Genome-wide analysis of small nucleolar RNAs of leishmania major reveals a rich repertoire of RNAs involved in modification and processing of rRNA

Dror Eliaz, Tirza Doniger, Itai Dov Tkacz, Viplov Kumar Biswas, Sachin Kumar Gupta, Nikolay G. Kolev, Ron Unger, Elisabetta Ullu, Christian Tschudi, Shulamit Michaeli

Research output: Contribution to journalArticlepeer-review

24 Scopus citations

Abstract

Trypanosomatids are protozoan parasites and the causative agent of infamous infectious diseases. These organisms regulate their gene expression mainly at the post-transcriptional level and possess characteristic RNA processing mechanisms. In this study, we analyzed the complete repertoire of Leishmania major small nucleolar (snoRNA) RNAs by performing RNA-seq analysis on RNAs that were affinity-purified using the C/D snoRNA core protein, SNU13, and the H/ ACA core protein, NHP2. This study revealed a large collection of C/D and H/ACA snoRNAs, organized in gene clusters generally containing both snoRNA types. Abundant snoRNAs were identified and predicted to guide trypanosomespecific rRNA cleavages. The repertoire of snoRNAs was compared to that of the closely related Trypanosoma brucei, and 80% of both C/D and H/ACA molecules were found to have functional homologues. The comparative analyses elucidated how snoRNAs evolved to generate molecules with analogous functions in both species. Interestingly, H/ACA RNAs have great flexibility in their ability to guide modifications, and several of the RNA species can guide more than one modification, compensating for the presence of single hairpin H/ACA snoRNA in these organisms. Placing the predicted modifications on the rRNA secondary structure revealed hypermodification regions mostly in domains which are modified in other eukaryotes, in addition to trypanosome-specific modifications.

Original languageEnglish
Pages (from-to)1222-1255
Number of pages34
JournalRNA Biology
Volume12
Issue number11
DOIs
StatePublished - 1 Jan 2015

Bibliographical note

Funding Information:
This work was supported by a grant from the Israel-US Binational Science Foundation (BSF), and the I-core Center of Excellence grant no 1796/12 from the Israel Science Foundation and by NIH grant [RO1 AI 056333] to EU. S.M. holds the David and Inez Myers Chair in RNA silencing of diseases.

Publisher Copyright:
© 2015 Taylor & Francis Group, LLC.

Keywords

  • C/D
  • H/ACA
  • Leishmania
  • Methylation
  • Pseudouridylation
  • RRNA processing
  • SnoRNA

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