A translation-independent role of oskar RNA in early Drosophila oogenesis

University of Cambridge, Cambridge, England, United Kingdom
Development (Impact Factor: 6.46). 09/2006; 133(15):2827-33. DOI: 10.1242/dev.02456
Source: PubMed


The Drosophila maternal effect gene oskar encodes the posterior determinant responsible for the formation of the posterior pole plasm in the egg, and thus of the abdomen and germline of the future fly. Previously identified oskar mutants give rise to offspring that lack both abdominal segments and a germline, thus defining the ;posterior group phenotype'. Common to these classical oskar alleles is that they all produce significant amounts of oskar mRNA. By contrast, two new oskar mutants in which oskar RNA levels are strongly reduced or undetectable are sterile, because of an early arrest of oogenesis. This egg-less phenotype is complemented by oskar nonsense mutant alleles, as well as by oskar transgenes, the protein-coding capacities of which have been annulled. Moreover, we show that expression of the oskar 3' untranslated region (3'UTR) is sufficient to rescue the egg-less defect of the RNA null mutant. Our analysis thus reveals an unexpected role for oskar RNA during early oogenesis, independent of Oskar protein. These findings indicate that oskar RNA acts as a scaffold or regulatory RNA essential for development of the oocyte.

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Available from: Andreas Jenny, Jan 30, 2014
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    • "Hence, it was important to determine the exact signal mediating transport of oskar mRNA from the nurse cells into the oocyte. It was previously shown that the 3 ′ UTR is sufficient for oskar mRNA accumulation in the oocyte (Jenny et al. 2006). To identify the minimal region mediating this early transport step, we generated transgenic flies expressing variants of the full-length oskar 3 ′ UTR (Fig. 1A) fused to the open reading frame of Enhanced Green Fluorescent Protein (EGFP). "
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    ABSTRACT: mRNA transport coupled with translational control underlies the intracellular localization of many proteins in eukaryotic cells. This is exemplified in Drosophila, where oskar mRNA transport and translation at the posterior pole of the oocyte direct posterior patterning of the embryo. oskar localization is a multistep process. Within the oocyte, a spliced oskar localization element (SOLE) targets oskar mRNA for plus end-directed transport by kinesin-1 to the posterior pole. However, the signals mediating the initial minus end-directed, dynein-dependent transport of the mRNA from nurse cells into the oocyte have remained unknown. Here, we show that a 67-nt stem-loop in the oskar 3' UTR promotes oskar mRNA delivery to the developing oocyte and that it shares functional features with the fs(1)K10 oocyte localization signal. Thus, two independent cis-acting signals, the oocyte entry signal (OES) and the SOLE, mediate sequential dynein- and kinesin-dependent phases of oskar mRNA transport during oogenesis. The OES also promotes apical localization of injected RNAs in blastoderm stage embryos, another dynein-mediated process. Similarly, when ectopically expressed in polarized cells of the follicular epithelium or salivary glands, reporter RNAs bearing the oskar OES are apically enriched, demonstrating that this element promotes mRNA localization independently of cell type. Our work sheds new light on how oskar mRNA is trafficked during oogenesis and the RNA features that mediate minus end-directed transport.
    Preview · Article · Feb 2014 · RNA
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    • "The example of LDMAR thus links regulation of gametogenesis by an lncRNA to organismal fertility. In the fruit fly Drosophila melanogaster, oogenesis is regulated by the oskar RNA, which has dual coding and noncoding functions (Jenny et al. 2006). Loss of oskar results in sterility due to early arrest of oocyte differentiation, a phenotype that can be rescued by expression of mutant oskar with a disrupted translation capacity. "
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    ABSTRACT: Long noncoding RNAs (lncRNAs) are transcripts longer than 200 nucleotides that do not have functional protein-coding capacity. They can regulate gene expression by affecting the transcription, translation, and stability of mRNA targets through diverse mechanisms. Dozens of eukaryotic lncRNAs have been functionally characterized to date, and they have been associated with important cellular processes such as meiosis, pluripotency, apoptosis, and lineage specification. An emerging theme among known lncRNA functions is therefore the modulation of cell differentiation states, often in response to developmental or environmental cues. This chapter discusses current models of lncRNA function during several well-characterized cell differentiation processes, from yeast to human, highlighting recent evidence that implicate lncRNAs in the regulation of animal development. © 2013 Springer Science+Business Media New York. All rights are reserved.
    Full-text · Chapter · Nov 2013
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    • "In Drosophila, oskar RNA was first characterized as a determinant responsible for formation of the posterior pole plasm in the egg, and thus, formation of the abdomen and germline of the future fly (Markussen et al. 1995). It has since been found that, independent of the protein, oskar mRNA—more specifically its 3′ UTR—has a function that is essential for the completion of oogenesis (Jenny et al. 2006). Recently, Pathak et al. (2013) described transcripts of several hundred nucleotides from the AAGAG repeats of the pericentromeric regions of Drosophila which appear to be critical components of the nuclear matrix. "
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    ABSTRACT: The study of long noncoding RNAs (lncRNAs) is still in its infancy with more putative RNAs identified than those with ascribed functions. Defined as transcripts that are longer than 200 nucleotides without a coding sequence, their numbers are on the rise and may well challenge protein coding transcripts in number and diversity. lncRNAs are often expressed at low levels and their sequences are frequently poorly conserved, making it unclear if they are transcriptional noise or bonafide effectors. Despite these limitations, inroads into their functions are being made and it is clear they make a contribution in regulating all aspects of biology. The early verdict on their activity, however, suggests the majority function as chromatin modifiers. A good proportion show a connection to disease highlighting their importance and the need to determine their function. The focus of this review is on lncRNAs which influence developmental processes which in itself covers a large range of known activities.
    Full-text · Article · Oct 2013 · Chromosome Research
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