Wnt/β-catenin signaling regulates VE-cadherin-mediated anastomosis of brain capillaries by counteracting S1pr1 signaling

Canonical Wnt signaling is crucial for vascularization of the central nervous system and blood-brain barrier (BBB) formation. BBB formation and modulation are not only important for development, but also relevant for vascular and neurodegenerative diseases. However, there is little understanding of...

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Published inNature communications Vol. 9; no. 1; pp. 4860 - 17
Main Authors Hübner, Kathleen, Cabochette, Pauline, Diéguez-Hurtado, Rodrigo, Wiesner, Cora, Wakayama, Yuki, Grassme, Kathrin S., Hubert, Marvin, Guenther, Stefan, Belting, Heinz-Georg, Affolter, Markus, Adams, Ralf H., Vanhollebeke, Benoit, Herzog, Wiebke
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 19.11.2018
Nature Publishing Group
Nature Portfolio
Subjects
13
14
14/19
38
38/91
42/70
631/136/16
631/136/334/1874/763
631/378/1341
64/116
96
Anastomosis
Angiogenesis
Animals
Animals, Genetically Modified
Antigens, CD - genetics
Antigens, CD - metabolism
beta Catenin - genetics
beta Catenin - metabolism
Blood-brain barrier
Blood-Brain Barrier - growth & development
Blood-Brain Barrier - metabolism
Brain - blood supply
Brain - growth & development
Brain - metabolism
Cadherins
Cadherins - genetics
Cadherins - metabolism
Capillaries
Capillaries - growth & development
Capillaries - metabolism
Cell Adhesion Molecules - genetics
Cell Adhesion Molecules - metabolism
Cell junctions
Central nervous system
Cerebrovascular Circulation - genetics
Embryo, Nonmammalian
Embryos
Gene Expression Regulation, Developmental
Genes, Reporter
Humanities and Social Sciences
Image resolution
Luminescent Proteins - genetics
Luminescent Proteins - metabolism
multidisciplinary
Neovascularization, Physiologic - genetics
Neurodegenerative diseases
Neuroimaging
Neurological diseases
Receptors, Lysosphingolipid - genetics
Receptors, Lysosphingolipid - metabolism
Red Fluorescent Protein
Science
Science (multidisciplinary)
Signaling
Sphingosine 1-phosphate
Vascularization
Wnt protein
Wnt Signaling Pathway
Zebrafish - genetics
Zebrafish - growth & development
Zebrafish - metabolism
Zebrafish Proteins - genetics
Zebrafish Proteins - metabolism
β-Catenin
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Abstract Canonical Wnt signaling is crucial for vascularization of the central nervous system and blood-brain barrier (BBB) formation. BBB formation and modulation are not only important for development, but also relevant for vascular and neurodegenerative diseases. However, there is little understanding of how Wnt signaling contributes to brain angiogenesis and BBB formation. Here we show, using high resolution in vivo imaging and temporal and spatial manipulation of Wnt signaling, different requirements for Wnt signaling during brain angiogenesis and BBB formation. In the absence of Wnt signaling, premature Sphingosine-1-phosphate receptor (S1pr) signaling reduces VE-cadherin and Esama at cell-cell junctions. We suggest that Wnt signaling suppresses S1pr signaling during angiogenesis to enable the dynamic junction formation during anastomosis, whereas later S1pr signaling regulates BBB maturation and VE-cadherin stabilization. Our data provides a link between brain angiogenesis and BBB formation and identifies Wnt signaling as coordinator of the timing and as regulator of anastomosis. Wnt signaling is known to regulate the formation of the blood-brain barrier. Here Hübner et al. dissect the underlying mechanisms using high resolution live imaging in zebrafish, and find that Wnt regulates anastomosis of angiogenic sprouts in the brain by counteracting sphingosine-1-phosphate receptor signaling.
AbstractList Abstract Canonical Wnt signaling is crucial for vascularization of the central nervous system and blood-brain barrier (BBB) formation. BBB formation and modulation are not only important for development, but also relevant for vascular and neurodegenerative diseases. However, there is little understanding of how Wnt signaling contributes to brain angiogenesis and BBB formation. Here we show, using high resolution in vivo imaging and temporal and spatial manipulation of Wnt signaling, different requirements for Wnt signaling during brain angiogenesis and BBB formation. In the absence of Wnt signaling, premature Sphingosine-1-phosphate receptor (S1pr) signaling reduces VE-cadherin and Esama at cell-cell junctions. We suggest that Wnt signaling suppresses S1pr signaling during angiogenesis to enable the dynamic junction formation during anastomosis, whereas later S1pr signaling regulates BBB maturation and VE-cadherin stabilization. Our data provides a link between brain angiogenesis and BBB formation and identifies Wnt signaling as coordinator of the timing and as regulator of anastomosis.
