Biomimetic-smart materials for osteochondral regeneration and repair

Qi-Peng Jia , Qun-Feng Li , Hamza Boucetta , Zhi-Ping Xu , Ling-Xiao Zhang

Microstructures ›› 2024, Vol. 4 ›› Issue (3) : 2024026

PDF
Microstructures ›› 2024, Vol. 4 ›› Issue (3) :2024026 DOI: 10.20517/microstructures.2023.84
Review

Biomimetic-smart materials for osteochondral regeneration and repair

Author information +
History +
PDF

Abstract

Osteochondral injuries represent prevalent clinical conditions with profound implications for functional impairment and diminished quality of life. Despite the considerable potential of tissue engineering in osteochondral repair, substantial strides in clinical implementation remain elusive. Biomimetic materials, designed to emulate natural cartilage, offer a stabilized structure and microenvironment capable of accommodating the diverse properties inherent in different cartilage regions. Smart materials, endowed with the ability to deliver drugs, metal ions, and growth factors contingent on the disease progression, exert precise control over the microenvironment and cellular epigenetic behaviors. This review scrutinizes the nuanced characteristics of cartilage in both physiological and pathological states. Subsequently, a succinct overview of recent applications of biomaterials with bionic and smart attributes in osteochondral regeneration and repair is provided. Finally, we propose our perspectives on the application of biomimetic-smart materials in osteochondral regeneration and repair, emphasizing their potential clinical translation.

Keywords

Osteochondral defect / tissue engineering / biomimetic-smart materials / regeneration and repair

Cite this article

Download citation ▾
Qi-Peng Jia, Qun-Feng Li, Hamza Boucetta, Zhi-Ping Xu, Ling-Xiao Zhang. Biomimetic-smart materials for osteochondral regeneration and repair. Microstructures, 2024, 4(3): 2024026 DOI:10.20517/microstructures.2023.84

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Krishnan Y.Cartilage diseases.Matrix Biol2018;71-2:51-69 PMCID:PMC6146013

[2]

Catalano E.Biophysical and biomechanical properties of cartilage. arXiv 2023.

[3]

Guilak F.Biomechanical factors in osteoarthritis.Best Pract Res Clin Rheumatol2011;25:815-23 PMCID:PMC3266544

[4]

Cui A,Wang D,Chen Y.Global, regional prevalence, incidence and risk factors of knee osteoarthritis in population-based studies.EClinicalMedicine2020;29-30:100587 PMCID:PMC7704420

[5]

Nordberg RC,Wang D,Athanasiou KA.Navigating regulatory pathways for translation of biologic cartilage repair products.Sci Transl Med2022;14:eabp8163 PMCID:PMC9918326

[6]

van Middelkoop M,Atchia I.The OA trial bank: meta-analysis of individual patient data from knee and hip osteoarthritis trials show that patients with severe pain exhibit greater benefit from intra-articular glucocorticoids.Osteoarthritis Cartilage2016;24:1143-52

[7]

Mcalindon TE,Harvey WF.Effect of intra-articular triamcinolone vs saline on knee cartilage volume and pain in patients with knee osteoarthritis: a randomized clinical trial.JAMA2017;317:1967-75 PMCID:PMC5815012

[8]

Block JA.Osteoarthritis: OA guidelines: improving care or merely codifying practice?.Nat Rev Rheumatol2014;10:324-6

[9]

Evans CH,Setton LA.Progress in intra-articular therapy.Nat Rev Rheumatol2014;10:11-22 PMCID:PMC4402210

[10]

Yasui Y,Murawski CD.Operative treatment for osteochondral lesions of the talus: biologics and scaffold-based therapy.Cartilage2017;8:42-9 PMCID:PMC5154422

[11]

Zelinka A,Kandel RA.Cellular therapy and tissue engineering for cartilage repair.Osteoarthritis Cartilage2022;30:1547-60

[12]

Redondo ML,Yanke AB.Cartilage restoration: microfracture and osteochondral autograft transplantation.J Knee Surg2018;31:231-8

[13]

Pareek A,Maak TG,Stuart MJ.Long-term outcomes after osteochondral autograft transfer: a systematic review at mean follow-up of 10.2 years.Arthroscopy2016;32:1174-84

