Abstract
Because head regeneration occurs in nerve-free hydra mutants, neurogenesis was regarded as dispensable for this process. Here, in wild-type hydra, we tested the function of the ParaHox gsx homolog gene, cnox-2, which is a specific marker for bipotent neuronal progenitors, expressed in cycling interstitial cells that give rise to apical neurons and gastric nematoblasts (i.e. sensory mechanoreceptor precursors). cnox-2 RNAi silencing leads to a dramatic downregulation of hyZic, prdl-a, gsc and cnASH, whereas hyCOUP-TF is upregulated. cnox-2 indeed acts as an upstream regulator of the neuronal and nematocyte differentiation pathways, as cnox-2(-) hydra display a drastic reduction in apical neurons and gastric nematoblasts, a disorganized apical nervous system and a decreased body size. During head regeneration, the locally restricted de novo neurogenesis that precedes head formation is cnox-2 dependent: cnox-2 expression is induced in neuronal precursors and differentiating neurons that appear in the regenerating tip; cnox-2 RNAi silencing reduces this de novo neurogenesis and delays head formation. Similarly, the disappearance of cnox-2(+) cells in sf-1 mutants also correlates with head regeneration blockade. Hence in wild-type hydra, head regeneration requires the cnox-2 neurogenic function. When neurogenesis is missing, an alternative, slower and less efficient, head developmental program is possibly activated.
Highlights
Hydra belongs to Cnidaria, a phylum that arose before bilaterians and provides model systems to trace back ancestral developmental processes, as such as apical and anterior patterning (Galliot and Miller, 2000), neuromuscular differentiation (Miljkovic-Licina et al, 2004; Seipel and Schmid, 2005) and regeneration (Holstein et al, 2003; Galliot et al, 2006)
The hydra nervous system is organized as a nerve net that extends throughout the animal and is made up of two cell lineages: the sensory mechanoreceptor cells, named nematocytes, and the neurons, with typical synapses (Westfall, 1996)
We have investigated the putative role of neurogenesis in head regeneration by dissecting the cellular and developmental regulation of cnox-2, the hydra gsx homolog gene
Summary
Hydra belongs to Cnidaria, a phylum that arose before bilaterians and provides model systems to trace back ancestral developmental processes, as such as apical and anterior patterning (Galliot and Miller, 2000), neuromuscular differentiation (Miljkovic-Licina et al, 2004; Seipel and Schmid, 2005) and regeneration (Holstein et al, 2003; Galliot et al, 2006). Throughout the animal, the body wall consists of two cell layers, the ectoderm and the endoderm, separated by an extracellular matrix called mesoglea These two cell layers are made up of myoepithelial cells and interstitial stem cells, which provide precursors for gland cells, neurons, nematocytes and germ cells. The hydra nervous system is organized as a nerve net that extends throughout the animal and is made up of two cell lineages: the sensory mechanoreceptor cells, named nematocytes, and the neurons, with typical synapses (Westfall, 1996). Those two cell types follow distinct differentiation pathways (Bode, 1996).
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