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

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

doi:10.7554/elife.59469

Yasmine Cantaut-Belarif, Claire Wyart + Show 4 more

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https://doi.org/10.7554/elife.59469

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Abstract

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.

Highlights

One of the major questions in the study of multicellular organism development is to understand how precise morphogenesis is ensured during embryonic and postembryonic stages while the animal grows into an adult
Using the pkd2l1 mutant, we show that the loss of calcium signaling in ventral cerebrospinal fluid (CSF)-cNs does not lead to a loss of urp2 expression nor embryonic body axis curvature
Using a combination of transcriptomic analyses together with in vivo calcium imaging and pharmacology, we show here that the Reissner fiber is essential for signaling to the developing CSF

Summary

Introduction

One of the major questions in the study of multicellular organism development is to understand how precise morphogenesis is ensured during embryonic and postembryonic stages while the animal grows into an adult This process requires coordination between cell specification signals and the control of the tissue shape (Chan et al, 2017). Disruption of cilia motility in this species has been long known to induce a typical phenotype consisting in a downward curvature of the posterior axis of the embryo (Brand et al, 1996; Jaffe et al, 2016; Kramer-Zucker et al, 2005; Sullivan-Brown et al, 2008) This phenotype has recently been linked to a role of the CSF in body axis curvature establishment and maintenance downstream of cilia function (Cantaut-Belarif et al, 2018; Grimes et al, 2016). We previously showed that the Reissner fiber (RF), a component of the CSF, is important for axis

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