In Vitro Mimetic Models for the Bone-Cartilage Interface Regeneration.

In embryonic development, pure cartilage structures are in the basis of bone-cartilage interfaces. Despite this fact, the mature bone and cartilage structures can vary greatly in composition and function. Nevertheless, they collaborate in the osteochondral region to create a smooth transition zone that supports the movements and forces resulting from the daily activities. In this sense, all the hierarchical organization is involved in the maintenance and reestablishment of the equilibrium in case of damage. Therefore, this interface has attracted a great deal of interest in order to understand the mechanisms of regeneration or disease progression in osteoarthritis. With that purpose, in vitro tissue models (either static or dynamic) have been studied. Static in vitro tissue models include monocultures, co-cultures, 3D cultures, and ex vivo cultures, mostly cultivated in flat surfaces, while dynamic models involve the use of bioreactors and microfluidic systems. The latter have emerged as alternatives to study the cellular interactions in a more authentic manner over some disadvantages of the static models. The current alternatives of in vitro mimetic models for bone-cartilage interface regeneration are overviewed and discussed herein.

[1]  C. L. Murphy,et al.  Effect of oxygen tension and alginate encapsulation on restoration of the differentiated phenotype of passaged chondrocytes. , 2001, Tissue engineering.

[2]  C. Archer,et al.  The development of articular cartilage: evidence for an appositional growth mechanism , 2001, Anatomy and Embryology.

[3]  H J Donahue,et al.  Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. , 2000, Journal of biomechanical engineering.

[4]  F. Yuan,et al.  A review of three-dimensional in vitro tissue models for drug discovery and transport studies. , 2011, Journal of pharmaceutical sciences.

[5]  Jun-Ha Hwang,et al.  Shear Stress Induced by an Interstitial Level of Slow Flow Increases the Osteogenic Differentiation of Mesenchymal Stem Cells through TAZ Activation , 2014, PloS one.

[6]  C. Hoemann,et al.  The Cartilage-Bone Interface , 2012, The journal of knee surgery.

[7]  Dean Wang,et al.  High Short-Term Failure Rate Associated With Decellularized Osteochondral Allograft for Treatment of Knee Cartilage Lesions. , 2017, Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association.

[8]  Yaxiong Liu,et al.  Study on the microstructure of human articular cartilage/bone interface , 2011 .

[9]  L. Orci,et al.  Chondrocytes inhibit endothelial sprout formation in vitro: Evidence for involvement of a transforming growth factor‐beta , 1991, Journal of cellular physiology.

[10]  T. Janvilisri,et al.  Microfluidics: innovative approaches for rapid diagnosis of antibiotic-resistant bacteria. , 2017, Essays in biochemistry.

[11]  S. Goldring,et al.  Changes in the osteochondral unit during osteoarthritis: structure, function and cartilage–bone crosstalk , 2016, Nature Reviews Rheumatology.

[12]  J. Fisher,et al.  Coculture strategies in bone tissue engineering: the impact of culture conditions on pluripotent stem cell populations. , 2012, Tissue engineering. Part B, Reviews.

[13]  A. Mikos,et al.  The effect of hypoxia on the chondrogenic differentiation of co-cultured articular chondrocytes and mesenchymal stem cells in scaffolds. , 2013, Biomaterials.

[14]  Feng Xu,et al.  Stem cell culture and differentiation in microfluidic devices toward organ-on-a-chip , 2017, Future science OA.

[15]  G. Finkenzeller,et al.  Human endothelial progenitor cells induce extracellular signal-regulated kinase-dependent differentiation of mesenchymal stem cells into smooth muscle cells upon cocultivation. , 2012, Tissue engineering. Part A.

[16]  X. Sui,et al.  In vivo cartilage repair using adipose‐derived stem cell‐loaded decellularized cartilage ECM scaffolds , 2014, Journal of tissue engineering and regenerative medicine.

[17]  F. O'Brien,et al.  In-vivo generation of bone via endochondral ossification by in-vitro chondrogenic priming of adult human and rat mesenchymal stem cells , 2011, BMC musculoskeletal disorders.

[18]  Lobat Tayebi,et al.  Enhanced osteogenic differentiation of stem cells via microfluidics synthesized nanoparticles. , 2015, Nanomedicine : nanotechnology, biology, and medicine.

[19]  P. Foehr,et al.  *Fabrication and Characterization of Biphasic Silk Fibroin Scaffolds for Tendon/Ligament-to-Bone Tissue Engineering , 2017 .

