Adenylation of Maternally Inherited MicroRNAs by Wispy

Lee, Mihye; Choi, Yeon; Kim, Ki Jun; Jin, Hua; Lim, Ju Young; Nguyen, Tuan Anh; Yang, Jian; Jeong, Minsun; Giráldez, Antonio J.; Ye, Hui; Patel, Dinshaw J.; Kim, V. Narry

doi:10.1016/j.molcel.2014.10.011

Cited by 91 publications

(118 citation statements)

References 64 publications

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“…In addition, our decay rates were similar to those measured by others in different systems (Krol et al 2010a;Rissland et al 2011). Nonetheless, we cannot exclude significant changes in miRNA stability in specific physiopathological contexts, as observed for maternal miRNAs during embryogenesis (Lee et al 2014). …”

Section: Discussion Mirna Degradation Dynamics Are Heterogeneoussupporting

confidence: 82%

“…5H) and might, therefore, be ascribed to the nuclear terminal uridylyl transferases (TUTases) (Krol et al 2010b;Lin and Gregory 2015). Conversely, adenylation, the most frequent tailing event, was similar among 5p and 3p miRNAs and likely occurs in the cytosol, as previously suggested (Lee et al 2014). Indeed, target-induced nontemplated nucleotide addition (tailing) is believed to occur in the cytosol, while miRNAs are bound to AGO2 (De et al 2013;de la Mata et al 2015).…”

Section: Fast Decaying Mirnas Are Enriched In Tailed and Trimmed Isofmentioning

confidence: 54%

“…Some reports suggested that slow turnover might not be a general feature of miRNAs and, in some instances, miRNA decay could be relatively fast (few hours), such as for miR-503 in fibroblasts (Rissland et al 2011), miR-29b during mitosis (Hwang et al 2007), and several neuronal miRNAs (Krol et al 2010a). The degradation dynamics of miRNAs and the mechanisms involved remain largely obscure, in particular in mammals, and apparently involve enzymatic activities able to modify miRNA ends by adding ("tailing") or removing ("trimming") nucleotides (Ramachandran and Chen 2008;Chatterjee and Grosshans 2009;Ameres et al 2010;Kim et al 2010;Burns et al 2011;Neilsen et al 2012;Ruegger and Grosshans 2012;Lee et al 2014). A target-dependent mechanism has also been identified, in which turnover is mediated by the interaction of miRNAs with their mRNA targets, promoting miRNA unloading from AGO and degradation (Baccarini et al 2011;Ruegger and Grosshans 2012;De et al 2013;de la Mata et al 2015).…”

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confidence: 99%

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Degradation dynamics of microRNAs revealed by a novel pulse-chase approach

et al. 2016

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The regulation of miRNAs is critical to the definition of cell identity and behavior in normal physiology and disease. To date, the dynamics of miRNA degradation and the mechanisms involved in remain largely obscure, in particular, in higher organisms. Here, we developed a pulse-chase approach based on metabolic RNA labeling to calculate miRNA decay rates at genome-wide scale in mammalian cells. Our analysis revealed heterogeneous miRNA half-lives, with many species behaving as stable molecules (T 1/2 > 24 h), while others, including passenger miRNAs and a number (25/129) of guide miRNAs, are quickly turned over (T 1/2 = 4-14 h). Decay rates were coupled with other features, including genomic organization, transcription rates, structural heterogeneity (isomiRs), and target abundance, measured through quantitative experimental approaches. This comprehensive analysis highlighted functional mechanisms that mediate miRNA degradation, as well as the importance of decay dynamics in the regulation of the miRNA pool under both steady-state conditions and during cell transitions.

