Patterning a multi-headed mutant in Hydractinia: enhancement of head formation and its phenotypic normalization.

Abstract

In a mutant strain of Hydractinia (Cnidaria: Hydrozoa), the polyps develop ectopic supernumerary tentacles and heads (hypostomes) after an initial phase of wild-type growth. In order to elucidate the molecular mechanisms implicated in the development of aberrant phenotypes, we tried to enhance or suppress the expressivity of this hypomorphic mutation by exposing subclones to factors supposedly influencing pattern formation. Upon iterated treatment with alsterpaullone, an inhibitor of GSK-3, the formation of additional, ectopic head structures and the budding of new polyps were dramatically accelerated and enhanced. The endogenous stoloninducing factor (SIF) had opposite effects by reducing head forming potential while increasing stolon-forming potential. SIF could be used to rescue extremely aberrant phenotypes. In these mutant colonies, long polyps with multiple heads eventually detach from stolons and lose the ability to regenerate stolons. Upon exposure to SIF, such free-floating multi-headed polyps resumed production of stolons and acquired wild-type morphology. We conclude that a canonical WNT signaling cascade is involved in patterning the body axis of polyps and in the initiation of budding, and that SIF counteracts this signaling system.

Wnt signaling in hydroid development: ectopic heads and giant buds induced by GSK-3beta inhibitors

“…GSK-3β is a downstream element in the cascade, but its blockage led to the establishment of upstream Wnt-expressing centers. This positive feedback loop corresponds aslo well to previous studies (Holstein et al, 2003;Müller et al, 2004b). Here we show that blockage of GSK-3β increases budding activity in terms of a novel experimental phenotype: not only more buds per stolon or per colony area are produced, but the size of the bud fields is tremendously enlarged.…”

Hydractinia, a pioneering model for stem cell biology and reprogramming somatic cells to pluripotency

“…3 D-1) depends on both tips sharing the same histocompatibility alleles. If applied to the growing medium at supra-natural concentration, SIF causes complete transformation of polyps into stolons (Lange and Müller, 1991;Müller et al, 2004b).…”

“…Like in Hydra, blocking GSK3 generally leads to oralization. Polyps of Hydractinia treated with paullones (Müller et al, 2004b) transform to phenocopies of a multi-headed mutant (Fig. 2D) (Müller, 2002).…”

Wnt signaling promotes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration

“…In cnidarians, components of the canonical Wnt signaling pathway are thought to be involved in the establishment of the anteriorposterior (AP) axis (Amiel and Houliston, 2009;Broun et al, 2005;Hobmayer et al, 2000;Kusserow et al, 2005;Lee et al, 2007;Müller et al, 2004b;Plickert et al, 2006). The above studies, and others, have shown that several Wnt genes are expressed asymmetrically in the adult form, the polyp, with the highest expression levels around the mouth area (i.e.…”

“…Nuclear -catenin was reported in the corresponding pole of the Nematostella embryo (Wikramanayake et al, 2003). Finally, it has been shown that misexpression of Wnt3, frizzled (Momose et al, 2008;Momose and Houliston, 2007) and -catenin (Gee et al, 2010), as well as blocking of GSK3 (Hassel et al, 1993;Müller et al, 2004b), affects AP axis formation, suggesting that a Wnt-mediated organizer acts to specify the position of the cnidarian head (Broun et al, 2005). There is no functional data in the literature on the effect of Wnt pathway inhibition on aboral structures (Tanaka and Weidinger, 2008).…”