Tissue engineering of articular cartilage with biomimetic zones

Tissue Engineering - Part B: Reviews

Volumn 15, Issue 2, 2009, Pages 143-157

  Klein, Travis J ^a   Malda, Jos ^a,b   Sah, Robert L ^c   Hutmacher, Dietmar W ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGING POPULATION; ARTICULAR CARTILAGES; CARTILAGE TISSUE ENGINEERING; CLINICAL USE; ENGINEERED TISSUES; EXTRACELLULAR MATRICES; FUTURE PROSPECTS; NORMAL TISSUE;

BIOMIMETICS; CELL CULTURE; LIGAMENTS; RESTORATION; TISSUE ENGINEERING; ULTRASONIC MEASUREMENT;

CARTILAGE;

ARTICULAR CARTILAGE; BIOMIMETICS; EXTRACELLULAR MATRIX; IMPLANTATION; IN VITRO STUDY; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING;

ANIMALS; BIOMIMETIC MATERIALS; CARTILAGE, ARTICULAR; HUMANS; TISSUE ENGINEERING;

EID: 70349954683     PISSN: 19373368     EISSN: None     Source Type: Journal    
DOI: 10.1089/ten.teb.2008.0563     Document Type: Review

References (166)

1. Lawrence, R.C., Felson, D.T., Helmick, C.G., Arnold, L.M., Choi, H., Deyo, R.A., Gabriel, S., Hirsch, R., Hochberg, M.C., Hunder, G.G., Jordan, J.M., Katz, J.N., Kremers, H.M., and Wolfe, F. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum 58, 26, 2008.
2. Kim, S. Changes in surgical loads and economic burden of hip and knee replacements in the US: 1997-2004. Arthritis Rheum 59, 481, 2008.
3. Rasanen, P., Paavolainen, P., Sintonen, H., Koivisto, A.M., Blom, M., Ryynanen, O.P., and Roine, R.P. Effectiveness of hip or knee replacement surgery in terms of quality-adjusted life years and costs. Acta Orthop 78, 108, 2007.
4. Kurtz, S.M., Ong, K.L., Schmier, J., Mowat, F., Saleh, K., Dybvik, E., Karrholm, J., Garellick, G., Havelin, L.I., Furnes, O., Malchau, H., and Lau, E. Future clinical and economic impact of revision total hip and knee arthroplasty. J Bone Joint Surg Am 89 Suppl 3, 144, 2007.
5. Mont, M.A., and Schmalzried, T.P. Modern metal-on-metal hip resurfacing: important observations from the first ten years. J Bone Joint Surg Am 90 Suppl 3, 3, 2008.
6. Goldberg, V.M., and Caplan, A.I. Biological resurfacing: an alternative to total joint arthroplasty. Orthopedics 17, 819, 1994.
7. Ruano-Ravina, A., and Jato Diaz, M. Autologous chondrocyte implantation: a systematic review. Osteoarthritis Cartilage 14, 47, 2006.
8. Williams, D. Biocompatibility. In: Van Blitterswijk, C., Thomsen, P., Lindahl, A., Hubbell, J., Williams, D., Can-cedda, R., De Bruijn, J., and Sohier, J., eds. Tissue Engineering. Amsterdam: Elsevier, 2008, pp. 255-278.
9. Stockwell, R.A. The interrelationship of cell density and cartilage thickness in mammalian articular cartilage. J Anat 109, 411, 1971.
10. Hunziker, E.B., Quinn, T.M., and Hauselmann, H. Quantitative structural organization of normal adult human articular cartilage. Osteoarthritis Cartilage 10, 564, 2002.
11. Glowacki, J. In vitro engineering of cartilage. J Rehabil Res Dev 37, 171, 2000.
12. Brama, P.A., Tekoppele, J.M., Bank, R.A., Karssenberg, D., Barneveld, A., and van Weeren, P.R. Topographical mapping of biochemical properties of articular cartilage in the equine fetlock joint. Equine Vet J 32, 19, 2000.
13. Rogers, B.A., Murphy, C.L., Cannon, S.R., and Briggs, T.W. Topographical variation in glycosaminoglycan content in human articular cartilage. J Bone Joint Surg Br 88, 1670, 2006.
14. Hunziker, E.B. Biologic repair of articular cartilage. Defect models in experimental animals and matrix requirements. Clin Orthop Relat Res 367, S135, 1999.
15. Reinholz, G.G., Lu, L., Saris, D.B., Yaszemski, M.J., and O'Driscoll, S.W. Animal models for cartilage reconstruction. Biomaterials 25, 1511, 2004.
16. LeRoux, M.A., Arokoski, J., Vail, T.P., Guilak, F., Hyttinen, M.M., Kirivanta, K., and Setton, L.A. Simultaneous changes in the mechanical properties, quantitative collagen organization, and proteoglycan concentration of articular cartilage following canine meniscectomy. J Orthop Res 18, 383, 2000.
17. Poole, A.R., Kojima, T., Yasuda, T., Mwale, F., Kobayashi, M., and Laverty, S. Composition and structure of articular cartilage: a template for tissue repair. Clin Orthop 391 Suppl, S26, 2001.
