The N-terminal extension of yeast ribosomal protein L8 is involved in two major remodeling events during late nuclear stages of 60S ribosomal subunit assembly

Tutuncuoglu, Beril; Jakovljevic, Jelena; Wu, Shan; Gao, Ning; Woolford, John L.

doi:10.1261/rna.055798.115

Cited by 18 publications

(18 citation statements)

References 71 publications

(89 reference statements)

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“…On the other hand, deletion of the eukaryote-specific N-terminal extension of L8 that intimately contacts ES31 L , causes a later, 7S pre-rRNA accumulation phenotype (Tutuncuoglu et al 2016), which is similar to the phenotype that ES31Δ L exhibits. Thus, what initially appeared to be an exception to the neighborhood-specific phenotype rule, turned out to be an informative sign about how eukaryote-specific RNAprotein elements that contact each other, exhibit similar functions in ribosome assembly.…”

Section: Viable Es Mutants Can Synthesize Mature 25s Rrnamentioning

confidence: 78%

Eukaryote-specific rRNA expansion segments function in ribosome biogenesis

Ramesh

Woolford

2016

RNA

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The secondary structure of ribosomal RNA (rRNA) is largely conserved across all kingdoms of life. However, eukaryotes have evolved extra blocks of rRNA sequences, relative to those of prokaryotes, called expansion segments (ES). A thorough characterization of the potential roles of ES remains to be done, possibly because of limitations in the availability of robust systems to study rRNA mutants. We sought to systematically investigate the potential functions, if any, of the ES in 25S rRNA of Saccharomyces cerevisiae by deletion mutagenesis. We deleted 14 of the 16 different eukaryote-specific ES in yeast 25S rRNA individually and assayed their phenotypes. Our results show that all but two of the ES tested are necessary for optimal growth and are required for production of 25S rRNA, suggesting that ES play roles in ribosome biogenesis. Further, we classified expansion segments into groups that participate in early nucleolar, middle, and late nucleoplasmic steps of ribosome biogenesis, by assaying their pre-rRNA processing phenotypes. This study is the first of its kind to systematically identify the functions of eukaryote-specific expansion segments by showing that they play roles in specific steps of ribosome biogenesis. The catalog of phenotypes we identified, combined with previous investigations of the roles ribosomal proteins in large subunit biogenesis, leads us to infer that assembling ribosomes are composed of distinct RNA and protein structural neighborhood clusters that participate in specific steps of ribosome biogenesis.

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Section: Viable Es Mutants Can Synthesize Mature 25s Rrnamentioning

confidence: 78%

Eukaryote-specific rRNA expansion segments function in ribosome biogenesis

Ramesh

Woolford

2016

RNA

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“…Recent studies have begun to reveal specific functions of r-protein extensions [56,66,71–73]. Deletion of r-protein extensions that bind the same domains of rRNA as their globular portion affects ribosome assembly in a manner similar to depletion of that r-protein [71].…”

Section: R-protein Extensions Are Crucial To Ribosome Assemblymentioning

confidence: 99%

“…Deletion of r-protein extensions that bind the same domains of rRNA as their globular portion affects ribosome assembly in a manner similar to depletion of that r-protein [71]. This effect probably reflects that the same domains of rRNA are structured by binding to the r-protein globular domains as to the extensions.…”

Section: R-protein Extensions Are Crucial To Ribosome Assemblymentioning

confidence: 99%

“…In contrast, r-protein extensions that span multiple rRNA domains are predicted to play a role in structuring or communicating structural changes across these domains during ribosome assembly. For example, a recent study showed that removing the N-terminal extension of L8 blocks later steps in assembly, than are blocked when the entire protein is depleted [71]. In this case, the globular domain of L8 binds to domain I of 25S rRNA, which assembles early, whereas the extension of L8 threads into domain V of 25S rRNA, which is constructed at later stages.…”

