Elimination of methicillin-resistant
Staphylococcus aureus biofilms on titanium implantsvia photo-thermally-triggered nitric oxide and immunotherapy for enhanced osseointegrationElimination of methicillin-resistant
Staphylococcus aureus biofilms on titanium implantsvia photo-thermally-triggered nitric oxide and immunotherapy for enhanced osseointegration- MMR 2024年11卷第2期 页码：157-179
- Affiliations：
1.Department of Pathology, Affiliated Hospital of Zunyi Medical University, Zunyi 563003, Guizhou, China
2.Laboratory Research Center, the First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China
3.Department of Blood Transfusion, Laboratory of Radiation Biology, the Second Affiliated Hospital, Army Military Medical University, Chongqing 400037, China
4.Department of Reproductive Endocrinology, Chongqing Health Center for Women and Children, Chongqing 401147, China
5.The Graduate School, Augusta University, Augusta, GA 30912, USA
6.Department of Stomatology, the Seventh Medical Center of PLA General Hospital, Beijing 100700, China
- Author bio：
*yuyonglin@zmu.edu.cn
kiki-happy@263.net
taobailong@hospital.cqmu.edu.cn
jiaoyang1989731@163.com
- Funds：the National Natural Science Foundation of China(82101069;82102537;82160411;82002278);the Natural Science Foundation of Chongqing Science and Technology Commission(CSTC2021JCYJ-MSXMX0170;CSTB2022BSXM-JCX0039);the First Affiliated Hospital of Chongqing Medical University Cultivating Fund(PYJJ2021-02);the Beijing Municipal Science & Technology Commission(Z221100007422130);the Youth Incubation Program of Medical Science and Technology of PLA(21QNPY116)
DOI：10.1186/s40779-023-00454-y
中图分类号：-
纸质出版：2024-04
- Accepted：
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Elimination of methicillin-resistant
Staphylococcus aureus biofilms on titanium implantsvia photo-thermally-triggered nitric oxide and immunotherapy for enhanced osseointegration[J]. MMR, 2024,11(2):157-179.Cite this article as: Yu YL, Wu JJ, Lin CC, Qin X, Tay FR, Miao L, et al. Elimination of methicillin-resistant Staphylococcus aureus biofilms on titanium implants via photothermally-triggered nitric oxide and immunotherapy for enhanced osseointegration. Mil Med Res. 2023;10(1):21.
Elimination of methicillin-resistant
Staphylococcus aureus biofilms on titanium implantsvia photo-thermally-triggered nitric oxide and immunotherapy for enhanced osseointegration[J]. MMR, 2024,11(2):157-179. DOI： 10.1186/s40779-023-00454-y.Cite this article as: Yu YL, Wu JJ, Lin CC, Qin X, Tay FR, Miao L, et al. Elimination of methicillin-resistant Staphylococcus aureus biofilms on titanium implants via photothermally-triggered nitric oxide and immunotherapy for enhanced osseointegration. Mil Med Res. 2023;10(1):21. DOI： 10.1186/s40779-023-00454-y.
摘要
Abstract
Background:
2
Treatment of methicillin-resistant Staphylococcus aureus (MRSA) biofilm infections in implant placement surgery is limited by the lack of antimicrobial activity of titanium (Ti) implants. There is a need to explore more effective approaches for the treatment of MRSA biofilm infections.
Methods:
2
Herein
an interfacial functionalization strategy is proposed by the integration of mesoporous polydopamine nanoparticles (PDA)
nitric oxide (NO) release donor sodium nitroprusside (SNP) and osteogenic growth peptide (OGP) onto Ti implants
denoted as Ti-PDA@SNP-OGP. The physical and chemical properties of Ti-PDA@SNP-OGP were assessed by scanning electron microscopy
X-ray photoelectron spectroscope
water contact angle
photothermal property and NO release behavior. The synergistic antibacterial effect and elimination of the MRSA biofilms were evaluated by 2′
7′-dichlorofluorescein diacetate probe
1-N-phenylnaphthylamine assay
adenosine triphosphate intensity
O-nitrophenyl-β-D-galactopyranoside hydrolysis activity
bicinchoninic acid leakage. Fluorescence staining
assays for alkaline phosphatase activity
collagen secretion and extracellular matrix mineralization
quantitative real-time reverse transcription-polymerase chain reaction
and enzyme-linked immunosorbent assay (ELISA) were used to evaluate the inflammatory response and osteogenic ability in bone marrow stromal cells (MSCs)
RAW264.7 cells and their co-culture system. Giemsa staining
ELISA
micro-CT
hematoxylin and eosin
Masson's trichrome and immunohistochemistry staining were used to evaluate the eradication of MRSA biofilms
inhibition of inflammatory response
and promotion of osseointegration of Ti-PDA@SNP-OGP in vivo.
