A WNT of things to come: Evolution of Wnt signaling and polarity in cnidarians

Lee, Patricia N.; Pang, Kevin; Matus, David Q.; Martindale, Mark Q.

doi:10.1016/j.semcdb.2006.05.002

Cited by 170 publications

(196 citation statements)

References 66 publications

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“…Recent work revealed that almost all bilaterian wnt gene subfamilies are present in cnidarians (Kusserow et al, 2005;Lee et al, 2006 unpublished work from the HR Bode, B Hobmayer and TW Holstein labs) suggesting that the main genes of the Wnt pathways are present in cnidarians.…”

Section: Members Of Cnidarian Wnt Signallingmentioning

confidence: 99%

“…These include orthologs of b-catenin (Hobmayer et al, 1996), GSK-3b, Tcf/Lef, Dsh, APC and Axin from the Wnt/ b-catenin pathway , Flamingo, Van Gogh, and JNK from the Wnt/PCP (planar cell polarity) pathway; and CamKII and PKC from the Wnt/Ca 2 þ pathway (Lee et al, 2006), but also for casein kinase 1a, 1d, 1g 2 , 1g 3 and 1e (T Lengfeld and TW Holstein, unpublished), which are all known to act in Wnt signalling (Price, 2006;Strutt et al, 2006). Furthermore, the evidences indicating Nematostella and Hydra have several kinds of receptors for canonical and non-canonical Wnts have now started to accumulate.…”

Section: Receptors and Intracellular Components Of Wnt Signallingmentioning

confidence: 99%

“…An analysis of the function of gsk-3b during gametogenesis indicates that an inhibition of Wnt signalling is crucial for oogenesis (Rentzsch et al, 2005). Transcripts of fzd, b-cat, and tcf are maternally supplied and persist throughout embryogenesis (Frobius et al, 2003), while wnt transcripts appear at the onset of gastrulation in Nematostella and other cnidarians (Kusserow et al, 2005;Lee et al, 2006;Plickert et al, 2006). However, it remains unclear whether one of the wnt genes is involved the early steps of embryogenesis.…”

Section: Wnt Signalling In Gastrulationmentioning

confidence: 99%

“…In Nematostella, nvDkk1/2/4 is first expressed at the gastrula stage in the aboral ectoderm, at the pole opposite that of the nvwnt expression domains (Lee et al, 2006), suggestive of a role in general limiting the range of Wnt activity. In late planula larvae and early polyps, nvDkk1/2/4 is also expressed in the endoderm of the developing mesenteries but is still absent from the oral-most regions of the animal (Lee et al, 2006).…”

Section: A Modulation Of Wnt Signalling In Cnidarians?mentioning

confidence: 99%

“…In late planula larvae and early polyps, nvDkk1/2/4 is also expressed in the endoderm of the developing mesenteries but is still absent from the oral-most regions of the animal (Lee et al, 2006). In addition to the sFRP and Dkk sequences, an anthozoan ortholog of another vertebrate Wnt antagonist, WIF-1, has been identified in EST data sets from Nematostella and Acropora .…”

Section: A Modulation Of Wnt Signalling In Cnidarians?mentioning

confidence: 99%

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The Wnt code: cnidarians signal the way