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Section: Discussion Mirna Degradation Dynamics Are Heterogeneoussupporting

confidence: 82%

Section: Fast Decaying Mirnas Are Enriched In Tailed and Trimmed Isofmentioning

confidence: 54%

mentioning

confidence: 99%

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Degradation dynamics of microRNAs revealed by a novel pulse-chase approach

et al. 2016

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“…1A; Kwak et al 2008). Recent data showed that in addition to mRNA adenylation, WISPY adenylates miRNAs in S2 cells leading to a reduction of miRNA levels (Lee et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Nucleotide specificity of the human terminal nucleotidyltransferase Gld2 (TUT2)

Chung

Heinemann

2016

RNA

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The nontemplated addition of single or multiple nucleotides to RNA transcripts is an efficient means to control RNA stability and processing. Cytoplasmic RNA adenylation and the less well-known uridylation are post-transcriptional mechanisms regulating RNA maturation, activity, and degradation. Gld2 is a member of the noncanonical poly(A) polymerases, which include enzymes with varying nucleotide specificity, ranging from strictly ATP to ambiguous to exclusive UTP adding enzymes. Human Gld2 has been associated with transcript stabilizing miRNA monoadenylation and cytoplasmic mRNA polyadenylation. Most recent data have uncovered an unexpected miRNA uridylation activity, which promotes miRNA maturation. These conflicting data raise the question of Gld2 nucleotide specificity. Here, we biochemically characterized human Gld2 and demonstrated that it is a bona fide adenylyltransferase with only weak activity toward other nucleotides. Despite its sequence similarity with uridylyltransferases (TUT4, TUT7), Gld2 displays an 83-fold preference of ATP over UTP. Gld2 is a promiscuous enzyme, with activity toward miRNA, pre-miRNA, and polyadenylated RNA substrates. Apo-Gld2 activity is restricted to adding single nucleotides and processivity likely relies on additional RNA-binding proteins. A phylogeny of the PAP/TUTase superfamily suggests that uridylyltransferases, which are derived from distinct adenylyltransferase ancestors, arose multiple times during evolution via insertion of an active site histidine. A corresponding histidine insertion into the Gld2 active site alters substrate specificity from ATP to UTP.

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“…The D. melanogaster genome contains seven genes encoding members of this enzyme family, either previously characterized experimentally or inferred from the sequence: CG1091, CG11265 (Trf4-1) (Nakamura et al 2008), CG7163 (monkey king protein; mkg-p), CG5732 (Gld2) ), CG11418, CG17462 (Trf4-2) (Nakamura et al 2008) and CG15737 (wispy; wisp) (Benoit et al 2008;Cui et al 2008;Lee et al 2014b). Coding sequences for all except wispy could be amplified from S2 cell RNA.…”

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confidence: 99%

Oligoadenylation of 3′ decay intermediates promotes cytoplasmic mRNA degradation in Drosophila cells

Harnisch

Cuzic-Feltens

Dohm

et al. 2016

RNA

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Post-transcriptional 3′ end addition of nucleotides is important in a variety of RNA decay pathways. We have examined the 3 ′ end addition of nucleotides during the decay of the Hsp70 mRNA and a corresponding reporter RNA in Drosophila S2 cells by conventional sequencing of cDNAs obtained after mRNA circularization and by deep sequencing of dedicated libraries enriched for 3 ′ decay intermediates along the length of the mRNA. Approximately 5%-10% of 3 ′ decay intermediates carried nonencoded oligo(A) tails with a mean length of 2-3 nucleotides. RNAi experiments showed that the oligoadenylated RNA fragments were intermediates of exosomal decay and the noncanonical poly(A) polymerase Trf4-1 was mainly responsible for A addition. A hot spot of A addition corresponded to an intermediate of 3′ decay that accumulated upon inhibition of decapping, and knockdown of Trf4-1 increased the abundance of this intermediate, suggesting that oligoadenylation facilitates 3 ′ decay. Oligoadenylated 3 ′ decay intermediates were found in the cytoplasmic fraction in association with ribosomes, and fluorescence microscopy revealed a cytoplasmic localization of Trf4-1. Thus, oligoadenylation enhances exosomal mRNA degradation in the cytoplasm.

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Adenylation of Maternally Inherited MicroRNAs by Wispy

Cited by 91 publications

References 64 publications

Degradation dynamics of microRNAs revealed by a novel pulse-chase approach

Degradation dynamics of microRNAs revealed by a novel pulse-chase approach

Nucleotide specificity of the human terminal nucleotidyltransferase Gld2 (TUT2)

Oligoadenylation of 3′ decay intermediates promotes cytoplasmic mRNA degradation in Drosophila cells

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