scholarly journals Analysis of cellular behavior and cytoskeletal dynamics reveal a constriction mechanism driving optic cup morphogenesis

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
María Nicolás-Pérez ◽  
Franz Kuchling ◽  
Joaquín Letelier ◽  
Rocío Polvillo ◽  
Jochen Wittbrodt ◽  
...  

Contractile actomyosin networks have been shown to power tissue morphogenesis. Although the basic cellular machinery generating mechanical tension appears largely conserved, tensions propagate in unique ways within each tissue. Here we use the vertebrate eye as a paradigm to investigate how tensions are generated and transmitted during the folding of a neuroepithelial layer. We record membrane pulsatile behavior and actomyosin dynamics during zebrafish optic cup morphogenesis by live imaging. We show that retinal neuroblasts undergo fast oscillations and that myosin condensation correlates with episodic contractions that progressively reduce basal feet area. Interference with lamc1 function impairs basal contractility and optic cup folding. Mapping of tensile forces by laser cutting uncover a developmental window in which local ablations trigger the displacement of the entire tissue. Our work shows that optic cup morphogenesis is driven by a constriction mechanism and indicates that supra-cellular transmission of mechanical tension depends on ECM attachment.

2016 ◽  
Author(s):  
María Nicolás-Pérez ◽  
Franz Kuchling ◽  
Joaquín Letelier ◽  
Rocío Polvillo ◽  
Jochen Wittbrodt ◽  
...  

2021 ◽  
Vol 476 ◽  
pp. 128-136
Author(s):  
Macaulie A. Casey ◽  
Sarah Lusk ◽  
Kristen M. Kwan

Development ◽  
1998 ◽  
Vol 125 (13) ◽  
pp. 2425-2432 ◽  
Author(s):  
T. Hollemann ◽  
E. Bellefroid ◽  
T. Pieler

Genetic circuits responsible for the development of photoreceptive organs appear to be evolutionarily conserved. Here, the Xenopus homologue Xtll of the Drosophila gene tailless (tll), which we find to be expressed during early eye development, is characterized with respect to its relationship to vertebrate regulators of eye morphogenesis, such as Pax6 and Rx. Expression of all three genes is first detected in the area corresponding to the eye anlagen within the open neural plate in partially overlapping, but not identical, patterns. During the evagination of the optic vesicle, Xtll expression is most prominent in the optic stalk, as well as in the distal tip of the forming vesicle. In tadpole-stage embryos, Xtll gene transcription is most prominent in the ciliary margin of the optic cup. Inhibition of Xtll function in Xenopus embryos interferes specifically with the evagination of the eye vesicle and, in consequence, Xpax6 gene expression is severely reduced in such manipulated embryos. These findings suggest that Xtll serves an important regulatory function in the earliest phases of vertebrate eye development.


Development ◽  
1991 ◽  
Vol 112 (4) ◽  
pp. 1053-1061 ◽  
Author(s):  
A.P. Monaghan ◽  
D.R. Davidson ◽  
C. Sime ◽  
E. Graham ◽  
R. Baldock ◽  
...  

The mouse Hox-7.1 gene has previously been shown to be related to the Drosophila Msh homeobox-containing gene. Here we report the isolation of a new member of this family which resides at an unlinked chromosomal location and has been designated Hox-8.1. Both Hox-7.1 and Hox-8.1 are expressed in the mouse embryo during the early stages of eye development in a distinct spatial and temporal relationship. Hox-8.1 is expressed in the surface ectoderm and in the optic vesicle before invagination occurs in regions corresponding to the prospective corneal epithelium and neural retina, respectively. Hox-7.1 is expressed after formation of the optic cup, marking the domain that will give rise to the ciliary body. The activity of these genes indicates that the inner layer of the optic cup is differentiated into three distinct compartments before overt cellular differentiation occurs. Our results suggest that these genes are involved in defining the region that gives rise to the inner layer of the optic cup and in patterning this tissue to define the iris, ciliary body and retina.


2019 ◽  
Vol 26 (2) ◽  
pp. 185-196 ◽  
Author(s):  
Marcos J. Cardozo ◽  
María Almuedo-Castillo ◽  
Paola Bovolenta

The primordium of the vertebrate eye is composed of a pseudostratified and apparently homogeneous neuroepithelium, which folds inward to generate a bilayered optic cup. During these early morphogenetic events, the optic vesicle is patterned along three different axes—proximo-distal, dorso-ventral, and naso-temporal—and three major domains: the neural retina, the retinal pigment epithelium (RPE), and the optic stalk. These fundamental steps that enable the subsequent development of a functional eye, entail the precise coordination among genetic programs. These programs are driven by the interplay of signaling pathways and transcription factors, which progressively dictate how each tissue should evolve. Here, we discuss the contribution of the Hh, Wnt, FGF, and BMP signaling pathways to the early patterning of the retina. Comparative studies in different vertebrate species have shown that their morphogenetic activity is repetitively used to orchestrate the progressive specification of the eye with evolutionary conserved mechanisms that have been adapted to match the specific need of a given species.


