Tudor staphylococcal nuclease is a structure-specific ribonuclease that degrades RNA at unstructured regions during microRNA decay

Li, Chia-Lung; Yang, Wei‐Zen; Shi, Zhonghao; Yuan, Hanna S.

doi:10.1261/rna.064501.117

Cited by 13 publications

(14 citation statements)

References 41 publications

(49 reference statements)

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“…11 b). The resulting domain fusion of Tudor and SNase (hence the name “extended Tudor”) became the ancestor of the eTudor family, in which the catalytic residues from the ancestral SNase domain are mutated, likely rendering it inactive [ 59 , 70 , 71 , 74 ] (Fig. 11 b).…”

Section: Resultsmentioning

confidence: 99%

Modified base-binding EVE and DCD domains: striking diversity of genomic contexts in prokaryotes and predicted involvement in a variety of cellular processes

2020

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Background DNA and RNA of all cellular life forms and many viruses contain an expansive repertoire of modified bases. The modified bases play diverse biological roles that include both regulation of transcription and translation, and protection against restriction endonucleases and antibiotics. Modified bases are often recognized by dedicated protein domains. However, the elaborate networks of interactions and processes mediated by modified bases are far from being completely understood. Results We present a comprehensive census and classification of EVE domains that belong to the PUA/ASCH domain superfamily and bind various modified bases in DNA and RNA. We employ the “guilt by association” approach to make functional inferences from comparative analysis of bacterial and archaeal genomes, based on the distribution and associations of EVE domains in (predicted) operons and functional networks of genes. Prokaryotes encode two classes of EVE domain proteins, slow-evolving and fast-evolving ones. Slow-evolving EVE domains in α-proteobacteria are embedded in conserved operons, potentially involved in coupling between translation and respiration, cytochrome c biogenesis in particular, via binding 5-methylcytosine in tRNAs. In β- and γ-proteobacteria, the conserved associations implicate the EVE domains in the coordination of cell division, biofilm formation, and global transcriptional regulation by non-coding 6S small RNAs, which are potentially modified and bound by the EVE domains. In eukaryotes, the EVE domain-containing THYN1-like proteins have been reported to inhibit PCD and regulate the cell cycle, potentially, via binding 5-methylcytosine and its derivatives in DNA and/or RNA. We hypothesize that the link between PCD and cytochrome c was inherited from the α-proteobacterial and proto-mitochondrial endosymbiont and, unexpectedly, could involve modified base recognition by EVE domains. Fast-evolving EVE domains are typically embedded in defense contexts, including toxin-antitoxin modules and type IV restriction systems, suggesting roles in the recognition of modified bases in invading DNA molecules and targeting them for restriction. We additionally identified EVE-like prokaryotic Development and Cell Death (DCD) domains that are also implicated in defense functions including PCD. This function was inherited by eukaryotes, but in animals, the DCD proteins apparently were displaced by the extended Tudor family proteins, whose partnership with Piwi-related Argonautes became the centerpiece of the Piwi-interacting RNA (piRNA) system. Conclusions Recognition of modified bases in DNA and RNA by EVE-like domains appears to be an important, but until now, under-appreciated, common denominator in a variety of processes including PCD, cell cycle control, antivirus immunity, stress response, and germline development in animals.

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Section: Resultsmentioning

confidence: 99%

Modified base-binding EVE and DCD domains: striking diversity of genomic contexts in prokaryotes and predicted involvement in a variety of cellular processes

2020

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“…The invariant domain composition of SND1 comprises a tandem of four SN-like domains at the N-terminus (SN1-4) followed by a C-terminal domain formed by a fusion of a Tudor domain and a truncated SN domain (5) (Figure 1). The potent interaction capacity of SN domains with RNA (6) and of the Tudor domain with modified (methylated) aminoacids (7, 8), together with its intrinsic endonuclease activity (9) for degrading double-stranded RNA (10) enable SND1 for participating in an unusual multiplicity of functions (summarized in Figure 1). We refer the reader to some recent reviews addressing the biochemistry and function of this protein (11–13).…”

