Driving cartilage formation in high-density human adipose-derived stem cell aggregate and sheet constructs without exogenous growth factor delivery

Tissue Engineering - Part A

Volumn 20, Issue 23-24, 2014, Pages 3163-3175

  Dang, Phuong N ^a   Solorio, Loran D ^a   Alsberg, Eben ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; CARTILAGE; CYTOLOGY; DEGRADATION; GROWTH KINETICS; MICROSPHERES; STEM CELLS; TISSUE ENGINEERING;

CARTILAGE FORMATION; CARTILAGE TISSUE ENGINEERING; GELATIN MICROSPHERES; HUMAN ADIPOSE DERIVED STEM CELLS; HUMAN ADIPOSE DERIVED STEM CELLS (HASCS); LOADING CONCENTRATION; POLYMER DEGRADATION; TRANSFORMING GROWTH FACTORS;

CELL ENGINEERING;

COLLAGEN TYPE 1; COLLAGEN TYPE 2; GELATIN; GENIPIN; GLYCOSAMINOGLYCAN; MICROSPHERE; POLYMER; TRANSFORMING GROWTH FACTOR BETA1;

ADIPOSE DERIVED STEM CELL; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE; CARTILAGE CELL; CHONDROGENESIS; CONTROLLED STUDY; DEGRADATION; DNA CONTENT; FEMALE; FREEZE DRYING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; TISSUE ENGINEERING; ADIPOCYTE; CYTOLOGY; DRUG EFFECTS; METABOLISM; PROCEDURES;

ADIPOCYTES; CHONDROCYTES; CHONDROGENESIS; GLYCOSAMINOGLYCANS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSPHERES; TISSUE ENGINEERING; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84915779039     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0551     Document Type: Article

References (74)

