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• W4379513767 abstract "•BMP signaling regulates notochord sheath segmentation in zebrafish •BMP signaling generates a differentiation wave in the notochord sheath •Metameric BMP signaling drives notochord segmentation upstream of Notch •A balance of Bmp3 and the antagonist Nog3 regulates precise notochord segmentation The vertebrate spine is a metameric structure composed of alternating vertebral bodies (centra) and intervertebral discs. 1 Bagnat M. Gray R.S. Development of a straight vertebrate body axis. Development. 2020; 147https://doi.org/10.1242/dev.175794 Crossref PubMed Scopus (28) Google Scholar Recent studies in zebrafish have shown that the epithelial sheath surrounding the notochord differentiates into alternating cartilage-like (col2a1/col9a2+) and mineralizing (entpd5a+) segments which serve as a blueprint for centra formation. 2 Wopat S. Bagwell J. Sumigray K.D. Dickson A.L. Huitema L.F.A. Poss K.D. Schulte-Merker S. Bagnat M. Spine patterning is guided by segmentation of the notochord sheath. Cell Rep. 2018; 22: 2026-2038 Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar ,3 Lleras Forero L. Narayanan R. Huitema L.F. VanBergen M. Apschner A. Peterson-Maduro J. Logister I. Valentin G. Morelli L.G. Oates A.C. Schulte-Merker S. Segmentation of the zebrafish axial skeleton relies on notochord sheath cells and not on the segmentation clock. Elife. 2018; : 7-e33843 Google Scholar ,4 Peskin B. Henke K. Cumplido N. Treaster S. Harris M.P. Bagnat M. Arratia G. Notochordal Signals Establish Phylogenetic Identity of the Teleost Spine. Curr. Biol. 2020; 30: 2805-2814.e3 Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar ,5 Pogoda H.M. Riedl-Quinkertz I. Löhr H. Waxman J.S. Dale R.M. Topczewski J. Schulte-Merker S. Hammerschmidt M. Direct activation of chordoblasts by retinoic acid is required for segmented centra mineralization during zebrafish spine development. Development. 2018; 145: dev159418https://doi.org/10.1242/dev.159418 Crossref PubMed Scopus (24) Google Scholar This process also defines the trajectories of migrating sclerotomal cells that form the mature vertebral bodies. 4 Peskin B. Henke K. Cumplido N. Treaster S. Harris M.P. Bagnat M. Arratia G. Notochordal Signals Establish Phylogenetic Identity of the Teleost Spine. Curr. Biol. 2020; 30: 2805-2814.e3 Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar Previous work demonstrated that notochord segmentation is typically sequential and involves the segmented activation of Notch signaling. 2 Wopat S. Bagwell J. Sumigray K.D. Dickson A.L. Huitema L.F.A. Poss K.D. Schulte-Merker S. Bagnat M. Spine patterning is guided by segmentation of the notochord sheath. Cell Rep. 2018; 22: 2026-2038 Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar However, it is unclear how Notch is activated in an alternating and sequential fashion. Furthermore, the molecular components that define segment size, regulate segment growth, and produce sharp segment boundaries have not been identified. In this study, we uncover that a BMP signaling wave acts upstream of Notch during zebrafish notochord segmentation. Using genetically encoded reporters of BMP activity and signaling pathway components, we show that BMP signaling is dynamic as axial patterning progresses, leading to the sequential formation of mineralizing domains in the notochord sheath. Genetic manipulations reveal that type I BMP receptor activation is sufficient to ectopically trigger Notch signaling. Moreover, loss of Bmpr1ba and Bmpr1aa or Bmp3 function disrupts ordered segment formation and growth, which is recapitulated by notochord-specific overexpression of the BMP antagonist, Noggin3. Our data suggest that BMP signaling in the notochord sheath precedes Notch activation and instructs segment growth, facilitating proper spine morphogenesis. The vertebrate spine is a metameric structure composed of alternating vertebral bodies (centra) and intervertebral discs. 1 Bagnat M. Gray R.S. Development of a straight vertebrate body axis. Development. 2020; 147https://doi.org/10.1242/dev.175794 Crossref PubMed Scopus (28) Google Scholar Recent studies in zebrafish have shown that the epithelial sheath surrounding the notochord differentiates into alternating cartilage-like (col2a1/col9a2+) and mineralizing (entpd5a+) segments which serve as a blueprint for centra formation. 2 Wopat S. Bagwell J. Sumigray K.D. Dickson A.L. Huitema L.F.A. Poss K.D. Schulte-Merker S. Bagnat M. Spine patterning is guided by segmentation of the notochord sheath. Cell Rep. 2018; 22: 2026-2038 Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar ,3 Lleras Forero L. Narayanan R. Huitema L.F. VanBergen M. Apschner A. Peterson-Maduro J. Logister I. Valentin G. Morelli L.G. Oates A.C. Schulte-Merker S. Segmentation of the zebrafish axial skeleton relies on notochord sheath cells and not on the segmentation clock. Elife. 2018; : 7-e33843 Google Scholar ,4 Peskin B. Henke K. Cumplido N. Treaster S. Harris M.P. Bagnat M. Arratia G. Notochordal Signals Establish Phylogenetic Identity of the Teleost Spine. Curr. Biol. 2020; 30: 2805-2814.e3 Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar ,5 Pogoda H.M. Riedl-Quinkertz I. Löhr H. Waxman J.S. Dale R.M. Topczewski J. Schulte-Merker S. Hammerschmidt M. Direct activation of chordoblasts by retinoic acid is required for segmented centra mineralization during zebrafish spine development. Development. 2018; 145: dev159418https://doi.org/10.1242/dev.159418 Crossref PubMed Scopus (24) Google Scholar This process also defines the trajectories of migrating sclerotomal cells that form the mature vertebral bodies. 4 Peskin B. Henke K. Cumplido N. Treaster S. Harris M.P. Bagnat M. Arratia G. Notochordal Signals Establish Phylogenetic Identity of the Teleost Spine. Curr. Biol. 2020; 30: 2805-2814.e3 Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar Previous work demonstrated that notochord segmentation is typically sequential and involves the segmented activation of Notch signaling. 2 Wopat S. Bagwell J. Sumigray K.D. Dickson A.L. Huitema L.F.A. Poss K.D. Schulte-Merker S. Bagnat M. Spine patterning is guided by segmentation of the notochord sheath. Cell Rep. 2018; 22: 2026-2038 Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar However, it is unclear how Notch is activated in an alternating and sequential fashion. Furthermore, the molecular components that define segment size, regulate segment growth, and produce sharp segment boundaries have not been identified. In this study, we uncover that a BMP signaling wave acts upstream of Notch during zebrafish notochord segmentation. Using genetically encoded reporters of BMP activity and signaling pathway components, we show that BMP signaling is dynamic as axial patterning progresses, leading to the sequential formation of mineralizing domains in the notochord sheath. Genetic manipulations reveal that type I BMP receptor activation is sufficient to ectopically trigger Notch signaling. Moreover, loss of Bmpr1ba and Bmpr1aa or Bmp3 function disrupts ordered segment formation and growth, which is recapitulated by notochord-specific overexpression of the BMP antagonist, Noggin3. Our data suggest that BMP signaling in the notochord sheath precedes Notch activation and instructs segment growth, facilitating proper spine morphogenesis." @default.
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• W4379513767 date "2023-06-01" @default.
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• W4379513767 title "Dynamic BMP signaling mediates notochord segmentation in zebrafish" @default.
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