18. Basser, P.J., Schneiderman, R., Bank, R.A., Wachtel, E., and Maroudas, A. Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. Arch Biochem Biophys 351, 207, 1998.
19. Eyre, D. Collagen of articular cartilage. Arthritis Res 4, 30, 2002.
20. Maroudas, A. Physico-chemical properties of articular cartilage. In: Freeman, M.A.R., ed. Adult Articular Cartilage. Tunbridge Wells, England: Pitman Medical, 1979, pp. 215-290.
21. Bank, R.A., Bayliss, M.T., Lafeber, F.P., Maroudas, A., and Tekoppele, J.M. Ageing and zonal variation in post-translational modification of collagen in normal human articular cartilage. The age-related increase in non-enzymatic glycation affects biomechanical properties of cartilage. Bio-chem J 330, 345, 1998.
22. Williamson, A.K., Chen, A.C., Masuda, K., Thonar, E.J.-M.A., and Sah, R.L. Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. J Orthop Res 21, 872, 2003.
23. Klein, T.J., Chaudhry, M., Bae, W.C., and Sah, R.L. Depth-dependent biomechanical and biochemical properties of fetal, newborn, and tissue-engineered articular cartilage. J Biomech 40, 182, 2007.
24. Palmer, A.W., Guldberg, R.E., and Levenston, M.E. Analysis of cartilage matrix fixed charge density and three-dimensional morphology via contrast-enhanced microcom-puted tomography. Proc Natl Acad Sci USA 103, 19255, 2006.
25. Aydelotte, M.B., Greenhill, R.R., and Kuettner, K.E. Differences between sub-populations of cultured bovine articular chondrocytes. II. Proteoglycan metabolism. Connect Tissue Res 18, 223, 1988.
26. Darling, E.M., Hu, J.C., and Athanasiou, K.A. Zonal and topographical differences in articular cartilage gene expression. J Orthop Res 22, 1182, 2004.
27. Schinagl, R.M., Gurskis, D., Chen, A.C., and Sah, R.L. Depth-dependent confined compression modulus of full-thickness bovine articular cartilage. J Orthop Res 15, 499, 1997.
28. Jadin, K.D., Wong, B.L., Bae, W.C., Li, K.W., Williamson, A.K., Schumacher, B.L., Price, J.H., and Sah, R.L. Depth-varying density and organization of chondrocytes in immature and mature bovine articular cartilage assessed by 3D imaging and analysis. J Histochem Cytochem 53, 1109, 2005.
29. Rolauffs, B., Williams, J.M., Grodzinsky, A.J., Kuettner, K.E., and Cole, A.A. Distinct horizontal patterns in the spatial organization of superficial zone chondrocytes of human joints. J Struct Biol 162, 335, 2008.
30. Swann, D.A., Sotman, S., Dixon, M., and Brooks, C. The isolation and partial characterization of the major glyco-protein (LGP-I) from the articular lubricating fraction of synovial fluid. Biochem J 161, 473, 1977.
31. Jay, G.D., Tantravahi, U., Britt, D.E., Barrach, H.J., and Cha, C.J. Homology of lubricin and superficial zone protein (SZP): products of megakaryocyte stimulating factor (MSF) gene expression by human synovial fibroblasts and articular chondrocytes localized to chromosome 1q25. J Orthop Res 19, 677, 2001.
32. Flannery, C.R., Hughes, C.E., Schumacher, B.L., Tudor, D., Aydelotte, M.B., Kuettner, K.E., and Caterson, B. Articular cartilage superficial zone protein (SZP) is homologous to megakaryocyte stimulating factor precursor and is a multifunctional proteoglycan with potential growth-promoting, cytoprotective, and lubricating properties in cartilage metabolism. Biochem Biophys Res Commun 254, 535, 1999.
33. Marcelino, J., Carpten, J.D., Suwairi, W.M., Gutierrez, O.M., Schwartz, S., Robbins, C., Sood, R., Makalowska, I., Bax-Evanis, A., Johnstone, B., Laxer, R.M., Zemel, L., Kim, C.A., Herd, J.K., Ihle, J., Williams, C., Johnson, M., Raman, V., Alonso, L.G., Brunoni, D., Gerstein, A., Papadopoulos, N., Bahabri, S.A., Trent, J.M., and Warman, M.L. CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathy-coxa vara-pericarditis syndrome. Nat Genet 23, 319, 1999.
34. Khan, I.M., Salter, D.M., Bayliss, M.T., Thomson, B.M., and Archer, C.W. Expression of clusterin in the superficial zone of bovine articular cartilage. Arthritis Rheum 44, 1795, 2001.
35. Connor, J.R., Kumar, S., Sathe, G., Mooney, J., O'Brien, S.P., Mui, P., Murdock, P.R., Gowen, M., and Lark, M.W. Clus-terin expression in adult human normal and osteoarthritic articular cartilage. Osteoarthritis Cartilage 9, 727, 2001.
36. Pfister, B.E., Aydelotte, M.B., Burkhart, W., Kuettner, K.E., and Schmid, T.M. Del1: a new protein in the superficial layer of articular cartilage. Biochem Biophys Res Commun 286, 268, 2001.
37. Woods, V.L., Jr., Schreck, P.J., Gesink, D.S., Pacheco, H.O., Amiel, D., Akeson, W.H., and Lotz, M. Integrin expression by human articular chondrocytes. Arthritis Rheum 37, 537, 1994.
