Frédéric Moret

Inserm

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Valérie Castellani

Université Claude Bernard Lyon 1

Muriel Bozon

Université Claude Bernard Lyon 1

Philippe Vernier

Université Paris-Sud

Karine Kindbeiter

Inserm

Isabelle Sanyas

Université Claude Bernard Lyon 1

Julien Falk

Centre National de la Recherche Scientifique

Ludovic Telley

University of Lausanne

Lionel Christiaen

University of Bergen

Karima Abouzid

Centre National de la Recherche Scientifique

Ahmad Bechara

Friedrich Miescher Institute

Cooperative Institutions

Centre National de la Recherche Scientifique

Inserm

Université Claude Bernard Lyon 1

Institut NeuroMyoGène

Laboratoire de Neurobiologie Cellulaire et Moléculaire

Sorbonne Université

Universitat de Barcelona

Centre de Génétique Moléculaire

Laboratoire de Génétique Cellulaire

Harvard University

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A balance of noncanonical Semaphorin signaling from the cerebrospinal fluid regulates apical cell dynamics during corticogenesis

Science Advances (2022)

Katrin Gerstmann Karine Kindbeiter Ludovic Telley Muriel Bozon Florie Reynaud

During corticogenesis, dynamic regulation of apical adhesion is fundamental to generate correct numbers and cell identities. While radial glial cells (RGCs) maintain basal and apical anchors, basal progenitors and neurons detach and settle at distal positions from the apical border. Whether diffusible signals delivered from the cerebrospinal fluid (CSF) contribute to the regulation of apical adhesion dynamics remains fully unknown. Secreted class 3 Semaphorins (Semas) trigger cell responses via Plexin-Neuropilin (Nrp) membrane receptor complexes. Here, we report that unconventional Sema3-Nrp preformed complexes are delivered by the CSF from sources including the choroid plexus to Plexin-expressing RGCs via their apical endfeet. Through analysis of mutant mouse models and various ex vivo assays mimicking ventricular delivery to RGCs, we found that two different complexes, Sema3B/Nrp2 and Sema3F/Nrp1, exert dual effects on apical endfeet dynamics, nuclei positioning, and RGC progeny. This reveals unexpected balance of CSF-delivered guidance molecules during cortical development.

Corticogenesis

Plexin

Apical membrane

10.1126/sciadv.abo4552

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Citations (7)

Contribution of the neuron-specific ATP1A3 to embryonic spinal circuit emergence

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Sarah Dinvaut S. Calvet Jean‐Christophe Comte Raphael Gury Olivier Pascual

Abstract The early neurodevelopmental contributions of ion pumps remain poorly characterized. Combining analysis of public human embryo single-cell transcriptomic datasets and an embryonic chicken model, we found a conserved differentiation sequence whereby spinal cord neurons switch on neuron-specific alpha3 subunit (ATP1A3) of Na + /K + ATPases. In the chicken model, ATP1A3 is distributed along axons and growth cones. Its knockdown alters axon pathfinding of dorsal interneurons (DIN) that wire spinocerebellar circuits. In mirror of reported electric field (EF)-driven cell migration, we found that DIN axons align in EFs, which was abolished by Na + /K + ATPase inhibitor Ouabain and ATP1A3 knockdown. We recorded an embryonic trans-neural-epithelial potential generating EF whose pharmacological and surgical manipulation mimicked ATP1A3 knock-down-induced altered DIN axon pathfinding. Using DINs transplantation paradigm, we found that ATP1A3 is required cell-autonomously for EF-mediated long-range guidance. Finally, dominant-negative ATP1A3 mutation causing an early ATP1A3 childhood disease disrupts this fundamental developmental process, revealing unexpected pathogenic mechanisms.

