Functional properties of cell-seeded three-dimensionally woven poly(ε-Caprolactone) scaffolds for cartilage tissue engineering

Tissue Engineering - Part A

Volumn 16, Issue 4, 2010, Pages 1291-1301

  Moutos, Franklin T ^a   Guilak, Farshid ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; CARTILAGE; CELL CULTURE; LIGAMENTS; SCAFFOLDS; STEM CELLS; TISSUE ENGINEERING; ULTRASONIC MEASUREMENT; WEAVING;

ARTICULAR CARTILAGES; ARTICULATING SURFACES; BIOMECHANICAL CHARACTERISTICS; BIOMECHANICAL TESTING; CAPROLACTONE; CARTILAGE TISSUE ENGINEERING; CHONDROGENIC; COEFFICIENT OF FRICTIONS; COMPOSITE SCAFFOLDS; CULTURE CONDITIONS; EXTRACELLULAR MATRICES; FIBER-REINFORCED COMPOSITE; FUNCTIONAL PROPERTIES; FUNCTIONAL TISSUE; HUMAN ADIPOSE; REPEATED LOADS; SHEAR PROPERTIES;

MECHANICAL PROPERTIES;

BIOMATERIAL; COLLAGEN; FIBRIN; POLYCAPROLACTONE; POLYESTER; TISSUE SCAFFOLD;

ADULT STEM CELL; ARTICLE; ARTICULAR CARTILAGE; BIOMECHANICS; CARTILAGE CELL; CHEMISTRY; CHONDROGENESIS; COMPRESSIVE STRENGTH; CYTOLOGY; EXTRACELLULAR MATRIX; FRICTION; HUMAN; HYDROGEL; MATERIALS TESTING; METABOLISM; METHODOLOGY; PHYSIOLOGY; REGENERATION; SCANNING ELECTRON MICROSCOPY; SHEAR STRENGTH; TENSILE STRENGTH; TISSUE ENGINEERING; TRANSPLANTATION;

ADULT STEM CELLS; BIOCOMPATIBLE MATERIALS; BIOMECHANICS; CARTILAGE, ARTICULAR; CHONDROCYTES; CHONDROGENESIS; COLLAGEN; COMPRESSIVE STRENGTH; EXTRACELLULAR MATRIX; FIBRIN; FRICTION; HUMANS; HYDROGELS; MATERIALS TESTING; MICROSCOPY, ELECTRON, SCANNING; POLYESTERS; REGENERATION; SHEAR STRENGTH; TENSILE STRENGTH; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 77950813444     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0480     Document Type: Article

References (69)