[14]

Inderhaug E.Osteochondral autograft transplant (mosaicplasty) for knee articular cartilage defects.JBJS Essent Surg Tech2019;9:e34.1-2 PMCID:PMC6974309

[15]

Krych AJ,Stuart MJ.Cartilage Injury in the knee: assessment and treatment options.J Am Acad Orthop Surg2020;28:914-22

[16]

Wei H,Lin K,Wang X.Recent advances in smart stimuli-responsive biomaterials for bone therapeutics and regeneration.Bone Res2022;10:17 PMCID:PMC8866424

[17]

Jin X,Zhao J.Bimetallic oxide Cu-Fe3O4 nanoclusters with multiple enzymatic activities for wound infection treatment and wound healing.Acta Biomater2024;173:403-19

[18]

Malta MD,Marques AP.Extracellular matrix in skin diseases: the road to new therapies.J Adv Res2023;51:149-60 PMCID:PMC10491993

[19]

Pfisterer K,Symmank D.The extracellular matrix in skin inflammation and infection.Front Cell Dev Biol2021;9:682414 PMCID:PMC8290172

[20]

Bouten CVC,Vermue IM,Passier R.Cardiovascular tissue engineering and regeneration: a plead for further knowledge convergence.Tissue Eng Part A2022;28:525-41

[21]

Lin X,Gao YG.The bone extracellular matrix in bone formation and regeneration.Front Pharmacol2020;11:757 PMCID:PMC7264100

[22]

Alford AI,Hankenson KD.Extracellular matrix networks in bone remodeling.Int J Biochem Cell Biol2015;65:20-31

[23]

Mansour A,Badran Z.*Extracellular matrices for bone regeneration: a literature review.Tissue Eng Part A2017;23:1436-51

[24]

Hao Y,Deng L.The first 3D-bioprinted personalized active bone to repair bone defects: a case report.Int J Biopaintion2022;9:654 PMCID:PMC10090529

[25]

Deng C,He H.3D bio-printed biphasic scaffolds with dual modification of silk fibroin for the integrated repair of osteochondral defects.Biomater Sci2021;9:4891-903

[26]

Liu G,Liu C.Cytomodulin-10 modified GelMA hydrogel with kartogenin for in-situ osteochondral regeneration.Acta Biomater2023;169:317-33

[27]

Ruan J,Cui H.A smart ROS/NIR dual-responsive melanin delivery platform for photoacoustic imaging-guided osteoarthritis therapy.Appl Mater Today2021;25:101216

[28]

Eming SA,Martin P.Inflammation and metabolism in tissue repair and regeneration.Science2017;356:1026-30

[29]

Wong SL,Martinod K.Diabetes primes neutrophils to undergo NETosis, which impairs wound healing.Nat Med2015;21:815-9 PMCID:PMC4631120

[30]

Knipper JA,Eming SA.Diabetes impedes the epigenetic switch of macrophages into repair mode.Immunity2019;51:199-201

[31]

Yang S,Ryu JH.Hypoxia-inducible factor-2alpha is a catabolic regulator of osteoarthritic cartilage destruction.Nat Med2010;16:687-93

[32]

Loeser RF.Molecular mechanisms of cartilage destruction: mechanics, inflammatory mediators, and aging collide.Arthritis Rheum2006;54:1357-60 PMCID:PMC1774815

[33]

Donell S.Subchondral bone remodelling in osteoarthritis.EFORT Open Rev2019;4:221-9 PMCID:PMC6549114

[34]

Jayasuriya CT,Liu W.The influence of tissue microenvironment on stem cell-based cartilage repair.Ann N Y Acad Sci2016;1383:21-33 PMCID:PMC5599120

[35]

Li M,Yan Z.The immune microenvironment in cartilage injury and repair.Acta Biomater2022;140:23-42

[36]

Huey DJ,Athanasiou KA.Unlike bone, cartilage regeneration remains elusive.Science2012;338:917-21 PMCID:PMC4327988

[37]

Ulrich-Vinther M,Schwarz EM,O'Keefe RJ.Articular cartilage biology.J Am Acad Orthop Surg2003;11:421-30

