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

PLoS biology, 2009-10, Vol.7 (10), p.e1000214-e1000214 [Peer Reviewed Journal]

Picker et al. 2009 ;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: Picker A, Cavodeassi F, Machate A, Bernauer S, Hans S, et al. (2009) Dynamic Coupling of Pattern Formation and Morphogenesis in the Developing Vertebrate Retina. PLoS Biol 7(10): e1000214. doi:10.1371/journal.pbio.1000214 ;ISSN: 1545-7885 ;ISSN: 1544-9173 ;EISSN: 1545-7885 ;DOI: 10.1371/journal.pbio.1000214 ;PMID: 19823566

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Title:
Dynamic coupling of pattern formation and morphogenesis in the developing vertebrate retina
Author: Picker, Alexander ; Cavodeassi, Florencia ; Machate, Anja ; Bernauer, Sabine ; Hans, Stefan ; Abe, Gembu ; Kawakami, Koichi ; Wilson, Stephen W ; Brand, Michael
Harris, William A.
Subjects: Animals ; Body Patterning - physiology ; Cell Biology/Cell Adhesion ; Cell Biology/Cell Signaling ; Cell Biology/Developmental Molecular Mechanisms ; Cell Biology/Gene Expression ; Cell Biology/Morphogenesis and Cell Biology ; Cellular biology ; Developmental Biology/Developmental Molecular Mechanisms ; Developmental Biology/Embryology ; Developmental Biology/Molecular Development ; Developmental Biology/Morphogenesis and Cell Biology ; Developmental Biology/Neurodevelopment ; Developmental Biology/Pattern Formation ; Embryo, Nonmammalian - embryology ; Embryos ; Female ; Fibroblast Growth Factor 3 - physiology ; Fibroblast Growth Factors - physiology ; Forkhead Transcription Factors - physiology ; Genetics and Genomics/Animal Genetics ; Neuroscience/Neurodevelopment ; Neuroscience/Sensory Systems ; Retina ; Retina - embryology ; Signal Transduction - physiology ; Zebrafish ; Zebrafish Proteins - physiology
Is Part Of: PLoS biology, 2009-10, Vol.7 (10), p.e1000214-e1000214
Description: 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.
Publisher: United States: Public Library of Science
Language: English
Identifier: ISSN: 1545-7885
ISSN: 1544-9173
EISSN: 1545-7885
DOI: 10.1371/journal.pbio.1000214
PMID: 19823566
Source: DOAJ : Directory of Open Access Journals
Public Library of Science (PLoS) Journals Open Access
Open Access: PubMed Central
Geneva Foundation Free Medical Journals at publisher websites
AUTh Library subscriptions: ProQuest Central
MEDLINE

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

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