Piwi regulates Vasa accumulation during embryogenesis in the sea urchin

Yajima, Mamiko; Gustafson, Eric A.; Song, Jia L.; Wessel, Gary M.

doi:10.1002/dvdy.24096

Cited by 18 publications

(17 citation statements)

References 38 publications

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“…We cannot rule out additional Vasa function in regulating piRNA production, as recently reported in flies (Xiol et al, 2014). The sea urchin embryo does have a large population of both miRNAs and piRNAs (Song et al, 2012), yet the phenotypes of Piwi, Drosha or Dicer knockdowns do not show a similar phenotype as the Vasa knockdown demonstrated in this report (Song et al, 2012;Yajima et al, 2014). Therefore, the somatic function of Vasa seen in the sea urchin might be independent of the piRNA (or miRNA) pathways, at least for the phenotypes seen herein.…”

Section: Discussioncontrasting

confidence: 50%

Essential elements for translation: the germline factor Vasa functions broadly in somatic cells

Yajima

Wessel

2015

Development

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Vasa is a conserved RNA-helicase found in the germ lines of all metazoans tested. Whereas Vasa presence is often indicated as a metric for germline determination in animals, it is also expressed in stem cells of diverse origin. Recent research suggests, however, that Vasa has a much broader function, including a significant role in cell cycle regulation. Results herein indicate that Vasa is utilized widely, and often induced transiently, during development in diverse somatic cells and adult precursor tissues. We identified that Vasa in the sea urchin is essential for: (1) general mRNA translation during embryogenesis, (2) developmental re-programming upon manipulations to the embryo and (3) larval wound healing. We also learned that Vasa interacted with mRNAs in the perinuclear area and at the spindle in an Importin-dependent manner during cell cycle progression. These results suggest that, when present, Vasa functions are essential to contributing to developmental regulation.

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Section: Discussioncontrasting

confidence: 50%

Essential elements for translation: the germline factor Vasa functions broadly in somatic cells

Yajima

Wessel

2015

Development

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“…These RNAs are typically ubiquitously distributed throughout the early embryo, and retained in the sMics, but turned over in somatic cells later. This pattern of acquisition is consistent with the observation that the sMics are transcriptionally repressed (Swartz et al, 2014; Voronina et al, 2008; Yajima et al, 2014). Furthermore, exogenous mRNA reporters injected into zygotes, while eventually degraded in somatic cells, are retained several days longer in the sMics (Gustafson & Wessel, 2010; Oulhen & Wessel, 2013).…”

Section: Differential Stability Of Mrna In the Germ Line And Somasupporting

confidence: 90%

“…Nanos is uniquely detectable in the sMics by in situ hybridization as early as the 32/64-cell stage. As in the sea star, Piwi mRNA is maternally supplied and ubiquitous in early embryos, but becomes restricted post-transcriptionally to the sMics by gastrula stages (Swartz et al, 2014; Yajima, Gustafson, Song, & Wessel, 2014). Intriguingly, the vegetal egg cortex and subsequently the sMics of the sea urchin Hemicentrotus pulcherrimus are enriched for mitochondrial rRNAs outside of the mitochondria themselves (Ogawa et al, 1999).…”

Section: Evolutionary Transition Of Pgc Segregation In the Echinodermsmentioning

confidence: 99%

Germ Line Versus Soma in the Transition from Egg to Embryo

Swartz

Wessel

2015

Current Topics in Developmental Biology

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With few exceptions, all animals acquire the ability to produce eggs or sperm at some point in their lifecycle. Despite this near universal requirement for sexual reproduction, there exists an incredible diversity in germ-line development. For example, animals exhibit a vast range of differences in the timing at which the germ line, which retains reproductive potential, separates from the soma, or terminally differentiated, non-reproductive cells. This separation may occur during embryonic development, after gastrulation, or even in adults, depending on the organism. The molecular mechanisms of germ line segregation are also highly diverse, and intimately intertwined with the overall transition from a fertilized egg to an embryo. The earliest embryonic stages of many species are largely controlled by maternally supplied factors. Later in development, patterning control shifts to the embryonic genome and, concomitantly with this transition, the maternally supplied factors are broadly degraded. This chapter attempts to integrate these processes – germ line segregation, and how the divergence of germ line and soma may utilize the egg to embryo transitions differently. In some embryos, this difference is subtle or maybe lacking altogether, whereas in other embryos, this difference in utilization may be a key step in the divergence of the two lineages. Here we will focus our discussion on the echinoderms, and in particular the sea urchins, in which recent studies have provided mechanistic understanding in germ line determination. We propose that the germ line in sea urchins requires an acquisition of maternal factors from the egg and, when compared to other members of the taxon, this appears to be a derived mechanism. The acquisition is early – at the 32 cell stage – and involves active protection of maternal mRNAs, which are instead degraded in somatic cells with the maternal to embryonic transition. We collectively refer to this model as the Time Capsule method for germ line determination.

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“…Additionally, we tested the transcript abundance of the endogenous Argonaute family member Seawi in the sMics with CNOT6 overexpression. Seawi transcript is normally present in all cells but is highly enriched in the sMics (Yajima et al, 2013). With CNOT6::mCherry expression, the sMics lose enrichment for Seawi RNA (Fig.…”

Section: Cnot6 Repression Is Required For Retention Of Germline Determentioning

confidence: 94%

Deadenylase depletion protects inherited mRNAs in primordial germ cells

et al. 2014

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A crucial event in animal development is the specification of primordial germ cells (PGCs), which become the stem cells that create sperm and eggs. How PGCs are created provides a valuable paradigm for understanding stem cells in general. We find that the PGCs of the sea urchin Strongylocentrotus purpuratus exhibit broad transcriptional repression, yet enrichment for a set of inherited mRNAs. Enrichment of several germline determinants in the PGCs requires the RNA-binding protein Nanos to target the transcript that encodes CNOT6, a deadenylase, for degradation in the PGCs, thereby creating a stable environment for RNA. Misexpression of CNOT6 in the PGCs results in their failure to retain Seawi transcripts and Vasa protein. Conversely, broad knockdown of CNOT6 expands the domain of Seawi RNA as well as exogenous reporters. Thus, Nanos-dependent spatially restricted CNOT6 differential expression is used to selectively localize germline RNAs to the PGCs. Our findings support a 'time capsule' model of germline determination, whereby the PGCs are insulated from differentiation by retaining the molecular characteristics of the totipotent egg and early embryo.

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Piwi regulates Vasa accumulation during embryogenesis in the sea urchin

Cited by 18 publications

References 38 publications

Essential elements for translation: the germline factor Vasa functions broadly in somatic cells

Essential elements for translation: the germline factor Vasa functions broadly in somatic cells

Germ Line Versus Soma in the Transition from Egg to Embryo

Deadenylase depletion protects inherited mRNAs in primordial germ cells

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