RECK in Neural Precursor Cells Plays a Critical Role in Mouse Forebrain Angiogenesis
RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also...
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| Published in | iScience Vol. 19; pp. 559 - 571 |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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27.09.2019
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| Abstract | RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also critical for brain angiogenesis. When Reck is inactivated in Foxg1-positive NPCs, mice die shortly after birth with hemorrhage in the forebrain, with angiogenic sprouts stalling at the periphery and forming abnormal aggregates reminiscent of those in EC-selective Reck knockout mice and Wnt7a/b-deficient mice. The hemorrhage can be pharmacologically suppressed by lithium chloride. An effect of RECK in WNT7-producing cells to enhance canonical WNT-signaling in reporter cells is detectable in mixed culture but not with conditioned medium. Our findings suggest that NPC-expressed RECK has a non-cell-autonomous function to promote forebrain angiogenesis through contact-dependent enhancement of WNT signaling in ECs, implying possible involvement of RECK in neurovascular coupling.
[Display omitted]
•Mice lacking RECK in Foxg1-positive neural precursor cells die shortly after birth•These mice show vascular defects similar to those in mice lacking endothelial RECK•The vascular phenotype can be suppressed by LiCl, an activator of WNT signaling•RECK in WNT7-producing cell enhances contact-dependent WNT signaling in adjacent cells
Vascular Remodeling; Neuroscience; Molecular Neuroscience; Developmental Neuroscience |
|---|---|
| AbstractList | RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also critical for brain angiogenesis. When
Reck
is inactivated in
Foxg1
-positive NPCs, mice die shortly after birth with hemorrhage in the forebrain, with angiogenic sprouts stalling at the periphery and forming abnormal aggregates reminiscent of those in EC-selective
Reck
knockout mice and
Wnt7a/b
-deficient mice. The hemorrhage can be pharmacologically suppressed by lithium chloride. An effect of RECK in WNT7-producing cells to enhance canonical WNT-signaling in reporter cells is detectable in mixed culture but not with conditioned medium. Our findings suggest that NPC-expressed RECK has a non-cell-autonomous function to promote forebrain angiogenesis through contact-dependent enhancement of WNT signaling in ECs, implying possible involvement of RECK in neurovascular coupling.
•
Mice lacking RECK in
Foxg1
-positive neural precursor cells die shortly after birth
•
These mice show vascular defects similar to those in mice lacking endothelial RECK
•
The vascular phenotype can be suppressed by LiCl, an activator of WNT signaling
•
RECK in WNT7-producing cell enhances contact-dependent WNT signaling in adjacent cells
Vascular Remodeling; Neuroscience; Molecular Neuroscience; Developmental Neuroscience RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also critical for brain angiogenesis. When Reck is inactivated in Foxg1-positive NPCs, mice die shortly after birth with hemorrhage in the forebrain, with angiogenic sprouts stalling at the periphery and forming abnormal aggregates reminiscent of those in EC-selective Reck knockout mice and Wnt7a/b-deficient mice. The hemorrhage can be pharmacologically suppressed by lithium chloride. An effect of RECK in WNT7-producing cells to enhance canonical WNT-signaling in reporter cells is detectable in mixed culture but not with conditioned medium. Our findings suggest that NPC-expressed RECK has a non-cell-autonomous function to promote forebrain angiogenesis through contact-dependent enhancement of WNT signaling in ECs, implying possible involvement of RECK in neurovascular coupling. [Display omitted] •Mice lacking RECK in Foxg1-positive neural precursor cells die shortly after birth•These mice show vascular defects similar to those in mice lacking endothelial RECK•The vascular phenotype can be suppressed by LiCl, an activator of WNT signaling•RECK in WNT7-producing cell enhances contact-dependent WNT signaling in adjacent cells Vascular Remodeling; Neuroscience; Molecular Neuroscience; Developmental Neuroscience RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also critical for brain angiogenesis. When Reck is inactivated in Foxg1-positive NPCs, mice die shortly after birth with hemorrhage in the forebrain, with angiogenic sprouts stalling at the periphery and forming abnormal aggregates reminiscent of those in EC-selective Reck knockout mice and Wnt7a/b-deficient mice. The hemorrhage can be pharmacologically suppressed by lithium chloride. An effect of RECK in WNT7-producing cells to enhance canonical WNT-signaling in reporter cells is detectable in mixed culture but not with conditioned medium. Our findings suggest that NPC-expressed RECK has a non-cell-autonomous function to promote forebrain angiogenesis through contact-dependent enhancement of WNT signaling in ECs, implying possible involvement of RECK in neurovascular coupling. RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also critical for brain angiogenesis. When Reck is inactivated in Foxg1-positive NPCs, mice die shortly after birth with hemorrhage in the forebrain, with angiogenic sprouts stalling at the periphery and forming abnormal aggregates reminiscent of those in EC-selective Reck knockout mice and Wnt7a/b-deficient mice. The hemorrhage can be pharmacologically suppressed by lithium chloride. An effect of RECK in WNT7-producing cells to enhance canonical WNT-signaling in reporter cells is detectable in mixed culture but not with conditioned medium. Our findings suggest that NPC-expressed RECK has a non-cell-autonomous function to promote forebrain angiogenesis through