TY - JOUR
T1 - The pre-vertebrate origins of neurogenic placodes
AU - Abitua, Philip Barron
AU - Gainous, T. Blair
AU - Kaczmarczyk, Angela N.
AU - Winchell, Christopher J.
AU - Hudson, Clare
AU - Kamata, Kaori
AU - Nakagawa, Masashi
AU - Tsuda, Motoyuki
AU - Kusakabe, Takehiro G.
AU - Levine, Michael
N1 - Funding Information:
Acknowledgements We thank Y. Miyamoto and M. Kotera for technical assistance and A.Stolfifor cloning Chordin.GFP. Thiswork was supported bya grantfromthe National Institutes of Health (NS076542) and by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (25650118, 25290067) and from the Japan Space Forum (h160179). Portions of this study were facilitated by the National Bio-Resource Project of the Ministry of Education, Culture, Sports, Science and Technology in Japan. The work of C.H. in the laboratory of H. Yasuo was funded by the Agence Nationale de la Recherche (ANR-09-BLAN-0013-01). P.B.A. and A.N.K. were supported by predoctoral fellowships from the National Science Foundation and California Institute for Regenerative Medicine, respectively.
Publisher Copyright:
© 2015 Macmillan Publishers Limited.
PY - 2015/8/27
Y1 - 2015/8/27
N2 - 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.
AB - 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.
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U2 - 10.1038/nature14657
DO - 10.1038/nature14657
M3 - Article
C2 - 26258298
AN - SCOPUS:84940533489
SN - 0028-0836
VL - 524
SP - 462
EP - 465
JO - Nature
JF - Nature
IS - 7566
ER -