Advanced strategies for articular cartilage defect repair

Materials

Volumn 6, Issue 2, 2013, Pages 637-668

  Matsiko, Amos ^a,b   Levingstone, Tanya J ^a,b   O'Brien, Fergal J ^a,b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Articular cartilage; Biomaterials; Chondrogenesis; Scaffolds; Tissue engineering

Indexed keywords

ARTICULAR CARTILAGE DEFECT REPAIR; ARTICULAR CARTILAGE REPAIR; ARTICULAR CARTILAGES; CHONDROGENESIS; FUNCTIONAL PROPERTIES; GROWTH FACTOR DELIVERY; PHYSICOCHEMICAL PROPERTY; REGENERATIVE CAPACITY;

BIOACTIVITY; BIOMATERIALS; CARTILAGE; CHEMICAL PROPERTIES; RESTORATION; SCAFFOLDS; TISSUE; TISSUE ENGINEERING;

SCAFFOLDS (BIOLOGY);

EID: 84875784036     PISSN: None     EISSN: 19961944     Source Type: Journal    
DOI: 10.3390/ma6020637     Document Type: Article

References (171)

1. Temenoff, J.S.; Mikos, A.G. Review: Tissue engineering for regeneration of articular cartilage. Biomaterials 2000, 21, 431-440.
2. Adam, C.; Eckstein, F.; Milz, S.; Schulte, E.; Becker, C.; Putz, R. The distribution of cartilage thickness in the knee-joints of old-aged individuals-Measurement by A-mode ultrasound. Clin. Biomech. 1998, 13, 1-10.
3. Kovach, I.S. A molecular theory of cartilage viscoelasticity. Biophys. Chem. 1996, 59, 61-73.
4. Soltz, M.A.; Ateshian, G.A. Interstitial fluid pressurization during confined compression cyclical loading of articular cartilage. Ann. Biomed. Eng. 2000, 28, 150-159.
5. Eyre, D. Collagen of articular cartilage. Arthritis Res. 2002, 4, 30-35.
6. Newman, A.P. Articular cartilage repair. Am. J. Sports Med. 1998, 26, 309-324.
7. Hunziker, E.B. Articular cartilage repair: Are the intrinsic biological constraints undermining this process insuperable? Osteoarthr. Cartil. 1999, 7, 15-28.
8. Shapiro, F.; Koide, S.; Glimcher, M.J. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J. Bone Joint Surg. 1993, 75, 532-553.
9. Beris, A.E.; Lykissas, M.G.; Papageorgiou, C.D.; Georgoulis, A.D. Advances in articular cartilage repair. Injury 2005, 36, S14-S23.
10. Behrens, P.; Bitter, T.; Kurz, B.; Russlies, M. Matrix-associated autologous chondrocyte transplantation/implantation (MACT/MACI)-5-year follow-up. Knee 2006, 13, 194-202.
11. Brittberg, M.; Lindahl, A.; Nilsson, A.; Ohlsson, C.; Isaksson, O.; Peterson, L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. New Engl. J. Med. 1994, 331, 889-895.
12. Kon, E.; Verdonk, P.; Condello, V.; Delcogliano, M.; Dhollander, A.; Filardo, G.; Pignotti, E.; Marcacci, M. Matrix-assisted autologous chondrocyte transplantation for the repair of cartilage defects of the knee. Am. J. Sports Med. 2009, 37, 156S-166S.
13. Plewes, L.W. Osteo-arthritis of the hip. Br. J. Surg. 1940, 27, 682-695.
14. Ghadially, J.A.; Ghadially, R.; Ghadially, F.N. Long-term results of deep defects in articular cartilage. Virchows Arch. B 1977, 25, 125-136.
15. Mankin, H.J. The response of articular cartilage to mechanical injury. J. Bone Joint Surg. Ser. A 1982, 64, 460-466.
16. Buckwalter, J.A. Chondral and osteochondral injuries: Mechanisms of injury and repair responses. Oper. Tech. Orthop. 1997, 7, 263-269.
17. Bekkers, J.E.J.; de Windt, T.S.; Brittberg, M.; Saris, D.B.F. Cartilage repair in football (soccer) athletes: What evidence leads to which treatment? A critical review of the literature. Cartilage 2012, 3, 43S-49S.
18. Cole, B.J.; Pascual-Garrido, C.; Grumet, R.C. Surgical management of articular cartilage defects in the knee. J. Bone Joint Surg. 2009, 91, 1778-1790.
19. Detterline, A.J.; Goldberg, S.; Bach, B.R., Jr.; Cole, B.J. Treatment Options for Articular Cartilage Defects of the Knee. Orthop. Nurs. 2005, 24, 361-366.
20. Owens, B.D.; Stickles, B.J.; Balikian, P.; Busconi, B.D. Prospective analysis of radiofrequency versus mechanical debridement of isolated patellar chondral lesions. Arthroscopy 2002, 18, 151-155.
21. Knutsen, G.; Engebretsen, L.; Ludvigsen, T.C.; Drogset, J.O.; Grøntvedt, T.; Solheim, E.; Strand, T.; Roberts, S.; Isaksen, V.; Johansen, O. Autologous chondrocyte implantation compared with microfracture in the knee: A randomized trial. J. Bone Joint Surg. 2004, 86, 455-464.
