PUBLICATION

Dynamic coupling of pattern formation and morphogenesis in the developing vertebrate retina

Authors
Picker, A., Cavodeassi, F., Machate, A., Bernauer, S., Hans, S., Abe, G., Kawakami, K., Wilson, S.W., and Brand, M.
ID
ZDB-PUB-091023-37
Date
2009
Source
PLoS Biology   7(10): e1000214 (Journal)
Registered Authors
Brand, Michael, Cavodeassi, Florencia, Hans, Stefan, Kawakami, Koichi, Machate, Anja, Wilson, Steve
Keywords
Vesicles, Retina, Embryos, Cloning, Eyes, Morphogenesis, Zebrafish, Cell movement
MeSH Terms
  • Signal Transduction/physiology
  • Embryo, Nonmammalian/embryology*
  • Retina/embryology*
  • Female
  • Body Patterning/physiology*
  • Zebrafish Proteins/physiology*
  • Fibroblast Growth Factors/physiology*
  • Animals
  • Zebrafish
  • Forkhead Transcription Factors/physiology
  • Fibroblast Growth Factor 3/physiology*
(all 11)
PubMed
19823566 Full text @ PLoS Biol.
Abstract
During embryonic development, pattern formation must be tightly synchronized with tissue morphogenesis to coordinate the establishment of the spatial identities of cells with their movements. In the vertebrate retina, patterning along the dorsal-ventral and nasal-temporal (anterior-posterior) axes is required for correct spatial representation in the retinotectal map. However, it is unknown how specification of axial cell positions in the retina occurs during the complex process of early eye morphogenesis. Studying zebrafish embryos, we show that morphogenetic tissue rearrangements during eye evagination result in progenitor cells in the nasal half of the retina primordium being brought into proximity to the sources of three fibroblast growth factors, Fgf8/3/24, outside the eye. Triple-mutant analysis shows that this combined Fgf signal fully controls nasal retina identity by regulating the nasal transcription factor Foxg1. Surprisingly, nasal-temporal axis specification occurs very early along the dorsal-ventral axis of the evaginating eye. By in vivo imaging GFP-tagged retinal progenitor cells, we find that subsequent eye morphogenesis requires gradual tissue compaction in the nasal half and directed cell movements into the temporal half of the retina. Balancing these processes drives the progressive alignment of the nasal-temporal retina axis with the anterior-posterior body axis and is controlled by a feed-forward effect of Fgf signaling on Foxg1-mediated cell cohesion. Thus, the mechanistic coupling and dynamic synchronization of tissue patterning with morphogenetic cell behavior through Fgf signaling leads to the graded allocation of cell positional identity in the eye, underlying retinotectal map formation.
Genes / Markers
Figures
Figure Gallery (16 images) / 2
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Expression
Phenotype
Mutations / Transgenics
Allele Construct Type Affected Genomic Region
kca66TgTransgenic Insertion
    nkhgn42aEtTransgenic Insertion
      pd1TgTransgenic Insertion
        t22030
          Point Mutation
          t24149
            Point Mutation
            ti282a
              Point Mutation
              tud103TgTransgenic Insertion
                vu119TgTransgenic Insertion
                  zf106TgTransgenic Insertion
                    1 - 9 of 9
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                    Human Disease / Model
                    No data available
                    Sequence Targeting Reagents
                    Target Reagent Reagent Type
                    fgf24MO1-fgf24MRPHLNO
                    foxg1aMO1-foxg1aMRPHLNO
                    foxg1aMO2-foxg1aMRPHLNO
                    1 - 3 of 3
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                    Fish
                    Antibodies
                    Orthology
                    Gene Orthology
                    foxd1
                    foxd2
                    1 - 2 of 2
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                    Engineered Foreign Genes
                    Marker Marker Type Name
                    DsRed2EFGDsRed2
                    EGFPEFGEGFP
                    GFPEFGGFP
                    1 - 3 of 3
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                    Mapping
                    No data available