Results:
2
Ti-PDA@SNP-OGP displayed a synergistic photothermal and NO-dependent antibacterial effect against MRSA following near-infrared light (NIR) irradiation
and effectively eliminated the formed MRSA biofilms by inducing reactive oxygen species (ROS)-mediated oxidative stress
destroying bacterial membrane integrity and causing leakage of intracellular components (
P
<
0.01). In vitro experiments revealed that Ti-PDA@SNP-OGP not only facilitated osteogenic differentiation of MSCs
but also promoted the polarization of pro-inflammatory M1 macrophages to the anti-inflammatory M2-phenotype (
P
<
0.05 or
P
<
0.01). The favorable osteo-immune microenvironment further facilitated osteogenesis of MSCs and the anti-inflammation of RAW264.7 cells via multiple paracrine signaling pathways (
P
<
0.01). In vivo evaluation confirmed the aforementioned results and revealed that Ti-PDA@SNP-OGP induced ameliorative osseointegration in an MRSA-infected femoral defect implantation model (
P
<
0.01).
Conclusions:
2
Ti-PDA@SNP-OGP is a promising multi-functional material for the high-efficient treatment of MRSA infections in implant replacement surgeries.
关键词
Keywords
references
Jiao Y , Niu LN , Ma S , Li J , Tay FR , Chen JH . Quaternary ammonium-based biomedical materials: state-of-the-art, toxicological aspects and antimicrobial resistance . Prog Polym Sci . 2017 ; 71 : 53 – 90 .
Zhao Q , Wu J , Li Y , Xu R , Zhu X , Jiao Y , et al . Promotion of bone formation and antibacterial properties of titanium coated with porous Si/Ag-doped titanium dioxide . Front Bioeng Biotechnol . 2022 ; 10 : 1001514 .
Zhang QY , Yan ZB , Meng YM , Hong XY , Shao G , Ma JJ , et al . Antimicrobial peptides: mechanism of action, activity and clinical potential . Mil Med Res . 2021 ; 8 ( 1 ): 48 .
Yang J , Wang C , Liu X , Yin Y , Ma YH , Gao Y , et al . Gallium-carbenicillin framework coated defect-rich hollow TiO 2 as a photocatalyzed oxidative stress amplifier against complex infections . Adv Funct Mater . 2020 ; 30 ( 43 ): 2004861 .
Jiao D , Yang S . Overcoming resistance to drugs targeting KRASG12C mutation . Innovation (Camb) . 2020 ; 1 ( 2 ): 100035 .
Baker S , Thomson N , Weill FX , Holt KE . Genomic insights into the emergence and spread of antimicrobial-resistant bacterial pathogens . Science . 2018 ; 360 ( 6390 ): 733 – 8 .
Makvandi P , Song H , Yiu CKY , Sartorius R , Zare EN , Rabiee N , et al . Bioengineered materials with selective antimicrobial toxicity in biomedicine . Mil Med Res . 2023 ; 10 ( 1 ): 8 .
Li Y , Liu XM , Li B , Zheng YF , Han Y , Chen DF , et al . Near-infrared light triggered phototherapy and immunotherapy for elimination of methicillinresistant Staphylococcus aureus biofilm infection on bone implant . ACS Nano . 2020 ; 14 ( 7 ): 8157 – 70 .
Zhao QM , Li B , Yu FX , Li YK , Wu JS , Peng Z , et al . Cu-Co co-doped microporous coating on titanium with osteogenic and antibacterial properties . J Biomed Nanotechnol . 2021 ; 17 ( 7 ): 1435 – 47 .
Han D , Li Y , Liu X , Yeung KWK , Zheng Y , Cui Z , et al . Photothermy-strengthened photocatalytic activity of polydopamine-modified metal-organic frameworks for rapid therapy of bacteria-infected wounds . J Mater Sci Technol . 2021 ; 62 : 83 – 95 .
