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BioMed Research International
Volume 2014, Article ID 539789, 10 pages
http://dx.doi.org/10.1155/2014/539789
Research Article

3D Dynamic Culture of Rabbit Articular Chondrocytes Encapsulated in Alginate Gel Beads Using Spinner Flasks for Cartilage Tissue Regeneration

State Key Laboratory of Bioreactor Engineering, School of Bioengineering, East China University of Science and Technology, 130 Mei-Long Road, P.O. Box 309, Shanghai 200237, China

Received 20 May 2014; Revised 11 September 2014; Accepted 14 September 2014; Published 24 November 2014

Academic Editor: Magali Cucchiarini

Copyright © 2014 Feiyue Xu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. N. Redman, S. F. Oldfield, C. W. Archer, P. J. Roughley, and C. Lee, “Current strategies for articular cartilage repair,” European Cells and Materials, vol. 9, pp. 23–32, 2005. View at Google Scholar · View at Scopus
  2. M. Brittberg, A. Lindahl, A. Nilsson, C. Ohlsson, O. Isaksson, and L. Peterson, “Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation,” The New England Journal of Medicine, vol. 331, no. 14, pp. 889–895, 1994. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Knutsen, J. O. Drogset, L. Engebretsen et al., “A randomized trial comparing autologous chondrocyte implantation with microfracture: findings at five years,” Journal of Bone and Joint Surgery A, vol. 89, no. 10, pp. 2105–2112, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. S. R. Tew, A. D. Murdoch, R. P. Rauchenberg, and T. E. Hardingham, “Cellular methods in cartilage research: primary human chondrocytes in culture and chondrogenesis in human bone marrow stem cells,” Methods, vol. 45, no. 1, pp. 2–9, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Schulze-Tanzil, “Activation and dedifferentiation of chondrocytes: implications in cartilage injury and repair,” Annals of Anatomy, vol. 191, no. 4, pp. 325–338, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. D. C. Crawford, T. M. DeBerardino, and R. J. Williams III, “NeoCart, an autologous cartilage tissue implant, compared with microfracture for treatment of distal femoral cartilage lesions: an FDA phase-II prospective, randomized clinical trial after two years,” Journal of Bone and Joint Surgery Series A, vol. 94, no. 11, pp. 979–989, 2012. View at Google Scholar · View at Scopus
  7. A. Barbero, S. Ploegert, M. Heberer, and I. Martin, “Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes,” Arthritis & Rheumatism, vol. 48, no. 5, pp. 1315–1325, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Malda, D. E. Martens, J. Tramper, C. A. van Blitterswijk, and J. Riesle, “Cartilage tissue engineering: controversy in the effect of oxygen,” Critical Reviews in Biotechnology, vol. 23, no. 3, pp. 175–194, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Schrobback, T. J. Klein, R. Crawford, Z. Upton, J. Malda, and D. I. Leavesley, “Effects of oxygen and culture system on in vitro propagation and redifferentiation of osteoarthritic human articular chondrocytes,” Cell and Tissue Research, vol. 347, no. 3, pp. 649–663, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Malda, E. Kreijveld, J. S. Temenoff, C. A. van Blitterswijk, and J. Riesle, “Expansion of human nasal chondrocytes on macroporous microcarriers enhances redifferentiation,” Biomaterials, vol. 24, no. 28, pp. 5153–5161, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. J. M. Melero-Martin, M.-A. Dowling, M. Smith, and M. Al-Rubeai, “Expansion of chondroprogenitor cells on macroporous microcarriers as an alternative to conventional monolayer systems,” Biomaterials, vol. 27, no. 15, pp. 2970–2979, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Schrobback, T. J. Klein, M. Schuetz, Z. Upton, D. I. Leavesley, and J. Malda, “Adult human articular chondrocytes in a microcarrier-based culture system: expansion and redifferentiation,” Journal of Orthopaedic Research, vol. 29, no. 4, pp. 539–546, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Takahashi, T. Ogasawara, Y. Asawa et al., “Three-dimensional microenvironments retain chondrocyte phenotypes during proliferation culture,” Tissue Engineering, vol. 13, no. 7, pp. 1583–1592, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. M. D. Buschmann, Y. A. Gluzband, A. J. Grodzinsky, J. H. Kimura, and E. B. Hunziker, “Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix,” Journal of Orthopaedic Research, vol. 10, no. 6, pp. 745–758, 1992. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Grandolfo, P. D'Andrea, S. Paoletti et al., “Culture and differentiation of chondrocytes entrapped in alginate gels,” Calcified Tissue International, vol. 52, no. 1, pp. 42–48, 1993. View at Publisher · View at Google Scholar · View at Scopus
