About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 598056, 11 pages
http://dx.doi.org/10.1155/2013/598056
Research Article

Biocompatibility Assessment of Novel Collagen-Sericin Scaffolds Improved with Hyaluronic Acid and Chondroitin Sulfate for Cartilage Regeneration

1Department of Biochemistry and Molecular Biology, University of Bucharest, 91-95 Splaiul Independentei, 050095 Bucharest, Romania
2Collagen Department, Leather and Footwear Research Institute, 93 Ion Minulescu, 031215 Bucharest, Romania
3Advanced Polymer Materials Group, Department of Bioresources and Polymer Science, University Politehnica of Bucharest, 149 Calea Victoriei, 010072 Bucharest, Romania
4Molecular Biology and Pathology Research Lab “Molimagex”, University Hospital Bucharest, 169 Splaiul Independentei, 050098 Bucharest, Romania
5Department of Histology, Faculty of Medicine, Pharmacy and Dentistry, Vasile Goldis Western University of Arad, 1 Feleacului, 310396 Arad, Romania
6Department of Experimental and Applied Biology, Institute of Life Sciences, Vasile Goldis Western University of Arad, 86 Rebreanu, 310414 Arad, Romania

Received 19 July 2013; Accepted 27 September 2013

Academic Editor: Antonio Salgado

Copyright © 2013 Sorina Dinescu 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. F. Guilak, “Functional tissue engineering: the role of biomechanics in reparative medicine,” Annals of the New York Academy of Sciences, vol. 961, pp. 193–195, 2002. View at Scopus
  2. R. Katayama, S. Wakitani, N. Tsumaki et al., “Repair of articular cartilage defects in rabbits using CDMP1 gene-transfected autologous mesenchymal cells derived from bone marrow,” Rheumatology, vol. 43, no. 8, pp. 980–985, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Fan, Y. Hu, C. Zhang et al., “Cartilage regeneration using mesenchymal stem cells and a PLGA-gelatin/chondroitin/hyaluronate hybrid scaffold,” Biomaterials, vol. 27, no. 26, pp. 4573–4580, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Park, B. Choi, J. Hu, and M. Lee, “Injectable chitosan hyaluronic acid hydrogels for cartilage tissue engineering,” Acta Biomaterialia, vol. 9, no. 1, pp. 4779–4786, 2013. View at Publisher · View at Google Scholar
  5. R. A. A. Muzzarelli, F. Greco, A. Busilacchi, V. Sollazzo, and A. Gigante, “Chitosan, hyaluronan and chondroitin sulfate in tissue engineering for cartilage regeneration: a review,” Carbohydrate Polymers, vol. 89, no. 3, pp. 723–739, 2012. View at Publisher · View at Google Scholar
  6. J. A. Buckwalter and H. J. Mankin, “Articular cartilage. Part I: tissue design and chondrocyte-matrix interactions,” Journal of Bone and Joint Surgery A, vol. 79, no. 4, pp. 600–611, 1997. View at Scopus
  7. Y. Wang, U.-J. Kim, D. J. Blasioli, H.-J. Kim, and D. L. Kaplan, “In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells,” Biomaterials, vol. 26, no. 34, pp. 7082–7094, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. C.-H. Chang, H.-C. Liu, C.-C. Lin, C.-H. Chou, and F.-H. Lin, “Gelatin-chondroitin-hyaluronan tri-copolymer scaffold for cartilage tissue engineering,” Biomaterials, vol. 24, no. 26, pp. 4853–4858, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Chung and J. A. Burdick, “Engineering cartilage tissue,” Advanced Drug Delivery Reviews, vol. 60, no. 2, pp. 243–262, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Wakitani, T. Goto, R. G. Young, J. M. Mansour, V. M. Goldberg, and A. I. Caplan, “Repair of large full-thickness articular cartilage defects with allograft articular chondrocytes embedded in a collagen gel,” Tissue Engineering, vol. 4, no. 4, pp. 429–444, 1998. View at Scopus
  11. C. R. Lee, A. J. Grodzinsky, H.-P. Hsu, and M. Spector, “Effects of a cultured autologous chondrocyte-seeded type II collagen scaffold on the healing of a chondral defect in a canine model,” Journal of Orthopaedic Research, vol. 21, no. 2, pp. 272–281, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Galateanu, S. Dinescu, A. Cimpean, A. Dinischiotu, and M. Costache, “Modulation of adipogenic conditions for prospective use of ASCs in adipose tissue engineering,” International Journal of Molecular Sciences, vol. 12, pp. 15881–15900, 2012.