[20]  R. Wilkins,et al.  Oxygen and reactive oxygen species in articular cartilage: modulators of ionic homeostasis , 2007, Pflügers Archiv - European Journal of Physiology.

[21]  P. Kasten,et al.  Chondrogenic pre-induction of human mesenchymal stem cells on beta-TCP: enhanced bone quality by endochondral heterotopic bone formation. , 2010, Acta biomaterialia.

[22]  E. Hunziker,et al.  The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. , 2007, Osteoarthritis and cartilage.

[23]  Y. Henrotin,et al.  Osteochondral plate angiogenesis: a new treatment target in osteoarthritis. , 2011, Joint, bone, spine : revue du rhumatisme.

[24]  S. Doty,et al.  In situ measurement of transport between subchondral bone and articular cartilage , 2009, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[25]  M. Brittberg,et al.  Co-culture of dedifferentiated and primary human chondrocytes obtained from cadaveric donor enhance the histological quality of repair tissue: an in-vivo animal study , 2017, Cell and Tissue Banking.

[26]  D. Argyle,et al.  In vitro models for the study of osteoarthritis. , 2016, Veterinary journal.

[27]  C. Archer,et al.  Pellet culture model for human primary osteoblasts. , 2010, European cells & materials.

[28]  S. Schulze,et al.  A supplement‐free osteoclast–osteoblast co‐culture for pre‐clinical application , 2018, Journal of cellular physiology.

[29]  C. Perka,et al.  Temporary arthrodesis using fixator rods in two-stage revision of septic knee prothesis with severe bone and tissue defects , 2014, Knee Surgery, Sports Traumatology, Arthroscopy.

[30]  D. Kaplan,et al.  A Silk Fibroin and Peptide Amphiphile-Based Co-Culture Model for Osteochondral Tissue Engineering. , 2016, Macromolecular bioscience.

[31]  G. Nash,et al.  Static and dynamic assays of cell adhesion relevant to the vasculature. , 2009, Methods in molecular biology.

[32]  G. Vunjak‐Novakovic,et al.  Spatial regulation of human mesenchymal stem cell differentiation in engineered osteochondral constructs: effects of pre-differentiation, soluble factors and medium perfusion. , 2010, Osteoarthritis and cartilage.

[33]  B. Mandelbaum,et al.  Emerging options for treatment of articular cartilage injury in the athlete. , 2009, Clinics in sports medicine.

[34]  R. Reis,et al.  Bilayered chitosan-based scaffolds for osteochondral tissue engineering: influence of hydroxyapatite on in vitro cytotoxicity and dynamic bioactivity studies in a specific double-chamber bioreactor. , 2009, Acta biomaterialia.

[35]  Liu Yang,et al.  Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation , 2014, Proceedings of the National Academy of Sciences.

[36]  Li-Hsin Han,et al.  Modeling Physiological Events in 2D vs. 3D Cell Culture. , 2017, Physiology.

[37]  J. Malda,et al.  Modulating endochondral ossification of multipotent stromal cells for bone regeneration. , 2010, Tissue engineering. Part B, Reviews.

[38]  O. Clément,et al.  Netrin-4 promotes mural cell adhesion and recruitment to endothelial cells , 2014, Vascular cell.

[39]  Shuyun Liu,et al.  Mesenchymal stem cells on a decellularized cartilage matrix for cartilage tissue engineering , 2011 .

[40]  Q. Guo,et al.  Bone-cartilage interface crosstalk in osteoarthritis: potential pathways and future therapeutic strategies. , 2014, Osteoarthritis and cartilage.

[41]  Gilda A. Barabino,et al.  Spatial Engineering of Osteochondral Tissue Constructs Through Microfluidically Directed Differentiation of Mesenchymal Stem Cells , 2016, BioResearch open access.

[42]  D. Beebe,et al.  The present and future role of microfluidics in biomedical research , 2014, Nature.

[43]  R. Reiter,et al.  Stage-related capacity for limb chondrogenesis in cell culture. , 1977, Developmental biology.

[44]  P. Foehr,et al.  * Fabrication and Characterization of Biphasic Silk Fibroin Scaffolds for Tendon/Ligament-to-Bone Tissue Engineering. , 2017, Tissue engineering. Part A.

[45]  R Umansky,et al.  The effect of cell population density on the developmental fate of reaggregating mouse limb bud mesenchyme. , 1966, Developmental biology.

[46]  Yuuki Imai,et al.  Repair of experimentally induced large osteochondral defects in rabbit knee with various concentrations of Escherichia coli-derived recombinant human bone morphogenetic protein-2 , 2010, International Orthopaedics.

