Biomaterials Translational ›› 2024, Vol. 5 ›› Issue (3): 257-273.doi: 10.12336/biomatertransl.2024.03.004
• REVIEW • Previous Articles Next Articles
Congyang Xue1,2,#, Liping Chen1,3,#, Nan Wang1, Heng Chen1, Wenqiang Xu1,3, Zhipeng Xi1,3, Qing Sun4, Ran Kang1,3,*(
), Lin Xie1,3,*(), Xin Liu1,2,3,*()
Received:2024-06-14
Revised:2024-07-22
Accepted:2024-08-30
Online:2024-09-28
Published:2024-09-28
Contact:
Xin Liu, liuxin@njucm.edu.cn; Lin Xie, xielin@njucm.edu.cn; Ran Kang, kangran126@126.com.
About author:#Author equally.
Xue, C.; Chen, L.; Wang, N.; Chen, H.; Xu, W.; Xi, Z.; Sun, Q.; Kang, R.; Xie, L.; Liu, X. Stimuli-responsive hydrogels for bone tissue engineering. Biomater Transl. 2024, 5(3), 257-273.
Figure 1. Sources and classification of hydrogel materials. Created with Microsoft PowerPoint 2016.
| Source of hydrogel | Response factor | Application |
|---|---|---|
| Chitosan | Temperature | The hydrogel encapsulates adipose-derived stromal cells and maintains their viability, promoting their cartilage formation for the repair of articular cartilage injuries. |
| pH | Excellent antibacterial, antioxidant, low cytotoxicity and angiogenic activity. Destroys bacteria, reduces inflammation and promotes angiogenesis to facilitate regeneration and healing of infected wound tissues. | |
| Hyaluronic acid | Light | Provides a supportive environment to support cartilage differentiation and also adapts to the irregular shape of cartilage lesions. |
| Sodium alginate | Temperature | Slow degradation enables use for long-term release of therapeutic DNA nanoparticles. |
| Promoting bone regeneration in a rat cranial defect model, demonstrating the promising application of this hydrogel in unloaded bone regeneration. | ||
| Dextran | pH | The hydrogel was able to well encapsulate adriamycin hydrochloride and exhibited a good slow release, while its release showed better behaviour at pH = 4.5 than at neutral pH. The hydrogel can be used as a drug delivery vehicle for the treatment of bone cancer and the promotion of bone repair. |
| Gelatine | Temperature | Encapsulation of adipose stem cells maintains their viability while continuous release of adipose stem cells due to degradation of gelatine to promote angiogenesis. |
| Its hydrophilic properties useful for growth, cell embedding and extracellular matrix secretion can be used as an ideal strategy to promote cartilage tissue formation. | ||
| Silk fibronectin | Multiple factors (e.g. pH, temperature and light) | Hydrogel shows excellent stimuli responsive drug release ability and may be used in bone tissue engineering in the future. |
| Temperature | It has some osteogenic capacity and can be used for bone repair and in regeneration. |
Table 1. The use of stimuli-responsive hydrogel-derived from natural materials for bone tissue engineering
| Source of hydrogel | Response factor | Application |
|---|---|---|
| Chitosan | Temperature | The hydrogel encapsulates adipose-derived stromal cells and maintains their viability, promoting their cartilage formation for the repair of articular cartilage injuries. |
| pH | Excellent antibacterial, antioxidant, low cytotoxicity and angiogenic activity. Destroys bacteria, reduces inflammation and promotes angiogenesis to facilitate regeneration and healing of infected wound tissues. | |
| Hyaluronic acid | Light | Provides a supportive environment to support cartilage differentiation and also adapts to the irregular shape of cartilage lesions. |
| Sodium alginate | Temperature | Slow degradation enables use for long-term release of therapeutic DNA nanoparticles. |
| Promoting bone regeneration in a rat cranial defect model, demonstrating the promising application of this hydrogel in unloaded bone regeneration. | ||
| Dextran | pH | The hydrogel was able to well encapsulate adriamycin hydrochloride and exhibited a good slow release, while its release showed better behaviour at pH = 4.5 than at neutral pH. The hydrogel can be used as a drug delivery vehicle for the treatment of bone cancer and the promotion of bone repair. |