22. Steadman, J.R.; Briggs, K.K.; Rodrigo, J.J.; Kocher, M.S.; Gill, T.J.; Rodkey, W.G. Outcomes of microfracture for traumatic chondral defects of the knee: Average 11-year follow-up. Arthroscopy 2003, 19, 477-484.
23. Kon, E.; Gobbi, A.; Filardo, G.; Delcogliano, M.; Zaffagnini, S.; Marcacci, M. Arthroscopic second-generation autologous chondrocyte implantation compared with microfracture for chondral lesions of the knee. Am. J. Sports Med. 2009, 37, 33-41.
24. Mithoefer, K.; McAdams, T.; Williams, R.J.; Kreuz, P.C.; Mandelbaum, B.R. Clinical efficacy of the microfracture technique for articular cartilage repair in the knee: an evidence-based systematic analysis. Am. J. Sports Med. 2009, 37, 2053-2063.
25. Saris, D.B.F.; Vanlauwe, J.; Victor, J.; Almqvist, K.F.; Verdonk, R.; Bellemans, J.; Luyten, F.P. Treatment of symptomatic cartilage defects of the knee. Am. J. Sports Med. 2009, 37, 10S-19S.
26. Minas, T. Nonarthroplasty management of knee arthritis in the young individual. Curr. Opin. Orthop. 1998, 9, 46-52.
27. Peterson, L.; Vasiliadis, H.S.; Brittberg, M.; Lindahl, A. Autologous chondrocyte implantation. Am. J. Sports Med. 2010, 38, 1117-1124.
28. Erggelet, C.; Endres, M.; Neumann, K.; Morawietz, L.; Ringe, J.; Haberstroh, K.; Sittinger, M.; Kaps, C. Formation of cartilage repair tissue in articular cartilage defects pretreated with microfracture and covered with cell-free polymer-based implants. J. Orthop. Res. 2009, 27, 1353-1360.
29. Gigante, A.; Cecconi, S.; Calcagno, S.; Busilacchi, A.; Enea, D. Arthroscopic knee cartilage repair with covered microfracture and bone marrow concentrate. Arthros. Tech. 2012, 1, e175-e180.
30. Bentley, G.; Biant, L.C.; Vijayan, S.; Macmull, S.; Skinner, J.A.; Carrington, R.W.J. Minimum ten-year results of a prospective randomised study of autologous chondrocyte implantation versus mosaicplasty for symptomatic articular cartilage lesions of the knee. J. Bone Joint Surg. Br. 2012, 94B, 504-509.
31. Huang, F.S.; Simonian, P.T.; Norman, A.G.; Clark, J.M. Effects of small incongruities in a sheep model of osteochondral autografting. Am. J. Sports Med. 2004, 32, 1842-1848.
32. Cascio, B.M.; Sharma, B. The future of cartilage repair. Oper. Tech. Sports Med. 2008, 16, 221-224.
33. Getgood, A.; Bhullar, T.P.S.; Rushton, N. Current concepts in articular cartilage repair. Orthop. Trauma 2009, 23, 189-200.
34. Fischman, J. How to build a body part. Time Magazine, 1 March 1999, Available online: http://www.time.com/time/magazine/article/0,9171,20592,00.html (Accessed on 1 December 2012).
35. Rawe, J. What will be the 10 hottest jobs? Time Magazine, 22 May 2000, Available online: http://www.time.com/time/magazine/article/0,9171,997028,00.html (Accessed on 1 December 2012).
36. Lyons, F.; Partap, S.; O'Brien, F.J. Part 1: Scaffolds and surfaces. Technol. Health Care 2008, 16, 305-317.
37. Fritz, J.R.; Pelaez, D.; Cheung, H.S. Current challenges in cartilage tissue engineering: A review of current cellular-based therapies. Curr. Rheumatol. Rev. 2009, 5, 8-14.
38. Matsiko, A.; Levingstone, T.J.; O'Brien, F.J.; Gleeson, J.P. Addition of hyaluronic acid improves cellular infiltration and promotes early-stage chondrogenesis in a collagen-based scaffold for cartilage tissue engineering. J. Mech. Behav. Biomed. Mater. 2012, 11, 41-52.
39. Hunziker, E.B. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthr. Cartil. 2002, 10, 432-463.
40. Appelman, T.P.; Mizrahi, J.; Elisseeff, J.H.; Seliktar, D. The influence of biological motifs and dynamic mechanical stimulation in hydrogel scaffold systems on the phenotype of chondrocytes. Biomaterials 2011, 32, 1508-1516.
41. Schuh, E.; Hofmann, S.; Stok, K.; Notbohm, H.; Müller, R.; Rotter, N. Chondrocyte redifferentiation in 3D: The effect of adhesion site density and substrate elasticity. J. Biomed. Mater. Res. A 2012, 100A, 38-47.
42. Frisbie, D.D.; Bowman, S.M.; Colhoun, H.A.; DiCarlo, E.F.; Kawcak, C.E.; McIlwraith, C.W. Evaluation of autologous chondrocyte transplantation via a collagen membrane in equine articular defects - results at 12 and 18 months. Osteoarthr. Cartil. 2008, 16, 667-679.
43. Driesang, I.M.; Hunziker, E.B. Delamination rates of tissue flaps used in articular cartilage repair. J. Orthop. Res. 2000, 18, 909-911.
44. Niemeyer, P.; Pestka, J.M.; Kreuz, P.C.; Erggelet, C.; Schmal, H.; Suedkamp, N.P.; Steinwachs, M. Characteristic complications after autologous chondrocyte implantation for cartilage defects of the knee joint. Am. J. Sports Med. 2008, 36, 2091-2099.