[38]

van der Kraan PM. The interaction between joint inflammation and cartilage repair.Tissue Eng Regen Med2019;16:327-34 PMCID:PMC6675839

[39]

Zhang S,Liu W.Articular cartilage regeneration: the role of endogenous mesenchymal stem/progenitor cell recruitment and migration.Semin Arthritis Rheu2020;50:198-208

[40]

Zhang H,Cui J.Maintaining hypoxia environment of subchondral bone alleviates osteoarthritis progression.Sci Adv2023;9:eabo7868 PMCID:PMC10075992

[41]

Monteagudo S.Cushioning the cartilage: a canonical Wnt restricting matter.Nat Rev Rheumatol2017;13:670-81

[42]

Xu W,Liu D.Roles of cartilage-resident stem/progenitor cells in cartilage physiology, development, repair and osteoarthritis.Cells2022;11:2305 PMCID:PMC9332847

[43]

Liu-Bryan R.Emerging regulators of the inflammatory process in osteoarthritis.Nat Rev Rheumatol2015;11:35-44 PMCID:PMC4374654

[44]

Qi K,Zhang Z.Tissue regeneration: the crosstalk between mesenchymal stem cells and immune response.Cell Immunol2018;326:86-93

[45]

Xiong Y,Lin Z.The role of the immune microenvironment in bone, cartilage, and soft tissue regeneration: from mechanism to therapeutic opportunity.Mil Med Res2022;9:65 PMCID:PMC9675067

[46]

Wu Y,Zeng Y.Exosomes rewire the cartilage microenvironment in osteoarthritis: from intercellular communication to therapeutic strategies.Int J Oral Sci2022;14:40 PMCID:PMC9352673

[47]

Jiang Y.Osteoarthritis year in review 2021: biology.Osteoarthritis Cartilage2022;30:207-15

[48]

Li M,Yan Z.The immune microenvironment in cartilage injury and repair.Acta Biomater2022;140:23-42

[49]

Silver IA,Etherington DJ.Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts.Exp Cell Res1988;175:266-76

[50]

Teitelbaum SL.Bone resorption by osteoclasts.Science2000;289:1504-8

[51]

Li R,Ma Y.A flexible and physically transient electrochemical sensor for real-time wireless nitric oxide monitoring.Nat Commun2020;11:3207 PMCID:PMC7316789

[52]

Zheng L,Sheng P.The role of metabolism in chondrocyte dysfunction and the progression of osteoarthritis.Ageing Res Rev2021;66:101249

[53]

Blanco FJ,Ruiz-Romero C.The role of mitochondria in osteoarthritis.Nat Rev Rheumatol2011;7:161-9

[54]

Terkeltaub R,Murphy A.Invited review: the mitochondrion in osteoarthritis.Mitochondrion2002;1:301-19

[55]

Bolduc JA,Loeser RF.Reactive oxygen species, aging and articular cartilage homeostasis.Free Radic Biol Med2019;132:73-82 PMCID:PMC6342625

[56]

Liang Q,Chen TS.Resveratrol protects rabbit articular chondrocyte against sodium nitroprusside-induced apoptosis via scavenging ROS.Apoptosis2014;19:1354-63

[57]

Lee HG.PCB126 induces apoptosis of chondrocytes via ROS-dependent pathways.Osteoarthritis Cartilage2012;20:1179-85

[58]

Gao Y,Huang J.The ECM-cell interaction of cartilage extracellular matrix on chondrocytes.Biomed Res Int2014;2014:648459 PMCID:PMC4052144

[59]

Guimarães CF,Marques AP.The stiffness of living tissues and its implications for tissue engineering.Nat Rev Mater2020;5:351-70

[60]

Smith LR,Discher DE.Stem cell differentiation is regulated by extracellular matrix mechanics.Physiology2018;33:16-25 PMCID:PMC5866410

[61]

Viswanathan P,Chirasatitsin S.3D surface topology guides stem cell adhesion and differentiation.Biomaterials2015;52:140-7 PMCID:PMC4379418

[62]

Kreeger PK,Masters KS.Engineering approaches to study cellular decision making.Annu Rev Biomed Eng2018;20:49-72 PMCID:PMC6327838

[63]

