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Retinoic acid signaling and neurogenic niche regulation in the developing peripheral nervous system of the cephalochordate amphioxus

Cellular and Molecular Life Sciences volume 75, pages2407–2429(2018)Cite this article

Abstract

The retinoic acid (RA) signaling pathway regulates axial patterning and neurogenesis in the developing central nervous system (CNS) of chordates, but little is known about its roles during peripheral nervous system (PNS) formation and about how these roles might have evolved. This study assesses the requirement of RA signaling for establishing a functional PNS in the cephalochordate amphioxus, the best available stand-in for the ancestral chordate condition. Pharmacological manipulation of RA signaling levels during embryogenesis reduces the ability of amphioxus larvae to respond to sensory stimulation and alters the number and distribution of ectodermal sensory neurons (ESNs) in a stage- and context-dependent manner. Using gene expression assays combined with immunohistochemistry, we show that this is because RA signaling specifically acts on a small population of soxb1c-expressing ESN progenitors, which form a neurogenic niche in the trunk ectoderm, to modulate ESN production during elongation of the larval body. Our findings reveal an important role for RA signaling in regulating neurogenic niche activity in the larval amphioxus PNS. Although only few studies have addressed this issue so far, comparable RA signaling functions have been reported for neurogenic niches in the CNS and in certain neurogenic placode derivatives of vertebrates. Accordingly, the here-described mechanism is likely a conserved feature of chordate embryonic and adult neural development.

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Acknowledgements

The authors would like to thank Thurston C. Lacalli, Nicholas D. Holland, and Linda Z. Holland for fruitful discussions. We are also grateful to Ram Reshef for his vital support with administrative issues.

Funding

This work was supported by a grant from the Agence Nationale de la Recherche (ANR-11-JSV2-002-01) and by funds from the Réseau André Picard (ANR-11-IDEX-0004-02, Sorbonne Universities) to MS and by a National Grant of the University of Genoa (2015) to SC. EZ was a doctoral fellow of the Studienstiftung der Deutschen Wirtschaft (SDW).

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Affiliations

  1. Laboratoire de Biologie du Développement de Villefranche-sur-Mer, Observatoire Océanologique de Villefranche-sur-Mer, Sorbonne Universités, UPMC Université Paris 06, CNRS, 181 Chemin du Lazaret, 06230, Villefranche-sur-Mer, France
    • Elisabeth Zieger
    • , Nicolas S. M. Robert
    • , Jenifer C. Croce
    •  & Michael Schubert
  2. Department of Earth, Environment and Life Sciences (Dipartimento di Scienze della Terra dell’Ambiente e della Vita, DISTAV), University of Genoa, Viale Benedetto XV 5, 16132, Genoa, Italy
    • Greta Garbarino
    •  & Simona Candiani
  3. Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, 11529, Taiwan
    • Jr-Kai Yu
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Contributions

EZ designed and performed experiments, analyzed and interpreted data, and wrote the manuscript. GG supported the collection of gene expression data, NSMR carried out phylogenetic analyses, and JKY contributed important advice concerning the selection of candidate genes. JKY, JCC, and SC provided methodological assistance, supported data analyses, and commented the manuscript. MS designed and supervised the study, analyzed and interpreted data, and wrote the manuscript. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Michael Schubert.

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All data used in this study are included in this published article and its supplementary materials.

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The authors declare that they have no competing interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Additional file 1: Movie S1. Movie showing reactions of amphioxus larvae at 48 hpf (hours post fertilization) to mechanical stimulation. Response A = quick muscular swimming movement away from the stimulus. Response B = intense wiggling and bending movements without clear directionality. Response C = short wiggling motion on the spot. Response D = short disconnected twitches or bends on the spot. Response E = no visible reaction (MP4 26973 kb)

Additional file 2: Movie S2. Movie showing responses of amphioxus larvae at 48 hpf (hours post fertilization) to chemical stimulation. As indicated in the movie, the amphioxus embryos were exposed to dimethyl sulfoxide (DMSO) (Control), the retinoic acid receptor (RAR) antagonist BMS493 or all-trans retinoic acid (RA), starting from treatment time points (t) at 6 or 24 hpf. Upon reaching the 48 hpf stage, the larvae were further exposed to agarose blocks, which had either been dissolved in artificial seawater (negative control) or in artificial seawater supplemented with 0.1 M l-glutamate (MP4 88999 kb)

Additional file 1: Movie S1. Movie showing reactions of amphioxus larvae at 48 hpf (hours post fertilization) to mechanical stimulation. Response A = quick muscular swimming movement away from the stimulus. Response B = intense wiggling and bending movements without clear directionality. Response C = short wiggling motion on the spot. Response D = short disconnected twitches or bends on the spot. Response E = no visible reaction (MP4 26973 kb)

Additional file 2: Movie S2. Movie showing responses of amphioxus larvae at 48 hpf (hours post fertilization) to chemical stimulation. As indicated in the movie, the amphioxus embryos were exposed to dimethyl sulfoxide (DMSO) (Control), the retinoic acid receptor (RAR) antagonist BMS493 or all-trans retinoic acid (RA), starting from treatment time points (t) at 6 or 24 hpf. Upon reaching the 48 hpf stage, the larvae were further exposed to agarose blocks, which had either been dissolved in artificial seawater (negative control) or in artificial seawater supplemented with 0.1 M l-glutamate (MP4 88999 kb)

