Publications by authors named "Changyou Gao"

315 Publications

3D printing of a tough double-network hydrogel and its use as a scaffold to construct a tissue-like hydrogel composite.

J Mater Chem B 2022 Jan 4. Epub 2022 Jan 4.

Ministry of Education Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China.

To mimic biological tissues with high toughness such as cartilage, it is highly desired to fabricate stable and tough hydrogels with intricate shapes to act as a structural support. Extrusion-based 3D printing is a promising method to fabricate 3D scaffolds with various architectures; however, printing tough hydrogel structures with high fidelity and resolution is still a challenge. In this work, we adopt the fast sol-to-gel transition of κ-carrageenan in the solution of acrylamide upon cooling to fix the printed scaffolds and polymerize the precursor solution to form the second network. The printed constructs of κ-carrageenan/polyacrylamide double-network gels are toughened by soaking in an aqueous solution of zirconyl chloride to form coordination complexes between the Zr ions and sulfate groups of κ-carrageenan. The obtained hydrogels are stable in water and possess good mechanical properties, with a tensile breaking stress of 1-2 MPa, breaking strain of 100-150%, and Young's modulus of 4-10 MPa. The printed grid can hold 150 times its own weight. 3D printed constructs with a high aspect ratio and shape fidelity are obtained by optimizing the printing parameters. Furthermore, a biomimetic strategy is applied to construct a hydrogel composite by filling the printed tough hydrogel scaffold with a cell-laden fibrin hydrogel as the soft substance. Chondrocytes in the hydrogel composite maintain high viability after cyclic compression, demonstrating the load-bearing capacity of the tough scaffold and favorable microenvironment for cells provided by the embedded soft fibrin gel. We envision that this printing strategy for hydrogel constructs with high toughness and good stability, as well as the method to form tough-soft hydrogel composites, can be extended to other systems to develop structural elements and scaffolds towards applications in biomedical devices and tissue engineering.
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http://dx.doi.org/10.1039/d1tb02465eDOI Listing
January 2022

Macrophage membrane-functionalized nanofibrous mats and their immunomodulatory effects on macrophage polarization.

Acta Biomater 2021 Dec 25. Epub 2021 Dec 25.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China; Dr. Li Dak Sum & Yip Yio Chin Center for Stem Cell and Regenerative Medicine, Zhejiang University, Hangzhou 310058, China. Electronic address:

Immunomodulation is an important phenomenon in the normal mammalian host response toward an injury, and plays a critical role in tissue regeneration and regenerative medicine. Different phenotypes of macrophages show an array of activation states compassing pro-inflammatory to pro-alleviating cells, which are the critical players to modulate immune response and tissue regeneration. In this study, macrophage membranes of different phenotypes (macrophages (M0), classically activated macrophages (M1) and alternatively activated macrophages (M2)) were coated onto poly-ε-caprolactone (PCL) nanofibers to acquire exterior surface proteins and similar functions of the natural membranes. In vitro results unveiled that these nanofibers, especially the M2-PCL nanofibers, can suppress the activities of inflammatory markers such as TNF-α and IL-1β, and stimulate anti-inflammatory markers such as Arg-1, IL-10 and TGF-β. In a C57BL/6 mouse model, the macrophage membrane-coated nanofibers, especially the M2-PCL nanofibers, displayed minimal cellular infiltration and low collagen deposition, increased anti-inflammatory CD206 and decreased inflammatory CD86 levels. The M2-PCL nanofibers most effectively neutralized inflammatory chemokines, regulated the expression of inflammation-associated genes as well as anti-inflammatory genes, and showed strong immunomodulatory effects than the PCL, M0-PCL and M1-PCL nanofibers. STATEMENT OF SIGNIFICANCE: Different types of macrophage membrane-functionalized PCL nanofibers were successfully prepared and well characterized. They inherited the surface proteins imitating the source macrophages, and played an important role in limiting cellular infiltration and collagen deposition. These different macrophages and their membrane-coated nanofibers (M0-PCL, M1-PCL and M2-PCL) behaved like their respective source cells. The M2 mimicking M2-PCL nanofibers effectively polarized macrophages to M2 phenotype and decreased the expression of inflammation-associated chemokines and promoted the anti-inflammation in vitro and in vivo, which is critical for tissue regeneration. The mice implanted with the bio-mimicking M2-PCL nanofibers effectively inhibited toll like receptors signaling induced NF-kB and IRF-5 and their target genes such as Edn-1, IL-6, iNOS, TNF-α, etc. compared to the PCL, and M0-PCL and M1-PCL macrophage membrane-coated nanofibers.
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http://dx.doi.org/10.1016/j.actbio.2021.12.026DOI Listing
December 2021

Micropatterned Poly(D,L-Lactide-Co-Caprolactone) Conduits With KHI-Peptide and NGF Promote Peripheral Nerve Repair After Severe Traction Injury.

Front Bioeng Biotechnol 2021 9;9:744230. Epub 2021 Dec 9.

Department of Thyroid Surgery, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China.

Severe traction injuries after stretch to peripheral nerves are common and challenging to repair. The nerve guidance conduits (NGCs) are promising in the regeneration and functional recovery after nerve injuries. To enhance the repair of severe nerve traction injuries, in this study KHIFSDDSSE (KHI) peptides were grafted on a porous and micropatterned poly(D,L-lactide-co-caprolactone) (PLCL) film (MPLCL), which was further loaded with a nerve growth factor (NGF). The adhesion number of Schwann cells (SCs), ratio of length/width (L/W), and percentage of elongated SCs were significantly higher in the MPLCL-peptide group and MPLCL-peptide-NGF group compared with those in the PLCL group . The electromyography (EMG) and morphological changes of the nerve after severe traction injury were improved significantly in the MPLCL-peptide group and MPLCL-peptide-NGF group compared with those in the PLCL group . Hence, the NGCs featured with both bioactive factors (KHI peptides and NGF) and physical topography (parallelly linear micropatterns) have synergistic effect on nerve reinnervation after severe traction injuries.
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http://dx.doi.org/10.3389/fbioe.2021.744230DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8696012PMC
December 2021

Micropatterns and peptide gradient on the inner surface of a guidance conduit synergistically promotes nerve regeneration .

