TitleThe pre-vertebrate origins of neurogenic placodes.
Publication TypeJournal Article
Year of Publication2015
AuthorsAbitua, PBarron, T Gainous, B, Kaczmarczyk, AN, Winchell, CJ, Hudson, C, Kamata, K, Nakagawa, M, Tsuda, M, Kusakabe, TG, Levine, M
Date Published2015 Aug 27
KeywordsAnimals, Body Patterning, Bone Morphogenetic Proteins, Ciona intestinalis, Ectoderm, Gonadotropin-Releasing Hormone, HEK293 Cells, Homeodomain Proteins, Humans, Intracellular Signaling Peptides and Proteins, Larva, Molecular Sequence Data, Neurons, Protein Tyrosine Phosphatases, Receptors, G-Protein-Coupled, Vertebrates

The sudden appearance of the neural crest and neurogenic placodes in early branching vertebrates has puzzled biologists for over a century. These embryonic tissues contribute to the development of the cranium and associated sensory organs, which were crucial for the evolution of the vertebrate "new head". A previous study suggests that rudimentary neural crest cells existed in ancestral chordates. However, the evolutionary origins of neurogenic placodes have remained obscure owing to a paucity of embryonic data from tunicates, the closest living relatives to those early vertebrates. Here we show that the tunicate Ciona intestinalis exhibits a proto-placodal ectoderm (PPE) that requires inhibition of bone morphogenetic protein (BMP) and expresses the key regulatory determinant Six1/2 and its co-factor Eya, a developmental process conserved across vertebrates. The Ciona PPE is shown to produce ciliated neurons that express genes for gonadotropin-releasing hormone (GnRH), a G-protein-coupled receptor for relaxin-3 (RXFP3) and a functional cyclic nucleotide-gated channel (CNGA), which suggests dual chemosensory and neurosecretory activities. These observations provide evidence that Ciona has a neurogenic proto-placode, which forms neurons that appear to be related to those derived from the olfactory placode and hypothalamic neurons of vertebrates. We discuss the possibility that the PPE-derived GnRH neurons of Ciona resemble an ancestral cell type, a progenitor to the complex neuronal circuit that integrates sensory information and neuroendocrine functions in vertebrates.

Alternate JournalNature