Additional file 3: Figure S1. Effects of retinoic acid (RA) signaling alterations on glutamate chemoreception and larval circling/spiraling behavior in amphioxus. Amphioxus embryos were exposed to dimethyl sulfoxide (DMSO) (Control, green bars), the RA receptor (RAR) antagonist BMS493 (blue bars) or all-trans RA (red bars), starting from treatment time points (t) at 6 or 24 hpf (hours post fertilization). Subsequently, by 48 hpf, the animals were further exposed to agarose blocks, which had either been dissolved in artificial seawater (negative control, dark-colored bars) or in artificial seawater supplemented with 0.1 M l-glutamate (light-colored bars). The size of the colored bars indicates the average number of circles amphioxus larvae swam without interruption and the error bars indicate the standard deviation (σ). The total number (n) of animals counted is given at the base of each colored bar. Asterisks (*) above an error bar indicate that the difference between this condition and the corresponding control is statistically significant with a p-value < 0.05 (one asterisk, *) or with a p-value < 0.01 (two asterisks, **). Only larvae that had passed by the agarose block within a 1 cm radius and within 0.5 to 10 min after introduction of the agarose block were taken into consideration. For RA treatments at 6 hpf, circling/spiraling was rarely observed, precluding statistical analyses (PNG 89 kb)

Additional file 4: Table S1. GenBank accession numbers of sequences used for phylogenetic analyses (DOCX 38 kb)

Additional file 5: Figure S2. Maximum-likelihood phylogenies for a ELAV, b TLX, and c SOXB1. Trees were inferred using RAxML with 1000 rapid bootstraps (PDF 198 kb)

Additional file 6: Figure S3. Effects of retinoic acid (RA) signaling alterations on the development of vglut-expressing cells in amphioxus. Larvae are shown in lateral (a-i) or dorsal (d’-i’) view with their anterior ends directed towards the right. Developmental stages are given as hours post fertilization (hpf). Embryos have been treated from the treatment stage (t) at 6 hpf with dimethyl sulfoxide (DMSO) (Control), the RA receptor (RAR) antagonist BMS493 or all-trans RA, as indicated. All scale bars are 50 µm. The scale bar in a applies also to b,c, the scale bar in d applies also to d’,e,e’,f,f’, and the scale bar in g applies also to g’,h,h’,i,i’ (TIFF 1376 kb)

Additional file 7: Figure S4. Expression of hu/elav during amphioxus development. a-e Lateral views of amphioxus embryos and larvae at different developmental stages from 15 to 36 hpf (hours post fertilization). Anterior ends are directed towards the right. a’-e’ Dorsal views of the amphioxus embryos and larvae shown, respectively, in a-e. c-e Dotted boxes indicate the ectodermal domain containing a conspicuously high density of hu/elav-expressing ectodermal sensory neuron progenitors (ESNPs). All scale bars are 50 µm. The scale bar in a, b, c, d, and e, respectively, also applies to a’, b’, c’, d’, and e’ (TIFF 3994 kb)

Additional file 8: Figure S5. Expression of tlx during amphioxus development. a-e Lateral views of amphioxus embryos and larvae at different developmental stages from 15 to 36 hpf (hours post fertilization). Anterior ends are directed towards the right. a’-e’ Dorsal views of the amphioxus embryos and larvae shown, respectively, in a-e. c-e Dotted boxes indicate the ectodermal domain containing a conspicuously high density of ectodermal sensory neurons (ESNs) (compare with Fig. 3), hu/elav-expressing ESN progenitors (ESNPs) (compare with Additional file 7: Figure S4) as well as soxb1c-expressing ESNPs (compare with Additional file 9: Figure S6), but not tlx-expressing ESNPs. All scale bars are 50 µm. The scale bar in a, b, c, d, and e, respectively, also applies to a’, b’, c’, d’, and e’ (TIFF 3531 kb)

Additional file 9: Figure S6. Expression of soxb1c during amphioxus development. a-e Lateral views of amphioxus embryos and larvae at different developmental stages from 15 to 36 hpf (hours post fertilization). The anterior is directed towards the right. a’-e’ Dorsal views of the amphioxus embryos and larvae shown, respectively, in a-e. The images in c-e’ are focused on soxb1c expression in the ectoderm. Dotted boxes indicate the ectodermal domain containing a conspicuously high density of soxb1c-expressing ectodermal sensory neuron progenitors (ESNPs). All scale bars are 50 µm. The scale bar in a, b, c, d, and e, respectively, also applies to a’, b’, c’, d’, and e’ (TIFF 3617 kb)

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Zieger, E., Garbarino, G., Robert, N.S.M. et al. Retinoic acid signaling and neurogenic niche regulation in the developing peripheral nervous system of the cephalochordate amphioxus. Cell. Mol. Life Sci. 75, 2407–2429 (2018) doi:10.1007/s00018-017-2734-3

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Keywords

  • Evolution of development
  • Lancelet
  • Neural stem cells
  • Retinoid pathway
  • Sensory functions