Author response: Analysis of cellular behavior and cytoskeletal dynamics reveal a constriction mechanism driving optic cup morphogenesis

Nicolás-Pérez, María; Kuchling, Franz; Letelier, Joaquin; Polvillo, Rocío; Wittbrodt, Jochen; Martı́nez-Morales, Juan Ramón

doi:10.7554/elife.15797.039

Cited by 4 publications

(5 citation statements)

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“…Although invagination in CF seems to start properly between 15.5–19.5 hpf, it progresses poorly so that OCs remain elongated. Such timing is reminiscent of the two steps described for OC invagination in zebrafish: basal constriction initiates the primary folding between 18–20 hpf (18–22 ss), followed by rim movement which brings the presumptive retina from the inner OV leaflet into the lens-facing epithelium between 20–24 hpf ( Heermann et al, 2015 ; Nicolas-Perez et al, 2016 ; Sidhaye and Norden, 2017 ). In Astyanax , 18ss corresponds to ∼16.5 hpf ( Hinaux et al, 2011 ), hence initial basal constriction leading to initiation of OC invagination may be partly conserved in cavefish.…”

Section: Resultsmentioning

confidence: 96%

“…The latter is weak but not absent in CF, as the posterior OC still manages to contact the lens, at later stages. The defective rim movement might be due to various causes, including defects in the basal membrane or failure to establish proper focal adhesion as in the ojoplano medaka mutant ( Martinez-Morales et al, 2009 ; Nicolas-Perez et al, 2016 ; Sidhaye and Norden, 2017 ). Alternatively, active migration could be altered by extrinsic signals, as in BMP overexpression experiments where the cell flow toward the lens-facing epithelium is reduced ( Heermann et al, 2015 ).…”

Section: Resultsmentioning

confidence: 99%

“…Cells fated to the retinal pigmented epithelium (RPE) expand and flatten to cover the back of the retina ( Cechmanek and McFarlane, 2017 ; Heermann et al, 2015 ). Together with basal constriction of lens-facing epithelial cells ( Martinez-Morales et al, 2009 ; Nicolas-Perez et al, 2016 ), these movements lead to optic cup (OC) invagination, and also to the formation of the optic fissure, which needs to close to have a proper, round eye ( Gestri et al, 2018 ). Finally, the entire forebrain rotates anteriorly, bringing the fissure in its final ventral position.…”

Section: Introductionmentioning

confidence: 99%

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Eye morphogenesis in the blind Mexican cavefish

et al. 2021

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The morphogenesis of the vertebrate eye consists of a complex choreography of cell movements, tightly coupled to axial regionalization and cell type specification processes. Disturbances in these events can lead to developmental defects and blindness. Here, we have deciphered the sequence of defective events leading to coloboma in the embryonic eye of the blind cavefish of the species Astyanax mexicanus. Using comparative live imaging on targeted enhancer-trap Zic1:hsp70:GFP reporter lines of both the normal, river-dwelling morph and the cave morph of the species, we identified defects in migratory cell behaviors during evagination which participate in the reduced optic vesicle size in cavefish, without proliferation defect. Further, impaired optic cup invagination shifts the relative position of the lens and contributes to coloboma in cavefish. Based on these results, we propose a developmental scenario to explain the cavefish phenotype and discuss developmental constraints to morphological evolution. The cavefish eye appears as an outstanding natural mutant model to study molecular and cellular processes involved in optic region morphogenesis.

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Section: Resultsmentioning

confidence: 96%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Eye morphogenesis in the blind Mexican cavefish

et al. 2021

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“…Later, the invagination i.e. the remodelling of the vesicle into a cup is suggested to occur through basal constriction in the centre of the retina epithelium, which may transmit tension at the tissue scale to trigger the bending of the retina 41,42 . Rim movements of cells from the medial layer of the cup into the lateral layer 40,42 , and the spreading of the retinal pigmented epithelium over the forming cup 69 have also been proposed to contribute to optic cup invagination.…”

Section: Discussionmentioning

confidence: 99%

“…The optic cup develops close to the OP in a deeper, more ventral position, through extensive evagination and invagination movements having both a strong lateral component 30,[38][39][40][41][42][43][44] (Figure 2A).…”

Section: Op and Eye Cell Movements Are Correlated Along The Mediolateral Axismentioning

confidence: 99%

Intertissue mechanical interactions shape the olfactory circuit in zebrafish

Monnot

Baraban

Pottin

et al. 2021

Preprint

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While the chemical signals guiding neuronal migration and axon elongation have been extensively studied, the influence of mechanical cues on these processes remains poorly studied in vivo. Here, we investigate how mechanical forces exerted by surrounding tissues steer neuronal movements and axon extension during the morphogenesis of the olfactory placode in zebrafish. We mainly focus on the mechanical contribution of the adjacent eye tissue, which develops underneath the placode through extensive evagination and invagination movements. Using quantitative analysis of cell movements and biomechanical manipulations, we show that the developing eye exerts lateral traction forces on the olfactory placode through extracellular matrix, mediating proper morphogenetic movements and axon extension within the placode. Our data shed new light on the key participation of intertissue mechanical interactions in the sculpting of neuronal circuits.

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Analysis of gene network bifurcation during optic cup morphogenesis in zebrafish

Bono

Naranjo

Moreno-Mármol

et al. 2020

Preprint

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SummarySight depends on the tight cooperation between photoreceptors and pigmented cells. Both derive from common progenitors in which a single gene regulatory network (GRN) bifurcates into the neural retina (NR) and retinal-pigmented epithelium (RPE) programs. Although genetic studies have identified upstream nodes controlling these networks, their regulatory logic remains poorly investigated. Here, we characterize transcriptome dynamics (RNA-seq) and chromatin accessibility (ATAC-seq) in segregating NR/RPE populations in zebrafish. Analysis of active cis-regulatory modules and enriched transcription factor (TF) motives suggest extensive network redundancy and context-dependent TF activity. Downstream targets identification highlights an early recruitment of desmosomal genes in the flattening RPE, revealing Tead factors as upstream regulators. Investigation of GRNs dynamics uncovers an unexpected sequence of TF recruitment during RPE specification, which is conserved in humans. This systematic interrogation of the NR/RPE bifurcation should improve both genetic counselling for eye disorders and hiPSCs-to-RPE differentiation protocols for cell-replacement therapies in degenerative diseases.

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Author response: Analysis of cellular behavior and cytoskeletal dynamics reveal a constriction mechanism driving optic cup morphogenesis

Cited by 4 publications

References 0 publications

Eye morphogenesis in the blind Mexican cavefish

Eye morphogenesis in the blind Mexican cavefish

Intertissue mechanical interactions shape the olfactory circuit in zebrafish

Analysis of gene network bifurcation during optic cup morphogenesis in zebrafish

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