Cnidarians: An evolutionarily conserved model system for regeneration?

Holstein, Thomas W.; Hobmayer, Engelbert; Technau, Ulrich

doi:10.1002/dvdy.10227

Cited by 196 publications

(133 citation statements)

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“…It is also crucial to clarify the localization of other intracellular Wnt signalling components (Dsh, GSK-3b Axin), as well as that of Wnt-responsive genes, for example chordin and brachyury Rentzsch et al, 2006). In that respect it should be pointed out that a Nematostella brachyury ortholog, NemBra1, is expressed at the site where gastrulation starts, together with wnts and b-catenin, suggesting a feedback loop between wnt and brachyury (Holstein et al, 2003). Also chordin mRNA first appear at the blastopore , reflecting conserved coupling of BMP and Wnt signalling at the invagination site.…”

Section: Wnt Signalling In Gastrulationmentioning

confidence: 99%

“…Hydra polyps can be dissociated into suspensions of single cells so that the original polarity of the animal is completely disorganized (Technau et al, 2000). Within 24 h ectoderm and endoderm form, after that new head organizers form de novo, organizing the surrounding tissue into new body axes that separate into individual polyps (Technau et al, 2000;Holstein et al, 2003). Similar to bud formation and head regenerates, hytcf and hyb-cat are homogeneously expressed before hywnt3a in early reaggregates (24 h) and are later downregulated except in regions where new head organizers are forming.…”

Section: Wnt/b-catenin Signalling During Regenerationmentioning

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 In Gastrulationmentioning

confidence: 99%

Section: Wnt/b-catenin Signalling During Regenerationmentioning

confidence: 99%

The Wnt code: cnidarians signal the way

et al. 2006

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“…Genetic cascades involved in developmental processes are highly conserved among bilaterians Gilbert (2000), but also from cnidarians to bilaterians Galliot (2000), Spring et al (2002), Holstein et al (2003). Among genes that show head-specific regulation, prdl-a displays a very unique dual regulation : On one hand in the hydra adult polyp, prdl-a is strictly expressed in neurons located in the ectodermal layer, mainly in the apical region, on the other hand during early hours of head regeneration, prdl-a is transiently expressed in a distinct cell lineage, likely epithelial endodermal cells of the stump, at a time and at a place where raising organizer activity was mapped by transplantation experiments MacWilliams (1983).…”

Section: Did Neurogenesis and Patterning Activity Evolved Simultaneoumentioning

confidence: 99%

Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

2004

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Cnidarians represent the first animal phylum with an organized nervous system and a complex active behavior. The hydra nervous system is formed of sensory-motoneurons, ganglia neurons and mechanoreceptor cells named nematocytes, which all differentiate from a common stem cell. The neurons are organized as a nerve net and a subset of neurons participate in a more complex structure, the nerve ring that was identified in most cnidarian species at the base of the tentacles. In order to better understand the genetic control of this neuronal network, we analysed the expression of evolutionarily-conserved regulatory genes in the hydra nervous system. The PRD-CLASS homeogene, prdl-b, and the nuclear orphan receptor, hyCOUP-TF, are expressed at strong levels in proliferating nematoblasts, a lineage where they were found repressed during patterning and morphogenesis, and at low levels in distinct subsets of neurons. Interestingly, PRD-CLASS homeobox and COUP-TF genes are also expressed during neurogenesis in bilaterians, suggesting that mechanoreceptor and neuronal cells derive from a common ancestral cell. Moreover, the PRD-CLASS homeobox gene prdl-a, the ANTP-CLASS homeobox gene msh, and the thrombospondin-related gene TSP1, which are expressed in distinct subset of neurons in the adult polyp, are also expressed during early budding and/or head regeneration. These data strengthen the fact that two distinct regulations, one for neurogenesis and another for patterning, already apply to these regulatory genes, a feature also identified in bilaterian related-genes.

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“…There are remarkable examples of tissue regeneration in the animal kingdom and they are valuable tools in the study of organ regeneration (Holstein et al, 2003;Poss et al, 2003). For unknown reasons, humans have lost this dramatic ability to regenerate tissues.…”

Section: Organ Regeneration and Repairmentioning

confidence: 99%