38. Penta, K., Varner, J.A., Liaw, L., Hidai, C., Schatzman, R., and Quertermous, T. Del1 induces integrin signaling and angiogenesis by ligation of alphaVbeta3. J Biol Chem 274, 11101, 1999.
39. Karlsson, C., Stenhamre, H., Sandstedt, J., and Lindahl, A. Neither Notch1 expression nor cellular size correlate with mesenchymal stem cell properties of adult articular chon-drocytes. Cells Tissues Organs 187, 275, 2008.
40. Karlsson, C., Brantsing, C., Egell, S., and Lindahl, A. Notch1, Jagged1, and HES5 are abundantly expressed in osteoar-thritis. Cells Tissues Organs 188, 287, 2008.
41. Hayes, A.J., Dowthwaite, G.P., Webster, S.V., and Archer, C.W. The distribution of Notch receptors and their ligands during articular cartilage development. J Anat 202, 495, 2003.
42. Lorenzo, P., Bayliss, M.T., and Heinegard, D. A novel cartilage protein (CILP) present in the mid-zone of human articular cartilage increases with age. J Biol Chem 273, 23463, 1998.
43. Valdes, A.M., Hart, D.J., Jones, K.A., Surdulescu, G., Swar-brick, P., Doyle, D.V., Schafer, A.J., and Spector, T.D. Association study of candidate genes for the prevalence and progression of knee osteoarthritis. Arthritis Rheum 50, 2497, 2004.
44. Hirose, J., Ryan, L.M., and Masuda, I. Up-regulated expression of cartilage intermediate-layer protein and ANK in articular hyaline cartilage from patients with calcium pyro-phosphate dihydrate crystal deposition disease. Arthritis Rheum 46, 3218, 2002.
45. Seki, S., Kawaguchi, Y., Chiba, K., Mikami, Y., Kizawa, H., Oya, T., Mio, F., Mori, M., Miyamoto, Y., Masuda, I., Tsunoda, T., Kamata, M., Kubo, T., Toyama, Y., Kimura, T., Nakamura, Y., and Ikegawa, S. A functional SNP in CILP, encoding cartilage intermediate layer protein, is associated with susceptibility to lumbar disc disease. Nat Genet 37, 607, 2005.
46. Ustunel, I., Ozenci, A.M., Sahin, Z., Ozbey, O., Acar, N., Tanriover, G., Celik-Ozenci, C., and Demir, R. The immu-nohistochemical localization of notch receptors and ligands in human articular cartilage, chondroprogenitor culture and ultrastructural characteristics of these progenitor cells. Acta Histochem 110, 397, 2008.
47. Rucklidge, G.J., Milne, G., and Robins, S.P. Collagen type X: a component of the surface of normal human, pig, and rat articular cartilage. Biochem Biophys Res Commun 224, 297, 1996.
48. Gannon, J.M., Walker, G., Fischer, M., Carpenter, R., Thompson, R.C., Jr., and Oegema, T.R., Jr. Localization of type X collagen in canine growth plate and adult canine articular cartilage. J Orthop Res 9, 485, 1991.
49. Vunjak-Novakovic, G., Obradovic, B., Martin, I., Bursac, P.M., Langer, R., and Freed, L.E. Dynamic cell seeding of polymer scaffolds for cartilage tissue engineering. Biotechnol Prog 14, 193, 1998.
50. Genzyme. Carticel (autologous cultured chondrocytes)- package insert. Cambridge, MA, 2007.
51. Klein, T.J., Schumacher, B.L., Blewis, M.E., Schmidt, T.A., Voegtline, M.S., Thonar, E.J., Masuda, K., and Sah, R.L. Tailoring secretion of proteoglycan 4 (PRG4) in tissue-engineered cartilage. Tissue Eng 12, 1429, 2006.
52. Blewis, M.E., Schumacher, B.L., Klein, T.J., Schmidt, T.A., Voegtline, M.S., and Sah, R.L. Microenvironment regulation of PRG4 phenotype of chondrocytes. J Orthop Res 25, 685, 2007.
53. Wong, M., Wuethrich, P., Eggli, P., and Hunziker, E. Zone-specific cell biosynthetic activity in mature bovine articular cartilage: a new method using confocal microscopic stere-ology and quantitative autoradiography. J Orthop Res 14, 424, 1996.
54. Barbero, A., Ploegert, S., Heberer, M., and Martin, I. Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes. Arthritis Rheum 48, 1315, 2003.
55. Dowthwaite, G.P., Bishop, J.C., Redman, S.N., Khan, I.M., Rooney, P., Evans, D.J., Haughton, L., Bayram, Z., Boyer, S., Thompson, B., Wolfe, M.S., and Archer, C.W. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 117, 889, 2004.
56. Majumdar, M.K., Thiede, M.A., Mosca, J.D., Moorman, M., and Gerson, S.L. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J Cell Physiol 176, 57, 1998.
57. Hayes, A.J., Tudor, D., Nowell, M.A., Caterson, B., and Hughes, C.E. Chondroitin sulfate sulfation motifs as putative biomarkers for isolation of articular cartilage progenitor cells. J Histochem Cytochem 56, 125, 2008.