contact-dependent enhancement of WNT signaling in ECs, implying possible involvement of RECK in neurovascular coupling. : Vascular Remodeling; Neuroscience; Molecular Neuroscience; Developmental Neuroscience Subject Areas: Vascular Remodeling, Neuroscience, Molecular Neuroscience, Developmental Neuroscience RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also critical for brain angiogenesis. When Reck is inactivated in Foxg1-positive NPCs, mice die shortly after birth with hemorrhage in the forebrain, with angiogenic sprouts stalling at the periphery and forming abnormal aggregates reminiscent of those in EC-selective Reck knockout mice and Wnt7a/b-deficient mice. The hemorrhage can be pharmacologically suppressed by lithium chloride. An effect of RECK in WNT7-producing cells to enhance canonical WNT-signaling in reporter cells is detectable in mixed culture but not with conditioned medium. Our findings suggest that NPC-expressed RECK has a non-cell-autonomous function to promote forebrain angiogenesis through contact-dependent enhancement of WNT signaling in ECs, implying possible involvement of RECK in neurovascular coupling.RECK in neural precursor cells (NPCs) was previously found to support Notch-dependent neurogenesis in mice. On the other hand, recent studies implicate RECK in endothelial cells (ECs) in WNT7-triggered canonical WNT signaling essential for brain angiogenesis. Here we report that RECK in NPCs is also critical for brain angiogenesis. When Reck is inactivated in Foxg1-positive NPCs, mice die shortly after birth with hemorrhage in the forebrain, with angiogenic sprouts stalling at the periphery and forming abnormal aggregates reminiscent of those in EC-selective Reck knockout mice and Wnt7a/b-deficient mice. The hemorrhage can be pharmacologically suppressed by lithium chloride. An effect of RECK in WNT7-producing cells to enhance canonical WNT-signaling in reporter cells is detectable in mixed culture but not with conditioned medium. Our findings suggest that NPC-expressed RECK has a non-cell-autonomous function to promote forebrain angiogenesis through contact-dependent enhancement of WNT signaling in ECs, implying possible involvement of RECK in neurovascular coupling. |
| Author | Noda, Makoto Miki, Takao Hanashima, Carina Watanabe, Naoki Almeida, Glícia Maria de Li, Huiping Matsuzaki, Tomoko Kuo, Calvin J. |
| AuthorAffiliation | 4 Stanford University School of Medicine, Department of Medicine, Division of Hematology, Lokey Stem Cell Research Building, 265 Campus Drive, Stanford, CA 94305, USA 5 Department of Pharmacology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan 2 Laboratory of Single-Molecule Cell Biology, Kyoto University Graduate School of Biostudies, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan 1 Department of Molecular Oncology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan 3 Department of Biology, Faculty of Education and Integrated Arts and Sciences, Waseda University, Shinjuku-ku, Tokyo 162-8480, Japan |
| AuthorAffiliation_xml | – name: 4 Stanford University School of Medicine, Department of Medicine, Division of Hematology, Lokey Stem Cell Research Building, 265 Campus Drive, Stanford, CA 94305, USA – name: 3 Department of Biology, Faculty of Education and Integrated Arts and Sciences, Waseda University, Shinjuku-ku, Tokyo 162-8480, Japan – name: 1 Department of Molecular Oncology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – name: 2 Laboratory of Single-Molecule Cell Biology, Kyoto University Graduate School of Biostudies, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – name: 5 Department of Pharmacology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan |
| Author_xml | – sequence: 1 givenname: Huiping surname: Li fullname: Li, Huiping organization: Department of Molecular Oncology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – sequence: 2 givenname: Takao surname: Miki fullname: Miki, Takao organization: Department of Molecular Oncology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – sequence: 3 givenname: Glícia Maria de surname: Almeida fullname: Almeida, Glícia Maria de organization: Department of Molecular Oncology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – sequence: 4 givenname: Carina surname: Hanashima fullname: Hanashima, Carina organization: Department of Biology, Faculty of Education and Integrated Arts and Sciences, Waseda University, Shinjuku-ku, Tokyo 162-8480, Japan – sequence: 5 givenname: Tomoko surname: Matsuzaki fullname: Matsuzaki, Tomoko organization: Department of Molecular Oncology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – sequence: 6 givenname: Calvin J. surname: Kuo fullname: Kuo, Calvin J. organization: Stanford University School of Medicine, Department of Medicine, Division of Hematology, Lokey Stem Cell Research Building, 265 Campus Drive, Stanford, CA 94305, USA – sequence: 7 givenname: Naoki surname: Watanabe fullname: Watanabe, Naoki organization: Laboratory of Single-Molecule Cell Biology, Kyoto University Graduate School of Biostudies, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan – sequence: 8 givenname: Makoto surname: Noda fullname: Noda, Makoto email: noda.makoto.3x@kyoto-u.ac.jp organization: Department of Molecular Oncology, Kyoto University Graduate School of Medicine, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan |
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| Keywords | Vascular Remodeling Neuroscience Molecular Neuroscience Developmental Neuroscience |
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| SubjectTerms | Developmental Neuroscience Molecular Neuroscience Neuroscience Vascular Remodeling |
| Title | RECK in Neural Precursor Cells Plays a Critical Role in Mouse Forebrain Angiogenesis |
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