Seawi—a sea urchin piwi/argonaute family member is a component of MT-RNP complexes

Rodríguez, A.; Seipel, Susan A.; Hamill, Danielle R.; Romancino, Daniele P.; Carlo, Marta Di; Suprenant, Kathy A.; Bonder, Edward M.

doi:10.1261/rna.7198205

Cited by 44 publications

(36 citation statements)

References 51 publications

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“…Interestingly, dDcp 1 of the oskar mRNP complex in Drosophila oocytes mislocates in mutants in which microtubule organization is abnormal (Lin et al 2006). Also, the Argonaute 1 homolog from sea urchins, Seawi, has been identified in a microtubule-associated protein complex that localizes in cytoplasmic puncta (Rodriguez et al 2005). It is not known whether SGs contain proteins associated with microtubules, but we and others (Ivanov et al 2003) observed that microtubule integrity is necessary for SG assembly.…”

Section: Hdac6 Links the Microtubule System And Sgsmentioning

confidence: 82%

The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response

Kwon¹,

Zhang²,

Matthias³

2007

Genes Dev.

363

382

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An essential part of the cellular response to environmental stress is a reversible translational suppression, taking place in dynamic cytoplasmic structures called stress granules (SGs). We discovered that HDAC6, a cytoplasmic deacetylase that acts on tubulin and HSP90 and also binds ubiquitinated proteins with high affinity, is a novel critical SG component. We found that HDAC6 interacts with another SG protein, G3BP (Ras-GTPase-activating protein SH3 domain-binding protein 1), and localizes to SGs under all stress conditions tested. We show that pharmacological inhibition or genetic ablation of HDAC6 abolishes SG formation. Intriguingly, we found that the ubiquitin-binding domain of HDAC6 is essential and that SGs are strongly positive for ubiquitin. Moreover, disruption of microtubule arrays or impairment of motor proteins also prevents formation of SGs. These findings identify HDAC6 as a central component of the stress response, and suggest that it coordinates the formation of SGs by mediating the motor-protein-driven movement of individual SG components along microtubules.[Keywords: HDAC6; acetylation; deacetylases; stress granules; RNA metabolism] Supplemental material is available at http://www.genesdev.org. Reversible protein acetylation has emerged in recent years as one of the major forms of protein modifications whose importance has been particularly well documented in the case of the N-terminal histone tails, and of a few transcription factors such as p53 and STAT3 (for reviews, see Kouzarides 2000;Caron et al. 2003;Glozak et al. 2005). Acetylation and deacetylation are catalyzed by histone acetylases (HATs) and histone deacetylases (HDACs). HDAC6 is a unique class II deacetylase (for reviews, see Verdin et al. 2003;Boyault et al. 2007a;Matthias et al. 2007) that contains two catalytic domains and also a C-terminal zinc finger domain (ZnF-UBP) binding with high-affinity free ubiquitin as well as mono-and polyubiquitinated proteins (Seigneurin-Berny et al. 2001;Hook et al. 2002;Boyault et al. 2006). HDAC6 is actively maintained in the cytoplasm (Verdel et al. 2000;Bertos et al. 2004), where it is found partly associated with the microtubule network. We and others have shown that HDAC6 can deacetylate tubulin as well as the microtubule network in vivo (Hubbert et al. 2002;Matsuyama et al. 2002;Zhang et al. 2003). HDAC6 associates with the chaperone-like AAA ATPase p97/VCP, a protein that is critical for proteasomal degradation of misfolded proteins. Thereby, the ratio of HDAC6 and p97/VCP modulates the levels of polyubiquitinated aggregates (Boyault et al. 2006). HDAC6 also facilitates the clearance of misfolded ubiquitinated proteins, promoting their accumulation in an aggresome, and protects cells from apoptosis following stress induced by misfolded proteins (Kawaguchi et al. 2003). At the same time, HDAC6 also controls the induction of heat-shock proteins in response to the accumulation of ubiquitinated protein aggregates (Boyault et al. 2007b). Furthermore, HDAC6 can deacetylate the chaperone Hsp90...

