Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2016 (2016), Article ID 6969726, 11 pages
http://dx.doi.org/10.1155/2016/6969726
Research Article

Chondrogenic Potency Analyses of Donor-Matched Chondrocytes and Mesenchymal Stem Cells Derived from Bone Marrow, Infrapatellar Fat Pad, and Subcutaneous Fat

ISTM, Keele University, Robert Jones and Agnes Hunt Orthopaedic Hospital NHS Foundation Trust, Oswestry, Shropshire SY10 7AG, UK

Received 22 July 2016; Accepted 4 September 2016

Academic Editor: Wesley N. Sivak

Copyright © 2016 John Garcia 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. 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
  2. A. M. Bhosale, J. H. Kuiper, W. E. B. Johnson, P. E. Harrison, and J. B. Richardson, “Midterm to long-term longitudinal outcome of autologous chondrocyte implantation in the knee joint: a multilevel analysis,” The American Journal of Sports Medicine, vol. 37, supplement 1, pp. 131S–138S, 2009. View at Google Scholar · View at Scopus
  3. J. B. Richardson, B. Caterson, E. H. Evans, B. A. Ashton, and S. Roberts, “Repair of human articular cartilage after implantation of autologous chondrocytes,” Journal of Bone and Joint Surgery—Series B, vol. 81, no. 6, pp. 1064–1068, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. D. B. F. Saris, J. Vanlauwe, J. Victor et al., “Treatment of symptomatic cartilage defects of the knee: characterized chondrocyte implantation results in better clinical outcome at 36 months in a randomized trial compared to microfracture,” The American Journal of Sports Medicine, vol. 37, supplement 1, pp. 10S–19S, 2009. View at Google Scholar · View at Scopus
  5. H. S. McCarthy, J. B. Richardson, J. C. Parker, and S. Roberts, “Evaluating joint morbidity after chondral harvest for autologous chondrocyte implantation (ACI): a study of ACI-treated ankles and hips with a knee chondral harvest,” Cartilage, vol. 7, no. 1, pp. 7–15, 2016. View at Publisher · View at Google Scholar
  6. H. Holtzer, J. Abbott, J. Lash, and S. Holtzer, “The loss of phenotypic traits by differentiated cells in vitro, I. dedifferentiation of cartilage cells,” Proceedings of the National Academy of Sciences, vol. 46, no. 12, pp. 1533–1542, 1960. View at Publisher · View at Google Scholar
  7. 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
  8. S. Wakitani, T. Okabe, S. Horibe et al., “Safety of autologous bone marrow-derived mesenchymal stem cell transplantation for cartilage repair in 41 patients with 45 joints followed for up to 11 years and 5 months,” Journal of Tissue Engineering and Regenerative Medicine, vol. 5, no. 2, pp. 146–150, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. I. Akgun, M. C. Unlu, O. A. Erdal et al., “Matrix-induced autologous mesenchymal stem cell implantation versus matrix-induced autologous chondrocyte implantation in the treatment of chondral defects of the knee: a 2-year randomized study,” Archives of Orthopaedic and Trauma Surgery, vol. 135, no. 2, pp. 251–263, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Vega, M. A. Martín-Ferrero, F. D. Canto et al., “Treatment of knee osteoarthritis with allogeneic bone marrow mesenchymal stem cells: a randomized controlled trial,” Transplantation, vol. 99, no. 8, pp. 1681–1690, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. J. L. Dragoo, B. Samimi, M. Zhu et al., “Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads,” The Journal of Bone & Joint Surgery—British Volume, vol. 85, no. 5, pp. 740–747, 2003. View at Google Scholar · View at Scopus
  12. J. Garcia, K. Wright, S. Roberts et al., “Characterisation of synovial fluid and infrapatellar fat pad derived mesenchymal stromal cells: the influence of tissue source and inflammatory stimulus,” Scientific Reports, vol. 6, Article ID 24295, 2016. View at Publisher · View at Google Scholar
  13. H. Busser, M. Najar, G. Raicevic et al., “Isolation and characterization of human mesenchymal stromal cell subpopulations: comparison of bone marrow and adipose tissue,” Stem Cells and Development, vol. 24, no. 18, pp. 2142–2157, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Freitag, J. Ford, D. Bates et al., “Adipose derived mesenchymal stem cell therapy in the treatment of isolated knee chondral lesions: design of a randomised controlled pilot study comparing arthroscopic microfracture versus arthroscopic microfracture combined with postoperative mesenchymal stem cell injections,” BMJ Open, vol. 5, no. 12, Article ID e009332, 2015. View at Publisher · View at Google Scholar
