Collective cell migration of primary zebrafish keratocytes

Rapanan, Jose L.; Cooper, Kimbal; Leyva, Kathryn J.; Hull, Elizabeth

doi:10.1016/j.yexcr.2014.06.011

Cited by 21 publications

(34 citation statements)

References 42 publications

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“…This dismisses the presence in detectable amount of scleroblasts or other mesenchymal cells in these cultures. The outgrowth pattern of the cubic cells keeping in close connection to each other in the fresh system was consistent with the behavior of the keratocytes in scale culture [42], thereby giving another indication of the epithelial nature of the fin cells at this stage. Interestingly, Moritz and Labbe [34] showed in the same fresh explant system that numerous cells within the explants are actively proliferating.…”

Section: Discussionsupporting

confidence: 73%

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Stabilization of gene expression and cell morphology after explant recycling during fin explant culture in goldfish

Chênais

Lareyre

Bail

et al. 2015

Experimental Cell Research

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Section: Discussionsupporting

confidence: 73%

“…The epidermis contains epithelial cells, also called keratinocytes [14] or keratocytes [42] and mucous cells. The dermis contains the pigment cells and the mesenchymal cells, and the presence of some stem cells is often proposed although not firmly demonstrated yet [38,51].…”

Section: Discussionmentioning

confidence: 99%

Stabilization of gene expression and cell morphology after explant recycling during fin explant culture in goldfish

Chênais

Lareyre

Bail

et al. 2015

Experimental Cell Research

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“…These retraction events are similar to those reported for primary zebrafish keratocyte collective cell migration on surfaces in the presences of RGD peptide, which inhibits integrin-mediated adhesion. [20] Differential substrate adhesion has been shown to be a main component of mechanosensing, durotaxis, and directional migration [53] and likely is a major contributor to the retraction behavior of the sheets on the different PEMU substrates. Third, individual cells in sheets exhibit morphologies indicative of increased tension (as in Figs.…”

Section: Discussionmentioning

confidence: 99%

“…[16] Edge cell formation of robust vinculin-containing focal adhesions in highly active lamellipodia, in which actin filament turnover is controlled by Rac-dependent signaling pathways, contributes to the traction at the sheet leading edge and development of tension across the sheet that is necessary for plithotaxis. [2–3, 17–20] Myosin II-dependent force production, controlled by Rho-dependent processes, maintains tensile forces on the focal adhesions in cells and across sheet cell-cell junctions. [21–24] Focal adhesions and stress fibers are components of mechanotransduction signaling pathways that enable a cell to sense physical cues from its environment such as surface modulus (stiffness) and intracellular shear stress.…”

Section: Introductionmentioning

confidence: 99%

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Collective epithelial cell sheet adhesion and migration on polyelectrolyte multilayers with uniform and gradients of compliance

Martinez

Schlenoff

Keller

2016

Experimental Cell Research

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Polyelectrolyte multilayers (PEMUs) are tunable thin films that could serve as coatings for biomedical implants. PEMUs built layer by layer with the polyanion poly(acrylic acid) (PAA) modified with a photosensitive 4-(2-hydroxyethoxy) benzophenone (PAABp) group and the polycation poly(allylamine hydrochloride) (PAH) are mechanically tunable by UV irradiation, which forms covalent bonds between the layers and increases PEMU stiffness. PAH-terminated PEMUs (PAH-PEMUs) that were uncrosslinked, UV-crosslinked to a uniform stiffness, or UV-crosslinked with an edge mask or through a neutral density optical gradient filter to form continuous compliance gradients were used to investigate how differences in PEMU stiffness affect the adhesion and migration of epithelial cell sheets from scales of the fish Poecilia sphenops (Black Molly) and Carassius auratus (Comet Goldfish). During the progressive collective cell migration, the edge cells (also known as ‘leader’ cells) in the sheets on softer uncrosslinked PEMUs and less crosslinked regions of the gradient formed more actin filaments and vinculin-containing adherens junctions and focal adhesions than formed in the sheet cells on stiffer PEMUs or glass. During sheet migration, the ratio of edge cell to internal cell (also known as ‘follower’ cells) motilities were greater on the softer PEMUs than on the stiffer PEMUs or glass, causing tension to develop across the sheet and periods of retraction, during which the edge cells lost adhesion to the substrate and regions of the sheet retracted toward the more adherent internal cell region. These retraction events were inhibited by the myosin II inhibitor Blebbistatin, which reduced the motility velocity ratios to those for sheets on the stiffer PEMUs. Blebbistatin also caused disassembly of actin filaments, reorganization of focal adhesions, increased cell spreading at the leading edge, as well as loss of edge cell-cell connections in epithelial cell sheets on all surfaces. Interestingly, cells throughout the interior region of the sheets on uncrosslinked PEMUs retained their actin and vinculin organization at adherens junctions after treatment with Blebbistatin. Like Blebbistatin, a Rho-kinase (ROCK) inhibitor, Y27632, promoted loss of cell-cell connections between edge cells, whereas a Rac1 inhibitor, NSC23766, primarily altered the lamellipodial protrusion in edge cells. Compliance gradient PAH-PEMUs promoted durotaxis of the cell sheets but not of individual keratocytes, demonstrating durotaxis, like plithotaxis, is an emergent property of cell sheet organization.

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Dual inhibition of TGFβR and ROCK reverses the epithelial to mesenchymal transition in collectively migrating zebrafish keratocytes

Pascual

Rapanan

Uppalapati

et al. 2021

Cell Biology International

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There is a growing controversy about the role of the epithelial to mesenchymal transition (EMT) in the fibrosis associated with chronic disease. Recent studies suggest that it is not the EMT transcriptional program but differentiation of progenitor cells, response to chronic inflammation, or some combination of both which cause the appearance of fibroblasts and the production of the extracellular matrix. To address this issue, we study the EMT process in the zebrafish keratocytes which migrate from primary explants of epithelial tissue as these cells are both terminally differentiated and able to divide. To firmly place this EMT process in the context of other systems, we first demonstrate that the zebrafish keratocyte EMT process involves nuclear accumulation of twist and snail/slug transcription factors as part of a TGFβR‐mediated EMT process. As assessed by the expression and localization of EMT transcription factors, the zebrafish keratocyte EMT process is reversed by the addition of Rho‐activated kinase (ROCK) in combination with TGFβR inhibitors. The complete cycle of EMT to MET observed in this system links these in vitro results more closely to the process of wound healing in vivo. However, the absence of observable activation of EMT transcription factors when keratocytes are cultured on compliant substrata in a TGFβ1‐containing medium suggests that ROCK signaling, initiated by tension within the sheet, is an essential contributor to the EMT process. Most importantly, the requirement for ROCK activation by culturing on noncompliant substrata suggests that EMT in these terminally differentiated cells would not occur in vivo.

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Collective cell migration of primary zebrafish keratocytes

Cited by 21 publications

References 42 publications

Stabilization of gene expression and cell morphology after explant recycling during fin explant culture in goldfish

Stabilization of gene expression and cell morphology after explant recycling during fin explant culture in goldfish

Collective epithelial cell sheet adhesion and migration on polyelectrolyte multilayers with uniform and gradients of compliance

Dual inhibition of TGFβR and ROCK reverses the epithelial to mesenchymal transition in collectively migrating zebrafish keratocytes

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