Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in Zebrafish
Summary: Signal gradients encode instructive information for numerous decision-making processes during embryonic development. A striking example of precise, scalable tissue-level patterning is the segmentation of somites—the precursors of the vertebral column—during which the fibroblast growth facto...
| Main Authors: | , |
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| Format: | Article |
| Language: | English |
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Elsevier
2018-07-01
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| Series: | Cell Reports |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124718309185 |
| _version_ | 1819090279423016960 |
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| author | M. Fethullah Simsek Ertuğrul M. Özbudak |
| author_facet | M. Fethullah Simsek Ertuğrul M. Özbudak |
| author_sort | M. Fethullah Simsek |
| collection | DOAJ |
| description | Summary: Signal gradients encode instructive information for numerous decision-making processes during embryonic development. A striking example of precise, scalable tissue-level patterning is the segmentation of somites—the precursors of the vertebral column—during which the fibroblast growth factor (FGF), Wnt, and retinoic acid (RA) pathways establish spatial gradients. Despite decades of studies proposing roles for all three pathways, the dynamic feature of these gradients that encodes instructive information determining segment sizes remained elusive. We developed a non-elongating tail explant system, integrated quantitative measurements with computational modeling, and tested alternative models to show that positional information is encoded solely by spatial fold change (SFC) in FGF signal output. Neighboring cells measure SFC to accurately position the determination front and thus determine segment size. The SFC model successfully recapitulates results of spatiotemporal perturbation experiments on both explants and intact embryos, and it shows that Wnt signaling acts permissively upstream of FGF signaling and that RA gradient is dispensable. : Simsek et al. use an elongation-arrested 3D explant system, integrated with quantitative measurements and computational modeling, to show that positional information for segmentation is encoded solely by spatial fold change (SFC) in FGF signal output. Neighboring cells measure SFC to accurately determine somite segment sizes. Wnt signaling acts permissively upstream of FGF signaling. |
| first_indexed | 2024-12-21T22:21:18Z |
| format | Article |
| id | doaj.art-1c85c0f8e77c4519aa6dfe545dd363ba |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-12-21T22:21:18Z |
| publishDate | 2018-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-1c85c0f8e77c4519aa6dfe545dd363ba2022-12-21T18:48:19ZengElsevierCell Reports2211-12472018-07-012416678.e8Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in ZebrafishM. Fethullah Simsek0Ertuğrul M. Özbudak1Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA; Department of Genetics, Albert Einstein College of Medicine, Bronx, NY 10461, USADivision of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45229, USA; Department of Genetics, Albert Einstein College of Medicine, Bronx, NY 10461, USA; Corresponding authorSummary: Signal gradients encode instructive information for numerous decision-making processes during embryonic development. A striking example of precise, scalable tissue-level patterning is the segmentation of somites—the precursors of the vertebral column—during which the fibroblast growth factor (FGF), Wnt, and retinoic acid (RA) pathways establish spatial gradients. Despite decades of studies proposing roles for all three pathways, the dynamic feature of these gradients that encodes instructive information determining segment sizes remained elusive. We developed a non-elongating tail explant system, integrated quantitative measurements with computational modeling, and tested alternative models to show that positional information is encoded solely by spatial fold change (SFC) in FGF signal output. Neighboring cells measure SFC to accurately position the determination front and thus determine segment size. The SFC model successfully recapitulates results of spatiotemporal perturbation experiments on both explants and intact embryos, and it shows that Wnt signaling acts permissively upstream of FGF signaling and that RA gradient is dispensable. : Simsek et al. use an elongation-arrested 3D explant system, integrated with quantitative measurements and computational modeling, to show that positional information for segmentation is encoded solely by spatial fold change (SFC) in FGF signal output. Neighboring cells measure SFC to accurately determine somite segment sizes. Wnt signaling acts permissively upstream of FGF signaling.http://www.sciencedirect.com/science/article/pii/S2211124718309185 |
| spellingShingle | M. Fethullah Simsek Ertuğrul M. Özbudak Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in Zebrafish Cell Reports |
| title | Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in Zebrafish |
| title_full | Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in Zebrafish |
| title_fullStr | Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in Zebrafish |
| title_full_unstemmed | Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in Zebrafish |
| title_short | Spatial Fold Change of FGF Signaling Encodes Positional Information for Segmental Determination in Zebrafish |
| title_sort | spatial fold change of fgf signaling encodes positional information for segmental determination in zebrafish |
| url | http://www.sciencedirect.com/science/article/pii/S2211124718309185 |
| work_keys_str_mv | AT mfethullahsimsek spatialfoldchangeoffgfsignalingencodespositionalinformationforsegmentaldeterminationinzebrafish AT ertugrulmozbudak spatialfoldchangeoffgfsignalingencodespositionalinformationforsegmentaldeterminationinzebrafish |