1. Hunziker, E.B. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 10, 432, 2002.
2. Chu, C.R., Convery, F.R., Akeson, W.H., Meyers, M., and Amiel, D. Articular cartilage transplantation. Clinical results in the knee. Clin Orthop Relat Res 360, 159, 1999.
3. Minas, T., and Nehrer, S. Current concepts in the treatment of articular cartilage defects. Orthopedics 20, 525, 1997.
4. Shapiro, F., Koide, S., and Glimcher, M.J. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 75, 532, 1993.
5. Smith, G.D., Knutsen, G., and Richardson, J.B. A clinical review of cartilage repair techniques. J Bone Joint Surg Br 87, 445, 2005.
6. Guilak, F., Butler, D.L., and Goldstein, S.A. Functional tissue engineering: the role of biomechanics in articular cartilage repair. Clin Orthop Relat Res 391 Suppl, S295, 2001.
7. Butler, D.L., Goldstein, S.A., and Guilak, F. Functional tissue engineering: the role of biomechanics. J Biomech Eng 122, 570, 2000.
8. Boublik, J., Park, H., Radisic, M., Tognana, E., Chen, F., Pei, M., Vunjak-Novakovic, G., and Freed, L.E. Mechanical properties and remodeling of hybrid cardiac constructs made from heart cells, fibrin, and biodegradable, elastomeric knitted fabric. Tissue Eng 11, 1122, 2005.
9. Dong, H., Ye, J.D., Wang, X.P., and Yang, J.J. Preparation of calcium phosphate cement tissue engineering scaffold reinforced with chitin fiber. J Inorg Mater 22, 1007, 2007.
10. Guarino, V., and Ambrosio, L. The synergic effect of polylactide fiber and calcium phosphate particle reinforcement in poly epsilon-caprolactone-based composite scaffolds. Acta Biomater 4, 1778, 2008.
11. Thomson, R.C., Yaszemski, M.J., Powers, J.M., and Mikos, A.G. Hydroxyapatite fiber reinforced poly(alpha-hydroxy ester) foams for bone regeneration. Biomaterials 19, 1935, 1998.
12. Altman, G.H., Horan, R.L., Lu, H.H., Moreau, J., Martin, I., Richmond, J.C., and Kaplan, D.L. Silk matrix for tissue engineered anterior cruciate ligaments. Biomaterials 23, 4131, 2002.
13. Horan, R.L., Collette, A.L., Lee, C., Antle, K., Chen, J.S., and Altman, G.H. Yarn design for functional tissue engineering. J Biomech 39, 2232, 2006.
14. Laurencin, C.T., and Freeman, J.W. Ligament tissue engineering: an evolutionary materials science approach. Biomaterials 26, 7530, 2005.
15. Baker, B.M., and Mauck, R.L. The effect of nanofiber alignment on the maturation of engineered meniscus constructs. Biomaterials 28, 1967, 2007.
16. Li, W.J., Cooper, J.A., Mauck, R.L., and Tuan, R.S. Fabrication and characterization of six electrospun poly(alphahydroxy ester)-based fibrous scaffolds for tissue engineering applications. Acta Biomater 2, 377, 2006.
17. Chen, G., Sato, T., Ushida, T., Hirochika, R., Shirasaki, Y., Ochiai, N., and Tateishi, T. The use of a novel PLGA fiber= collagen composite web as a scaffold for engineering of articular cartilage tissue with adjustable thickness. J Biomed Mater Res A 67, 1170, 2003.
18. Schmal, H., Mehlhorn, A.T., Kurze, C., Zwingmann, J., Niemeyer, P., Finkenzeller, G., Dauner, M., Sudkamp, N.P., and Kostler, W. [In vitro study on the influence of fibrin in cartilage constructs based on PGA fleece materials]. Orthopade 37, 424, 2008.
19. Slivka, M.A., Leatherbury, N.C., Kieswetter, K., and Niederauer, G.G. Porous, resorbable, fiber-reinforced scaffolds tailored for articular cartilage repair. Tissue Eng 7, 767, 2001.
20. Webb, A.R., Macrie, B.D., Ray, A.S., Russo, J.E., Siegel, A.M., Glucksberg, M.R., and Ameer, G.A. In vitro characterization of a compliant biodegradable scaffold with a novel bioreactor system. Ann Biomed Eng 35, 1357, 2007.
21. Moutos, F.T., Freed, L.E., and Guilak, F. A biomimetic threedimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater 6, 162, 2007.
22. Moutos, F.T., and Guilak, F. Composite scaffolds for cartilage tissue engineering. Biorheology 45, 501, 2008.
23. Moutos, F.T. Biomimetic composite scaffolds for the functional tissue engineering of articular cartilage. Doctoral dissertation, Duke University, Durham, NC, 2009.
24. 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 86A, 455, 2004.
25. Lee, C.R., Grodzinsky, A.J., Hsu, H.P., Martin, S.D., and Spector, M. Effects of harvest and selected cartilage repair procedures on the physical and biochemical properties of articular cartilage in the canine knee. J Orthop Res 18, 790, 2000.