Jiao Y , Tay FR , Niu LN , Chen JH . Advancing antimicrobial strategies for managing oral biofilm infections . Int J Oral Sci . 2019 ; 11 ( 3 ): 28 .
Huo J , Jia Q , Huang H , Zhang J , Li P , Dong X , et al . Emerging photothermal-derived multimodal synergistic therapy in combating bacterial infections . Chem Soc Rev . 2021 ; 50 ( 15 ): 8762 – 89 .
Jiao Y , Wang X , Chen JH . Biofabrication of AuNPs using Coriandrum sativum leaf extract and their antioxidant, analgesic activity . Sci Total Environ . 2021 ; 767 : 144914 .
Ma T , Zhai X , Jin M , Huang Y , Zhang M , Pan H , et al . Multifunctional wound dressing for highly efficient treatment of chronic diabetic wounds . View . 2022 ; 3 ( 6 ): 20220045 .
Xiao J , Hai L , Li Y , Li H , Gong M , Wang Z , et al . An ultrasmall Fe 3 O 4 - decorated polydopamine hybrid nanozyme enables continuous conversion of oxygen into toxic hydroxyl radical via GSH-depleted cascade redox reactions for intensive wound disinfection . Small . 2022 ; 18 ( 9 ): 2105465 .
Liang Y , Xu H , Li Z , Zhangji A , Guo B . Bioinspired injectable self-healing hydrogel sealant with fault-tolerant and repeated thermo-responsive adhesion for sutureless post-wound-closure and wound healing . Nanomicro Lett . 2022 ; 14 ( 1 ): 185 .
Yuan Z , Tao B , He Y , Liu J , Lin C , Shen X , et al . Biocompatible MoS2/PDARGD coating on titanium implant with antibacterial property via intrinsic ROS-independent oxidative stress and NIR irradiation . Biomaterials . 2019 ; 217 : 119290 .
Zheng Y , Cao T , Han X , Cao P , Zhan Q . Structurally diverse polydopamine-based nanomedicines for cancer therapy . Acta Mater Med . 2022 ; 1 ( 4 ): 427 – 44 .
Cheng S , Ke J , Yao M , Shao H , Zhou J , Wang M , et al . Improved osteointegration and angiogenesis of strontium-incorporated 3D-printed tantalum scaffold via bioinspired polydopamine coating . J Mater Sci Technol . 2021 ; 69 : 106 – 18 .
Yuan Z , Tao B , He Y , Mu C , Liu G , Zhang J , et al . Remote eradication of biofilm on titanium implant via near-infrared light triggered photothermal/photodynamic therapy strategy . Biomaterials . 2019 ; 223 : 119479 .
Tao B , Lin C , Yuan Z , He Y , Chen M , Li K , et al . Near infrared light-triggered on-demand Cur release from Gel-PDA@Cur composite hydrogel for antibacterial wound healing . Chem Eng J . 2021 ; 403 : 126182 .
Li D , Wang D , He Y , Tao B , Liu X , Yang Y , et al . A HAase/NIR responsive surface on titanium implants for treating bacterial infection and improving osseointegration . J Mater Sci Technol . 2023 ; 143 : 93 – 106 .
Yuan Z , Lin C , He Y , Tao B , Chen M , Zhang J , et al . Near-infrared light-triggered nitric-oxide-enhanced photodynamic therapy and low-temperature photothermal therapy for biofilm elimination . ACS Nano . 2020 ; 14 ( 3 ): 3546 – 62 .
Hu D , Li H , Wang B , Ye Z , Lei W , Jia F , et al . Surface-adaptive gold nanoparticles with effective adherence and enhanced photothermal ablation of methicillin-resistant Staphylococcus aureus biofilm . ACS Nano . 2017 ; 11 ( 9 ): 9330 – 9 .
Li J , Liu X , Tan L , Cui Z , Yang X , Liang Y , et al . Zinc-doped Prussian blue enhances photothermal clearance of Staphylococcus aureus and promotes tissue repair in infected wounds . Nat Commun . 2019 ; 10 ( 1 ): 4490 .
Fan W , Lu N , Huang P , Liu Y , Yang Z , Wang S , et al . Glucose-responsive sequential generation of hydrogen peroxide and nitric oxide for synergistic cancer starving-like gas therapy . Angew Chem Int Ed Engl . 2017 ; 56 ( 5 ): 1229 – 33 .