[47]  J. Fisher,et al.  Bone tissue engineering bioreactors: dynamic culture and the influence of shear stress. , 2011, Bone.

[48]  R. Cancedda,et al.  Cartilage repair in the knee with subchondral drilling augmented with a platelet-rich plasma-immersed polymer-based implant , 2013, Knee Surgery, Sports Traumatology, Arthroscopy.

[49]  B. Waterman,et al.  Limitations and sources of bias in clinical knee cartilage research. , 2012, Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association.

[50]  Eamon J. Sheehy,et al.  Tissue engineering scaled-up, anatomically shaped osteochondral constructs for joint resurfacing. , 2015, European cells & materials.

[51]  M. Karsdal,et al.  Characterization of an Ex vivo Femoral Head Model Assessed by Markers of Bone and Cartilage Turnover , 2011, Cartilage.

[52]  C. Jorgensen,et al.  Antiinflammatory and chondroprotective effects of intraarticular injection of adipose-derived stem cells in experimental osteoarthritis. , 2012, Arthritis and rheumatism.

[53]  A. Mikos,et al.  Enhancing chondrogenic phenotype for cartilage tissue engineering: monoculture and coculture of articular chondrocytes and mesenchymal stem cells. , 2014, Tissue engineering. Part B, Reviews.

[54]  A. Allori,et al.  A Novel Flow-Perfusion Bioreactor Supports 3D Dynamic Cell Culture , 2009, Journal of biomedicine & biotechnology.

[55]  S. Marino,et al.  Models of ex vivo explant cultures: applications in bone research , 2016, BoneKEy reports.

[56]  F. Dell’Accio,et al.  High density micromass cultures of a human chondrocyte cell line: a reliable assay system to reveal the modulatory functions of pharmacological agents. , 2011, Biochemical pharmacology.

[57]  J. Xie,et al.  Crosstalk between adipose-derived stem cells and chondrocytes: when growth factors matter , 2016, Bone Research.

[58]  Rocky S Tuan,et al.  Three-dimensional osteochondral microtissue to model pathogenesis of osteoarthritis , 2013, Stem Cell Research & Therapy.

[59]  A. Nagy,et al.  Cartilage tissue formation using redifferentiated passaged chondrocytes in vitro. , 2009, Tissue engineering. Part A.

[60]  C. Cunha,et al.  Osteochondral tissue engineering approaches for articular cartilage and subchondral bone regeneration , 2012, Knee Surgery, Sports Traumatology, Arthroscopy.

[61]  Frank P. Luyten,et al.  Biological aspects of early osteoarthritis , 2012, Knee Surgery, Sports Traumatology, Arthroscopy.

[62]  N. Shelke,et al.  Guided differentiation of bone marrow stromal cells on co-cultured cartilage and bone scaffolds. , 2015, Soft matter.

[63]  Rocky S Tuan,et al.  Three-dimensional osteogenic and chondrogenic systems to model osteochondral physiology and degenerative joint diseases , 2014, Experimental biology and medicine.

[64]  A. Atala,et al.  Multilayer scaffolds in orthopaedic tissue engineering , 2016, Knee Surgery, Sports Traumatology, Arthroscopy.

[65]  T. O’Shea,et al.  Bilayered scaffolds for osteochondral tissue engineering. , 2008, Tissue engineering. Part B, Reviews.

[66]  Lasse Evensen,et al.  Mural Cell Associated VEGF Is Required for Organotypic Vessel Formation , 2009, PloS one.

[67]  A. Vaziri,et al.  Biomechanics and mechanobiology of trabecular bone: a review. , 2015, Journal of biomechanical engineering.

[68]  Sang-Hoon Lee,et al.  Microfluidic spinning of micro- and nano-scale fibers for tissue engineering. , 2014, Lab on a chip.

[69]  R P Pirraco,et al.  Cell interactions in bone tissue engineering , 2009, Journal of cellular and molecular medicine.

[70]  Clemens A van Blitterswijk,et al.  Trophic effects of mesenchymal stem cells increase chondrocyte proliferation and matrix formation. , 2011, Tissue engineering. Part A.

[71]  S. Panseri,et al.  Biomimetic Scaffold with Aligned Microporosity Designed for Dentin Regeneration , 2016, Front. Bioeng. Biotechnol..

[72]  Bin Wang,et al.  Elevated cross-talk between subchondral bone and cartilage in osteoarthritic joints. , 2012, Bone.

[73]  Nora T. Khanarian,et al.  FTIR‐I Compositional Mapping of the Cartilage‐to‐Bone Interface as a Function of Tissue Region and Age , 2014, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[74]  G. Whitesides The origins and the future of microfluidics , 2006, Nature.