2018 ◽  
Author(s):  
Girish R. Kale ◽  
Xingbo Yang ◽  
Jean-Marc Philippe ◽  
Madhav Mani ◽  
Pierre-François Lenne ◽  
...  

AbstractDuring epithelial morphogenesis, cell contacts (junctions) are constantly remodeled by mechanical forces that work against adhesive forces. E-cadherin complexes play a pivotal role in this process by providing persistent cell adhesion and by transmitting mechanical tension. In this context, it is unclear how mechanical forces affect E-cadherin adhesion and junction dynamics.During Drosophila embryo axis elongation, Myosin-II activity in the apico-medial and junctional cortex generates mechanical forces to drive junction remodeling. Here we report that the ratio between Vinculin and E-cadherin intensities acts as a ratiometric readout for these mechanical forces (load) at E-cadherin complexes. Medial Myosin-II loads E-cadherin complexes on all junctions, exerts tensile forces, and increases levels of E-cadherin. Junctional Myosin-II, on the other hand, biases the distribution of load between junctions of the same cell, exerts shear forces, and decreases the levels of E-cadherin. This work suggests distinct effects of tensile versus shear stresses on E-cadherin adhesion.


2014 ◽  
Author(s):  
Stephan Heermann ◽  
Lucas Schuetz ◽  
Steffen Lemke ◽  
Kerstin Krieglstein ◽  
Joachim Wittbrodt

The transformation of the oval optic vesicle to a hemispheric bi-layered optic cup involves major morphological changes during early vertebrate eye development. According to the classical view, the lens-averted epithelium differentiates into the retinal pigmented epithelium (RPE), while the lens-facing epithelium forms the neuroretina. We find a 4.7 fold increase of the entire basal surface of the optic cup. Although the area an individual RPC demands at its basal surface declines during optic cup formation, we find a 4.7 fold increase of the entire basal surface of the optic cup. We demonstrate that the lens-averted epithelium functions as reservoir and contributes to the growing neuroretina by epithelial flow around the distal rims of the optic cup. This flow is negatively modulated by BMP, which arrests epithelial flow. This inhibition results in persisting neuroretina in the RPE domain and ultimately in coloboma.


eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Stephan Heermann ◽  
Lucas Schütz ◽  
Steffen Lemke ◽  
Kerstin Krieglstein ◽  
Joachim Wittbrodt

The hemispheric, bi-layered optic cup forms from an oval optic vesicle during early vertebrate eye development through major morphological transformations. The overall basal surface, facing the developing lens, is increasing, while, at the same time, the space basally occupied by individual cells is decreasing. This cannot be explained by the classical view of eye development. Using zebrafish (Danio rerio) as a model, we show that the lens-averted epithelium functions as a reservoir that contributes to the growing neuroretina through epithelial flow around the distal rims of the optic cup. We propose that this flow couples morphogenesis and retinal determination. Our 4D data indicate that future stem cells flow from their origin in the lens-averted domain of the optic vesicle to their destination in the ciliary marginal zone. BMP-mediated inhibition of the flow results in ectopic neuroretina in the RPE domain. Ultimately the ventral fissure fails to close resulting in coloboma.


Development ◽  
1970 ◽  
Vol 23 (2) ◽  
pp. 491-507
Author(s):  
Thomas L. Pearce ◽  
Johan Zwaan

The first sign of differentiation of the lens rudiment is a change in cellular shape, as in many other embryonic systems (Tilney, 1968a). This occurs some time before the beginning of overt chemical differentiation, the appearance of specific proteins (Zwaan, 1968). From stage 11 (Hamburger & Hamilton, 1951), just after the optic cup contacts the surface ectoderm, to stage 13, before the onset of invagination, the lens Anlage is rapidly transformed from a cuboidal to a high columnar epithelium, a process described by McKeehan (1951) as palisading. This is slightly preceded in time by nuclear rearrangement. First irregular in outline and randomly oriented, the nuclei become smooth and oval, and aligned at right angles to the surface. They take up positions in the basal portions of the cells (McKeehan, 1951). The development of a highly asymmetric cell form probably leads to the creation of tensile forces at the cell surface.


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