Development of three-layer collagen scaffolds to spatially direct tissue-specific cell differentiation for enthesis repair

Thomopoulos, 2010, The development and morphogenesis of the tendon-to-bone insertion - what development can teach us about healing, J. Musculoskelet. Neuronal Interact., 10, 35 Lu, 2013, Functional attachment of soft tissues to bone: development, healing, and tissue engineering, Annu. Rev. Biomed. Eng., 15, 201, 10.1146/annurev-bioeng-071910-124656 Patel, 2018, Integrating soft and hard tissues via interface tissue engineering, J. Orthop. Res., 36, 1069, 10.1002/jor.23810 Kuntz, 2018, Biomarkers for tissue engineering of the tendon-bone interface, PLoS One, 13, 10.1371/journal.pone.0189668 Angeline, 2012, Biologics in the management of rotator cuff surgery, Clin. Sports Med., 31, 645, 10.1016/j.csm.2012.07.003 Chen, 2022, Engineering an enthesis-like graft for rotator cuff repair: an approach to fabricate highly biomimetic scaffold capable of zone-specifically releasing stem cell differentiation inducers, Bioact. Mater., 16, 451, 10.1016/j.bioactmat.2021.12.021 Bunker, 2014, Tendon to bone healing and its implications for surgery, Muscles Ligaments Tendons J, 4, 343, 10.32098/mltj.03.2014.13 Ratcliffe, 2015, Scaffolds for tendon and ligament repair and regeneration, Ann. Biomed. Eng., 43, 819, 10.1007/s10439-015-1263-1 Nau, 2015, Regeneration of the anterior cruciate ligament: current strategies in tissue engineering, World J. Orthoped., 6, 127, 10.5312/wjo.v6.i1.127 Wang, 2013, Bioreactor design for tendon/ligament engineering, Tissue Eng. B Rev., 19, 133, 10.1089/ten.teb.2012.0295 Leung, 2015, A comparative study on the biomechanical and histological properties of bone-to-bone, bone-to-tendon, and tendon-to-tendon healing: an Achilles tendon-calcaneus model in goats, Am. J. Sports Med., 43, 1413, 10.1177/0363546515576904 Derwin, 2018, Enthesis repair: challenges and opportunities for effective tendon-to-bone healing, J Bone Joint Surg Am, 100, e109, 10.2106/JBJS.18.00200 Samitier, 2015, Failure of anterior cruciate ligament reconstruction, Arch Bone Jt Surg, 3, 220 Jensen, 2018, Assembly, maturation, and degradation of the supraspinatus enthesis, J. Shoulder Elbow Surg., 27, 739, 10.1016/j.jse.2017.10.030 Mansat, 1997, Complications of rotator cuff repair, Orthop. Clin. N. Am., 28, 205, 10.1016/S0030-5898(05)70280-7 Rokito, 1996, Strength after surgical repair of the rotator cuff, J. Shoulder Elbow Surg., 5, 12, 10.1016/S1058-2746(96)80025-5 Galatz, 2005, Delayed repair of tendon to bone injuries leads to decreased biomechanical properties and bone loss, J. Orthop. Res., 23, 1441, 10.1016/j.orthres.2005.05.005.1100230629 Calvert, 1986, Arthrography of the shoulder after operative repair of the torn rotator cuff, J Bone Joint Surg Br, 68, 147, 10.1302/0301-620X.68B1.3941132 Gerber, 2000, The results of repair of massive tears of the rotator cuff, J Bone Joint Surg Am, 82, 505, 10.2106/00004623-200004000-00006 Su, 2019, Preparation of decellularized triphasic hierarchical bone-fibrocartilage-tendon composite extracellular matrix for enthesis regeneration, Adv Healthc Mater, 8 Liu, 2018, Novel engineered tendon-fibrocartilage-bone composite with cyclic tension for rotator cuff repair, J Tissue Eng Regen Med, 12, 1690, 10.1002/term.2696 Blaudez, 2020, An overview of decellularisation techniques of native tissues and tissue engineered products for bone, ligament and tendon regeneration, Methods, 171, 28, 10.1016/j.ymeth.2019.08.002 Xiao, 2021, Cell-free