Sensory Neurons Contacting the Cerebrospinal Fluid Require the Reissner Fiber to Detect Spinal Curvature In Vivo

Orts-Del’Immagine, Adeline; Cantaut-Belarif, Yasmine; Thouvenin, Olivier; Roussel, Julian; Baskaran, Asha; Langui, Dominique; Koëth, Fanny; Bivas, Paul; Lejeune, François‐Xavier; Bardet, Pierre-Luc; Wyart, Claire

doi:10.1016/j.cub.2019.12.071

Cited by 67 publications

(72 citation statements)

References 62 publications

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“…One question remaining is how the Reissner Fiber controls calcium variations in ventral CSF-cNs. We recently showed that the Reissner fiber is functionally coupled to the mechano-sensory function of these interoceptive neurons in the larva ( Orts-Del'Immagine et al, 2020 ). However, embryonic CSF-cNs are not fully differentiated, as they do not harbor a fully developed apical extension known to tune their mechanosensory function at larval stage ( Desban et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

“…At the embryonic stage, undifferentiated CSF-cNs that are located ventrally in the neural tube are the only ones expressing Urp neuropeptides and exhibiting spontaneous calcium transients at rest ( Sternberg et al, 2018 ). Recently, the Reissner fiber was shown to be required in the larva for the mechanosensory function leading to intracellular calcium increase in differentiated CSF-cNs ( Orts-Del'Immagine et al, 2020 ). However, the role of the Reissner fiber in CSF-cN spontaneous activity at the embryonic stage when they express Urp neuropeptides is unknown.…”

Section: Introductionmentioning

confidence: 99%

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Adrenergic activation modulates the signal from the Reissner fiber to cerebrospinal fluid-contacting neurons during development

Cantaut-Belarif

Orts-Del’Immagine

Penru

et al. 2020

eLife

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The cerebrospinal fluid (CSF) contains an extracellular thread conserved in vertebrates, the Reissner fiber, which controls body axis morphogenesis in the zebrafish embryo. Yet, the signaling cascade originating from this fiber to ensure body axis straightening is not understood. Here, we explore the functional link between the Reissner fiber and undifferentiated spinal neurons contacting the CSF (CSF-cNs). First, we show that the Reissner fiber is required in vivo for the expression of urp2, a neuropeptide expressed in CSF-cNs. We show that the Reissner fiber is also required for embryonic calcium transients in these spinal neurons. Finally, we study how local adrenergic activation can substitute for the Reissner fiber-signaling pathway to CSF-cNs and rescue body axis morphogenesis. Our results show that the Reissner fiber acts on CSF-cNs and thereby contributes to establish body axis morphogenesis, and suggest it does so by controlling the availability of a chemical signal in the CSF.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Adrenergic activation modulates the signal from the Reissner fiber to cerebrospinal fluid-contacting neurons during development

Cantaut-Belarif

Orts-Del’Immagine

Penru

et al. 2020

eLife

Self Cite

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“…Thus, the lamprey studies are an invaluable inspiration for the studies in genetically tractable vertebrate models, which are increasingly used to dissect locomotor circuitries. Experiments in zebrafish using genetic tools have uncovered a modular organisation of spinal cell populations controlling speed ( Figure 1B, for review, see [25,26]), the role of reticulospinal neurons in providing excitation to spinal swimming circuits [27] and in the control of steering movements [28], and a key role for mechanosensory feedback in the control of swimming [29][30][31] (Figure 1B). In mice, several cell types have recently been genetically defined, including MLR cells controlling locomotor speed and gait transitions [32][33][34], reticulospinal cell types relaying locomotor commands [35][36][37] or steering commands to the spinal cord [38], and spinal cell types involved in locomotor rhythmogenesis and coordination (for review, see [39]) ( Figure 1D).…”

