RNA Localization in the Vertebrate Oocyte: Establishment of Oocyte Polarity and Localized mRNA Assemblages

Oh, Denise; Houston, Douglas

doi:10.1007/978-3-319-60855-6_9

Cited by 17 publications

(22 citation statements)

References 109 publications

(167 reference statements)

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“…Nonetheless, the striking overlap in their function in Drosophila or zebrafish was frequently highlighted [e.g. 29 ], but experiments directly addressing the functional conservation of Osk and Buc are not available.…”

Section: Introductionmentioning

confidence: 99%

Functional equivalence of germ plasm organizers

et al. 2018

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The proteins Oskar (Osk) in Drosophila and Bucky ball (Buc) in zebrafish act as germ plasm organizers. Both proteins recapitulate germ plasm activities but seem to be unique to their animal groups. Here, we discover that Osk and Buc show similar activities during germ cell specification. Drosophila Osk induces additional PGCs in zebrafish. Surprisingly, Osk and Buc do not show homologous protein motifs that would explain their related function. Nonetheless, we detect that both proteins contain stretches of intrinsically disordered regions (IDRs), which seem to be involved in protein aggregation. IDRs are known to rapidly change their sequence during evolution, which might obscure biochemical interaction motifs. Indeed, we show that Buc binds to the known Oskar interactors Vasa protein and nanos mRNA indicating conserved biochemical activities. These data provide a molecular framework for two proteins with unrelated sequence but with equivalent function to assemble a conserved core-complex nucleating germ plasm.

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Section: Introductionmentioning

confidence: 99%

Functional equivalence of germ plasm organizers

et al. 2018

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“…The organization of islands may be under strict regulation to properly control the expression/ silencing of germline determinants in a membrane less structure which contains numerous proteins and transcripts. Islands have been known to transition between fluid and viscous states altering protein-protein interactions (Oh and Houston, 2017) and the expression of maternal transcripts held within the islands must be specifically regulated temporally and spatially. Inappropriately timed expression or degradation of these transcripts will lead to a loss of germ cells in the embryo as development is a specifically controlled process.…”

Section: Germ Plasm Island Aggregation Patterns From Oocyte To Early mentioning

confidence: 99%

The role of maternal syntabulin in Xenopus primordial germ cell development and germ cell specification

Oh¹

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In anuran amphibian and teleost embryos, cytoplasmic localizations in the egg are essential for establishing initial differences in cell fates. The cytoplasmic inheritance of germ plasm, which consists of mitochondria, germ line granules, and various RNAs, specifies primordial germ cell (PGC) fate. In Xenopus, the germ plasm originates within the mitochondrial cloud. The roles of several of these RNAs in PGC formation have been well characterized; recently however, it has become apparent that a subset of germ plasm RNAs in the vegetal cortex may have roles in dorsal axis formation. These include trim36 and dnd1 in Xenopus, which are predicted to facilitate microtubule assembly during cortical rotation, and syntabulin (sybu), which encodes a kinesin motor protein linker.Sybu is defective in ventralized tokkeabi mutant zebrafish and mRNA knockdown of sybu in Xenopus results in ventralized embryos. Thus, Sybu is thought to function in the transport of dorsal determinants in the zygote. Here I further examine the germline functions of Sybu in early Xenopus development. In contrast to the case in zebrafish, Xenopus sybu mRNA remains localized to the germ plasm of early embryos through the gastrula stage. Maternal antisense inhibition of sybu results in embryos lacking PGCs by the tailbud stage, and analysis of sybu-depleted embryos revealed altered germ plasm dynamics, reducing germ plasm aggregation. In addition, during initial cell divisions, a novel accelerated wave of germ plasm was discovered to mediate trafficking toward the cleavage furrows, which was found to be dependent on Syntabulin. As Syntabulin is a motor linker protein I also detected interactions with the kinesins Kif3b and Kif4a to mediate germ plasm aggregation. Depletion of any of these factors resulted in a reduction of PGC formation and altered migration patterns within gastrulating embryos and early iii tadpoles. I also found that Syntabulin is required for recruitment of the germ plasm to a perinuclear position in gastrula stage blastomeres, indicating that Syntabulin is required at multiple steps for proper organization and localization of the germ plasm. iv PUBLIC ABSTRACTNumerous events must occur within the fertilized egg and early cell divisions in the embryo to establish developmental cell fates. The egg must be transformed into a complex multicellular organism where the cells are specialized for specific functions. Not only are cells specified, but they are clearly positioned within the animals. Visibly there are notable differences between an organism's front and back, top and bottom, and left and right sides. The egg may appear simple as a single cell, but it is very complex as it contains a multitude of interacting genetic materials, proteins, and organelles. The egg is also visibly uniform as a spherical structure, however, the factors contained within this cell are specifically positioned to regulate fate decisions during embryonic development.This manuscript will describe one particularly localized factor known as Syntabulin, and it...

