Serotonin signaling is required for Wnt-dependent GRP specification and leftward flow in Xenopus

Tina Beyer, Michael Danilchik, Thomas Thumberger, Philipp Vick, Matthias Tisler, Isabelle Schneider, Susanne Bogusch, Philipp Andre, Bärbel Ulmer, Peter Walentek, Beate Niesler, Martin Blum, Axel Schweickert

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

In vertebrates, most inner organs are asymmetrically arranged with respect to the main body axis [1]. Symmetry breakage in fish, amphibian, and mammalian embryos depends on cilia-driven leftward flow of extracellular fluid during neurulation [2-5]. Flow induces the asymmetric nodal cascade that governs asymmetric organ morphogenesis and placement [1, 6, 7]. In the frog Xenopus, an alternative laterality-generating mechanism involving asymmetric localization of serotonin at the 32-cell stage has been proposed [8]. However, no functional linkage between this early localization and flow at neurula stage has emerged. Here, we report that serotonin signaling is required for specification of the superficial mesoderm (SM), which gives rise to the ciliated gastrocoel roof plate (GRP) where flow occurs [5, 9]. Flow and asymmetry were lost in embryos in which serotonin signaling was downregulated. Serotonin, which we found uniformly distributed along the main body axes in the early embryo, was required for Wnt signaling, which provides the instructive signal to specify the GRP. Importantly, serotonin was required for Wnt-induced double-axis formation as well. Our data confirm flow as primary mechanism of symmetry breakage and suggest a general role of serotonin as competence factor for Wnt signaling during axis formation in Xenopus.

Original languageEnglish (US)
Pages (from-to)33-39
Number of pages7
JournalCurrent Biology
Volume22
Issue number1
DOIs
StatePublished - Jan 10 2012

Fingerprint

Xenopus
serotonin
Roofs
Serotonin
Specifications
embryo (animal)
Embryonic Structures
Wnt Proteins
Neurulation
Mammalian Embryo
extracellular fluids
Cilia
Extracellular Fluid
Amphibians
cilia
Mesoderm
Morphogenesis
Anura
Mental Competency
Fish

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Serotonin signaling is required for Wnt-dependent GRP specification and leftward flow in Xenopus. / Beyer, Tina; Danilchik, Michael; Thumberger, Thomas; Vick, Philipp; Tisler, Matthias; Schneider, Isabelle; Bogusch, Susanne; Andre, Philipp; Ulmer, Bärbel; Walentek, Peter; Niesler, Beate; Blum, Martin; Schweickert, Axel.

In: Current Biology, Vol. 22, No. 1, 10.01.2012, p. 33-39.

Research output: Contribution to journalArticle

Beyer, T, Danilchik, M, Thumberger, T, Vick, P, Tisler, M, Schneider, I, Bogusch, S, Andre, P, Ulmer, B, Walentek, P, Niesler, B, Blum, M & Schweickert, A 2012, 'Serotonin signaling is required for Wnt-dependent GRP specification and leftward flow in Xenopus', Current Biology, vol. 22, no. 1, pp. 33-39. https://doi.org/10.1016/j.cub.2011.11.027
Beyer, Tina ; Danilchik, Michael ; Thumberger, Thomas ; Vick, Philipp ; Tisler, Matthias ; Schneider, Isabelle ; Bogusch, Susanne ; Andre, Philipp ; Ulmer, Bärbel ; Walentek, Peter ; Niesler, Beate ; Blum, Martin ; Schweickert, Axel. / Serotonin signaling is required for Wnt-dependent GRP specification and leftward flow in Xenopus. In: Current Biology. 2012 ; Vol. 22, No. 1. pp. 33-39.
@article{162d202fecb041d6aee1b07244f1109e,
title = "Serotonin signaling is required for Wnt-dependent GRP specification and leftward flow in Xenopus",
abstract = "In vertebrates, most inner organs are asymmetrically arranged with respect to the main body axis [1]. Symmetry breakage in fish, amphibian, and mammalian embryos depends on cilia-driven leftward flow of extracellular fluid during neurulation [2-5]. Flow induces the asymmetric nodal cascade that governs asymmetric organ morphogenesis and placement [1, 6, 7]. In the frog Xenopus, an alternative laterality-generating mechanism involving asymmetric localization of serotonin at the 32-cell stage has been proposed [8]. However, no functional linkage between this early localization and flow at neurula stage has emerged. Here, we report that serotonin signaling is required for specification of the superficial mesoderm (SM), which gives rise to the ciliated gastrocoel roof plate (GRP) where flow occurs [5, 9]. Flow and asymmetry were lost in embryos in which serotonin signaling was downregulated. Serotonin, which we found uniformly distributed along the main body axes in the early embryo, was required for Wnt signaling, which provides the instructive signal to specify the GRP. Importantly, serotonin was required for Wnt-induced double-axis formation as well. Our data confirm flow as primary mechanism of symmetry breakage and suggest a general role of serotonin as competence factor for Wnt signaling during axis formation in Xenopus.",
author = "Tina Beyer and Michael Danilchik and Thomas Thumberger and Philipp Vick and Matthias Tisler and Isabelle Schneider and Susanne Bogusch and Philipp Andre and B{\"a}rbel Ulmer and Peter Walentek and Beate Niesler and Martin Blum and Axel Schweickert",
year = "2012",
month = "1",
day = "10",
doi = "10.1016/j.cub.2011.11.027",
language = "English (US)",
volume = "22",
pages = "33--39",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Cell Press",
number = "1",