| Gelatine | Temperature | Encapsulation of adipose stem cells maintains their viability while continuous release of adipose stem cells due to degradation of gelatine to promote angiogenesis. |
| Its hydrophilic properties useful for growth, cell embedding and extracellular matrix secretion can be used as an ideal strategy to promote cartilage tissue formation. | ||
| Silk fibronectin | Multiple factors (e.g. pH, temperature and light) | Hydrogel shows excellent stimuli responsive drug release ability and may be used in bone tissue engineering in the future. |
| Temperature | It has some osteogenic capacity and can be used for bone repair and in regeneration. |
| Source of hydrogel | Response factor | Application |
|---|---|---|
| Poly(ethylene glycol) | Temperature | It has excellent in vitro osteogenic properties and has a positive effect on bone repair. It also significantly improves the injectability, washout resistance and in vitro degradability of the bone cement. |
| pH | The ability to adapt to bone defects in an acidic environment caused by trauma, thus promoting bone repair and regeneration. | |
| Poly(vinyl alcohol) | Activated oxygen levels | Releases diclofenac sodium encapsulated in a hydrogel to reduce oxidative stress, reduce post-traumatic inflammation, and promote cartilage regeneration. |
| Poly(γ-glutamic acid) | pH | Due to the pH sensitivity, flexible, highly absorbent and smoother hydrogels are produced to serve as useful bone substitutes for repairing bone defects. |
Table 2. The use of stimuli-responsive hydrogel-derived from synthetic materials for bone tissue engineering
| Source of hydrogel | Response factor | Application |
|---|---|---|
| Poly(ethylene glycol) | Temperature | It has excellent in vitro osteogenic properties and has a positive effect on bone repair. It also significantly improves the injectability, washout resistance and in vitro degradability of the bone cement. |
| pH | The ability to adapt to bone defects in an acidic environment caused by trauma, thus promoting bone repair and regeneration. | |
| Poly(vinyl alcohol) | Activated oxygen levels | Releases diclofenac sodium encapsulated in a hydrogel to reduce oxidative stress, reduce post-traumatic inflammation, and promote cartilage regeneration. |
| Poly(γ-glutamic acid) | pH | Due to the pH sensitivity, flexible, highly absorbent and smoother hydrogels are produced to serve as useful bone substitutes for repairing bone defects. |
| Study | Year | Source of hydrogel | Classification | Stem cells | Application model | Mechanisms |
|---|---|---|---|---|---|---|
| Bi et al. | 2023 | Living active glass/gellan hydrogel | Temperature-sensitive hydrogels | Bone marrow mesenchymal stem cell | Porcine cartilage defect model | Promote the proliferation of bone marrow mesenchymal stem cells |
| Filippi et al. | 2019 | Poly(ethylene glycol)/magnetic nanoparticles | Magneto-responsive hydrogels | Adipose-derived stromal vascular fraction cells | Mice | Alkaline phosphatase activity, expression of osteogenic markers (Runx2, and collagen I) and deposition of mineralised matrix were enhanced. It has the potential to promote osteogenesis and angiogenesis. |
| Islam et al. | 2023 | Gelatine | Magnetic-responsive | Adipose-derived mesenchymal stem cells | No | Magnetic fields can control the differentiation of adipose stem cells into different lineages and promote their differentiation into adipose or osteoblasts |
| Wang et al. | 2024 | Hyaluronic acid and poly(ethylene glycol) | Environmental stimulus response | Bone marrow mesenchymal stem cells | Rat femoral condylar defect model | Effectively reduces inflammation, accelerates haemoreduction and promotes tissue mineralisation. |
Table 3. Hydrogel loaded with stem cells for bone tissue engineering
| Study | Year | Source of hydrogel | Classification | Stem cells | Application model | Mechanisms |
|---|---|---|---|---|---|---|
| Bi et al. | 2023 | Living active glass/gellan hydrogel | Temperature-sensitive hydrogels | Bone marrow mesenchymal stem cell | Porcine cartilage defect model | Promote the proliferation of bone marrow mesenchymal stem cells |