Bioact Mater 2022 Mar 15;9:134-146. Epub 2021 Jul 15.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

Both of the surface topographical features and distribution of biochemical cues can influence the cell-substrate interactions and thereby tissue regeneration . However, they have not been combined simultaneously onto a biodegradable scaffold to demonstrate the synergistic role so far. In this study, a proof-of-concept study is performed to prepare micropatterns and peptide gradient on the inner wall of a poly (D,L-lactide--caprolactone) (PLCL) guidance conduit and its advantages in regeneration of peripheral nerve . After linear ridges/grooves of 20/40 μm in width are created on the PLCL film, its surface is aminolyzed in a kinetically controlled manner to obtain the continuous gradient of amino groups, which are then transferred to CQAASIKVAV peptide density gradient via covalent coupling of glutaraldehyde. The Schwann cells are better aligned along with the stripes, and show a faster migration rate toward the region of higher peptide density. Implantation of the nerve guidance conduit made of the PLCL film having both the micropatterns and peptide gradient can significantly accelerate the regeneration of sciatic nerve in terms of rate, function recovery and microstructures, and reduction of fibrosis in muscle tissues. Moreover, this nerve conduit can also benefit the M2 polarization of macrophages and promote vascularization .
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http://dx.doi.org/10.1016/j.bioactmat.2021.07.010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8586031PMC
March 2022

Alleviating Oxidative Injury of Myocardial Infarction by a Fibrous Polyurethane Patch with Condensed ROS-Scavenging Backbone Units.

Adv Healthc Mater 2021 Nov 22:e2101855. Epub 2021 Nov 22.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

Excessive reactive oxygen species (ROS) generated after myocardial infarction (MI) result in the oxidative injury in myocardium. Implantation of antioxidant biomaterials, without the use of any type of drugs, is very appealing for clinical translation, leading to the great demand of novel biomaterials with high efficiency of ROS elimination. In this study, a segmented polyurethane (PFTU) with a high density of ROS-scavenging backbone units is synthesized by the reaction of poly(thioketal) dithiol (PTK) and poly(propylene fumarate) diol (PPF) (soft segments), thioketal diamine (chain extender), and 1,6-hexamethylene diisocyanate (HDI). Its chemical structure is verified by gel permeation chromatography (GPC), H nuclear magnetic resonance ( H NMR) spectroscopy, and Fourier transform infrared (FTIR) spectroscopy. The electrospun composite PFTU/gelatin (PFTU/Gt) fibrous patches show good antioxidation capacity and ROS-responsive degradation in vitro. Implantation of the PFTU/gelatin patches on the heart tissue surface in MI rats consistently decreases the ROS level, membrane peroxidation, and cell apoptosis at the earlier stage, which are not observed in the non-ROS-responsive polyurethane patch. Inflammation and fibrosis are also reduced in the PFTU/gelatin-treated hearts, resulting in the reduced left ventricular remodeling and better cardiac functions postimplantation for 28 d.
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http://dx.doi.org/10.1002/adhm.202101855DOI Listing
November 2021

Inflammation-modulating nanoparticles for pneumonia therapy.

Wiley Interdiscip Rev Nanomed Nanobiotechnol 2021 Oct 29:e1763. Epub 2021 Oct 29.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, China.

Pneumonia is a common but serious infectious disease, and is the sixth leading cause for death. The foreign pathogens such as viruses, fungi, and bacteria establish an inflammation response after interaction with lung, leading to the filling of bronchioles and alveoli with fluids. Although the pharmacotherapies have shown their great effectiveness to combat pathogens, advanced methods are under developing to treat complicated cases such as virus-infection and lung inflammation or acute lung injury (ALI). The inflammation modulation nanoparticles (NPs) can effectively suppress immune cells and inhibit inflammatory molecules in the lung site, and thereby alleviate pneumonia and ALI. In this review, the pathological inflammatory microenvironments in pneumonia, which are instructive for the design of biomaterials therapy, are summarized. The focus is then paid to the inflammation-modulating NPs that modulate the inflammatory cells, cytokines and chemokines, and microenvironments of pneumonia for better therapeutic effects. This article is categorized under: Therapeutic Approaches and Drug Discovery > Nanomedicine for Respiratory Disease.
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http://dx.doi.org/10.1002/wnan.1763DOI Listing
October 2021

Artificial osteochondral interface of bioactive fibrous membranes mediating calcified cartilage reconstruction.

J Mater Chem B 2021 09 29;9(37):7782-7792. Epub 2021 Sep 29.

Bio-nanomaterials and Regenerative Medicine Research Division, Zhejiang-California International Nanosystem Institute, Zhejiang University, Hangzhou 310058, China.

Calcified cartilage is a mineralized osteochondral interface region between the hyaline cartilage and subchondral bone. There are few reported artificial biomaterials that could offer bioactivities for substantial reconstruction of calcified cartilage. Herein we developed new poly(L-lactide--caprolactone) (PLCL)-based trilayered fibrous membranes as a functional interface for calcified cartilage reconstruction and superficial cartilage restoration. The trilayered membranes were prepared by the electrospinning technique, and the fibrous morphology was maintained when the chondroitin sulfate (CS) or bioactive glass (BG) particles were introduced in the upper or bottom layer, respectively. Although 30% BG in the bottom layer led to a significant decrease in tensile resistance, the inorganic ion release was remarkably higher than that in the counterpart with 10% BG. The studies showed that the fibrous membranes as osteochondral interfaces exhibited different biological performances on superficial cartilage restoration and calcified cartilage reconstruction. All of the implanted host hyaline cartilage enabled a self-healing process and an increase in the BG content in the membranes was desirable for promoting the repair of the calcified cartilage with time. The histological staining confirmed the osteochondral interface in the 30% BG bottom membrane maintained appreciable calcified cartilage repair after 12 weeks. These findings demonstrated that such an integrated artificial osteochondral interface containing appropriate bioactive ions are potentially applicable for osteochondral interface tissue engineering.
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http://dx.doi.org/10.1039/d1tb01238jDOI Listing
September 2021

3DICE coding matrix multidirectional macro-architecture modulates cell organization, shape, and co-cultures endothelization network.

