Diverse and pervasive subcellular distributions for both coding and long noncoding RNAs

Wilk, Ronit; Hu, Jiantao; Blotsky, Dmitry; Krause, Henry M.

doi:10.1101/gad.276931.115

Cited by 118 publications

(136 citation statements)

References 66 publications

(75 reference statements)

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“…Although Dpp activity is known to be present in the larval midgut [21][22][23][24], the function of Dpp in this tissue remains unknown. To examine the spatial localization of Dpp we used dpp-GAL4 to drive expression of UAS-GFP (dpp > GFP), which revealed distinct GFP-positive cells in the midgut (Figs.…”

Section: Dpp Signaling In the Larval Midgut Blocks Degradationmentioning

confidence: 99%

Dpp regulates autophagy-dependent midgut removal and signals to block ecdysone production

Denton

Dayan

et al. 2018

Cell Death Differ

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Animal development and homeostasis require the programmed removal of cells. Autophagy-dependent cell deletion is a unique form of cell death often involved in bulk degradation of tissues. In Drosophila the steroid hormone ecdysone controls developmental transitions and triggers the autophagy-dependent removal of the obsolete larval midgut. The production of ecdysone is exquisitely coordinated with signals from numerous organ systems to mediate the correct timing of such developmental programs. Here we report an unexpected role for the Drosophila bone morphogenetic protein/transforming growth factor β ligand, Decapentaplegic (Dpp), in the regulation of ecdysone-mediated midgut degradation. We show that blocking Dpp signaling induces premature autophagy, rapid cell death, and midgut degradation, whereas sustained Dpp signaling inhibits autophagy induction. Furthermore, Dpp signaling in the midgut prevents the expression of ecdysone responsive genes and impairs ecdysone production in the prothoracic gland. We propose that Dpp has dual roles: one within the midgut to prevent improper tissue degradation, and one in interorgan communication to coordinate ecdysone biosynthesis and developmental timing.

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Section: Dpp Signaling In the Larval Midgut Blocks Degradationmentioning

confidence: 99%

Dpp regulates autophagy-dependent midgut removal and signals to block ecdysone production

Denton

Dayan

et al. 2018

Cell Death Differ

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“…APC/C components are consistently expressed in post-mitotic, differentiating cells in Drosophila : for example, Fzr/Cdh1 and APC1/Shtd are expressed at higher levels after cell cycle exit in developing eye discs posterior to the MF (Pimentel and Venkatesh, 2005; Tanaka-Matakatsu et al, 2007). In addition, Fzr/Cdh1 is also expressed in wing tissue of 24 and 38hrs old pupae (Buttitta et al, 2010; and Fly-FISH: Lecuyer et al, 2007; Wilk et al, 2016). Therefore, we first wanted to confirm with several APC/C subunits and its co-activators whether the entire complex and its enzymatic activity affected PCP in post-mitotic cells.…”

Section: Resultsmentioning

confidence: 99%

APC/CFzr/Cdh1-Dependent Regulation of Planar Cell Polarity Establishment via Nek2 Kinase Acting on Dishevelled

Weber

Mlodzik

2017

Developmental Cell

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The Anaphase Promoting Complex/Cyclosome (APC/C) is an E3 ubiquitin ligase, well known for its role in cell cycle progression. However, it has been linked to additional functions, mainly in neuronal contexts, when using the co-activator Cdh1/Fzr. Here, our data indicate a post-mitotic requirement for the APC/CFzr/Cdh1 in epithelial cell patterning and planar cell polarity (PCP) in Drosophila. PCP signalling is critical for development by establishing cellular asymmetries and orientation within the plane of an epithelium, via differential localization of distinct complexes of core PCP factors. Loss of APC/C function leads to reduced Dishevelled (Dsh) levels, a core PCP factor. The effect of APC/C on Dsh is mediated by Nek2 kinase, which can phosphorylate Dsh and is a direct APC/CFzr/Cdh1 substrate. We have thus uncovered a pathway of regulation whereby APC/CFzr/Cdh1 negatively regulates Nek2, which negatively regulates Dsh, to ensure its proper stoichiometric requirement and localization during PCP establishment.

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“…With the accumulation of comprehensive studies using high‐throughput imaging or subcellular transcriptomics profiling to assess RNA distribution features on a transcriptome‐wide scale, RNA localization has emerged as a highly prevalent regulatory step in the control of gene expression . For example, large‐scale fluorescent in situ hybridization studies on Drosophila oocytes and embryos showed that a large proportion of mRNAs and long noncoding RNAs (lncRNA) exhibit precise localization to specific organelles and subcellular structures (e.g., plasma membrane, mitotic apparatus, cell junctions, subnuclear domains), emphasizing the high prevalence of this mechanism . Moreover, a large number of studies have employed biochemical purification and RNA expression profiling strategies to characterize organelle‐enriched RNA populations, including both coding and noncoding RNA species .…”

Section: Biological Functions and Prevalence Of Rna Localizationmentioning

confidence: 99%

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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Diverse and pervasive subcellular distributions for both coding and long noncoding RNAs

Cited by 118 publications

References 66 publications

Dpp regulates autophagy-dependent midgut removal and signals to block ecdysone production

Dpp regulates autophagy-dependent midgut removal and signals to block ecdysone production

APC/CFzr/Cdh1-Dependent Regulation of Planar Cell Polarity Establishment via Nek2 Kinase Acting on Dishevelled

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

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