Boosting cartilage repair with silk fibroin-DNA hydrogel-based cartilage organoid precursor

Author(s): Congyi Shen ^a ^, ^b ^, ^c ^, ^d ^, ^e ^, ¹ , Jian Wang ^a ^, ^b ^, ^c ^, ^e ^, ^f ^, ¹ , Guangfeng Li ^a ^, ^b ^, ^c ^, ^e ^, ^g ^, ¹ , Shuyue Hao ^a ^, ^b ^, ^c ^, ^d ^, ^e ^, ¹ , Yan Wu ^a ^, ^b ^, ^e , Peiran Song ^a ^, ^b ^, ^e , Yafei Han ^a ^, ^b ^, ^c ^, ^e , Mengmeng Li ^a ^, ^b ^, ^e , Guangchao Wang ^f , Ke Xu ^a ^, ^b ^, ^e , Hao Zhang ^a ^, ^b ^, ^e , Xiaoxiang Ren ^a ^, ^b ^, ^e , Yingying Jing ^a ^, ^b ^, ^e ^, ^∗∗ , Ru Yang ^h ^, ^∗∗∗ , Zhen Geng ^a ^, ^b ^, ^e ^, ^∗∗∗∗ , Jiacan Su ^a ^, ^b ^, ^e ^, ^f ^, ^∗

Publication date (Electronic): 16 February 2024

Journal: Bioactive Materials

Publisher: KeAi Publishing

Keywords: Silk fibroin-DNA hydrogel, Microsphere, Chondrogenesis, Cartilage organoid, Cartilage repair

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Abstract

Osteoarthritis (OA), a common degenerative disease, is characterized by high disability and imposes substantial economic impacts on individuals and society. Current clinical treatments remain inadequate for effectively managing OA. Organoids, miniature 3D tissue structures from directed differentiation of stem or progenitor cells, mimic native organ structures and functions. They are useful for drug testing and serve as active grafts for organ repair. However, organoid construction requires extracellular matrix-like 3D scaffolds for cellular growth. Hydrogel microspheres, with tunable physical and chemical properties, show promise in cartilage tissue engineering by replicating the natural microenvironment. Building on prior work on SF-DNA dual-network hydrogels for cartilage regeneration, we developed a novel RGD-SF-DNA hydrogel microsphere (RSD-MS) via a microfluidic system by integrating photopolymerization with self-assembly techniques and then modified with Pep-RGDfKA. The RSD-MSs exhibited uniform size, porous surface, and optimal swelling and degradation properties. In vitro studies demonstrated that RSD-MSs enhanced bone marrow mesenchymal stem cells (BMSCs) proliferation, adhesion, and chondrogenic differentiation. Transcriptomic analysis showed RSD-MSs induced chondrogenesis mainly through integrin-mediated adhesion pathways and glycosaminoglycan biosynthesis. Moreover, in vivo studies showed that seeding BMSCs onto RSD-MSs to create cartilage organoid precursors (COPs) significantly enhanced cartilage regeneration. In conclusion, RSD-MS was an ideal candidate for the construction and long-term cultivation of cartilage organoids, offering an innovative strategy and material choice for cartilage regeneration and tissue engineering.

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Highlights

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RGD-SF-DNA hydrogel microspheres (RSD-MSs) were prepared through photopolymerization and self-assembly.
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RSD-MSs up-regulated integrin-mediated cell adhesion and focal adhesion pathways.
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Cartilage organoid precursors significantly enhanced cartilage regeneration.
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RSD-MS emerged as an ideal candidate for the construction of cartilage organoids.

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Most cited references 55

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Organogenesis in a dish: modeling development and disease using organoid technologies.

M. Lancaster, J Knoblich (2014)

Classical experiments performed half a century ago demonstrated the immense self-organizing capacity of vertebrate cells. Even after complete dissociation, cells can reaggregate and reconstruct the original architecture of an organ. More recently, this outstanding feature was used to rebuild organ parts or even complete organs from tissue or embryonic stem cells. Such stem cell-derived three-dimensional cultures are called organoids. Because organoids can be grown from human stem cells and from patient-derived induced pluripotent stem cells, they have the potential to model human development and disease. Furthermore, they have potential for drug testing and even future organ replacement strategies. Here, we summarize this rapidly evolving field and outline the potential of organoid technology for future biomedical research.