Biomaterials 2021 10 31;277:121112. Epub 2021 Aug 31.

3B's Research Group, I3Bs, Research Institute on Biomaterials, Biodegradables and Biomimetics, University of Minho, Headquarters of the European Institute of Excellence on Tissue Engineering and Regenerative Medicine, Zona Industrial da Gandra, AvePark, Barco GMR, 4805-017, Portugal; ICVS/3B's, PT Government Associate Laboratory, Braga, Guimarães, Portugal. Electronic address:

Natural extracellular matrix governs cells providing biomechanical and biofunctional outstanding properties, despite being porous and mostly made of soft materials. Among organs, specific tissues present specialized macro-architectures. For instance, hepatic lobules present radial organization, while vascular sinusoids are branched from vertical veins, providing specific biofunctional features. Therefore, it is imperative to mimic such structures while modeling tissues. So far, there is limited capability of coupling oriented macro-structures with interconnected micro-channels in programmable long-range vertical and radial sequential orientations. Herein, a three-directional ice crystal elongation (3DICE) system is presented to code geometries in cryogels. Using 3DICE, guided ice crystals growth templates vertical and radial pores through bulky cryogels. Translucent isotropic and anisotropic architectures of radial or vertical pores are fabricated with tunable mechanical response. Furthermore, 3D combinations of vertical and radial pore orientations are coded at the centimeter scale. Cell morphological response to macro-architectures is demonstrated. The formation of endothelial segments, CYP450 activity, and osteopontin expression, as liver fibrosis biomarkers, present direct response and specific cellular organization within radial, linear, and random architectures. These results unlock the potential of ice-templating demonstrating the relevance of macro-architectures to model tissues, and broad possibilities for drug testing, tissue engineering, and regenerative medicine.
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http://dx.doi.org/10.1016/j.biomaterials.2021.121112DOI Listing
October 2021

A cell-free ROS-responsive hydrogel/oriented poly(lactide-co-glycolide) hybrid scaffold for reducing inflammation and restoring full-thickness cartilage defects.

Biomed Mater 2021 09 14;16(6). Epub 2021 Sep 14.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, People's Republic of China.

The modulation of inflammation in tissue microenvironment takes an important role in cartilage repair and regeneration. In this study, a novel hybrid scaffold was designed and fabricated by filling a reactive oxygen species (ROS)-scavenging hydrogel (RS Gel) into a radially oriented poly(lactide-co-glycolide) (PLGA) scaffold. The radially oriented PLGA scaffolds were fabricated through a temperature gradient-guided phase separation and freeze-drying method. The RS Gel was formed by crosslinking the mixture of ROS-responsive hyperbranched polymers and biocompatible methacrylated hyaluronic acid (HA-MA). The hybrid scaffolds exhibited a proper compressive modulus, good ROS-scavenging capability, and cell compatibility.tests showed that the hybrid scaffolds significantly regulated inflammation and promoted regeneration of hyaline cartilage after they were implanted into full-thickness cartilage defects in rabbits for 12 w. In comparison with the PLGA scaffolds, the neo-cartilage in the hybrid scaffolds group possessed more deposition of glycosaminoglycans and collagen type II, and were well integrated with the surrounding tissue.
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http://dx.doi.org/10.1088/1748-605X/ac21ddDOI Listing
September 2021

Stimuli-Sensitive Nanotherapies for the Treatment of Osteoarthritis.

Macromol Biosci 2021 Nov 16;21(11):e2100280. Epub 2021 Aug 16.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

Osteoarthritis (OA) is a common chronic inflammatory disease in the joints. It is one of the leading causes of disability with increasing morbidity, which has become one of the serious clinical issues. Current treatments would only provide temporary relief due to the lack of early diagnosis and effective therapy, and thus the replacement of joints may be needed when the OA deteriorates. Although the intra-articular injection and oral administration of drugs are helpful for OA treatment, they are suffering from systemic toxicity, short retention time in joint, and insufficient bioavailability. Nanomedicine is potential to improve the drug delivery efficiency and targeting ability. In this focused progress review, the particle-based drug loading systems that can achieve targeted and triggered release are summarized. Stimuli-responsive nanocarriers that are sensitive to endogenous microenvironmental signals such as reactive oxygen species, enzymes, pH, and temperature, as well as external stimuli such as light for OA therapy are introduced in this review. Furthermore, the nanocarriers associated with targeted therapy and imaging for OA treatment are summarized. The potential applications of nanotherapies for OA treatment are finally discussed.
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http://dx.doi.org/10.1002/mabi.202100280DOI Listing
November 2021

Research advances of biomaterials-based microenvironment-regulation therapies for repair and regeneration of spinal cord injury.

Biomed Mater 2021 08 27;16(5). Epub 2021 Aug 27.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, People's Republic of China.