book-shaped decellularized tendon matrix graft capable of controlled release of BMP-12 to improve tendon healing in a rat model, Am. J. Sports Med., 49, 1333, 10.1177/0363546521994555 Garcia-Gareta, 2020, Decellularised scaffolds: just a framework? Current knowledge and future directions, J. Tissue Eng., 11 Cao, 2020, Three-dimensional printed multiphasic scaffolds with stratified cell-laden gelatin methacrylate hydrogels for biomimetic tendon-to-bone interface engineering, J Orthop Translat, 23, 89, 10.1016/j.jot.2020.01.004 Kim, 2014, Human collagen-based multilayer scaffolds for tendon-to-bone interface tissue engineering, J. Biomed. Mater. Res., 102, 4044, 10.1002/jbm.a.35057 He, 2012, In vitro ligament-bone interface regeneration using a trilineage coculture system on a hybrid silk scaffold, Biomacromolecules, 13, 2692, 10.1021/bm300651q Spalazzi, 2008, In vivo evaluation of a multiphased scaffold designed for orthopaedic interface tissue engineering and soft tissue-to-bone integration, J. Biomed. Mater. Res., 86, 1 Font Tellado, 2018, Heparin functionalization increases retention of TGF-beta2 and GDF5 on biphasic silk fibroin scaffolds for tendon/ligament-to-bone tissue engineering, Acta Biomater., 72, 150, 10.1016/j.actbio.2018.03.017 Criscenti, 2016, Triphasic scaffolds for the regeneration of the bone-ligament interface, Biofabrication, 8, 10.1088/1758-5090/8/1/015009 Caliari, 2015, Collagen scaffolds incorporating coincident gradations of instructive structural and biochemical cues for osteotendinous junction engineering, Adv Healthc Mater, 4, 831, 10.1002/adhm.201400809 Font Tellado, 2015, Strategies to engineer tendon/ligament-to-bone interface: biomaterials, cells and growth factors, Adv. Drug Deliv. Rev., 94, 126, 10.1016/j.addr.2015.03.004 Smith, 2012, Tissue-engineering strategies for the tendon/ligament-to-bone insertion, Connect. Tissue Res., 53, 95, 10.3109/03008207.2011.650804 Samorezov, 2015, Spatial regulation of controlled bioactive factor delivery for bone tissue engineering, Adv. Drug Deliv. Rev., 84, 45, 10.1016/j.addr.2014.11.018 Clegg, 2019, Modular fabrication of intelligent material-tissue interfaces for bioinspired and biomimetic devices, Prog. Mater. Sci., 106, 10.1016/j.pmatsci.2019.100589 Pugliese, 2018, Advancements and challenges in multidomain multicargo delivery vehicles, Adv. Mater., 30, 10.1002/adma.201704324 Levingstone, 2021, Layer-specific stem cell differentiation in tri-layered tissue engineering biomaterials: towards development of a single-stage cell-based approach for osteochondral defect repair, Mater Today Bio, 12 Li, 2014, A novel silk-TCP-PEEK construct for anterior cruciate ligament reconstruction: an off-the shelf alternative to a bone-tendon-bone autograft, Biofabrication, 6, 10.1088/1758-5082/6/1/015010 Seong, 2017, Calcium phosphate-collagen scaffold with aligned pore channels for enhanced osteochondral regeneration, Adv Healthc Mater, 6, 10.1002/adhm.201700966 Zhu, 2018, Design and fabrication of a hierarchically structured scaffold for tendon-to-bone repair, Adv. Mater., 30 Wang, 2022, Key considerations on the development of biodegradable biomaterials for clinical translation of medical devices: with cartilage repair products as an example, Bioact. Mater., 9, 332, 10.1016/j.bioactmat.2021.07.031 Williams, 2019, Challenges with the development of biomaterials for sustainable tissue engineering, Front. Bioeng. Biotechnol., 7, 127, 10.3389/fbioe.2019.00127 Darnell, 2017, Leveraging advances in biology to design