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Plant cell adhesion and growth on artificial fibrous scaffolds as an in vitro model for plant development.

ABSTRACT: Mechanistic studies of plant development would benefit from an in vitro model that mimics the endogenous physical interactions between cells and their microenvironment. Here, we present artificial scaffolds to which both solid- and liquid-cultured tobacco BY-2 cells adhere without perturbing cell morphology, division, and cortical microtubule organization. Scaffolds consisting of polyvinylidene tri-fluoroethylene (PVDF-TrFE) were prepared to mimic the cell wall’s fibrillar structure and its relative hydrophobicity and piezoelectric property. We found that cells adhered best to scaffolds consisting of nanosized aligned fibers. In addition, poling of PVDF-TrFE, which orients the fiber dipoles and renders the scaffold more piezoelectric, increased cell adhesion. Enzymatic treatments revealed that the plant cell wall polysaccharide, pectin, is largely responsible for cell adhesion to scaffolds, analogous to pectin-mediated cell adhesion in plant tissues. Together, this work establishes the first plant biomimetic scaffolds that will enable studies of how cell-cell and cell-matrix interactions affect plant developmental pathways.

SUBMITTER: Calcutt R

PROVIDER: S-EPMC8528414 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Plant cell adhesion and growth on artificial fibrous scaffolds as an in vitro model for plant development.

Calcutt Ryan R Vincent Richard R Dean Derrick D Arinzeh Treena Livingston TL Dixit Ram R

Science advances 20211020 43

Mechanistic studies of plant development would benefit from an in vitro model that mimics the endogenous physical interactions between cells and their microenvironment. Here, we present artificial scaffolds to which both solid- and liquid-cultured tobacco BY-2 cells adhere without perturbing cell morphology, division, and cortical microtubule organization. Scaffolds consisting of polyvinylidene tri-fluoroethylene (PVDF-TrFE) were prepared to mimic the cell wall’s fibrillar structure and its rela ...[more]

PMID: 34669469

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Project description:Development of natural protein-based fibrous scaffolds with tunable physical properties and biocompatibility is highly desirable to construct three-dimensional (3D), fully cellularized scaffolds for wound healing. Herein, we demonstrated a simple and effective technique to construct electrospun 3D fibrous scaffolds for accelerated wound healing using a photocrosslinkable hydrogel based on gelatin methacryloyl (GelMA). We found that the physical properties of the photocrosslinkable hydrogel including water retention, stiffness, strength, elasticity and degradation can be tailored by changing the light exposure time. We further observed that the optimized hydrogel fibrous scaffolds which were soft and elastic could support cell adhesion, proliferation and migration into the whole scaffolds, facilitating regeneration and formation of cutaneous tissues within two weeks. Such tunable characteristics of the fibrous GelMA scaffolds distinguished them from other reported substrates developed for reconstruction of wound defects including glutaraldehyde-crosslinked gelatin or poly (lactic-co-glycolic acid) (PLGA), whose physical and chemical properties were difficult to modify to allow cell infiltration into the 3D scaffolds for tissue regeneration. We anticipate that the ability to become fully cellularized will make the engineered GelMA fibrous scaffolds suitable for widespread applications as skin substitutes or wound dressings.Statement of significanceIn present study, we generate three-dimensional photocrosslinkable gelatin (GelMA)-based fibrous scaffolds with tunable physical and biological properties by using a combined photocrosslinking/electrospinning approach. The developed GelMA fibrous scaffolds can not only support cell viability and cell adhesion, but also facilitate cell migration and proliferation, accelerating regeneration and formation of cutaneous tissues. In addition, the physical properties of the engineered fibrous GelMA hydrogel including water retention capability, mechanical properties and biodegradability can be tuned to accommodate different patients' needs, making it a promising candidate for skin tissue engineering.

Project description:Defining the final size and geometry of engineered tissues through precise control of the scalar and vector components of tissue growth is a necessary benchmark for regenerative medicine, but it has proved to be a significant challenge for tissue engineers. The growth plate cartilage that promotes elongation of the long bones is a good model system for studying morphogenetic mechanisms because cartilage is composed of a single cell type, the chondrocyte; chondrocytes are readily maintained in culture; and growth trajectory is predominately in a single vector. In this cartilage, growth is generated via a differentiation program that is spatially and temporally regulated by an interconnected network composed of long- and short-range signaling mechanisms that together result in the formation of functionally distinct cellular zones. To facilitate investigation of the mechanisms underlying anisotropic growth, we developed an in vitro model of the growth plate cartilage by using neonatal mouse growth plate chondrocytes encapsulated in alginate hydrogel beads. In bead cultures, encapsulated chondrocytes showed high viability, cartilage matrix deposition, low levels of chondrocyte hypertrophy, and a progressive increase in cell proliferation over 7 days in culture. Exogenous factors were used to test functionality of the parathyroid-related protein-Indian hedgehog (PTHrP-IHH) signaling interaction, which is a crucial feedback loop for regulation of growth. Consistent with in vivo observations, exogenous PTHrP stimulated cell proliferation and inhibited hypertrophy, whereas IHH signaling stimulated chondrocyte hypertrophy. Importantly, the treatment of alginate bead cultures with IHH or thyroxine resulted in formation of a discrete domain of hypertrophic cells that mimics tissue architecture of native growth plate cartilage. Together, these studies are the first demonstration of a tunable in vitro system to model the signaling network interactions that are required to induce zonal architecture in growth plate chondrocytes, which could also potentially be used to grow cartilage cultures of specific geometries to meet personalized patient needs.

Dataset Information

Plant cell adhesion and growth on artificial fibrous scaffolds as an in vitro model for plant development.

Publications

Plant cell adhesion and growth on artificial fibrous scaffolds as an in vitro model for plant development.

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