10.1101/2024.06.11.598491

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Nocturnal Behavior and RhythmicPeriodGene Expression in a Lancelet,Branchiostoma lanceolatum

Journal of Biological Rhythms (2008)

Christof Schomerus Horst‐Werner Korf Elke Laedtke Frédéric Moret Qian Zhang

The authors here present the first anatomical, molecular biological, and ethological data on the organization of the circadian system of a lancelet, Branchiostoma lanceolatum, a close invertebrate relative of vertebrates. B. lanceolatum was found to be a nocturnal animal and, since its rhythmic activity persisted under constant darkness, it also appears to possess an endogenous, circadian oscillator. The authors cloned a homolog of the clock gene Period (Per), which plays a central (inhibitory) role in the biochemical machinery of the circadian oscillators of both vertebrates and protostomians. This gene from B. lanceolatum was designated as amphiPer. Both the sequence of its cDNA and that of the predicted protein are more similar to those of the Per paralogs of vertebrates than to those of the single protostomian Per gene. A strong expression of amphiPer was found in a small cell group in the anterior neural tube. The amphiPer mRNA levels fluctuated in a rhythmic manner, being high early in the day and low late at night. The authors' data suggest a homology of the amphiPer expessing cells to the suprachiasmatic nucleus of vertebrates.

10.1177/0748730407313363

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Citations (10)

A midline switch of receptor processing regulates commissural axon guidance in vertebrates

Genes & Development (2010)

Homaira Nawabi Anne Briançon‐Marjollet Christopher Clark Isabelle Sanyas Hyota Takamatsu

Commissural axon guidance requires complex modulations of growth cone sensitivity to midline-derived cues, but underlying mechanisms in vertebrates remain largely unknown. By using combinations of ex vivo and in vivo approaches, we uncovered a molecular pathway controlling the gain of response to a midline repellent, Semaphorin3B (Sema3B). First, we provide evidence that Semaphorin3B/Plexin-A1 signaling participates in the guidance of commissural projections at the vertebrate ventral midline. Second, we show that, at the precrossing stage, commissural neurons synthesize the Neuropilin-2 and Plexin-A1 Semaphorin3B receptor subunits, but Plexin-A1 expression is prevented by a calpain1-mediated processing, resulting in silencing commissural responsiveness. Third, we report that, during floor plate (FP) in-growth, calpain1 activity is suppressed by local signals, allowing Plexin-A1 accumulation in the growth cone and sensitization to Sema3B. Finally, we show that the FP cue NrCAM mediates the switch of Plexin-A1 processing underlying growth cone sensitization to Sema3B. This reveals pathway-dependent modulation of guidance receptor processing as a novel mechanism for regulating guidance decisions at intermediate targets.

Plexin

Commissure

Growth cone

Ephrin

Floor plate

10.1101/gad.542510

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Citations (138)

Distribution of tyrosine hydroxylase, dopamine, and serotonin in the central nervous system of amphioxus (Branchiostoma lanceolatum): Implications for the evolution of catecholamine systems in vertebrates

The Journal of Comparative Neurology (2003)

Frédéric Moret J.-C. Guilland Sophie Coudouel Luc Rochette Philippe Vernier

Abstract To investigate the evolutionary transition that has shaped the catecholaminergic systems of vertebrates, the organization of catecholamine‐synthesizing neurons and the nature of the catecholamines were examined in the central nervous system of adult amphioxus ( Branchiostoma lanceolatum ), a cephalochordate. We isolated a gene transcript encoding tyrosine hydroxylase (TH), the limiting enzyme of catecholamine biosynthesis, and studied its distribution together with that of dopamine and serotonin. Dopamine and TH are found in the same neurons of which they are three separate populations. Two are located in the anterior brain, the first being dorsal and lying in a row and the second being more posterior and lateral. A third population comprising a few dorsal commissural neurons was found in the posterior brain. The anterior dopaminergic cells innervate the ventral commissure of the cephalic vesicle, the hindbrain, and the spinal cord. A serotonin‐containing cell group is located in the same plane as the second dopaminergic cell population but is more caudal, marking the probable transition between anterior brain and hindbrain, as deduced from gene expression patterns. The overall distribution of dopaminergic and serotoninergic systems is similar in amphioxus and vertebrate central nervous system and could be an ancestral character of chordates. As assayed by high‐performance liquid chromatrography and electrochemical detection, significant amounts of dopamine and octopamine, but not of noradrenaline, are present in amphioxus head. This finding is consistent with data obtained from most prostomian species. We conclude that the noradrenergic system is probably an innovation of vertebrates that appeared along with the neural crest and specific hindbrain nuclei. J. Comp. Neurol. 468:135–150, 2004. © 2003 Wiley‐Liss, Inc.