58. Richardson, K., Khan, I.M., and Archer, C.W. Identifying progenitor cells within articular cartilage. Eur Cell Mater 12, 70, 2006.
59. Hattori, S., Oxford, C., and Reddi, A.H. Identification of superficial zone articular chondrocyte stem=progenitor cells. Biochem Biophys Res Commun 358, 99, 2007.
60. Alsalameh, S., Amin, R., Gemba, T., and Lotz, M. Identification of mesenchymal progenitor cells in normal and os-teoarthritic human articular cartilage. Arthritis Rheum 50, 1522, 2004.
61. Fickert, S., Fiedler, J., and Brenner, R.E. Identification of sub-populations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Res Ther 6, R422, 2004.
62. Redman, S.N., Bateman, N., Haughton, L.M., Dowthwaite, G.P., Williams, A.S., and Archer, C.W. Evidence of a chon-droprogenitor population in human osteoarthritic cartilage. Eur Cell Mater 12, 69, 2006.
63. English, A., Jones, E.A., Corscadden, D., Henshaw, K., Chapman, T., Emery, P., and McGonagle, D. A comparative assessment of cartilage and joint fat pad as a potential source of cells for autologous therapy development in knee osteo-arthritis. Rheumatology (Oxf) 46, 1676, 2007.
64. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
65. Murdoch, A.D., Grady, L.M., Ablett, M.P., Katopodi, T., Meadows, R.S., and Hardingham, T.E. Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: generation of scaffold-free cartilage. Stem Cells 25, 2786, 2007.
66. Awad, H.A., Wickham, M.Q., Leddy, H.A., Gimble, J.M., and Guilak, F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25, 3211, 2004.
67. Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz, A.J., Benhaim, P., Lorenz, H.P., and Hedrick, M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7, 211, 2001.
68. Sakaguchi, Y., Sekiya, I., Yagishita, K., and Muneta, T. Comparison of human stem cells derived from various mes-enchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52, 2521, 2005.
69. Pei, M., He, F., and Vunjak-Novakovic, G. Synovium-derived stem cell-based chondrogenesis. Differentiation 76, 1044, 2008.
70. Sarugaser, R., Lickorish, D., Baksh, D., Hosseini, M.M., and Davies, J.E. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23, 220, 2005.
71. Wang, H.S., Hung, S.C., Peng, S.T., Huang, C.C., Wei, H.M., Guo, Y.J., Fu, Y.S., Lai, M.C., and Chen, C.C. Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. Stem Cells 22, 1330, 2004.
72. Rider, D.A., Dombrowski, C., Sawyer, A.A., Ng, G.H., Leong, D., Hutmacher, D.W., Nurcombe, V., and Cool, S.M. Autocrine fibroblast growth factor 2 increases the multi-potentiality of human adipose-derived mesenchymal stem cells. Stem Cells 26, 1598, 2008.
73. De Bari, C., Dell'Accio, F., Tylzanowski, P., and Luyten, F.P. Multipotent mesenchymal stem cells from adult human sy-novial membrane. Arthritis Rheum 44, 1928, 2001.
74. Kurth, T., Hedbom, E., Shintani, N., Sugimoto, M., Chen, F.H., Haspl, M., Martinovic, S., and Hunziker, E.B. Chon-drogenic potential of human synovial mesenchymal stem cells in alginate. Osteoarthritis Cartilage 15, 1178, 2007.
75. Pei, M., He, F., Kish, V.L., and Vunjak-Novakovic, G. Engineering of functional cartilage tissue using stem cells from synovial lining: a preliminary study. Clin Orthop Relat Res 466, 1880, 2008.
76. Schumacher, B.L., Hughes, C.E., Kuettner, K.E., Caterson, B., and Aydelotte, M.B. Immunodetection and partial cDNA sequence of the proteoglycan, superficial zone protein, synthesized by cells lining synovial joints. J Orthop Res 17, 110, 1999.
77. Darling, E.M., and Athanasiou, K.A. Retaining zonal chon-drocyte phenotype by means of novel growth environments. Tissue Eng 11, 395, 2005.
78. Grogan, S.P., Barbero, A., Winkelmann, V., Rieser, F., Fitz-simmons, J.S., O'Driscoll, S., Martin, I., and Mainil-Varlet, P. Visual histological grading system for the evaluation of in vitro-generated neocartilage. Tissue Eng 12, 2141, 2006.
79. Bonaventure, J., Kadhom, N., Cohen-Solal, L., Ng, K.H., Bourguignon, J., Lasselin, C., and Freisinger, P. Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads. Exp Cell Res 212, 97, 1994.
80. Masuda, K., Sah, R.L., Hejna, M.J., and Thonar, E.J. A novel two-step method for the formation of tissue-engineered cartilage by mature bovine chondrocytes: the alginate-recovered-chondrocyte (ARC) method. J Orthop Res 21, 139, 2003.
81. Masuda, K. Tissue engineered cartilage for biological repair of cartilage defects. Clin Calcium 14, 79, 2004.
82. Klein, T.J., Schumacher, B.L., Schmidt, T.A., Li, K.W., Voegt-line, M.S., Masuda, K., Thonar, E.J., and Sah, R.L. Tissue engineering of stratified articular cartilage from chondrocyte subpopulations. Osteoarthritis Cartilage 11, 595, 2003.
