The forkhead transcription factor FoxY regulates Nanos

Department of Molecular Biology, Cellular Biology and Biochemistry, Brown University, Providence, Rhode Island.
Molecular Reproduction and Development (Impact Factor: 2.53). 10/2012; 79(10):680-8. DOI: 10.1002/mrd.22073
Source: PubMed


FoxY is a member of the forkhead transcription factor family that appeared enriched in the presumptive germ line of sea urchins (Ransick et al. Dev Biol 2002;246:132). Here, we test the hypothesis that FoxY is involved in germ line determination in this animal. We found two splice forms of FoxY that share the same DNA-binding domain, but vary in the carboxy-terminal trans-activation/repression domain. Both forms of the FoxY protein are present in the egg and in the early embryo, and their mRNAs accumulate to their highest levels in the small micromeres and adjacent non-skeletogenic mesoderm. Knockdown of FoxY resulted in a dramatic decrease in Nanos mRNA and protein levels as well as a loss of coelomic pouches in 2-week-old larvae. Our results indicate that FoxY positively regulates Nanos at the transcriptional level and is essential for reproductive potential in this organism. Mol. Reprod. Dev. 79: 680-688, 2012. © 2012 Wiley Periodicals, Inc.

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    • "Moreover, the FoxY morpholino disrupts the coelomic pouch development (Song and Wessel, 2012; Materna et al, 2013) and the embryos present a phenotype similar to the Nanos-knockdown (Juliano et al., 2010). Interestingly , most of the forkhead transcription factors bind FIG. 1. Expression of Sp-nanos1/nanos2 and Sp-nanos3 mRNA in the small micromere lineage by in situ hybridization (Juliano et al., 2010). "
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    ABSTRACT: Nanos is an essential factor of germ line success in all animals tested. This gene encodes a Zn-finger RNA-binding protein that in complex with its partner pumilio, binds to and changes the fate of several known transcripts. We summarize here the documented functions of nanos in several key organisms, and then emphasize echinoderms as a working model for how nanos expression is regulated. Nanos presence outside of the target cells is often detrimental to the animal, and in sea urchins, nanos expression appears to be regulated at every step of transcription, and post-transcriptional activity, making this gene product exciting, every which way. © 2013 Wiley Periodicals, Inc.
    Full-text · Article · Mar 2014 · genesis
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    • "The OAn domain can be subdivided into two sub-domains: a larger one that is adjacent to the myogenic domain, where Ese, Tbx6, Maf, SoxC and MYP are expressed; and a smaller one that derives from SM descendants, points towards the animal pole of the embryo and expresses only FoxY, Nanos and Twist. FoxY is known to be expressed at the very tip of the archenteron together with the germ cell markers Nanos and Vasa[57,60]. These cells contribute to the primordial germ cell lineage of the adult [42]. "
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    ABSTRACT: In sea urchin larvae the circumesophageal fibers form a prominent muscle system of mesodermal origin. Although the morphology and later development of this muscle system has been well-described, little is known about the molecular signature of these cells or their precise origin in the early embryo. As an invertebrate deuterostome that is more closely related to the vertebrates than other commonly used model systems in myogenesis, the sea urchin fills an important phylogenetic gap and provides a unique perspective on the evolution of muscle cell development. Here, we present a comprehensive description of the development of the sea urchin larval circumesophageal muscle lineage beginning with its mesodermal origin using high-resolution localization of the expression of several myogenic transcriptional regulators and differentiation genes. A few myoblasts are bilaterally distributed at the oral vegetal side of the tip of the archenteron and first appear at the late gastrula stage. The expression of the differentiation genes Myosin Heavy Chain, Tropomyosin I and II, as well as the regulatory genes MyoD2, FoxF, FoxC, FoxL1, Myocardin, Twist, and Tbx6 uniquely identify these cells. Interestingly, evolutionarily conserved myogenic factors such as Mef2, MyoR and Six1/2 are not expressed in sea urchin myoblasts but are found in other mesodermal domains of the tip of the archenteron. The regulatory states of these domains were characterized in detail. Moreover, using a combinatorial analysis of gene expression we followed the development of the FoxF/FoxC positive cells from the onset of expression to the end of gastrulation. Our data allowed us to build a complete map of the Non-Skeletogenic Mesoderm at the very early gastrula stage, in which specific molecular signatures identify the precursors of different cell types. Among them, a small group of cells within the FoxY domain, which also express FoxC and SoxE, have been identified as plausible myoblast precursors. Together, these data support a very early gastrula stage segregation of the myogenic lineage. From this analysis, we are able to precisely define the regulatory and differentiation signatures of the circumesophageal muscle in the sea urchin embryo. Our findings have important implications in understanding the evolution of development of the muscle cell lineage at the molecular level. The data presented here suggest a high level of conservation of the myogenic specification mechanisms across wide phylogenetic distances, but also reveal clear cases of gene cooption.
    Full-text · Article · Dec 2013 · EvoDevo
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    • "In Strongylocentrotus purpuratus, each of the coelomic pouches initially contains only about ten cells, but their descendants are major contributors to various adult structures (Pearse and Cameron, 1991); at metamorphosis, ~90% of the 150,000 larval cells are located in the juvenile (Cameron et al., 1989; Song and Wessel, 2012), illustrating that coelomic pouch cells are multipotent progenitors. "
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    ABSTRACT: Indirect development, in which embryogenesis gives rise to a larval form, requires that some cells retain developmental potency until they contribute to the different tissues in the adult, including the germ line, in a later, post-embryonic phase. In sea urchins, the coelomic pouches are the major contributor to the adult, but how coelomic pouch cells (CPCs) are specified during embryogenesis is unknown. Here we identify the key signaling inputs into the CPC specification network and show that the forkhead factor foxY is the first transcription factor specifically expressed in CPC progenitors. Through dissection of its cis-regulatory apparatus we determine that the foxY expression pattern is the result of two signaling inputs: first, Delta/Notch signaling activates foxY in CPC progenitors; second, Nodal signaling restricts its expression to the left side, where the adult rudiment will form, through direct repression by the Nodal target pitx2. A third signal, Hedgehog, is required for coelomic pouch morphogenesis and institution of laterality, but does not directly affect foxY transcription. Knockdown of foxY results in a failure to form coelomic pouches and disrupts the expression of virtually all transcription factors known to be expressed in this cell type. Our experiments place foxY at the top of the regulatory hierarchy underlying the specification of a cell type that maintains developmental potency.
    Full-text · Article · Apr 2013 · Development
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