  16. H. J. Häuselmann, R. J. Fernandas, S. S. Mok et al., “Phenotypic stability of bovine articular chondrocytes after long-term culture in alginate beads,” Journal of Cell Science, vol. 107, part 1, pp. 17–27, 1994. View at Google Scholar · View at Scopus
  17. J. Bonaventure, N. Kadhom, L. Cohen-Solal et al., “Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads,” Experimental Cell Research, vol. 212, no. 1, pp. 97–104, 1994. View at Publisher · View at Google Scholar · View at Scopus
  18. M. M. J. Caron, P. J. Emans, M. M. E. Coolsen et al., “Redifferentiation of dedifferentiated human articular chondrocytes: comparison of 2D and 3D cultures,” Osteoarthritis and Cartilage, vol. 20, no. 10, pp. 1170–1178, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Lemare, N. Steimberg, C. le Griel, S. Demignot, and M. Adolphe, “Dedifferentiated chondrocytes cultured in alginate beads: restoration of the differentiated phenotype and of the metabolic responses to interleukin-1beta,” Journal of Cellular Physiology, vol. 176, no. 2, pp. 303–313, 1998. View at Google Scholar
  20. J. Heyland, K. Wiegandt, C. Goepfert et al., “Redifferentiation of chondrocytes and cartilage formation under intermittent hydrostatic pressure,” Biotechnology Letters, vol. 28, no. 20, pp. 1641–1648, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. D. M. García Cruz, M. Salmerón-Sánchez, and J. L. Gómez-Ribelles, “Stirred flow bioreactor modulates chondrocyte growth and extracellular matrix biosynthesis in chitosan scaffolds,” Journal of Biomedical Materials Research Part A, vol. 100, no. 9, pp. 2330–2341, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. T.-J. Lee, S. H. Bhang, W.-G. La et al., “Spinner-flask culture induces redifferentiation of de-differentiated chondrocytes,” Biotechnology Letters, vol. 33, no. 4, pp. 829–836, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Xu, Q. Wang, F. Xu, Z. Ye, Y. Zhou, and W. S. Tan, “Mesenchymal stem cells downregulate articular chondrocyte differentiation in noncontact coculture systems: Implications in cartilage tissue regeneration,” Stem Cells and Development, vol. 22, no. 11, pp. 1657–1669, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. R. L. Y. Sah, J.-Y. H. Doong, and A. J. Grodzinsky, “Fluorometric assay of DNA in cartilage explants using Hoechst 33258,” Analytical Biochemistry, vol. 174, no. 1, pp. 168–176, 1988. View at Publisher · View at Google Scholar · View at Scopus
  25. B. O. Enobakhare, D. L. Bader, and D. A. Lee, “Quantification of sulfated glycosaminoglycans in chondrocyte/alginate cultures, by use of 1,9-dimethylmethylene blue,” Analytical Biochemistry, vol. 243, no. 1, pp. 189–191, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. P. C. M. Verdonk, K. F. Almqvist, R. Verdonk, K. L. Verstraete, and G. Verbruggen, “Allogeneic chondrocyte-based cartilage repair using alginate beads,” in Cartilage Repair Strategies, R. J. Williams, Ed., pp. 219–232, Humana Press, Totowa, NJ, USA, 2007. View at Google Scholar
  27. C. J. O'Conor, N. Case, and F. Guilak, “Mechanical regulation of chondrogenesis,” Stem Cell Research and Therapy, vol. 4, no. 4, article 61, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. N. H. Veilleux, I. V. Yannas, and M. Spector, “Effect of passage number and collagen type on the proliferative, biosynthetic, and contractile activity of adult canine articular chondrocytes in type I and II collagen-glycosaminoglycan matrices in vitro,” Tissue Engineering, vol. 10, no. 1-2, pp. 119–127, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Schulze-Tanzil, P. de Souza, H. Villegas Castrejon et al., “Redifferentiation of dedifferentiated human chondrocytes in high-density