Genipin-crosslinked cartilage-derived matrix as a scaffold for human adipose-derived stem cell chondrogenesis

Tissue Engineering - Part A

Volumn 19, Issue 3-4, 2013, Pages 484-496

  Cheng, Nai Chen ^a,b,c   Estes, Bradley T ^a   Young, Tai Horng ^b   Guilak, Farshid ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOMATERIALS; BIOMECHANICS; CARTILAGE; CELL CULTURE; CROSSLINKING; GENE EXPRESSION; MECHANICAL PROPERTIES; STEM CELLS;

ADIPOSE DERIVED STEM CELLS; ARTICULAR CARTILAGES; CARTILAGE DEFECTS; CARTILAGE TISSUE ENGINEERING; CELL-BASED; CHEMICAL CROSS-LINKING; CHONDROGENESIS; CHONDROGENIC PHENOTYPES; CHONDROGENIC POTENTIAL; CLINICAL APPLICATION; CROSS-LINKING DEGREE; CROSS-LINKING DENSITY; CROSSLINKED; CROSSLINKER; EXOGENOUS GROWTH; EXTRACELLULAR MATRICES; GENIPIN; POROUS SCAFFOLD; THREE-DIMENSIONAL SCAFFOLDS;

SCAFFOLDS (BIOLOGY);

CROSS LINKING REAGENT; GENIPIN; IRIDOID; TISSUE SCAFFOLD;

ADIPOCYTE; ARTICLE; CELL CULTURE; CHEMISTRY; CHONDROGENESIS; CYTOLOGY; DRUG EFFECT; DRUG IMPLANT; EQUIPMENT DESIGN; EQUIPMENT FAILURE; EXTRACELLULAR MATRIX; HUMAN; NANOMEDICINE; PHYSIOLOGY; STEM CELL;

ADIPOCYTES; CELLS, CULTURED; CHONDROGENESIS; CROSS-LINKING REAGENTS; DRUG IMPLANTS; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; EXTRACELLULAR MATRIX; HUMANS; IRIDOIDS; NANOMEDICINE; STEM CELLS; TISSUE SCAFFOLDS;

MLCS; MLOWN;

EID: 84872106944     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0384     Document Type: Article

References (63)

