Dynamic Tissue Rearrangements during Vertebrate Eye Morphogenesis: Insights from Fish Models

Cavodeassi, Florencia

doi:10.3390/jdb6010004

Cited by 19 publications

(21 citation statements)

References 61 publications

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“…Owing to technological improvements, this process has been increasingly investigated in the last decade, especially on teleost models which are amenable to live imaging due to their external development and transparency (England et al, 2006; Ivanovitch et al, 2013; Kwan et al, 2012; Martinez-Morales et al, 2009; Nicolas-Perez et al, 2016; Picker et al, 2009; Rembold et al, 2006; Sidhaye and Norden, 2017). This focus on morphogenesis led to the description of cell and tissue movements during eye development in fish (reviewed in Cavodeassi, 2018) ( Fig. S1 ).…”

Section: Introductionmentioning

confidence: 99%

Eye morphogenesis in the blind Mexican cavefish

Devos

Agnès

Edouard

et al. 2019

Preprint

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24The morphogenesis of the vertebrate eye consists of a complex choreography of cell 25 movements, tightly coupled to axial regionalization and cell type specification processes. Any 26 disturbance in these events can lead to developmental defects and blindness. Here we have 27 deciphered the sequence of defective events leading to coloboma phenotype in the 28 embryonic eye of the blind cavefish of the species Astyanax mexicanus. Using comparative 29 live imaging on targeted enhancer-trap Zic1:hsp70:GFP reporter lines of both the normal, 30 river-dwelling morph and the cave morph of the species, we identified major defects in initial 31 optic vesicle size and optic cup invagination in cavefish. Combining these results with gene 32 expression analyses, we also discovered defects in axial patterning affecting mainly the 33 temporal retina, in optic stalk tissue specification, and in the spreading processes involving 34 the retinal pigmented epithelium cells. Based on these results, we propose a developmental 35 scenario to explain the cavefish phenotype and discuss developmental constraints to 36 morphological evolution. The cavefish eye appears as an outstanding natural mutant model 37 to study molecular and cellular processes involved in optic region morphogenesis. 38 39 65 pigmented epithelium (RPE), expand and flatten to cover the back of the retina (Cechmanek 66 and McFarlane, 2017; Heermann et al., 2015). Together with the basal constriction of lens-67 facing epithelial cells (Martinez-Morales et al., 2009; Nicolas-Perez et al., 2016), these 68 movements lead to optic cup invagination. The invagination process leads to the formation of 69 the optic fissure at the level of the connection of the eye with the optic stalk. This fissure 70allows bloods vessels to invade the eye and leads the way of retino-fugal axons, but needs to 71 close to have a functional and round eye (Gestri et al., 2018). Finally, the entire eye, together 72 with the forebrain, rotates anteriorly, bringing the optic fissure in its final ventral position. 73 Hence, cells that are initially located in the dorsal or ventral part of the optic vesicles 74 contribute to the nasal or temporal quadrant of the retina, respectively (Picker et al., 2009). 75 Failure to correctly complete any of these steps can lead to vision defects; for example, failure 76 to properly close the optic fissure is termed coloboma and can lead to congenital blindness. 77 During the eye morphogenetic process, three types of tissues emerge: (1) the neural retina, 78 facing the lens and composed of various neuronal types, (2) the RPE at the back of the neural 79 retina, with multiple functions including nurturing of photoreceptors (Strauss, 2018), and (3) 80 the optic stalk, transiently connecting the retina to the neural tube. This thin ventral structure 81 is invaded by the ganglionic cells axons and guides them on their way to the tectum. Optic 82 stalk cells then differentiate into reticular astrocytes surrounding the optic nerve (Macdonald 83 et al.,...

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Section: Introductionmentioning

confidence: 99%

Eye morphogenesis in the blind Mexican cavefish

Devos

Agnès

Edouard

et al. 2019

Preprint

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“…AS development begins after the establishment of the optic cup, when POM cells migrate into the periocular space between the retina and the newly established corneal epithelium (5, 7). These mesenchymal cells will eventually differentiate into the corneal stroma and endothelium, iris and ciliary body stroma, and the iridocorneal angle, amongst others.…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal characterization of periocular mesenchyme heterogeneity during anterior segment development

Famulski

Meulen

Vöcking

et al. 2019

Preprint

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Establishment of the ocular anterior segment (AS) is a critical event during development of the vertebrate visual system. Failure in this process leads to Anterior Segment Dysgenesis (ASD), which is characterized by congenital blindness and predisposition to glaucoma. The anterior segment is largely formed via a neural crest-derived population, the Periocular Mesenchyme (POM). In this study, we aimed to characterize POM behaviors and identities during zebrafish AS development. POM distributions and migratory dynamics were analyzed using transgenic zebrafish embryos (Tg[foxC1b:GFP], Tg[foxD3:GFP], Tg[pitx2:GFP], Tg[lmx1b.1:GFP], and Tg[sox10:GFP] throughout the course of early AS development (24-72hpf). In vivo imaging analysis revealed unique AS distribution and migratory behavior among the reporter lines, suggesting AS mesenchyme (ASM) is a heterogenous population. This was confirmed using double in situ hybridization. Furthermore, we generated ASM transcriptomic profiles from our reporter lines and using a four-way comparison analysis uncovered unique ASM subpopulation expression patterns. Taken together, our data reveal for the first time that AS-associated POM is not homogeneous but rather comprised of several unique subpopulations identifiable by their distributions, behaviors, and transcriptomic profiles.

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“…The distinctive anterior of the neural plate (ANP) where the eye and forebrain develop, does not undergo this same neurulation as once thought [ 3 , 23 ]. Its development begins earlier than neurulation, largely as a single coherent field of retinal progenitor cells (RPCs) that contracts from an early broad field to then bifurcate and evaginate to form bilateral optic vesicles [ 1 , 2 , 4 , 15 , 23 , 31 , 33 , 46 , 53 , 64 , 76 , 80 ].…”

Section: Introductionmentioning

confidence: 99%

An enigmatic translocation of the vertebrate primordial eye field

2020

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The primordial eye field of the vertebrate embryo is a single entity of retinal progenitor cells spanning the anterior neural plate before bifurcating to form bilateral optic vesicles. Here we review fate mapping data from zebrafish suggesting that prior to evagination of the optic vesicles the eye field may undergo a Maypole-plait migration of progenitor cells through the midline influenced by the anteriorly subducting diencephalon. Such an enigmatic translocation of scaffolding progenitors could have evolutionary significance if pointing, by way of homology, to an ancient mechanism for transition of the single eye field in chordates to contralateral eye fields in vertebrates.

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Dynamic Tissue Rearrangements during Vertebrate Eye Morphogenesis: Insights from Fish Models

Cited by 19 publications

References 61 publications

Eye morphogenesis in the blind Mexican cavefish

Eye morphogenesis in the blind Mexican cavefish

Spatiotemporal characterization of periocular mesenchyme heterogeneity during anterior segment development

An enigmatic translocation of the vertebrate primordial eye field

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