biomaterials, Nat. Mater., 16, 1178, 10.1038/nmat4991 Sallent, 2020, The few who made it: commercially and clinically successful innovative bone grafts, Front. Bioeng. Biotechnol., 8, 952, 10.3389/fbioe.2020.00952 Zeugolis, 2008, Factors influencing the properties of reconstituted collagen fibers prior to self-assembly: animal species and collagen extraction method, J. Biomed. Mater. Res., 86, 892, 10.1002/jbm.a.31694 Delgado, 2017, Acetic acid and pepsin result in high yield, high purity and low macrophage response collagen for biomedical applications, Biomed. Mater., 12, 10.1088/1748-605X/aa838d Sorushanova, 2021, The influence of animal species, gender and tissue on the structural, biophysical, biochemical and biological properties of collagen sponges, J. Mater. Sci. Mater. Med., 32, 12, 10.1007/s10856-020-06485-4 Wu, 2021, In the quest of the optimal chondrichthyan for the development of collagen sponges for articular cartilage, J. Sci.: Adv. Mater. Dev., 6, 390 Wu, 2021, In the quest of the optimal tissue source (porcine male and female articular, tracheal and auricular cartilage) for the development of collagen sponges for articular cartilage, Biomed. Eng. Adv., 1, 10.1016/j.bea.2021.100002 Capella-Monsonis, 2018, An experimental toolbox for characterization of mammalian collagen type I in biological specimens, Nat. Protoc., 13, 507, 10.1038/nprot.2017.117 Levingstone, 2014, A biomimetic multi-layered collagen-based scaffold for osteochondral repair, Acta Biomater., 10, 1996, 10.1016/j.actbio.2014.01.005 Helling, 2017, In vitro enzymatic degradation of tissue grafts and collagen biomaterials by matrix metalloproteinases: improving the collagenase assay, ACS Biomater. Sci. Eng., 3, 1922, 10.1021/acsbiomaterials.5b00563 Tan, 2012, A 1-min method for homogenous cell seeding in porous scaffolds, J. Biomater. Appl., 26, 877, 10.1177/0885328210389504 Barbosa, 2003, Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies, Glycobiology, 13, 647, 10.1093/glycob/cwg082 Ryan, 2021, A combined physicochemical approach towards human tenocyte phenotype maintenance, Mater Today Bio, 12 Kane, 2015, Hydroxyapatite reinforced collagen scaffolds with improved architecture and mechanical properties, Acta Biomater., 17, 16, 10.1016/j.actbio.2015.01.031 Lin, 2009, Study of hydroxyapatite osteoinductivity with an osteogenic differentiation of mesenchymal stem cells, J. Biomed. Mater. Res., 89, 326, 10.1002/jbm.a.31994 Zhou, 2020, Biphasic fish collagen scaffold for osteochondral regeneration, Mater. Des., 195, 10.1016/j.matdes.2020.108947 Zhang, 2014, Pore size effect of collagen scaffolds on cartilage regeneration, Acta Biomater., 10, 2005, 10.1016/j.actbio.2013.12.042 Eviana Putri, 2020, Preparation of PLGA-collagen hybrid scaffolds with controlled pore structures for cartilage tissue engineering, Prog. Nat. Sci.: Mater. Int., 30, 642, 10.1016/j.pnsc.2020.07.003 Thomas, 2014, A shape-controlled tuneable microgel platform to modulate angiogenic paracrine responses in stem cells, Biomaterials, 35, 8757, 10.1016/j.biomaterials.2014.06.053 Wahl, 2006, Collagen-hydroxyapatite composites for hard tissue repair, Eur. Cell. Mater., 11, 43, 10.22203/eCM.v011a06 Stock, 2015, The mineral-collagen interface in bone, Calcif. Tissue Int., 97, 262, 10.1007/s00223-015-9984-6 Rodimova, 2019, Metabolic activity and intracellular pH in induced pluripotent stem cells differentiating in dermal and epidermal directions, Methods Appl. Fluoresc., 7, 10.1088/2050-6120/ab3b3d Dunn, 1978, Contact guidance on oriented collagen