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

Cantaut-Belarif, Yasmine; Orts-Del’Immagine, Adeline; Penru, Margot; Pézeron, Guillaume; Wyart, Claire; Bardet, Pierre-Luc

doi:10.7554/elife.59469

Cited by 29 publications

(58 citation statements)

References 55 publications

(102 reference statements)

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“…It has been found that scospondin mutant embryos lacking the Reissner fibre fail to extend a straight body axis during embryonic development [45,46]. Interestingly, the Reissner fibre appears to be required for the expression of urp2 in CSF-contacting neurons [13,14], which is in agreement with recent findings showing that it is functionally coupled to the mechanosensory function of CSF-contacting neurons [49]. The Reissner fibre is highly conserved and present in the central canal of almost all vertebrate species [48] including X. laevis [50].…”

Section: Discussionmentioning

confidence: 99%

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Conserved role of the urotensin II receptor 4 signalling pathway to control body straightness in a tetrapod

Alejevski¹,

Leemans²,

Gaillard³

et al. 2021

Open Biol.

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Urp1 and Urp2 are two neuropeptides of the urotensin II family identified in teleost fish and mainly expressed in cerebrospinal fluid (CSF)-contacting neurons. It has been recently proposed that Urp1 and Urp2 are required for correct axis formation and maintenance. Their action is thought to be mediated by the receptor Uts2r3, which is specifically expressed in dorsal somites. In support of this view, it has been demonstrated that the loss of uts2r3 results in severe scoliosis in adult zebrafish. In the present study, we report for the first time the occurrence of urp2, but not of urp1 , in two tetrapod species of the Xenopus genus. In X. laevis , we show that urp2 mRNA-containing cells are CSF-contacting neurons. Furthermore, we identified utr4, the X. laevis counterparts of zebrafish uts2r3, and we demonstrate that, as in zebrafish, it is expressed in the dorsal somatic musculature. Finally, we reveal that, in X. laevis, the disruption of utr4 results in an abnormal curvature of the antero-posterior axis of the tadpoles. Taken together, our results suggest that the role of the Utr4 signalling pathway in the control of body straightness is an ancestral feature of bony vertebrates and not just a peculiarity of ray-finned fishes.

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Section: Discussionmentioning

confidence: 99%

“…In contrast with those of UII, the functions of Urps are much less understood. However, recent studies in zebrafish (Danio rerio) have shown that Urp1 and Urp2 play a critical role in spine morphogenesis [12][13][14].…”

mentioning

confidence: 99%

Conserved role of the urotensin II receptor 4 signalling pathway to control body straightness in a tetrapod

Alejevski¹,

Leemans²,

Gaillard³

et al. 2021

Open Biol.

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“…And What is its function? In the last few years, RF has been studied using new methodological approaches, such as tandem mass spectrophotometry [ 35 ] and mutant zebrafish lines [ 29 , 33 , 34 , 36 , 37 , 148 ], providing some insight on these historical questions.…”

Section: Reissner Fiber: Composition Formation and Movementmentioning

confidence: 99%

“…Transcriptomic analysis of sspo zebrafish mutants [ 36 , 148 ] revealed high downregulation of urotensin neuropeptide 2 (Urp2). This peptide is secreted in the spinal cord by ventral cerebrospinal fluid-contacting neurons (CSFcNs), a group of mechanosensory neurons that extend motile cilia and microvilli toward the central canal that will eventually contact the RF, detecting the spinal curvature in a directional manner (Fig.…”

Section: Function Of the Sco Sco-spondin And Rfmentioning

confidence: 99%

SCO-spondin, a giant matricellular protein that regulates cerebrospinal fluid activity

Sepúlveda

Maurelia

González

et al. 2021

Fluids Barriers CNS

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Cerebrospinal fluid is a clear fluid that occupies the ventricular and subarachnoid spaces within and around the brain and spinal cord. Cerebrospinal fluid is a dynamic signaling milieu that transports nutrients, waste materials and neuroactive substances that are crucial for the development, homeostasis and functionality of the central nervous system. The mechanisms that enable cerebrospinal fluid to simultaneously exert these homeostatic/dynamic functions are not fully understood. SCO-spondin is a large glycoprotein secreted since the early stages of development into the cerebrospinal fluid. Its domain architecture resembles a combination of a matricellular protein and the ligand-binding region of LDL receptor family. The matricellular proteins are a group of extracellular proteins with the capacity to interact with different molecules, such as growth factors, cytokines and cellular receptors; enabling the integration of information to modulate various physiological and pathological processes. In the same way, the LDL receptor family interacts with many ligands, including β-amyloid peptide and different growth factors. The domains similarity suggests that SCO-spondin is a matricellular protein enabled to bind, modulate, and transport different cerebrospinal fluid molecules. SCO-spondin can be found soluble or polymerized into a dynamic threadlike structure called the Reissner fiber, which extends from the diencephalon to the caudal tip of the spinal cord. Reissner fiber continuously moves caudally as new SCO-spondin molecules are added at the cephalic end and are disaggregated at the caudal end. This movement, like a conveyor belt, allows the transport of the bound molecules, thereby increasing their lifespan and action radius. The binding of SCO-spondin to some relevant molecules has already been reported; however, in this review we suggest more than 30 possible binding partners, including peptide β-amyloid and several growth factors. This new perspective characterizes SCO-spondin as a regulator of cerebrospinal fluid activity, explaining its high evolutionary conservation, its apparent multifunctionality, and the lethality or severe malformations, such as hydrocephalus and curved body axis, of knockout embryos. Understanding the regulation and identifying binding partners of SCO-spondin are crucial for better comprehension of cerebrospinal fluid physiology.

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“…When the axis is straight, RF floats in the neural canal, but when it curves comes into contact with mechanosensory neurons in the neural tube’s inner wall that activate axial musculature, restoring the body’s stiffness axis ( Orts-Del’Immagine et al, 2020 ). Two further articles have shed additional insight into RF- CSF-cn mechanosensory transduction ( Cantaut-Belarif et al, 2020 ; Lu et al, 2020 ). These studies showed that URP requires an intact RF to be expressed and is downregulated in SCO-spondin mutants, which results in impaired signaling to trunk muscles.…”

Section: Hypotheses About Rf’s Functionsmentioning

confidence: 99%

The Enigmatic Reissner’s Fiber and the Origin of Chordates

Aboitiz

Montiel

2021

Front. Neuroanat.

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Reissner’s fiber (RF) is a secreted filament that floats in the neural canal of chordates. Since its discovery in 1860, there has been no agreement on its primary function, and its strong conservation across chordate species has remained a mystery for comparative neuroanatomists. Several findings, including the chemical composition and the phylogenetic history of RF, clinical observations associating RF with the development of the neural canal, and more recent studies suggesting that RF is needed to develop a straight vertebral column, may shed light on the functions of this structure across chordates. In this article, we will briefly review the evidence mentioned above to suggest a role of RF in the origin of fundamental innovations of the chordate body plan, especially the elongation of the neural tube and maintenance of the body axis. We will also mention the relevance of RF for medical conditions like hydrocephalus, scoliosis of the vertebral spine and possibly regeneration of the spinal cord.

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

Cited by 29 publications

References 55 publications

Conserved role of the urotensin II receptor 4 signalling pathway to control body straightness in a tetrapod

Conserved role of the urotensin II receptor 4 signalling pathway to control body straightness in a tetrapod

SCO-spondin, a giant matricellular protein that regulates cerebrospinal fluid activity

The Enigmatic Reissner’s Fiber and the Origin of Chordates

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