Collective cell migration during optic cup formation features changing cell-matrix interactions linked to matrix topology

Soans, Karen G.; Ramos, Ana Patricia; Sidhaye, Jaydeep; Krishna, Abhijeet; Solomatina, Anastasia I.; Hoffmann, Karl B.; Schlüßler, Raimund; Guck, Jochen; Sbalzarini, Ivo F.; Modes, Carl D.; Norden, Caren

doi:10.1016/j.cub.2022.09.034

Cited by 15 publications

(11 citation statements)

References 57 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These material properties are properly influenced by characteristics of the BM partially described in this Review: BM composition, turnover, thickness, polarization, density, microstructure, and crosslinking are structural changes described for different mechanisms that can appear during development and direct morphogenesis. Live imaging of fluorescently tagged BM components helped to understand how the BM acted in vivo in the past years, and measurements using FRAP or optogenetics can be used to quantify BM turnover and elastic or viscoelastic behavior of BM components ( Keeley et al, 2020 ; Matsubayashi et al, 2017 , 2020 ; Morgner et al, 2023 ; Soans et al, 2022 ). Additionally, Atomic force microscopy and Brillouin microscopy have emerged as excellent tools for studying BM mechanics ( Prevedel et al, 2019 ; Töpfer et al, 2022b ; Viji Babu and Radmacher, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

Basement membrane dynamics and mechanics in tissue morphogenesis

Töpfer

2023

Biology Open

View full text Add to dashboard Cite

The basement membrane (BM) is a thin, planar-organized extracellular matrix that underlies epithelia and surrounds most organs. During development, the BM is highly dynamic and simultaneously provides mechanical properties that stabilize tissue structure and shape organs. Moreover, it is important for cell polarity, cell migration, and cell signaling. Thereby BM diverges regarding molecular composition, structure, and modes of assembly. Different BM organization leads to various physical features. The mechanisms that regulate BM composition and structure and how this affects mechanical properties are not fully understood. Recent studies show that precise control of BM deposition or degradation can result in BMs with locally different protein densities, compositions, thicknesses, or polarization. Such heterogeneous matrices can induce temporospatial force anisotropy and enable tissue sculpting. In this Review, I address recent findings that provide new perspectives on the role of the BM in morphogenesis.

show abstract

Section: Discussionmentioning

confidence: 99%

Basement membrane dynamics and mechanics in tissue morphogenesis

Töpfer

2023

Biology Open

View full text Add to dashboard Cite

show abstract

“…As the OV bends inwards, the lateral-NR layer keeps growing through the continuous incorporation of neuroepithelial cells from the medial OV layer through a collective migration process ( Sidhaye and Norden, 2017 ; Soans et al, 2022 ) known as ‘rim involution’ or ‘epithelial flow’ ( Heermann et al, 2015 ; Kwan et al, 2012 ; Picker et al, 2009 ; Sidhaye and Norden, 2017 ). This event is part of broader cellular rearrangements characterized by ‘pinwheel’-like movements that begin with OV evagination, displacing NR and RPE precursors into more posterior positions, and promoting the incorporation of new cells from the neural tube ( Kwan et al, 2012 ).…”

Section: Folding Of the Optic Vesicle Into An Optic Cup In Fast-devel...mentioning

confidence: 99%

“…Rim involution takes place mostly at the ventral hinge ( Fig. 2 A) through the dynamic extrusion of cryptic basal lamellipodia that extend in the direction of migration, attaching to the ECM ( Heermann et al, 2015 ; Kwan et al, 2012 ; Sidhaye and Norden, 2017 ; Soans et al, 2022 ), thereby enabling cellular translocation ( Heermann et al, 2015 ; Sidhaye and Norden, 2017 ). Notably, the ECM surrounding the OV, in part deposited by periocular neural crest cells ( Bryan et al, 2020 ), undergoes topological changes that are associated with different cellular dynamics, thereby influencing the efficiency of directed collective rim cell migration ( Soans et al, 2022 ).…”

