Chance and necessity in the evolution of RNase P

Gopalan, Venkat; Jarrous, Nayef; Krasilnikov, Andrey S.

doi:10.1261/rna.063107.117

Cited by 28 publications

(27 citation statements)

References 48 publications

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“…RNase MRP is evolutionarily related to RNase P, a ribozyme-based RNP primarily involved in the maturation of tRNA (15)(16)(17). RNase MRP appears to have split from the RNase P lineage early in the evolution of eukaryotes, acquiring distinct substrate specificity and cellular functions (5,18,19).…”

Section: One Sentence Summarymentioning

confidence: 99%

“…RNase MRP is localized to the nucleolus and, transiently, to the cytoplasm (3). Known RNase MRP functions include its participation in the maturation of rRNA and in the metabolism of specific mRNAs involved in the regulation of the cell cycle (6-13).Defects in RNase MRP result in a range of pleiotropic developmental disorders in humans (14).RNase MRP is evolutionarily related to RNase P, a ribozyme-based RNP primarily involved in the maturation of tRNA (15)(16)(17). RNase MRP appears to have split from the RNase P lineage early in the evolution of eukaryotes, acquiring distinct substrate specificity and cellular functions (5,18,19).The catalytic (C-) domain of RNase MRP RNA (Fig.…”

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confidence: 99%

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Cryo-EM structure of catalytic ribonucleoprotein complex RNase MRP

Perederina

Lee

et al. 2020

Preprint

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RNase MRP is an essential eukaryotic ribonucleoprotein complex involved in the maturation of rRNA and the regulation of the cell cycle. RNase MRP is related to the ribozyme-based RNase P, but it has evolved to have distinct cellular roles. We report a cryo-EM structure of the S. cerevisiae RNase MRP holoenzyme solved to 3.0 Å. We describe the structure of this 450 kDa complex, interactions between its components, and the organization of its catalytic RNA. We show that while the catalytic center of RNase MRP is inherited from the ancestral enzyme RNase P, the substrate binding pocket of RNase MRP is significantly altered by the addition of unique RNA and protein elements, as well as by RNA-driven protein remodeling. One Sentence Summary:Changes in peripheral RNA elements and RNA-driven protein remodeling result in diversification of related catalytic RNPs 2 Main Text:Ribonuclease (RNase) MRP, a site-specific endoribonuclease, is a ribonucleoprotein complex (RNP) comprising a catalytic RNA moiety and multiple (ten in S. cerevisiae) protein components (1-4). RNase MRP is an essential eukaryotic enzyme that has been found in practically all eukaryotes analyzed (5). RNase MRP is localized to the nucleolus and, transiently, to the cytoplasm (3). Known RNase MRP functions include its participation in the maturation of rRNA and in the metabolism of specific mRNAs involved in the regulation of the cell cycle (6-13).Defects in RNase MRP result in a range of pleiotropic developmental disorders in humans (14).RNase MRP is evolutionarily related to RNase P, a ribozyme-based RNP primarily involved in the maturation of tRNA (15)(16)(17). RNase MRP appears to have split from the RNase P lineage early in the evolution of eukaryotes, acquiring distinct substrate specificity and cellular functions (5,18,19).The catalytic (C-) domain of RNase MRP RNA (Fig. 1A) has the secondary structure closely resembling that of the C-domain of RNase P (Figs. 1B) and includes elements forming a highly conserved catalytic core (3-5). The specificity (S-) domain of RNase MRP RNA does not have any apparent similarities with the S-domain of RNase P (Figs 1A, B). Crosslinking studies (20) indicate the involvement of the RNase MRP S-domain in substrate recognition.Most of the RNase MRP protein components are also found in eukaryotic RNase P (2). S.cerevisiae RNase MRP and RNase P share 8 proteins (Pop1, and Rpp1 (2 copies); RNase MRP protein Snm1 has a homologue in RNase P (Rpr2), while Rmp1 3 is found only in RNase MRP. Shared proteins bind to both C-and S-domains (21-23). RNase MRP proteins Pop1, Pop6, Pop7 are also an essential part of yeast telomerase, where they form a structural module that stabilizes the binding of telomerase components Est1 and Est2 (24).Here, we report a cryo-EM structure of the S. cerevisiae RNase MRP holoenzyme solved to the nominal resolution of 3.0 Å. We reveal the overall architecture of the RNP, the structural organization of its catalytic RNA moiety, the substrate binding pocket of the enzyme, and interactions between RN...

