Strategies for zonal cartilage repair using hydrogels.

Articular cartilage is a highly hydrated tissue with depth-dependent cellular and matrix properties that provide low-friction load bearing in joints. However, the structure and function are frequently lost and there is insufficient repair response to regenerate high-quality cartilage. Several hydrogel-based tissue-engineering strategies have recently been developed to form constructs with biomimetic zonal variations to improve cartilage repair. Modular hydrogel systems allow for systematic control over hydrogel properties, and advanced fabrication techniques allow for control over construct organization. These technologies have great potential to address many unanswered questions involved in prescribing zonal properties to tissue-engineered constructs for cartilage repair.

[1]  A. Metters,et al.  Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: Engineering cell-invasion characteristics , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[2]  L. Bonassar,et al.  Review of injectable cartilage engineering using fibrin gel in mice and swine models. , 2006, Tissue engineering.

[3]  Joseph M. Mansour,et al.  Mesenchymal Cell-Based Repair of Large Full Thickness Defects of Articular Cartilage , 1994 .

[4]  R. Schneiderman,et al.  Depth-dependent compressive properties of normal aged human femoral head articular cartilage: relationship to fixed charge density. , 2001, Osteoarthritis and cartilage.

[5]  Bernd Baumann,et al.  Chondrogenic differentiation of human mesenchymal stem cells in collagen type I hydrogels. , 2007, Journal of biomedical materials research. Part A.

[6]  K. Kawasaki,et al.  Transplantation of cartilage-like tissue made by tissue engineering in the treatment of cartilage defects of the knee. , 2002, The Journal of bone and joint surgery. British volume.

[7]  Robert E. Guldberg,et al.  Analysis of cartilage matrix fixed charge density and three-dimensional morphology via contrast-enhanced microcomputed tomography , 2006, Proceedings of the National Academy of Sciences.

[8]  Dietmar W Hutmacher,et al.  Repair and regeneration of osteochondral defects in the articular joints. , 2007, Biomolecular engineering.

[9]  W. Hennink,et al.  Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. , 2007, Tissue engineering.

[10]  Kristi S Anseth,et al.  Three-dimensional biochemical patterning of click-based composite hydrogels via thiolene photopolymerization. , 2008, Biomacromolecules.

[11]  Ralph Müller,et al.  Recombinant protein-co-PEG networks as cell-adhesive and proteolytically degradable hydrogel matrixes. Part II: biofunctional characteristics. , 2006, Biomacromolecules.

[12]  Albert C. Chen,et al.  Compressive properties and function—composition relationships of developing bovine articular cartilage , 2001, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[13]  P. Benya,et al.  Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels , 1982, Cell.

[14]  E. Hunziker,et al.  Development of mechanically stable alginate/chondrocyte constructs: effects of guluronic acid content and matrix synthesis , 2001, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[15]  David J Mooney,et al.  Alginate hydrogels as biomaterials. , 2006, Macromolecular bioscience.

[16]  Ralph Müller,et al.  Repair of bone defects using synthetic mimetics of collagenous extracellular matrices , 2003, Nature Biotechnology.

[17]  Sunny Kim Changes in surgical loads and economic burden of hip and knee replacements in the US: 1997-2004. , 2008, Arthritis and rheumatism.

[18]  S. Bryant,et al.  Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly(ethylene glycol) hydrogels. , 2002, Journal of biomedical materials research.

[19]  Adam C. Canver,et al.  Response of zonal chondrocytes to extracellular matrix‐hydrogels , 2007, FEBS letters.

[20]  Zhaohui Zheng,et al.  Allogeneic mesenchymal stem cell and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. , 2008, Rheumatology.

[21]  Jason P. Gleghorn,et al.  Adhesive properties of laminated alginate gels for tissue engineering of layered structures. , 2008, Journal of biomedical materials research. Part A.

[22]  Farshid Guilak,et al.  Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. , 2004, Biomaterials.

[23]  L. Galois,et al.  Bovine chondrocyte behaviour in three-dimensional type I collagen gel in terms of gel contraction, proliferation and gene expression. , 2006, Biomaterials.

[24]  C. Rorabeck,et al.  Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration. , 1995, The Journal of clinical investigation.

