Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 7053465, 11 pages
https://doi.org/10.1155/2017/7053465
Research Article

Successful Low-Cost Scaffold-Free Cartilage Tissue Engineering Using Human Cartilage Progenitor Cell Spheroids Formed by Micromolded Nonadhesive Hydrogel

1Laboratório de Bioengenharia Tecidual, Instituto Nacional de Metrologia, Qualidade e Tecnologia (Inmetro), Duque de Caxias, RJ, Brazil
2Programa de Pós-graduação em Biotecnologia, Instituto Nacional de Metrologia, Qualidade e Tecnologia (Inmetro), Duque de Caxias, RJ, Brazil
3Programa de Pós-graduação em Biomedicina Translacional, Universidade do Grande Rio (UNIGRANRIO), Duque de Caxias, RJ, Brazil
4Núcleo Multidisciplinar de Pesquisa em Biologia (Numpex-Bio), Universidade Federal do Rio de Janeiro (UFRJ) Polo de Xerém, Duque de Caxias, RJ, Brazil
5Department of Chemistry, University of Illinois at Urbana–Champaign, Urbana, IL 61801, USA
6Escola de Odontologia, Universidade Federal Fluminense (UFF), Niterói, RJ, Brazil
7Regenerative Medicine Center, Sechenov Medical University, Moscow, Russia

Correspondence should be addressed to Leandra S. Baptista; moc.liamg@atsitpab.ardnael

Received 19 July 2017; Revised 5 October 2017; Accepted 31 October 2017; Published 20 December 2017