83. Yu, H., Grynpas, M., and Kandel, R.A. Composition of cartilagenous tissue with mineralized and non-mineralized zones formed in vitro. Biomaterials 18, 1425, 1997.
84. Waldman, S.D., Grynpas, M.D., Pilliar, R.M., and Kandel, R.A. The use of specific chondrocyte populations to modulate the properties of tissue-engineered cartilage. J Orthop Res 21, 132, 2003.
85. Kandel, R., Hurtig, M., and Grynpas, M. Characterization of the mineral in calcified articular cartilagenous tissue formed in vitro. Tissue Eng 5, 25, 1999.
86. Allan, K.S., Pilliar, R.M., Wang, J., Grynpas, M.D., and Kandel, R.A. Formation of biphasic constructs containing cartilage with a calcified zone interface. Tissue Eng 13, 167, 2007.
87. Hayes, A.J., Hall, A., Brown, L., Tubo, R., and Caterson, B. Macromolecular organization and in vitro growth characteristics of scaffold-free neocartilage grafts. J Histochem Cytochem 55, 853, 2007.
88. Steadman, J.R., Rodkey, W.G., and Rodrigo, J.J. Micro-fracture: surgical technique and rehabilitation to treat chon-dral defects. Clin Orthop Relat Res 391 Suppl, S362, 2001.
89. Knutsen, G., Engebretsen, L., Ludvigsen, T.C., Drogset, J.O., Grontvedt, T., Solheim, E., Strand, T., Roberts, S., Isaksen, V., and Johansen, O. Autologous chondrocyte implantation compared with microfracture in the knee. A randomized trial. J Bone Joint Surg Am 86-A, 455, 2004.
90. Hutmacher, D.W. Scaffolds in tissue engineering bone and cartilage. Biomaterials 21, 2529, 2000.
91. Wendt, D., Marsano, A., Jakob, M., Heberer, M., and Martin, I. Oscillating perfusion of cell suspensions through three-dimensional scaffolds enhances cell seeding efficiency and uniformity. Biotechnol Bioeng 84, 205, 2003.
92. Hutmacher, D.W., Sittinger, M., and Risbud, M.V. Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems. Trends Bio-technol 22, 354, 2004.
93. Woodfield, T.B., Van Blitterswijk, C.A., De Wijn, J., Sims, T.J., Hollander, A.P., and Riesle, J. Polymer scaffolds fabricated with pore-size gradients as a model for studying the zonal organization within tissue-engineered cartilage constructs. Tissue Eng 11, 1297, 2005.
94. Moutos, F.T., Freed, L.E., and Guilak, F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater 6, 162, 2007.
95. Chen, Z.C., Ekaputra, A.K., Gauthaman, K., Adaikan, P.G., Yu, H., and Hutmacher, D.W. In vitro and in vivo analysis of co-electrospun scaffolds made of medical grade poly(epsi-lon-caprolactone) and porcine collagen. J Biomater Sci Polym Ed 19, 693, 2008.
96. Li, W.J., Jiang, Y.J., and Tuan, R.S. Chondrocyte phenotype in engineered fibrous matrix is regulated by fiber size. Tissue Eng 12, 1775, 2006.
97. Li, W.J., Tuli, R., Okafor, C., Derfoul, A., Danielson, K.G., Hall, D.J., and Tuan, R.S. A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mes-enchymal stem cells. Biomaterials 26, 599, 2005.
98. Wise, J.K., Yarin, A.L., Megaridis, C.M., and Cho, M. Chondrogenic Differentiation of human mesenchymal stem cells on oriented nanofibrous scaffolds: engineering the superficial zone of articular cartilage. Tissue Eng A [Epub ahead of print]; Doi:10.1089=ten.tea.2008.0109.
99. Gooding, C.R., Bartlett, W., Bentley, G., Skinner, J.A., Car-rington, R., and Flanagan, A. A prospective, randomised study comparing two techniques of autologous chondrocyte implantation for osteochondral defects in the knee: periosteum covered versus type I=III collagen covered. Knee 13, 203, 2006.
100. Bartlett, W., Skinner, J.A., Gooding, C.R., Carrington, R.W., Flanagan, A.M., Briggs, T.W., and Bentley, G. Autologous chondrocyte implantation versus matrix-induced autolo-gous chondrocyte implantation for osteochondral defects of the knee: a prospective, randomised study. J Bone Joint Surg Br 87, 640, 2005.
101. Welsch, G.H., Mamisch, T.C., Domayer, S.E., Dorotka, R., Kutscha-Lissberg, F., Marlovits, S., White, L.M., and Trattnig, S. Cartilage T2 assessment at 3-T MR imaging: in vivo differentiation of normal hyaline cartilage from re-parative tissue after two cartilage repair procedures-initial experience. Radiology 247, 154, 2008.
102. White, L.M., Sussman, M.S., Hurtig, M., Probyn, L., Tom-linson, G., and Kandel, R. Cartilage T2 assessment: differentiation of normal hyaline cartilage and reparative tissue after arthroscopic cartilage repair in equine subjects. Radiology 241, 407, 2006.