Traumatic spinal cord injury (SCI) usually results in restricted behaviour recovery and even life-changing paralysis, accompanied with numerous complications. Pathologically, the initial injuries trigger a series of secondary injuries, leading to an expansion of lesion site, a mass of neuron loss, and eventual failure of endogenous axon regeneration. As the advances rapidly spring up in regenerative medicine and tissue engineering biomaterials, regulation of these secondary injuries becomes possible, shedding a light on normal functional restoration. The successful tissue regeneration lies in proper regulation of the inflammatory microenvironment, including the inflammatory immune cells and inflammatory factors that lead to oxidative stress, inhibitory glial scar and neuroexcitatory toxicity. Specifically, the approaches based on microenvironment-regulating biomaterials have shown great promise in the repair and regeneration of SCI. In this review, the pathological inflammatory microenvironments of SCI are discussed, followed by the introduction of microenvironment-regulating biomaterials in terms of their impressive therapeutic effect in attenuation of secondary inflammation and promotion of axon regrowth. With the emphasis on regulating secondary events, the biomaterials for SCI treatment will become promising for clinical applications.
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http://dx.doi.org/10.1088/1748-605X/ac1d3cDOI Listing
August 2021

Grafting of CAG peptides and (polyethylene glycol) on unsaturated polyurethane films to promote selective adhesion and migration of urethral epithelial cells.

J Mater Chem B 2021 08 27;9(31):6201-6211. Epub 2021 Jul 27.

Department of Polymer Science and Engineering, MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Zhejiang University, Hangzhou 310027, China.

Selective adhesion and migration of urethral epithelial cells (HUCs) over fibroblasts (FIBs) are very important in the reconstruction of the urethral epithelial layer and prevention of ureteral scarring and stenosis. In this study, unsaturated polyurethane (PPFU-CO-SS) films were co-grafted with a cell-resisting poly(ethylene glycol) (PEG) layer and HUC-selective Cys-Ala-Gly (CAG) peptides, whose physicochemical changes were confirmed by X-ray photon spectroscopy, fluorescence spectroscopy and water contact angle measurements. The adhesion and activation of platelets on the PEG/CAG grafted surface were significantly reduced compared to those on the PPFU-CO-SS, resulting in a similar status as that on a PEG-grafted surface. The HUC-selective material could obviously promote the adhesion and migration of HUCs. The ratio of the urethral epithelial cells to fibroblasts on the PEG/CAG grafted surface was nearly 3-fold that on the unmodified PPFU-CO-SS in a co-culture competitive environment. The urethral epithelial cells cultured on the PEG/CAG grafted surface also had the highest migration rate, which was 2.24-fold compared to that on the PPFU-CO-SS control.
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http://dx.doi.org/10.1039/d1tb00547bDOI Listing
August 2021

Influence of enantiomeric polylysine grafted on gold nanorods on the uptake and inflammatory response of bone marrow-derived macrophages in vitro.

J Biomed Mater Res A 2022 Jan 21;110(1):143-155. Epub 2021 Jul 21.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, China.

The macrophages take significant roles in homeostasis, phagocytosis of pathogenic organisms, and modulation of host defense and inflammatory processes. In this study, the enantiomeric poly-D-lysine (PDL) and poly-L-lysine (PLL) were conjugated to gold nanorods (AuNRs) to study their influence on the polarization of macrophages. The AuNRs capped with cetyl trimethyl ammonium bromide (CTAB) ([email protected]) exhibited larger toxicity to macrophages when their concentration was higher than 50 μg/ml, whereas the [email protected] and [email protected] showed neglectable toxicity at the same concentration compared with the control. The [email protected] and [email protected] were internalized into the macrophages with a higher value than the [email protected] as revealed by transmission electron microscopy (TEM) and inductively coupled plasma mass spectrometry (ICP-MS) characterization. Unlike the grafted PDL/PLL on flat substrates, the [email protected] and [email protected] were not able to polarize M0 macrophages to any other phenotype after internalization as confirmed by ELISA, flow cytometry, and fluorescence microscopy analysis. Nonetheless, the expression of M1 phenotype markers was reduced after the internalization of [email protected] and [email protected] by M1 macrophages. The assays of ELISA, flow cytometry, and reactive oxygen species levels exhibited decrease in inflammation of the M1 macrophages.
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http://dx.doi.org/10.1002/jbm.a.37272DOI Listing
January 2022

Large fuzzy biodegradable polyester microspheres with dopamine deposition enhance cell adhesion and bone regeneration in vivo.

Biomaterials 2021 05 24;272:120783. Epub 2021 Mar 24.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China; Dr. Li Dak Sum & Yip Yio Chin Center for Stem Cell and Regenerative Medicine, Zhejiang University, Hangzhou, 310058, China. Electronic address:

The biodegradable polymer microparticles with different surface morphology and chemical compositions may influence significantly the behaviors of cells, and thereby further the performance of tissue regeneration in vivo. In this study, multi-stage hierarchical textures of poly(D,L-lactic-co-glycolide) (PLGA)/PLGA-b-PEG (poly(ethylene glycol)) microspheres with a diameter as large as 50-100 μm are fabricated based on interfacial instability of an emulsion. The obtained fuzzy structures on the microspheres are sensitive to annealing, which are changed gradually to a smooth one after treatment at 37 °C for 6 d or 80 °C for 1 h. The surface microstructures that are chemically dominated by PEG can be stabilized against annealing by dopamine deposition. By the combination use of annealing and dopamine deposition, a series of microspheres with robust surface topologies are facilely prepared. The fuzzy microstructures and dopamine deposition show a synergetic role to enhance cell-material interaction, leading to a larger number of adherent bone marrow-derived mesenchymal stem cells (BMSCs), A549 and MC 3T3 cells. The fuzzy microspheres with dopamine deposition can significantly promote bone regeneration 12 w post surgery in vivo, as revealed by micro-CT, histological, western blotting and RT-PCR analyses.
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http://dx.doi.org/10.1016/j.biomaterials.2021.120783DOI Listing
May 2021

Dimethyl Itaconate-Loaded Nanofibers Rewrite Macrophage Polarization, Reduce Inflammation, and Enhance Repair of Myocardic Infarction.

