ABSTRACT
Stabilization of beta-catenin by inhibiting the activity of glycogen synthase kinase-3beta has been shown to initiate axis formation or axial patterning processes in many bilaterians. In hydra, the head organizer is located in the hypostome, the apical portion of the head. Treatment of hydra with alsterpaullone, a specific inhibitor of glycogen synthase kinase-3beta, results in the body column acquiring 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.
Subject(s)
Head/growth & development , Hydra/growth & development , Hydra/metabolism , Intercellular Signaling Peptides and Proteins/metabolism , Signal Transduction , Animals , Benzazepines/pharmacology , Cell Cycle/drug effects , Cell Membrane/drug effects , Cell Membrane/metabolism , Cell Nucleus/drug effects , Cell Nucleus/metabolism , Cytoskeletal Proteins/metabolism , Glycogen Synthase Kinase 3/antagonists & inhibitors , Glycogen Synthase Kinase 3/genetics , Glycogen Synthase Kinase 3/metabolism , Glycogen Synthase Kinase 3 beta , Head/physiology , Hydra/cytology , Hydra/drug effects , Indoles/pharmacology , Intercellular Signaling Peptides and Proteins/genetics , Intracellular Signaling Peptides and Proteins/pharmacology , Signal Transduction/drug effects , Trans-Activators/metabolism , Wnt Proteins , beta CateninABSTRACT
Developmental gradients play a central role in axial patterning in hydra. As part of the effort towards elucidating the molecular basis of these gradients as well as investigating the evolution of the mechanisms underlying axial patterning, genes encoding signaling molecules are under investigation. We report the isolation and characterization of HyBMP5-8b, a BMP5-8 orthologue, from hydra. Processes governing axial patterning are continuously active in adult hydra. Expression patterns of HyBMP5-8b in normal animals and during bud formation, hydra's asexual form of reproduction, were examined. These patterns, coupled with changes in patterns of expression in manipulated tissues during head regeneration, foot regeneration as well as under conditions that alter the positional value gradient indicate that the gene is active in two different processes. The gene plays a role in tentacle formation and in patterning the lower end of the body axis.
Subject(s)
Body Patterning/genetics , Bone Morphogenetic Proteins/genetics , Hydra/embryology , Amino Acid Sequence , Animals , Base Sequence , Blotting, Northern , Blotting, Southern , Bone Morphogenetic Protein 5 , Bone Morphogenetic Proteins/chemistry , DNA Primers , In Situ Hybridization , Molecular Sequence Data , Morphogenesis , Phylogeny , Sequence Homology, Amino AcidABSTRACT
A central process in the maintenance of axial patterning in the adult hydra is the head activation gradient, i.e. the potential to form a secondary axis, which is maximal in the head and is graded down the body column. Earlier evidence suggested that this gradient was based on a single parameter. Using transplantation experiments, we provide evidence that the hypostome, the apical part of the head, has the characteristics of an organizer in that it has the capacity to induce host tissue to form most of the second axis. By contrast, tissue of the body column has a self-organizing capacity, but not an inductive capacity. That the inductive capacity is confined to the hypostome is supported by experiments involving a hypostome-contact graft. The hypostome, but not the body column, transmits a signal(s) leading to the formation of a second axis. In addition, variations of the transplantation grafts and hypostome-contact grafts provide evidence for several characteristics of the organizer. The inductive capacity of the head and the self-organizing capacity of the body column are based on different pathways. Head inhibition, yya signal produced in the head and transmitted to the body column to prevent head formation, represses the effect of the inducing signal by interfering with formation of the hypostome/organizer. These results indicate that the organizer characteristics of the hypostome of an adult hydra are similar to those of the organizer region of vertebrate embryos. They also indicate that the Gierer-Meinhardt model provides a reasonable framework for the mechanisms that underlie the organizer and its activities. In addition, the results suggest that a region of an embryo or adult with the characteristics of an organizer arose early in metazoan evolution.
