The pre-vertebrate origins of neurogenic placodes

Abitua, Philip B.; Gainous, T. Blair; Kaczmarczyk, Angela N.; Winchell, Christopher J.; Hudson, C. S.; Kamata, Kaori; Nakagawa, Masashi; Tsuda, Motoyuki; Kusakabe, Takehiro; Levine, Michael

doi:10.1038/nature14657

Cited by 111 publications

(108 citation statements)

References 46 publications

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“…S4), and urochordates, similar to its role in the vertebrate NPB and PPE. The PPE is the neurogenic ectoderm anterolateral to the NPB, and is considered the epidermal subdomain of the vertebrate neural border that mostly contributes to cranial sensory systems (1,37). The PPE also gives rise to mechanosensing hair cells of lateral lines in the trunk of anamniote vertebrates and those in vertebrate inner ears (1).…”

Section: Discussionmentioning

confidence: 99%

Conserved gene regulatory module specifies lateral neural borders across bilaterians

Zhao

Horie

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The lateral neural plate border (NPB), the neural part of the vertebrate neural border, is composed of central nervous system (CNS) progenitors and peripheral nervous system (PNS) progenitors. In invertebrates, PNS progenitors are also juxtaposed to the lateral boundary of the CNS. Whether there are conserved molecular mechanisms determining vertebrate and invertebrate lateral neural borders remains unclear. Using single-cell-resolution gene-expression profiling and genetic analysis, we present evidence that orthologs of the NPB specification module specify the invertebrate lateral neural border, which is composed of CNS and PNS progenitors. First, like in vertebrates, the conserved neuroectoderm lateral border specifier Msx/vab-15 specifies lateral neuroblasts in Caenorhabditis elegans. Second, orthologs of the vertebrate NPB specification module (Msx/vab-15, Pax3/7/pax-3, and Zic/ref-2) are significantly enriched in worm lateral neuroblasts. In addition, like in other bilaterians, the expression domain of Msx/vab-15 is more lateral than those of Pax3/7/pax-3 and Zic/ref-2 in C. elegans. Third, we show that Msx/vab-15 regulates the development of mechanosensory neurons derived from lateral neural progenitors in multiple invertebrate species, including C. elegans, Drosophila melanogaster, and Ciona intestinalis. We also identify a novel lateral neural border specifier, ZNF703/tlp-1, which functions synergistically with Msx/vab-15 in both C. elegans and Xenopus laevis. These data suggest a common origin of the molecular mechanism specifying lateral neural borders across bilaterians.C. elegans | neural plate border | neural border | Msx/vab-15 | ZNF703/tlp-1 T he vertebrate neural border is a transient embryonic domain located between the neural plate and nonneurogenic ectoderm from late gastrulation to early neurulation. The neural border is composed of the lateral neural plate border (NPB) and preplacode ectoderm (PPE) subdomains (1, 2). The NPB and PPE give rise to the neural crest and placode, respectively, both of which undergo epithelial-to-mesenchymal transition/delamination, migrate in prototypical paths, and give rise to the peripheral nervous system (PNS) and many other cell types (3, 4). However, the NPB and PPE also have many different features (5). For example, the PPE is confined to the anterior half of embryos and does not contribute to the central nervous system (CNS), whereas the NPB is the lateral border of the whole neural plate and consists not only of progenitors for the PNS but also those for the CNS in the dorsal neural tube. The juxtaposed localization of the CNS neuroectoderm and PNS progenitors also occurs in the trunk of invertebrate embryos such as nematodes, arthropods, annelids, and urochordates (6-9), reminiscent of vertebrate NPB. In Caenorhabditis elegans, lateral neuroblasts (P, Q, and V5 cells) are located between the embryonic CNS and skin from the birth of these cells (10). In addition, worm lateral neuroblasts possess several key cellular and developmental features of vertebra...