Fernandez-Yague MA,McNamara L,Pandit A.Biomimetic approaches in bone tissue engineering: integrating biological and physicomechanical strategies.Adv Drug Deliv Rev2015;84:1-29

[64]

Chen T,Tian J,Zheng H.A single integrated osteochondral in situ composite scaffold with a multi-layered functional structure.Colloids Surf B Biointerfaces2018;167:354-63

[65]

Wang Z,Wu F.A triphasic biomimetic BMSC-loaded scaffold for osteochondral integrated regeneration in rabbits and pigs.Biomater Sci2023;11:2924-34

[66]

Cao R,Ci Z.A biomimetic biphasic scaffold consisting of decellularized cartilage and decalcified bone matrixes for osteochondral defect repair.Front Cell Dev Biol2021;9:639006 PMCID:PMC7933472

[67]

Chen P,Zhu S.Radially oriented collagen scaffold with SDF-1 promotes osteochondral repair by facilitating cell homing.Biomaterials2015;39:114-23

[68]

Peng Y,Liu Y.Bioinspired gradient scaffolds for osteochondral tissue engineering.Exploration2023;3:20210043 PMCID:PMC10624381

[69]

Zhang W,Li D.The effect of interface microstructure on interfacial shear strength for osteochondral scaffolds based on biomimetic design and 3D printing.Mater Sci Eng C Mater Biol Appl2015;46:10-5

[70]

Harris JD,Brophy R,Carey J.Failures, re-operations, and complications after autologous chondrocyte implantation-a systematic review.Osteoarthritis Cartilage2011;19:779-91

[71]

Xu N,Qiang L.3D-printed composite bioceramic scaffolds for bone and cartilage integrated regeneration.ACS Omega2023;8:37918-26 PMCID:PMC10586016

[72]

Deng C,Li J.Bioactive scaffolds for regeneration of cartilage and subchondral bone interface.Theranostics2018;8:1940-55 PMCID:PMC5858510

[73]

Cao R,Xu Y.Development of Tri-layered biomimetic atelocollagen scaffolds with interfaces for osteochondral tissue engineering.Adv Healthc Mater2022;11:e2101643

[74]

Khetan S.Patterning hydrogels in three dimensions towards controlling cellular interactions.Soft Matter2011;7:830-8

[75]

Woodfield TB,Malda J.Combinatorial approaches to controlling cell behaviour and tissue formation in 3D via rapid-prototyping and smart scaffold design.Comb Chem High Throughput Screen2009;12:562-79

[76]

Lin S,Razafiarison T,Varghese S.Influence of physical properties of biomaterials on cellular behavior.Pharm Res2011;28:1422-30 PMCID:PMC3099000

[77]

Li X,Fan Y,Cui FZ.Nanostructured scaffolds for bone tissue engineering.J Biomed Mater Res A2013;101:2424-35

[78]

Wang C,Wang W.Strontium released bi-lineage scaffolds with immunomodulatory properties induce a pro-regenerative environment for osteochondral regeneration.Mater Sci Eng C Mater Biol Appl2019;103:109833

[79]

Lin R,Li X.Copper-incorporated bioactive glass-ceramics inducing anti-inflammatory phenotype and regeneration of cartilage/bone interface.Theranostics2019;9:6300-13 PMCID:PMC6735521

[80]

Xing M,Bi W.Strontium ions protect hearts against myocardial ischemia/reperfusion injury.Sci Adv2021;7:eabe0726 PMCID:PMC7810382

[81]

Li Y,Yan J.Tannic acid/Sr2+-coated silk/graphene oxide-based meniscus scaffold with anti-inflammatory and anti-ROS functions for cartilage protection and delaying osteoarthritis.Acta Biomater2021;126:119-31

[82]

Pan Z,Liu X.Effect of porosities of bilayered porous scaffolds on spontaneous osteochondral repair in cartilage tissue engineering.Regen Biomater2015;2:9-19 PMCID:PMC4669027

[83]

Li J,Hou W.The response of host blood vessels to graded distribution of macro-pores size in the process of ectopic osteogenesis.Mater Sci Eng C Mater Biol Appl2020;109:110641

[84]