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Section: One Sentence Summarymentioning

confidence: 99%

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confidence: 99%

Cryo-EM structure of catalytic ribonucleoprotein complex RNase MRP

Perederina

Lee

et al. 2020

Preprint

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“…In fact, it can tolerate single or even double mutations in its target sequences . This key enzymatic activity is found in virtually all organisms, though it is present in either a ribozyme‐based ribonucleoprotein or just as a protein enzyme in the cases of human mitochondria, plant organelles, and plant nuclei …”

Section: Review Of Identified Motifsmentioning

confidence: 99%

“…46,91 This key enzymatic activity is found in virtually all organisms, though it is present in either a ribozyme-based ribonucleoprotein or just as a protein enzyme in the cases of human mitochondria, plant organelles, and plant nuclei. [92][93][94] Sensitivity to RNase P is an accepted tool to detect tRNA-like elements in different RNAs, or at least a strong indication of their past presence in them. 95 Since the discovery of tRNA-like elements at the 3 end of plant viral RNA genomes, it has been observed that RNase P can recognize this type of structure, as it is the case with other tRNA-processing enzymes.…”

Section: Review Of Identified Motifsmentioning

confidence: 99%

The archaeology of coding RNA

Ariza-Mateos

Briones

Perales

et al. 2019

Annals of the New York Academy of Sciences

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Different theories concerning the origin of RNA (and, in particular, mRNA) point to the concatenation and expansion of proto‐tRNA−like structures. Different biochemical and biophysical tools have been used to search for ancient‐like RNA elements with a specific structure in genomic viral RNAs, including that of the hepatitis C virus, as well as in cellular mRNA populations, in particular those of human hepatocytes. We define this method as “archaeological,” and it has been designed to discover evolutionary patterns through a nonphylogenetic and nonrepresentational strategy. tRNA‐like elements were found in structurally or functionally relevant positions both in viral RNA and in one of the liver mRNAs examined, the antagonist interferon‐alpha subtype 5 (IFNA5) mRNA. Additionally, tRNA‐like elements are highly represented within the hepatic mRNA population, which suggests that they could have participated in the formation of coding RNAs in the distant past. Expanding on this finding, we have observed a recurring dsRNA‐like motif next to the tRNA‐like elements in both viral RNAs and IFNA5 mRNA. This suggested that the concatenation of these RNA motifs was an activity present in the RNA pools that might have been relevant in the RNA world. The extensive alteration of sequences that likely triggered the transition from the predecessors of coding RNAs to the first fully functional mRNAs (which was not the case in the stepwise construction of noncoding rRNAs) hinders the phylogeny‐based identification of RNA elements (both sequences and structures) that might have been active before the advent of protein synthesis. Therefore, our RNA archaeological method is presented as a way to better understand the structural/functional versatility of a variety of RNA elements, which might represent “the losers” in the process of RNA evolution as they had to adapt to the selective pressures favoring the coding capacity of the progressively longer mRNAs.

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“…Here, we continue our investigation of Rpp29 function in H3.3 chromatin assembly. RNase P is an endoribonuclease found in all three domains of life as either a ribozyme-centered ribonucleoprotein (RNP) or a protein-only enzyme, which is essential for cleaving the 5Ј leader sequence from precursor tRNAs (41,42). In its RNP form, RNase P is composed of a single catalytic RNA and up to nine protein subunits.…”

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Rpp29 regulates histone H3.3 chromatin assembly through transcriptional mechanisms

Shastrula

Lund

Garcia

et al. 2018

Journal of Biological Chemistry

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The histone H3 variant H3.3 is a highly conserved and dynamic regulator of chromatin organization. Therefore, fully elucidating its nucleosome incorporation mechanisms is essential to understanding its functions in epigenetic inheritance. We previously identified the RNase P protein subunit, Rpp29, as a repressor of H3.3 chromatin assembly. Here, we use a biochemical assay to show that Rpp29 interacts with H3.3 through a sequence element in its own N terminus, and we identify a novel interaction with histone H2B at an adjacent site. The fact that archaeal Rpp29 does not include this N-terminal region suggests that it evolved to regulate eukaryote-specific functions. Oncogenic H3.3 mutations alter the H3.3-Rpp29 interaction, which suggests that they could dysregulate Rpp29 function in chromatin assembly. We also used KNS42 cells, an H3.3(G34V) pediatric high-grade glioma cell line, to show that Rpp29 1) represses H3.3 incorporation into transcriptionally active protein-coding, rRNA, and tRNA genes; 2) represses mRNA, protein expression, and antisense RNA; and 3) represses euchromatic post-translational modifications (PTMs) and promotes heterochromatic PTM deposition ( histone H3 Lys-9 trimethylation (H3K9me3) and H3.1/2/3K27me3). Notably, we also found that K27me2 is increased and K36me1 decreased on H3.3(G34V), which suggests that Gly-34 mutations dysregulate Lys-27 and Lys-36 methylation in The fact that Rpp29 represses H3.3 chromatin assembly and sense and antisense RNA and promotes H3K9me3 and H3K27me3 suggests that Rpp29 regulates H3.3-mediated epigenetic mechanisms by processing a transcribed signal that recruits H3.3 to its incorporation sites.

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Chance and necessity in the evolution of RNase P

Cited by 28 publications

References 48 publications

Cryo-EM structure of catalytic ribonucleoprotein complex RNase MRP

Cryo-EM structure of catalytic ribonucleoprotein complex RNase MRP

The archaeology of coding RNA

Rpp29 regulates histone H3.3 chromatin assembly through transcriptional mechanisms

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