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Section: Discussionmentioning

confidence: 99%

Conserved gene regulatory module specifies lateral neural borders across bilaterians

Zhao

Horie

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Neural crest precursors have been claimed to exist in lancelets and ascidians based on molecular and neuroanatomical evidence (Abitua, et al, 2015, Abitua, et al, 2012, Fritzsch and Northcutt, 1993a, Häming, Simoes-Costa, Uy, Valencia, Sauka-Spengler and Bronner-Fraser, 2011), but in these taxa they do not form peripheral ganglia per se but rather other neural crest-typical derivatives such as (scattered) peripheral sensory neurons and mesenchymal cell types (Pasini et al 2012, Häming et al 2011). The evidence for the presence of bona fide autonomic ganglia in cyclostomes is scanty and then only in association with the vagus nerve.…”

Section: Evolutionary History Of Neural Crest-derived Sympathetic Andmentioning

confidence: 99%

Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature

2017

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Several concepts developed in the 19th century have formed the basis of much of our neuroanatomical teaching today. Not all of these were based on solid evidence nor have withstood the test of time. Recent evidence on the evolution and development of the autonomic nervous system, combined with molecular insights into the development and diversification of motor neurons, challenges some of the ideas held for over 100 years about the organization of autonomic motor outflow. This review provides an overview of the original ideas and quality of supporting data and contrasts this with more accurate and in depth insight provided by studies using modern techniques. Several lines of data demonstrate that branchial motor neurons are a distinct motor neuron population within the vertebrate brainstem, from which parasympathetic visceral motor neurons of the brainstem evolved. The lack of an autonomic nervous system in jawless vertebrates implies that spinal visceral motor neurons evolved out of spinal somatic motor neurons. Consistent with the evolutionary origin of brainstem parasympathetic motor neurons out of branchial motor neurons and spinal sympathetic motor neurons out of spinal motor neurons is the recent revision of the organization of the autonomic nervous system into a cranial parasympathetic and a spinal sympathetic division (that is, there is no sacral parasympathetic division). We propose a new nomenclature that takes all of these new insights into account and avoids the conceptual misunderstandings and incorrect interpretation of limited and technically inferior data inherent in the old nomenclature.

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“…Although Ciona embryos might also have a rudimentary neural crest and rudimentary placodes (Abitua et al, 2015(Abitua et al, , 2012Ikeda et al, 2013;Manni et al, 2004;Stolfi et al, 2015a;Wagner and Levine, 2012;Waki et al, 2015), Tfap2-r.b expression is downregulated in these lineages by Fgf signaling. Because Tfap2 is also expressed only in the non-neural ectoderm of embryos of another basal chordate, Branchiostoma floridae (Meulemans and Bronner-Fraser, 2002), the ancestral function of Tfap2 might be to specify epidermal fate.…”

Section: Downregulation Of Tfap2-rb In Non-epidermal Cellsmentioning

confidence: 99%

Tfap2 and Sox1/2/3 cooperatively specify ectodermal fates in ascidian embryos

et al. 2016

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Epidermis and neural tissues differentiate from the ectoderm in animal embryos. Although epidermal fate is thought to be induced in vertebrate embryos, embryological evidence has indicated that no intercellular interactions during early stages are required for epidermal fate in ascidian embryos. To test this hypothesis, we determined the gene regulatory circuits for epidermal and neural specification in the ascidian embryo. These circuits started with Tfap2-r.b and Sox1/2/3, which are expressed in the ectodermal lineage immediately after zygotic genome activation. Tfap2-r.b expression was diminished in the neural lineages upon activation of fibroblast growth factor signaling, which is known to induce neural fate, and sustained only in the epidermal lineage. Tfap2-r. b specified the epidermal fate cooperatively with Dlx

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The pre-vertebrate origins of neurogenic placodes

Cited by 111 publications

References 46 publications

Conserved gene regulatory module specifies lateral neural borders across bilaterians

Conserved gene regulatory module specifies lateral neural borders across bilaterians

Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature

Tfap2 and Sox1/2/3 cooperatively specify ectodermal fates in ascidian embryos

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