Extracellular matrix contribution to skin wound re-epithelialization

Rousselle, Patricia; Montmasson, Marine; Garnier, Cécile

doi:10.1016/j.matbio.2018.01.002

Cited by 225 publications

(206 citation statements)

References 180 publications

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“…This underscores that rearranging laminins into fibrous structures via traction stresses is a fundamentally important feature of tissue organization. Similar phenomena might occur in vivo , since extracellular spaces where vasculogenesis takes place during development (35, 36), or angiogenesis during tissue regeneration (37) are generally rich in laminin.…”

Section: Discussionmentioning

confidence: 74%

Cell based strain stiffening of a non-fibrous matrix as organizing principle for morphogenesis

Rüdiger

Kick

Goychuk

et al. 2019

Preprint

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Endothelial tube formation on a reconstituted extracellular matrix (Matrigel) is a wellestablished in vitro model for studying the processes of angiogenesis and vasculogenesis. However, to date, the organizing principles that underlie the morphogenesis of this network, and that shape the initial process of cell-cell finding remain elusive. Furthermore, it is unclear how in vitro results extrapolate to in vivo morphogenesis. Here, we identify a mechanism that allows cells to form networks by mechanically reorganizing and stiffening their extracellular matrix, independent of chemical guidance cues. Interestingly, we find that this cellular self-organization strongly depends on the connectivity and topology of the surrounding matrix, as well as on cell contractility and cell density. Cells rearrange the matrix, and form bridges of matrix material that are stiffer than their surroundings, thus creating a durotactic track for the initiation of cell-cell contacts. This contractility-based communication via strain stiffening and matrix rearrangement might be a general organizing principle during tissue development or regeneration.3 Significance StatementIn addition to chemotactic gradients, biomechanical cues are important for guiding biological pattern formation. Self-assembly of cells has often been ascribed to reorganization of collagen fibres in the extracellular matrix. However, the basement membrane surrounding vascular cells, is per se non-fibrous. Here, we find that this difference in matrix topology can crucially influence cell behaviour and pattern formation. In a homogeneously elastic environment like the basement membrane, endothelial cells rearrange extracellular matrix proteins by contractile force, forming stiff intercellular bridges as tracks for cell-cell contacts. Our findings shine some light why there is a lot of merit in having multiple approaches to matrix elasticity (like continuum theories or dilated network approaches). Our observations might help to understand why vascular nets look different in different tissues and after rearrangement of the extracellular matrix during disease.

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Section: Discussionmentioning

confidence: 74%

Cell based strain stiffening of a non-fibrous matrix as organizing principle for morphogenesis

Rüdiger

Kick

Goychuk

et al. 2019

Preprint

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“…Numerous investigations have shown that reepithelialization is necessary for restoration of the epidermis during the burn wound healing (Rousselle, Montmasson, & Garnier, ). Our results showed that ECSs exert important functions in promoting reepithelialization during this process.…”

Section: Discussionmentioning

confidence: 99%

Curcumin promotes burn wound healing in mice by upregulating caveolin‐1 in epidermal stem cells

Yang

Wang

Zhou

et al. 2018

Phytotherapy Research

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We aimed to explore the effect of curcumin on epidermal stem cells (ESCs) in regulating wound healing and the underlying molecular mechanism. We treated mouse ESCs isolated from skin tissues with curcumin, and then assessed the proliferation ability of cells induced by epidermal growth factor using cell counting kit-8 assay. The pluripotency of ESCs was evaluated as well through examination of Nanog expression in ESCs. Further, mice with skin burns were treated with ESCs with or without curcumin pretreatments. Histological evaluations were then preformed to determine wound scores, cell proliferation, reepithelialization, and capillary density in wounds.Curcumin treatment promoted the proliferative ability of ESCs and conditioned medium from curcumin-treated ESCs enhanced human umbilical vein endothelial cell (HUVEC) tube formation. We also found curcumin treatment elevated caveolin-1 expression in ESCs, which was required for the beneficial effect of curcumin on ESC proliferation and HUVEC tube formation. Next, using a mouse model of burn wound healing, curcumin-treated ESCs exhibited enhanced wound closure, which also required caveolin-1 expression. Our current study demonstrates the beneficial effect of curcumin on burn wound healing in mice, which is mediated by upregulating caveolin-1 in ESCs, and supports the potential therapeutic role of curcumin in ESC-based treatment against skin wound healing.

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“…The blister plane induced by alkylating agents such as SM coincides precisely with the histological location of laminin‐332 (LM‐332). In normal healthy skin, basal keratinocytes adhere to the basement membrane and the underlying dermis by stable anchoring complexes (made of type VII collagen) attached to anchoring filaments composed of LM‐332 (Marinkovich et al, 1993; Rousselle et al, 1997, 2019; Brittingham et al, 2006; Marinkovich, 2008; Rousselle and Beck, 2013). LM‐332 is a glycoprotein made up of three polypeptide chains (α3, β3, and γ2) that are distinct gene products (see Fig.…”

Section: Figurementioning

confidence: 99%

Expression of Laminin γ2 Proteolytic Fragments in Murine Skin Following Exposure to Sulfur Mustard

Chang

Wang

Chang

et al. 2020

The Anatomical Record

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Laminin-332 is a basement membrane protein composed of three genetically distinct polypeptide chains that actively promote both skin epidermal cell adhesion and migration. Proteolytic fragments of the laminin γ2 chain stimulate migration and scattering of keratinocytes and cancer cells. Sulfur mustard (SM) is a bifunctional alkylating agent that induces separation of basal keratinocytes from the dermal-epidermal junction and invokes a strong inflammatory response leading to delayed wound repair. In the present studies, the role of laminin γ2 in SM-induced skin injury and wound repair was investigated using the mouse ear vesicant model. We found that laminin γ2 chain mRNA was preferentially upregulated in mouse ear skin exposed to SM. In situ hybridization confirmed overexpression of laminin γ2 transcript. Western blot analysis showed increased protein expression of the full-length proform of laminin γ2 and smaller processed fragments of laminin γ2 in skin exposed to SM. Dual immunofluorescence labeling indicated that laminin γ2 fragments are prevalent in suprabasal keratinocytes behind the leading edge in areas of hyperplasia in injured skin. In addition, co-expression of laminin γ2 and the senescent marker, p16 INK4a was found to overlap with the hyperplastic migratory epithelial sheet. This observation is similar to hypermotile keratinocytes reported in invasive carcinoma cells. Overall, our studies indicate that laminin γ2 is preferentially expressed in skin post SM exposure and that protein expression appears to become progressively more fragmented. The laminin γ2 fragments may play a role in regulating SM-induced skin wound repair. Anat

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Extracellular matrix contribution to skin wound re-epithelialization

Cited by 225 publications

References 180 publications

Cell based strain stiffening of a non-fibrous matrix as organizing principle for morphogenesis

Cell based strain stiffening of a non-fibrous matrix as organizing principle for morphogenesis

Curcumin promotes burn wound healing in mice by upregulating caveolin‐1 in epidermal stem cells

Expression of Laminin γ2 Proteolytic Fragments in Murine Skin Following Exposure to Sulfur Mustard

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