  13. G. H. Altman, F. Diaz, C. Jakuba et al., “Silk-based biomaterials,” Biomaterials, vol. 24, no. 3, pp. 401–416, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Terada, T. Nishimura, M. Sasaki, H. Yamada, and M. Miki, “Sericin, a protein derived from silkworms, accelerates the proliferation of several mammalian cell lines including a hybridoma,” Cytotechnology, vol. 40, no. 1–3, pp. 3–12, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Tsubouchi, Y. Igarashi, Y. Takasu, and H. Yamada, “Sericin enhances attachment of cultured human skin fibroblasts,” Bioscience, Biotechnology and Biochemistry, vol. 69, no. 2, pp. 403–405, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Terada, M. Sasaki, K. Yanagihara, and H. Yamada, “Preparation of silk protein sericin as mitogenic factor for better mammalian cell culture,” Journal of Bioscience and Bioengineering, vol. 100, no. 6, pp. 667–671, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Aramwit, S. Kanokpanont, W. De-Eknamkul, K. Kamei, and T. Srichana, “The effect of sericin with variable amino-acid content from different silk strains on the production of collagen and nitric oxide,” Journal of Biomaterials Science, Polymer Edition, vol. 20, no. 9, pp. 1295–1306, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Aramwit and A. Sangcakul, “The effects of sericin cream on wound healing in rats,” Bioscience, Biotechnology and Biochemistry, vol. 71, no. 10, pp. 2473–2477, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Aramwit, S. Kanokpanont, T. Nakpheng, and T. Srichana, “The effect of sericin from various extraction methods on cell viability and collagen production,” International Journal of Molecular Sciences, vol. 11, no. 5, pp. 2200–2211, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Yamane, N. Iwasaki, T. Majima et al., “Feasibility of chitosan-based hyaluronic acid hybrid biomaterial for a novel scaffold in cartilage tissue engineering,” Biomaterials, vol. 26, no. 6, pp. 611–619, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. H. B. Fan, Y. Y. Hu, and X. S. Li, “Experimental study on gelatin-chondroitin sulfate-sodium hyaluronate tri-copolymer as novel scaffolds for cartilage tissue engineering,” Chinese Journal of Reparatıve and Reconstructıve Surgery, vol. 19, pp. 473–477, 2005.
  22. Y.-L. Chen, H.-P. Lee, H.-Y. Chan, L.-Y. Sung, H.-C. Chen, and Y.-C. Hu, “Composite chondroitin-6-sulfate/dermatan sulfate/chitosan scaffolds for cartilage tissue engineering,” Biomaterials, vol. 28, no. 14, pp. 2294–2305, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Tan, C. R. Chu, K. A. Payne, and K. G. Marra, “Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for cartilage tissue engineering,” Biomaterials, vol. 30, no. 13, pp. 2499–2506, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Jin, L. S. Moreira Teixeira, P. J. Dijkstra, C. A. van Blitterswijk, M. Karperien, and J. Feijen, “Enzymatically-crosslinked injectable hydrogels based on biomimetic dextran-hyaluronic acid conjugates for cartilage tissue engineering,” Biomaterials, vol. 31, no. 11, pp. 3103–3113, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. K.-Y. Chang, L.-W. Cheng, G.-H. Ho, Y.-P. Huang, and Y.-D. Lee, “Fabrication and characterization of poly(γ-glutamic acid)-graft-chondroitin sulfate/polycaprolactone porous scaffolds for cartilage tissue engineering,” Acta Biomaterialia, vol. 5, no. 6, pp. 1937–1947, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Hu, D. Li, F. Zhou, and C. Gao, “Biological hydrogel synthesized from hyaluronic acid, gelatin and chondroitin sulfate by click chemistry,” Acta Biomaterialia, vol. 7, no. 4, pp. 1618–1626, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. B. P. Toole, “Hyaluronan in morphogenesis,” Seminars in Cell and Developmental Biology, vol. 12, no. 2, pp. 79–87, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Tognana, R. F. Padera, F. Chen, G. Vunjak-Novakovic, and L. E. Freed, “Development and remodeling of engineered cartilage-explant composites in vitro and in vivo,” Osteoarthritis and Cartilage, vol. 13, no. 10, pp. 896–905, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Gerwin, C. Hops, and A. Lucke, “Intraarticular drug delivery in osteoarthritis,” Advanced Drug Delivery Reviews, vol. 58, no. 2, pp. 226–242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Akmal, A. Singh, A. Anand et al., “The effects of hyaluronic acid on articular chondrocytes,” Journal of Bone and Joint Surgery B, vol. 87, no. 8, pp. 1143–1149, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Jerosch, “Effects of glucosamine and chondroitin sulfate on cartilage metabolism in OA: outlook on other nutrient partners especially omega-3 fatty acids,” International Journal of Rheumatology, vol. 2011, Article ID 969012, 17 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Servaty, J. Schiller, H. Binder, and K. Arnold, “Hydration of polymeric components of cartilage—an infrared spectroscopic study on hyaluronic acid and chondroitin sulfate,” International Journal of Biological Macromolecules, vol. 28, no. 2, pp. 121–127, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. X. He, Y. Wang, and G. Wu, “Layer-by-layer assembly of type I collagen and chondroitin sulfate on aminolyzed PU for potential cartilage tissue engineering application,” Applied Surface Science, vol. 258, no. 24, pp. 9918–9925, 2012. View at Publisher · View at Google Scholar
