Widespread RNA segregation in a spiralian embryo

Kingsley, Evan P.; Chan, Xin Yi; Duan, Yingli; Lambert, J. David

doi:10.1111/j.1525-142x.2007.00194.x

Cited by 90 publications

(81 citation statements)

References 43 publications

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“…As with the studies of Blower et al (2007), Kingsley et al, (2007), and Lecuyer et al (2007), a significant percentage of these Spisula centrosome-associated RNAs (cnRNAs) have not been identified. Another unique quality of this set of RNAs is that they are exceedingly intron-poor, which stands in contrast to Tld, Eve, Dpp, Bub3, cyclin B1, and the others named above, all of which have an intron content comparable with the balance of their respective genomes.…”

Section: Findings Of Specific Nucleic Acids Associated With the Centrmentioning

confidence: 93%

“…Nevertheless, the study demonstrates a class of centrosomeassociated RNAs, even if the association is transient and exemplifies an extrinsic function. A subsequent screen for centrosome-associated RNAs in Ilyanassa embryos resulted in the identification of approximately 50 additional molecules considered highly enriched (Kingsley et al, 2007). A theme common to this and other studies (Alliegro et al, 2006;Blower et al 2007;Lecuyer et al, 2007;Alliegro et al, 2008) is a preponderance of genes unmatched in databases as well as an over-representation of genes involved in DNA and RNA metabolism.…”

Section: Findings Of Specific Nucleic Acids Associated With the Centrmentioning

confidence: 93%

“…Today, unless we choose to discount the technique of in situ RNA hybridization altogether, the evidence for specific RNAs associated with the spindle and centrosomes is overwhelming. At least fifteen distinct molecules for which the full length sequences are known have been localized to the centrosome by in situ hybridization in four laboratories (Lambert and Nagy, 2004;Alliegro et al, 2006;Alliegro and Alliegro, 2008;Kingsley et al, 2007;Lecuyer et al, 2007). Others have been localized to the spindle (Groismann et al, 2000;Lecuyer et al, 2007;Alliegro et al, 2010) and dozens more are either presumed (by biochemical enrichment) or known (by in situ localization based on partial sequences) to be present in these structures (Lecuyer et al, 2007;Alliegro and Alliegro, 2008).…”

Section: Discussionmentioning

confidence: 99%

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The centrosome and spindle as a ribonucleoprotein complex

Alliegro

2011

Chromosome Res

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1 The Subject in ContextThe presence of nucleic acids in centrosomes and the spindle have been proposed, observed, and reported since the 1950s. Why did the subject remain, perhaps even until today, such a controversial issue? The explanation is manifold, and includes legitimate concern over contamination from other cellular compartments in biochemical preparations. With a typically high background of cytoplasmic ribosomes, even microscopic images of stained intact cells could be difficult to interpret. Also, evidence for RNA and DNA in centrosomes accumulated for approximately 40 years but was interspersed with contradictory studies, primarily regarding the presence of DNA (reviewed in Johnson and Rosenbaum, 1991;Marshall and Rosenbaum, 2000). Perhaps less tangible but still a likely cause for lingering controversy is that the presence of nucleic acids in the spindle or centrosomes will require us to look differently at these structures from a functional, and more to the point, evolutionary standpoint.From the earliest studies, our overriding focus has been on the protein components of the cell division apparatus. The centrosome, centriole, and particularly the spindle, were long thought of as, first and foremost, microtubule-based structures. After all, microtubules are the most visually dominant structures, at least with the imaging techniques and probes we have had until recently, and tubulin is the dominant protein component. As other protein components were discovered, the analytical frame of reference was usually their protein-protein interactions with tubulin. Nucleic acids, in the form of chromatin, were cargo (albeit with a more proactive role, we learned as time passed). However, there is evidence that all four classes of biomolecules -protein, 2 carbohydrate (Chang et al., 2004), lipid (Ackerman, 1961Tsai et al., 2006), nucleic acid (references below) -are closely associated with the spindle, and integral to its structure and function. We are likely selling this biological machine short by referring to it only as a ribonucleoprotein complex (RNP). These other classes of biomolecules must be incorporated into our models for the genesis and function of the centrosomes and spindle, especially since their presence and activities may precede those of the hallmark proteins we have focused on for so long.Thinking of the cell division apparatus as not just a protein machine, but as a comprehensive unit composed of all classes of biomolecules (almost a cell within a cell) may also help us to understand its evolution, and by extension, eukaryosis. We agree that approaching the cell division apparatus as an evolutionary seme (Margulis et al., 2009) will ultimately be more informative than focusing on individual (or small groups of) molecules. This can make the difference, for example, between viewing nucleic acids or lipids and their respective metabolizing enzymes as later recruits rather than original components. A step in this direction is to broaden our description of the cell division apparatus to that ...

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Section: Findings Of Specific Nucleic Acids Associated With the Centrmentioning

confidence: 93%

Section: Findings Of Specific Nucleic Acids Associated With the Centrmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

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The centrosome and spindle as a ribonucleoprotein complex

Alliegro

2011

Chromosome Res

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“…Kingsley et al 19 expanded on an earlier report of RNA at the centrosome in Ilyanassa embryos. 21 These investigators hypothesize that RNAs are targeted to the centrosome for distribution to selected blastomeres in order to localize developmental information.…”

Section: Point Of Viewmentioning

confidence: 99%

“…We should keep in mind the vehement arguments made against of prokaryotes than of metazoans and this observation may hold for potential cnRNA homologues in the sea urchin (Strongylocentrotus purpuratus) genome as well. Now, just within the last year, the existence of RNA at the centrosome has been substantiated in four species: The surf clam Spisula solidissima, 17 Xenopus, 18 the snail Ilyanassa 19 and Drosophila. 20 There are important similarities and differences between the observations and perspectives in these studies, but more important is that no one of them practically or conceptually excludes the others.…”

Section: Point Of Viewmentioning

confidence: 99%

The implications of centrosomal RNA

Alliegro

2008

RNA Biology

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Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian molluscCrepidula

Perry

Lyons

Truchado-Garcia

et al. 2015

Developmental Dynamics

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Background: During gastrulation, endoderm and mesoderm are specified from a bipotential precursor (endomesoderm) that is argued to be homologous across bilaterians. Spiralians also generate mesoderm from ectodermal precursors (ectomesoderm), which arises near the blastopore. While a conserved gene regulatory network controls specification of endomesoderm in deuterostomes and ecdysozoans, little is known about genes controlling specification or behavior of either source of spiralian mesoderm or the digestive tract. Results: Using the mollusc Crepidula, we examined conserved regulatory factors and compared their expression to fate maps to score expression in the germ layers, blastopore lip, and digestive tract. Many genes were expressed in both ecto-and endomesoderm, but only five were expressed in ectomesoderm exclusively. The latter may contribute to epithelial-to-mesenchymal transition seen in ectomesoderm. Conclusions: We present the first comparison of genes expressed during spiralian gastrulation in the context of high-resolution fate maps. We found variation of genes expressed in the blastopore lip, mouth, and cells that will form the anus. Shared expression of many genes in both mesodermal sources suggests that components of the conserved endomesoderm program were either co-opted for ectomesoderm formation or that ecto-and endomesoderm are derived from a common mesodermal precursor that became subdivided into distinct domains during evolution.

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Widespread RNA segregation in a spiralian embryo

Cited by 90 publications

References 43 publications

The centrosome and spindle as a ribonucleoprotein complex

The centrosome and spindle as a ribonucleoprotein complex

The implications of centrosomal RNA

Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian molluscCrepidula

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