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Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks

Doris Zauchner Orcid Logo, Monica Zippora Müller, Marion Horrer Orcid Logo, Leana Bissig Orcid Logo, Feihu Zhao Orcid Logo, Philipp Fisch Orcid Logo, Sung Sik Lee Orcid Logo, Marcy Zenobi-Wong Orcid Logo, Ralph Müller Orcid Logo, Xiao-Hua Qin Orcid Logo

Nature Communications, Volume: 15, Issue: 1

Swansea University Author: Feihu Zhao Orcid Logo

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DOI (Published version): 10.1038/s41467-024-49280-3

Abstract

Generating 3D bone cell networks in vitro that mimic the dynamic process during early bone formation remains challenging. Here, we report a synthetic biodegradable microporous hydrogel for efficient formation of 3D networks from human primary cells, analysis of cell-secreted extracellular matrix (EC...

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Published in: Nature Communications
ISSN: 2041-1723
Published: Springer Science and Business Media LLC 2024
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URI: https://cronfa.swan.ac.uk/Record/cronfa68087
first_indexed 2024-10-29T09:21:59Z
last_indexed 2025-01-09T20:32:36Z
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spelling 2024-12-12T15:12:41.1216259 v2 68087 2024-10-29 Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks 1c6e79b6edd08c88a8d17a241cd78630 0000-0003-0515-6808 Feihu Zhao Feihu Zhao true false 2024-10-29 EAAS Generating 3D bone cell networks in vitro that mimic the dynamic process during early bone formation remains challenging. Here, we report a synthetic biodegradable microporous hydrogel for efficient formation of 3D networks from human primary cells, analysis of cell-secreted extracellular matrix (ECM) and microfluidic integration. Using polymerization-induced phase separation, we demonstrate dynamic in situ formation of microporosity (5–20 µm) within matrix metalloproteinase-degradable polyethylene glycol hydrogels in the presence of living cells. Pore formation is triggered by thiol-Michael-addition crosslinking of a viscous precursor solution supplemented with hyaluronic acid and dextran. The resulting microporous architecture can be fine-tuned by adjusting the concentration and molecular weight of dextran. After encapsulation in microporous hydrogels, human mesenchymal stromal cells and osteoblasts spread rapidly and form 3D networks within 24 hours. We demonstrate that matrix degradability controls cell-matrix remodeling, osteogenic differentiation, and deposition of ECM proteins such as collagen. Finally, we report microfluidic integration and proof-of-concept osteogenic differentiation of 3D cell networks under perfusion on chip. Altogether, this work introduces a synthetic microporous hydrogel to efficiently differentiate 3D human bone cell networks, facilitating future in vitro studies on early bone development. Journal Article Nature Communications 15 1 Springer Science and Business Media LLC 2041-1723 13 6 2024 2024-06-13 10.1038/s41467-024-49280-3 COLLEGE NANME Engineering and Applied Sciences School COLLEGE CODE EAAS Swansea University Another institution paid the OA fee The authors thank Sophie Zengerle, Isabel Hui, Wanwan Qiu, Christian Gehre, Margherita Bernero, Dr. Bregje de Wildt, and Dr. Yinyin Bao for experimental support; Dr. Cecilia Giunta and Prof. Dr. Marianne Rohrbach at the University Children’s Hospital Zurich for providing with some of the primary human osteoblasts; and Dr. Tobias Schwarz in the Scientific Center for Optical and Electron Microscopy (ScopeM) of ETH Zurich for technical support. This project was supported by the Swiss National Science Foundation (no. 190345, 206501, 188522, X.H.Q.) and the Swiss State Secretariat for Education, Research and Innovation (no. MB23.00008, X.H.Q.). 2024-12-12T15:12:41.1216259 2024-10-29T09:18:56.0801038 Faculty of Science and Engineering School of Engineering and Applied Sciences - Biomedical Engineering Doris Zauchner 0000-0001-7770-9497 1 Monica Zippora Müller 2 Marion Horrer 0000-0001-6565-971x 3 Leana Bissig 0009-0005-0356-8720 4 Feihu Zhao 0000-0003-0515-6808 5 Philipp Fisch 0000-0003-4384-6682 6 Sung Sik Lee 0000-0001-9267-232x 7 Marcy Zenobi-Wong 0000-0002-8522-9909 8 Ralph Müller 0000-0002-5811-7725 9 Xiao-Hua Qin 0000-0001-8355-3230 10
title Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks
spellingShingle Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks
Feihu Zhao
title_short Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks
title_full Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks
title_fullStr Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks
title_full_unstemmed Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks
title_sort Synthetic biodegradable microporous hydrogels for in vitro 3D culture of functional human bone cell networks
author_id_str_mv 1c6e79b6edd08c88a8d17a241cd78630
author_id_fullname_str_mv 1c6e79b6edd08c88a8d17a241cd78630_***_Feihu Zhao
author Feihu Zhao
author2 Doris Zauchner
Monica Zippora Müller
Marion Horrer
Leana Bissig
Feihu Zhao
Philipp Fisch
Sung Sik Lee
Marcy Zenobi-Wong
Ralph Müller
Xiao-Hua Qin
format Journal article
container_title Nature Communications
container_volume 15
container_issue 1
publishDate 2024
institution Swansea University
issn 2041-1723
doi_str_mv 10.1038/s41467-024-49280-3
publisher Springer Science and Business Media LLC
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Engineering and Applied Sciences - Biomedical Engineering{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Engineering and Applied Sciences - Biomedical Engineering
document_store_str 0
active_str 0
description Generating 3D bone cell networks in vitro that mimic the dynamic process during early bone formation remains challenging. Here, we report a synthetic biodegradable microporous hydrogel for efficient formation of 3D networks from human primary cells, analysis of cell-secreted extracellular matrix (ECM) and microfluidic integration. Using polymerization-induced phase separation, we demonstrate dynamic in situ formation of microporosity (5–20 µm) within matrix metalloproteinase-degradable polyethylene glycol hydrogels in the presence of living cells. Pore formation is triggered by thiol-Michael-addition crosslinking of a viscous precursor solution supplemented with hyaluronic acid and dextran. The resulting microporous architecture can be fine-tuned by adjusting the concentration and molecular weight of dextran. After encapsulation in microporous hydrogels, human mesenchymal stromal cells and osteoblasts spread rapidly and form 3D networks within 24 hours. We demonstrate that matrix degradability controls cell-matrix remodeling, osteogenic differentiation, and deposition of ECM proteins such as collagen. Finally, we report microfluidic integration and proof-of-concept osteogenic differentiation of 3D cell networks under perfusion on chip. Altogether, this work introduces a synthetic microporous hydrogel to efficiently differentiate 3D human bone cell networks, facilitating future in vitro studies on early bone development.
published_date 2024-06-13T05:40:22Z
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