Hindbrain

10.1002/cne.10965

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Citations (59)

Performing Axon Orientation Assays with Secreted Semaphorins and Other Guidance Cues

Methods in molecular biology (2016)

Céline Delloye‐Bourgeois Frédéric Moret Valérie Castellani

Biological neural network

10.1007/978-1-4939-6448-2_17

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FAK–MAPK-dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse

The EMBO Journal (2008)

Ahmad Bechara Homaira Nawabi Frédéric Moret Avraham Yaron Eli Weaver

Plexin

SEMA3A

Growth cone

Neuropilin

10.1038/emboj.2008.86

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Citations (127)

Cerebrospinal fluid-derived Semaphorin3B orients neuroepithelial cell divisions in the apicobasal axis

Nature Communications (2015)

Elise Arbeille Florie Reynaud Isabelle Sanyas Muriel Bozon Karine Kindbeiter

The spatial orientation of cell divisions is fundamental for tissue architecture and homeostasis. Here we analysed neuroepithelial progenitors in the developing mouse spinal cord to determine whether extracellular signals orient the mitotic spindle. We report that Semaphorin3B (Sema3B) released from the floor plate and the nascent choroid plexus in the cerebrospinal fluid (CSF) controls progenitor division orientation. Delivery of exogenous Sema3B to neural progenitors after neural tube opening in living embryos promotes planar orientation of their division. Preventing progenitor access to cues present in the CSF by genetically engineered canal obstruction affects the proportion of planar and oblique divisions. Sema3B knockout phenocopies the loss of progenitor access to the CSF. Sema3B binds to the apical surface of mitotic progenitors and exerts its effect via Neuropilin receptors, GSK3 activation and subsequent inhibition of the microtubule stabilizer CRMP2. Thus, extrinsic control mediated by the Semaphorin signalling orients progenitor divisions in neurogenic zones. The spatial orientation of cell divisions is fundamental for tissue architecture and homeostasis but the extracellular cues regulating this process are largely unknown. Here, the authors show that Semaphorin3B released from the floor plate and the nascent choroid plexus controls progenitor division orientation in the developing mouse spinal cord.

Neuroepithelial cell

Floor plate

Progenitor

10.1038/ncomms7366

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Citations (35)

An unconventional cerebrospinal fluid-derived Semaphorin-signalling regulates apical progenitor dynamics in the developing neocortex

bioRxiv (Cold Spring Harbor Laboratory) (2020)

Katrin Gerstmann Karine Kindbeiter Ludovic Telley Muriel Bozon Camille Charoy

Summary In the embryonic brain, dynamic regulation of apical adhesion is fundamental to generate correct numbers and identity of precursors and neurons. Radial glial cells (RGC) in the cerebral cortex are tightly attached to adjacent neighbours. However, cells committed to differentiate reduce their adhesiveness to detach and settle at distal position from the apical border. Whether diffusible signals delivered from the cerebrospinal fluid (CSF) contribute to the regulation of apical adhesion dynamics remain fully unknown. Here we report that unconventional pre-formed complexes of class3-Semaphorins (Sema) and Neuropilins (Nrp) are released into the cerebrospinal fluid (CSF) from sources including the choroid plexus. Through analysis of mutant mouse models and various ex vivo assays, we propose that two different complexes, Sema3B/Nrp2 and Sema3F/Nrp1, bind to apical endfeet of RGCs, and exert dual regulation of their attachment, nuclei dynamics, that oppositely promotes or inhibits basal progenitor and neuron differentiation. This reveals unexpected contributions of CSF-delivered guidance molecules during cortical development.

Neocortex

Plexin

Progenitor

Compartment (ship)

10.1101/2020.05.20.106526

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Citations (5)

Regulatory gene expressions in the ascidian ventral sensory vesicle: evolutionary relationships with the vertebrate hypothalamus

Developmental Biology (2004)

Frédéric Moret Lionel Christiaen Carole Deyts Maryline Blin Philippe Vernier

10.1016/j.ydbio.2004.11.004

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Citations (61)