Melica ME,Parri M,Romagnani P.Substrate stiffness modulates renal progenitor cell properties via a ROCK-mediated mechanotransduction mechanism.Cells2019;8:1561 PMCID:PMC6953094

[85]

Rufaihah AJ,Mazlan MDM.The effect of scaffold modulus on the morphology and remodeling of fetal mesenchymal stem cells.Front Physiol2018;9:1555 PMCID:PMC6308149

[86]

Murphy CM,Haugh MG,O'Brien FJ.Mesenchymal stem cell fate is regulated by the composition and mechanical properties of collagen-glycosaminoglycan scaffolds.J Mech Behav Biomed Mater2012;11:53-62

[87]

Hong Y,Wu J.Chitosan modified Fe3O4/KGN self-assembled nanoprobes for osteochondral MR diagnose and regeneration.Theranostics2020;10:5565-77 PMCID:PMC7196312

[88]

Przekora A.Current Trends in fabrication of biomaterials for bone and cartilage regeneration: materials modifications and biophysical stimulations.Int J Mol Sci2019;20:435 PMCID:PMC6359292

[89]

Malinauskas M,Aukstikalne L.Cartilage regeneration using improved surface electrospun bilayer polycaprolactone scaffolds loaded with transforming growth factor-beta 3 and rabbit muscle-derived stem cells.Front Bioeng Biotechnol2022;10:971294 PMCID:PMC9445302

[90]

Zhou S,Wei J.Mussel-inspired injectable chitosan hydrogel modified with catechol for cell adhesion and cartilage defect repair.J Mater Chem B2022;10:1019-30

[91]

Wang W,Ambler WS.Enhancing the hydrophilicity and cell attachment of 3D printed PCL/graphene scaffolds for bone tissue engineering.Materials2016;9:992 PMCID:PMC5456956

[92]

Hasani-Sadrabadi MM,Pouraghaei S.An engineered cell-laden adhesive hydrogel promotes craniofacial bone tissue regeneration in rats.Sci Transl Med2020;12:eaay6853.

[93]

O'Connor SK,Oswald SJ,Guilak F.Formation of osteochondral organoids from murine induced pluripotent stem cells.Tissue Eng Part A2021;27:1099-109 PMCID:PMC8392116

[94]

Li ZA,Xiang S.Articular tissue-mimicking organoids derived from mesenchymal stem cells and induced pluripotent stem cells.Organoids2022;1:135-48

[95]

Zeng D,Liao Z.Cartilage organoids and osteoarthritis research: a narrative review.Front Bioeng Biotechnol2023;11:1278692 PMCID:PMC10666186

[96]

Crispim JF.De novo neo-hyaline-cartilage from bovine organoids in viscoelastic hydrogels.Acta Biomater2021;128:236-49

[97]

Abe K,Morioka M.Engraftment of allogeneic iPS cell-derived cartilage organoid in a primate model of articular cartilage defect.Nat Commun2023;14:804 PMCID:PMC9941131

[98]

Yang Z,Liu W.In situ self-assembled organoid for osteochondral tissue regeneration with dual functional units.Bioact Mater2023;27:200-15 PMCID:PMC10121637

[99]

Barui S,Laurencin CT.Osteochondral regenerative engineering: challenges, state-of-the-art and translational perspectives.Regen Biomater2023;10:rbac109 PMCID:PMC9845524

[100]

Sarsenova M,Issabekova A.Regeneration of osteochondral defects by combined delivery of synovium-derived mesenchymal stem cells, TGF-β1 and BMP-4 in heparin-conjugated fibrin hydrogel.Polymers2022;14:5343 PMCID:PMC9780905

[101]

Jiang Q.Stimulus-responsive drug delivery nanoplatforms for osteoarthritis therapy.Small2023;19:e2206929

[102]

Zou F,Ma M.Synergistic strategy constructed novel double-network scaffolds with active micro-environment pH stabilization and M2-macrophage polarization for cartilage defect repair.Compos Part B Eng2023;258:110709

[103]

Liu Z,Yu H.Near-infrared light-controlled kartogenin delivery of multifunctional Prussian blue nanocomposites for cartilage defect repair.Nanoscale2023;15:9076-93

[104]