1. Guilak, F., and Hung, C.T. Physical regulation of cartilage metabolism. In: Mow, V.C., and Huiskes, R., eds. Basic Orthopaedic Biomechanics and Mechano-Biology, 3rd edition. Philadelphia: Lippincott Williams & Wilkins, 2004, pp. 259-300.
2. Baumgaertner, M.R., Cannon, W.D., Jr., Vittori, J.M., Schmidt, E.S., and Maurer, R.C. Arthroscopic debridement of the arthritic knee. Clin Orthop Relat Res 197, 1990.
3. Johnson, L.L. Arthroscopic abrasion arthroplasty: a review. Clin Orthop Relat Res S306, 2001.
4. Breinan, H.A., Minas, T., Hsu, H.P., Nehrer, S., Sledge, C.B., and Spector, M. Effect of cultured autologous chondrocytes on repair of chondral defects in a canine model. J Bone Joint Surg Am 79, 1439, 1997.
5. Brittberg, M., Lindahl, A., Nilsson, A., Ohlsson, C., Isaksson, O., and Peterson, L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331, 889, 1994.
6. Knutsen, G., Engebretsen, L., Ludvigsen, T.C., Drogset, J.O., Grontvedt, T., Solheim, E., et al. Autologous chondrocyte implantation compared with microfracture in the knee. A randomized trial. J Bone Joint Surg Am 86-A, 455, 2004.
7. Mobasheri, A., Csaki, C., Clutterbuck, A.L., Rahmanzadeh, M., and Shakibaei, M. Mesenchymal stem cells in connective tissue engineering and regenerative medicine: applications in cartilage repair and osteoarthritis therapy. Histol Histo-pathol 24, 347, 2009.
8. 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, S295, 2001.
9. Raghunath, J., Salacinski, H.J., Sales, K.M., Butler, P.E., and Seifalian, A.M. Advancing cartilage tissue engineering: the application of stem cell technology. Curr Opin Biotechnol 16, 503, 2005.
10. Kim, H.A., Suh, D.I., and Song, Y.W. Relationship between chondrocyte apoptosis and matrix depletion in human ar-ticular cartilage. J Rheumatol 28, 2038, 2001.
11. Bonaventure, J., Kadhom, N., Cohen-Solal, L., Ng, K.H., Bourguignon, J., Lasselin, C., et al. Reexpression of cartilage-specific genes by dedifferentiated human articular chon-drocytes cultured in alginate beads. Exp Cell Res 212, 97, 1994.
12. 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.
13. Thirion, S., and Berenbaum, F. Culture and phenotyping of chondrocytes in primary culture. Methods Mol Med 100, 1, 2004.
14. Wang, Y., Kim, U.J., Blasioli, D.J., Kim, H.J., and Kaplan, D.L. In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. Biomaterials 26, 7082, 2005.
15. Wayne, J.S., McDowell, C.L., Shields, K.J., and Tuan, R.S. In vivo response of polylactic acid-alginate scaffolds and bone marrow-derived cells for cartilage tissue engineering. Tissue Eng 11, 953, 2005.
16. Wei, Y., Hu, Y., Hao, W., Han, Y., Meng, G., Zhang, D., et al. A novel injectable scaffold for cartilage tissue engineering using adipose-derived adult stem cells. J Orthop Res 26, 27, 2008.
17. Williams, C.G., Kim, T.K., Taboas, A., Malik, A., Manson, P., and Elisseeff, J. In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel. Tissue Eng 9, 679, 2003.
18. Estes, B.T., Diekman, B.O., Gimble, J.M., and Guilak, F. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc 5, 1294, 2010.
19. Guilak, F., Lott, K.E., Awad, H.A., Cao, Q., Hicok, K.C., Fermor, B., et al. Clonal analysis of the differentiation po-tential of human adipose-derived adult stem cells. J Cell Physiol 206, 229, 2006.
20. Cheng, N.C., Wang, S., and Young, T.H. The influence of spheroid formation of human adipose-derived stem cells on chitosan films on stemness and differentiation capabilities. Biomaterials 33, 1748, 2012.
21. Estes, B.T., Wu, A.W., Storms, R.W., and Guilak, F. Ex-tended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J Cell Physiol 209, 987, 2006.
22. 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.
23. 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.
24. Hofmann, S., Knecht, S., Langer, R., Kaplan, D.L., Vunjak-Novakovic, G., Merkle, H.P., et al. Cartilage-like tissue en-gineering using silk scaffolds and mesenchymal stem cells. Tissue Eng 12, 2729, 2006.
25. Guilak, F., Estes, B.T., Diekman, B.O., Moutos, F.T., and Gimble, J.M. 2010 Nicolas Andry Award: Multipotent adult stem cells from adipose tissue for musculoskeletal tissue engineering. Clin Orthop Relat Res 468, 2530, 2010.
26. Ott, H.C., Matthiesen, T.S., Goh, S.K., Black, L.D., Kren, S.M., Netoff, T.I., et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 14, 213, 2008.
27. Urist, M.R. Bone: formation by autoinduction. Science 150, 893, 1965.
28. Cheng, N.C., Estes, B.T., Awad, H.A., and Guilak, F. Chondrogenic differentiation of adipose-derived adult stem cells by a porous scaffold derived from native articular cartilage extracellular matrix. Tissue Eng Part A 15, 231, 2009.
29. Cheng, N.C., Estes, B.T., Young, T.H., and Guilak, F. Engineered cartilage using primary chondrocytes cultured in a porous cartilage-derived matrix. Regen Med 6, 81, 2011.
30. Diekman, B.O., Estes, B.T., and Guilak, F. The effects of BMP6 overexpression on adipose stem cell chondrogenesis: Interactions with dexamethasone and exogenous growth factors. J Biomed Mater Res Part A 93, 994, 2010.
31. Vickers, S.M., Squitieri, L.S., and Spector, M. Effects of cross-linking type II collagen-GAG scaffolds on chondrogenesis in vitro: dynamic pore reduction promotes cartilage forma-tion. Tissue Eng 12, 1345, 2006.
32. Tang, S., and Spector, M. Incorporation of hyaluronic acid into collagen scaffolds for the control of chondrocyte-mediated contraction and chondrogenesis. Biomed Mater 2, S135, 2007.
