The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing

Kass, Susan; Tyc, Kazimierz; Steitz, Joan A.; Sollner‐Webb, Barbara

doi:10.1016/0092-8674(90)90338-f

Cited by 425 publications

(285 citation statements)

References 53 publications

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“…In yeast, U3 base pairs in the 5Ј ETS and is essential for cleavage within the 5Ј ETS, but cleavage does not occur at the binding site (14). There is additional evidence that U3 may be acting at a site within mature 18S, facilitating the formation of a pseudoknot, which is present in the mature ribosome (11).…”

Section: Discussionmentioning

confidence: 95%

“…U3, the most abundant and ubiquitous snoRNA, is essential for the accumulation of mature 18S rRNA; Saccharomyces cerevisiae cells genetically depleted of U3 snoRNA fail to accumulate 18S rRNA (12). Xenopus oocytes depleted of U3 by RNase H-mediated degradation show altered pre-rRNA processing (28), and extracts depleted of U3 will not process exogenous pre-rRNA (14). In addition, U3 has the potential to base pair with pre-rRNA (4,11) and has been cross-linked in vitro to sites within the 5Ј external transcribed spacer (5Ј ETS) (Fig.…”

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confidence: 99%

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The Sequence of the 5′ End of the U8 Small Nucleolar RNA Is Critical for 5.8S and 28S rRNA Maturation

Peculis

1997

Molecular and Cellular Biology

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Ribosome biogenesis in eucaryotes involves many small nucleolar ribonucleoprotein particles (snoRNP), a few of which are essential for processing pre-rRNA. Previously, U8 snoRNA was shown to play a critical role in pre-rRNA processing, being essential for accumulation of mature 28S and 5.8S rRNAs. Here, evidence which identifies a functional site of interaction on the U8 RNA is presented. RNAs with mutations, insertions, or deletions within the 5 -most 15 nucleotides of U8 do not function in pre-rRNA processing. In vivo competitions in Xenopus oocytes with 2 O-methyl oligoribonucleotides have confirmed this region as a functional site of a base-pairing interaction. Cross-species hybrid molecules of U8 RNA show that this region of the U8 snoRNP is necessary for processing of pre-rRNA but not sufficient to direct efficient cleavage of the pre-rRNA substrate; the structure or proteins comprising, or recruited by, the U8 snoRNP modulate the efficiency of cleavage. Intriguingly, these 15 nucleotides have the potential to base pair with the 5 end of 28S rRNA in a region where, in the mature ribosome, the 5 end of 28S interacts with the 3 end of 5.8S. The 28S-5.8S interaction is evolutionarily conserved and critical for pre-rRNA processing in Xenopus laevis. Taken together these data strongly suggest that the 5 end of U8 RNA has the potential to bind pre-rRNA and in so doing, may regulate or alter the pre-rRNA folding pathway. The rest of the U8 particle may then facilitate cleavage or recruitment of other factors which are essential for pre-rRNA processing.

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Section: Discussionmentioning

confidence: 95%

mentioning

confidence: 99%

The Sequence of the 5′ End of the U8 Small Nucleolar RNA Is Critical for 5.8S and 28S rRNA Maturation

Peculis

1997

Molecular and Cellular Biology

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“…U3 and U14 are transiently associated with some 5Ј-ETS and 18S sequences of pre-rRNA (Beltrame and Tollervey, 1995;Liang and Fournier, 1995), and they have been suggested to assemble into a hypothetical multiple-snoRNP complex (Maxwell and Fournier, 1995;Ghisolfi-Nieto et al, 1996). In addition, electron-dense "terminal balls" at the leading ends of nascent pre-rRNA transcripts have been identified as the 5Ј-ETS primary processing complexes (Kass et al, 1990;Mougey et al, 1993a), which appear to contain U3 snoRNA (Kass et al, 1990), fibrillarin (Scheer and Benavente, 1990;Mougey et al, 1993b), and nucleolin (Ghisolfi-Nieto et al, 1996;Ginisty et al, 1998). Thus, the NDF may be a means of preserving the integrity of these processing complexes until the reformed postmitotic nucleoli become fully functional.…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, specific components of the RNA pol I transcription machinery were not present in the NDF; this is in agreement with previous findings indicating the spatial separation of pre-rRNA transcription machinery and pre-rRNA processing components during mitosis. One pre-rRNA processing component found in the NDF was U3 small nucleolar (sno)RNA, which is essential for cleavage at the primary processing site of the 5Ј-external transcribed spacer (ETS) and subsequent processing events around the 18S rRNA region (Kass et al, 1990;Savino and Gerbi, 1990;Hughes and Ares, 1991) as well as the M phase phosphoprotein 10 component of U3 small nucleolar ribonucleoprotein (sno-RNP) implicated in 18S pre-rRNA processing in yeast (Dunbar et al, 1997;Westendorf et al, 1998). In addition, Beven et al (1996) localized U14 snoRNA, which is involved in processing steps in the vicinity of the 18S rRNA region (Li et al, 1990;Liang and Fournier, 1995) and U3 snoRNA in numerous particles, termed prenucleolar bodies, located throughout the cytoplasm in pea root cells during anaphase.…”