45. Zaslav, K.; Cole, B.; Brewster, R.; DeBerardino, T.; Farr, J.; Fowler, P.; Nissen, C. A prospective study of autologous chondrocyte implantation in patients with failed prior treatment for articular cartilage defect of the knee: Results of the Study of the Treatment of Articular Repair (STAR) clinical trial. Am. J. Sports Med. 2009, 37, 42-55.
46. Mithoefer, K.; Hambly, K.; Villa, S.D.; Silvers, H.; Mandelbaum, B.R. Return to sports participation after articular cartilage repair in the knee. Am. J. Sports Med. 2009, 37, 167S-176S.
47. Gooding, C.R.; Bartlett, W.; Bentley, G.; Skinner, J.A.; Carrington, R.; 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 2006, 13, 203-210.
48. Krishnan, S.P.; Skinner, J.A.; Carrington, R.W.; Flanagan, A.M.; Briggs, T.W.; Bentley, G. Collagen-covered autologous chondrocyte implantation for osteochondritis dissecans of the knee: Two- to seven-year results. J. Bone Joint Surg. Br. 2006, 88, 203-205.
49. Robertson, W.B.; Fick, D.; Wood, D.J.; Linklater, J.M.; Zheng, M.H.; Ackland, T.R. MRI and clinical evaluation of collagen-covered autologous chondrocyte implantation (CACI) at two years. Knee 2007, 14, 117-127.
50. Haddo, O.; Mahroof, S.; Higgs, D.; David, L.; Pringle, J.; Bayliss, M.; Cannon, S.R.; Briggs, T.W. The use of chondrogide membrane in autologous chondrocyte implantation. Knee 2004, 11, 51-55.
51. Briggs, T.W.; Mahroof, S.; David, L.A.; Flannelly, J.; Pringle, J.; Bayliss, M. Histological evaluation of chondral defects after autologous chondrocyte implantation of the knee. J. Bone Joint Surg. Br. 2003, 85, 1077-1083.
52. Steinwachs, M.R.; Guggi, T.; Kreuz, P.C. Marrow stimulation techniques. Injury 2008, 39, S26-S31.
53. Filardo, G.; Vannini, F.; Marcacci, M.; Andriolo, L.; Ferruzzi, A.; Giannini, S.; Kon, E. Matrix-assisted autologous chondrocyte transplantation for cartilage regeneration in osteoarthritic knees. Am. J. Sports Med. 2012, 41, 95-100.
54. Zheng, M.H.; Willers, C.; Kirilak, L.; Yates, P.; Xu, J.; Wood, D.; Shimmin, A. Matrix-induced autologous chondrocyte implantation (MACI): Biological and histological assessment. Tissue Eng. 2007, 13, 737-746.
55. Ehlers, E.M.; Fuss, M.; Rohwedel, J.; Russlies, M.; Kuhnel, W.; Behrens, P. Development of a biocomposite to fill out articular cartilage lesions. Light, scanning and transmission electron microscopy of sheep chondrocytes cultured on a collagen I/III sponge. Ann. Anat. 1999, 181, 513-518.
56. Cherubino, P.; Grassi, F.A.; Bulgheroni, P.; Ronga, M. Autologous chondrocyte implantation using a bilayer collagen membrane: A preliminary report. J. Orthop. Surg. 2003, 11, 10-15.
57. Benya, P.D.; Shaffer, J.D. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 1982, 30, 215-224.
58. Marcacci, M.; Berruto, M.; Brocchetta, D.; Delcogliano, A.; Ghinelli, D.; Gobbi, A.; Kon, E.; Pederzini, L.; Rosa, D.; Sacchetti, G.L.; Stefani, G.; Zanasi, S. Articular cartilage engineering with Hyalograft C: 3-year clinical results. Clin. Orthop. Relat. Res. 2005, 96-105.
59. Steinert, A.F.; Ghivizzani, S.C.; Rethwilm, A.; Tuan, R.S.; Evans, C.H.; Noth, U. Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res. Ther. 2007, 9, doi:10.1186/ar2195.
60. Dell'Accio, F.; Vanlauwe, J.; Bellemans, J.; Neys, J.; de Bari, C.; Luyten, F.P. Expanded phenotypically stable chondrocytes persist in the repair tissue and contribute to cartilage matrix formation and structural integration in a goat model of autologous chondrocyte implantation. J. Orthop. Res. 2003, 21, 123-131.
61. Wood, J.J.; Malek, M.A.; Frassica, F.J.; Polder, J.A.; Mohan, A.K.; Bloom, E.T.; Braun, M.M.; Coté, T.R. Autologous cultured chondrocytes: adverse events reported to the United States Food and Drug Administration. J. Bone Joint Surg. Am. 2006, 88, 503-507.
62. Selmi, T.A.; Verdonk, P.; Chambat, P.; Dubrana, F.; Potel, J.F.; Barnouin, L.; Neyret, P. Autologous chondrocyte implantation in a novel alginate-agarose hydrogel: Outcome at two years. J. Bone Joint Surg. Br. 2008, 90, 597-604.
63. Barry, F.; Boynton, R.E.; Liu, B.; Murphy, J.M. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: Differentiation-dependent gene expression of matrix components. Exp. Cell Res. 2001, 268, 189-200.
64. Caplan, A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 2007, 213, 341-347.
65. 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.; Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284, 143-147.