[25]  Dietmar W. Hutmacher,et al.  Scaffold design and fabrication technologies for engineering tissues — state of the art and future perspectives , 2001, Journal of biomaterials science. Polymer edition.

[26]  S. Bryant,et al.  Crosslinking Density Influences Chondrocyte Metabolism in Dynamically Loaded Photocrosslinked Poly(ethylene glycol) Hydrogels , 2004, Annals of Biomedical Engineering.

[27]  S. Gabriel,et al.  Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. , 2008, Arthritis and rheumatism.

[28]  Vladimir Mironov,et al.  Review: bioprinting: a beginning. , 2006, Tissue engineering.

[29]  H. Sintonen,et al.  Effectiveness of hip or knee replacement surgery in terms of quality-adjusted life years and costs , 2007, Acta orthopaedica.

[30]  Jennifer L West,et al.  Covalently immobilized gradients of bFGF on hydrogel scaffolds for directed cell migration. , 2005, Biomaterials.

[31]  Matthias P Lutolf,et al.  Bovine primary chondrocyte culture in synthetic matrix metalloproteinase-sensitive poly(ethylene glycol)-based hydrogels as a scaffold for cartilage repair. , 2004, Tissue engineering.

[32]  M E Levenston,et al.  Articular chondrocytes derived from distinct tissue zones differentially respond to in vitro oscillatory tensile loading. , 2008, Osteoarthritis and cartilage.

[33]  G A Ateshian,et al.  Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. , 2000, Journal of biomechanical engineering.

[34]  K. Anseth,et al.  Decorin moieties tethered into PEG networks induce chondrogenesis of human mesenchymal stem cells. , 2009, Journal of biomedical materials research. Part A.

[35]  A. Cole,et al.  Horizontally oriented clusters of multiple chondrons in the superficial zone of ankle, but not knee articular cartilage , 2002, The Anatomical record.

[36]  M. Schünke,et al.  Influence of various alginate brands on the redifferentiation of dedifferentiated bovine articular chondrocytes in alginate bead culture under high and low oxygen tension. , 2004, Tissue engineering.

[37]  B Kurz,et al.  Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension. , 2002, Osteoarthritis and cartilage.

[38]  Jennifer L. West,et al.  Tethered-TGF-β increases extracellular matrix production of vascular smooth muscle cells , 2001 .

[39]  F Dubrana,et al.  Autologous chondrocyte implantation in a novel alginate-agarose hydrogel: outcome at two years. , 2008, The Journal of bone and joint surgery. British volume.

[40]  D. Eyre Articular cartilage and changes in Arthritis: Collagen of articular cartilage , 2001, Arthritis research.

[41]  J. Block,et al.  A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage. , 1994, Archives of biochemistry and biophysics.

[42]  Kristi S Anseth,et al.  The enhancement of chondrogenic differentiation of human mesenchymal stem cells by enzymatically regulated RGD functionalities. , 2008, Biomaterials.

[43]  J. Bonaventure,et al.  Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads. , 1994, Experimental cell research.

[44]  J. Elisseeff,et al.  Experimental model for cartilage tissue engineering to regenerate the zonal organization of articular cartilage. , 2003, Osteoarthritis and cartilage.

[45]  Jason P. Gleghorn,et al.  Integration of layered chondrocyte-seeded alginate hydrogel scaffolds. , 2007, Biomaterials.

[46]  Stephanie J Bryant,et al.  Encapsulating chondrocytes in degrading PEG hydrogels with high modulus: Engineering gel structural changes to facilitate cartilaginous tissue production , 2004, Biotechnology and bioengineering.

[47]  M. Yaremchuk,et al.  Injectable tissue-engineered cartilage using a fibrin glue polymer. , 1999, Plastic and reconstructive surgery.

[48]  D J Mooney,et al.  Alginate hydrogels as synthetic extracellular matrix materials. , 1999, Biomaterials.

[49]  J. Darmawan,et al.  Rheumatic Diseases in China , 2008, Arthritis research & therapy.

[50]  Stephanie J Bryant,et al.  Controlling the spatial distribution of ECM components in degradable PEG hydrogels for tissue engineering cartilage. , 2003, Journal of biomedical materials research. Part A.