103. Singh, M., Berkland, C., and Detamore, M.S. Strategies and applications for incorporating physical and chemical signal gradients in tissue engineering. Tissue Eng B Rev 14, 341, 2008.
104. Yamamoto, M., Yanase, K., and Tabata, Y. Fabrication of three-dimensional cell scaffolds with spatial gradients of biomolecules. Inflamm Regen 27, 102, 2007.
105. Sherwood, J., Riley, S., Palazzolo, R., Brown, S., Monkhouse, D., Coates, M., Griffith, L., Landeen, L., and Ratcliffe, A. A three-dimensional osteochondral composite scaffold for articular cartilage repair. Biomaterials 23, 4739, 2002.
106. Suciati, T., Howard, D., Barry, J., Everitt, N.M., Shakesheff, K.M., and Rose, F.R. Zonal release of proteins within tissue engineering scaffolds. J Mater Sci Mater Med 17, 1049, 2006.
107. Singh, M., Morris, C.P., Ellis, R.J., Detamore, M.S., and Berkland, C. Microsphere-based seamless scaffolds containing macroscopic gradients of encapsulated factors for tissue engineering. Tissue Eng C Methods 14, 299, 2008.
108. Hung, C.T., Lima, E.G., Mauck, R.L., Taki, E., LeRoux, M.A., Lu, H.H., Stark, R.G., Guo, X.E., and Ateshian, G.A. Anatomically shaped osteochondral constructs for articular cartilage repair. J Biomech 36, 1853, 2003.
109. Alhadlaq, A., and Mao, J.J. Tissue-engineered neogenesis of human-shaped mandibular condyle from rat mesenchymal stem cells. J Dent Res 82, 951, 2003.
110. Pluen, A., Netti, P.A., Jain, R.K., and Berk, D.A. Diffusion of macromolecules in agarose gels: comparison of linear and globular configurations. Biophys J 77, 542, 1999.
111. Benya, P.D., and Shaffer, J.D. Dedifferentiated chon-drocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30, 215, 1982.
112. Domm, C., Schunke, M., Christesen, K., and Kurz, B. Re-differentiation of dedifferentiated bovine articular chon-drocytes in alginate culture under low oxygen tension. Osteoarthritis Cartilage 10, 13, 2002.
113. Lynn, A.K., Yannas, I.V., and Bonfield, W. Antigenicity and immunogenicity of collagen. J Biomed Mater Res B Appl Biomater 71, 343, 2004.
114. Mimura, T., Imai, S., Kubo, M., Isoya, E., Ando, K., Oku-mura, N., and Matsusue, Y. A novel exogenous concentration-gradient collagen scaffold augments full-thickness articular cartilage repair. Osteoarthritis Cartilage 16, 1083, 2008.
115. Ng, K.W., Wang, C.C., Mauck, R.L., Kelly, T.N., Chahine, N.O., Costa, K.D., Ateshian, G.A., and Hung, C.T. A layered agarose approach to fabricate depth-dependent inho-mogeneity in chondrocyte-seeded constructs. J Orthop Res 23, 134, 2005.
116. Gleghorn, J.P., Jones, A.R., Flannery, C.R., and Bonassar, L.J. Boundary mode frictional properties of engineered cartilaginous tissues. Eur Cell Mater 14, 20, 2007.
117. Selmi, T.A., Verdonk, P., Chambat, P., Dubrana, F., Potel, J.F., Barnouin, L., and Neyret, P. Autologous chondrocyte implantation in a novel alginate-agarose hydrogel: outcome at two years. J Bone Joint Surg Br 90, 597, 2008.
118. Elisseeff, J., Anseth, K., Sims, D., McIntosh, W., Randolph, M., and Langer, R. Transdermal photopolymerization for minimally invasive implantation. Proc Natl Acad Sci USA 96, 3104, 1999.
119. Kim, T.K., Sharma, B., Williams, C.G., Ruffner, M.A., Malik, A., McFarland, E.G., and Elisseeff, J.H. Experimental model for cartilage tissue engineering to regenerate the zonal organization of articular cartilage. Osteoarthritis Cartilage 11, 653, 2003.
120. Rizzi, S.C., and Hubbell, J.A. Recombinant protein-co-PEG networks as cell-adhesive and proteolytically degradable hydrogel matrixes. Part I: Development and physicochem-ical characteristics. Biomacromolecules 6, 1226, 2005.
121. Lutolf, M.P., Lauer-Fields, J.L., Schmoekel, H.G., Metters, A.T., Weber, F.E., Fields, G.B., and Hubbell, J.A. Synthetic matrix metalloproteinase- sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci USA 100, 5413, 2003.
122. Kisiday, J., Jin, M., Kurz, B., Hung, H., Semino, C., Zhang, S., and Grodzinsky, A.J. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair. Proc Natl Acad Sci USA 99, 9996, 2002.
123. Hwang, N.S., Varghese, S., Lee, H.J., Theprungsirikul, P., Canver, A., Sharma, B., and Elisseeff, J. Response of zonal chondrocytes to extracellular matrix-hydrogels. FEBS Lett 581, 4172, 2007.
124. Sharma, B., and Elisseeff, J.H. Engineering structurally organized cartilage and bone tissues. Ann Biomed Eng 32, 148, 2004.