1. Cohen, N.P., Foster, R.J., and Mow, V.C. Composition and dynamics of articular cartilage: structure, function, and maintaining healthy state. J Orthop Sports Phys Ther 28, 203, 1998.
2. 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.
3. Martel-Pelletier, J., Wildi, L.M., and Pelletier, J.P. Future therapeutics for osteoarthritis. Bone 51, 297, 2012.
4. Redman, S.N., Oldfield, S.F., and Archer, C.W. Current strategies for articular cartilage repair. Eur Cell Mater 9, 23, 2005; discussion 23-32.
5. Hunziker, E.B., Driesang, I.M., and Saager, C. Structural barrier principle for growth factor-based articular cartilage repair. Clin Orthop Relat Res 391 Suppl, S182, 2001.
6. Ahmed, T.A., and Hincke, M.T. Strategies for articular cartilage lesion repair and functional restoration. Tissue Eng Part B Rev 16, 305, 2010.
7. Batty, L., Dance, S., Bajaj, S., and Cole, B.J. Autologous chondrocyte implantation: an overview of technique and outcomes. ANZ J Surg 81, 18, 2011.
8. Zhang, L., Hu, J., and Athanasiou, K.A. The role of tissue engineering in articular cartilage repair and regeneration. Crit Rev Biomed Eng 37, 1, 2009.
9. Bijlsma, J.W., Berenbaum, F., and Lafeber, F.P. Osteoarthritis: an update with relevance for clinical practice. Lancet 377, 2115, 2011.
10. Gimble, J., and Guilak, F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 5, 362, 2003.
11. Ronziere, M.C., Perrier, E., Mallein-Gerin, F., and Freyria, A.M. Chondrogenic potential of bone marrow-and adipose tissue-derived adult human mesenchymal stem cells. Biomed Mater Eng 20, 145, 2010.
12. Hildner, F., Albrecht, C., Gabriel, C., Redl, H., and van Griensven, M. State of the art and future perspectives of articular cartilage regeneration: a focus on adipose-derived stem cells and platelet-derived products. J Tissue Eng Regen Med 5, e36, 2011.
13. Solchaga, L.A., Penick, K., Goldberg, V.M., Caplan, A.I., and Welter, J.F. Fibroblast growth factor-2 enhances proliferation and delays loss of chondrogenic potential in human adult bone-marrow-derived mesenchymal stem cells. Tissue Eng Part A 16, 1009, 2010.
14. Estes, B.T., Wu, A.W., Storms, R.W., and Guilak, F. Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adiposederived adult stem cells. J Cell Physiol 209, 987, 2006.
15. Gonda, K., Shigeura, T., Sato, T., Matsumoto, D., Suga, H., Inoue, K., et al. Preserved proliferative capacity and multipotency of human adipose-derived stem cells after longterm cryopreservation. Plastic Reconstr Surg 121, 401, 2008.
16. Puetzer, J.L., Petitte, J.N., and Loboa, E.G. Comparative review of growth factors for induction of three-dimensional in vitro chondrogenesis in human mesenchymal stem cells isolated from bone marrow and adipose tissue. Tissue Eng Part B Rev 16, 435, 2010.
17. Estes, B.T., and Guilak, F. Three-dimensional culture systems to induce chondrogenesis of adipose-derived stem cells. Methods Mol Biol 702, 201, 2011.
18. Awad, H.A., Halvorsen, Y.D., Gimble, J.M., and Guilak, F. Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng 9, 1301, 2003.
19. 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.
20. 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.
21. 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.
22. Xu, Y., Balooch, G., Chiou, M., Bekerman, E., Ritchie, R.O., and Longaker, M.T. Analysis of the material properties of early chondrogenic differentiated adipose-derived stromal cells (ASC) using an in vitro three-dimensional micromass culture system. Biochem Biophys Res Commun 359, 311, 2007.
23. Winter, A., Breit, S., Parsch, D., Benz, K., Steck, E., Hauner, H., et al. Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 48, 418, 2003.
24. Huang, J.I., Zuk, P.A., Jones, N.F., Zhu, M., Lorenz, H.P., Hedrick, M.H., et al. Chondrogenic potential of multipotential cells from human adipose tissue. Plastic Reconstr Surg 113, 585, 2004.
25. Huang, J.I., Kazmi, N., Durbhakula, M.M., Hering, T.M., Yoo, J.U., and Johnstone, B. Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: a patient-matched comparison. J Orthop Res 23, 1383, 2005.
26. Afizah, H., Yang, Z., Hui, J.H., Ouyang, H.W., and Lee, E.H. A comparison between the chondrogenic potential of human bone marrow stem cells (BMSCs) and adiposederived stem cells (ADSCs) taken from the same donors. Tissue Eng 13, 659, 2007.
