjiolova, K.V., Nicoloso, M., Mazan, S., Hadjiolov, A.A. and Bachellerie, J.P. (1993) Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis. Eur. J. Biochem., 212, 211-215.
16. Gerbi, S.A. and Borovjagin, A.V. (2004) Pre-ribosomal RNA processing in multicellular organisms. In: Olson, M.O.J. (ed.), The Nucleolus. Eurekah.com and Kluwer Academic/Plenum Publishers, New York, pp. 170-198.
17. Choesmel, V., Bacqueville, D., Rouquette, J., Noaillac-Depeyre, J., Fribourg, S., Crétien, A., Leblanc, T., Tchernia, G., Da Costa, L. and Gleizes, P.-E. (2007) Impaired ribosome biogenesis in Diamond-Blackfan anemia. Blood, 109, 1275-1283.
18. Flygare, J., Aspesi, A., Bailey, J.C., Miyake, K., Caffrey, J.M., Karlsson, S. and Ellis, S.R. (2007) Human RPS19, the gene mutated in Diamond-Blackfan anemia, encodes a ribosomal protein required for the maturation of 40S ribosomal subunits. Blood, 109, 980-986.
19. Idol, R.A., Robledo, S., Du, H.-Y., Crimmins, D.L., Wilson, D.B., Ladenson, J.H., Bessler, M. and Mason, P.J. (2007) Cells depleted for RPS19, a protein associated with Diamond Blackfan Anemia, show defects in 18S ribosomal RNA synthesis and small ribosomal subunit production. Blood Cells Mol. Dis., 39, 35-43.
20. Doherty, L., Sheen, M.R., Vlachos, A., Choesmel, V., O'Donohue, M.-F., Clinton, C., Schneider, H.E., Sieff, C.A., Newburger, P.E., Ball, S.E. et al. (2010) Ribosomal protein genes RPS10 and RPS26 are commonly mutated in Diamond-Blackfan anemia. Am. J. Hum. Genet., 86, 222-228.
21. Cmejla, R., Cmejlova, J., Handrkova, H., Petrak, J. and Pospisilova, D. (2007) Ribosomal protein S17 gene (RPS17) is mutated in Diamond-Blackfan anemia. Hum. Mutat., 28, 1178-1182.
22. Gazda, H.T., Preti, M., Sheen, M.R., O'Donohue, M.-F., Vlachos, A., Davies, S.M., Kattamis, A., Doherty, L., Landowski, M., Buros, C. et al. (2012) Frameshift mutation in p53 regulator RPL26 is associated with multiple physical abnormalities and a specific pre-rRNA processing defect in Diamond-Blackfan anemia. Hum. Mutat., 33, 1037-1044.
23. Kiss, T. and Filipowicz, W. (1993) Small nucleolar RNAs encoded by introns of the human cell cycle regulatory gene RCC1. EMBO J., 12, 2913-2920.
24. Wang, M. and Pestov, D.G. (2011) 50-end surveillance by Xrn2 acts as a shared mechanism for mammalian pre-rRNA maturation and decay. Nucleic Acids Res., 39, 1811-1822.
25. O'Donohue, M.-F., Choesmel, V., Faubladier, M., Fichant, G. and Gleizes, P.-E. (2010) Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J. Cell Biol., 190, 853-866.
26. Sahasranaman, A., Dembowski, J., Strahler, J., Andrews, P., Maddock, J. and Woolford, J.L. (2011) Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: role of factors required for 27S pre-rRNA processing. EMBO J., 30, 4020-4032.
27. Zemp, I., Wild, T., O'Donohue, M.-F., Wandrey, F., Widmann, B., Gleizes, P.-E. and Kutay, U. (2009) Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol., 185, 1167-1180.
28. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M. and Tollervey, D. (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 30-50 exoribonucleases. Cell, 91, 457-466.
29. LaCava, J., Houseley, J., Saveanu, C., Petfalski, E., Thompson, E., Jacquier, A. and Tollervey, D. (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell, 121, 713-724.
30. Briggs, M.W., Burkard, K.T. and Butler, J.S. (1998) Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 30 end formation. J. Biol. Chem., 273, 13255-13263.