66. Devine, S.M.; Bartholomew, A.M.; Mahmud, N.; Nelson, M.; Patil, S.; Hardy, W.; Sturgeon, C.; Hewett, T.; Chung, T.; Stock, W.; Sher, D.; Weissman, S.; Ferrer, K.; Mosca, J.; Deans, R.; Moseley, A.; Hoffman, R. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp. Hematol. 2001, 29, 244-255.
67. Beyth, S.; Borovsky, Z.; Mevorach, D.; Liebergall, M.; Gazit, Z.; Aslan, H.; Galun, E.; Rachmilewitz, J. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005, 105, 2214-2219.
68. Chen, L.; Tredget, E.E.; Wu, P.Y.; Wu, Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008, 3, doi:10.1371/journal.pone.0001886.
69. Shi, Y.; Hu, G.; Su, J.; Li, W.; Chen, Q.; Shou, P.; Xu, C.; Chen, X.; Huang, Y.; Zhu, Z.; Huang, X.; Han, X.; Xie, N.; Ren, G. Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Res. 2010, 20, 510-518.
70. Mueller, S.M.; Glowacki, J. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J. Cell. Biochem. 2001, 82, 583-590.
71. Kim, Y.-J.; Kim, H.-J.; Im, G.-I. PTHrP promotes chondrogenesis and suppresses hypertrophy from both bone marrow-derived and adipose tissue-derived MSCs. Biochem. Biophys. Res. Commun. 2008, 373, 104-108.
72. Lin, G.; Garcia, M.; Ning, H.; Banie, L.; Guo, Y.L.; Lue, T.F.; Lin, C.S. Defining stem and progenitor cells within adipose tissue. Stem Cells Dev. 2008, 17, 1053-1063.
73. Khan, W.; Tew, S.; Adesida, A.; Hardingham, T. Human infrapatellar fat pad-derived stem cells express the pericyte marker 3G5 and show enhanced chondrogenesis after expansion in fibroblast growth factor-2. Arthritis Res. Ther. 2008, 10, 1-11.
74. Yoshimura, H.; Muneta, T.; Nimura, A.; Yokoyama, A.; Koga, H.; Sekiya, I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res. 2007, 327, 449-462.
75. Caplan, A.I. Review: Mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng. 2005, 11, 1198-1211.
76. Kim, H.J.; Lee, J.H.; Im, G.I. Chondrogenesis using mesenchymal stem cells and PCL scaffolds. J. Biomed. Mater. Res. A 2010, 92, 659-666.
77. Farrell, E.; O'Brien, F.J.; Doyle, P.; Fischer, J.; Yannas, I.; Harley, B.A.; O'Connell, B.; Prendergast, P.J.; Campbell, V.A. A collagen-glycosaminoglycan scaffold supports adult rat mesenchymal stem cell differentiation along osteogenic and chondrogenic routes. Tissue Eng. 2006, 12, 459-468.
78. Guilak, F.; Awad, H.A.; Fermor, B.; Leddy, H.A.; Gimble, J.M. Adipose-derived adult stem cells for cartilage tissue engineering. Biorheology 2004, 41, 389-399.
79. Awad, H.A.; Quinn Wickham, M.; Leddy, H.A.; Gimble, J.M.; Guilak, F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 2004, 25, 3211-3222.
80. Erickson, G.R.; Gimble, J.M.; Franklin, D.M.; Rice, H.E.; Awad, H.; Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Research Commun. 2002, 290, 763-769.
81. Gronthos, S.; Franklin, D.M.; Leddy, H.A.; Robey, P.G.; Storms, R.W.; Gimble, J.M. Surface protein characterization of human adipose tissue-derived stromal cells. J. Cell. Physiol. 2001, 189, 54-63.
82. Dragoo, J.L.; Samimi, B.; Zhu, M.; Hame, S.L.; Thomas, B.J.; Lieberman, J.R.; Hedrick, M.H.; Benhaim, P. Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads. J. Bone Joint Surg. Br. 2003, 85B, 740-747.
83. Khan, W.S.; Adesida, A.B.; Hardingham, T.E. Hypoxic conditions increase hypoxia-inducible transcription factor 2alpha and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res. Ther. 2007, 9, R55-R55.
84. Buckley, C.T.; Vinardell, T.; Thorpe, S.D.; Haugh, M.G.; Jones, E.; McGonagle, D.; Kelly, D.J. Functional properties of cartilaginous tissues engineered from infrapatellar fat pad-derived mesenchymal stem cells. J. Biomech. 2010, 43, 920-926.
85. de Bari, C.; Dell'Accio, F.; Tylzanowski, P.; Luyten, F.P. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001, 44, 1928-1942.
86. Shirasawa, S.; Sekiya, I.; Sakaguchi, Y.; Yagishita, K.; Ichinose, S.; Muneta, T. In vitro chondrogenesis of human synovium-derived mesenchymal stem cells: Optimal condition and comparison with bone marrow-derived cells. J. Cell. Biochem. 2006, 97, 84-97.
87. Fan, J.; Varshney, R.R.; Ren, L.; Cai, D.; Wang, D.A. Synovium-derived mesenchymal stem cells: a new cell source for musculoskeletal regeneration. Tissue Eng. B Rev. 2009, 15, 75-86.
88. Koga, H.; Muneta, T.; Nagase, T.; Nimura, A.; Ju, Y.-J.; Mochizuki, T.; Sekiya, I. Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res. 2008, 333, 207-215.
