Coaxial nanofibrous scaffolds mimicking the extracellular matrix transition in the wound healing process promoting skin regeneration through enhancing immunomodulation

Author(s): Luyao Sun ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Jing Li ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Wendong Gao ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Miao Shi ⁶ ^, ⁷ ^, ⁵ ^, ⁸ ^, ³ , Fengling Tang ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Xiaoling Fu ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Xiaofeng Chen ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵

Publication date (Electronic): 2021

Journal: Journal of Materials Chemistry B

Publisher: Royal Society of Chemistry (RSC)

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Abstract

A degradable coaxial nanofibrous scaffold that mimics ECM transition in the wound healing process is designed to achieve better healing outcomes.

Abstract

Numerous studies have shown that scaffolds incorporated with extracellular matrix (ECM) proteins could regulate cell behaviors and improve wound healing. However, most ECM-containing scaffolds fail to capture the dynamic features of the native ECM. In this regard, nanofibrous scaffolds which mimic the composition transition of the ECM during wound healing may have great potential in promoting skin regeneration through dynamically modulating the microenvironment. Herein, we report a novel skin ECM-biomimetic coaxial nanofibrous scaffold for the repair of chronic wounds. Two essential ECM proteins, fibrinogen and collagen I, were incorporated into the shell and the core of nanofibers, respectively, to mimic the sequential appearance of fibrinogen and collagen I in the wound healing process. The regulation of the biomimetic coaxial scaffolds on adipose-derived mesenchymal stromal cells (ASCs) was compared with that of the PLGA/fibrinogen, PLGA/collagen I and PLGA uniaxial scaffolds. Our results showed that the biomimetic coaxial scaffolds remarkably promoted the immunomodulatory paracrine secretion of ASCs. By incubating macrophages with ASC conditioned medium, the enhanced immunomodulation of ASCs on the biomimetic coaxial scaffolds was confirmed by the enhanced M1-to-M2 polarization of macrophages. Furthermore, the biomimetic coaxial scaffolds effectively promoted wound repair through resolving inflammation in diabetic rats. These findings helped reveal the role of the dynamic ECM change in regulating wound healing and suggest the potential utility of the biomimetic coaxial scaffolds as a promising alternative to treat chronic wounds.

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The repair of wounds is one of the most complex biological processes that occur during human life. After an injury, multiple biological pathways immediately become activated and are synchronized to respond. In human adults, the wound repair process commonly leads to a non-functioning mass of fibrotic tissue known as a scar. By contrast, early in gestation, injured fetal tissues can be completely recreated, without fibrosis, in a process resembling regeneration. Some organisms, however, retain the ability to regenerate tissue throughout adult life. Knowledge gained from studying such organisms might help to unlock latent regenerative pathways in humans, which would change medical practice as much as the introduction of antibiotics did in the twentieth century.

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Wound healing is an evolutionarily conserved, complex, multicellular process that, in skin, aims at barrier restoration. This process involves the coordinated efforts of several cell types including keratinocytes, fibroblasts, endothelial cells, macrophages, and platelets. The migration, infiltration, proliferation, and differentiation of these cells will culminate in an inflammatory response, the formation of new tissue and ultimately wound closure. This complex process is executed and regulated by an equally complex signaling network involving numerous growth factors, cytokines and chemokines. Of particular importance is the epidermal growth factor (EGF) family, transforming growth factor beta (TGF-beta) family, fibroblast growth factor (FGF) family, vascular endothelial growth factor (VEGF), granulocyte macrophage colony stimulating factor (GM-CSF), platelet-derived growth factor (PDGF), connective tissue growth factor (CTGF), interleukin (IL) family, and tumor necrosis factor-alpha family. Currently, patients are treated by three growth factors: PDGF-BB, bFGF, and GM-CSF. Only PDGF-BB has successfully completed randomized clinical trials in the Unites States. With gene therapy now in clinical trial and the discovery of biodegradable polymers, fibrin mesh, and human collagen serving as potential delivery systems other growth factors may soon be available to patients. This review will focus on the specific roles of these growth factors and cytokines during the wound healing process.

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