cultures,” Cell and Tissue Research, vol. 308, no. 3, pp. 371–379, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Schnabel, S. Marlovits, G. Eckhoff et al., “Dedifferentiation-associated changes in morphology and gene expression in primary human articular chondrocytes in cell culture,” Osteoarthritis and Cartilage, vol. 10, no. 1, pp. 62–70, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Domm, M. Schünke, K. Christesen, and B. Kurz, “Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension,” Osteoarthritis and Cartilage, vol. 10, no. 1, pp. 13–22, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Zhang, H. Song, and X. Zhao, “Optimum combination of insulin-transferrin-selenium and fetal bovine serum for culture of rabbit articular chondrocytes in three-dimensional alginate scaffolds,” International Journal of Cell Biology, vol. 2009, Article ID 747016, 6 pages, 2009. View at Publisher · View at Google Scholar
  33. K. F. Almqvist, L. Wang, J. Wang et al., “Culture of chondrocytes in alginate surrounded by fibrin gel: characteristics of the cells over a period of eight weeks,” Annals of the Rheumatic Diseases, vol. 60, no. 8, pp. 781–790, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Jonitz, K. Lochner, K. Peters et al., “Differentiation capacity of human chondrocytes embedded in alginate matrix,” Connective Tissue Research, vol. 52, no. 6, pp. 503–511, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Zeiter, M. van der Werf, and K. Ito, “The fate of bovine bone marrow stromal cells in hydrogels: a comparison to nucleus pulposus cells and articular chondrocytes,” Journal of Tissue Engineering and Regenerative Medicine, vol. 3, no. 4, pp. 310–320, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. C. R. Lee, A. J. Grodzinsky, and M. Spector, “Biosynthetic response of passaged chondrocytes in a type II collagen scaffold to mechanical compression,” Journal of Biomedical Materials Research A, vol. 64, no. 3, pp. 560–569, 2003. View at Google Scholar · View at Scopus
  37. S. P. Grogan, S. Sovani, C. Pauli et al., “Effects of perfusion and dynamic loading on human neocartilage formation in alginate hydrogels,” Tissue Engineering—Part A, vol. 18, no. 17-18, pp. 1784–1792, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Shahin and P. M. Doran, “Strategies for enhancing the accumulation and retention of extracellular matrix in tissue-engineered cartilage cultured in bioreactors,” PLoS ONE, vol. 6, no. 8, Article ID e23119, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Diaz-Romero, D. Nesic, S. P. Grogan, P. Heini, and P. Mainil-Varlet, “Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells,” Journal of Cellular Physiology, vol. 214, no. 1, pp. 75–83, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Chubinskaya, K. Huch, M. Schulze, L. Otten, M. B. Aydelotte, and A. A. Cole, “Gene expression by human articular chondrocytes cultured in alginate beads,” Journal of Histochemistry and Cytochemistry, vol. 49, no. 10, pp. 1211–1220, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Dickhut, K. Pelttari, P. Janicki et al., “Calcification or dedifferentiation: requirement to lock mesenchymal stem cells in a desired differentiation stage,” Journal of Cellular Physiology, vol. 219, no. 1, pp. 219–226, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. E. J. Mackie, Y. A. Ahmed, L. Tatarczuch, K.-S. Chen, and M. Mirams, “Endochondral ossification: How cartilage is converted into bone in the developing skeleton,” The International Journal of Biochemistry & Cell Biology, vol. 40, no. 1, pp. 46–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Wu, E. Delassus, D. Patra, W. Liao, and L. J. Sandell, “Effects of serum and compressive loading on the cartilage matrix synthesis and spatiotemporal deposition around chondrocytes in 3D culture,” Tissue Engineering—Part A, vol. 19, no. 9-10, pp. 1199–1208, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Xue, Y. Zhu, Y. Zhang, C. Chiang, G. Zhou, and K. Liu, “Xenogeneic chondrocytes promote stable subcutaneous chondrogenesis of bone marrow-derived stromal cells,” International Journal of Molecular Medicine, vol. 29, no. 2, pp. 146–152, 2012. View at Publisher · View at Google Scholar · View at Scopus