89. Jitsuiki, J.I.; Ochi, M.; Ikuta, Y. Meniscal repair enhanced by an interpositional free synovial autograft: An experimental study in rabbits. Arthroscopy 1994, 10, 659-666.
90. Hunziker, E.B.; Rosenberg, L.C. Repair of partial-thickness defects in articular cartilage: Cell recruitment from the synovial membrane. J. Bone Joint Surg. 1996, 78, 721-733.
91. Strioga, M.; Viswanathan, S.; Darinskas, A.; Slaby, O.; Michalek, J. Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev. 2012, 21, 2724-2752.
92. Dowthwaite, G.P.; Bishop, J.C.; Redman, S.N.; Khan, I.M.; Rooney, P.; Evans, D.J.R.; Haughton, L.; Bayram, Z.; Boyer, S.; Thomson, B.; Wolfe, M.S.; Archer, C.W. The surface of articular cartilage contains a progenitor cell population. J. Cell Sci. 2004, 117, 889-897.
93. Sakaguchi, Y.; Sekiya, I.; Yagishita, K.; Muneta, T. Comparison of human stem cells derived from various mesenchymal tissues: Superiority of synovium as a cell source. Arthritis Rheum. 2005, 52, 2521-2529.
94. Havlas, V.; Kos, P.; Jendelova, P.; Lesny, P.; Trc, T.; Sykova, E. Comparison of chondrogenic differentiation of adipose tissue-derived mesenchymal stem cells with cultured chondrocytes and bone marrow mesenchymal stem cells. Acta Chir. Orthop. Traumatol. Cech. 2011, 78, 138-144.
95. Vidal, M.A.; Robinson, S.O.; Lopez, M.J.; Paulsen, D.B.; Borkhsenious, O.; Johnson, J.R.; Moore, R.M.; Gimble, J.M. Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow. Vet. Surg. 2008, 37, 713-724.
96. Reich, C.M.; Raabe, O.; Wenisch, S.; Bridger, P.S.; Kramer, M.; Arnhold, S. Isolation, culture and chondrogenic differentiation of canine adipose tissue- and bone marrow-derived mesenchymal stem cells-a comparative study. Vet. Res. Commun. 2012, 36, 139-148.
97. Sekiya, I.; Vuoristo, J.T.; Larson, B.L.; Prockop, D.J. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc. Natl. Acad. Soc. USA 2002, 99, 4397-4402.
98. Fischer, J.; Dickhut, A.; Rickert, M.; Richter, W. Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum. 2010, 62, 2696-2706.
99. Bian, L.; Zhai, D.Y.; Mauck, R.L.; Burdick, J.A. Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage. Tissue Eng. A 2011, 17, 1137-1145.
100. Wu, L.; Leijten, J.C.; Georgi, N.; Post, J.N.; van Blitterswijk, C.A.; Karperien, M. Trophic effects of mesenchymal stem cells increase chondrocyte proliferation and matrix formation. Tissue Eng. A 2011, 17, 1425-1436.
101. Acharya, C.; Adesida, A.; Zajac, P.; Mumme, M.; Riesle, J.; Martin, I.; Barbero, A. Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation. J. Cell. Physiol. 2012, 227, 88-97.
102. Capito, R.M.; Spector, M. Scaffold-based articular cartilage repair. IEEE Eng. Med. Biol. Mag. 2003, 22, 42-50.
103. Coutts, R.D.; Healey, R.M.; Ostrander, R.; Sah, R.L.; Goomer, R.; Amiel, D. Matrices for cartilage repair. Clin. Orthop. Relat. Res. 2001, 391, S271-S279.
104. Pieper, J.S.; van Wachem, P.B.; van Luyn, M.J.A.; Brouwer, L.A.; Hafmans, T.; Veerkamp, J.H.; van Kuppevelt, T.H. Attachment of glycosaminoglycans to collagenous matrices modulates the tissue response in rats. Biomaterials 2000, 21, 1689-1699.
105. Schagemann, J.C.; Kurz, H.; Casper, M.E.; Stone, J.S.; Dadsetan, M.; Yu-Long, S.; Mrosek, E.H.; Fitzsimmons, J.S.; O'Driscoll, S.W.; Reinholz, G.G. The effect of scaffold composition on the early structural characteristics of chondrocytes and expression of adhesion molecules. Biomaterials 2010, 31, 2798-2805.
106. Freed, L.E.; Vunjak-Novakovic, G.; Biron, R.J.; Eagles, D.B.; Lesnoy, D.C.; Barlow, S.K.; Langer, R. Biodegradable Polymer Scaffolds for Tissue Engineering. Nat. Biotechnol. 1994, 12, 689-693.
107. Agrawal, C.M.; Ray, R.B. Biodegradable polymeric scaffolds for musculoskeletal tissue engineering. J. Biomed. Mater. Res. 2001, 55, 141-150.
108. Maquet, V.; Boccaccini, A.R.; Pravata, L.; Notingher, I.; Jérôme, R. Porous poly(α-hydroxyacid)/Bioglass® composite scaffolds for bone tissue engineering. I. Preparation and in vitro characterisation. Biomaterials 2004, 25, 4185-4194.
109. Oh, S.H.; Kim, T.H.; Im, G.I.; Lee, J.H. Investigation of pore size effect on chondrogenic differentiation of adipose stem cells using a pore size gradient scaffold. Biomacromolecules 2010, 11, 1948-1955.
