Nucleo-cytosolic Shuttling of ARGONAUTE1 Prompts a Revised Model of the Plant MicroRNA Pathway

Bologna, Nicolas Gerardo; Iselin, Raphael; Abriata, Luciano A.; Sarazin, Alexis; Pumplin, Nathan; Jay, Florence; Grentzinger, Thomas; Peraro, Matteo Dal; Voinnet, Olivier

doi:10.1016/j.molcel.2018.01.007

Cited by 208 publications

(226 citation statements)

References 77 publications

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“…These miRNAs are transferred to the cytoplasm by HASTY, a homologue of Exportin-5 [18,19]. However, a revised model has recently been put forward where miRNAs are loaded onto AGO1 whereafter the complex is transported out of the nucleus by a HASTY-independent pathway [20]. …”

Section: Introductionmentioning

confidence: 99%

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

et al. 2018

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Micro (mi)RNAs regulate gene expression in many eukaryotic organisms where they control diverse biological processes. Their biogenesis, from primary transcripts to mature miRNAs, have been extensively characterized in animals and plants, showing distinct differences between these phylogenetically distant groups of organisms. However, comparably little is known about miRNA biogenesis in organisms whose evolutionary position is placed in between plants and animals and/or in unicellular organisms. Here, we investigate miRNA maturation in the unicellular amoeba Dictyostelium discoideum, belonging to Amoebozoa, which branched out after plants but before animals. High-throughput sequencing of small RNAs and poly(A)-selected RNAs demonstrated that the Dicer-like protein DrnB is required, and essentially specific, for global miRNA maturation in D. discoideum. Our RNA-seq data also showed that longer miRNA transcripts, generally preceded by a T-rich putative promoter motif, accumulate in a drnB knock-out strain. For two model miRNAs we defined the transcriptional start sites (TSSs) of primary (pri)-miRNAs and showed that they carry the RNA polymerase II specific m7G-cap. The generation of the 3ʹ-ends of these pri-miRNAs differs, with pri-mir-1177 reading into the downstream gene, and pri-mir-1176 displaying a distinct end. This 3´-end is processed to shorter intermediates, stabilized in DrnB-depleted cells, of which some carry a short oligo(A)-tail. Furthermore, we identified 10 new miRNAs, all DrnB dependent and developmentally regulated. Thus, the miRNA machinery in D. discoideum shares features with both plants and animals, which is in agreement with its evolutionary position and perhaps also an adaptation to its complex lifestyle: unicellular growth and multicellular development.

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Section: Introductionmentioning

confidence: 99%

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

et al. 2018

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“…After cutting the pri‐miRNA, the processing machinery releases a double‐stranded miRNA of approximately 21 nt with 2‐nt 3′ overhangs (an miRNA/miRNA* duplex). This molecule is loaded to an AGO protein, generally AGO1, with the aid of HFSP90 (Iki et al ., ; Zhang et al ., 2014b; Bologna et al ., ). AGO1 then retains one strand and releases the other, commonly the miRNA*.…”

Section: Microrna Processing In Plantsmentioning

confidence: 97%

“…The mechanisms for strand selection of miRNA over miRNA* and AGO loading are not yet fully understood in plants; however, the structure of the duplex and the identity of the 5′ base (reviewed in Fang and Qi, ), as well as HYL1 (Eamens et al ., ), have been shown to be important for the selection of the miRNA strand. It has been recently proposed that empty AGO1 is localized in the nucleus, but after loading of the miRNA a conformational change exposes a nuclear export signal, so that the AGO1‐miRNA complex moves to the cytoplasm where it exerts its function (Bologna et al ., ). Thus, all steps of miRNA biogenesis seem to occur in the plant nucleus.…”

Section: Microrna Processing In Plantsmentioning

confidence: 97%

Keep calm and carry on: miRNA biogenesis under stress

2019

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Summary MicroRNAs (miRNAs) are major post‐transcriptional regulators of gene expression. Their biogenesis relies on the cleavage of longer precursors by a nuclear localized processing machinery. The evolutionary preference of plant miRNAs to silence transcription factors turned these small molecules into key actors during growth and adaptive responses. Furthermore, during their life cycle plants are subject to changes in the environmental conditions surrounding them. In order to face these changes, plants display unique adaptive capacities based on an enormous developmental plasticity, where miRNAs play central roles. Many individual miRNAs have been shown to modulate the plant response to different environmental cues and stresses. In the last few years, increasing evidence has shown that not only individual genes encoding miRNAs but also the miRNA pathway as a whole is subject to regulation in response to external stimulus. In this review, we discuss the current knowledge about the miRNA pathway. We dissect the pathway to analyze the events leading to the generation of these small RNAs and emphasize the regulation of core components of the miRNA biogenesis machinery.

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“…C), as has been shown for Neat‐1 in paraspeckle formation . On the other hand, miRNAs constitute part of the miRISC complex, along with their associated effectors, Argonaute proteins, another trans‐ acting‐binding partner . Loaded miRNAs bind target transcripts through partial or full antisense base–pairing interactions to destabilize or silence their translation .…”

Section: Mechanisms Of Rna Localizationmentioning

confidence: 82%

Biological functions, regulatory mechanisms, and disease relevance of RNA localization pathways

et al. 2018

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The asymmetric subcellular distribution of RNA molecules from their sites of transcription to specific compartments of the cell is an important aspect of post-transcriptional gene regulation. This involves the interplay of intrinsic cis-regulatory elements within the RNA molecules with trans-acting RNAbinding proteins and associated factors. Together, these interactions dictate the intracellular localization route of RNAs, whose downstream impacts have wide-ranging implications in cellular physiology. In this review, we examine the mechanisms underlying RNA localization and discuss their biological significance. We also review the growing body of evidence pointing to aberrant RNA localization pathways in the development and progression of diseases.Keywords: Cis-regulatory elements; RNA disease; RNA localization; RNA-binding proteinsThe asymmetric organization of cells is a pervasive feature that ensures the homeostasis of prokaryotic and eukaryotic organisms. This relies on the capacity of cells to organize their contents, including lipids, nucleic acids, and proteins, into specific subcellular structures and organelles. While much of this organization has been attributed to subcellular protein transport [1], a growing body of work indicates that the regulated localization of RNA molecules is also a key process observed across evolutionary timescales [2][3][4][5][6]. This form of post-transcriptional regulation where coding and noncoding RNA molecules actively associate with trans-acting partners, such as RNA-binding proteins (RBPs), serves to dictate both the function and intra-or extracellular destiny of the RNA. During RNA localization, cis-regulatory elements found within the RNA molecule, whether coding or noncoding, act as recognition sites for the recruitment of trans-acting RBPs, which dictate the intra-/extra-cellular fate of the RNA and, ultimately, its functional state. Over the years, the wide-ranging implications of RNA localization on cellular physiology have become apparent, affecting many aspects of cell organization and function. Indeed, RNA localization pathways have been linked to numerous important processes, including developmental patterning, cell polarity, spindle assembly, formation of nonmembranous compartments, localized translation, and cell motility [2][3][4][5][6].

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Nucleo-cytosolic Shuttling of ARGONAUTE1 Prompts a Revised Model of the Plant MicroRNA Pathway

Cited by 208 publications

References 77 publications

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum

Keep calm and carry on: miRNA biogenesis under stress

Biological functions, regulatory mechanisms, and disease relevance of RNA localization pathways

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