27. Bunnell, B.A., Flaat, M., Gagliardi, C., Patel, B., and Ripoll, C. Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45, 115, 2008.
28. Johnstone, B., Hering, T.M., Caplan, A.I., Goldberg, V.M., and Yoo, J.U. In vitro chondrogenesis of bone marrowderived mesenchymal progenitor cells. Exp Cell Res 238, 265, 1998.
29. Yoo, J.U., Barthel, T.S., Nishimura, K., Solchaga, L., Caplan, A.I., Goldberg, V.M., et al. The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells. J Bone Joint Surg Am 80, 1745, 1998.
30. Yang, J., Yamato, M., Shimizu, T., Sekine, H., Ohashi, K., Kanzaki, M., et al. Reconstruction of functional tissues with cell sheet engineering. Biomaterials 28, 5033, 2007.
31. Labbe, B., Marceau-Fortier, G., and Fradette, J. Cell sheet technology for tissue engineering: the self-assembly approach using adipose-derived stromal cells. Methods Mol Biol 702, 429, 2011.
32. Gilpin, D.A., Weidenbecher, M.S., and Dennis, J.E. Scaffold-free tissue-engineered cartilage implants for laryngotracheal reconstruction. Laryngoscope 120, 612, 2010.
33. Tani, G., Usui, N., Kamiyama, M., Oue, T., and Fukuzawa, M. In vitro construction of scaffold-free cylindrical cartilage using cell sheet-based tissue engineering. Pediatr Surg Int 26, 179, 2010.
34. Yang, J., Yamato, M., Nishida, K., Ohki, T., Kanzaki, M., Sekine, H., et al. Cell delivery in regenerative medicine: the cell sheet engineering approach. J Control Release 116, 193, 2006.
35. Solorio, L.D., Fu, A.S., Hernandez-Irizarry, R., and Alsberg, E. Chondrogenic differentiation of human mesenchymal stem cell aggregates via controlled release of TGF-beta1 from incorporated polymer microspheres. J Biomed Mater Res A 92, 1139, 2010.
36. Kaneshiro, N., Sato, M., Ishihara, M., Mitani, G., Sakai, H., and Mochida, J. Bioengineered chondrocyte sheets may be potentially useful for the treatment of partial thickness defects of articular cartilage. Biochem Biophys Res Commun 349, 723, 2006.
37. 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.
38. Mayer-Wagner, S., Schiergens, T.S., Sievers, B., Docheva, D., Schieker, M., Betz, O.B., et al. Membrane-based cultures generate scaffold-free neocartilage in vitro: influence of growth factors. Tissue Eng Part A 16, 513, 2010.
39. Solorio, L.D., Vieregge, E.L., Dhami, C.D., Dang, P.N., and Alsberg, E. Engineered cartilage via self-assembled hMSC sheets with incorporated biodegradable gelatin microspheres releasing transforming growth factor-beta1. J Control Release 158, 224, 2012.
40. Ikada, Y., and Tabata, Y. Protein release from gelatin matrices. Adv Drug Deliv Rev 31, 287, 1998.
41. Young, S., Wong, M., Tabata, Y., and Mikos, A.G. Gelatin as a delivery vehicle for the controlled release of bioactive molecules. J Control Release 109, 256, 2005.
42. Hayashi, K., and Tabata, Y. Preparation of stem cell aggregates with gelatin microspheres to enhance biological functions. Acta Biomater 7, 2797, 2011.
43. Ogawa, T., Akazawa, T., and Tabata, Y. In vitro proliferation and chondrogenic differentiation of rat bone marrow stem cells cultured with gelatin hydrogel microspheres for TGF-beta1 release. J Biomater Sci Polym Ed 21, 609, 2010.
44. 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.
45. Chiou, M., Xu, Y., and Longaker, M.T. Mitogenic and chondrogenic effects of fibroblast growth factor-2 in adiposederived mesenchymal cells. Biochem Biophys Res Commun 343, 644, 2006.
46. Han, Y., Wei, Y., Wang, S., and Song, Y. Enhanced chondrogenesis of adipose-derived stem cells by the controlled release of transforming growth factor-beta1 from hybrid microspheres. Gerontology 55, 592, 2009.
47. Merceron, C., Vinatier, C., Portron, S., Masson, M., Amiaud, J., Guigand, L., et al. Differential effects of hypoxia on osteochondrogenic potential of human adipose-derived stem cells. Am J Physiol Cell Physiol 298, C355, 2010.
48. Penick, K.J., Solchaga, L.A., and Welter, J.F. Highthroughput aggregate culture system to assess the chondrogenic potential of mesenchymal stem cells. Biotechniques 39, 687, 2005.
49. Yamamoto, M., Ikada, Y., and Tabata, Y. Controlled release of growth factors based on biodegradation of gelatin hydrogel. J Biomater Sci Polym Ed 12, 77, 2001.
50. Solorio, L., Zwolinski, C., Lund, A.W., Farrell, M.J., and Stegemann, J.P. Gelatin microspheres crosslinked with genipin for local delivery of growth factors. J Tissue Eng Regen Med 4, 514, 2010.