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Emily Callander, David Hunter, Deborah Schofield (2014)

Osteoarthritis (OA) is a highly prevalent, disabling disease, with a commensurate tremendous individual and socioeconomic burden. This Perspectives article focuses on the burden of OA for the individual, the health-care system and society, to draw attention to the magnitude of the current problem with some reference to projected figures. We have an urgent opportunity to make fundamental changes to the way we care for individuals with OA that will have an effect upon the direct and indirect costs of this disease. By focusing on the burden of this prevalent, disabling, and costly disease, we hope to highlight the opportunity for shifts in health-care policy towards prevention and chronic-disease management.

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Engineering organoids

Moritz Hofer, Matthias Lutolf (2021)

Organoids are in vitro miniaturized and simplified model systems of organs that have gained enormous interest for modelling tissue development and disease, and for personalized medicine, drug screening and cell therapy. Despite considerable success in culturing physiologically relevant organoids, challenges remain to achieve real-life applications. In particular, the high variability of self-organizing growth and restricted experimental and analytical access hamper the translatability of organoid systems. In this Review, we argue that many limitations of traditional organoid culture can be addressed by engineering approaches at all levels of organoid systems. We investigate cell surface and genetic engineering approaches, and discuss stem cell niche engineering based on the design of matrices that allow spatiotemporal control of organoid growth and shape-guided morphogenesis. We examine how microfluidic approaches and lessons learnt from organs-on-a-chip enable the integration of mechano-physiological parameters and increase accessibility of organoids to improve functional readouts. Applying engineering principles to organoids increases reproducibility and provides experimental control, which will, ultimately, be required to enable clinical translation.

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Author and article information

Contributors

Yingying Jing

Ru Yang

Zhen Geng

Jiacan Su

Journal

Journal ID (nlm-ta): Bioact Mater

Journal ID (iso-abbrev): Bioact Mater

Title: Bioactive Materials

Publisher: KeAi Publishing

ISSN (Electronic): 2452-199X

Publication date PMC-release: 16 February 2024

Publication date Collection: May 2024

Publication date (Electronic): 16 February 2024

Volume: 35

Pages: 429-444

Affiliations

[a ]Institute of Translational Medicine, Shanghai University, Shanghai, 200444, China

[b ]Organoid Research Center, Shanghai University, Shanghai, 200444, China

[c ]School of Medicine, Shanghai University, Shanghai, 200444, China

[d ]School of Life Sciences, Shanghai University, Shanghai, 200444, China

[e ]National Center for Translational Medicine (Shanghai) SHU Branch, Shanghai University, Shanghai, 200444, China

[f ]Department of Orthopedics, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200092, China

[g ]Department of Orthopedics, Shanghai Zhongye Hospital, Shanghai, 200941, China

[h ]Second Affiliated Hospital of Soochow University, Departments of Rheumatology and Immunology, Soochow, 215000, China

Author notes

[∗ ]Corresponding authors. Institute of Translational Medicine, Shanghai University, Shanghai, 200444, China. drsujiacan@ 123456163.com

[∗∗ ]Corresponding author. Institute of Translational Medicine, Shanghai University, Shanghai, 200444, China. jingy4172@ 123456shu.edu.cn

[∗∗∗ ]Corresponding author. Second Affiliated Hospital of Soochow University, Departments of Rheumatology and Immunology, Soochow, 215000, China. yangru923@ 123456126.com

[∗∗∗∗ ]Corresponding author. Institute of Translational Medicine, Shanghai University, Shanghai, 200444, China. nanboshan1987@ 123456163.com

[1]

These authors contributed equally to this study.

Article

Publisher Item ID: S2452-199X(24)00061-6

DOI: 10.1016/j.bioactmat.2024.02.016

PMC ID: 10881360

PubMed ID: 38390528

SO-VID: a232da8f-660b-45cf-8849-bfcc31c7849a

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

History

Date received : 2 January 2024

Date revision received : 12 February 2024

Date accepted : 14 February 2024

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Boosting cartilage repair with silk fibroin-DNA hydrogel-based cartilage organoid precursor

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Abstract

Graphical abstract

Highlights

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Recursive Rule based Visual Categorization

Most cited references 55

Organogenesis in a dish: modeling development and disease using organoid technologies.

The individual and socioeconomic impact of osteoarthritis.

Engineering organoids

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Journal

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Cited by 4

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