| Filippi et al. | 2019 | Poly(ethylene glycol)/magnetic nanoparticles | Magneto-responsive hydrogels | Adipose-derived stromal vascular fraction cells | Mice | Alkaline phosphatase activity, expression of osteogenic markers (Runx2, and collagen I) and deposition of mineralised matrix were enhanced. It has the potential to promote osteogenesis and angiogenesis. |
| Islam et al. | 2023 | Gelatine | Magnetic-responsive | Adipose-derived mesenchymal stem cells | No | Magnetic fields can control the differentiation of adipose stem cells into different lineages and promote their differentiation into adipose or osteoblasts |
| Wang et al. | 2024 | Hyaluronic acid and poly(ethylene glycol) | Environmental stimulus response | Bone marrow mesenchymal stem cells | Rat femoral condylar defect model | Effectively reduces inflammation, accelerates haemoreduction and promotes tissue mineralisation. |
| Study | Year | Source of hydrogel | Classification | Bioactive factors or drugs | Application model | Mechanisms |
|---|---|---|---|---|---|---|
| Madani et al. | 2020 | Alginate iron hydrogel | Magneto-responsive hydrogels | Bone morphogenetic protein 2 | No | Promote the aggregation of osteoprogenitor cells to the defect site, proliferation, and differentiation into osteoblasts |
| Yao et al. | 2021 | Gelatine methacryloyl -oxidised sodium alginate hydrogel | pH-sensitive hydrogels | Gentamycin sulfate and phenamil | Mouse calvarial defect model | Promote the repair of large bone defects by enhancing antibacterial activity |
| Chauhan et al. | 2021 | Amylopectin - poly(ethylene glycol) hydrogel | pH-sensitive hydrogels | Dexamethasone | Mouse osteoblasts | Enhance cell viability and proliferation, and induce osteoblast differentiation. |
| Liu et al. | 2022 | Photocrosslinked chitosan hydrogel | Glucose-sensitive hydrogels | Tannic acid | No | Inhibit the production of NO, IL-6, and TNF-α in stimulated macrophages and exhibits potent antibacterial and anti-inflammatory activities. |
| Feng et al. | 2024 | Sodium alginate/chitosan | Glucose-sensitive hydrogels | Epigallocatechin-3-gallate | No | Good antioxidant and anti-inflammatory properties; modulatory effect on macrophage phenotype, providing a favourable immune microenvironment. |
Table 4. Hydrogel loaded with bioactive factors or drugs for bone tissue engineering
| Study | Year | Source of hydrogel | Classification | Bioactive factors or drugs | Application model | Mechanisms |
|---|---|---|---|---|---|---|
| Madani et al. | 2020 | Alginate iron hydrogel | Magneto-responsive hydrogels | Bone morphogenetic protein 2 | No | Promote the aggregation of osteoprogenitor cells to the defect site, proliferation, and differentiation into osteoblasts |
| Yao et al. | 2021 | Gelatine methacryloyl -oxidised sodium alginate hydrogel | pH-sensitive hydrogels | Gentamycin sulfate and phenamil | Mouse calvarial defect model | Promote the repair of large bone defects by enhancing antibacterial activity |
| Chauhan et al. | 2021 | Amylopectin - poly(ethylene glycol) hydrogel | pH-sensitive hydrogels | Dexamethasone | Mouse osteoblasts | Enhance cell viability and proliferation, and induce osteoblast differentiation. |
| Liu et al. | 2022 | Photocrosslinked chitosan hydrogel | Glucose-sensitive hydrogels | Tannic acid | No | Inhibit the production of NO, IL-6, and TNF-α in stimulated macrophages and exhibits potent antibacterial and anti-inflammatory activities. |
| Feng et al. | 2024 | Sodium alginate/chitosan | Glucose-sensitive hydrogels | Epigallocatechin-3-gallate | No | Good antioxidant and anti-inflammatory properties; modulatory effect on macrophage phenotype, providing a favourable immune microenvironment. |
Figure 2. Schematic representation of magneto-responsive hydrogel preparation and cross-linking chemistry. Magnetic manipulation of low concentrations of cellulose nanocrystals decorated with magnetic nanoparticles in enzyme cross-linked gelatine-based hydrogels can be achieved by applying a low intensity magnetic field. Reprinted with permission from Araújo-Custódio et al.85 Copyright 2019, American Chemical Society. N: north; S: south.
