Two orthogonal cleavages separate subunit RNAs in mouse ribosome biogenesis

Nucleic Acids Research

Volumn 42, Issue 17, 2014, Pages 11180-11191

  Wang, Minshi ^a,b   Anikin, Leonid ^a,b   Pestov, Dimitri G ^a  

^a UMDNJ School of Osteopathic Medicine   (United States)

^b ROWAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FCF1 PROTEIN; INTERNAL TRANSCRIBED SPACER 1; LARGE SUBUNIT RIBOSOMAL RNA; PROTEIN NOG1; PROTEIN PES1; PROTEIN RCL1; RIBOSOME RNA; SMALL SUBUNIT RIBOSOMAL RNA; UNCLASSIFIED DRUG; UTP23 PROTEIN; UTP24 PROTEIN; RIBOSOMAL SPACER DNA; RIBOSOME PROTEIN; RNA 18S; RNA PRECURSOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RATIO ANALYSIS OF MULTIPLE PRECURSOR; RNA ANALYSIS; RNA CLEAVAGE; RNA PROCESSING; RNA SYNTHESIS; RNA TRANSCRIPTION; STRUCTURE ANALYSIS; 3T3 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL CULTURE; CHEMISTRY; LARGE RIBOSOMAL SUBUNIT; METABOLISM; RNA INTERFERENCE; SMALL RIBOSOMAL SUBUNIT;

MAMMALIA;

ANIMALS; BALB 3T3 CELLS; CELLS, CULTURED; DNA, RIBOSOMAL SPACER; MICE; MODELS, GENETIC; NIH 3T3 CELLS; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA CLEAVAGE; RNA INTERFERENCE; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 18S;

EID: 84926197782     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku787     Document Type: Article

References (56)