[75]  F. Mussano,et al.  Overcoming physical constraints in bone engineering: ‘the importance of being vascularized’ , 2016, Journal of biomaterials applications.

[76]  A. Rastogi,et al.  Role of autologous chondrocyte transplantation in articular cartilage defects: An experimental study , 2013, Indian journal of orthopaedics.

[77]  Jerry C. Hu,et al.  Biomechanics‐driven chondrogenesis: from embryo to adult , 2012, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[78]  R. Reis,et al.  Bilayered silk/silk-nanoCaP scaffolds for osteochondral tissue engineering: In vitro and in vivo assessment of biological performance. , 2015, Acta biomaterialia.

[79]  R. Haines The histology of epiphyseal union in mammals. , 1975, Journal of anatomy.

[80]  H Weinans,et al.  The use of a cartilage decellularized matrix scaffold for the repair of osteochondral defects: the importance of long-term studies in a large animal model. , 2017, Osteoarthritis and cartilage.

[81]  G D Smith,et al.  A clinical review of cartilage repair techniques. , 2005, The Journal of bone and joint surgery. British volume.

[82]  S H Elder,et al.  Cyclic hydrostatic compression stimulates chondroinduction of C3H/10T1/2 cells , 2005, Biomechanics and modeling in mechanobiology.

[83]  W. Cui,et al.  Co-culture of chondrocytes and bone marrow mesenchymal stem cells in vitro enhances the expression of cartilaginous extracellular matrix components. , 2011, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[84]  V. Castronovo,et al.  Phenotypic characterization of osteoblasts from the sclerotic zones of osteoarthritic subchondral bone. , 2008, Arthritis and rheumatism.

[85]  C James Kirkpatrick,et al.  Co-culture systems for vascularization--learning from nature. , 2011, Advanced drug delivery reviews.

[86]  P. Hauschka,et al.  Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. , 1996, The Biochemical journal.

[87]  Ali Khademhosseini,et al.  Microfluidic techniques for development of 3D vascularized tissue. , 2014, Biomaterials.

[88]  R. Mason,et al.  Modulation of bovine articular chondrocyte gene expression in vitro by oxygen tension. , 2001, Osteoarthritis and cartilage.

[89]  Rui L Reis,et al.  Novel hydroxyapatite/chitosan bilayered scaffold for osteochondral tissue-engineering applications: Scaffold design and its performance when seeded with goat bone marrow stromal cells. , 2006, Biomaterials.

[90]  C. Hidaka,et al.  Interaction between zonal populations of articular chondrocytes suppresses chondrocyte mineralization and this process is mediated by PTHrP. , 2008, Osteoarthritis and cartilage.

[91]  Anh-Vu Do,et al.  3D Printing of Scaffolds for Tissue Regeneration Applications , 2015, Advanced healthcare materials.

[92]  Emily C. Beck,et al.  Decellularized Cartilage May Be a Chondroinductive Material for Osteochondral Tissue Engineering , 2015, PloS one.

[93]  Kayla J Bayless,et al.  Molecular basis of endothelial cell morphogenesis in three‐dimensional extracellular matrices , 2002, The Anatomical record.

[94]  Jeremy Baldwin,et al.  In vitro pre-vascularisation of tissue-engineered constructs A co-culture perspective , 2014, Vascular cell.

[95]  J. Verhaar,et al.  An osteochondral culture model to study mechanisms involved in articular cartilage repair. , 2012, Tissue engineering. Part C, Methods.

[96]  P. Bourgine,et al.  Engineering of a functional bone organ through endochondral ossification , 2013, Proceedings of the National Academy of Sciences.

[97]  Amber N. Stratman,et al.  Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting. , 2011, International review of cell and molecular biology.

[98]  Haines Rw The histology of epiphyseal union in mammals. , 1975 .

[99]  G. Im,et al.  Osteogenic differentiation and angiogenesis with cocultured adipose-derived stromal cells and bone marrow stromal cells. , 2014, Biomaterials.

[100]  C James Kirkpatrick,et al.  Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials. , 2007, Biomaterials.

[101]  Johnna S Temenoff,et al.  Engineering orthopedic tissue interfaces. , 2009, Tissue engineering. Part B, Reviews.

[102]  Cato T Laurencin,et al.  Bone tissue engineering: recent advances and challenges. , 2012, Critical reviews in biomedical engineering.

[103]  Fernando Jorge Monteiro,et al.  The role of perfusion bioreactors in bone tissue engineering , 2012, Biomatter.