31. Dziembowski, A., Lorentzen, E., Conti, E. and Séraphin, B. (2007) A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol., 14, 15-22.
32. Staals, R., Bronkhorst, A., Schilders, G., Slomovic, S., Schuster, G., Heck, A., Raijmakers, R. and Pruijn, G. (2010) Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J., 29, 2358-2367.
33. Tomecki, R., Kristiansen, M., Lykke-Andersen, S., Chlebowski, A., Larsen, K., Szczesny, R., Drazkowska, K., Pastula, A., Andersen, J.S., Stepien, P. et al. (2010) The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J., 29, 2342-2357.
34. Astuti, D., Morris, M., Cooper, W., Staals, R., Wake, N., Fews, G., Gill, H., Gentle, D., Shuib, S., Ricketts, C. et al. (2012) Germline mutations in DIS3L2 cause the Perlman syndrome of overgrowth and Wilms tumor susceptibility. Nat. Genet., 44, 277-284.
35. 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.
36. Wilkie, N.M. and Smellie, R.M. (1968) Polyribonucleotide synthesis by subfractions of microsomes from rat liver. Biochem. J., 109, 229-238.
37. Hozumi, N., Haruna, I., Watanabe, I., Mikoshiba, K. and Tsukada, Y. (1975) Poly(U) polymerase in rat brain. Nature, 256, 337-339.
38. Milchev, G.I. and Hadjiolov, A.A. (1978) Association of poly(A) and poly(U) polymerases with cytoplasmic ribosomes. Eur. J. Biochem., 84, 113-121.
39. Hayashi, T.T. and MacFarlane, K. (1979) Comparison of endogenous and exogenous RNA primers of poly(U) polymerase in rat hepatic ribosomes. Biochem. J., 177, 895-902.
40. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
41. 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.
42. Raziuddin, Little, R.D., Labella, T. and Schlessinger, D. (1989) Transcription and processing of RNA from mouse ribosomal DNA transfected into hamster cells. Mol. Cell. Biol., 9, 1667-1671.
43. Shumard, C.M., Torres, C. and Eichler, D.C. (1990) In vitro processing at the 30-terminal region of pre-18S rRNA by a nucleolar endoribonuclease. Mol. Cell. Biol., 10, 3868-3872.
44. Strezoska, Z., Pestov, D.G. and Lau, L.F. (2000) Bop1 is a mouse WD40 repeat nucleolar protein involved in 28S and 5. 8S rRNA processing and 60S ribosome biogenesis. Mol. Cell. Biol., 20, 5516-5528.
45. Cavaillé, J., Hadjiolov, A.A. and Bachellerie, J.P. (1996) Processing of mammalian rRNA precursors at the 30 end of 18S rRNA. Identification of cis-acting signals suggests the involvement of U13 small nucleolar RNA. Eur. J. Biochem., 242, 206-213.
46. Rissland, O.S. and Norbury, C.J. (2008) The Cid1 poly(U) polymerase. Biochim. Biophys. Acta, 1779, 286-294.
47. Wilusz, C.J. and Wilusz, J. (2008) New ways to meet your (30) end oligouridylation as a step on the path to destruction. Genes Dev., 22, 1-7.
48. Trippe, R., Richly, H. and Benecke, B.-J. (2003) Biochemical characterization of a U6 small nuclear RNA-specific terminal uridylyltransferase. Eur. J. Biochem., 270, 971-980.
49. Trippe, R., Guschina, E., Hossbach, M., Urlaub, H., Luhrmann, R. and Benecke, B.-J. (2006) Identification, cloning, and functional analysis of the human U6 snRNA-specific terminal uridylyl transferase. RNA, 12, 1494-1504.
50. Mullen, T.E. and Marzluff, W.F. (2008) Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 50 to 30 and 30 to 50. Genes Dev., 22, 50-65.
51. Shcherbik, N., Wang, M., Lapik, Y.R., Srivastava, L. and Pestov, D.G. (2010) Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep., 11, 106-111.
52. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M. and Barton, G.J. (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics, 25, 1189-1191.