gels, Exp. Cell Res., 111, 475, 10.1016/0014-4827(78)90196-9 Orr, 2015, Aligned multilayered electrospun scaffolds for rotator cuff tendon tissue engineering, Acta Biomater., 24, 117, 10.1016/j.actbio.2015.06.010 Younesi, 2014, Tenogenic induction of human MSCs by anisotropically aligned collagen biotextiles, Adv. Funct. Mater., 24, 5762, 10.1002/adfm.201400828 Caliari, 2014, Structural and biochemical modification of a collagen scaffold to selectively enhance MSC tenogenic, chondrogenic, and osteogenic differentiation, Adv Healthc Mater, 3, 1086, 10.1002/adhm.201300646 Lee, 2014, Influence of chondroitin sulfate and hyaluronic acid presence in nanofibers and its alignment on the bone marrow stromal cells: cartilage regeneration, J. Biomed. Nanotechnol., 10, 1469, 10.1166/jbn.2014.1831 Wise, 2009, Chondrogenic differentiation of human mesenchymal stem cells on oriented nanofibrous scaffolds: engineering the superficial zone of articular cartilage, Tissue Eng Part A, 15, 913, 10.1089/ten.tea.2008.0109 Genin, 2009, Functional grading of mineral and collagen in the attachment of tendon to bone, Biophys. J., 97, 976, 10.1016/j.bpj.2009.05.043 Engler, 2006, Matrix elasticity directs stem cell lineage specification, Cell, 126, 677, 10.1016/j.cell.2006.06.044 Zhu, 2021, Augmenting tendon-to-bone repair with functionally graded scaffolds, Adv Healthc Mater, 10, 10.1002/adhm.202002269 Sharma, 2012, Paracrine interactions between mesenchymal stem cells affect substrate driven differentiation toward tendon and bone phenotypes, PLoS One, 7, 10.1371/journal.pone.0031504 Guo, 2009, In vitro generation of an osteochondral construct using injectable hydrogel composites encapsulating rabbit marrow mesenchymal stem cells, Biomaterials, 30, 2741, 10.1016/j.biomaterials.2009.01.048 Qazi, 2017, Biomaterials that promote cell-cell interactions enhance the paracrine function of MSCs, Biomaterials, 140, 103, 10.1016/j.biomaterials.2017.06.019 Singh, 2011, Negative feedback through mRNA provides the best control of gene-expression noise, IEEE Trans. NanoBioscience, 10, 194, 10.1109/TNB.2011.2168826 Mueller, 2008, Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells, Arthritis Rheum., 58, 1377, 10.1002/art.23370 Calejo, 2019, Enthesis tissue engineering: biological requirements meet at the interface, Tissue Eng. B Rev., 25, 330, 10.1089/ten.teb.2018.0383 Prabhath, 2018, Growth factor delivery strategies for rotator cuff repair and regeneration, Int. J. Pharm., 544, 358, 10.1016/j.ijpharm.2018.01.006 Chen, 2010, Toward delivery of multiple growth factors in tissue engineering, Biomaterials, 31, 6279, 10.1016/j.biomaterials.2010.04.053 Pearson, 2022, Growth factor immobilization strategies for musculoskeletal disorders, Curr. Osteoporos. Rep., 20, 13, 10.1007/s11914-022-00718-x Lee, 2011, Growth factor delivery-based tissue engineering: general approaches and a review of recent developments, J. R. Soc. Interface, 8, 153, 10.1098/rsif.2010.0223 Lee, 2002, Preparation and characterization of mono-PEGylated epidermal growth factor: evaluation of in vitro biologic activity, Pharm. Res. (N. Y.), 19, 845, 10.1023/A:1016113117851 Re'em, 2012, Chondrogenesis of hMSC in affinity-bound TGF-beta scaffolds, Biomaterials, 33, 751, 10.1016/j.biomaterials.2011.10.007 Gluhak, 1996, Tenascin-C is associated with early stages of chondrogenesis by chick mandibular ectomesenchymal cells in vivo and in vitro, Dev. Dynam., 205, 24, 10.1002/(SICI)1097-0177(199601)205:1<24::AID-AJA3>3.0.CO;2-7 Mackie, 