Picker, A;
Cavodeassi, F;
Machate, A;
Bernauer, S;
Hans, S;
Abe, G;
Kawakami, K;
... Brand, M; + view all
(2009)
Dynamic Coupling of Pattern Formation and Morphogenesis in the Developing Vertebrate Retina.
PLOS BIOL
, 7
(10)
, Article e1000214. 10.1371/journal.pbio.1000214.
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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.
| Type: | Article |
|---|---|
| Title: | Dynamic Coupling of Pattern Formation and Morphogenesis in the Developing Vertebrate Retina |
| Open access status: | An open access version is available from UCL Discovery |
| DOI: | 10.1371/journal.pbio.1000214 |
| Publisher version: | http://dx.doi.org/10.1371/journal.pbio.1000214 |
| Language: | English |
| Additional information: | © 2009 Picker et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by grants to MB by the Deutsche Forschungsgemeinschaft (SFB 655) and the European Union (Zf-Models and Endotrack), the Medical Research Council and Wellcome Trust to SW, and the National BioResource Project and grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan to KK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. |
| Keywords: | MIDBRAIN-HINDBRAIN BOUNDARY, DEVELOPING CHICK RETINA, ZEBRAFISH LATERAL-LINE, GLASS-ONION LOCUS, SIGNALING CENTER, NEURAL RETINA, IN-VIVO, EPITHELIAL MORPHOGENESIS, PROJECTION MAP, OPTIC VESICLE |
| UCL classification: | UCL UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Cell and Developmental Biology |
| URI: | https://discovery-pp.ucl.ac.uk/id/eprint/121065 |
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