Small 2021 04 14;17(17):e2006992. Epub 2021 Mar 14.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

Cellular metabolism plays a major role in the regulation of inflammation. The inflammatory macrophages undergo a wide-range of metabolic rewriting due to the production of significant amount of itaconate metabolite from cis-aconitate in the tricarboxylic acid cycle. This itaconate molecule has been recently described as a promising immunoregulator. However, its function and mode of action on macrophages and tissue repair and regeneration are yet unclear. Herein, the itaconate-derivative dimethyl itaconate (DMI) suppresses the IL-23/IL-17 inflammatory axis-associated genes and promotes antioxidant nuclear factor erythroid 2-related factor 2 target genes. The poly-ε-caprolactone (PCL)/DMI nanofibers implanted in mice initially maintain inflammation by suppressing anti-inflammatory activity and particular inflammation, while at later stage promotes anti-inflammatory activity for an appropriate tissue repair. Furthermore, the PCL/DMI nanofiber patches show an excellent myocardial protection by reducing infarct area and improving ventricular function via time-dependent regulation of myocardium-associated genes. This study unveils potential DMI macrophage modulatory functions in tissue microenvironment and macrophages rewriting for proper tissue repair.
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http://dx.doi.org/10.1002/smll.202006992DOI Listing
April 2021

The Dynamic Inflammatory Tissue Microenvironment: Signality and Disease Therapy by Biomaterials.

Research (Wash D C) 2021 3;2021:4189516. Epub 2021 Feb 3.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China.

Tissue regeneration is an active multiplex process involving the dynamic inflammatory microenvironment. Under a normal physiological framework, inflammation is necessary for the systematic immunity including tissue repair and regeneration as well as returning to homeostasis. Inflammatory cellular response and metabolic mechanisms play key roles in the well-orchestrated tissue regeneration. If this response is dysregulated, it becomes chronic, which in turn causes progressive fibrosis, improper repair, and autoimmune disorders, ultimately leading to organ failure and death. Therefore, understanding of the complex inflammatory multiple player responses and their cellular metabolisms facilitates the latest insights and brings novel therapeutic methods for early diseases and modern health challenges. This review discusses the recent advances in molecular interactions of immune cells, controlled shift of pro- to anti-inflammation, reparative inflammatory metabolisms in tissue regeneration, controlling of an unfavorable microenvironment, dysregulated inflammatory diseases, and emerging therapeutic strategies including the use of biomaterials, which expand therapeutic views and briefly denote important gaps that are still prevailing.
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http://dx.doi.org/10.34133/2021/4189516DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7879376PMC
February 2021

Immunomodulatory biomaterials and their application in therapies for chronic inflammation-related diseases.

Acta Biomater 2021 03 21;123:1-30. Epub 2021 Jan 21.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China; Dr. Li Dak Sum & Yip Yio Chin Center for Stem Cell and Regenerative Medicine, Zhejiang University, Hangzhou 310058, China. Electronic address:

The degree of tissue injuries such as the level of scarring or organ dysfunction, and the immune response against them primarily determine the outcome and speed of healing process. The successful regeneration of functional tissues requires proper modulation of inflammation-producing immune cells and bioactive factors existing in the damaged microenvironment. In the tissue repair and regeneration processes, different types of biomaterials are implanted either alone or by combined with other bioactive factors, which will interact with the immune systems including immune cells, cytokines and chemokines etc. to achieve different results highly depending on this interplay. In this review article, the influences of different types of biomaterials such as nanoparticles, hydrogels and scaffolds on the immune cells and the modification of immune-responsive factors such as reactive oxygen species (ROS), cytokines, chemokines, enzymes, and metalloproteinases in tissue microenvironment are summarized. In addition, the recent advances of immune-responsive biomaterials in therapy of inflammation-associated diseases such as myocardial infarction, spinal cord injury, osteoarthritis, inflammatory bowel disease and diabetic ulcer are discussed.
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http://dx.doi.org/10.1016/j.actbio.2021.01.025DOI Listing
March 2021

formation of tetraphenylethylene nano-structures on microgels inside living cells reduction-responsive self-assembly.

Nanoscale 2021 Jan;13(1):138-149

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

Controlling the assembly of synthetic molecules in living systems is of significance for their adaptive applications. However, it is difficult to achieve, especially for composite self-assemblies, due to the complexity and dynamic change of the intracellular environment, and there exist technical difficulties for the direct visualization of organic and polymer self-assemblies. Herein, we demonstrate a novel strategy for the in situ formation of self-assembled micro-nano composite structures in a cell milieu using reduction-responsive microgels (MGs) as a platform. The MGs were prepared by a templating and crosslinking method using a synthetic amphiphlic polymer as the basic material and porous CaCO3 microparticles as the template. The aggregation-induced emission (AIE) tetraphenylethylene moieties and reduction-labile disulfide bonds in the MGs were employed as the self-assembly building blocks and triggering sites for the intracellular self-assembly, respectively. In the presence of reductive agents such as glutathione, nano-spikes were gradually formed on the MGs. After the MGs were internalized by cells, the in situ formation of microgel/nano-spike composite structures was evidenced by the enhanced fluorescence intensity and was further confirmed by direct transmission electron microscopy observation. This work provides an effective strategy to cope with the challenging task of achieving and probing controlled self-assembly in a cell milieu, leading to new insights into investigating biological self-assembly and promoting the development of micro-/nanomaterials by learning from nature.
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http://dx.doi.org/10.1039/d0nr06661cDOI Listing
January 2021

Covalent grafting of hyperbranched poly-L-lysine on Ti-based implants achieves dual functions of antibacteria and promoted osteointegration in vivo.

