A genome-wide analysis of C/D and H/ACA-like small nucleolar RNAs in <i>Trypanosoma brucei</i> reveals a trypanosome-specific pattern of rRNA modification

Liang, Xiaojing; Uliel, Shai; Hury, Avraham; Barth, Sarit; Doniger, Tirza; Unger, Ron; Michaeli, Shulamit

doi:10.1261/rna.7174805

Cited by 73 publications

(130 citation statements)

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“…1B). The number of 2′-O methylations (66 sites) remarkably exceeds that in other eukaryotes, which is consistent with bioinformatics analysis (9) and the modifications on the Leishmania ribosome structure recently revealed (10).…”

Section: Resultssupporting

confidence: 84%

Structure and assembly model for the Trypanosoma cruzi 60S ribosomal subunit

Liu

Gutierrez-Vargas

Jia

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Ribosomes of trypanosomatids, a family of protozoan parasites causing debilitating human diseases, possess multiply fragmented rRNAs that together are analogous to 28S rRNA, unusually large rRNA expansion segments, and r-protein variations compared with other eukaryotic ribosomes. To investigate the architecture of the trypanosomatid ribosomes, we determined the 2.5-Å structure of the Trypanosoma cruzi ribosome large subunit by single-particle cryo-EM. Examination of this structure and comparative analysis of the yeast ribosomal assembly pathway allowed us to develop a stepwise assembly model for the eight pieces of the large subunit rRNAs and a number of ancillary "glue" proteins. This model can be applied to the characterization of Trypanosoma brucei and Leishmania spp. ribosomes as well. Together with other details, our atomic-level structure may provide a foundation for structurebased design of antitrypanosome drugs.ribosome structure | Trypanosoma cruzi | biogenesis | multiply fragmented rRNA | antitrypanosome drug design

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Section: Resultssupporting

confidence: 84%

Structure and assembly model for the Trypanosoma cruzi 60S ribosomal subunit

Liu

Gutierrez-Vargas

Jia

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…These variations stem from either a difference in the number of genes encoding for each snoRNA species or the efficacy of processing of the snoRNA within its cluster (42). Indeed, we have recently demonstrated that the numbers of different snoRNA clusters vary from 1 to 10, and therefore the copy numbers of individual H/ACA genes differ considerably (10). In addition, we noticed a difference in the level of snoRNAs emerging from the same polycistronic RNA, most probably as a result of differential processing efficacy (43).…”

Section: Resultsmentioning

confidence: 77%

“…However, we expect that such RNAs do exist. Recently, we described a genome-wide analysis of H/ACA RNA in T. brucei (10). However, among the 34 H/ACA-like molecules identified, we detected no small Cajal body-specific RNA (scaRNAs) or conventional RNAs that could guide ⌿ modification on U snRNAs (10).…”

Section: Modifications On U Snrnas Are Carried Out In Part By H/aca-imentioning

confidence: 91%

“…Based on these data, we hypothesized that an snR30 homologue should exist in trypanosomes. A search was conducted on the recently described H/ACA repertoire for this RNA (10).…”

Section: Sla1 Depletion Eliminates the ⌿28 Of The Sl Rna And Also Affmentioning

confidence: 99%

“…Recently, we described a genome-wide analysis of H/ACA RNA in T. brucei (10). However, among the 34 H/ACA-like molecules identified, we detected no small Cajal body-specific RNA (scaRNAs) or conventional RNAs that could guide ⌿ modification on U snRNAs (10). Note that all of the H/ACA identified so far in T. brucei are present in clusters also containing C/D snoRNAs, since our search used the SnoScan tool (available on the World Wide Web at rna.wustl.edu/ snoRNAdb/code) that specifically identifies C/D snoRNAs.…”

Section: Modifications On U Snrnas Are Carried Out In Part By H/aca-imentioning

confidence: 99%

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Elucidating the Role of H/ACA-like RNAs in trans-Splicing and rRNA Processing via RNA Interference Silencing of the Trypanosoma brucei CBF5 Pseudouridine Synthase

Barth¹,

Hury²,

Liang

et al. 2005

Journal of Biological Chemistry

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Most pseudouridinylation in eukaryotic rRNA and small nuclear RNAs is guided by H/ACA small nucleolar RNAs. In this study, the Trypanosoma brucei pseudouridine synthase, Cbf5p, a snoRNP protein, was identified and silenced by RNAi. Depletion of this protein destabilized all small nucleolar RNAs of the H/ACA-like family. Following silencing, defects in rRNA processing, such as accumulation of precursors and inhibition of cleavages to generate the mature rRNA, were observed. snR30, an H/ACA RNA involved in rRNA maturation, was identified based on prototypical conserved domains characteristic of this RNA in other eukaryotes. The silencing of CBF5 also eliminated the spliced leader-associated (SLA1) RNA that directs pseudouridylation on the spliced leader RNA (SL RNA), which is the substrate for the trans-splicing reaction. Surprisingly, the depletion of Cbf5p not only eliminated the pseudouridine on the SL RNA but also abolished capping at the fourth cap-4 nucleotide. As a result of defects in the SL RNA and decreased modification on the U small nuclear RNA, trans-splicing was inhibited at the first step of the reaction, providing evidence for the essential role of H/ACA RNAs and the modifications they guide on trans-splicing.

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Euglena Transcript Processing

McWatters

Russell

2017

Advances in Experimental Medicine and Biology

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RNA transcript processing is an important stage in the gene expression pathway of all organisms and is subject to various mechanisms of control that influence the final levels of gene products. RNA processing involves events such as nuclease-mediated cleavage, removal of intervening sequences referred to as introns and modifications to RNA structure (nucleoside modification and editing). In Euglena, RNA transcript processing was initially examined in chloroplasts because of historical interest in the secondary endosymbiotic origin of this organelle in this organism. More recent efforts to examine mitochondrial genome structure and RNA maturation have been stimulated by the discovery of unusual processing pathways in other Euglenozoans such as kinetoplastids and diplonemids. Eukaryotes containing large genomes are now known to typically contain large collections of introns and regulatory RNAs involved in RNA processing events, and Euglena gracilis in particular has a relatively large genome for a protist. Studies examining the structure of nuclear genes and the mechanisms involved in nuclear RNA processing have revealed that indeed Euglena contains large numbers of introns in the limited set of genes so far examined and also possesses large numbers of specific classes of regulatory and processing RNAs, such as small nucleolar RNAs (snoRNAs). Most interestingly, these studies have also revealed that Euglena possesses novel processing pathways generating highly fragmented cytosolic ribosomal RNAs and subunits and non-conventional intron classes removed by unknown splicing mechanisms. This unexpected diversity in RNA processing pathways emphasizes the importance of identifying the components involved in these processing mechanisms and their evolutionary emergence in Euglena species.

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A genome-wide analysis of C/D and H/ACA-like small nucleolar RNAs in Trypanosoma brucei reveals a trypanosome-specific pattern of rRNA modification

Cited by 73 publications

References 59 publications

Structure and assembly model for the Trypanosoma cruzi 60S ribosomal subunit

Structure and assembly model for the Trypanosoma cruzi 60S ribosomal subunit

Elucidating the Role of H/ACA-like RNAs in trans-Splicing and rRNA Processing via RNA Interference Silencing of the Trypanosoma brucei CBF5 Pseudouridine Synthase

Euglena Transcript Processing

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