1. Mullineux, S. and Lafontaine, D.L.L. (2012) Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie, 94, 1521-1532.
2. Kressler, D., Hurt, E. and Bassler, J. (2010) Driving ribosome assembly. Biochim. Biophys. Acta, 1803, 673-683.
3. Woolford, J.L.J. and Baserga, S.J. (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics, 195, 643-681.
4. Lapik, Y.R., Fernandes, C.J., Lau, L.F. and Pestov, D.G. (2004) Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol. Cell, 15, 17-29.
5. Gérus, M., Bonnart, C., Caizergues-Ferrer, M., Henry, Y. and Henras, A.K. (2010) Evolutionarily conserved function of RRP36 in early cleavages of the pre-rRNA and production of the 40S ribosomal subunit. Mol. Cell. Biol., 30, 1130-1144.
6. Schillewaert, S., Wacheul, L., Lhomme, F. and Lafontaine, D.L.L. (2012) The evolutionarily conserved protein Las1 is required for pre-rRNA processing at both ends of ITS2. Mol. Cell. Biol., 32, 430-444.
7. Castle, C.D., Cassimere, E.K. and Denicourt, C. (2012) LAS1L interacts with the mammalian Rix1 complex to regulate ribosome biogenesis. Mol Biol. Cell, 23, 716-728.
8. Peculis, B.A. and Steitz, J.A. (1993) Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell, 73, 1233-1245.
9. Cavaillé, J., Hadjiolov, A.A. and Bachellerie, J.P. (1996) Processing of mammalian rRNA precursors at the 3' end of 18S rRNA. Identification of cis-acting signals suggests the involvement of U13 small nucleolar RNA. Eur. J. Biochem., 242, 206-213.
10. Freed, E.F., Prieto, J., McCann, K.L., McStay, B. and Baserga, S.J. (2012) NOL11, implicated in the pathogenesis of North American Indian childhood cirrhosis, is required for pre-rRNA transcription and processing. PLoS Genet., 8, e1002892.
11. Tafforeau, L., Zorbas, C, Langhendries, J., Mullineux, S., Stamatopoulou, V, Mullier, R., Wacheul, L. and Lafontaine, D.L.J. (2013) The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of pre-rRNA processing factors. Mol Cell, 51, 539-551.
12. Morello, L.G., Coltri, PP, Quaresma, A.J.C, Simabuco, F.M., Silva, T.C.L., Singh, G., Nickerson, J.A., Oliveira, C.C, Moore, M.J. and Zanchin, N.I.T. (2011) The human nucleolar protein FTSJ3 associates with NIP7 and functions in pre-rRNA processing. PLoS One, 6, e29174.
13. Osheim, YN, French, S.L., Keck, K.M., Champion, E.A., Spasov, K, Dragon, F, Baserga, S.J. and Beyer, A.L. (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.
14. Kos, M. and Tollervey, D. (2010) Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol Cell, 37, 809-820.
15. Carron, C, O'Donohue, M., Choesmel, V, Faubladier, M. and Gleizes, P (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.
16. Preti, M., O'Donohue, M., Montel-Lehry, N, Bortolin-Cavaillé, M., Choesmel, V. and Gleizes, P (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.
17. Sloan, K.E., Mattijssen, S., Lebaron, S., Tollervey, D., Pruijn, GJ.M. and Watkins, NJ. (2013) Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J. Cell. Biol, 200, 577-588.
18. Coleman, A.W. (2013) Analysis of mammalian rDNA internal transcribed spacers. PLoS One, 8, e79122.
19. 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.
20. Bleichert, F, Granneman, S., Osheim, YN, 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.
21. 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.
22. 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.
23. Hoareau-Aveilla, C, Fayet-Lebaron, E., Jady, B.E., Henras, A.K. and Kiss, T (2012) Utp23p is required for dissociation of snR30 small nucleolar RNP from preribosomal particles. Nucleic Acids Res., 40, 3641-3652.
24. Sloan, K.E., Bohnsack, M.T, Schneider, C. and Watkins, NJ. (2014) The roles of SSU processome components and surveillance factors in the initial processing of human ribosomal RNA. RNA, 20, 540-550.
25. Grimm, T, Hölzel, M, Rohrmoser, M., Harasim, T, Malamoussi, A., Gruber-Eber, A., Kremmer, E. and Eick, D. (2006) Dominant-negative Pes1 mutants inhibit ribosomal RNA processing and cell proliferation via incorporation into the PeBoW-complex. Nucleic Acids Res., 34, 3030-3043.
26. Lapik, YR., Misra, J.M., Lau, L.F and Pestov, DG (2007) Restricting conformational flexibility of the switch II region creates a dominant-inhibitory phenotype in Obg GTPase Nog1. Mol Cell. Biol, 27, 7735-7744.
27. 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.
28. Shcherbik, N, Wang, M., Lapik, YR., Srivastava, L. and Pestov, D.G (2010) Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep., 11, 106-111.
29. Mansour, FH. and Pestov, D.G (2013) Separation of long RNA by agarose-formaldehyde gel electrophoresis. Anal. Biochem., 441, 18-20.