33. Badylak, S.F. The extracellular matrix as a scaffold for tissue reconstruction. Semin Cell Dev Biol 13, 377, 2002.
34. Huang, L.L., Sung, H.W., Tsai, C.C., and Huang, D.M. Biocompatibility study of a biological tissue fixed with a naturally occurring crosslinking reagent. J Biomed Mater Res 42, 568, 1998.
35. Chang, Y., Hsu, C.K., Wei, H.J., Chen, S.C., Liang, H.C., Lai, P.H., et al. Cell-free xenogenic vascular grafts fixed with glutaraldehyde or genipin: in vitro and in vivo studies. J Biotechnol 120, 207, 2005.
36. Chang, Y., Lee, M.H., Liang, H.C., Hsu, C.K., and Sung, H.W. Acellular bovine pericardia with distinct porous structures fixed with genipin as an extracellular matrix. Tissue Eng 10, 881, 2004.
37. Sell, S.A., Francis, M.P., Garg, K., McClure, M.J., Simpson, D.G., and Bowlin, G.L. Cross-linking methods of electrospun fibrinogen scaffolds for tissue engineering applications. Biomed Mater 3, 45001, 2008.
38. Silva, S.S., Motta, A., Rodrigues, M.T., Pinheiro, A.F., Gomes, M.E., Mano, J.F., et al. Novel genipin-cross-linked chitosan/silk fibroin sponges for cartilage engineering strategies. Biomacromolecules 9, 2764, 2008.
39. Lima, E.G., Tan, A.R., Tai, T., Marra, K.G., DeFail, A., Ateshian, G.A., et al. Genipin enhances the mechanical properties of tissue-engineered cartilage and protects against inflammatory degradation when used as a me-dium supplement. J Biomed Mater Res Part A 91, 692, 2009.
40. Cauich-Rodriguez, J.V., Deb, S., and Smith, R. Effect of cross-linking agents on the dynamic mechanical properties of hydrogel blends of poly(acrylic acid)-poly(vinyl alcohol-vinyl acetate). Biomaterials 17, 2259, 1996.
41. Sung, H.W., Huang, R.N., Huang, L.L., and Tsai, C.C. In vitro evaluation of cytotoxicity of a naturally occurring cross-linking reagent for biological tissue fixation. J Biomater Sci Polym Ed 10, 63, 1999.
42. Sung, H.W., Huang, R.N., Huang, L.L., Tsai, C.C., and Chiu, C.T. Feasibility study of a natural crosslinking reagent for biological tissue fixation. J Biomed Mater Res 42, 560, 1998.
43. Stryer, L. Biochemistry, 3rd edition. New York: Freeman, 1988, p. 50.
44. Kim, U.J., Park, J., Kim, H.J., Wada, M., and Kaplan, D.L. Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin. Biomaterials 26, 2775, 2005.
45. Chomczynski, P., and Sacchi, N. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1, 581, 2006.
46. Mehlhorn, A.T., Niemeyer, P., Kaiser, S., Finkenzeller, G., Stark, G.B., Sudkamp, N.P., et al. Differential expression pattern of extracellular matrix molecules during chon-drogenesis of mesenchymal stem cells from bone marrow and adipose tissue. Tissue Eng 12, 2853, 2006.
47. 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.
48. Badylak, S.F. The extracellular matrix as a biologic scaffold material. Biomaterials 28, 3587, 2007.
49. Little, D., Guilak, F., and Ruch, D.S. Ligament-derived matrix stimulates a ligamentous phenotype in human adipose-derived stem cells. Tissue Eng Part A 16,2307, 2010.
50. O'Brien, F.J., Harley, B.A., Yannas, I.V., and Gibson, L.J. The effect of pore size on cell adhesion in collagen-GAG scaf-folds. Biomaterials 26, 433, 2005.
51. Jeong, C.G., Zhang, H., and Hollister, S.J. Three-dimensional poly(1,8-octanediol-co-citrate) scaffold pore shape and per-meability effects on sub-cutaneous in vivo chondrogenesis using primary chondrocytes. Acta Biomaterialia 7,505, 2011.
52. Yamane, S., Iwasaki, N., Kasahara, Y., Harada, K., Majima, T., Monde, K., et al. Effect of pore size on in vitro cartilage formation using chitosan-based hyaluronic acid hybrid polymer fibers. J Biomed Mater Res Part A 81, 586, 2007.
53. Wang, D.A., Varghese, S., Sharma, B., Strehin, I., Fermanian, S., Gorham, J., et al. Multifunctional chondroitin sulphate for cartilage tissue-biomaterial integration. Nat Mater 6, 385, 2007.
54. Seda Tigli, R., Ghosh, S., Laha, M.M., Shevde, N.K., Daheron, L., Gimble, J., et al. Comparative chondrogenesis of human cell sources in 3D scaffolds. J Tissue Eng Regen Med 3, 348, 2009.
55. Ahmed, N., Dreier, R., Gopferich, A., Grifka, J., and Grassel, S. Soluble signalling factors derived from differentiated cartilage tissue affect chondrogenic differentiation of rat adult marrow stromal cells. Cell Physiol Biochem 20, 665, 2007.
56. Bi, L., Cao, Z., Hu, Y., Song, Y., Yu, L., Yang, B., et al. Effects of different cross-linking conditions on the properties of genipin-cross-linked chitosan/collagen scaffolds for carti-lage tissue engineering. J Mater Sci Mater Med 22, 51, 2011.
57. Hennig, T., Lorenz, H., Thiel, A., Goetzke, K., Dickhut, A., Geiger, F., et al. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profile and is overcome by BMP-6. J Cell Physiol 211, 682, 2007.
58. Butler, D.L., Goldstein, S.A., and Guilak, F. Functional tissue engineering: the role of biomechanics. J Biomech Eng 122, 570, 2000.
59. 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 car-tilage. J Orthop Res 9, 330, 1991.
60. Moutos, F.T., Estes, B.T., and Guilak, F. Multifunctional hybrid three-dimensionally woven scaffolds for cartilage tissue engineering. Macromol Biosci 10, 1355, 2010.
61. Mauck, R.L., Soltz, MA., Wang, C.C., Wong, D.D., Chao, P.H., Valhmu, W.B., et al. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122, 252, 2000.
62. Liang, H.C., Chang, Y., Hsu, C.K., Lee, M.H., and Sung, H.W. Effects of crosslinking degree of an acellular biological tissue on its tissue regeneration pattern. Biomaterials 25, 3541, 2004.
63. Badylak, S.F., and Gilbert, T.W. Immune response to bio-logic scaffold materials. Semin Immunol 20, 109, 2008.