Biomaterials 2021 02 16;269:120534. Epub 2020 Nov 16.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China; Dr. Li Dak Sum & Yip Yio Chin Center for Stem Cell and Regenerative Medicine, Zhejiang University, Hangzhou, 310058, China. Electronic address:

The dual functional implants of antibacteria and osteointegration are highly demanded in orthopedic and dentistry, especially for patients who suffer from diabetes or osteoporosis simultaneously. However, there is lack of the facile and robust method to produce clinically applicable implants with this dual function although coatings possessing single function have been extensively developed. Herein, hyperbranched poly-L-lysine (HBPL) polymers were covalently immobilized onto the alkali-heat treated titanium (Ti) substrates and implants by using 3-glycidyloxypropyltrimethoxysilane (GPTMS) as the coupling agent, which displayed excellent antibacterial activity against S. aureus and E. coli with an efficiency as high as 89.4% and 92.2% in vitro, respectively. The HBPL coating also significantly promoted the adhesion, spreading, proliferation and osteogenic differentiation of MC3T3-E1 cells in vitro. Furthermore, the results of a S. aureus infection rat model in vivo ulteriorly verified that the HBPL-modified screws had good antibacterial and anti-inflammatory abilities at an early stage of implantation and better osteointegration compared with the control Ti screws.
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http://dx.doi.org/10.1016/j.biomaterials.2020.120534DOI Listing
February 2021

Adaptable hydrogel with reversible linkages for regenerative medicine: Dynamic mechanical microenvironment for cells.

Bioact Mater 2021 May 10;6(5):1375-1387. Epub 2020 Nov 10.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

Hydrogels are three-dimensional platforms that serve as substitutes for native extracellular matrix. These materials are starting to play important roles in regenerative medicine because of their similarities to native matrix in water content and flexibility. It would be very advantagoues for researchers to be able to regulate cell behavior and fate with specific hydrogels that have tunable mechanical properties as biophysical cues. Recent developments in dynamic chemistry have yielded designs of adaptable hydrogels that mimic dynamic nature of extracellular matrix. The current review provides a comprehensive overview for adaptable hydrogel in regenerative medicine as follows. First, we outline strategies to design adaptable hydrogel network with reversible linkages according to previous findings in supramolecular chemistry and dynamic covalent chemistry. Next, we describe the mechanism of dynamic mechanical microenvironment influence cell behaviors and fate, including how stress relaxation influences on cell behavior and how mechanosignals regulate matrix remodeling. Finally, we highlight techniques such as bioprinting which utilize adaptable hydrogel in regenerative medicine. We conclude by discussing the limitations and challenges for adaptable hydrogel, and we present perspectives for future studies.
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http://dx.doi.org/10.1016/j.bioactmat.2020.10.029DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7658331PMC
May 2021

Bone tissue regeneration: The role of finely tuned pore architecture of bioactive scaffolds before clinical translation.

Bioact Mater 2021 May 7;6(5):1242-1254. Epub 2020 Nov 7.

Department of Orthopedics, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, 310003, China.

Spatial dimension of pores and interconnection in macroporous scaffolds is of particular importance in facilitating endogenous cell migration and bone tissue ingrowth. However, it is still a challenge to widely tune structure parameters of scaffolds by conventional methods because of inevitable pore geometrical deformation and poor pore interconnectivity. Here, the long-term biological performances of nonstoichiometric bioceramic scaffolds with different pore dimensions were assessed in critical-size femoral bone defect model. The 6% Mg-substituted wollastonite (CSi-Mg6) powders were prepared via wet-chemical precipitation and the scaffolds elaborately printed by ceramic stereolithography, displaying designed constant pore strut and tailorable pore height (200, 320, 450, 600 μm), were investigated thoroughly in the bone regeneration process. Together with detailed structural stability and mechanical properties were collaboratively outlined. Both μCT and histological analyses indicated that bone tissue ingrowth was retarded in 200 μm scaffolds in the whole stage (2-16 weeks) but the 320 μm scaffolds showed appreciable bone tissue in the center of porous constructs at 6-10 weeks and matured bone tissue were uniformly invaded in the whole pore networks at 16 weeks. Interestingly, the neo-tissue ingrowth was facilitated in the 450 μm and 600 μm scaffolds after 2 weeks and higher extent of bone regeneration and remodeling at the later stage. These new findings provide critical information on how engineered porous architecture impact bone regeneration . Simultaneously, this study shows important implications for optimizing the porous scaffolds design by advanced additive manufacture technique to match the clinical translation with high performance.
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http://dx.doi.org/10.1016/j.bioactmat.2020.11.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7653208PMC
May 2021

Spatiotemporal Measurement of Osmotic Pressures by FRET Imaging.

Angew Chem Int Ed Engl 2021 03 3;60(12):6488-6495. Epub 2021 Feb 3.

Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476, Potsdam, Germany.

Osmotic pressures (OPs) play essential roles in biological processes and numerous technological applications. However, the measurement of OP in situ with spatiotemporal resolution has not been achieved so far. Herein, we introduce a novel kind of OP sensor based on liposomes loaded with water-soluble fluorescent dyes exhibiting resonance energy transfer (FRET). The liposomes experience volume changes in response to OP due to water outflux. The FRET efficiency depends on the average distance between the entrapped dyes and thus provides a direct measure of the OP surrounding each liposome. The sensors exhibit high sensitivity to OP in the biologically relevant range of 0-0.3 MPa in aqueous solutions of salt, small organic molecules, and macromolecules. With the help of FRET microscopy, we demonstrate the feasibility of spatiotemporal OP imaging, which can be a promising new tool to investigate phenomena involving OPs and their dynamics in biology and technology.
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http://dx.doi.org/10.1002/anie.202011983DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7986915PMC
March 2021

A Reactive Oxygen Species Scavenging and O Generating Injectable Hydrogel for Myocardial Infarction Treatment In vivo.