Section: Introductionmentioning

confidence: 99%

Partially Processed pre-rRNA Is Preserved in Association with Processing Components in Nucleolus-derived Foci during Mitosis

Dundr

Olson

1998

MBoC

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Previous studies showed that components implicated in pre-rRNA processing, including U3 small nucleolar (sno)RNA, fibrillarin, nucleolin, and proteins B23 and p52, accumulate in perichromosomal regions and in numerous mitotic cytoplasmic particles, termed nucleolus-derived foci (NDF) between early anaphase and late telophase. The latter structures were analyzed for the presence of pre-rRNA by fluorescence in situ hybridization using probes for segments of pre-rRNA with known half-lives. The NDF did not contain the short-lived 5Ј-external transcribed spacer (ETS) leader segment upstream from the primary processing site in 47S pre-rRNA. However, the NDF contained sequences from the 5Ј-ETS core, 18S, internal transcribed spacer 1 (ITS1), and 28S segments and also had detectable, but significantly reduced, levels of the 3Ј-ETS sequence. Northern analyses showed that in mitotic cells, the latter sequences were present predominantly in 45S-46S pre-rRNAs, indicating that high-molecular weight processing intermediates are preserved during mitosis. Two additional essential processing components were also found in the NDF: U8 snoRNA and hPop1 (a protein component of RNase MRP and RNase P). Thus, the NDF appear to be large complexes containing partially processed pre-rRNA associated with processing components in which processing has been significantly suppressed. The NDF may facilitate coordinated assembly of postmitotic nucleoli. INTRODUCTIONThe nucleolus is a prominent membraneless subnuclear compartment assembled around clusters of tandemly repeated rDNA genes from which prerRNA is transcribed and subsequently folded, processed, modified, and assembled into small and large ribosomal subunits (Scheer et al., 1993;Shaw and Jordan, 1995;Maden and Hughes, 1997). A remarkable aspect of the cell cycle is the disintegration of the nucleolus during mitosis and its reassembly as the daughter cells proceed toward G 1 phase. A pivotal event in this process is the repression of RNA polymerase (pol) I-driven pre-rRNA synthesis between prophase and telophase (Prescott and Bender, 1962). At the same time, nucleolar components disperse to various subcellular locations as the maternal nucleoli diassemble (Goessens, 1984).A comprehensive understanding of the locations and fates of nucleolar components during mitosis is slowly emerging (Scheer et al., 1993;Hernandez-Verdun and Gautier, 1994). For example, much of the RNA pol I transcription machinery and DNA topoisomerase I remain associated with the nucleolus organizer regions (NORs) 1 of chromosomes between nucleolar disassembly in late prophase and reassembly in telophase (Scheer et al., 1993; Weisenberger and * Corresponding author. 1 Abbrevations used: DFC, dense fibrillar component; ETS, external transcribed spacer; GC, granular component; ITS, internal transcribed spacer; NDF, nucleolus-derived foci; NOR, nucleolus organizer region; PNB, prenucleolar body; pol, polymerase; snoRNA, small nucleolar RNA; sno-RNP, small nucleolar ribonucleoprotein.© 1998 by The American Society for Ce...

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“…In mammals, significant U3-dependent cleavage occurs at this site in the ETS as an early event in rRNA processing (site AЈ in Fig. 1; Kass et al 1990;Enright et al 1996). However, cleavage at site AЈ is barely, or not FIGURE 8.…”

Section: U3 Snornp Docking On Pre-rrnamentioning

confidence: 99%

Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction

Borovjagin

Gerbi²

2004

RNA

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U3 small nucleolar RNA (snoRNA) is essential for rRNA processing to form 18S ribosomal RNA (rRNA). Previously, it has been shown that nucleolin is needed to load U3 snoRNA on pre-rRNA. However, as documented here, this is not sufficient. We present data that base-pairing between the U3 hinges and the external transcribed spacer (ETS) is critical for functional alignment of U3 on its pre-rRNA substrate. Additionally, the interaction between the U3 hinges and the ETS is proposed to serve as an anchor to hold U3 on the pre-rRNA substrate, while box A at the 5 end of U3 snoRNA swivels from ETS contacts to 18S rRNA contacts. Compensatory base changes revealed base-pairing between the 3 hinge of U3 snoRNA and region E1 of the ETS in Xenopus pre-rRNA; this novel interaction is required for 18S rRNA production. In contrast, base-pairing between the 5 hinge of U3 snoRNA and region E2 of the ETS is auxiliary, unlike the case in yeast where it is required. Thus, higher and lower eukaryotes use different interactions for functional association of U3 with pre-rRNA. The U3 hinge sequence varies between species, but covariation in the ETS retains complementarity. This species-specific U3-pre-rRNA interaction offers a potential target for a new class of antibiotics to prevent ribosome biogenesis in eukaryotic pathogens.

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The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing

Cited by 425 publications

References 53 publications

The Sequence of the 5′ End of the U8 Small Nucleolar RNA Is Critical for 5.8S and 28S rRNA Maturation

The Sequence of the 5′ End of the U8 Small Nucleolar RNA Is Critical for 5.8S and 28S rRNA Maturation

Partially Processed pre-rRNA Is Preserved in Association with Processing Components in Nucleolus-derived Foci during Mitosis

Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction

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