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Nano Research 2023, 16(1): 792-809 https://doi.org/10.1007/s12274-022-4670-2
Research Article | Issue | Published: 10 August 2022

Soft nanofiber modified micropatterned substrates enhance native-like endothelium maturation via CXCR4/calcium-mediated actin cytoskeleton assembly

Show Author's Information Bingcheng Yi1,2,  Boya Zhou2,  Wufei Dai2,  Xinwu Lu1,  Wei Liu2( )
Department of Vascular Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China
Department of Plastic and Reconstructive Surgery, Shanghai Key Laboratory of Tissue Engineering, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China
Keywords:
nanofibers, small-diameter vascular grafts, parallel microgrooves, cell–matrix interaction, endothelial regeneration
Topics:
Biomaterials Surface structureTissue engineering
Cite this article:
Yi B, Zhou B, Dai W, et al. Soft nanofiber modified micropatterned substrates enhance native-like endothelium maturation via CXCR4/calcium-mediated actin cytoskeleton assembly. Nano Research, 2023, 16(1): 792-809. https://doi.org/10.1007/s12274-022-4670-2
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Abstract Full text Electronic supplementary material About this article

Regeneration and maturation of native-like endothelium is crucial for material-guided small-diameter vascular regeneration. Although parallel-microgroove-patterned (micropatterned) substrates are capable of promoting endothelial regeneration with native-like endothelial cell (EC) alignment, their unbefitting high-stiffness acutely inhibits cell–matrix interaction and endothelial maturation. Given that the sufficient softness of nanofibers allows cells to deform the local matrix architecture to satisfy cell survival and functional requirements, in this study, an effective strategy of decorating micropatterned substrate with soft nanofibers was exploited to enhance cell–matrix interaction for engineering healthy endothelium. Results demonstrated that the micropatterned nanofibrous membranes were successfully obtained with high-resolution parallel microgrooves (groove width: ~ 15 µm; groove depth: ~ 5 µm) and adequate softness (bulk modulus: 2.27 ± 0.18 MPa). This particular substrate markedly accelerated the formation and maturation of confluent native-like endothelium by synchronously increasing cell–cell and cell–matrix interactions. Transcriptome analysis revealed that compared with smooth features, the microgrooved pattern was likely to promote endothelial remodeling via integrin α5-mediated microtubule disassembly and type I interleukin 1 receptor-mediated signaling pathways, whereas the nanofibrous pattern was likely to guide endothelial regeneration via integrin α5β8-guided actin cytoskeleton remodeling. Nevertheless, endowing micropatterned substrate with soft nanofibers was demonstrated to accelerate endothelial maturation via chemokine (C-X-C motif) receptor 4/calcium-mediated actin cytoskeleton assembly. Furthermore, numerical simulation results of hemodynamics indicated the positive impact of the micropatterned nanofibers on maintaining stable hemodynamics. Summarily, our current work supports an affirmation that the micropatterned nanofibrous substrates can significantly promote regeneration and maturation of native-like endothelium, which provides an innovative method for constructing vascular grafts with functional endothelium.


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Electronic supplementary material
About this article

Soft nanofiber modified micropatterned substrates enhance native-like endothelium maturation via CXCR4/calcium-mediated actin cytoskeleton assembly

Show Author's information Bingcheng Yi1,2, Boya Zhou2, Wufei Dai2, Xinwu Lu1, Wei Liu2( )
Department of Vascular Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China
Department of Plastic and Reconstructive Surgery, Shanghai Key Laboratory of Tissue Engineering, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China

Abstract

Regeneration and maturation of native-like endothelium is crucial for material-guided small-diameter vascular regeneration. Although parallel-microgroove-patterned (micropatterned) substrates are capable of promoting endothelial regeneration with native-like endothelial cell (EC) alignment, their unbefitting high-stiffness acutely inhibits cell–matrix interaction and endothelial maturation. Given that the sufficient softness of nanofibers allows cells to deform the local matrix architecture to satisfy cell survival and functional requirements, in this study, an effective strategy of decorating micropatterned substrate with soft nanofibers was exploited to enhance cell–matrix interaction for engineering healthy endothelium. Results demonstrated that the micropatterned nanofibrous membranes were successfully obtained with high-resolution parallel microgrooves (groove width: ~ 15 µm; groove depth: ~ 5 µm) and adequate softness (bulk modulus: 2.27 ± 0.18 MPa). This particular substrate markedly accelerated the formation and maturation of confluent native-like endothelium by synchronously increasing cell–cell and cell–matrix interactions. Transcriptome analysis revealed that compared with smooth features, the microgrooved pattern was likely to promote endothelial remodeling via integrin α5-mediated microtubule disassembly and type I interleukin 1 receptor-mediated signaling pathways, whereas the nanofibrous pattern was likely to guide endothelial regeneration via integrin α5β8-guided actin cytoskeleton remodeling. Nevertheless, endowing micropatterned substrate with soft nanofibers was demonstrated to accelerate endothelial maturation via chemokine (C-X-C motif) receptor 4/calcium-mediated actin cytoskeleton assembly. Furthermore, numerical simulation results of hemodynamics indicated the positive impact of the micropatterned nanofibers on maintaining stable hemodynamics. Summarily, our current work supports an affirmation that the micropatterned nanofibrous substrates can significantly promote regeneration and maturation of native-like endothelium, which provides an innovative method for constructing vascular grafts with functional endothelium.

Keywords: nanofibers, small-diameter vascular grafts, parallel microgrooves, cell–matrix interaction, endothelial regeneration

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Acknowledgements

Publication history

Received: 28 April 2022
Revised: 11 June 2022
Accepted: 16 June 2022
Published: 10 August 2022
Issue date: January 2023

Copyright

© Tsinghua University Press 2022

Acknowledgements

Acknowledgements

This work was supported by National Key Research and Development Program of China (No. 2018YFC1105800), China Postdoctoral Science Foundation (No. 2020M681322), and National Natural Science Foundation of China (No. 31870967). We are also grateful to Shiyanjia Lab (www.shiyanjia.com) for his kind help in performing the numerical simulations.

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