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Section: Hdac6 Links the Microtubule System And Sgsmentioning

confidence: 82%

The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response

Kwon¹,

Zhang²,

Matthias³

2007

Genes Dev.

363

382

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“…Taken together the results suggest that piRNAs have a dynamic expression pattern in the early sea urchin embryo. This increase of piRNA expression may correspond with the specification of the piwi -positive small micromere lineage (Juliano et al, 2006; Rodriguez et al, 2005). …”

Section: Resultsmentioning

confidence: 98%

Select microRNAs are essential for early development in the sea urchin

Song

Stoeckius

Maaskola

et al. 2012

Developmental Biology

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Summary microRNAs (miRNAs) are small noncoding RNAs that mediate post-transcriptional gene regulation and have emerged as essential regulators of many developmental events. The transcriptional network during early embryogenesis of the purple sea urchin, Strongylocentrotus purpuratus, is well described and would serve as an excellent model to test functional contributions of miRNAs in embryogenesis. We examined the loss of function phenotypes of the major components of the miRNA biogenesis pathway. Inhibition of de novo synthesis of Drosha and Dicer in the embryo led to consistent developmental defects, a failure to gastrulate, and embryonic lethality, including changes in the steady state levels of transcription factors and signaling molecules involved in germ layer specification. We annotated and profiled small RNA expression from the ovary and several early embryonic stages by deep sequencing followed by computational analysis. All miRNAs have dynamic accumulation profiles through early development as do a large population of putative piRNAs (piwi-interacting RNAs). Defects in morphogenesis caused by loss of Drosha can be rescued with four miRNAs which permits a strong miRNA functional assay. Taken together our results indicate that post-transcriptional gene regulation directed by miRNAs is functionally important for early embryogenesis and is an integral part of the early embryonic gene regulatory network in S. purpuratus.

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“…Recent studies have suggested that PIWI proteins in sea urchin (Seawi) and Xenopus (Xiwi) can interact with the MTs of the meiotic spindle (Rodriguez et al 2005;Lau et al 2009), while fly ovarioles with mutations in any of several piRNA pathway genes, including spn-E, aub, and armi, have disorganized MTs (Chen et al 2007;Klattenhoff et al 2007;Pane et al 2007). This raises the possibility for either a functional role of PIWI proteins in the machinery that impacts on MT organization (in addition to transposon silencing), a role of the MT cytoskeleton in piRNA generation, or both.…”

Section: Discussionmentioning

confidence: 99%

Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC

Sato

Nishida²,

Shibuya³

et al. 2011

Genes Dev.

103

124

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The establishment of body axes in multicellular organisms requires accurate control of microtubule polarization. Mutations in Drosophila PIWI-interacting RNA (piRNA) pathway genes often disrupt the axes of the oocyte. This results from the activation of the DNA damage checkpoint factor Checkpoint kinase 2 (Chk2) due to transposon derepression. A piRNA pathway gene, maelstrom (mael), is critical for the establishment of oocyte polarity in the developing egg chamber during Drosophila oogenesis. We show that Mael forms complexes with microtubuleorganizing center (MTOC) components, including Centrosomin, Mini spindles, and gTubulin. We also show that Mael colocalizes with aTubulin and gTubulin to centrosomes in dividing cyst cells and follicle cells. MTOC components mislocalize in mael mutant germarium and egg chambers, leading to centrosome migration defects. During oogenesis, the loss of mael affects oocyte determination and induces egg chamber fusion. Finally, we show that the axis specification defects in mael mutants are not suppressed by a mutation in mnk, which encodes a Chk2 homolog. These findings suggest a model in which Mael serves as a platform that nucleates other MTOC components to form a functional MTOC in early oocyte development, which is independent of Chk2 activation and DNA damage signaling.

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Seawi—a sea urchin piwi/argonaute family member is a component of MT-RNP complexes

Cited by 44 publications

References 51 publications

The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response

The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response

Select microRNAs are essential for early development in the sea urchin

Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC

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