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FGF Signaling in Gastrulation and Neural Development in Nematostella Vectensis, an Anthozoan Cnidarian

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FGF Signaling in Gastrulation and Neural Development in Nematostella Vectensis, an Anthozoan Cnidarian Dev Genes Evol DOI 10.1007/s00427-006-0122-3 ORIGINAL ARTICLE FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian David Q. Matus & Gerald H. Thomsen & Mark Q. Martindale Received: 8 June 2006 /Accepted: 3 November 2006 # Springer-Verlag 2007 Abstract The fibroblast growth factor (FGF) signal trans- planula stages known as the apical tuft. These results duction pathway serves as one of the key regulators of early suggest a conserved role for FGF signaling molecules in metazoan development, displaying conserved roles in the coordinating both gastrulation and neural induction that specification of endodermal, mesodermal, and neural fates predates the Cambrian explosion and the origins of the during vertebrate development. FGF signals also regulate Bilateria. gastrulation, in part, by triggering epithelial to mesenchy- mal transitions in embryos of both vertebrates and Keywords Gastrulation . Neurogenesis . invertebrates. Thus, FGF signals coordinate gastrulation Evolution of development movements across many different phyla. To help under- stand the breadth of FGF signaling deployment across the animal kingdom, we have examined the presence and Introduction expression of genes encoding FGF pathway components in the anthozoan cnidarian Nematostella vectensis. We isolat- Fibroblast growth factors (FGFs) were originally isolated ed three FGF ligands (NvFGF8A, NvFGF8B,and from vertebrate brain and pituitary fibroblasts for their roles NvFGF1A), two FGF receptors (NvFGFRa and NvFGFRb), in angiogenesis, mitogenesis, cellular differentiation, mi- and two orthologs of vertebrate FGF responsive genes, gration, and tissue-injury repair (Itoh and Ornitz 2004; Sprouty (NvSprouty), an inhibitor of FGF signaling, and Ornitz and Itoh 2001; Popovici et al. 2005). FGFs signal Churchill (NvChurchill), a Zn finger transcription factor. through fibroblast growth factor receptors (FGFRs), which We found these FGF ligands, receptors, and response gene are membrane-associated class IV receptor tyrosine kinases expressed asymmetrically along the oral/aboral axis during (RTKs). The interaction of FGF ligands with these gastrulation and in a developing chemosensory structure of receptors are stabilized by co-binding of heparin or heparin sulfate proteoglycans, which prevent thermal denaturation Communicated by D. A. Weisblat and proteolysis (Itoh and Ornitz 2004; Popovici et al. Electronic supplementary material Supplementary material is 2005). Ligand binding results in receptor dimerization and available in the online version of this article at http://dx.doi.org/ autophosphorylation of several intracellular tyrosines, 10.1007/s00427-006-0122-3 and is accessible for authorized users. which leads to activation of the GTPase Ras, resulting in : D. Q. Matus M. Q. Martindale (*) a cascade of kinase signaling including Raf, mitogen- Kewalo Marine Lab, Pacific Bioscience Research Centre, activated and extracellular signal-regulated kinase (MEK), ’ University of Hawai i, and mitogen-activated protein kinase (MAPK; Nutt et al. 41 Ahui Street, Honolulu, HI 96813, USA 2001). FGF signals often work in concert with other e-mail: [email protected] important pathways, such as transforming growth factor-β (TGF-β), Wnt, Hedgehog, and Notch (Gerhart 1999). In G. H. Thomsen both invertebrates and vertebrates, FGF signaling func- Department of Biochemistry and Cell Biology, Center for Developmental Genetics, Stony Brook University, tions in body plan patterning, including mesoderm and Stony Brook, NY 11794-5215, USA neural induction and coordinate cell movements during Dev Genes Evol gastrulation (Bertrand et al. 2003; De Robertis and Kuroda stome and deuterostome development. In Drosophila,a 2004; Isaacs et al. 1994; Popovici et al. 2005; Rossant et al. second receptor (heartless) and pair of FGF ligands (pyramus 1997; Sheng et al. 2003; Sivak et al. 2005; Stathopoulos and thisbe) coordinate gastrulation movements and meso- et al. 2004). derm induction (Huang and Stern 2005; Stathopoulos et al. 2004). Heartless is required for cell-autonomous spreading FGF signaling complexity in the Metazoa of mesodermal cells, as they migrate dorsolaterally under the neurogenic ectoderm, which expresses the FGF ligands Genome duplications within the vertebrates (Huang and pyramus and thisbe (Stathopoulos et al. 2004). Functional Stern 2005; Itoh and Ornitz 2004; Popovici et al. 2005; tests in ascidian urochordates have shown that FGF signals Powers et al. 2000) have made it difficult to decipher the induce mesodermal mesenchymal cells (Bertrand et al. molecular machinery underlying FGF signaling due to the 2003). Roles