Li S , Liu R , Jiang X , Qiu Y , Song X , Huang GM , et al . Near-infrared light-triggered sulfur dioxide gas therapy of cancer . ACS Nano. 2019 ; 13 ( 2 ): 2103 – 13 .
Opoku-Damoah Y , Zhang R , Ta HT , Xu ZP . Therapeutic gas-releasing nanomedicines with controlled release: advances and perspectives . Exploration . 2022 ; 2 ( 5 ): 20210181 .
Zhang W , Zhou Y , Fan Y , Cao R , Xu Y , Weng Z , et al . Metal-organic-framework-based hydrogen-release platform for multieffective Helicobacter pylori targeting therapy and intestinal flora protective capabilities . Adv Mater . 2022 ; 34 ( 2 ): 2105738 .
Yuan Z , Lin C , Dai L , He Y , Hu J , Xu K , et al . Near-infrared light-activatable dual-action nanoparticle combats the established biofilms of methicillinresistant Staphylococcus aureus and its accompanying inflammation . Small . 2021 ; 17 ( 13 ): e2007522 .
Zhang S , Guan K , Zhang Y , Zhang J , Hongyu F , Ting W , Ouyang D , Liu C , Qiang W , Chen Z . A self-activated NO-releasing hydrogel depot for photothermal enhanced sterilization . Nano Res . 2022 . https://doi.org/10.1007/s12274-022-5239-9.
Ding X , Tang Q , Xu Z , Xu Y , Zhang H , Zheng D , et al . Challenges and innovations in treating chronic and acute wound infections: from basic science to clinical practice . Burns Trauma . 2022 . https://doi.org/10.1093/burnst/tkac014.
Guo QL , Dai XL , Yin MY , Cheng HW , Qian HS , Wang H , et al . Nanosensitizers for sonodynamic therapy for glioblastoma multiforme: current progress and future perspectives . Mil Med Res . 2022 ; 9 ( 1 ): 26 .
Yao X , Yang B , Xu J , He Q , Yang W . Novel gas-based nanomedicines for cancer therapy . View . 2022 ; 3 ( 1 ): 20200185 .
Gehring J , Trepka B , Klinkenberg N , Bronner H , Schleheck D , Polarz S . Sunlight-triggered nanoparticle synergy: teamwork of reactive oxygen species and nitric oxide released from mesoporous organosilica with advanced antibacterial activity . J Am Chem Soc . 2016 ; 138 ( 9 ): 3076 – 84 .
Hossain S , Nisbett LM , Boon EM . Discovery of two bacterial nitric oxide-responsive proteins and their roles in bacterial biofilm regulation . Acc Chem Res . 2017 ; 50 ( 7 ): 1633 – 9 .
Zhang G , Wu Z , Yang Y , Shi J , Lv J , Fang Y , et al . A multifunctional antibacterial coating on bone implants for osteosarcoma therapy and enhanced osteointegration . Chem Eng J . 2022 ; 428 : 131155 .
Qi M , Ren X , Li W , Sun Y , Sun X , Li C , et al . NIR responsive nitric oxide nanogenerator for enhanced biofilm eradication and inflammation immunotherapy against periodontal diseases . Nano Today . 2022 ; 43 : 101447 .
Beurton J , Boudier A , Seabra AB , Vrana NE , Clarot I , Lavalle P . Nitric oxide delivering surfaces: an overview of functionalization strategies and efficiency progress . Adv Healthc Mater . 2022 ; 11 ( 13 ): e2102692 .
Wu Y , Deng G , Jiang K , Wang H , Song Z , Han H . Photothermally triggered nitric oxide nanogenerator targeting type IV pili for precise therapy of bacterial infections . Biomaterials . 2021 ; 268 : 120588 .
Chen W , Xie G , Lu Y , Wang J , Feng B , Wang Q , et al . An improved osseointegration of metal implants by pitavastatin loaded multilayer films with osteogenic and angiogenic properties . Biomaterials . 2022 ; 280 : 121260 .
Tao B , Lin C , He Y , Yuan Z , Chen M , Xu K , et al . Osteo-immunomodulation mediating improved osteointegration by OGP-loaded cobalt-metal organic framework on titanium implants with antibacterial property . Chem Eng J . 2021 ; 423 : 130176 .
Liu H , Jiao Y , Zhou W , Bai S , Feng Z , Dong Y , et al . Endothelial progenitor cells improve the therapeutic effect of mesenchymal stem cell sheets on irradiated bone defect repair in a rat model . J Transl Med . 2018 ; 16 ( 1 ): 137 .