et al. 2006

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Cnidarians are the simplest metazoans with a nervous system. They are well known for their regeneration capacity, which is based on the restoration of a signalling centre (organizer). Recent work has identified the canonical Wnt pathway in the freshwater polyp Hydra, where it acts in organizer formation and regeneration. Wnt signalling is also essential for cnidarian embryogenesis. In the sea anemone Nematostella vectensis 11 of the 12 known wnt gene subfamilies were identified. Different wnt genes exhibit serial and overlapping expression domains along the oral-aboral axis of the embryo (the 'wnt code'). This is reminiscent of the hox code (cluster) in bilaterian embryogenesis that is, however, absent in cnidarians. It is proposed that the common ancestor of cnidarians and bilaterians invented a set of wnt genes that patterned the ancient main body axis. Major antagonists of Wnt ligands (e.g. Dkk 1/2/4) that were previously known only from chordates, are also present in cnidarians and exhibit a similar conserved function. The unexpectedly high level of genetic complexity of wnt genes evolved in early multi-cellular animals about 650 Myr ago and suggests a radical expansion of the genetic repertoire, concurrent with the evolution of multi-cellularity and the diversification of eumetazoan body plans. Oncogene (2006Oncogene ( ) 25, 7450-7460. doi:10.1038 Keywords: Wnt signalling; regeneration; axis formation; Hydra; Nematostella; cnidaria Cnidarians are genetically complexThe Cnidaria is an ancient metazoan phylum of diploblastic animals including freshwater polyps and hydroids, sea anemones and corals, and jellyfish. All cnidarians share the same simple body plan that is reminiscent of an early bilaterian gastrula. However, they are lacking the mesoderm and possess only two germ layers, an outer ectoderm and inner endoderm that are separated by an acellular mesogloea. Cnidaria are a sister-group to the Bilateria (Figure 1), and the fossil record reveals that cnidarians are >500 Myr old (Chen et al., 2000(Chen et al., , 2002Conway Morris, 2000). They are of crucial importance for unravelling the origin and evolution of major signalling pathways in animal evolution.There are two major genetic model systems for cnidarians: the well-known freshwater polyp Hydra (Steele, 2006) and the starlet sea anemone Nematostella vectensis (Holland, 2004;Darling et al., 2005), which was introduced by the pioneering work of Cadet Hand (Hand and Uhlinger, 1992). Recent EST projects in these and some other cnidarian taxa have revealed an astonishing and unexpected genetic complexity of cnidarians. Analyses of ESTs from the anthozoans Acropora millepora and Nematostella vectensis have lead to the identification of 16 571 non-redundant ESTs and 12 547 predicted peptides across the two species (7484 from Nematostella and 5063 from Acropora (Miller et al., 2005;Technau et al., 2005). Both data sets are far from saturation and one can estimate that anthozoan genomes are likely to contain 25 000 genes, which is in the same range as vertebr...

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Section: Members Of Cnidarian Wnt Signallingmentioning

confidence: 99%

Section: Receptors and Intracellular Components Of Wnt Signallingmentioning

confidence: 99%

Section: Wnt Signalling In Gastrulationmentioning

confidence: 99%

Section: A Modulation Of Wnt Signalling In Cnidarians?mentioning

confidence: 99%

Section: A Modulation Of Wnt Signalling In Cnidarians?mentioning

confidence: 99%

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The Wnt code: cnidarians signal the way

et al. 2006

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The basal chordate amphioxus as a simple model for elucidating developmental mechanisms in vertebrates

Koop

Holland

2008

Birth Defects Research Pt C

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This review examines the basal chordate, amphioxus, as a simple model for providing insights into the development and evolution of the vertebrates, with which it shares many features, including a pharynx perforated with gill slits, a dorsal nerve cord, segmented muscles, and a notochord. Conversely, amphioxus is simpler than vertebrates in lacking neural crest and paired cephalic sensory organs. Amphioxus embryos are less derived than those of vertebrates, because it lacks large quantities of yolk and/or extra-embryonic tissues. Embryogenesis involves only a simple folding of tissue layers. In addition, the amphioxus genome lacks the large-scale gene duplications of vertebrates. However, in spite of the comparative simplicity of amphioxus, its developmental mechanisms are proving to be highly conserved with those of vertebrates. Thus, studies of amphioxus development can shed light on similar, but more complex, development of vertebrates. Such studies are especially interesting for their insights into the genetic basis of craniofacial birth defects in humans.

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Beta‐catenin and axis formation in planarians

Meinhardt

2009

BioEssays

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In three recent articles it was shown that beta-catenin is crucial for the establishment and the maintenance of the overall polarity and especially for the character 'posterior' in planarians. If the transcription of the beta-catenin gene was silenced by RNA interference, the overall polarity is lost, and in regenerating fragments a posterior blastema displays anterior characters by forming eyes and anterior ganglia. An attempt is made to integrate these new data, well-known older observations, and observations from other regenerating systems into an outline of a model that will clarify our current understanding as well as highlight areas still to be developed.

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A WNT of things to come: Evolution of Wnt signaling and polarity in cnidarians

Cited by 170 publications

References 66 publications

The Wnt code: cnidarians signal the way

The Wnt code: cnidarians signal the way

The basal chordate amphioxus as a simple model for elucidating developmental mechanisms in vertebrates

Beta‐catenin and axis formation in planarians

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