Small 2020 12 9;16(48):e2005038. Epub 2020 Nov 9.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

The excessive reactive oxygen species (ROS) and hypoxia deteriorate the inflammation-related diseases such as myocardial infarction (MI), and thereby deter the normal tissue repair and recovery and further lead to severe fibrosis and malfunction of tissues and organs. In particular, the MI has become one of the leading causes of death nowadays. In this study, a novel type of injectable hydrogel with dual functions of ROS scavenging and O generating is fabricated for MI treatment in vivo. The hydrogel is formed within 3 s from the synthetic ROS-cleavable hyperbranched polymers and methacrylate hyaluronic acid (HA-MA) under UV-irradiation. Addition of biocompatible and applicable catalase in vivo enables the further transition of H O , a major type of ROS, to O and H O. Results of rat MI model demonstrate that this hydrogel can significantly remove excessive ROS, inhibit cell apoptosis, increase M2/M1 macrophage ratio, promote angiogenesis, reduce infarcted area, and improve cardiac functions. With the appropriate degradation rate, simple structure and composition without cell seeding, and very excellent MI therapeutic effect, this ROS scavenging and O generating hydrogel has a great promise to be applied clinically.
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http://dx.doi.org/10.1002/smll.202005038DOI Listing
December 2020

Antiviral Activity of Nanomaterials against Coronaviruses.

Macromol Biosci 2020 10 11;20(10):e2000196. Epub 2020 Aug 11.

W. Muhammad, Z. Zhai, Prof. C. Gao, MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China.

One of the challenges facing by world nowadays is the generation of new pathogens that cause public health issues. Coronavirus (CoV) is one of the severe pathogens that possess the RNA (ribonucleic acid) envelop, and extensively infect humans, birds, and other mammals. The novel strain "SARS-CoV-2" (severe acute respiratory syndrome coronavirus-2) causes deadly infection all over the world and presents a pandemic situation nowadays. The SARS-CoV-2 has 40 different strains that create a worrying situation for health authorities. The virus develops serious pneumonia in infected persons and causes severe damage to the lungs. There is no vaccine available for this virus up to present. To cure this type of infections by making vaccines and antiviral drugs is still a major challenge for researchers. Nanotechnology covering a multidisciplinary field may find the solution to this lethal infection. The interaction of nanomaterials and microorganisms is considered as a potential treatment method because the nanomaterials owe unique physicochemical properties. The aim of this review is to present an overview of previous and recent studies of nanomaterials against coronaviruses and to provide possible new strategies for upcoming research using the nanotechnology platform.
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http://dx.doi.org/10.1002/mabi.202000196DOI Listing
October 2020

A tarsus construct of a novel branched polyethylene with good elasticity for eyelid reconstruction .

Regen Biomater 2020 Jun 7;7(3):259-269. Epub 2020 Feb 7.

Department of Ophthalmology, The Second Affiliated Hospital of Zhejiang University, College of Medicine, Hangzhou, Zhejiang 310009, China.

Branched polyethylene (B-PE) elastomer was investigated for its potential medical application as a tarsus construct. The results showed that the B-PE and processed B-PE films or scaffolds did not exhibit noticeable cytotoxicity to the NIH3T3 fibroblasts and human vascular endothelial cells (ECs). The B-PE scaffolds with a pore size of 280-480 µm were prepared by using a gelatin porogen-leaching method. The porous scaffolds implanted subcutaneously in rats exhibited mild inflammatory response, collagen deposition and fast fibrovascularization, suggesting their good biocompatibility. Quantitative real-time PCR analysis showed low expression of pro-inflammatory genes and up-regulated expressions of collagen deposition and vascularization-related genes, validating the results of historical evaluation in a molecular level. The B-PE scaffolds and Medpor controls were transplanted in rabbits with eyelid defects. The B-PE scaffolds exhibited a similar elastic modulus and provided desirable repair effects with mild fibrous capsulation, less eyelid deformities, and were well integrated with the fibrovascular tissue compared with the Medpor controls.
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http://dx.doi.org/10.1093/rb/rbaa001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7266665PMC
June 2020

Age-Related Regeneration of Osteochondral and Tibial Defects by a Fibrin-Based Construct .

Front Bioeng Biotechnol 2020 5;8:404. Epub 2020 May 5.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, China.

Tissue-biomaterial interactions in different microenvironments influence significantly the repair and regeneration outcomes when a scaffold or construct is implanted. In order to elucidate this issue, a fibrin gel filled macroporous fibrin scaffold (fibrin-based scaffold) was fabricated by loading fibrinogen via a negative pressure method, following with thrombin crosslinking. The macroporous fibrin scaffold exhibited a porous structure with porosity of (88.1 ± 1.3)%, and achieved a modulus of 19.8 ± 0.4 kPa at a wet state after fibrin gel filling, providing a suitable microenvironment for bone marrow-derived mesenchymal stem cells (BMSCs). The cellular culture revealed that the fibrin-based scaffold could support the adhesion, spreading, and proliferation of BMSCs in appropriate cell encapsulation concentrations. The fibrin-based scaffolds were then combined with BMSCs and lipofectamine/plasmid deoxyribonucleic acid (DNA) encoding mouse-transforming growth factor β1 (pDNA-TGF-β1) complexes to obtain the fibrin-based constructs, which were implanted into osteochondral and tibial defects at young adult rabbits (3 months old) and aged adult rabbits (12 months old) to evaluate their respective repair effects. Partial repair of osteochondral defects and perfect restoration of tibial defects were realized at 18 weeks post-surgery for the young adult rabbits, whereas only partial repair of subchondral bone and tibial bone defects were found at the same time for the aged adult rabbits, confirming the adaptability of the fibrin-based constructs to the different tissue microenvironments by tissue-biomaterial interplays.
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http://dx.doi.org/10.3389/fbioe.2020.00404DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7214756PMC
May 2020

Micro- and nanoparticles-based immunoregulation of macrophages for tissue repair and regeneration.