Bai J , Wang H , Chen H , Ge G , Wang M , Gao A , et al . Biomimetic osteogenic peptide with mussel adhesion and osteoimmunomodulatory functions to ameliorate interfacial osseointegration under chronic inflammation . Biomaterials . 2020 ; 255 : 120197 .
Tao B , Zhao W , Lin C , Yuan Z , He Y , Lu L , et al . Surface modification of titanium implants by ZIF-8@Levo/LBL coating for inhibition of bacterial-associated infection and enhancement of in vivo osseointegration . Chem Eng J . 2020 ; 390 : 124621 .
Shen X , Zhang Y , Ma P , Sutrisno L , Luo Z , Hu Y , et al . Fabrication of magnesium/zinc-metal organic framework on titanium implants to inhibit bacterial infection and promote bone regeneration . Biomaterials . 2019 ; 212 : 1 – 16 .
Cao B , Xiao F , Xing D , Hu X . Polyprodrug antimicrobials: remarkable membrane damage and concurrent drug release to combat antibiotic resistance of methicillin-resistant Staphylococcus aureus . Small . 2018 ; 14 ( 41 ): 1802008 .
Yu Y , Li P , Zhu C , Ning N , Zhang S , Vancso GJ . Multifunctional and recyclable photothermally responsive cryogels as efficient platforms for wound healing . Adv Funct Mater . 2019 ; 29 ( 35 ): 1904402 .
Han D , Li Y , Liu X , Li B , Han Y , Zheng Y , et al . Rapid bacteria trapping and killing of metal-organic frameworks strengthened photo-responsive hydrogel for rapid tissue repair of bacterial infected wounds . Chem Eng J . 2020 ; 396 : 125194 .
Han D , Liu X , Wu S . Metal organic framework-based antibacterial agents and their underlying mechanisms . Chem Soc Rev . 2022 ; 51 ( 16 ): 7138 – 69 .
Gong C , Guan W , Liu X , Zheng Y , Li Z , Zhang Y , et al . Biomimetic bacteriophage-like particles formed from probiotic extracts and NO donors for eradicating multidrug-resistant Staphylococcus aureus . Adv Mater . 2022 ; 34 ( 45 ): e2206134 .
Guan W , Tan L , Liu X , Cui Z , Zheng Y , Yeung KWK , et al . Ultrasonic interfacial engineering of red phosphorous-metal for eradicating MRSA infection effectively . Adv Mater . 2021 ; 33 ( 5 ): e2006047 .
Zhou J , Zhang Z , Joseph J , Zhang X , Ferdows BE , Patel DN , et al . Biomaterials and nanomedicine for bone regeneration: progress and future prospects . Exploration . 2021 ; 1 ( 2 ): 20210011 .
Yang L , Liu Y , Sun L , Zhao C , Chen G , Zhao Y . Biomass microcapsules with stem cell encapsulation for bone repair . Nanomicro Lett . 2021 ; 14 ( 1 ): 4 .
Liu Q , Wen Y , Qiu J , Zhang Z , Jin Z , Cao M , et al . Local SDF-1α application enhances the therapeutic efficacy of BMSCs transplantation in osteoporotic bone healing . Heliyon . 2020 ; 6 ( 6 ): e04347 .
Yu F , Geng D , Kuang Z , Huang S , Cheng Y , Chen Y , et al . Sequentially releasing self-healing hydrogel fabricated with TGFβ3-microspheres and bFGF to facilitate rat alveolar bone defect repair . Asian J Pharm Sci . 2022 ; 17 ( 3 ): 425 – 34 .
Zhao Q , Shi M , Yin C , Zhao Z , Zhang J , Wang J , et al . Dual-wavelength photosensitive nano-in-micro scaffold regulates innate and adaptive immune responses for osteogenesis . Nanomicro Lett . 2020 ; 13 ( 1 ): 28 .
Amini-Nik S , Abdullahi A , Vinaik R , Yao RJR , Yu N , Datu A , et al . Aging impairs the cellular interplay between myeloid cells and mesenchymal cells during skin healing in mice . Aging Dis . 2022 ; 13 ( 2 ): 540 – 51 .
Yuan Z , Wu J , Fu Z , Meng S , Dai LL , Cai K . Polydopamine-mediated interfacial functionalization of implants for accelerating infected bone repair through light-activatable antibiosis and carbon monoxide gas regulated macrophage polarization . Adv Funct Mater . 2022 ; 32 ( 27 ): 2200374 .