}

TY - JOUR

T1 - Serotonin signaling is required for Wnt-dependent GRP specification and leftward flow in Xenopus

AU - Beyer, Tina

AU - Danilchik, Michael

AU - Thumberger, Thomas

AU - Vick, Philipp

AU - Tisler, Matthias

AU - Schneider, Isabelle

AU - Bogusch, Susanne

AU - Andre, Philipp

AU - Ulmer, Bärbel

AU - Walentek, Peter

AU - Niesler, Beate

AU - Blum, Martin

AU - Schweickert, Axel

PY - 2012/1/10

Y1 - 2012/1/10

N2 - In vertebrates, most inner organs are asymmetrically arranged with respect to the main body axis [1]. Symmetry breakage in fish, amphibian, and mammalian embryos depends on cilia-driven leftward flow of extracellular fluid during neurulation [2-5]. Flow induces the asymmetric nodal cascade that governs asymmetric organ morphogenesis and placement [1, 6, 7]. In the frog Xenopus, an alternative laterality-generating mechanism involving asymmetric localization of serotonin at the 32-cell stage has been proposed [8]. However, no functional linkage between this early localization and flow at neurula stage has emerged. Here, we report that serotonin signaling is required for specification of the superficial mesoderm (SM), which gives rise to the ciliated gastrocoel roof plate (GRP) where flow occurs [5, 9]. Flow and asymmetry were lost in embryos in which serotonin signaling was downregulated. Serotonin, which we found uniformly distributed along the main body axes in the early embryo, was required for Wnt signaling, which provides the instructive signal to specify the GRP. Importantly, serotonin was required for Wnt-induced double-axis formation as well. Our data confirm flow as primary mechanism of symmetry breakage and suggest a general role of serotonin as competence factor for Wnt signaling during axis formation in Xenopus.

AB - In vertebrates, most inner organs are asymmetrically arranged with respect to the main body axis [1]. Symmetry breakage in fish, amphibian, and mammalian embryos depends on cilia-driven leftward flow of extracellular fluid during neurulation [2-5]. Flow induces the asymmetric nodal cascade that governs asymmetric organ morphogenesis and placement [1, 6, 7]. In the frog Xenopus, an alternative laterality-generating mechanism involving asymmetric localization of serotonin at the 32-cell stage has been proposed [8]. However, no functional linkage between this early localization and flow at neurula stage has emerged. Here, we report that serotonin signaling is required for specification of the superficial mesoderm (SM), which gives rise to the ciliated gastrocoel roof plate (GRP) where flow occurs [5, 9]. Flow and asymmetry were lost in embryos in which serotonin signaling was downregulated. Serotonin, which we found uniformly distributed along the main body axes in the early embryo, was required for Wnt signaling, which provides the instructive signal to specify the GRP. Importantly, serotonin was required for Wnt-induced double-axis formation as well. Our data confirm flow as primary mechanism of symmetry breakage and suggest a general role of serotonin as competence factor for Wnt signaling during axis formation in Xenopus.

UR - http://www.scopus.com/inward/record.url?scp=84855672231&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84855672231&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2011.11.027

DO - 10.1016/j.cub.2011.11.027

M3 - Article

VL - 22

SP - 33

EP - 39

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 1

ER -