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confidence: 99%

Walking with Salamanders: From Molecules to Biorobotics

Ryczko

Simon

Ijspeert

2020

Trends in Neurosciences

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How do four-legged animals adapt their locomotion to the environment? How do central and peripheral mechanisms interact within the spinal cord to produce adaptive locomotion and how is locomotion recovered when spinal circuits are perturbed? Salamanders are the only tetrapods that regenerate voluntary locomotion after full spinal transection. Given their evolutionary position, they provide a unique opportunity to bridge discoveries made in fish and mammalian models. Genetic dissection of salamander neural circuits is becoming feasible with new methods for precise manipulation, elimination, and visualisation of cells. These approaches can be combined with classical tools in neuroscience and with modelling and a robotic environment. We propose that salamanders provide a blueprint of the function, evolution, and regeneration of tetrapod locomotor circuits. Salamanders as a Model Organism for Studying Locomotion Two major challenges in neuroscience are to decipher how the interplay between central and peripheral mechanisms controls locomotion in four-legged animals (tetrapods) and to delineate the reorganisation of motor circuits after spinal lesion. In this review, we outline the reasons why salamanders are ideally suited to address these two problems. First, salamanders are the only tetrapods capable of regenerating their locomotor circuits after full transection at adult stage [1-3]. Second, they are the closest extant representatives of the first tetrapods that transitioned from aquatic to terrestrial life [4]. This key evolutionary position makes salamanders ideal to provide a bridge between discoveries in fish (such as zebrafish) and mammals (such as mouse). Salamanders swim underwater and walk on ground [4], allowing researchers to investigate to what extent body dynamics and sensory feedback shape these locomotor patterns. Third, high precision dissection of their neural circuits is becoming possible thanks to new tools that will allow visualisation and optogenetic and chemogenetic manipulations that can be combined with classical neuroscience tools and advanced modelling and robotic environments. It is thus timely to highlight the recent advances in salamander research at the intersection of genomics, systems neuroscience, modelling, and robotics, which altogether provide a unique opportunity to decode locomotor control in the intact and regenerated tetrapod nervous system. In this review, we systematically place these approaches and recent results into a cross-species comparative setting, with a special focus on zebrafish and mouse as comparative models for which most data on the genetic identity of locomotor circuits are available. For closer examination of the locomotor circuitries of other related animal models such as lamprey, cat, and Xenopus embryo, we refer readers to prior reviews (lamprey: [5], cat: [6], Xenopus embryo: [7]). The Salamander Nervous System: A Bridge between Fish and Mammalian Models Salamander locomotor circuits include the main features found in all vertebrates (Figure 1A,C). Their...

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“…More comprehensive analysis of the non-complementing Group IA mutants, stl297 and stl300, found in this screen, demonstrated these are nonsynonymous mutations of the scospondin gene, causing disassembly of the RF during larval development leading to AIS-like spine defects (Troutwine et al, 2020). Given the similarity of Group IA phenotypes and the molecular implications for these mutations causing instability of the RF during larval development, it will be intriguing to determine whether the onset of whole- (Knafo and Wyart, 2018;Orts-Del'Immagine et al, 2020;Zhang et al, 2018). CSF-contacting neurons are conserved in vertebrates, suggesting that while RF may be absent in humans, these neurons still function in postural control, while their stimulation may be different.…”

Section: Discussionmentioning

confidence: 88%

Postembryonic screen for mutations affecting spine development in zebrafish

Gray

González

Ackerman

et al. 2020

Preprint

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The spinal vertebral column gives structural support for the adult body plan, protects the spinal cord, and provides muscle attachment and stability, which allows the animal to move within its environment. The development and maturation of the spine and its physiology involve the integration of multiple musculoskeletal tissues including bone, cartilage, and fibrocartilaginous joints, as well as innervation and control by the nervous system. One of the most common disorders of the spine in human is adolescent idiopathic scoliosis (AIS), which is characterized by the onset of an abnormal lateral curvature of the spine of <10° around adolescence, in otherwise healthy children. The genetic basis of AIS is largely unknown. Systematic genome-wide mutagenesis screens for embryonic phenotypes in zebrafish have been instrumental in the understanding of early patterning of embryonic tissues necessary to build and pattern the embryonic spine. However, the mechanisms required for postembryonic maturation and homeostasis of the spine remain poorly understood. Here we report the results from a small-scale forward genetic screen for adult-viable recessive and dominant mutant zebrafish, displaying overt morphological abnormalities of the adult spine. Germline mutations induced with N-ethyl N-nitrosourea (ENU) were transmitted and screened for dominant phenotypes in 1,229 F1 animals, and subsequently bred to homozygosity in F3 families, from these, 314 haploid genomes were screened for recessive phenotypes. We cumulatively found 39 adult-viable (3 dominant and 36 recessive) mutations each leading to a defect in the morphogenesis of the spine. The largest phenotypic group displayed larval onset axial curvatures, leading to whole-body scoliosis without vertebral dysplasia in adult fish. Pairwise complementation testing within this phenotypic group revealed at least 16 independent mutant loci. Using massively-parallel whole genome or whole exome sequencing and meiotic mapping we defined the molecular identity of several loci for larval onset whole-body scoliosis in zebrafish. We identified a new mutation in the skolios/kinesin family member 6 (kif6) gene, causing neurodevelopmental and ependymal cilia defects in mouse and zebrafish. We also report several recessive alleles of the scospondin and a disintegrin and metalloproteinase with thrombospondin motifs 9 (adamts9) genes, which all display defects in spine morphogenesis. Many of the alleles characterized thus far are non-synonymous mutations in known essential scospondin and adamts9 genes. Our results provide evidence of monogenic traits that are critical for normal spine development in zebrafish, that may help to establish new candidate risk loci for spine disorders in humans.

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Sensory Neurons Contacting the Cerebrospinal Fluid Require the Reissner Fiber to Detect Spinal Curvature In Vivo

Cited by 67 publications

References 62 publications

Adrenergic activation modulates the signal from the Reissner fiber to cerebrospinal fluid-contacting neurons during development

Adrenergic activation modulates the signal from the Reissner fiber to cerebrospinal fluid-contacting neurons during development

Walking with Salamanders: From Molecules to Biorobotics

Postembryonic screen for mutations affecting spine development in zebrafish

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