Translational Regulation and RNA Localization in <i>Drosophila</i> Oocytes and Embryos

Johnstone, Oona; Lasko, Paul

doi:10.1146/annurev.genet.35.102401.090756

Cited by 305 publications

(227 citation statements)

References 256 publications

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“…These patterns range from nuclear accumulation during the early cleavage stages to the enrichment at the boundary between adjacent myotubes. Studies of mRNA localization patterns of protein-coding genes in yeast (e.g., ASH1) (Long et al 1997) and flies (e.g., bicoid, oskar, gurken) (for review, see Johnstone and Lasko 2001) have shown that the subcellular localization of specific RNAs is essential for normal development. Thus, enrichment of lncRNAs in specific subcellular compartments may be of fundamental importance for the regulatory functions of ncRNAs.…”

Section: Discussionmentioning

confidence: 99%

Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis

Pauli¹,

Valen²,

Lin³

et al. 2011

Genome Res.

739

830

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Long noncoding RNAs (lncRNAs) comprise a diverse class of transcripts that structurally resemble mRNAs but do not encode proteins. Recent genome-wide studies in humans and the mouse have annotated lncRNAs expressed in cell lines and adult tissues, but a systematic analysis of lncRNAs expressed during vertebrate embryogenesis has been elusive. To identify lncRNAs with potential functions in vertebrate embryogenesis, we performed a time-series of RNA-seq experiments at eight stages during early zebrafish development. We reconstructed 56,535 high-confidence transcripts in 28,912 loci, recovering the vast majority of expressed RefSeq transcripts while identifying thousands of novel isoforms and expressed loci. We defined a stringent set of 1133 noncoding multi-exonic transcripts expressed during embryogenesis. These include long intergenic ncRNAs (lincRNAs), intronic overlapping lncRNAs, exonic antisense overlapping lncRNAs, and precursors for small RNAs (sRNAs). Zebrafish lncRNAs share many of the characteristics of their mammalian counterparts: relatively short length, low exon number, low expression, and conservation levels comparable to that of introns. Subsets of lncRNAs carry chromatin signatures characteristic of genes with developmental functions. The temporal expression profile of lncRNAs revealed two novel properties: lncRNAs are expressed in narrower time windows than are protein-coding genes and are specifically enriched in early-stage embryos. In addition, several lncRNAs show tissue-specific expression and distinct subcellular localization patterns. Integrative computational analyses associated individual lncRNAs with specific pathways and functions, ranging from cell cycle regulation to morphogenesis. Our study provides the first systematic identification of lncRNAs in a vertebrate embryo and forms the foundation for future genetic, genomic, and evolutionary studies.

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Section: Discussionmentioning

confidence: 99%

Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis

Pauli¹,

Valen²,

Lin³

et al. 2011

Genome Res.

739

830

View full text Add to dashboard Cite

show abstract

“…Several other proteins acting as translational regulators have been reported in the fly embryo and oocyte [50][51][52][53][54][55][56][57], and in other eukaryotic species [58][59][60], oftentimes in a developmental context. These findings hint at the possibility that the regulatory principle implemented by bicoid protein and caudal mRNA in Drosophila may be at work also in other developmental systems.…”

Section: Discussionmentioning

confidence: 99%

“…Since these regulatory proteins bind to DNA, it is plausible that they could also bind to mRNA, thereby regulating translation; this is known to happen in the large class of homeodomain proteins [45][46][47] and for the Argonaute family proteins [48,49], for several other proteins that fulfill important functions in the Drosophila embryo and oocyte [50][51][52][53][54][55][56][57], but also in other eukaryotic species [58][59][60] and in prokaryotes [61][62][63][64][65][66][67]. Intuitively, each mRNA molecule could act as an independent sensor of the input concentration, and averaging over these multiple sensors could reduce the input noise and thereby allow for more effective information transmission at low input concentrations.…”

Section: Introductionmentioning

confidence: 99%

Extending the dynamic range of transcription factor action by translational regulation

Sokolowski¹,

Walczak²,

Bialek³

et al. 2016

Phys. Rev. E

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A crucial step in the regulation of gene expression is binding of transcription factor (TF) proteins to regulatory sites along the DNA. But transcription factors act at nanomolar concentrations, and noise due to random arrival of these molecules at their binding sites can severely limit the precision of regulation. Recent work on the optimization of information flow through regulatory networks indicates that the lower end of the dynamic range of concentrations is simply inaccessible, overwhelmed by the impact of this noise. Motivated by the behavior of homeodomain proteins, such as the maternal morphogen Bicoid in the fruit fly embryo, we suggest a scheme in which transcription factors also act as indirect translational regulators, binding to the mRNA of other regulatory proteins. Intuitively, each mRNA molecule acts as an independent sensor of the input concentration, and averaging over these multiple sensors reduces the noise. We analyze information flow through this scheme and identify conditions under which it outperforms direct transcriptional regulation. Our results suggest that the dual role of homeodomain proteins is not just a historical accident, but a solution to a crucial physics problem in the regulation of gene expression.

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“…Translational control and mRNA localization, achieved via a variety of mechanisms, are important for the delivery of certain cytoplasmically synthesized proteins to their functional destinations within cells of animals (Johnstone and Lasko, 2001;Palacios and Johnston, 2001), plants (Choi et al, 2000), and yeast (Zoladek et al, 1995;Lithgow et al, 1997;Corral-Debrinski et al, 2000). In general, these strategies seem to reinforce targeting information present within the protein products themselves.…”

Section: Introductionmentioning

confidence: 99%

Interactions amongCOX1,COX2, andCOX3mRNA-specific Translational Activator Proteins on the Inner Surface of the Mitochondrial Inner Membrane ofSaccharomyces cerevisiae

Naithani

Saracco

Butler

et al. 2003

MBoC

144

117

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The core of the cytochrome c oxidase complex is composed of its three largest subunits, Cox1p, Cox2p, and Cox3p, which are encoded in mitochondrial DNA of Saccharomyces cerevisiae and inserted into the inner membrane from the inside. Mitochondrial translation of the COX1,COX2, and COX3 mRNAs is activated mRNA specifically by the nuclearly coded proteins Pet309p, Pet111p, and the concerted action of Pet54p, Pet122p, and Pet494p, respectively. Because the translational activators recognize sites in the 5′-untranslated leaders of these mRNAs and because untranslated mRNA sequences contain information for targeting their protein products, the activators are likely to play a role in localizing translation. Herein, we report physical associations among the mRNA-specific translational activator proteins, located on the matrix side of the inner membrane. These interactions, detected by coimmune precipitation and by two-hybrid experiments, suggest that the translational activator proteins could be organized on the surface of the inner membrane such that synthesis of Cox1p, Cox2p, and Cox3p would be colocalized in a way that facilitates assembly of the core of the cytochrome c oxidase complex. In addition, we found interactions between Nam1p/Mtf2p and the translational activators, suggesting an organized delivery of mitochondrial mRNAs to the translation system.

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Translational Regulation and RNA Localization in Drosophila Oocytes and Embryos

Cited by 305 publications

References 256 publications

Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis

Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis

Extending the dynamic range of transcription factor action by translational regulation

Interactions amongCOX1,COX2, andCOX3mRNA-specific Translational Activator Proteins on the Inner Surface of the Mitochondrial Inner Membrane ofSaccharomyces cerevisiae

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