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Emerging roles for the Ro 60‐kDa autoantigen in noncoding RNA metabolism

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Soyeong Sim, Sandra L. Wolin

Published Online: Apr 21 2011

DOI: 10.1002/wrna.85

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Abstract All cells contain an enormous variety of ribonucleoprotein (RNP) complexes that function in diverse processes. Although the mechanisms by which many of these RNPs contribute to cell metabolism are well understood, the roles of others are only now beginning to be revealed. A member of this latter category, the Ro 60‐kDa protein and its associated noncoding Y RNAs, was discovered because the protein component is a frequent target of the autoimmune response in patients with the rheumatic diseases systemic lupus erythematosus and Sjögren's syndrome. Recent studies have shown that Ro is ring shaped, binds the single‐stranded ends of misfolded noncoding RNAs in its central cavity, and may function in noncoding RNA quality control. Although Ro is not present in yeast, many bacterial genomes contain potential Ro orthologs. In the radiation‐resistant eubacterium Deinococcus radiodurans, the Ro ortholog functions with exoribonucleases during stress‐induced changes in RNA metabolism. Moreover, in both D. radiodurans and animal cells, Ro is involved in the response to multiple types of environmental stress. Finally, Y RNAs can influence the subcellular location of Ro, inhibit access of the central cavity to other RNAs, and may also act as binding sites for proteins that influence Ro function. WIREs RNA 2011 2 686–699 DOI: 10.1002/wrna.85 This article is categorized under: RNA Evolution and Genomics > RNA and Ribonucleoprotein Evolution RNA Processing > Processing of Small RNAs RNA Turnover and Surveillance > Turnover/Surveillance Mechanisms

Model for the role of Ro in pre‐5S rRNA quality control. Newly synthesized pre‐5S rRNA can either fold into the correct structure (a) or can misfold (b). Changes in the 5S rRNA secondary structure are depicted by bold lines. Binding by Ro could sequester the misfolded RNA, preventing ribosome incorporation, and/or recruit nucleases that degrade the RNA. The drawing is not to scale.

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Predicted secondary structures of Y RNAs. (a) The four human Y RNAs are shown. The conserved boxed sequences are critical for Ro recognition.62,75,76 (b) Predicted structures for the identified Y RNAs in Caenorhabditis elegans and Deinococcus radiodurans.17,19

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Models for the roles of Deinococcus radiodurans Rsr (Ro sixty‐related) in modulating rRNA metabolism during stress. (a) During D. radiodurans growth at 30°C, 23S rRNA maturation by polynucleotide phosphorylase (PNPase) is inefficient. At 37°C, a heat stress temperature, Rsr maturation becomes efficient and requires Y RNA‐free Rsr, RNase II, and RNase PH.24 (b) During prolonged growth in stationary phase, a form of starvation, translation becomes inefficient and the levels of free ribosomal subunits increase. Rsr recruits PNPase to ribosomal subunits, thereby promoting rRNA degradation. In addition to Rsr and PNPase, at least one other nuclease participates in degradation.25 The models in (a) and (b) are not to scale.

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Unrooted phylogenetic tree showing the relationships of putative Ro orthologs from selected species. Sequence alignments were performed using ClustalW66 and the tree was drawn by the neighbor‐joining method using Phylip.67

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Structures of Ro proteins. (a) Domain structure of Xenopus laevis Ro.62 Ro is colored according to the rainbow, with the N‐terminus in blue and the C‐terminus in red. N‐terminal HEAT repeats form a ring that is closed by a von Willebrand factor A (vWFA) domain. The vWFA domain contains a divalent cation‐binding site known as a metal ion‐dependent adhesion site (MIDAS) that in integrins is a ligand‐binding site.65 Green sphere: Mg²⁺ from the crystallization buffer. (b) Molecular surface representation of X. laevis Ro bound to a fragment of misfolded pre‐5S rRNA.53 Basic residues on the surface are colored bright blue. The single‐stranded 3′ end binds in the cavity and the helix binds to a basic platform on the outer surface. Most of the interactions of Ro with the helix are to the backbone. (c) Domain structure of Deinococcus radiodurans Rsr (Ro sixty‐related) shown in the same orientation and colors as X. laevis Ro (a). Green sphere: Ca²⁺ from the crystallization buffer.64 (d) Molecular surface representation of X. laevis Ro bound to a Y RNA fragment containing the conserved helix that is required for high‐affinity binding. The bulged helix binds on the outer surface of Ro. In this structure, a single‐stranded RNA (one of the strands used to form the Y RNA duplex) binds in the central cavity.62

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