26. Stokes, D.G., Liu, G., Coimbra, I.B., Piera-Velazquez, S., Crowl, R.M., and Jimenez, S.A. Assessment of the gene expression profile of differentiated and dedifferentiated human fetal chondrocytes by microarray analysis. Arthritis Rheum 46, 404, 2002.
27. Thirion, S., and Berenbaum, F. Culture and phenotyping of chondrocytes in primary culture. Methods Mol Med 100, 1, 2004.
28. Erickson, G.R., Gimble, J.M., Franklin, D.M., Rice, H.E., Awad, H., and Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 290, 763, 2002.
29. Wei, Y.Y., Hu, Y., Hao, W., Han, Y.S., Meng, G.L., Zhang, D.Z., Wu, Z.X., and Wang, H.Q. A novel injectable scaffold for cartilage tissue engineering using adipose-derived adult stem cells. Journal of Orthopaedic Research 26, 27, 2008.
30. Estes, B.T., Wu, A.W., and Guilak, F. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum 54, 1222, 2006.
31. Hennig, T., Lorenz, H., Thiel, A., Goetzke, K., Dickhut, A., Geiger, F., and Richter, W. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGF beta receptor and BMP profile and is overcome by BMP-6. J Cell Physiol 211, 682, 2007.
32. Sheyn, D., Pelled, G., Zilberman, Y., Talasazan, F., Frank, J.M., Gazit, D., and Gazit, Z. Nonvirally engineered porcine adipose tissue-derived stem cells: use in posterior spinal fusion. Stem Cells 26, 1056, 2008.
33. Awad, H.A., Wickham, M.Q., Leddy, H.A., Gimble, J.M., and Guilak, F. Chondrogenic differentiation of adiposederived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25, 3211, 2004.
34. Eyrich, D., Brandl, F., Appel, B., Wiese, H., Maier, G., Wenzel, M., Staudenmaier, R., Goepferich, A., and Blunk, T. Long-term stable fibrin gels for cartilage engineering. Biomaterials 28, 55, 2007.
35. Passaretti, D., Silverman, R.P., Huang, W., Kirchhoff, C.H., Ashiku, S., Randolph, M.A., and Yaremchuk, M.J. Cultured chondrocytes produce injectable tissue-engineered cartilage in hydrogel polymer. Tissue Eng 7, 805, 2001.
36. Peretti, G.M., Randolph, M.A., Zaporojan, V., Bonassar, L.J., Xu, J.W., Fellers, J.C., and Yaremchuk, M.J. A biomechanical analysis of an engineered cell-scaffold implant for cartilage repair. Ann Plast Surg 46, 533, 2001.
37. Silverman, R.P., Passaretti, D., Huang, W., Randolph, M.A., and Yaremchuk, M. Injectable tissue-engineered cartilage using a fibrin glue polymer. Plast Reconstr Surg 103, 1809, 1999.
38. Xu, J.W., Zaporojan, V., Peretti, G.M., Roses, R.E., Morse, K.B., Roy, A.K., Mesa, J.M., Randolph, M.A., Bonassar, L.J., and Yaremchuk, M.J. Injectable tissue-engineered cartilage with different chondrocyte sources. Plast Reconstr Surg 113, 1361, 2004.
39. Weinand, C., Gupta, R., Huang, A.Y., Weinberg, E., Madisch, I., Qudsi, R.A., Neville, C.M., Pomerantseva, I., and Vacanti, J.P. Comparison of hydrogels in the in vivo formation of tissueengineered bone using mesenchymal stem cells and betatricalcium phosphate. Tissue Eng 13, 757, 2007.
40. Xu, J.W., Nazzal, J., Peretti, G.M., Kirchhoff, C.H., Randolph, M.A., and Yaremchuk, M.J. Tissue-engineered cartilage composite with expanded polytetrafluoroethylene membrane. Ann Plast Surg 46, 527, 2001.
41. Van Lieshout, M., Peters, G., Rutten, M., and Baaijens, F. A knitted, fibrin-covered polycaprolactone scaffold for tissue engineering of the aortic valve. Tissue Eng 12, 481, 2006.
42. Huang, M.H., Li, S.M., Hutmacher, D.W., Coudane, J., and Vert, M. Degradation characteristics of poly(epsiloncaprolactone)- based copolymers and blends. J Appl Polym Sci 102, 1681, 2006.
43. Rohner, D., Hutmacher, D.W., Cheng, T.K., Oberholzer, M., and Hammer, B. In vivo efficacy of bone-marrow-coated polycaprolactone scaffolds for the reconstruction of orbital defects in the pig. J Biomed Mater Res B Appl Biomater 66, 574, 2003.
44. Chew, S.Y., Wen, Y., Dzenis, Y., and Leong, K.W. The role of electrospinning in the emerging field of nanomedicine. Curr Pharm Des 12, 4751, 2006.
45. Huang, Q., Goh, J.C., Hutmacher, D.W., and Lee, E.H. In vivo mesenchymal cell recruitment by a scaffold loaded with transforming growth factor beta1 and the potential for in situ chondrogenesis. Tissue Eng 8, 469, 2002.
46. Hutmacher, D.W. Scaffold design and fabrication technologies for engineering tissues-state of the art and future perspectives. J Biomater Sci Polym Ed 12, 107, 2001.
47. Zein, I., Hutmacher, D.W., Tan, K.C., and Teoh, S.H. Fused deposition modeling of novel scaffold architectures for tissue engineering applications. Biomaterials 23, 1169, 2002.