51. McGowan, K.B., Kurtis, M.S., Lottman, L.M., Watson, D., and Sah, R.L. Biochemical quantification of DNA in human articular and septal cartilage using PicoGreen and Hoechst 33258. Osteoarthritis Cartilage 10, 580, 2002.
52. Farndale, R.W., Buttle, D.J., and Barrett, A.J. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883, 173, 1986.
53. Yang, X., Shang, H., Katz, A., and Li, X. A modified aggregate culture for chondrogenesis of human adipose-derived stem cells genetically modified with growth and differentiation factor 5. Biores Open Access 2, 258, 2013.
54. Chua, K.H., Aminuddin, B.S., Fuzina, N.H., and Ruszymah, B.H. Insulin-transferrin-selenium prevent human chondrocyte dedifferentiation and promote the formation of high quality tissue engineered human hyaline cartilage. Eur Cell Mater 9, 58, 2005; discussion.
55. Sandell, L.J., and Daniel, J.C. Effects of ascorbic acid on collagen mRNA levels in short term chondrocyte cultures. Connect Tissue Res 17, 11, 1988.
56. Sekiya, I., Koopman, P., Tsuji, K., Mertin, S., Harley, V., Yamada, Y., et al. Dexamethasone enhances SOX9 expression in chondrocytes. J Endocrinol 169, 573, 2001.
57. Marques, M.E., Coelho, K.I., Sotto, M.N., and Bacchi, C.E. Comparison between histochemical and immunohistochemical methods for diagnosis of sporotrichosis. J Clin Pathol 45, 1089, 1992.
58. Obert, L.A., Sobocinski, G.P., Bobrowski, W.F., Metz, A.L., Rolsma, M.D., Altrogge, D.M., et al. An immunohistochemical approach to differentiate hepatic lipidosis from hepatic phospholipidosis in rats. Toxicol Pathol 35, 728, 2007.
59. 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.
60. 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.
61. Diekman, B.O., Rowland, C.R., Lennon, D.P., Caplan, A.I., and Guilak, F. Chondrogenesis of adult stem cells from adipose tissue and bone marrow: induction by growth factors and cartilage-derived matrix. Tissue Eng Part A 16, 523, 2010.
62. 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 chondrogenesis of mesenchymal stem cells from bone marrow and adipose tissue. Tissue Eng 12, 2853, 2006.
63. Kisiday, J.D., Kopesky, P.W., Evans, C.H., Grodzinsky, A.J., McIlwraith, C.W., and Frisbie, D.D. Evaluation of adult equine bone marrow-and adipose-derived progenitor cell chondrogenesis in hydrogel cultures. J Orthop Res 26, 322, 2008.
64. 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.
65. Hildner, F., Peterbauer, A., Wolbank, S., Nurnberger, S., Marlovits, S., Redl, H., et al. FGF-2 abolishes the chondrogenic effect of combined BMP-6 and TGF-beta in human adipose derived stem cells. J Biomed Mater Res A 94, 978, 2010.
66. Lima, E.G., Bian, L., Ng, K.W., Mauck, R.L., Byers, B.A., Tuan, R.S., et al. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with TGF-beta3. Osteoarthritis Cartilage 15, 1025, 2007.
67. Kelly, D.J., Crawford, A., Dickinson, S.C., Sims, T.J., Mundy, J., Hollander, A.P., et al. Biochemical markers of the mechanical quality of engineered hyaline cartilage. J Mater Sci Mater Med 18, 273, 2007.
68. Tran, S.C., Cooley, A.J., and Elder, S.H. Effect of a mechanical stimulation bioreactor on tissue engineered, scaffoldfree cartilage. Biotechnol Bioeng 108, 1421, 2011.
69. Sophia Fox, A.J., Bedi, A., and Rodeo, S.A. The basic science of articular cartilage: structure, composition, and function. Sports Health 1, 461, 2009.
70. Mansour, J.M. Biomechanics of cartilage. In: Oatis, C., ed. Kinesiology: The Mechanics and Pathomechanics of Human Movement. Philadelphia, PA: Lippincott Williams and Wilkins, 2003. pp. 66-79.
71. Puissant, B., Barreau, C., Bourin, P., Clavel, C., Corre, J., Bousquet, C., et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129, 118, 2005.
72. Melief, S.M., Zwaginga, J.J., Fibbe, W.E., and Roelofs, H. Adipose tissue-derived multipotent stromal cells have a higher immunomodulatory capacity than their bone marrow-derived counterparts. Stem Cells Transl Med 2, 455, 2013.
73. Yoo, K.H., Jang, I.K., Lee, M.W., Kim, H.E., Yang, M.S., Eom, Y., et al. Comparison of immunomodulatory properties of mesenchymal stem cells derived from adult human tissues. Cell Immunol 259, 150, 2009.
74. Mehlhorn, A.T., Niemeyer, P., Kaschte, K., Muller, L., Finkenzeller, G., Hartl, D., et al. Differential effects of BMP-2 and TGF-beta1 on chondrogenic differentiation of adipose derived stem cells. Cell Prolif 40, 809, 2007