for FGF signaling in vertebrate gastrulation diversity and sheer number of FGF ligands and receptors are well known. FGF4 and FGF8 are required during among the various vertebrate lineages. As many as 22 FGF mouse gastrulation for specification of endodermal and ligands and 4 receptors have been identified in the human mesodermal derivatives and cell migration through the genome, with alternative splice forms of the receptors primitive streak (Amaya et al. 1993; Isaacs et al. 1994; adding significantly to their complexity (Satou et al. 2002). Schulte-Merker and Smith 1995). These FGFs also specify The scope of FGF pathway members has been investigated mesodermal fates and regulate gastrulation movements in in lower chordates that diversified before vertebrate the frog, Xenopus (Isaacs et al. 1994), zebrafish (Griffin et genome duplications, and this has provided a clearer picture al. 1995), and chick (Yang et al. 2002). Signaling through of FGF family evolution within the deuterostomes. In the FGFR1 orchestrates epithelial–mesenchymal transforma- urochordate ascidians Ciona intestinalis and Ciona savigny tion (EMT) during mouse gastrulation by activating a (whose genomes have been sequenced) there are six FGF genetic network, which includes snail and E-cadherin ligands and one FGF receptor (Imai et al. 2002, 2003). genes (Ciruna and Rossant 2001). Within the protostomes, FGF ligand and receptor diversity has been explored in the ecdysozoan model FGFs in neural induction systems of Caenorhabditis elegans and Drosophila mela- nogaster, where only a few FGFs and one or two receptors Neural induction is another function for FGF signaling in have been isolated. In C. elegans, two FGF ligands (egl-17 bilaterian development. In Drosophila, the FGFR heartless and LET-756) and a single FGFR (egl-15) have been is required for neurogenesis, functioning in both glia described (Branda and Stern 2000). Likely due to a lack of migration and morphogenesis as a downstream mediator sampling, no FGF ligands have been described for any of Neuroglian cell-adhesion molecules (Forni et al. 2004; lophotrochozoan (e.g., molluscs, annelids, platyhelminths). Garcia-Alonso et al. 2000). In C. elegans, FGF signaling affects axon outgrowth via egl-15 (Bulow et al. 2004). In Conserved roles of FGF signaling deuterostomes, FGF signaling has been implicated in neural induction in ascidians and all vertebrate models tested thus FGFs and the control of branching morphogenesis far (Bertrand et al. 2003; Darras and Nishida 2001;De Robertis and Kuroda 2004; Imai et al. 2002). Although no Mutant analysis in Drosophila has revealed that an FGF data exists on FGF ligand expression in the Lophotrocho- ligand (branchless) and its receptor (breathless) regulate zoa, FGFRs have, however, been implicated in a role in tracheal development (Klambt et al. 1992; Sutherland et al. neurogenesis of the platyhelminth Dugesia japonica 1996). In mouse, FGF signaling through FGF-10 and (Cebria et al. 2002; Mineta et al. 2003), suggesting that a FGFR2-IIIb direct branching morphogenesis of the lungs conserved role for FGF signaling in neural induction at (Min et al. 1998; Shishido et al. 1997; Stathopoulos et al. least extends to the Lophotrochozoa. 2004), and although mammalian lungs and insect trachea may not be directly homologous, these data suggest a FGF signaling in non-bilaterians conserved role for FGF signaling in controlling branching morphogenesis in organisms as diverse as flies and Modern molecular phylogenetics suggest that cnidarians, mammals. and possibly placozoans, represent the closest extant animals related to the triploblastic, bilaterally symmetric FGFs in gastrulation bilaterians (protostomes and deuterostomes; Collins et al. 2005; Wallberg et al. 2004). Recent molecular evidence FGF signaling during fly, vertebrate, and ascidian gastru- suggests that these diverse groups use many of the same lation suggests a more conserved role for FGFs in proto- signal transduction pathways and transcription factors Dev Genes Evol during early development (Kusserow et al. 2005; Miller et (EF068140–EF068151). Gene-specific primer sequences al. 2005; Technau et al. 2005; Technau and Scholz 2003). are available upon request. Two recent studies have examined the FGF signaling pathway in Cnidaria. Sudhop et al. (2004) showed that an Linkage analysis FGFR-like gene kringelchen is expressed during bud detachment during asexual reproduction of the hydrozoan An assembly of the N. vectensis genome (Joint Genome Hydra vulgaris and a recent expressed sequence tag (EST) Institute) was searched using nucleotide sequences of all survey of the anthozoans Nematostella vectensis and isolated FGF ligands and NvSprouty utilizing BLASTN Acropora millepora yielded several members of FGF search parameters. Where multiple genes were found to signaling pathways (Technau et al. 2005).
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