Section: Introductionmentioning

confidence: 99%

Insights Into SND1 Oncogene Promoter Regulation

2018

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The staphylococcal nuclease and Tudor domain containing 1 gene (SND1), also known as Tudor-SN, TSN or p100, encodes an evolutionarily conserved protein with invariant domain composition. SND1 contains four repeated staphylococcal nuclease domains and a single Tudor domain, which confer it endonuclease activity and extraordinary capacity for interacting with nucleic acids, individual proteins and protein complexes. Originally described as a transcriptional coactivator, SND1 plays fundamental roles in the regulation of gene expression, including RNA splicing, interference, stability, and editing, as well as in the regulation of protein and lipid homeostasis. Recently, SND1 has gained attention as a potential disease biomarker due to its positive correlation with cancer progression and metastatic spread. Such functional diversity of SND1 marks this gene as interesting for further analysis in relation with the multiple levels of regulation of SND1 protein production. In this review, we summarize the SND1 genomic region and promoter architecture, the set of transcription factors that can bind the proximal promoter, and the evidence supporting transactivation of SND1 promoter by a number of signal transduction pathways operating in different cell types and conditions. Unraveling the mechanisms responsible for SND1 promoter regulation is of utmost interest to decipher the SND1 contribution in the realm of both normal and abnormal physiology.

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“…The activity of MC1 is mainly regulated at the gene expression level and a wide range of abiotic and biotic stresses induce MC1 (Kwon and Hwang ). TSN1 ( Tudor‐domain proteins 1 ) is an RNA‐binding protein that performs several different functions, including activation of transcription, RNA transport and localization, mRNA splicing and regulation of RNA silencing (Li et al ). There are no reports, to our knowledge, on the roles of MC1 and TNS1 in a gene network context of barley drought stress responses.…”

Section: Discussionmentioning

confidence: 99%

Plausible association between drought stress tolerance of barley (Hordeum vulgare L.) and programmed cell death via MC1 and TSN1 genes

Shamloo‐Dashtpagerdi¹,

Lindlöf

Aliakbari

et al. 2020

Physiologia Plantarum

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Studying the drought-responsive transcriptome is of high interest as it can serve as a blueprint for stress adaptation strategies. Despite extensive studies in this area, there are still many details to be uncovered, such as the importance of each gene involved in the stress response as well as the relationship between these genes and the physiochemical processes governing stress tolerance. This study was designed to address such important details and to gain insights into molecular responses of barley (Hordeum vulgare L.) to drought stress. To that, we combined RNA-seq data analysis with field and greenhouse drought experiments in a systems biology approach. RNA-sequence analysis identified a total of 665 differentially expressed genes (DEGs) belonging to diverse functional categories. A gene network was derived from the DEGs, which comprised of a total of 131 nodes and 257 edges. Gene network topology analysis highlighted two programmed cell death (PCD) modulating genes, MC1 (metacaspase 1) and TSN1 (Tudor-SN 1), as important (hub) genes in the predicted network. Based on the field trial, a drought-tolerant and a drought-susceptible barley genotype was identified from eight tested cultivars. Identified genotypes exhibited different physiochemical characteristics, including proline content, chlorophyll concentration, percentage of electrolyte leakage and malondialdehyde content as well as expression profiles of MC1 and TSN1 genes. Machine learning and correspondence analysis revealed a significant relationship between drought tolerance and measured characteristics in the context of PCD. Our study provides new insights which bridge barley drought tolerance to PCD through MC1 and TSN1 pathway.

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Tudor staphylococcal nuclease is a structure-specific ribonuclease that degrades RNA at unstructured regions during microRNA decay

Cited by 13 publications

References 41 publications

Modified base-binding EVE and DCD domains: striking diversity of genomic contexts in prokaryotes and predicted involvement in a variety of cellular processes

Modified base-binding EVE and DCD domains: striking diversity of genomic contexts in prokaryotes and predicted involvement in a variety of cellular processes

Insights Into SND1 Oncogene Promoter Regulation

Plausible association between drought stress tolerance of barley (Hordeum vulgare L.) and programmed cell death via MC1 and TSN1 genes

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