125. Mironov, V., Reis, N., and Derby, B. Review: bioprinting: a beginning. Tissue Eng 12, 631, 2006.
126. Cohen, D.L., Malone, E., Lipson, H., and Bonassar, L.J. Direct freeform fabrication of seeded hydrogels in arbitrary geometries. Tissue Eng 12, 1325, 2006.
127. Fedorovich, N.E., Alblas, J., de Wijn, J.R., Hennink, W.E., Verbout, A.J., and Dhert, W.J. Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. Tissue Eng 13, 1905, 2007.
128. Campbell, P.G., and Weiss, L.E. Tissue engineering with the aid of inkjet printers. Expert Opin Biol Ther 7, 1123, 2007.
129. Fedorovich, N.E., De Wijn, J.R., Verbout, A.J., Alblas, J., and Dhert, W.J. Three-dimensional fiber deposition of cell-laden, viable, patterned constructs for bone tissue printing. Tissue Eng A 14, 127, 2008.
130. Chang, R., Nam, J., and Sun, W. Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. Tissue Eng A 14, 41, 2008.
131. Li, K.W., Klein, T.J., Chawla, K., Nugent, G.E., Bae, W.C., and Sah, R.L. In vitro physical stimulation of tissue-engineered and native cartilage. Methods Mol Med 100, 325, 2004.
132. Schmidt, T.A., Schumacher, B.L., Han, E.H., Klein, T.J., Voegtline, M.S., and Sah, R.L. Chemo-mechanical coupling in articular cartilage: IL-1a and TGF-b1 regulate chon-drocyte synthesis and secretion of lubricin=superficial zone protein. In: Aaron, R.K., and Bolander, M.E., eds. Physical Regulation of Skeletal Repair. Chicago: American Academy of Orthopaedic Surgeons, 2005, pp. 151-162.
133. Niikura, T., and Reddi, A.H. Differential regulation of lubricin=superficial zone protein by transforming growth factor beta=bone morphogenetic protein superfamily members in articular chondrocytes and synoviocytes. Arthritis Rheum 56, 2312, 2007.
134. Khalafi, A., Schmid, T.M., Neu, C., and Reddi, A.H. Increased accumulation of superficial zone protein (SZP) in articular cartilage in response to bone morphogenetic pro-tein-7 and growth factors. J Orthop Res 25, 293, 2007.
135. Jones, A.R., and Flannery, C.R. Bioregulation of lubricin expression by growth factors and cytokines. Eur Cell Mater 13, 40, 2007.
136. Ehrbar, M., Rizzi, S.C., Hlushchuk, R., Djonov, V., Zisch, A.H., Hubbell, J.A., Weber, F.E., and Lutolf, M.P. Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering. Biomaterials 28, 3856, 2007.
137. Sucosky, P., Osorio, D.F., Brown, J.B., and Neitzel, G.P. Fluid mechanics of a spinner-flask bioreactor. Biotechnol Bioeng 85, 34, 2004.
138. Begley, C.M., and Kleis, S.J. The fluid dynamic and shear environment in the NASA=JSC rotating-wall perfused-vessel bioreactor. Biotechnol Bioeng 70, 32, 2000.
139. Heyland, J., Wiegandt, K., Goepfert, C., Nagel-Heyer, S., Ilinich, E., Schumacher, U., and Portner, R. Redifferentia-tion of chondrocytes and cartilage formation under intermittent hydrostatic pressure. Biotechnol Lett 28, 1641, 2006.
140. Raimondi, M.T., Boschetti, F., Falcone, L., Migliavacca, F., Remuzzi, A., and Dubini, G. The effect of media perfusion on three-dimensional cultures of human chondrocytes: integration of experimental and computational approaches. Biorheology 41, 401, 2004.
141. Galban, C.J., and Locke, B.R. Effects of spatial variation of cells and nutrient and product concentrations coupled with product inhibition on cell growth in a polymer scaffold. Biotechnol Bioeng 64, 633, 1999.
142. Vunjak-Novakovic, G., Obradovic, B., Martin, I., and Freed, L.E. Bioreactor studies of native and tissue engineered cartilage. Biorheology 39, 259, 2002.
143. Marsano, A., Wendt, D., Quinn, T.M., Sims, T.J., Farhadi, J., Jakob, M., Heberer, M., and Martin, I. Bi-zonal cartilaginous tissues engineered in a rotary cell culture system. Biorheology 43, 553, 2006.
144. Mizuno, S. A novel method for assessing effects of hydrostatic fluid pressure on intracellular calcium: a study with bovine articular chondrocytes. Am J Physiol Cell Physiol 288, C329, 2005.
145. Davisson, T.H., Sah, R.L., and Ratcliffe, A.R. Perfusion increases cell content and matrix synthesis in chondrocyte three-dimensional cultures. Tissue Eng 8, 807, 2002.
146. Dunkelman, N.S., Zimber, M.P., LeBaron, R.G., Pavelec, R., Kwan, M., and Purchio, A.F. Cartilage production by rabbit articular chondrocytes on polyglycolic acid scaffolds in a closed bioreactor system. Biotechnol Bioeng 46, 299, 1995.
147. Vanderploeg, E.J., Wilson, C.G., and Levenston, M.E. Articular chondrocytes derived from distinct tissue zones differentially respond to in vitro oscillatory tensile loading. Osteoarthritis Cartilage 16, 1228, 2008.