48. Ng, K.W., Khor, H.L., and Hutmacher, D.W. In vitro characterization of natural and synthetic dermal matrices cultured with human dermal fibroblasts. Biomaterials 25, 2807, 2004.
49. Serrano, M.C., Portoles, M.T., Vallet-Regi, M., Izquierdo, I., Galletti, L., Comas, J.V., and Pagani, R. Vascular endothelial and smooth muscle cell culture on NaOH-treated poly(epsilon-caprolactone) films: a preliminary study for vascular graft development. Macromol Biosci 5, 415, 2005.
50. Tsuji, H., Ishida, T., and Fukuda, N. Surface hydrophilicity and enzymatic hydrolyzability of biodegradable polyesters: Effects of alkaline treatment. Polym Int 52, 843, 2003.
51. Elliott, D.M., Guilak, F., Vail, T.P., Wang, J.Y., and Setton, L.A. Tensile properties of articular cartilage are altered by meniscectomy in a canine model of osteoarthritis. J Orthop Res 17, 503, 1999.
52. Mow, V.C., Kuei, S.C., Lai, W.M., and Armstrong, C.G. Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. J Biomech Eng 102, 73, 1980.
53. Guilak, F., Ratcliffe, A., Lane, N., Rosenwasser, M.P., and Mow, V.C. Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis. J Orthop Res 12, 474, 1994.
54. Wang, H., and Ateshian, G.A. The normal stress effect and equilibrium friction coefficient of articular cartilage under steady frictional shear. J Biomech 30, 771, 1997.
55. Athanasiou, K.A., Rosenwasser, M.P., Buckwalter, J.A., Malinin, T.I., and Mow, V.C. Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J Orthop Res 9, 330, 1991.
56. Setton, L.A., Zhu, W., and Mow, V.C. The biphasic poroviscoelastic behavior of articular cartilage: role of the surface zone in governing the compressive behavior. J Biomech 26, 581, 1993.
57. Bader, D.L., Kempson, G.E., Barrett, A.J., and Webb, W. The effects of leucocyte elastase on the mechanical properties of adult human articular cartilage in tension. Biochim Biophys Acta 677, 103, 1981.
58. Kempson, G.E., Tuke, M.A., Dingle, J.T., Barrett, A.J., and Horsfield, P.H. The effects of proteolytic enzymes on the mechanical properties of adult human articular cartilage. Biochim Biophys Acta 428, 741, 1976.
59. Akizuki, S., Mow, V.C., Muller, F., Pita, J.C., Howell, D.S., and Manicourt, D.H. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J Orthop Res 4, 379, 1986.
60. 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.
61. Soltz, M.A., and Ateshian, G.A. Experimental verification and theoretical prediction of cartilage interstitial fluid pressurization at an impermeable contact interface in confined compression. J Biomech 31, 927, 1998.
62. Ando, W., Tateishi, K., Hart, D.A., Katakai, D., Tanaka, Y., Nakata, K., Hashimoto, J., Fujie, H., Shino, K., Yoshikawa, H., and Nakamura, N. Cartilage repair using an in vitro generated scaffold-free tissue-engineered construct derived from porcine synovial mesenchymal stem cells. Biomaterials 28, 5462, 2007.
63. 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; discussion 28, 2007.
64. Lima, E.G., Bang, L.M., Serebrov, A., Mauck, R., Byers, B.A., Tuan, R., Ateshian, G.A., and Hung, C.T. Measuring the frictional properties of tissue-engineered cartilage constructs. Trans Orthop Res Soc 31, 1501, 2006.
65. Plainfosse, M., Hatton, P.V., Crawford, A., Jin, Z.M., and Fisher, J. Influence of the extracellular matrix on the frictional properties of tissue-engineered cartilage. Biochem Soc Trans 35(Pt 4), 677, 2007.
66. Morita, Y., Tomita, N., Aoki, H., Sonobe, M., Wakitani, S., Tamada, Y., Suguro, T., and Ikeuchi, K. Frictional properties of regenerated cartilage in vitro. J Biomech 39, 103, 2006.
67. Krishnan, R., Park, S., Eckstein, F., and Ateshian, G.A. Inhomogeneous cartilage properties enhance superficial interstitial fluid support and frictional properties, but do not provide a homogeneous state of stress. J Biomech Eng 125, 569, 2003.
68. Kirilak, Y., Pavlos, N.J., Willers, C.R., Han, R., Feng, H., Xu, J., Asokananthan, N., Stewart, G.A., Henry, P., Wood, D., and Zheng, M.H. Fibrin sealant promotes migration and proliferation of human articular chondrocytes: possible involvement of thrombin and protease-activated receptors. Int J Mol Med 17, 551, 2006.
69. Willers, C., Chen, J., Wood, D., Xu, J., and Zheng, M.H. Autologous chondrocyte implantation with collagen bioscaffold for the treatment of osteochondral defects in rabbits. Tissue Eng 11, 1065, 2000