Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus

Colozza, Gabriele; Robertis, Edward M. De

doi:10.1016/j.diff.2014.03.002

Cited by 45 publications

(56 citation statements)

References 72 publications

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“…In tailbud stages the most notable expression pattern was in neural regions including the eye, cranial ganglia, neural tube, nasal placodes, brain, otic vesicle and the intersegmental region between the somites. Vegetally enriched transcripts that have previously been shown to be involved in neural pathways included efnb1, sybu, wnk2 and otx1 (Colozza and De Robertis, 2014;Bovolenta et al, 2006;Rinehart et al, 2011;. Taken together, these data suggest that genes enriched at the vegetal pole of Xenopus oocytes contribute to both germline and neural specification during development.…”

Section: Expression Of Vegetally Localized Rnas During Developmentsupporting

confidence: 50%

High-throughput analysis reveals novel maternal germline RNAs crucial for primordial germ cell preservation and proper migration

et al. 2017

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During oogenesis, hundreds of maternal RNAs are selectively localized to the animal or vegetal pole, including determinants of somatic and germline fates. Although microarray analysis has identified localized determinants, it is not comprehensive and is limited to known transcripts. Here, we utilized high-throughput RNAsequencing analysis to comprehensively interrogate animal and vegetal pole RNAs in the fully grown Xenopus laevis oocyte. We identified 411 (198 annotated) and 27 (15 annotated) enriched mRNAs at the vegetal and animal pole, respectively. Ninety were novel mRNAs over 4-fold enriched at the vegetal pole and six were over 10-fold enriched at the animal pole. Unlike mRNAs, microRNAs were not asymmetrically distributed. Whole-mount in situ hybridization confirmed that all 17 selected mRNAs were localized. Biological function and network analysis of vegetally enriched transcripts identified protein-modifying enzymes, receptors, ligands, RNA-binding proteins, transcription factors and co-factors with five defining hubs linking 47 genes in a network. Initial functional studies of maternal vegetally localized mRNAs show that sox7 plays a novel and important role in primordial germ cell (PGC) development and that ephrinB1 (efnb1) is required for proper PGC migration. We propose potential pathways operating at the vegetal pole that highlight where future investigations might be most fruitful.

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Section: Expression Of Vegetally Localized Rnas During Developmentsupporting

confidence: 50%

High-throughput analysis reveals novel maternal germline RNAs crucial for primordial germ cell preservation and proper migration

et al. 2017

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“…We verified this expression pattern in Xenopus , showing as previously reported that sybu localizes to the mitochondrial cloud of stage I oocytes and remains with the cloud as it fragments and disperses to the vegetal cortex during oogenesis (Colozza and De Robertis, 2014). In fertilized eggs, sybu is maintained in a germ plasm pattern, concentrating at the vegetal apex and at cleavage furrows, and later becoming restricted to a small group of vegetal cells in the gastrula (Fig.…”

Section: Resultssupporting

confidence: 86%

“…In Xenopus and zebrafish, sybu is expressed in the mitochondrial cloud/Balbiani body (Bb) of pre-vitellogenic oocytes and in the vegetal cortex of full-grown oocytes and eggs, congruent with the germ plasm (Colozza and De Robertis, 2014; Nojima et al, 2010). We verified this expression pattern in Xenopus , showing as previously reported that sybu localizes to the mitochondrial cloud of stage I oocytes and remains with the cloud as it fragments and disperses to the vegetal cortex during oogenesis (Colozza and De Robertis, 2014).…”

Section: Resultsmentioning

confidence: 99%

“…However, both Sybu and Grip2a protein and RNA fail to accumulate in the aggregating germ plasm following its transport to the forming blastodisc and thus do not localize to embryonic germ plasm. By contrast, in Xenopus , sybu and grip2a do associate with germ plasm in oocytes (Colozza and De Robertis, 2014; Kaneshiro et al 2007; Tarbashevich et al 2007) but also remain localized to the germ plasm throughout early embryogenesis. Depletion of Grip2a in fertilized embryos using morpholino antisense oligos in Xenopus can result in PGC migration defects (Kirilenko et al 2008) but a role in axis formation was not specifically tested by depletion of maternal grip2a mRNA in oocytes.…”

Section: Introductionmentioning

confidence: 89%

“…Depletion of Grip2a in fertilized embryos using morpholino antisense oligos in Xenopus can result in PGC migration defects (Kirilenko et al 2008) but a role in axis formation was not specifically tested by depletion of maternal grip2a mRNA in oocytes. Maternal depletion of sybu by the host-transfer procedure does indeed result in axis deficient embryos (Colozza and De Robertis, 2014) but it remains unclear to what extent Sybu is acting similarly in fish and frogs. Nevertheless, the localization of sybu mRNA to the germ plasm in cleavage stage embryos prompted us to examine its roles in the germ plasm.…”

Section: Introductionmentioning

confidence: 99%

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Role of maternal Xenopus syntabulin in germ plasm aggregation and primordial germ cell specification

Houston

2017

Developmental Biology

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The localization and organization of mitochondria- and ribonucleoprotein granule-rich germ plasm is essential for many aspects of germ cell development. In Xenopus, germ plasm is maternally inherited and is required for the specification of primordial germ cells (PGCs). Germ plasm is aggregated into larger patches during egg activation and cleavage and is ultimately translocated perinuclearly during gastrulation. Although microtubule dynamics and a kinesin (Kif4a) have been implicated in Xenopus germ plasm localization, little is known about how germ plasm distribution is regulated. Here, we identify a role for maternal Xenopus Syntabulin in the aggregation of germ plasm following fertilization. We show that depletion of sybu mRNA using antisense oligonucleotides injected into oocytes results in defects in the aggregation and perinuclear transport of germ plasm and subsequently in reduced PGC numbers. Using live imaging analysis, we also characterize a novel role for Sybu in the collection of germ plasm in vegetal cleavage furrows by surface contraction waves. Additionally, we show that a localized kinesin-like protein, Kif3b, is also required for germ plasm aggregation and that Sybu functionally interacts with Kif3b and Kif4a in germ plasm aggregation. Overall, these data suggest multiple coordinate roles for kinesins and adaptor proteins in controlling the localization and distribution of a cytoplasmic determinant in early development.

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The translational regulation of maternal mRNAs in time and space

Winata

Korzh

2018

FEBS Letters

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Since their discovery, the study of maternal mRNAs has led to the identification of mechanisms underlying their spatiotemporal regulation within the context of oogenesis and early embryogenesis. Following synthesis in the oocyte, maternal mRNAs are translationally silenced and sequestered into storage in cytoplasmic granules. At the same time, their unique distribution patterns throughout the oocyte and embryo are tightly controlled and connected to their functions in downstream embryonic processes. At certain points in oogenesis and early embryogenesis, maternal mRNAs are translationally activated to perform their functions in a timely manner. The cytoplasmic polyadenylation machinery is responsible for the translational activation of maternal mRNAs, and its role in initiating the maternal to zygotic transition events has recently come to light. Here, we summarize the current knowledge on maternal mRNA regulation, with particular focus on cytoplasmic polyadenylation as a mechanism for translational regulation.

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Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus

Cited by 45 publications

References 72 publications

High-throughput analysis reveals novel maternal germline RNAs crucial for primordial germ cell preservation and proper migration

High-throughput analysis reveals novel maternal germline RNAs crucial for primordial germ cell preservation and proper migration

Role of maternal Xenopus syntabulin in germ plasm aggregation and primordial germ cell specification

The translational regulation of maternal mRNAs in time and space

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