Jiao Y , Liu Q , Chen J . Construction of N-halamine biocompatible multilayers onto BMP2 loaded titanium nanotubes for bacterial infection inhibition and osteogenic effect improvement . Mater Lett . 2020 ; 267 : 127526 .
Feng Y , Zhang R , Wang YR , Chen F , Luo Q , Cai C , et al . Inhibition of endoplasmic reticulum stress by 4-phenyl butyric acid presents therapeutic effects on periodontitis: experimental studies in vitro and in rats . Stem Cells Int . 2021 ; 2021 : 6618943 .
Wu J , Shen P , Qin X , Yang L , Lin C , Li X , et al . Self-supply of H 2 O 2 and O 2 by a composite nanogenerator for chemodynamic therapy/hypoxia improvement and rapid therapy of biofilm-infected wounds . Chem Eng J . 2023 ; 459 : 141507 .
Pajarinen J , Lin T , Gibon E , Kohno Y , Maruyama M , Nathan K , et al . Mesenchymal stem cell-macrophage crosstalk and bone healing . Biomaterials . 2019 ; 196 : 80 – 9 .
Sun J , Huang Y , Zhao H , Niu J , Ling X , Zhu C , et al . Bio-clickable musselinspired peptides improve titanium-based material osseointegration synergistically with immunopolarization-regulation . Bioact Mater . 2021 ; 9 : 1 – 14 .
Dai H , Fan Q , Wang C . Recent applications of immunomodulatory biomaterials for disease immunotherapy . Exploration . 2022 ; 2 ( 6 ): 20210157 .
Shen P , Chen Y , Luo S , Fan Z , Wang J , Chang J , et al . Applications of biomaterials for immunosuppression in tissue repair and regeneration . Acta Biomater . 2021 ; 126 : 31 – 44 .
Xie L , Wang G , Wu Y , Liao Q , Mo S , Ren X , et al . Programmed surface on poly(aryl-ether-ether-ketone) initiating immune mediation and fulfilling bone regeneration sequentially . Innovation . 2021 ; 2 ( 3 ): 100148 .
Ding Y , Tao B , Ma R , Zhao X , Liu P , Cai K . Surface modification of titanium implant for repairing/improving microenvironment of bone injury and promoting osseointegration . J Mater Sci Technol . 2023 ; 143 : 1 – 11 .
Huyer LD , Pascual-Gil S , Wang Y , Mandla S , Yee B , Radisic M . Advanced strategies for modulation of the material-macrophage interface . Adv Funct Mater . 2020 ; 30 ( 44 ): 1909331 .
Wang Y , Li C , Wan Y , Qi M , Chen Q , Sun Y , et al . Quercetin-loaded ceria nanocomposite potentiate dual-directional immunoregulation via macrophage polarization against periodontal inflammation . Small . 2021 ; 17 ( 41 ): e2101505 .
Zhang J , Tong D , Song H , Ruan R , Sun Y , Lin Y , et al . Osteoimmunity-regulating biomimetically hierarchical scaffold for augmented bone regeneration . Adv Mater . 2022 ; 34 ( 36 ): e2202044 .
Xiong Y , Mi BB , Lin Z , Hu YQ , Yu L , Zha KK , et al . The role of the immune microenvironment in bone, cartilage, and soft tissue regeneration: from mechanism to therapeutic opportunity . Mil Med Res . 2022 ; 9 ( 1 ): 65 .
Wang T , Bai J , Lu M , Huang C , Geng D , Chen G , et al . Engineering immunomodulatory and osteoinductive implant surfaces via mussel adhesion-mediated ion coordination and molecular clicking . Nat Commun . 2022 ; 13 ( 1 ): 160 .
Luo ML , Jiao Y , Gong WP , Li Y , Niu LN , Tay FR , et al . Macrophages enhance mesenchymal stem cell osteogenesis via down-regulation of reactive oxygen species . J Dent . 2020 ; 94 : 103297 .
Tao B , Yi W , Qian X , Wu J , Li K , Guo A , et al . Improvement of antibacterial, anti-inflammatory, and osteogenic properties of OGP loaded Co-MOF coating on titanium implants for advanced osseointegration . J Mater Sci Technol . 2023 ; 146 : 131 – 44 .
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