Colloids Surf B Biointerfaces 2020 Apr 25;192:111075. Epub 2020 Apr 25.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China. Electronic address:

The importance of inflammatory tissue microenvironment on the repair and regeneration of tissues and organs has been well recognized. In particular, the phenotypes of macrophages can significantly influence on the processes of tissue repair and remodeling. Among the many types of biomaterials, the particles in the range from nanometers to submicron meters have been extensively studied and applied in tissue engineering and regenerative medicine. They can actively interact with cells in different levels, and show the ability to regulate the polarization of macrophages. In this review, the influence of physicochemical properties such as size, surface charge, chemical components and surface modification of micro-nanoparticles on the immune behavior of macrophages, including endocytosis and phenotype switch, shall be introduced. The important roles of nanoparticles-based immunoregulation of macrophages on the chronic skin wounds regeneration, myocardial repair, liver repair and bone regeneration are discussed.
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http://dx.doi.org/10.1016/j.colsurfb.2020.111075DOI Listing
April 2020

Adsorption of serum proteins on titania nanotubes and its role on regulating adhesion and migration of mesenchymal stem cells.

J Biomed Mater Res A 2020 11 17;108(11):2305-2318. Epub 2020 Jun 17.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, China.

Migration and differentiation of bone marrow-derived mesenchymal stem cells (BMSCs) is an important biological process in tissue regeneration. Nanostructured titanium materials are believed to play a fundamental role in dental and orthopedic applications. However, the protein adsorption on nanostructured titanium materials and its correlation with the subsequent cell behaviors have not been studied. In this work, the titania nanotube arrays with different tubular diameters ranging from 27.3 to 88.2 nm were fabricated by using an electrochemical etching method. The adsorbed amounts and types of cell adhesion-related proteins (such as fibronectin, vitronectin, and laminin) from serum were investigated, revealing that these proteins were preferred to bind onto the surface with nanotubes of a smaller diameter. Adhesion and migration of BMSCs were studied as a function of different nanotube diameters in the presence or absence of serum proteins. Compared with the nanotube surface with a larger tubular diameter (88.2 nm), the surface with a smaller one could better support BMSCs in terms of adhesion and spreading. The pre-adsorbed serum proteins significantly enhanced adhesion and migration abilities of BMSCs. However, the adequate interactions between cells and serum proteins on the nanotubes surface with smallest nanotubes in diameter weakened cell mobility. Arrangement of cytoskeleton and expressions of key genes and proteins were studied, revealing that the nanostructured surfaces and pre-adsorbed proteins jointly mediated the adhesion and migration of BMSCs.
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http://dx.doi.org/10.1002/jbm.a.36987DOI Listing
November 2020

Unsaturated polyurethane films grafted with enantiomeric polylysine promotes macrophage polarization to a M2 phenotype through PI3K/Akt1/mTOR axis.

Biomaterials 2020 07 31;246:120012. Epub 2020 Mar 31.

MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou, 310027, China; Dr. Li Dak Sum & Yip Yio Chin Center for Stem Cell and Regenerative Medicine, Zhejiang University, Hangzhou, 310058, China. Electronic address:

The immune system responds immediately to tissue trauma and to biomaterial implants under the participation of M1/M2 macrophages polarization. The surface properties of biomaterials can significantly influence the tissue repair progress through modulating the macrophage functions. In this study, the surface of poly(propylene fumarate) polyurethane films (PPFU) is grafted with a same density of enantiomeric poly-l-lysine (PPFU-g-PLL) and poly-d-lysine (PPFU-g-PDL), leading to a similar level of enhanced surface wettability for the PPFU-g-PLL and PPFU-g-PDL. The polylysine-grafted PPFU can restrict the M1 polarization, whereas promote M2 polarization of macrophages in vitro, judging from the secretion of cytokines and expression of key M1 and M2 related genes. Comparatively, the PPFU-g-PDL has a stronger effect in inducing M2 polarization in vivo, resulting in a thinner fibrous capsule surrounding the implant biomaterials. The CD44 and integrins of macrophages participate in the polarization process probably by activating focal adhesion kinase (FAK) and Rho-associated protein kinase (ROCK), and downstream PI3K/Akt1/mTOR signal axis to up regulate M2 related gene expression. This study confirms for the first time that polylysine coating is an effective method to regulate the immune response of biomaterials, and the polylysine-modified thermoplastic PPFU with the advantage to promote M2 polarization may be applied widely in regenerative medicine.
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http://dx.doi.org/10.1016/j.biomaterials.2020.120012DOI Listing
July 2020

Smart Flexible Electronics-Integrated Wound Dressing for Real-Time Monitoring and On-Demand Treatment of Infected Wounds.

Adv Sci (Weinh) 2020 Mar 10;7(6):1902673. Epub 2020 Jan 10.

College of Computer Science and Technology Zhejiang University Hangzhou 310027 China.

As the most frequent wound complication, infection has become a major clinical challenge in wound management. To overcome the "Black Box" status of the wound-healing process, next-generation wound dressings with the abilities of real-time monitoring, diagnosis during early stages, and on-demand therapy has attracted considerable attention. Here, by combining the emerging development of bioelectronics, a smart flexible electronics-integrated wound dressing with a double-layer structure, the upper layer of which is polydimethylsiloxane-encapsulated flexible electronics integrated with a temperature sensor and ultraviolet (UV) light-emitting diodes, and the lower layer of which is a UV-responsive antibacterial hydrogel, is designed. This dressing is expected to provide early infection diagnosis via real-time wound-temperature monitoring by the integrated sensor and on-demand infection treatment by the release of antibiotics from the hydrogel by in situ UV irradiation. The integrated system possesses good flexibility, excellent compatibility, and high monitoring sensitivity and durability. Animal experiment results demonstrate that the integrated system is capable of monitoring wound status in real time, detecting bacterial infection and providing effective treatment on the basis of need. This proof-of-concept research holds great promise in developing new strategies to significantly improve wound management and other pathological diagnoses and treatments.
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http://dx.doi.org/10.1002/advs.201902673DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7080536PMC
March 2020
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