148. Mauck, R.L., Soltz, M.A., Wang, C.C., Wong, D.D., Chao, P.H., Valhmu, W.B., Hung, C.T., and Ateshian, G.A. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122, 252, 2000.
149. Davisson, T., Kunig, S., Chen, A., Sah, R., and Ratcliffe, A. Static and dynamic compression modulate matrix metabolism in tissue engineered cartilage. J Orthop Res 20, 842, 2002.
150. Demarteau, O., Wendt, D., Braccini, A., Jakob, M., Schafer, D., Heberer, M., and Martin, I. Dynamic compression of cartilage constructs engineered from expanded human articular chondrocytes. Biochem Biophys Res Commun 310, 580, 2003.
151. Ng, K.W., Mauck, R.L., Statman, L.Y., Lin, E.Y., Ateshian, G.A., and Hung, C.T. Dynamic deformational loading results in selective application of mechanical stimulation in a layered, tissue-engineered cartilage construct. Biorheology 43, 497, 2006.
152. Lima, E.G., Mauck, R.L., Han, S.H., Park, S., Ng, K.W., Ateshian, G.A., and Hung, C.T. Functional tissue engineering of chondral and osteochondral constructs. Bio-rheology 41, 577, 2004.
153. Grad, S., Lee, C.R., Gorna, K., Gogolewski, S., Wimmer, M.A., and Alini, M. Surface motion upregulates superficial zone protein and hyaluronan production in chondrocyte-seeded three-dimensional scaffolds. Tissue Eng 11, 249, 2005.
154. Nugent-Derfus, G.E., Takara, T., O'Neill J, K., Cahill, S.B., Gortz, S., Pong, T., Inoue, H., Aneloski, N.M., Wang, W.W., Vega, K.I., Klein, T.J., Hsieh-Bonassera, N.D., Bae, W.C., Burke, J.D., Bugbee, W.D., and Sah, R.L. Continuous passive motion applied to whole joints stimulates chondrocyte biosynthesis of PRG4. Osteoarthritis Cartilage 15, 566, 2007.
155. Ostrander, R.V., Goomer, R.S., Tontz, W.L., Khatod, M., Harwood, F.L., Maris, T.M., and Amiel, D. Donor cell fate in tissue engineering for articular cartilage repair. Clin Orthop Relat Res 389, 228, 2001.
156. Mierisch, C.M., Wilson, H.A., Turner, M.A., Milbrandt, T.A., Berthoux, L., Hammarskjold, M.L., Rekosh, D., Balian, G., and Diduch, D.R. Chondrocyte transplantation into articular cartilage defects with use of calcium alginate: the fate of the cells. J Bone Joint Surg Am 85-A, 1757, 2003.
157. Chawla, K., Klein, T.J., Schumacher, B.L., Jadin, K.D., Shah, B.H., Nakagawa, K., Wong, V.W., Chen, A.C., Masuda, K., and Sah, R.L. Short-term retention of labeled chondrocyte subpopulations in stratified tissue-engineered cartilaginous constructs implanted in vivo in mini-pigs. Tissue Eng 13, 1525, 2007.
158. Obradovic, B., Martin, I., Padera, R.F., Treppo, S., Freed, L.E., and Vunjak-Novakovic, G. Integration of engineered cartilage. J Orthop Res 19, 1089, 2001.
159. Caterson, B., Flannery, C.R., Hughes, C.E., and Little, C.B. Mechanisms involved in cartilage proteoglycan catabolism. Matrix Biol 19, 333, 2000.
160. Xia, Y., Moody, J.B., Alhadlaq, H., and Hu, J. Imaging the physical and morphological properties of a multi-zone young articular cartilage at microscopic resolution. J Magn Reson Imaging 17, 365, 2003.
161. Gillis, A., Bashir, A., McKeon, B., Scheller, A., Gray, M.L., and Burstein, D. Magnetic resonance imaging of relative glycosaminoglycan distribution in patients with autolo-gous chondrocyte transplants. Invest Radiol 36, 743, 2001.
162. Lee, J., Cuddihy, M.J., and Kotov, N.A. Three-dimensional cell culture matrices: state of the art. Tissue Eng B Rev 14, 61, 2008.
163. Griffith, L.G., and Naughton, G. Tissue engineering- current challenges and expanding opportunities. Science 295, 1009, 2002.
164. Hollander, A.P., Pidoux, I., Reiner, A., Rorabeck, C., Bourne, R., and Poole, A.R. 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. J Clin Invest 96, 2859, 1995.
165. Kurkijarvi, J.E., Nissi, M.J., Rieppo, J., Toyras, J., Kiviranta, I., Nieminen, M.T., and Jurvelin, J.S. The zonal architecture of human articular cartilage described by T2 relaxation time in the presence of Gd-DTPA2. Magn Reson Imaging 26, 602, 2008.
166. Roberts, S., McCall, I.W., Darby, A.J., Menage, J., Evans, H., Harrison, P.E., and Richardson, J.B. Autologous chon-drocyte implantation for cartilage repair: monitoring its success by magnetic resonance imaging and histology. Arthritis Res Ther 5, R60, 2003.