Self-oxygenation of engineered living tissues orchestrates osteogenic commitment of mesenchymal stem cells

Hassan, Shabir; Wang, Ting; Shi, Kun; Huang, Yike; Urbina, Mariely; Gan, Kaifeng; Chen, Mo; Willemen, Niels; Kalam, Haroon; Luna‐Cerón, Eder; Çeçen, Berivan; Elbait, Gihan Daw; Li, Jinghang; García‐Rivera, Luis Enrique; Gurian, Melvin; Banday, Mudassir Meraj; Yang, Kisuk; Lee, Myung Chul; Zhuang, Weida; Johnbosco, Castro; Jeon, Oju; Alsberg, Eben; Leijten, Jeroen; Shin, Su Ryon

doi:10.1016/j.biomaterials.2023.122179

Cited by 13 publications

(2 citation statements)

References 68 publications

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“…In addition, CPP-L/GelMA promoted the proliferation of human umbilical vascular ECs (HUVECs) in a low oxygen environment, and the prolonged oxygen-enriched microenvironment created by CPP-L/GelMA hydrogel significantly promoted angiogenesis and osteogenesis and inhibited osteoblasts, and favorable bone regeneration in a mouse cranial defect model was recorded after the implantation of the CPP-L/GelMA hybrid hydrogel. In another work reported by Hassan and the colleagues, the effects of calcium peroxide (CPO)-based oxygen-generating microparticles (OMPs) on the osteogenic fate of human BMSCs (hBMSCs) in a severely hypoxic microenvironment were explored and confirmed [ 32 ]. Three kinds of hydrogels were constructed: GelMA hydrogels containing osteoinductive silicate nanoparticles (SNP hydrogels), OMPS (OMP hydrogels), or SNP and OMP (SNP/OMP hydrogels).…”

Section: Gelma-based Vascularized Bone Scaffoldsmentioning

confidence: 99%

GelMA-based bioactive hydrogel scaffolds with multiple bone defect repair functions: therapeutic strategies and recent advances

Zhou,

Jiang,

Zhou

et al. 2023

Biomater Res

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Currently, the clinical treatment of critical bone defects attributed to various causes remains a great challenge, and repairing these defects with synthetic bone substitutes is the most common strategy. In general, tissue engineering materials that mimic the structural, mechanical and biological properties of natural bone have been extensively applied to fill bone defects and promote in situ bone regeneration. Hydrogels with extracellular matrix (ECM)-like properties are common tissue engineering materials, among which methacrylate-based gelatin (GelMA) hydrogels are widely used because of their tunable mechanical properties, excellent photocrosslinking capability and good biocompatibility. Owing to their lack of osteogenic activity, however, GelMA hydrogels are combined with other types of materials with osteogenic activities to improve the osteogenic capability of the current composites. There are three main aspects to consider when enhancing the bone regenerative performance of composite materials: osteoconductivity, vascularization and osteoinduction. Bioceramics, bioglass, biomimetic scaffolds, inorganic ions, bionic periosteum, growth factors and two-dimensional (2D) nanomaterials have been applied in various combinations to achieve enhanced osteogenic and bone regeneration activities. Three-dimensional (3D)-bioprinted scaffolds are a popular research topic in bone tissue engineering (BTE), and printed and customized scaffolds are suitable for restoring large irregular bone defects due to their shape and structural tunability, enhanced mechanical properties, and good biocompatibility. Herein, the recent progress in research on GelMA-based composite hydrogel scaffolds as multifunctional platforms for restoring critical bone defects in plastic or orthopedic clinics is systematically reviewed and summarized. These strategies pave the way for the design of biomimetic bone substitutes for effective bone reconstruction with good biosafety. Graphical Abstract This review provides novel insights into the development and current trends of research on GelMA-based hydrogels as effective bone tissue engineering (BTE) scaffolds for correcting bone defects, and these contents are summarized and emphasized from various perspectives (osteoconductivity, vascularization, osteoinduction and 3D-bioprinting). In addition, advantages and deficiencies of GelMA-based bone substitutes used for bone regeneration are put forward, and corresponding improvement measures are presented prior to their clinical application in near future (created with BioRender.com).