30. Pestov, D.G., Lapik, YR. and Lau, L.F (2008) Assays for ribosomal RNA processing and ribosome assembly. Curr. Protoc. Cell. Biol, 39, 22.11.1-22.11.16.
31. Wang, M. and Pestov, DG (2011) 5'-end surveillance by Xrn2 acts as a shared mechanism for mammalian pre-rRNA maturation and decay. Nucleic Acids Res., 39, 1811-1822.
32. 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.
33. O'Donohue, M., Choesmel, V, Faubladier, M., Fichant, G. and Gleizes, P (2010) Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J. Cell. Biol, 190, 853-866.
34. Kent, T, Lapik, YR. and Pestov, DG. (2009) The 5' external transcribed spacer in mouse ribosomal RNA contains two cleavage sites. RNA, 15, 14-20.
35. Oeffinger, M., Leung, A., Lamond, A. and Tollervey, D (2002) Yeast Pescadillo is required for multiple activities during 60S ribosomal subunit synthesis. RNA, 8, 626-636.
36. Jensen, B.C., Wang, Q., Kfer, C.T and Parsons, M. (2003) The NOG1 GTP-binding protein is required for biogenesis of the 60 S ribosomal subunit. J. Biol. Chem., 278, 32204-32211.
37. Miles, TD., Jakovljevic, J., Horsey, E.W., Harnpicharnchai, P, Tang, L. and Woolford, J.L.L. (2005) Ytm1, Nop7, and Erb1 form a complex necessary for maturation of yeast 66S preribosomes. Mol Cell. Biol, 25, 10419-10432.
38. Saveanu, C, Namane, A., Gleizes, P, Lebreton, A., Rousselle, J., Noaillac-Depeyre, J., Gas, N, Jacquier, A. and Fromont-Racine, M. (2003) Sequential protein association with nascent 60S ribosomal particles. Mol Cell. Biol, 23, 4449-4460.
39. Tang, L., Sahasranaman, A., Jakovljevic, J., Schleifman, E. and Woolford, J.L.L. (2008) Interactions among Ytm1, Erb1, and Nop7 required for assembly of the Nop7-subcomplex in yeast preribosomes. Mol Biol. Cell, 19, 2844-2856.
40. Sahasranaman, A., Dembowski, J., Strahler, J., Andrews, P, Maddock, J. and Woolford, J.L.L. (2011) Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: role of factors required for 27S pre-rRNA processing. EMBO J., 30, 4020-4032.
41. Talkish, J., Zhang, J., Jakovljevic, J., Horsey, E.W. and Woolford, J.L.J. (2012) Hierarchical recruitment into nascent ribosomes of assembly factors required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res., 40, 8646-8661.
42. Lau, L.F and Nathans, D (1987) Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc. Natl. Acad. Sci. U.S.A., 84, 1182-1186.
43. Freed, E.F., Bleichert, F, Dutca, L.M. and Baserga, S.J. (2010) When ribosomes go bad: diseases of ribosome biogenesis. Mol Biosyst., 6, 481-493.
44. Fumagalli, S. and Thomas, G. (2011) The role of p53 in ribosomopathies. Semin. Hematol, 48, 97-105.
45. Hölzel, M., Orban, M., Hochstatter, J., Rohrmoser, M., Harasim, T, Malamoussi, A., Kremmer, E., Längst, G and Eick, D. (2010) Defects in 18 S or 28 S rRNA processing activate the p53 pathway. J. Biol. Chem., 285, 6364-6370.
46. Gazda, H.T., Preti, M., Sheen, M.R., O'Donohue, M., 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-ribosomal RNA processing defect in diamond-blackfan anemia. Hum. Mutat., 33, 1037-1044.
47. Strezoska, Z., Pestov, D.G and Lau, L.F (2002) Functional inactivation of the mouse nucleolar protein Bop1 inhibits multiple steps in pre-rRNA processing and blocks cell cycle progression. J. Biol. Chem., 277, 29617-29625.
48. Robledo, S., Idol, R.A., Crimmins, D.L., Ladenson, J.H., Mason, P.J. and Bessler, M. (2008) The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA, 14, 1918-1929.
49. Goldman, W.E., Goldberg, G., Bowman, L.H., Steinmetz, D. and Schlessinger, D. (1983) Mouse rDNA: sequences and evolutionary analysis of spacer and mature RNA regions. Mol. Cell. Biol., 3, 1488-1500.
50. Venema, J. and Tollervey, D. (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet., 33, 261-311.
51. Adams, C.C., Jakovljevic, J., Roman, J., Harnpicharnchai, P. and Woolford, J.L.L. (2002) Saccharomyces cerevisiae nucleolar protein Nop7p is necessary for biogenesis of 60S ribosomal subunits. RNA, 8, 150-165.
52. Kallstrom, G., Hedges, J. and Johnson, A. (2003) The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol. Cell. Biol., 23, 4344-4355.
53. Dabeva, M.D., Dudov, K.P., Hadjiolov, A.A., Emanuilov, I. and Todorov, B.N. (1976) Intranuclear maturation pathways of rat liver ribosomal ribonucleic acids. Biochem. J., 160, 495-503.
54. Bowman, L.H., Rabin, B. and Schlessinger, D. (1981) Multiple ribosomal RNA cleavage pathways in mammalian cells. Nucleic Acids Res., 9, 4951-4966.
55. Savino, R. and Gerbi, S.A. (1990) In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J., 9, 2299-2308.
56. 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.