Canonical Wnt signaling is crucial for vascularization of the central nervous system and blood-brain barrier (BBB) formation. BBB formation and modulation are not only important for development, but also relevant for vascular and neurodegenerative diseases. However, there is little understanding of how Wnt signaling contributes to brain angiogenesis and BBB formation. Here we show, using high resolution in vivo imaging and temporal and spatial manipulation of Wnt signaling, different requirements for Wnt signaling during brain angiogenesis and BBB formation. In the absence of Wnt signaling, premature Sphingosine-1-phosphate receptor (S1pr) signaling reduces VE-cadherin and Esama at cell-cell junctions. We suggest that Wnt signaling suppresses S1pr signaling during angiogenesis to enable the dynamic junction formation during anastomosis, whereas later S1pr signaling regulates BBB maturation and VE-cadherin stabilization. Our data provides a link between brain angiogenesis and BBB formation and identifies Wnt signaling as coordinator of the timing and as regulator of anastomosis. Wnt signaling is known to regulate the formation of the blood-brain barrier. Here Hübner et al. dissect the underlying mechanisms using high resolution live imaging in zebrafish, and find that Wnt regulates anastomosis of angiogenic sprouts in the brain by counteracting sphingosine-1-phosphate receptor signaling.
Canonical Wnt signaling is crucial for vascularization of the central nervous system and blood-brain barrier (BBB) formation. BBB formation and modulation are not only important for development, but also relevant for vascular and neurodegenerative diseases. However, there is little understanding of how Wnt signaling contributes to brain angiogenesis and BBB formation. Here we show, using high resolution in vivo imaging and temporal and spatial manipulation of Wnt signaling, different requirements for Wnt signaling during brain angiogenesis and BBB formation. In the absence of Wnt signaling, premature Sphingosine-1-phosphate receptor (S1pr) signaling reduces VE-cadherin and Esama at cell-cell junctions. We suggest that Wnt signaling suppresses S1pr signaling during angiogenesis to enable the dynamic junction formation during anastomosis, whereas later S1pr signaling regulates BBB maturation and VE-cadherin stabilization. Our data provides a link between brain angiogenesis and BBB formation and identifies Wnt signaling as coordinator of the timing and as regulator of anastomosis.
Wnt signaling is known to regulate the formation of the blood-brain barrier. Here Hübner et al. dissect the underlying mechanisms using high resolution live imaging in zebrafish, and find that Wnt regulates anastomosis of angiogenic sprouts in the brain by counteracting sphingosine-1-phosphate receptor signaling.
ArticleNumber 4860
Author Grassme, Kathrin S.
Hubert, Marvin
Belting, Heinz-Georg
Vanhollebeke, Benoit
Hübner, Kathleen
Guenther, Stefan
Herzog, Wiebke
Diéguez-Hurtado, Rodrigo
Wiesner, Cora
Affolter, Markus
Wakayama, Yuki
Cabochette, Pauline
Adams, Ralf H.
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  email: wiebke.herzog@uni-muenster.de
  organization: University of Muenster, Cells-in-Motion Cluster of Excellence (EXC 1003 – CiM), University of Muenster, Max Planck Institute for Molecular Biomedicine
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30451830$$D View this record in MEDLINE/PubMed
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SSID ssj0000391844
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Snippet Canonical Wnt signaling is crucial for vascularization of the central nervous system and blood-brain barrier (BBB) formation. BBB formation and modulation are...
Abstract Canonical Wnt signaling is crucial for vascularization of the central nervous system and blood-brain barrier (BBB) formation. BBB formation and...
Wnt signaling is known to regulate the formation of the blood-brain barrier. Here Hübner et al. dissect the underlying mechanisms using high resolution live...
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SubjectTerms 13
14
14/19
38
38/91
42/70
631/136/16
631/136/334/1874/763
631/378/1341
64/116
96
Anastomosis
Angiogenesis
Animals
Animals, Genetically Modified
Antigens, CD - genetics
Antigens, CD - metabolism
beta Catenin - genetics
beta Catenin - metabolism
Blood-brain barrier
Blood-Brain Barrier - growth & development
Blood-Brain Barrier - metabolism
Brain - blood supply
Brain - growth & development
Brain - metabolism
Cadherins
Cadherins - genetics
Cadherins - metabolism
Capillaries
Capillaries - growth & development
Capillaries - metabolism
Cell Adhesion Molecules - genetics
Cell Adhesion Molecules - metabolism
Cell junctions
Central nervous system
Cerebrovascular Circulation - genetics
Embryo, Nonmammalian
Embryos
Gene Expression Regulation, Developmental
Genes, Reporter
Humanities and Social Sciences
Image resolution
Luminescent Proteins - genetics
Luminescent Proteins - metabolism
multidisciplinary
Neovascularization, Physiologic - genetics
Neurodegenerative diseases
Neuroimaging
Neurological diseases
Receptors, Lysosphingolipid - genetics
Receptors, Lysosphingolipid - metabolism
Red Fluorescent Protein
Science
Science (multidisciplinary)
Signaling
Sphingosine 1-phosphate
Vascularization
Wnt protein
Wnt Signaling Pathway
Zebrafish - genetics
Zebrafish - growth & development
Zebrafish - metabolism
Zebrafish Proteins - genetics
Zebrafish Proteins - metabolism
β-Catenin
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Title Wnt/β-catenin signaling regulates VE-cadherin-mediated anastomosis of brain capillaries by counteracting S1pr1 signaling
URI https://link.springer.com/article/10.1038/s41467-018-07302-x
https://www.ncbi.nlm.nih.gov/pubmed/30451830
https://www.proquest.com/docview/2135625808
https://search.proquest.com/docview/2135639547
https://pubmed.ncbi.nlm.nih.gov/PMC6242933
https://doaj.org/article/24e4c6a49599424898a125c7c9be3b6f
Volume 9
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