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Section: Gelma-based Vascularized Bone Scaffoldsmentioning

confidence: 99%

GelMA-based bioactive hydrogel scaffolds with multiple bone defect repair functions: therapeutic strategies and recent advances

Zhou,

Jiang,

Zhou

et al. 2023

Biomater Res

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“…[ 15 ] Moreover, the importance of local oxygenation in wound healing is well‐established. [ 16 ] Alleviating the hypoxic environment supports the metabolism and regeneration of local cells. Extensive research has been conducted on the facilitative role of copper elements in osteogenesis and angiogenesis.…”

Section: Introductionmentioning

confidence: 99%

Enhanced Bacterial Cuproptosis‐Like Death via Reversal of Hypoxia Microenvironment for Biofilm Infection Treatment

Luo,

Lu,

Shi

et al. 2024

Advanced Science

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A recently emerging cell death pathway, known as copper‐induced cell death, has demonstrated significant potential for treating infections. Existing research suggests that cells utilizing aerobic respiration, as opposed to those reliant on glycolysis, exhibit greater sensitivity to copper‐induced death. Herein, a MnO2‐loaded copper metal–organic frameworks platform is developed denoted as MCM, to enhance bacterial cuproptosis‐like death via the remodeling of bacterial respiratory metabolism. The reversal of hypoxic microenvironments induced a cascade of responses, encompassing the reactivation of suppressed immune responses and the promotion of osteogenesis and angiogenesis. Initially, MCM catalyzed O2 production, alleviating hypoxia within the biofilm and inducing a transition in bacterial respiration mode from glycolysis to aerobic respiration. Subsequently, the sensitized bacteria, characterized by enhanced tricarboxylic acid cycle activity, underwent cuproptosis‐like death owing to increased copper concentrations and aggregated intracellular dihydrolipoamide S‐acetyltransferase (DLAT). The disruption of hypoxia also stimulated suppressed dendritic cells and macrophages, thereby strengthening their antimicrobial activity through chemotaxis and phagocytosis. Moreover, the nutritional effects of copper elements, coupled with hypoxia alleviation, synergistically facilitated the regeneration of bones and blood vessels. Overall, reshaping the infection microenvironment to enhance cuproptosis‐like cell death presents a promising avenue for eradicating biofilms.

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Implantable Multifunctional Micro‐Oxygen Reservoir System for Promoting Vascular‐Osteogenesis via Remodeling Regenerative Microenvironment

Rui,

Mao,

et al. 2024

Advanced Science

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Hypoxia and reactive oxygen species (ROS) overaccumulation cause persistent oxidative stress and impair intrinsic regenerative potential upon tissue injury. For local tissue injury with hypoxia, such as bone fracture and defects, a localized‐sufficient oxygen supply is highly desirable but remains challenging. Therefore, to explore a strategy and its intrinsic mechanism for supplying oxygen locally and remodeling the regenerative microenvironment, an innovative oxygenating hydrogel microsphere system with sustained oxygenation and antioxidant properties is introduced by loading CaO2@SiO2@PDA (CSP) nanoparticles. Specifically, the CSP nanoparticles exhibited broad‐spectrum free radicals scavenging ability, along with prolonged controlled‐release of oxygen once integrated into the gelatin methacrylate anhydride (GelMA) microspheres (CSP‐GM). The CSP‐GM with extra cellular matrix (ECM)‐mimicking structures reconstructed living niches, promoting the adhesion and proliferation of bone marrow stromal cells (BMSCs). As a multifaceted microenvironment regulator, CSP‐GM remodeled the regenerative microenvironment by synergistically producing oxygen and scavenging ROS, recovering mitochondrial homeostasis and antioxidant defenses of BMSCs, promoting angiogenesis and osteogenesis under hypoxia conditions via precisely modulating the Nrf2/HO‐1 signaling pathway. The multiple pro‐regenerative effects of the implantable functionalized micro‐oxygen reservoir on bone repair are further corroborated by the enhanced vascularized bone formation in rat femoral defects, presenting a comprehensive and promising strategy for tissue repair.

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Self-oxygenation of engineered living tissues orchestrates osteogenic commitment of mesenchymal stem cells

Cited by 13 publications

References 68 publications

GelMA-based bioactive hydrogel scaffolds with multiple bone defect repair functions: therapeutic strategies and recent advances

GelMA-based bioactive hydrogel scaffolds with multiple bone defect repair functions: therapeutic strategies and recent advances

Enhanced Bacterial Cuproptosis‐Like Death via Reversal of Hypoxia Microenvironment for Biofilm Infection Treatment

Implantable Multifunctional Micro‐Oxygen Reservoir System for Promoting Vascular‐Osteogenesis via Remodeling Regenerative Microenvironment

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