110. Yang, F.; Murugan, R.; Wang, S.; Ramakrishna, S. Electrospinning of nano/micro scale poly(l-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 2005, 26, 2603-2610.
111. Hutmacher, D.W. Scaffold design and fabrication technologies for engineering tissues state of the art and future perspectives. J. Biomater. Sci. Polym. Ed. 2001, 12, 107-124.
112. Pieper, J.S.; van der Kraan, P.M.; Hafmans, T.; Kamp, J.; Buma, P.; van Susante, J.L.C.; van den Berg, W.B.; Veerkamp, J.H.; van Kuppevelt, T.H. Crosslinked type II collagen matrices: Preparation, characterization, and potential for cartilage engineering. Biomaterials 2002, 23, 3183-3192.
113. Hadjipanayi, E.; Mudera, V.; Brown, R.A. Close dependence of fibroblast proliferation on collagen scaffold matrix stiffness. J. Tissue Eng. Regen. Med. 2009, 3, 77-84.
114. Harley, B.A.; Leung, J.H.; Silva, E.C.C.M.; Gibson, L.J. Mechanical characterization of collagen-glycosaminoglycan scaffolds. Acta Biomater. 2007, 3, 463-474.
115. Haugh, M.G.; Murphy, C.M.; McKiernan, R.C.; Altenbuchner, C.; OBrien, F.J. Crosslinking and mechanical properties significantly influence cell attachment, proliferation, and migration within collagen glycosaminoglycan scaffolds. Tissue Eng. A 2011, 17, 1201-1208.
116. Mueller, S.M.; Shortkroff, S.; Schneider, T.O.; Breinan, H.A.; Yannas, I.V.; Spector, M. Meniscus cells seeded in type I and type II collagen-GAG matrices in vitro. Biomaterials 1999, 20, 701-709.
117. Bosnakovski, D.; Mizuno, M.; Kim, G.; Takagi, S.; Okumura, M.; Fujinaga, T. Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: Influence of collagen type II extracellular matrix on MSC chondrogenesis. Biotechnol. Bioeng. 2006, 93, 1152-1163.
118. Tierney, C.M.; Jaasma, M.J.; OBrien, F.J. Osteoblast activity on collagen-GAG scaffolds is affected by collagen and GAG concentrations. J. Biomed. Mater. Res. A 2009, 91A, 92-101.
119. Yannas, I.V.; Burke, J.F. Design of an artificial skin. I. Basic design principles. J. Biomed. Mater. Res. 1980, 14, 65-81.
120. Louie, L.K.; Yannas, I.V.; Hsu, H.P.; Spector, M. Healing of tendon defects implanted with a porous collagen-GAG matrix: Histological evaluation. Tissue Eng. 1997, 3, 187-195.
121. Chamberlain, L.J.; Yannas, I.V.; Hsu, H.P.; Strichartz, G.; Spector, M. Collagen-GAG substrate enhances the quality of nerve regeneration through collagen tubes up to level of autograft. Exp. Neurol. 1998, 154, 315-329.
122. O'Brien, F.J.; Harley, B.A.; Yannas, I.V.; Gibson, L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 2005, 26, 433-441.
123. Alhag, M.; Farrell, E.; Toner, M.; Claffey, N.; Lee, T.; O'Brien, F. Evaluation of early healing events around mesenchymal stem cell-seeded collagen-glycosaminoglycan scaffold. An experimental study in Wistar rats. Oral Maxillofac. Surg. 2011, 15, 31-39.
124. van Susante, J.L.C.; Pieper, J.; Buma, P.; van Kuppevelt, T.H.; van Beuningen, H.; van der Kraan, P.M.; Veerkamp, J.H.; van den Berg, W.B.; Veth, R.P.H. Linkage of chondroitin-sulfate to type I collagen scaffolds stimulates the bioactivity of seeded chondrocytes in vitro. Biomaterials 2001, 22, 2359-2369.
125. Nehrer, S.; Breinan, H.A.; Ramappa, A.; Young, G.; Shortkroff, S.; Louie, L.K.; Sledge, C.B.; Yannas, I.V.; Spector, M. Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes. Biomaterials 1997, 18, 769-776.
126. Grigolo, B.; Lisignoli, G.; Piacentini, A.; Fiorini, M.; Gobbi, P.; Mazzotti, G.; Duca, M.; Pavesio, A.; Facchini, A. Evidence for redifferentiation of human chondrocytes grown on a hyaluronan-based biomaterial (HYAFF®11): Molecular, immunohistochemical and ultrastructural analysis. Biomaterials 2002, 23, 1187-1195.
127. Gobbi, A.; Kon, E.; Berruto, M.; Francisco, R.; Filardo, G.; Marcacci, M. Patellofemoral full-thickness chondral defects treated with Hyalograft-C. Am. J. Sports Med. 2006, 34, 1763-1773.
128. Murphy, C.M.; Haugh, M.G.; OBrien, F.J. The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 2010, 31, 461-466.
129. Karageorgiou, V.; Kaplan, D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005, 26, 5474-5491.
130. Zeltinger, J.; Sherwood, J.K.; Graham, D.A.; Müeller, R.; Griffith, L.G. Effect of pore size and void fraction on cellular adhesion, proliferation, and matrix deposition. Tissue Eng. 2001, 7, 557-572.