  34. Q. Li, C. G. Williams, D. D. N. Sun, J. Wang, K. Leong, and J. H. Elisseeff, “Photocrosslinkable polysaccharides based on chondroitin sulfate,” Journal of Biomedical Materials Research A, vol. 68, no. 1, pp. 28–33, 2004. View at Scopus
  35. J. M. Gimble, A. J. Katz, and B. A. Bunnell, “Adipose-derived stem cells for regenerative medicine,” Circulation Research, vol. 100, no. 9, pp. 1249–1260, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. J. K. Fraser, I. Wulur, Z. Alfonso, and M. H. Hedrick, “Fat tissue: an underappreciated source of stem cells for biotechnology,” Trends in Biotechnology, vol. 24, no. 4, pp. 150–154, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. T. G. Ebrahimian, F. Pouzoulet, C. Squiban et al., “Cell therapy based on adipose tissue-derived stromal cells promotes physiological and pathological wound healing,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 4, pp. 503–510, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. A. T. Badillo, R. A. Redden, L. Zhang, E. J. Doolin, and K. W. Liechty, “Treatment of diabetic wounds with fetal murine mesenchymal stromal cells enhances wound closure,” Cell and Tissue Research, vol. 329, no. 2, pp. 301–311, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. N. San Martín and B. G. Gálvez, “A new paradigm for the understanding of obesity: the role of stem cells,” Archives of Physiology and Biochemistry, vol. 117, no. 3, pp. 188–194, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. P. A. Zuk, M. Zhu, P. Ashjian et al., “Human adipose tissue is a source of multipotent stem cells,” Molecular Biology of the Cell, vol. 13, no. 12, pp. 4279–4295, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. H. A. Awad, Y.-D. C. Halvorsen, J. M. Gimble, and F. Guilak, “Effects of transforming growth factor β1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells,” Tissue Engineering, vol. 9, no. 6, pp. 1301–1312, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. J. M. Gimble and F. Guilak, “Adipose-derived adult stem cells: isolation, characterization, and differentiation potential,” Cytotherapy, vol. 5, no. 5, pp. 362–369, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Gronthos, D. M. Franklin, H. A. Leddy, P. G. Robey, R. W. Storms, and J. M. Gimble, “Surface protein characterization of human adipose tissue-derived stromal cells,” Journal of Cellular Physiology, vol. 189, no. 1, pp. 54–63, 2001. View at Publisher · View at Google Scholar
  45. H. Mizuno, P. A. Zuk, M. Zhu, H. P. Lorenz, P. Benhaim, and M. H. Hedrick, “Myogenic differentiation by human processed lipoaspirate cells,” Plastic and Reconstructive Surgery, vol. 109, no. 1, pp. 199–209, 2002. View at Scopus
  46. K. M. Safford, S. D. Safford, J. M. Gimble, A. K. Shetty, and H. E. Rice, “Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells,” Experimental Neurology, vol. 187, no. 2, pp. 319–328, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. P. A. Zuk, M. Zhu, H. Mizuno et al., “Multilineage cells from human adipose tissue: implications for cell-based therapies,” Tissue Engineering, vol. 7, no. 2, pp. 211–228, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. R. B. Jakobsen, A. Shahdadfar, F. P. Reinholt, and J. E. Brinchmann, “Chondrogenesis in a hyaluronic acid scaffold: comparison between chondrocytes and MSC from bone marrow and adipose tissue,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 18, no. 10, pp. 1407–1416, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. M. G. Albu, Collagen Gels and Matrices for Biomedical Applications, Lambert Academic Publishing, Saarbrücken, Germany, 2011.
  50. S. Dinescu, B. Galateanu, M. G. Albu, A. Cimpean, A. Dinischiotu, and M. Costache, “Sericin enhances the bioperformance of collagen-based matrices preseeded with ASCs,” International Journal of Molecular Sciences, vol. 14, no. 1, pp. 1870–1889, 2013.
  51. A. Lungu, M. G. Albu, N. M. Florea, I. C. Stancu, E. Vasile, and H. Iovu, “The influence of glycosaminoglycan type on the collagen-glycosaminoglycan porous scaffolds,” Digest Journal of Nanomaterials and Biostructures, vol. 6, no. 4, pp. 1867–1875, 2011. View at Scopus
  52. A. Lungu, M. G. Albu, I. C. Stancu, N. M. Florea, E. Vasile, and H. Iovu, “Superporous collagen-sericin scaffolds,” Journal of Applied Polymer Science, vol. 127, no. 3, pp. 2269–2279, 2013. View at Publisher · View at Google Scholar
  53. M. G. Albu, M. Ferdes, D. A. Kaya et al., “Collagen wound dressings with anti-inflammatory activity,” Molecular Crystals and Liquid Crystals, vol. 555, no. 1, pp. 271–279, 2012. View at Publisher · View at Google Scholar · View at Scopus