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.
Self-organization has been demonstrated in a variety of systems ranging from chemical-molecular to ecosystem levels, and evidence is accumulating that it is also fundamental for animal development. Yet, self-organization can be approached experimentally in only a few animal systems. Cells isolated from the simple metazoan Hydra can aggregate and form a complete animal by self-organization. By using this experimental system, we found that clusters of 5-15 epithelial cells are necessary and sufficient to form de novo head-organizing centers in an aggregate. Such organizers presumably arise by a community effect from a small number of cells that express the conserved HyBra1 and HyWnt genes. These local sources then act to pattern and instruct the surrounding cells as well as generate a field of lateral inhibition that ranges up to 1,000 m. We propose that conserved patterning systems in higher animals originate from extremely robust and flexible molecular self-organizing systems that were selected for during early metazoan evolution.A nimal development is commonly explained in terms of hierarchical genetic cascades that begin with an initial asymmetry based on either maternal or external cues. In Drosophila, for instance, complex cellular interactions during oogenesis eventually lead to the local deposition of maternal messages in the oocyte that determine the body axes (1, 2). In the Xenopus embryo, a pre-established animal-vegetal asymmetry in the egg and sperm entry point determine the location of the anterior-posterior and the dorsoventral axes by locally initiating genetic cascades that lead to the formation of the future organizer (3, 4). Less clear is how an organizer is set up in tissue without inherent asymmetry or external cues.Only a few animal systems are amenable to the experimental analysis of self-organization during development (5-7). The simple metazoan Hydra is particularly useful in this context, because its body plan and any positional information can be completely destroyed and re-established in dissociationreaggregation studies. Hydra consists of a single axis with a head and foot at either end of a tubular body column. The axial pattern of the animal is maintained by a gradient of head formation competence, commonly referred to as the head activation gradient (8), or source density gradient (9). The term gradient of head formation competence, or more simply gradient of head competence, is in line with current terminology and will be used in this work. (The term head activation will be used for the actual process of head formation.) This head competence gradient reflects the ability of tissue of the body column to form a head either on bisection leading to head regeneration at the apical end of the lower half, or on transplantation of a piece of the body column to the body column of a second animal. The gradient is maximal near the head decreasing down the body column and is a relatively stable property of the body column (8). Head formation in the body column is prevented by a head inhibition...
TheHydranervous system is the paradigm of a simple nerve net. Nerve cells inHydra, as in many cnidarian polyps, are organized in a nerve net extending throughout the body column. This nerve net is required for control of spontaneous behavior: elimination of nerve cells leads to polyps that do not move and are incapable of capturing and ingesting prey (Campbell, 1976). We have re-examined the structure of theHydranerve net by immunostaining fixed polyps with a novel pan-neuronal antibody that stains all nerve cells. Confocal imaging shows that there are two distinct nerve nets, one in the ectoderm and one in the endoderm, with the unexpected absence of nerve cells in the endoderm of the tentacles. The nerve nets in the ectoderm and endoderm do not contact each other. High-resolution images show that the nerve nets consist of bundles of parallel overlapping neurites. Transmission and serial block face scanning electron microscopy show that nerve bundles in the ectoderm are closely associated with ectodermal muscle processes. Nerve bundles in the endoderm are separate from muscle processes. The occurrence of bundles of neurites supports a model for continuous growth and differentiation of the nerve net by lateral addition of new nerve cells to the existing net. This model was confirmed by tracking newly differentiated nerve cells.
The Hydra nervous system is the paradigm of a “simple nerve net”. Nerve cells in Hydra, as in many cnidarian polyps, are organized in a nerve net extending throughout the body column. This nerve net is required for control of spontaneous behavior: elimination of nerve cells leads to polyps that do not move and are incapable of capturing and ingesting prey (Campbell, 1976). We have re-examined the structure of the Hydra nerve net by immunostaining fixed polyps with a novel pan-neuronal antibody that stains all nerve cells. Confocal imaging shows that there are two distinct nerve nets, one in the ectoderm and one in the endoderm, with the unexpected absence of nerve cells in the endoderm of the tentacles. The nerve nets in the ectoderm and endoderm do not contact each other. High-resolution images show that the nerve nets consist of bundles of parallel overlapping neurites. Transmission and serial block face scanning electron microscopy show that nerve bundles in the ectoderm are closely associated with ectodermal muscle processes. Nerve bundles in the endoderm are separate from muscle processes. The occurrence of bundles of neurites supports a model for continuous growth and differentiation of the nerve net by lateral addition of new nerve cells to the existing net. This model was confirmed by tracking newly differentiated nerve cells.
The Hydra nervous system is the paradigm of a “simple nerve net”. Nerve cells in Hydra, as in many cnidarian polyps, are organized in a nerve net extending throughout the body column. This nerve net is required for control of spontaneous behavior: elimination of nerve cells leads to polyps that do not move and are incapable of capturing and ingesting prey (Campbell, 1976). We have re-examined the structure of the Hydra nerve net by immunostaining fixed polyps with a novel pan-neuronal antibody that stains all nerve cells. Confocal imaging shows that there are two distinct nerve nets, one in the ectoderm and one in the endoderm, with the unexpected absence of nerve cells in the endoderm of the tentacles. The nerve nets in the ectoderm and endoderm do not contact each other. High-resolution images show that the nerve nets consist of bundles of parallel overlapping neurites. Transmission and serial block face scanning electron microscopy show that nerve bundles in the ectoderm are closely associated with ectodermal muscle processes. Nerve bundles in the endoderm are separate from muscle processes. The occurrence of bundles of neurites supports a model for continuous growth and differentiation of the nerve net by lateral addition of new nerve cells to the existing net. This model was confirmed by tracking newly differentiated nerve cells.
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