131. Salem, A.K.; Stevens, R.; Pearson, R.G.; Davies, M.C.; Tendler, S.J.B.; Roberts, C.J.; Williams, P.M.; Shakesheff, K.M. Interactions of 3T3 fibroblasts and endothelial cells with defined pore features. J. Biomed. Mater. Res. 2002, 61, 212-217.
132. Engler, A.J.; Sen, S.; Sweeney, H.L.; Discher, D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126, 677-689.
133. Murphy, C.M.; Matsiko, A.; Haugh, M.G.; Gleeson, J.P.; OBrien, F.J. Mesenchymal stem cell fate is regulated by the composition and mechanical properties of collagen-glycosaminoglycan scaffolds. J. Mech. Behav. Biomed. Mater. 2012, 11, 53-62.
134. Tse, J.R.; Engler, A.J. Stiffness gradients mimicking tissue variation regulate mesenchymal stem cell fate. PLoS One 2011, 6, doi:10.1371/journal.pone.0015978.
135. Discher, D.E.; Mooney, D.J.; Zandstra, P.W. Growth factors, matrices, and forces combine and control stem cells. Science 2009, 324, 1673-1677.
136. Discher, D.E.; Janmey, P.; Wang, Y.-l. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310, 1139-1143.
137. Reilly, G.C.; Engler, A.J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 2010, 43, 55-62.
138. Atkins, E.D.; Sheehan, J.K. Structure for hyaluronic acid. Nat. New Biol. 1972, 235, 253-254.
139. Fukumoto, T.; Sperling, J.W.; Sanyal, A.; Fitzsimmons, J.S.; Reinholz, G.G.; Conover, C.A.; O'Driscoll, S.W. Combined effects of insulin-like growth factor-1 and transforming growth factor-β1 on periosteal mesenchymal cells during chondrogenesis in vitro. Osteoarthr. Cartil. 2003, 11, 55-64.
140. Zhang, X.; Ziran, N.; Goater, J.J.; Schwarz, E.M.; Puzas, J.E.; Rosier, R.N.; Zuscik, M.; Drissi, H.; O'Keefe, R.J. Primary murine limb bud mesenchymal cells in long-term culture complete chondrocyte differentiation: TGF-β delays hypertrophy and PGE2 inhibits terminal differentiation. Bone 2004, 34, 809-817.
141. Buckley, C.T.; Kelly, D.J. Expansion in the presence of FGF-2 enhances the functional development of cartilaginous tissues engineered using infrapatellar fat pad derived MSCs. J. Mech. Behav. Biomed. Mater. 2012, 11, 102-111.
142. Diekman, B.O.; Estes, B.T.; Guilak, F. The effects of BMP6 overexpression on adipose stem cell chondrogenesis: Interactions with dexamethasone and exogenous growth factors. J. Biomed. Mater. Res. A 2010, 93A, 994-1003.
143. Jones, J.I.; Gockerman, A.; Busby, W.H., Jr.; Camacho-Hubner, C.; Clemmons, D.R. Extracellular matrix contains insulin-like growth factor binding protein-5: Potentiation of the effects of IGF-I. J. Cell Biol. 1993, 121, 679-687.
144. Martin, I.; Suetterlin, R.; Baschong, W.; Heberer, M.; Vunjak-Novakovic, G.; Freed, L.E. Enhanced cartilage tissue engineering by sequential exposure of chondrocytes to FGF-2 during 2D expansion and BMP-2 during 3D cultivation. J. Cell. Biochem. 2001, 83, 121-128.
145. Dickhut, A.; Dexheimer, V.; Martin, K.; Lauinger, R.; Heisel, C.; Richter, W. Chondrogenesis of human mesenchymal stem cells by local transforming growth factor-beta delivery in a biphasic resorbable carrier. Tissue Eng. A 2010, 16, 453-464.
146. Yaeger, P.C.; Masi, T.S.L.; de Ortiz, J.L.B.; Binette, F.O.; Tubo, R.; McPherson, J.M. Synergistic action of transforming growth factor-[beta] and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp. Cell Res. 1997, 237, 318-325.
147. Guo, J.; Chung, U.-I.; Yang, D.; Karsenty, G.; Bringhurst, F.R.; Kronenberg, H.M. PTH/PTHrP receptor delays chondrocyte hypertrophy via both Runx2-dependent and -independent pathways. Dev. Biol. 2006, 292, 116-128.
148. Kieswetter, K.; Schwartz, Z.; Alderete, M.; Dean, D.D.; Boyan, B.D. Platelet derived growth factor stimulates chondrocyte proliferation but prevents endochondral maturation. Endocrine 1997, 6, 257-264.
149. Brandl, A.; Angele, P.; Roll, C.; Prantl, L.; Kujat, R.; Kinner, B. Influence of the growth factors PDGF-BB, TGF-beta1 and bFGF on the replicative aging of human articular chondrocytes during in vitro expansion. J. Orthop. Res. 2010, 28, 354-360.
150. Lee, K.; Silva, E.A.; Mooney, D.J. Growth factor delivery-based tissue engineering: General approaches and a review of recent developments. J. R. Soc. Interface 2011, 8, 153-170.
151. Ulijn, R.V.; Bibi, N.; Jayawarna, V.; Thornton, P.D.; Todd, S.J.; Mart, R.J.; Smith, A.M.; Gough, J.E. Bioresponsive hydrogels. Mater. Today 2007, 10, 40-48.
152. Park, H.; Temenoff, J.S.; Tabata, Y.; Caplan, A.I.; Mikos, A.G. Injectable biodegradable hydrogel composites for rabbit marrow mesenchymal stem cell and growth factor delivery for cartilage tissue engineering. Biomaterials 2007, 28, 3217-3227.
