WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra

Abstract

Members of the Wnt/wingless family of secreted proteins act as short-range inducers and long-range organizers during axis formation, organogenesis and tumorigenesis in many developing tissues. Wnt signalling pathways are conserved in nematodes, insects and vertebrates. Despite its developmental significance, the evolutionary origin of Wnt signalling is unclear. Here we describe the molecular characterization of members of the Wnt signalling pathway--Wnt, Dishevelled, GSK3, beta-Catenin and Tcf/Lef--in Hydra, a member of the evolutionarily old metazoan phylum Cnidaria. Wnt and Tcf are expressed in the putative Hydra head organizer, the upper part of the hypostome. Wnt, beta-Catenin and Tcf are transcriptionally upregulated when head organizers are established early in bud formation and head regeneration. Wnt and Tcf expression domains also define head organizers created by de novo pattern formation in aggregates. Our results indicate that Wnt signalling may be involved in axis formation in Hydra and support the idea that it was central in the evolution of axial differentiation in early multicellular animals.

The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration

“…Work over the past 10 years has shown that Hydra relies on the activation of the Wnt-βcatenin pathway to regenerate its head [33][34][35][36][37][38][39] . However this activation dramatically varies according to the amputation level 39 : Indeed after decapitation Wnt3 is rapidly and strongly up-regulated in the epithelial cells 33,37 , whereas after mid-gastric bisection the Wnt3 protein is first detected in the interstitial cells that undergo apoptosis-induced compensatory proliferation (see GLOSSARY) and subsequently Wnt3 is up-regulated in the epithelial cells 37,39 .…”

“…However this activation dramatically varies according to the amputation level 39 : Indeed after decapitation Wnt3 is rapidly and strongly up-regulated in the epithelial cells 33,37 , whereas after mid-gastric bisection the Wnt3 protein is first detected in the interstitial cells that undergo apoptosis-induced compensatory proliferation (see GLOSSARY) and subsequently Wnt3 is up-regulated in the epithelial cells 37,39 . This single or dual mode of Wnt-βcatenin activation in fact reflects two different processes for regenerating a head, morphallactic after decapitation, epimorphic-like after mid-gastric bisection (see GLOSSARY).…”

Expression of the AmphiTcf gene in amphioxus: Insights into the evolution of the TCF/LEF gene family during vertebrate evolution

“…In this respect, amphioxus resembles several other invertebrates, which have only a single TCF/LEF genenamely Pop1 in Caenorhabditis (Lin et al, 1995), Pangolin in Drosophila (van de Wetering et al, 1997), Tcf in hydra (Hobmayer et al, 2000), Tcf/Lef in sea urchins (Huang et al, 2000), and Tcf/Lef in ascidian tunicates (Satou and Satoh, 2005). In contrast, four such genes are present in most vertebrates (Korinek et al, 1998): Tcf1 (synonymously as Tcf7), Lef1 (essentially Tcf2), Tcf3, and Tcf4.…”

Entre homéostasie et développement, quelles stratégies pour régénérer ?

“…En effet, pendant une très courte période, le cytoplasme de ces cellules apparaît fortement Wnt3 immunopositif. Cependant cette phase immédiate et transitoire de surproduction de la protéine Wnt3 ne semble pas être sous contrôle transcriptionnel dans la mesure où une augmentation significative de l'abondance des transcrits n'est détectée que quelques heures plus tard (Hobmayer et al, 2000;Chera et al, 2009;Lengfeld et al, 2009). Un scénario probable est que la protéine Wnt3 est en fait déjà présente dans les cellules qui vont mourir, vraisembablement séquestrée dans un complexe dont la conformation, la cohésion ou la composition est modifiée par suite du stress de l'amputation.…”

“…Régulation monophasique ou biphasique de la voie Wnt3 au cours de la régénération de la tête en fonction du niveau d'amputation L'analyse de la régulation temporo-spatiale du gène Wnt3 après décapitation et après bissection migastrique a effectivement montré une surexpression dans les cellules épithéliales du bourgeon, précoce après décapitation (dès une heure), retardée après bissection mi-gastrique, les transcrits étant fortement détectés à partir de trois heures (Hobmayer et al, 2000;Chera et al, 2009;Lengfeld et al, 2009). 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).…”