The pre-vertebrate origins of neurogenic placodes
Nature. 2015 Aug 27;524(7566):462-5. doi: 10.1038/nature14657. Epub 2015 Aug 10.
Philip Barron Abitua 1 , T Blair Gainous 1 , Angela N Kaczmarczyk 1 , Christopher J Winchell 1 , Clare Hudson 2 , Kaori Kamata 3 , Masashi Nakagawa 3 , Motoyuki Tsuda 3 , Takehiro G Kusakabe 4 , Michael Levine 1
1 Center for Integrative Genomics, Division of Genetics, Genomics and Development, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA.
2 Sorbonne Universités, Université Pierre et Marie Curie, Centre National de la Recherche Scientifique, Laboratoire de Biologie du Développement de Villefranche-sur-mer, Observatoire Océanologique, 06230 Villefranche-sur-mer, France.
3 Graduate School of Life Science, University of Hyogo, Kamigori, Hyogo 678-1297, Japan.
4 Institute for Integrative Neurobiology and Department of Biology, Faculty of Science and Engineering, Konan University, Kobe 658-8501, Japan.
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.
Body Patterning
Ciona intestinalis / cytology*
Ciona intestinalis / embryology*
Ciona intestinalis / genetics
Ciona intestinalis / metabolism
Ectoderm / metabolism
Gonadotropin-Releasing Hormone / metabolism
HEK293 Cells
Homeodomain Proteins / metabolism
Intracellular Signaling Peptides and Proteins / metabolism
Larva / cytology
Larva / metabolism
Neurons / cytology*
Neurons / metabolism
Protein Tyrosine Phosphatases / metabolism
Receptors, G-Protein-Coupled / metabolism
Vertebrates / anatomy & histology*
Vertebrates / embryology*
Vertebrates / physiology
Homeodomain Proteins
Intracellular Signaling Peptides and Proteins
Receptors, G-Protein-Coupled
Gonadotropin-Releasing Hormone
GENBANK/KR902348
R01 NS076542/NS/NINDS NIH HHS/United States
NS076542/NS/NINDS NIH HHS/United States