Section: Folding Of the Optic Vesicle Into An Optic Cup In Fast-devel...mentioning

confidence: 99%

“…2 A) through the dynamic extrusion of cryptic basal lamellipodia that extend in the direction of migration, attaching to the ECM ( Heermann et al, 2015 ; Kwan et al, 2012 ; Sidhaye and Norden, 2017 ; Soans et al, 2022 ), thereby enabling cellular translocation ( Heermann et al, 2015 ; Sidhaye and Norden, 2017 ). Notably, the ECM surrounding the OV, in part deposited by periocular neural crest cells ( Bryan et al, 2020 ), undergoes topological changes that are associated with different cellular dynamics, thereby influencing the efficiency of directed collective rim cell migration ( Soans et al, 2022 ). Besides the important role of the surrounding ECM, bone morphogenetic protein (BMP) signalling seems to facilitate this involution ( Heermann et al, 2015 ), which, if disrupted, either by manipulating BMP signalling or by interfering with lamellipodia formation, prevents the acquisition of a proper cup shape.…”

Section: Folding Of the Optic Vesicle Into An Optic Cup In Fast-devel...mentioning

confidence: 99%

See 1 more Smart Citation

Optic cup morphogenesis across species and related inborn human eye defects

2023

View full text Add to dashboard Cite

The vertebrate eye is shaped as a cup, a conformation that optimizes vision and is acquired early in development through a process known as optic cup morphogenesis. Imaging living, transparent teleost embryos and mammalian stem cell-derived organoids has provided insights into the rearrangements that eye progenitors undergo to adopt such a shape. Molecular and pharmacological interference with these rearrangements has further identified the underlying molecular machineries and the physical forces involved in this morphogenetic process. In this Review, we summarize the resulting scenarios and proposed models that include common and species-specific events. We further discuss how these studies and those in environmentally adapted blind species may shed light on human inborn eye malformations that result from failures in optic cup morphogenesis, including microphthalmia, anophthalmia and coloboma.

show abstract

“…At the individual scale, cells polarize along a leading-trailing axis. Protrusion and adhesion formation are biased to cells' leading edges, and contractility and adhesion removal to their trailing edges, much as in cells migrating solo [6][7][8] . At the tissue scale, cells throughout the epithelium are polarized such that their leading edges preferentially point in the direction of migration, and trailing edges in the opposite direction, a form of planar cell polarity.…”

Section: Introductionmentioning

confidence: 99%

Fat2 polarizes Lar and Sema5c to coordinate the motility of collectively migrating epithelial cells

Williams

Horne‐Badovinac

2023

Preprint

View full text Add to dashboard Cite

Migrating epithelial cells globally align their migration machinery to achieve tissue-level movement. Biochemical signaling across leading-trailing cell-cell interfaces can promote this alignment by partitioning migratory behaviors like protrusion and retraction to opposite sides of the interface. However, how the necessary signaling proteins become organized at this site is poorly understood. The follicular epithelial cells ofDrosophila melanogasterhave two signaling modules at their leading-trailing interfaces—one composed of the atypical cadherin Fat2 and the receptor tyrosine phosphatase Lar, and one composed of Semaphorin 5c and its receptor Plexin A. Here we show that these modules form one interface signaling system with Fat2 at its core. Trailing edge-enriched Fat2 concentrates both Lar and Sema5c at cells’ leading edges, likely by slowing their turnover at this site. Once localized, Lar and Sema5c act in parallel to promote collective migration. Our data suggest a model in which Fat2 couples and polarizes the distributions of multiple effectors that work together to align the migration machinery of neighboring cells.

show abstract

Collective cell migration during optic cup formation features changing cell-matrix interactions linked to matrix topology

Cited by 15 publications

References 57 publications

Basement membrane dynamics and mechanics in tissue morphogenesis

Basement membrane dynamics and mechanics in tissue morphogenesis

Optic cup morphogenesis across species and related inborn human eye defects

Fat2 polarizes Lar and Sema5c to coordinate the motility of collectively migrating epithelial cells

Contact Info

Product

Resources

About