Figure 3. Temperature-sensitive hydrogel for bone tissue engineering cases. (A) Simvastatin was loaded into a 3DTi using a thermosensitive PLGA-PEG-PLGA hydrogel. Reprinted from Jing et al.89 (B) Bifunctional thermosensitive hydrogel for reducing infection and promoting bone regeneration in infected bone defects. Reprinted from Tian et al.30 BMP-2: bone morphogenetic protein 2; CS: chitosan; NOX2: reduced nicotinamide adenine dinucleotide phosphate oxidase 2; PEG: poly(ethylene glycol); PLGA: poly(lactic-co-glycolic) acid; QCS: quaternised chitosan; TF: transferrin.
Figure 4. Preparation and application of photosensitive hydrogels. (A) Absorption wavelength distribution of different photosensitizers. (B) Structural formulae of representative photosensitizers. A and B were reprinted from Zhu et al.91 Copyright WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim. (C) Schematic for the preparation of customizable BTHs and their application in bionic tissue engineering. Reprinted from Wei et al.92 Copyright 2022 American Chemical Society. AAm: acrylamide; BTH: biomineralised tough hydrogels; CaP: calcium phosphate; I2959: 2‐hydroxy‐1‐[4‐(hydroxy ethoxy)phenyl]‐2‐methyl‐1‐propanone; MBA: methylene diacrylamide; Nd: neodymium; P2CK: sodium 3,3′-((((1E,1′E)-(2-oxocyclopentane-1,3-diylidene)-bis(methaneylylidene))-bis(4,1-phenylene))-bis(methylazanediyl))-dipropionate; PAAm: polyacrylamide; PPD: phosphonodiol; UCNP: upconversion nanoparticles; Yb: ytterbium.
Figure 5. Preparation and application of pH-sensitive hydrogels and ion-sensitive hydrogels. (A) Mechanism of pH-sensitive GelMA OSA hydrogel for dual release of GS and benzylamine (Phe) to enhance antimicrobial activity and promote repair of large bone defects figure. Reprinted from Yao et al.74 Copyright 2021 Published by Elsevier Inc. (B) Preparation of biomineralised surface hydrogels based on the binding of chondroitin sulphate to charged ions such as calcium and phosphate for bone tissue engineering figure. Reprinted from Kim et al.99 Copyright 2017 American Chemical Society. E. coli: Escherichia coli; GelMA: gelatine methacryloyl; GS: gentamicin sulfate; hTMSCs: human mesenchymal stem cells; MeCS: methacrylated chondroitin sulfate; MSN: mesoporous silica nanoparticles; OSA: oxidised sodium alginate; PEGDA: poly(ethylene glycol) diacrylate; S. aureus: Staphylococcus aureus; UV: ultraviolet.
Figure 6. Glucose-sensitive hydrogels and enzyme-sensitive hydrogels. (A) The mechanism of chitosan-PEO hydrogel’s glucose sensitivity and controlled drug release process. Reprinted from Xiao et al.100 Copyright 2015 Elsevier Ltd. (B) Schematic diagram showing the fabrication procedures of a MMP‐responsive phosphatidylserine (PS)‐encapsulated injectable hydrogel (PEG‐pp‐PS) for rat calvaria bone defect regeneration. Reprinted from Zhang et al.104 Arg-1: arginase-1; BMP2: bone morphogenetic protein 2; IL-1β: interleukin-1β; iNOS: inducible nitric oxide synthase; MMP: matrix‐metalloproteinase; MSCs: mesenchymal stem cells; PEO: polyethylene oxide; pp: peptide; RUNX2: Runt-related transcription factor 2; SG: succinimidyl glutarate.
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