Lin T,Wu M,Yeh M.A bilineage thermosensitive hydrogel system for stimulation of mesenchymal stem cell differentiation and enhancement of osteochondral regeneration.Compos Part B Eng2022;233:109614

[105]

Ji X,Li X.Injectable immunomodulation-based porous chitosan microspheres/HPCH hydrogel composites as a controlled drug delivery system for osteochondral regeneration.Biomaterials2022;285:121530

[106]

Yu H,Kong X.Nanoarchitectonics of cartilage-targeting hydrogel microspheres with reactive oxygen species responsiveness for the repair of osteoarthritis.ACS Appl Mater Interfaces2022;14:40711-23

[107]

Liu Y,Le TT.Exercise-induced piezoelectric stimulation for cartilage regeneration in rabbits.Science Transl Med2022;14:eabi7282

[108]

Vinikoor T,Le TT.Injectable and biodegradable piezoelectric hydrogel for osteoarthritis treatment.Nat Commun2023;14:6257 PMCID:PMC10558537

[109]

Wu S,Wang S.Ultrasound-triggered in situ gelation with ROS-controlled drug release for cartilage repair.Mater Horiz2023;10:3507-22

[110]

Gao C,Wang X.Magnesium gradient‐based hierarchical scaffold for dual-lineage regeneration of osteochondral defect.Adv Funct Mater2023;33:2304829

[111]

Khader A.Biodegradable zinc oxide composite scaffolds promote osteochondral differentiation of mesenchymal stem cells.Biotechnol Bioeng2020;117:194-209

[112]

Shu C,Chen L.Metal-organic framework functionalized bioceramic scaffolds with antioxidative activity for enhanced osteochondral regeneration.Adv Sci2023;10:e2206875 PMCID:PMC10161093

[113]

Chasapis CT,Spiliopoulou CA.Recent aspects of the effects of zinc on human health.Arch Toxicol2020;94:1443-60

[114]

Sun Y,Zhu Y.Tunable and controlled release of cobalt ions from metal-organic framework hydrogel nanocomposites enhances bone regeneration.ACS Appl Mater Interfaces2021;13:59051-66

[115]

Deng C,Sun X.Bioactive scaffolds with Li and Si ions-synergistic effects for osteochondral defects regeneration.Appl Mater Today2018;10:203-16

[116]

Pirmohamed T,Singh S.Nanoceria exhibit redox state-dependent catalase mimetic activity.Chem Commun2010;46:2736-8 PMCID:PMC3038687

[117]

Lu M,Ren G.Superoxide-like Cu/GO single-atom catalysts nanozyme with high specificity and activity for removing superoxide free radicals.Nano Res2022;15:8804-9

[118]

Komkova MA,Karyakin AA.Catalytically synthesized prussian blue nanoparticles defeating natural enzyme peroxidase.J Am Chem Soc2018;140:11302-7

[119]

Kumar S,Brown SB,Sharma B.Manganese dioxide nanoparticles protect cartilage from inflammation-induced oxidative stress.Biomaterials2019;224:119467 PMCID:PMC7025913

[120]

Cao Z,Chen J.Silk-based hydrogel incorporated with metal-organic framework nanozymes for enhanced osteochondral regeneration.Bioact Mater2023;20:221-42 PMCID:PMC9163388

[121]

Liu C,Wang J.Facile preparation of homogeneous copper nanoclusters exhibiting excellent tetraenzyme mimetic activities for colorimetric glutathione sensing and fluorimetric ascorbic acid sensing.ACS Appl Mater Interfaces2020;12:42521-30

[122]

Wu T,Yang H.Bimetal biomimetic engineering utilizing metal-organic frameworks for superoxide dismutase mimic.ACS Mater Lett2022;4:751-7

[123]

Liu X,Xuan C.A biomimetic biphasic osteochondral scaffold with layer-specific release of stem cell differentiation inducers for the reconstruction of osteochondral defects.Adv Healthc Mater2020;9:e2000076

[124]

Zheng L,Wang W.Bilayered scaffold prepared from a kartogenin-loaded hydrogel and BMP-2-derived peptide-loaded porous nanofibrous scaffold for osteochondral defect repair.ACS Biomater Sci Eng2019;5:4564-73

AI Summary AI Mindmap
PDF

117

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/