Hydra, a model system to trace the emergence of boundaries in developing eumetazoans

Abstract

In developing embryos, boundary formation between neighbouring groups of cells is essential to establish compartments which later fulfil specialized functions. The ability to form such boundaries has likely developed early in animal evolution -due to functional requirements imposed by the necessity to separate tissues which protect the animal, take up food or ensure propagation. Essential for boundary formation are local cues which may be provided by the intersection of diffusible molecules or set locally by activation of membrane-bound receptors and transcription factors. In the simple diploblastic Hydra, a representative of the basally branching metazoan Cnidaria, tissue boundaries are morphologically detectable between the body column and terminally differentiated head and foot structures. In adult polyps, these borders correspond to sharp lines of differential gene expression. They form de novo during regeneration and budding of a young polyp. Functional studies strongly suggest the involvement of FGFR/Notch signalling in the establishment of the parent-bud boundary, and it is very likely that these pathways interact with the WNT and BMP systems. How boundaries in the head and foot regions are generated is still unclear. Expression patterns of transcription factors like Cngsc, HyAlx, HyBra, HyOtx, Prdl-a, CnNK2 and Manacle show strong position dependency and may be involved in regulating gene expression on either side of the boundaries, by interpreting positional information during their formation and maintenance. Due to its simplicity, the easy accessibility to pharmacological interference and, recently, transgenesis, Hydra is an interesting prebilaterian model system to study the emergence of boundary-forming mechanisms during evolution.

Stemness in Hydra - a current perspective

“…1). The boundaries of the corresponding body regions, where terminal differentiation occurs, are defined by the expression of genes that act in positiondependent differentiation (see Böttger and Hassel, 2012). Regeneration experiments and tracking of GFP-positive epithelial cells in transgenic polyps have demonstrated that every proliferating cell of the body column has the potential to give rise to all three types of differentiated cells (Wittlieb et al, 2006).…”

Hydra, a model system for environmental studies

“…The mouth and tentacles are called the hydranth (Holdway, 2005). The rest of this organism is known as the column and has four distinctive sections: the gastric section located between the tentacles and the first (apical) bud; the budding section which produces the buds; the peduncle which is located between the lowest bud and basal disc and the basal disc which is the foot-like formation (Holdway, 2005; see also in this issue Böttger and Hassel, 2012). This structural complexity, simpler than vertebrates with central nervous system and specialized organs, but more complex than cultured cells, makes Hydra comparable to a living tissue whose cells and distant regions are physiologically connected (Galliot et al, 2006).…”

“…This gives the opportunity to examine the outcomes of energy allocation upon various environmental stresses on the fitness of Hydra. Under asexual reproduction Hydra that are well fed use the excess of cells that are produced by forming buds in the middle of their body (Müller, 1996;Böttger and Hassel, 2012). The ability of Hydra to regenerate is due to the constantly proliferating epithelial and interstitial cells in its body column, in the absence of bisection this constant cell renewal allows the animal to bud at a rapid rate (Hoffmeister-Ullerich, 2007).…”

The Nematocyst: a molecular map of the Cnidarian stinging organelle

“…The maturation step is clearly detectable by in situ hybridization experiments for structural molecular components of the nematocyst , Engel et al, 2001. Gene expression for these molecules is restricted to the body column of the animal and terminated at a sharp border below the head (see also in this issue Böttger and Hassel, 2012). In the tentacles mature nematocysts are incorporated into large battery cells that harbor several types of capsules in a close arrangement (Fig.…”