Academic Editor: Celeste Scotti

Copyright © 2017 Mellannie P. Stuart 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. D. F. Williams, “On the nature of biomaterials,” Biomaterials, vol. 30, no. 30, pp. 5897–5909, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. E. Fennema, N. Rivron, J. Rouwkema, C. van Blitterswijk, and J. de Boer, “Spheroid culture as a tool for creating 3D complex tissues,” Trends in Biotechnology, vol. 31, no. 2, pp. 108–115, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. A. P. Napolitano, P. Chai, D. M. Dean, and R. Morgan, “Dynamics of the self- assembly of complex cellular aggregates on micromoldednonadhesive hydrogels,” Tissue Engineering, vol. 13, no. 8, pp. 2087–2094, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Fujie, R. Nansai, W. Ando et al., “Zone-specific integrated cartilage repair using a scaffold-free tissue engineered construct derived from allogenic synovial mesenchymal stem cells: biomechanical and histological assessments,” Journal of Biomechanics, vol. 48, no. 15, pp. 4101–4108, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Ishihara, K. Nakayama, S. Akieda, S. Matsuda, and Y. Iwamoto, “Simultaneous regeneration of full-thickness cartilage and subchondral bone defects in vivo using a three-dimensional scaffold-free autologous construct derived from high-density bone marrow-derived mesenchymal stem cells,” Journal of Orthopaedic Surgery Research, vol. 9, no. 98, pp. 1–10, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. T. M. Achilli, J. Meyer, and J. R. Morgan, “Advances in the formation, use and understanding of multi-cellular spheroids,” Expert Opinion on Biological Therapy, vol. 12, no. 10, pp. 1347–1360, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. S. K. Kapur, X. Wang, H. Shang et al., “Human adipose stem cells maintain proliferative, synthetic and multipotential properties when suspension cultured as self-assembling spheroids,” Biofabrication, vol. 4, no. 2, pp. 1–12, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Xie, M. Mao, L. Zhou, and B. Jiang, “Spheroid mesenchymal stem cells and mesenchymal stem cell-derived microvesicles: two potential therapeutic strategies,” Stem Cells and Development, vol. 25, no. 3, pp. 203–213, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. B. E. Bobick, F. H. Chen, A. M. Le, and R. S. Tuan, “Regulation of the chondrogenic phenotype in culture,” Birth Defects Research, vol. 87, no. 4, pp. 351–371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. E. S. Tzanakakis, L. K. Hansen, and W. S. Hu, “The role of actin filaments and microtubules in hepatocyte spheroid self-assembly,” Cytoskeleton, vol. 48, no. 3, pp. 175–189, 2001. View at Publisher · View at Google Scholar
  11. L. Bian, M. Guvendiren, R. L. Mauck, and J. A. Burdick, “Hydrogels that mimic developmentally relevant matrix and N-cadherin interactions enhance MSC chondrogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 25, pp. 10117–10122, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. A. M. DeLise, L. Fischer, and R. S. Tuan, “Cellular interactions and signaling in cartilage development,” Osteoarthritis and Cartilage, vol. 8, no. 5, pp. 309–334, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. B. K. Hall and T. Miyake, “Divide, accumulate, differentiate: cell condensation in skeletal development revisited,” International Journal of Developmental Biology, vol. 39, no. 6, pp. 881–893, 1995. View at Google Scholar
  14. S. Sart, A. C. Tsai, Y. Li, and T. Ma, “Three-dimensional aggregates of mesenchymal stem cells: cellular mechanisms, biological properties, and applications,” Tissue Engineering Part B: Reviews, vol. 20, no. 5, pp. 365–380, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. B. Sridharan, S. M. Lin, A. T. Hwu, A. D. Laflin, and M. S. Detamore, “Stem cells in aggregate form to enhance chondrogenesis in hydrogels,” PLoS One, vol. 10, no. 12, article e0141479, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. R. A. Somoza, J. F. Welter, D. Correa, and A. I. Caplan, “Chondrogenic differentiation of mesenchymal stem cells: challenges and unfulfilled expectations,” Tissue Engineering Part B: Reviews, vol. 20, no. 6, pp. 596–608, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Jiang and S. Tuan, “Origin and function of cartilage stem/progenitor cells in osteoarthritis,” Nature Reviews Rheumatology, vol. 11, no. 4, pp. 206–212, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Shafiee, M. Kabiri, N. Ahmadbeigi et al., “Nasal septum-derived multipotent progenitors: a potent source for stem cell-based regenerative medicine,” Stem Cells and Development, vol. 20, no. 12, pp. 2077–2091, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. R. J. F. C. do Amaral, C. S. G. Pedrosa, M. C. L. Kochem et al., “Isolation of human nasoseptal chondrogenic cells: a promise for cartilage engineering,” Stem Cell Research, vol. 8, no. 2, pp. 292–299, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. L. S. Baptista, K. R. Silva, C. S. Pedrosa et al., “Bioengineered cartilage in a scaffold-free method by human cartilage-derived progenitor cells: a comparison with human adipose-derived mesenchymal stromal cells,” Artificial Organs, vol. 37, no. 12, pp. 1068–1075, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. T. J. Bartosh, J. H. Ylöstalo, A. Mohammadipoor et al., “Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their anti-inflammatory properties,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 31, pp. 13724–13729, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. J. M. Kelm and M. Fussenegger, “Scaffold-free cell delivery for use in regenerative medicine,” Advanced Drug Reviews, vol. 62, no. 7-8, pp. 753–764, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Polacek, J. A. Bruun, O. Johansen, and I. Martinez, “Comparative analyses of the secretome from dedifferentiated and redifferentiated adult articular chondrocytes,” Cartilage, vol. 2, no. 2, pp. 186–196, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Murata, S. Tokunaga, T. Tamura et al., “A preliminary study of osteochondral regeneration using a scaffold-free three-dimensional construct of porcine adipose tissue-derived mesenchymal stem cells,” Journal of Orthopaedic and Surgery Research, vol. 18, pp. 10–35, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. M. W. Laschke and M. D. Menger, “Life is 3D: boosting spheroid function for tissue engineering,” Trends in Biotechnology, vol. 35, no. 2, pp. 133–144, 2017. View at Publisher · View at Google Scholar
  26. K. R. Silva, G. S. Kronemberger, I. Côrtes et al., “Improving clinical uses of mesenchymal stromal cells by 3D scaffold-free constructs,” in Mesenchymal Stromal Cells (MSCs): Biology, Mechanisms of Action and Clinical Uses, Nova Science Publisher, New York, 1 edition, 2016. View at Google Scholar
  27. K. C. Murphy, S. Y. Fang, and J. K. Leach, “Human mesenchymal stem cell spheroids in fibrin hydrogels exhibit improved cell survival and potential for bone healing,” Cell Tissue Research, vol. 357, no. 1, pp. 91–99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. Q. O. Tang, K. Shakib, M. Heliotis, and E. Tsiridis, “TGF-β3: a potential biological therapy for enhancing chondrogenesis,” Expert Opinion on Biological Therapy, vol. 9, no. 6, pp. 689–701, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. R. K. Elmallah, J. J. Cherian, J. J. Jauregui, T. P. Pierce, W. B. Beaver, and M. A. Mont, “Genetically modified chondrocytes expressing TGF-β1: a revolutionary treatment for articular cartilage damage?” Expert Opinion on Biological Therapy, vol. 15, no. 3, pp. 455–464, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Pfeiffer, S. M. Vickers, E. Frank, A. Grodzinsky, and M. Spector, “The effects of glycosaminoglycan content on the compressive modulus of cartilage engineered in typeII collagen scaffolds,” Osteoarthritis and Cartilage, vol. 16, no. 10, pp. 1237–1244, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Nakazora, A. Matsumine, T. Iino, M. Hasegawa, A. Kinoshita, and K. Uemura, “The cleavage of N-cadherin is essential for chondrocyte differentiation,” Biochemical and Biophysical Research Communications, vol. 400, no. 4, pp. 493–499, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Bian, M. Guvendiren, R. L. Mauck, and J. A. Burdick, “Hydrogels that mimic developmentally relevant matrix and N-cadherin interactions enhance MSC chondrogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 25, pp. 10117–10122, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. D. E. Leckband, Q. le Duc, N. Wang, and J. de Rooij, “Mechanotransduction at cadherin-mediated adhesions,” Current Opinion in Cell Biology, vol. 23, no. 5, pp. 523–530, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. C. F. Liu and V. Lefebvre, “The transcription factors SOX9 and SOX5/SOX6 cooperate genome-wide through super-enhancers to drive chondrogenesis,” Nucleic Acids Research, vol. 43, no. 17, pp. 8183–8203, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Jakab, C. Norotte, B. Damon et al., “Tissue engineering by self-assembly of cells printed into topologically defined structures,” Tissue Engineering Part A, vol. 14, no. 3, pp. 413–421, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Itoh, K. Nakayama, R. Noguchi et al., “Correction: scaffold-free tubular tissues created by a bio-3D printer undergo remodeling and endothelialization when implanted in rat aortae,” PLoS One, vol. 19, no. 12, article e0145971, 2015. View at Publisher · View at Google Scholar · View at Scopus