Dynamic coupling of pattern formation and morphogenesis in the developing vertebrate retina
| Autor: | Anja Machate, Michael Brand, Stefan Hans, Sabine Bernauer, Alexander Picker, Stephen W. Wilson, Gembu Abe, Koichi Kawakami, Florencia Cavodeassi |
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| Rok vydání: | 2009 |
| Předmět: |
Embryo
Nonmammalian Body Patterning genetic structures Cell Biology/Cell Signaling Developmental Biology/Pattern Formation Developmental Biology/Molecular Development 0302 clinical medicine Developmental Biology/Developmental Molecular Mechanisms Biology (General) Zebrafish Developmental Biology/Embryology 0303 health sciences Developmental Biology/Morphogenesis and Cell Biology General Neuroscience Forkhead Transcription Factors Optic vesicle Anatomy Neuroscience/Neurodevelopment Cell biology medicine.anatomical_structure Female General Agricultural and Biological Sciences Signal Transduction Research Article Genetics and Genomics/Animal Genetics QH301-705.5 Fibroblast Growth Factor 3 Cell Biology/Developmental Molecular Mechanisms Morphogenesis Biology General Biochemistry Genetics and Molecular Biology Retina 03 medical and health sciences FGF8 medicine Animals Axis specification Cell Biology/Gene Expression 030304 developmental biology Eye morphogenesis General Immunology and Microbiology Neuroscience/Sensory Systems Zebrafish Proteins biology.organism_classification eye diseases Fibroblast Growth Factors Developmental Biology/Neurodevelopment Cell Biology/Cell Adhesion Cell Biology/Morphogenesis and Cell Biology sense organs 030217 neurology & neurosurgery |
| Zdroj: | PLoS Biology PLoS Biology, Vol 7, Iss 10, p e1000214 (2009) |
| ISSN: | 1545-7885 |
| Popis: | In this Research Article, Picker et al. show how cells in the retina get their spatial coordinates. 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. Author Summary The vertebrate brain contains a point-to-point representation of sensory input from the eye. This visual map forms during embryonic development, by neuronal cells of the retina sending targeted axon projections to the brain. Since the projection needs to wire up neighboring cell positions in the retina to neighboring target areas in the brain, all retinal cells must harbor a defined spatial coordinate as prerequisite for map formation. How such a retinal coordinate system is established and maintained in the dynamically evolving embryo is a fundamental, but unresolved, question. By combining genetic analysis and in vivo imaging in zebrafish embryos, we have tracked the developmental origin of cell coordinates in the retina. We find that three related Fgf signals emanating from outside the eye define relative cell positions in the retina very early, already at the onset of its formation. But the absolute position of retinal cells relative to the body axes is greatly rearranged during subsequent development. In this phase, surprisingly, the same Fgf signals that at first defined retinal cell positions now balance asymmetric cell movements and cell shape changes, which are required for harmonic retinal growth and the final alignment of cell coordinates in the eye. |
| Databáze: | OpenAIRE |
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