[51]  Won C Bae,et al.  Depth-varying Density and Organization of Chondrocytes in Immature and Mature Bovine Articular Cartilage Assessed by 3D Imaging and Analysis , 2005, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[52]  Hinrich Wiese,et al.  Long-term stable fibrin gels for cartilage engineering. , 2007, Biomaterials.

[53]  S. Schwartz,et al.  CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathy-coxa vara-pericarditis syndrome , 1999, Nature Genetics.

[54]  K Masuda,et al.  Tissue engineering of stratified articular cartilage from chondrocyte subpopulations. , 2003, Osteoarthritis and cartilage.

[55]  J. Hubbell,et al.  Recombinant protein-co-PEG networks as cell-adhesive and proteolytically degradable hydrogel matrixes. Part I: Development and physicochemical characteristics. , 2005, Biomacromolecules.

[56]  N. Ahmed,et al.  Influence of cellular microenvironment and paracrine signals on chondrogenic differentiation. , 2007, Frontiers in bioscience : a journal and virtual library.

[57]  Phil G Campbell,et al.  Tissue engineering with the aid of inkjet printers , 2007, Expert opinion on biological therapy.

[58]  Albert C. Chen,et al.  Depth‐dependent confined compression modulus of full‐thickness bovine articular cartilage , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[59]  E B Hunziker,et al.  Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. , 1995, Journal of cell science.

[60]  J. Hubbell,et al.  Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering , 2005, Nature Biotechnology.

[61]  Matthias P Lutolf,et al.  Biomolecular hydrogels formed and degraded via site-specific enzymatic reactions. , 2007, Biomacromolecules.

[62]  Andrés J. García,et al.  Inhibition of in vitro chondrogenesis in RGD-modified three-dimensional alginate gels. , 2007, Biomaterials.

[63]  G. Ateshian,et al.  Dynamic deformational loading results in selective application of mechanical stimulation in a layered, tissue-engineered cartilage construct. , 2006, Biorheology.

[64]  G. Ateshian,et al.  A layered agarose approach to fabricate depth‐dependent inhomogeneity in chondrocyte‐seeded constructs , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[65]  I. Kiviranta,et al.  The zonal architecture of human articular cartilage described by T2 relaxation time in the presence of Gd-DTPA2-. , 2008, Magnetic resonance imaging.

[66]  M. Hincke,et al.  Fibrin: a versatile scaffold for tissue engineering applications. , 2008, Tissue engineering. Part B, Reviews.

[67]  Eben Alsberg,et al.  Photocrosslinked alginate hydrogels with tunable biodegradation rates and mechanical properties. , 2009, Biomaterials.

[68]  D K MacCallum,et al.  Culture and growth characteristics of chondrocytes encapsulated in alginate beads. , 1989, Connective tissue research.

[69]  Kam Leong,et al.  Designing zonal organization into tissue-engineered cartilage. , 2006, Tissue engineering.

[70]  Stephanie J Bryant,et al.  Incorporation of tissue-specific molecules alters chondrocyte metabolism and gene expression in photocrosslinked hydrogels. , 2005, Acta biomaterialia.

[71]  T. Segura,et al.  DNA delivery from matrix metalloproteinase degradable poly(ethylene glycol) hydrogels to mouse cloned mesenchymal stem cells. , 2009, Biomaterials.

[72]  L. Griffith,et al.  Capturing complex 3D tissue physiology in vitro , 2006, Nature Reviews Molecular Cell Biology.

[73]  Matthias P Lutolf,et al.  Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering. , 2007, Biomaterials.

[74]  Clemens A van Blitterswijk,et al.  Co‐culture in cartilage tissue engineering , 2007, Journal of tissue engineering and regenerative medicine.

[75]  K. Athanasiou,et al.  Retaining zonal chondrocyte phenotype by means of novel growth environments. , 2005, Tissue engineering.

[76]  Remo Guidieri Res , 1995, RES: Anthropology and Aesthetics.

[77]  Timothy M Wright,et al.  Image-guided tissue engineering of anatomically shaped implants via MRI and micro-CT using injection molding. , 2008, Tissue engineering. Part A.

[78]  A. Poole,et al.  Composition and structure of articular cartilage: a template for tissue repair. , 2001, Clinical orthopaedics and related research.