Section: R-protein Extensions Are Crucial To Ribosome Assemblymentioning

confidence: 99%

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Principles of 60S ribosomal subunit assembly emerging from recent studies in yeast

Konikkat

Woolford

2017

Biochemical Journal

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Ribosome biogenesis requires the intertwined processes of folding, modification, and processing of ribosomal RNA, together with binding of ribosomal proteins. In eukaryotic cells, ribosome assembly begins in the nucleolus, continues in the nucleoplasm, and is not completed until after nascent particles are exported to the cytoplasm. The efficiency and fidelity of ribosome biogenesis are facilitated by >200 assembly factors and ~76 different small nucleolar RNAs. The pathway is driven forward by numerous remodeling events to rearrange the ribonucleoprotein architecture of pre-ribosomes. Here, we describe principles of ribosome assembly that have emerged from recent studies of biogenesis of the large ribosomal subunit in the yeast Saccharomyces cerevisiae. We describe tools that have empowered investigations of ribosome biogenesis, and then summarize recent discoveries about each of the consecutive steps of subunit assembly.

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“…One of the Brix domain-containing proteins is the Saccharomyces cerevisiae ribosome assembly factor Rpf2 (Ribosome production factor 2), which in complex with Rrs1 plays a role in the early steps of the 60S ribosome subunit maturation (Zhang et al, 2007;Henras et al, 2015;Kressler et al, 2017). Rpf2 binds the Rpl5 and Rpl11 ribosomal proteins and the Rrs1 protein, forming both the 5S ribonucleoprotein particle necessary for 25S rRNA maturation and the large 60S ribosomal subunit (Tutuncuoglu et al, 2016). Depletion of Rpf2 results in defects in pre-rRNA processing (Wehner, Baserga, 2002).…”

Section: Introductionmentioning

confidence: 99%

Non3 is an essential Drosophila gene required for proper nucleolus assembly

et al. 2019

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The nucleolus is a dynamic non-membrane-bound nuclear organelle, which plays key roles not only in ribosome biogenesis but also in many other cellular processes. Consistent with its multiple functions, the nucleolus has been implicated in many human diseases, including cancer and degenerative pathologies of the nervous system and heart. Here, we report the characterization of the Drosophila Non3 (Novel nucleolar protein 3) gene, which encodes a protein homologous to the human Brix domain-containing Rpf2 that has been shown to control ribosomal RNA (rRNA) processing. We used imprecise P-element excision to generate four new mutant alleles in the Non3 gene. Complementation and phenotypic analyses showed that these Non3 mutations can be arranged in an allelic series that includes both viable and lethal alleles. The strongest lethal allele (Non3∆600) is a genetically null allele that carries a large deletion of the gene and exhibits early lethality when homozygous. Flies heterozygous for Non3∆600 occasionally exhibit a mild reduction in the bristle size, but develop normally and are fertile. However, heteroallelic combinations of viable Non3 mutations (Non3197, Non3310 and Non3259) display a Minute-like phenotype, consisting in delayed development and short and thin bristles, suggesting that they are defective in ribosome biogenesis. We also demonstrate that the Non3 protein localizes to the nucleolus of larval brain cells and it is required for proper nucleolar localization of Fibrillarin, a protein important for post-translational modification and processing of rRNAs. In summary, we generated a number of genetic and biochemical tools that were exploited for an initial characterization of Non3, and will be instrumental for future functional studies on this gene and its protein product.

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The N-terminal extension of yeast ribosomal protein L8 is involved in two major remodeling events during late nuclear stages of 60S ribosomal subunit assembly

Cited by 18 publications

References 71 publications

Eukaryote-specific rRNA expansion segments function in ribosome biogenesis

Eukaryote-specific rRNA expansion segments function in ribosome biogenesis

Principles of 60S ribosomal subunit assembly emerging from recent studies in yeast

Non3 is an essential Drosophila gene required for proper nucleolus assembly

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