1987, Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro, J. Cell Biol., 105, 2569, 10.1083/jcb.105.6.2569 Li, 2016, Tenascin C affects mineralization of SaOS2 osteoblast-like cells through matrix vesicles, Drug Discov Ther, 10, 82, 10.5582/ddt.2016.01009 Sasano, 2000, Immunohistochemical localization of type I collagen, fibronectin and tenascin C during embryonic osteogenesis in the dentary of mandibles and tibias in rats, Histochem. J., 32, 591, 10.1023/A:1026720003564 Sarrigiannidis, 2021, A tough act to follow: collagen hydrogel modifications to improve mechanical and growth factor loading capabilities, Mater Today Bio, 10 Kumar, 2018, Low oxygen tension and macromolecular crowding accelerate extracellular matrix deposition in human corneal fibroblast culture, J Tissue Eng Regen Med, 12, 6, 10.1002/term.2283 Coentro, 2022, Dual drug delivery collagen vehicles for modulation of skin fibrosisin vitro, Biomed. Mater., 17, 10.1088/1748-605X/ac5673 Madry, 2014, Transforming growth factor beta-releasing scaffolds for cartilage tissue engineering, Tissue Eng. B Rev., 20, 106, 10.1089/ten.teb.2013.0271 Sieron, 2002, Site-specific interaction of bone morphogenetic protein 2 with procollagen II, Cytokine, 18, 214, 10.1006/cyto.2002.1035 McKay, 2007, A comprehensive clinical review of recombinant human bone morphogenetic protein-2 (INFUSE Bone Graft), Int. Orthop., 31, 729, 10.1007/s00264-007-0418-6 Glue, 2000, Pegylated interferon-alpha2b: pharmacokinetics, pharmacodynamics, safety, and preliminary efficacy data. Hepatitis C Intervention Therapy Group, Clin. Pharmacol. Ther., 68, 556, 10.1067/mcp.2000.110973 Wunderli, 2020, Tendon explant models for physiologically relevant in vitro study of tissue biology - a perspective, Connect. Tissue Res., 61, 262, 10.1080/03008207.2019.1700962 Newsham-West, 2007, Long-term morphology of a healing bone-tendon interface: a histological observation in the sheep model, J. Anat., 210, 318 Tayalia, 2009, Controlled growth factor delivery for tissue engineering, Adv. Mater., 21, 3269, 10.1002/adma.200900241 Murray, 2003, The effect of selected growth factors on human anterior cruciate ligament cell interactions with a three-dimensional collagen-GAG scaffold, J. Orthop. Res., 21, 238, 10.1016/S0736-0266(02)00142-0 Monibi, 2016, Development of a micronized meniscus extracellular matrix scaffold for potential augmentation of meniscal repair and regeneration, Tissue Eng. C Methods, 22, 1059, 10.1089/ten.tec.2016.0276 Woon, 2011, Optimization of human tendon tissue engineering: peracetic acid oxidation for enhanced reseeding of acellularized intrasynovial tendon, Plast. Reconstr. Surg., 127, 1107, 10.1097/PRS.0b013e318205f298 Liu, 2010, Biomimetic hydrogels for chondrogenic differentiation of human mesenchymal stem cells to neocartilage, Biomaterials, 31, 7298, 10.1016/j.biomaterials.2010.06.001 Nam, 2011, Modulation of embryonic mesenchymal progenitor cell differentiation via control over pure mechanical modulus in electrospun nanofibers, Acta Biomater., 7, 1516, 10.1016/j.actbio.2010.11.022 Toh, 2012, Modulation of mesenchymal stem cell chondrogenesis in a tunable hyaluronic acid hydrogel microenvironment, Biomaterials, 33, 3835, 10.1016/j.biomaterials.2012.01.065 Goffin, 2006, Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers, J. Cell Biol., 172, 259, 10.1083/jcb.200506179 Sharma, 2010, Biochemical and biomechanical gradients for directed bone marrow stromal cell differentiation toward tendon and bone, Biomaterials, 31, 7695, 10.1016/j.biomaterials.2010.06.046