153. Li, B.; Davidson, J.M.; Guelcher, S.A. The effect of the local delivery of platelet-derived growth factor from reactive two-component polyurethane scaffolds on the healing in rat skin excisional wounds. Biomaterials 2009, 30, 3486-3494.
154. Buket Basmanav, F.; Kose, G.T.; Hasirci, V. Sequential growth factor delivery from complexed microspheres for bone tissue engineering. Biomaterials 2008, 29, 4195-4204.
155. Jaklenec, A.; Hinckfuss, A.; Bilgen, B.; Ciombor, D.M.; Aaron, R.; Mathiowitz, E. Sequential release of bioactive IGF-I and TGF-β1 from PLGA microsphere-based scaffolds. Biomaterials 2008, 29, 1518-1525.
156. Lee, J.E.; Kim, K.E.; Kwon, I.C.; Ahn, H.J.; Lee, S.-H.; Cho, H.; Kim, H.J.; Seong, S.C.; Lee, M.C. Effects of the controlled-released TGF-[beta]1 from chitosan microspheres on chondrocytes cultured in a collagen/chitosan/glycosaminoglycan scaffold. Biomaterials 2004, 25, 4163-4173.
157. O'Brien, F.J. Biomaterials & scaffolds for tissue engineering. Mater. Today 2011, 14, 88-95.
158. Sgaglione, N.A. The future of cartilage restoration. J. Knee Surg. 2004, 17, 235-243.
159. Palmer, G.D.; Steinert, A.; Pascher, A.; Gouze, E.; Gouze, J.-N.; Betz, O.; Johnstone, B.; Evans, C.H.; Ghivizzani, S.C. Gene-induced chondrogenesis of primary mesenchymal stem cells in vitro. Mol. Ther. 2005, 12, 219-228.
160. Bonadio, J.; Smiley, E.; Patil, P.; Goldstein, S. Localized, direct plasmid gene delivery in vivo: Prolonged therapy results in reproducible tissue regeneration. Nat. Med. 1999, 5, 753-759.
161. Tierney, E.G.; Duffy, G.P.; Hibbitts, A.J.; Cryan, S.-A.; OBrien, F.J. The development of non-viral gene-activated matrices for bone regeneration using polyethyleneimine (PEI) and collagen-based scaffolds. J. Control. Release 2012, 158, 304-311.
162. Bolliet, C.; Bohn, M.C.; Spector, M. Non-viral delivery of the gene for glial cell line-derived neurotrophic factor to mesenchymal stem cells in vitro via a collagen scaffold. Tissue Eng. C Methods 2008, 14, 207-219.
163. Im, G.I.; Kim, H.J.; Lee, J.H. Chondrogenesis of adipose stem cells in a porous PLGA scaffold impregnated with plasmid DNA containing SOX trio (SOX-5,-6 and -9) genes. Biomaterials 2011, 32, 4385-4392.
164. Doukas, J.; Chandler, L.A.; Gonzalez, A.M.; Gu, D.; Hoganson, D.K.; Ma, C.; Nguyen, T.; Printz, M.A.; Nesbit, M.; Herlyn, M.; Crombleholme, T.M.; Aukerman, S.L.; Sosnowski, B.A.; Pierce, G.F. Matrix immobilization enhances the tissue repair activity of growth factor gene therapy vectors. Hum. Gene Ther. 2001, 12, 783-798.
165. Madry, H.; Kaul, G.; Cucchiarini, M.; Stein, U.; Zurakowski, D.; Remberger, K.; Menger, M.D.; Kohn, D.; Trippel, S.B. Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Ther. 2005, 12, 1171-1179.
166. Goldstein, S.A. In vivo nonviral delivery factors to enhance bone repair. Clin. Orthop. Related Res. 2000, 379, S113-S119.
167. Capito, R.M.; Spector, M. Collagen scaffolds for nonviral IGF-1 gene delivery in articular cartilage tissue engineering. Gene Ther. 2007, 14, 721-732.
168. Haupt, J.L.; Frisbie, D.D.; McIlwraith, C.W.; Robbins, P.D.; Ghivizzani, S.; Evans, C.H.; Nixon, A.J. Dual transduction of insulin-like growth factor-I and interleukin-l receptor antagonist protein controls cartilage degradation in an osteoarthritic culture model. J. Orthop. Res. 2005, 23, 118-126.
169. Nixon, A.J.; Haupt, J.L.; Frisbie, D.D.; Morisset, S.S.; McIlwraith, C.W.; Robbins, P.D.; Evans, C.H.; Ghivizzani, S. Gene-mediated restoration of cartilage matrix by combination insulin-like growth factor-I//interleukin-1 receptor antagonist therapy. Gene Ther. 2004, 12, 177-186.
170. Mason, J.M.; Breitbart, A.S.; Barcia, M.; Porti, D.; Pergolizzi, R.G.; Grande, D.A. Cartilage and bone regeneration using gene-enhanced tissue engineering. Clin. Orthop. Relat. Res. 2000, 379, S171-S178.
171. Musgrave, D.S.; Pruchnic, R.; Bosch, P.; Ziran, B.H.; Whalen, J.; Huard, J. Human skeletal muscle cells in ex vivo gene therapy to deliver bone morphogenetic protein-2. J. Bone Joint Surg. Br. 2002, 84B, 120-127.