Developmental Signaling in Hydra: What Does It Take to Build a “Simple” Animal?

Abstract

Developmental processes in multicellular animals depend on an array of signal transduction pathways. Studies of model organisms have identified a number of such pathways and dissected them in detail. However, these model organisms are all bilaterians. Investigations of the roles of signal transduction pathways in the early-diverging metazoan Hydra have revealed that a number of the well-known developmental signaling pathways were already in place in the last common ancestor of Hydra and bilaterians. In addition to these shared pathways, it appears that developmental processes in Hydra make use of pathways involving a variety of peptides. Such pathways have not yet been identified as developmental regulators in more recently diverged animals. In this review I will summarize work to date on developmental signaling pathways in Hydra and discuss the future directions in which such work will need to proceed to realize the potential that lies in this simple animal.

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

“…In fact, after decapitation, head regeneration is initiated from a region that, prior to amputation, is populated with apical progenitors actively dividing and differentiating, until they migrate or get displaced to the tentacles. By contrast, after mid-gastric bisection, head regeneration takes place in a less determined region where proliferating stem cells are not yet committed to an apical or basal fate 8 . Therefore Hydra provides a model system where at least three distinct types of regeneration can be studied, i) foot regeneration that does not require a complex morphogenesis and hence could be considered as a form of tissue repair, ii) apical head regeneration and iii) basal head regeneration that follow two distinct routes that differ in their dependence upon cell division -morphallactic after decapitation but epimorphic-like after mid-gastric bisection.…”

“…Despite this simple anatomy, Hydra is already equipped to elaborate complex behaviors based on neuromuscular transmission 7 . Its two tissue layers contain a dozen cell types that correspond to the basic cell types shared by eumetazoans: typical epithelial cells that also differentiate myofibrils, gland cells that secrete digestive enzymes (also named 'pancreatic cells'), mucous cells, sensory-motor neurons and interneurons named ganglion cells 8 . In addition, cnidarians differentiate phylum-specific mechanosensory cells named cnidocytes (or nematocytes) that resemble the bilaterian mechano-sensory cells thanks to their cnidocil, but also differentiate, as a phylumspecific trait, a venom capsule (the nematocyst or cnidocyst).…”

“…That the Hydra model system is highly amenable to address this question is supported by the vast cellular knowledge based on transplantation, cell-lineage and quantitative cellular analyses that has been accumulated over the past 40 years 8,12,[40][41][42][43][44][45] . These studies identified the differentiation pathways of most cell types in homeostatic and regenerative conditions.…”

Entre homéostasie et développement, quelles stratégies pour régénérer ?

“…Au contraire, après bissection migastrique, l'hypostome se forme d'abord suivi des tentacules (Technau & Holstein, 1995). Cette différence peut s'expliquer par des différences quantitatives et qualitatives significatives entre ces deux régions: d'une part les cellules souches sont beaucoup plus nombreuses dans la région centrale de la colonne corporelle que dans les régions apicale et distale (David & Plotnick, 1980), d'autre part les cellules précurseurs situées à proximité des régions apicales et distales ont entamé leur détermination tandis qu'au niveau mi-gastrique, les cellules souches ne sont pas engagées vers une voie de différenciation apicale ou basale (Steele, 2002).…”

“…En effet l'Hydre utilise la prolifération compensatrice induite par l'apoptose seulement après bissection au niveau mi-gastrique, tandis que ce processus n'est pas activé après décapitation. Ces deux régions à partir desquelles la régénération de la tête est activée sont en fait très différentes: la région mi-gastrique contient une forte proportion de cellules souches tandis que la partie supérieure de la colonne gastrique contient peu de cellules souches mais des cellules progénitrices en voie de différenciation et des cellules différenciées (David & Plotnick, 1980;Steele, 2002). Ces résultats suggèrent fortement que, comme dans le cas de la Drosophile, l'environnement cellulaire influence de façon irrémédiable la réponse induite par la blessure qui lance le programme de régénération de la tête.…”