Formation of the head organizer in hydra involves the canonical Wnt pathway

Broun, Mariya; Gee, Lydia; Reinhardt, Beate; Bode, Hans R.

doi:10.1242/dev.01848

Cited by 259 publications

(322 citation statements)

References 56 publications

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“…Hydra's head organizer is located at the apical tip of the hypostome and was described for the first time by Browne (1909). When this hypostomal tissue is transplanted to ectopic positions along the body column of a host polyp it organizes a secondary body axis by recruiting host tissue (Technau et al, 2000;Broun and Bode, 2002;Broun et al, 2005). The hypostome is homologous to the blastopore of the cnidarian embryo and can be compared to the vertebrate organizer based on a conserved set of genes expressed in both organizers.…”

Section: Wnt Signalling During Organizer Formation and Regenerationmentioning

confidence: 99%

“…Hyb-cat protein is localized at the apical membrane and in nuclei of epithelial cells. However, cells in the hypostome have much higher levels of nuclear b-catenin than cells in the body column ( Figure 3a) (Cramer von Laue, 2003;Broun et al, 2005) indicating that Wnt signalling is active in the hypostome. Wnt/b-catenin signalling is also active during bud formation.…”

Section: Wnt Signalling In the Hydra Head Organizermentioning

confidence: 99%

“…The function of Wnt signalling in axial patterning of Hydra has been recently elegantly demonstrated by pharmacological experiments using alsterpaullone, a kinase inhibitor that specifically blocks GSK-3b function in Hydra (Broun et al, 2005). Earlier experiments using LiCl treatment of Hydra (Hassel et al, 1993) already indicated that an inhibition of GSK-3b activity (Klein et al, 1996) can stimulate head formation.…”

Section: Activation Of Wnt/b-catenin Signallingmentioning

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: Wnt Signalling During Organizer Formation and Regenerationmentioning

confidence: 99%

Section: Wnt Signalling In the Hydra Head Organizermentioning

confidence: 99%

Section: Activation Of Wnt/b-catenin Signallingmentioning

confidence: 99%

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The Wnt code: cnidarians signal the way

et al. 2006

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“…Both showed that activation of STK (Cardenas et al 2000;Cardenas and Salgado 2003;Manuel et al 2006;Arvizu et al 2006), GSK3 (Broun et al 2005), PKC, Pi3K, ERK 1-2 (Manuel et al 2006;Arvizu et al 2006), MAPK and RSK (Kaloulis et al 2004;Chera et al 2011) are indeed necessary over the first hours following bisection (see…”

Section: Activation Of Stk Pi3k Erk and Mapk Pathways During Head Bmentioning

confidence: 99%

Injury-induced asymmetric cell death as a driving force for head regeneration in Hydra

Galliot

2012

Dev Genes Evol

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The freshwater Hydra polyp provides a unique model system to decipher the mechanisms underlying adult regeneration. Indeed a single cut initiates two distinct regenerative processes, foot regeneration on one side, head regeneration on the other side, the latter relying on the rapid formation of a local head organizer. Two aspects are discussed here, the asymmetric cellular remodeling induced by mid-gastric bisection and the signaling events that trigger head organizer formation. In head-regenerating tips (but not in foot ones) a wave of cell death takes place immediately, leading the apoptotic cells to transiently release Wnt3 and activate the β-catenin pathway in the neighboring cycling cells to push them through mitosis. This process, which mimics the apoptosis-induced compensatory proliferation process deciphered in Drosophila larvae regenerating their discs likely corresponds to an evolutionarily-conserved mechanism, also at work in Xenopus tadpoles regenerating their tale or mice regenerating their skin or liver. How is this process generated in Hydra? Several studies pointed to the necessary activation of the ERK 1-2 and MAPK pathways during early head regeneration and indeed ERK 1-2 inhibition or RSK, CREB, CBP knockdown prevent injury-induced apoptosis and head regeneration. The current scenario involves an asymmetric activation of the MAPK/CREB pathway to trigger injury-induced apoptosis in the interstitial cells, and, in the epithelial cells a CREB/CBP-dependent transcriptional activation of early genes essential for head organizing activity as wnt3, HyBra1, prdl-a. The question now is how bisection in the rather uniform central region of the polyp can generate this immediately asymmetric signaling.

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“…Cette induction de l'expression du gène Wnt3 correspond au moment où l'activité organisatrice commence à apparaître dans le bourgeon, comme l'ont montré les expériences de transplantation (MacWilliams, 1983;Broun et al, 2005;Lengfeld et al, 2009). Parmi les différents gènes de type Wnt, Wnt3 est effectivement le premier dont l'expression est induite, ce qui suggère que Wnt3 joue un rôle instructeur dans la formation du centre organisateur.…”

Section: Les Cellules Apoptotiques Source De Signalisation De La Voiunclassified

Entre homéostasie et développement, quelles stratégies pour régénérer ?

Galliot

2011

Biologie Aujourd'hui

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Formation of the head organizer in hydra involves the canonical Wnt pathway

Abstract: characteristics of the head organizer, as measured by transplantation experiments, and by the expression of genes associated with the head organizer. Hence, the role of the canonical Wnt pathway for the initiation of axis formation was established early in metazoan evolution.

Cited by 259 publications

References 56 publications

The Wnt code: cnidarians signal the way

The Wnt code: cnidarians signal the way

Injury-induced asymmetric cell death as a driving force for head regeneration in Hydra

Entre homéostasie et développement, quelles stratégies pour régénérer ?

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