Abstract:We have studied the evolution of Wnt genes in cnidarians and the expression pattern of all Wnt ligands in the hydrozoan Hydractinia echinata. Current views favor a scenario in which 12 Wnt sub-families were jointly inherited by cnidarians and bilaterians from their last common ancestor. Our phylogenetic analyses clustered all medusozoan genes in distinct, well-supported clades, but many orthologous relationships between medusozoan Wnts and anthozoan and bilaterian Wnt genes were poorly supported. Only seven an… Show more
“…The third cluster contained genes that were upregulated at a later stage (Fig. 5a3), beginning at hour 24, and was thus termed “late upregulated”, with only three Wnt factors: Wnts1 , 2 and A , which are closely related in a Wnt family cladistics analysis as reported by Hensel et al [72] but are more distantly related according to Kusserow et al [73]. This clustering of different pathway components indicates a pattern of co-regulation, elucidation of which may be important for deciphering the different stages of the oral vs. aboral patterning process in regeneration in the future studies.Fig.…”
BackgroundThe ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.ResultsIn order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.ConclusionsThis work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.
“…The third cluster contained genes that were upregulated at a later stage (Fig. 5a3), beginning at hour 24, and was thus termed “late upregulated”, with only three Wnt factors: Wnts1 , 2 and A , which are closely related in a Wnt family cladistics analysis as reported by Hensel et al [72] but are more distantly related according to Kusserow et al [73]. This clustering of different pathway components indicates a pattern of co-regulation, elucidation of which may be important for deciphering the different stages of the oral vs. aboral patterning process in regeneration in the future studies.Fig.…”
BackgroundThe ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.ResultsIn order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.ConclusionsThis work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.
“…It is possible that CK1 kinases were first linked to canonical Wnt signaling and then adopted by the core PCP factors, or they may be generally associated with Fz-mediated processes and their functions evolved with the added complexity of additional Fz-mediated signaling features. It should be interesting to address such questions in primitive organisms, like hydra, that require Wnt-signaling (Hensel et al, 2014; Holstein, 2008; Lengfeld et al, 2009; Philipp et al, 2009) but have fewer isoforms of the respective genes.…”
Epithelial tissues are polarized along two axes. In addition to apical-basal polarity they are often polarized within the plane of the epithelium, so-called Planar Cell Polarity (PCP). PCP depends upon Wnt/Frizzled (Fz) signaling factors, including Fz itself and Van Gogh (Vang/Vangl). We sought to understand how Vang interaction with other core PCP factors affects Vang function. We find that Fz induces Vang phosphorylation in a cell-autonomous manner. Vang phosphorylation occurs on conserved N-terminal serine/threonine residues, is mediated by CK1ε/Dco and is critical for polarized membrane localization of Vang and other PCP proteins. This regulatory mechanism does not require Fz signaling through Dishevelled, and thus represents a cell-autonomous upstream interaction between Fz and Vang. Furthermore, this signaling event appears to be related to Wnt5a-mediated Vangl2 phosphorylation during mouse limb patterning, and may thus be a general mechanism underlying Wnt-regulated PCP establishment.
“…Cnidarian dickkopf ( dkk ) sequences were mined from both NCBI's nr protein and Compagen (Hemmrich and Bosch ) databases and aligned using ClustalΩ (Sievers et al ). DE expressed Wnt ligands were combined with cnidarian Wnt sequences recently published by Hensel et al (), as well as those available on NCBI's nr protein database, and aligned with the L‐insi alignment algorithm in Mafft (Katoh et al ). Medusozoan sequences of membrane bound frizzled receptors were mined from NCBI's nr protein database and aligned using Mafft with the L‐insi alignment algorithm (Katoh et al ).…”
Hydrozoans are known for their complex life cycles, alternating between benthic, asexually reproducing polyps and pelagic, sexually reproducing medusae. Although patterning in hydrozoan polyps has been well studied, little is known about the signaling mechanisms governing medusa development. In order to investigate the role of Wnt signaling in medusa development, we use RNA-Seq data collected from three discrete life cycle stages of Podocoryna carnea to assemble, annotate, and assess enrichment and differential expression (DE) of Wnt pathway elements in P. carnea's transcriptome. Enrichment analyses revealed a statistically significant enrichment of DE Wnt signaling transcripts in the transcriptome of P. carnea, of which, the vast majority of these were significantly up-regulated in developing and adult medusae stages. Whole mount in situ hybridization (ISH) reveals co-expression of the Wnt ligand, Wnt3, and a membrane bound Wnt receptor, frizzled3, at the distal and oral ends of the developmental axes of medusae and polyps in P. carnea. DE and ISH results presented here reveal expression of Wnt signaling components consistent with it playing a role in medusa development. Specifically, Wnt ligand expression in the oral region suggests that the Wnt pathway may play a role in medusa patterning, similar to that of polyps. Previous Wnt expression studies in hydrozoan taxa with reduced medusa have failed to detect co-expression of Wnt3 and a frizzled receptor at their truncated developmental axes, suggesting that down regulation of Wnt pathway elements may play a key role in the loss of the medusa life cycle stage in hydrozoan evolution.
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