Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis

Abstract

Animal evolution is closely linked to the emergence of the nervous system. At present it is unknown how the basic mechanisms of neural induction and formation of central nervous systems evolved. We addressed this question in Nematostella vectensis, a member of cnidarians, the ancient sister group of bilaterians. We found that β-catenin signalling is crucial for the early induction of the embryonic nervous system. β-Catenin activity at the blastopore induces specific neurogenic genes required for development of the oral nervous system. β-Catenin signalling induces also Bmp signalling, which, at later larval stages, becomes indispensible for the maintenance and asymmetric patterning of the oral nervous system along the primary and secondary (directive) axes. We hypothesize that the consecutive and functionally linked involvement of β-catenin and Bmp signalling in the formation of the cnidarian oral nervous system reflects an ancestral mechanism that evolved before the cnidarian/bilaterian split.

Back to the Basics: Cnidarians Start to Fire

“…For example, in the sea anemone Nematostella vectensis neurons are generated throughout the ectoderm as well as in the endoderm [98]. The molecular control of neurogenesis is remarkably similar to that in vertebrates: Notch signalling controls the number of neural progenitor cells, soxB and bHLH transcription factor encoding genes regulate their further development and Wnt signaling gradients are involved in the patterning of the nervous system [99–101]. The spatially broad neurogenic potential of cnidarians poses specific challenges for the developmental control of neurogenesis, e.g.…”

Localization of planarian β-CATENIN-1 reveals multiple roles during anterior-posterior regeneration and organogenesis

“…Our findings thus support three major roles of β-catenin-1 in anterior regeneration: (1) the specification and maintenance of the anterior signaling center, defined by the tiprelated expression of notum (Petersen and Reddien, 2011) and other genes (Chen et al, 2013;Gaviño et al, 2013;Roberts-Galbraith and Newmark, 2013;Scimone et al, 2014;Vásquez-Doorman and Petersen, 2014;Vogg et al, 2014) (Fig. 6A,B); (2) the regeneration of the brain, through the regulation of the brain-related expression of notum (Hill and Petersen, 2015); and (3) the specification of different neuronal cell types, as described in most animal models (Ciani and Salinas, 2005;Hari et al, 2002;Lewis et al, 2004;Machon et al, 2003;Watanabe et al, 2014;Yu and Malenka, 2003;Zechner et al, 2003).…”

“…During early animal embryogenesis, β-catenin specifies the site of endoderm internalization and promotes posterior fates in most studied systems (Byrum and Wikramanayake, 2013;Darras et al, 2011;Haegel et al, 1995;Henry et al, 2008;Lee et al, 2006;Logan et al, 1999;Srivastava et al, 2014;Wikramanayake et al, 2003). In later stages of development, the canonical Wnt pathway influences the formation of multiple cell types, tissues and organ systems (Aulehla et al, 2008;Grigoryan et al, 2008;Hari et al, 2002;Holland et al, 2005;Kiecker and Niehrs, 2001; Lewis et al, 2004;Petersen and Reddien, 2009a;Schneider and Bowerman, 2007;Tan et al, 2006;Watanabe et al, 2014), and most prominently, the anteroposterior (AP) patterning of the vertebrate central nervous system (Ciani and Salinas, 2005). In adult organisms β-catenin is essential for tissue homeostasis and its deregulation leads to degenerative diseases and cancers (Clevers and Nusse, 2012).…”

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

“…In addition to this role in axis specification, Matus et al [41] propose that the co-expression of transcripts from multiple TGF-b signalling components in the early endoderm of N. vectensis suggests an important role for this pathway in patterning germ layer identity. Indeed, studies of spatial expression of TGF-b components across basal metazoans have uncovered multiple roles for TGF-b signalling in the development and maintenance of differentiated cell types, including: regenerating head cells, tentacles, the oral nerve ring and adult endo/gastrodermal cells in cnidarians [47,48,55,56] and the embryonic pigment ring in sponges [30]. Finally, pharmacological studies in the facultatively symbiotic sea anemone Aiptasia pallida suggest a potential role for TGF-b in facilitating the interaction between the cnidarian host and algal symbiont [57].…”