The Reissner Fiber in the Cerebrospinal Fluid Controls Morphogenesis of the Body Axis

• Published in: Current biology 2018-08, Vol.28 (15), p.2479-2486.e4
• Main Authors: Cantaut-Belarif, Yasmine, Sternberg, Jenna R., Thouvenin, Olivier, Wyart, Claire, Bardet, Pierre-Luc
• Format: Article
• Language: English
• Subjects: Animals; body axis morphogenesis; Body Patterning - physiology; Cell Adhesion Molecules, Neuronal - genetics; Cell Adhesion Molecules, Neuronal - metabolism; central canal; cerebrospinal fluid; Cerebrospinal Fluid - metabolism; cilia; Cilia - physiology; development; extracellular protein; fluid dynamics; Life Sciences; Mutation; Reissner fiber; zebrafish; Zebrafish - embryology; Zebrafish - growth & development
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2018.05.079

Organ development depends on the integration of coordinated long-range communication between cells. The cerebrospinal fluid composition and flow properties regulate several aspects of central nervous system development, including progenitor proliferation, neurogenesis, and migration [1–3]. One understudied component of the cerebrospinal fluid, described over a century ago in vertebrates, is the Reissner fiber. This extracellular thread forming early in development results from the assembly of the SCO-spondin protein in the third and fourth brain ventricles and central canal of the spinal cord [4]. Up to now, the function of the Reissner fiber has remained elusive, partly due to the lack of genetic invalidation models [4]. Here, by mutating the scospondin gene, we demonstrate that the Reissner fiber is critical for the morphogenesis of a straight posterior body axis. In zebrafish mutants where the Reissner fiber is lost, ciliogenesis and cerebrospinal fluid flow are intact but body axis morphogenesis is impaired. Our results also explain the frequently observed phenotype that mutant embryos with defective cilia exhibit defects in body axis curvature. Here, we reveal that these mutants systematically fail to assemble the Reissner fiber. We show that cilia promote the formation of the Reissner fiber and that the fiber is necessary for proper body axis morphogenesis. Our study sets the stage for future investigations of the mechanisms linking the Reissner fiber to the control of body axis curvature during vertebrate development. [Display omitted] •Zebrafish scospondin mutants lose the Reissner fiber in the cerebrospinal fluid•scospondin mutants show a curled-down axis similar to cilia-defective embryos•scospondin mutants exhibit normal cilia and cerebrospinal fluid circulation•Straight axis morphogenesis requires cilia-dependent assembly of the Reissner fiber Cantaut-Belarif et al. unravel a developmental role for the Reissner fiber, a long-known structure found in the cerebrospinal fluid. Zebrafish embryos lacking this extracellular thread develop a curled-down axis reminiscent of cilia-defective mutants. This fiber needs cilia to form and is required for straight axis morphogenesis.