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“…Life is able to accumulate matter and, through metabolic processes, transform that matter into energy or other biochemical components. 7,8 Arguably the most important feature of life is the ability to replicate or reproduce itself. However, underlying these processes is the organization and compartmentalization of the biochemical reactions and building blocks which are required to performs all these tasks.…”

Section: What Is Life?mentioning

confidence: 99%

“…14 The polymerization of these compounds, and their derivatives, would have driven the evolution of self-replicating polymers, which would become the basis of life. 8,15 Two requirements must be met for a biological polymer to self-replicate, the ability to encode heritable information and catalyze directed reactions. Of the major biological molecules, only ribonucleic acid (RNA) is known to have both of these capabilities.…”

Section: Prebiotic Earth Was a Cauldron Of Inorganic Molecules Expermentioning

confidence: 99%

“…Of the major biological molecules, only ribonucleic acid (RNA) is known to have both of these capabilities. 8 A shared feature of the methods used to spontaneously synthesize organic molecules is heat. High temperatures, though required for chemical synthesis of precursors, likely did more harm than good for early life because RNA is not stable at high temperatures.…”

Section: Prebiotic Earth Was a Cauldron Of Inorganic Molecules Expermentioning

confidence: 99%

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Investigating the organization and regulation of aggregated proteins within sub-nuclear organelles

Hayes¹

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Protein aggregation has long been associated with disease states, such as Alzheimer's, Huntington's, and Parkinson's diseases. This model is challenged by increasing recognition of functional protein aggregates. Our focus has been exploration of intra-aggregate organization, and investigation of the ability of ATP to mediate energy independent aggregate solubilization by acting as a hydrotrope. Furthering our understanding of the composition and regulation of these structures will provide insight into how their dysregulation gives rise to disease, and provide a template for the development of novel therapeutics. Sub-nuclear organelles are a class of non-membrane bound organelle. These compartments form through liquid-liquid phase separation of their components, resulting in a functional aggregate that demonstrates liquid properties. Many of the factors driving liquid-liquid phase separation also drive the formation of amyloid fibrils. In vitro studies have demonstrated that liquid-liquid phase separation can promote amyloid fibril formation, and that liquid-liquid phase separated droplets can mature through amyloid fibril formation. In vivo, functional amyloids are known to contribute to peptide hormone storage, melanin production, and maintenance of long-term memory. Despite these findings, there has been limited investigation into the relationship between liquid-liquid phase separated droplets and amyloid fibrils in vivo. Our exploration of intra-aggregate organization took advantage of the numerous protein aggregates found within Xenopus oocytes. Using a dye and antibodies specific to the defining cross-β structure of amyloid, we demonstrated that amyloids form as a normal part of Xenopus oogenesis. Amyloid was detected within nuclear and cytosolic aggregates. In the cytosol, amyloid was observed within yolk platelets and a population of cortical particles whose identity has yet to be determined. In the nucleus, multiple liquid-liquid phase separated sub-nuclear organelles, including those associated with vi RNA polymerase I, II and III transcription as well as RNA processing, were found to have an amyloid component. Proteomic analysis of aggregate enriched material revealed proteins associated with ribonucleoprotein complex biogenesis, DNA replication, RNA processing and DNA-templated transcription. Our analysis further demonstrated that nuclear amyloids were stable, remaining intact for hours post isolation, but rapidly destabilized following treatment with RNase. Recently, adenosine triphosphate (ATP) was demonstrated to act as a hydrotrope in vitro. Physiologic levels were shown to maintain protein solubility and solubilize recombinant liquid-liquid phase separated droplets, in the absence of ATP hydrolysis. These observations suggest that this previously unappreciated activity of ATP has a large influence on liquid-liquid phase separated droplet stability. However, these observations were made under conditions that diverge from those found in vivo. The liquid-liquid phase separated droplets tested were de...

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RNA Localization in the Vertebrate Oocyte: Establishment of Oocyte Polarity and Localized mRNA Assemblages

Cited by 17 publications

References 109 publications

Functional equivalence of germ plasm organizers

Functional equivalence of germ plasm organizers

The role of maternal syntabulin in Xenopus primordial germ cell development and germ cell specification

Investigating the organization and regulation of aggregated proteins within sub-nuclear organelles

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