  15. A. E. Aksu, J. P. Rubin, J. R. Dudas, and K. G. Marra, “Role of gender and anatomical region on induction of osteogenic differentiation of human adipose-derived stem cells,” Annals of Plastic Surgery, vol. 60, no. 3, pp. 306–322, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. K. A. Payne, D. M. Didiano, and C. R. Chu, “Donor sex and age influence the chondrogenic potential of human femoral bone marrow stem cells,” Osteoarthritis and Cartilage, vol. 18, no. 5, pp. 705–713, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. M. S. Choudhery, M. Badowski, A. Muise, J. Pierce, and D. T. Harris, “Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation,” Journal of Translational Medicine, vol. 12, no. 1, article 8, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Dell'Accio, C. De Bari, and F. P. Luyten, “Molecular markers predictive of the capacity of expanded human articular chondrocytes to form stable cartilage in vivo,” Arthritis and Rheumatism, vol. 44, no. 7, pp. 1608–1619, 2001. View at Google Scholar · View at Scopus
  19. T. D. Schmittgen and K. J. Livak, “Analyzing real-time PCR data by the comparative CT method,” Nature Protocols, vol. 3, no. 6, pp. 1101–1108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. S. P. Grogan, A. Barbero, J. Diaz-Romero et al., “Identification of markers to characterize and sort human articular chondrocytes with enhanced in vitro chondrogenic capacity,” Arthritis and Rheumatism, vol. 56, no. 2, pp. 586–595, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. C. Arufe, A. De la Fuente, I. Fuentes, F. J. de Toro, and F. J. Blanco, “Chondrogenic potential of subpopulations of cells expressing mesenchymal stem cell markers derived from human synovial membranes,” Journal of Cellular Biochemistry, vol. 111, no. 4, pp. 834–845, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Jiang, W. Liu, X. Lv et al., “Potent in vitro chondrogenesis of CD105 enriched human adipose-derived stem cells,” Biomaterials, vol. 31, no. 13, pp. 3564–3571, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Pretzel, S. Linss, S. Rochler et al., “Relative percentage and zonal distribution of mesenchymal progenitor cells in human osteoarthritic and normal cartilage,” Arthritis Research & Therapy, vol. 13, no. 2, article R64, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Niemeyer, J. M. Pestka, G. M. Salzmann, N. P. Südkamp, and H. Schmal, “Influence of cell quality on clinical outcome after autologous chondrocyte implantation,” American Journal of Sports Medicine, vol. 40, no. 3, pp. 556–561, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. C. B. Chang, S. A. Han, E. M. Kim, S. Lee, S. C. Seong, and M. C. Lee, “Chondrogenic potentials of human synovium-derived cells sorted by specific surface markers,” Osteoarthritis and Cartilage, vol. 21, no. 1, pp. 190–199, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Gullo and C. De Bari, “Prospective purification of a subpopulation of human synovial mesenchymal stem cells with enhanced chondro-osteogenic potency,” Rheumatology, vol. 52, no. 10, pp. 1758–1768, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Mifune, T. Matsumoto, S. Murasawa et al., “Therapeutic superiority for cartilage repair by CD271-positive marrow stromal cell transplantation,” Cell Transplantation, vol. 22, no. 7, pp. 1201–1211, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Johnstone, T. M. Hering, A. I. Caplan, V. M. Goldberg, and J. U. Yoo, “In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells,” Experimental Cell Research, vol. 238, no. 1, pp. 265–272, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. R. W. Farndale, C. A. Sayers, and A. J. Barrett, “A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures,” Connective Tissue Research, vol. 9, no. 4, pp. 247–248, 1982. View at Publisher · View at Google Scholar · View at Scopus
  31. R. W. Farndale, D. J. Buttle, and A. J. Barrett, “Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue,” Biochim Biophys Acta, vol. 883, no. 2, pp. 173–177, 1986. View at Publisher · View at Google Scholar · View at Scopus
  32. S. P. Grogan, A. Barbero, V. Winkelmann et al., “Visual histological grading system for the evaluation of in vitro-generated neocartilage,” Tissue Engineering, vol. 12, no. 8, pp. 2141–2149, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Bourin, B. A. Bunnell, L. Casteilla et al., “Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT),” Cytotherapy, vol. 15, no. 6, pp. 641–648, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Karlsson, C. Brantsing, T. Svensson et al., “Differentiation of human mesenchymal stem cells and articular chondrocytes: analysis of chondrogenic potential and expression pattern of differentiation-related transcription factors,” Journal of Orthopaedic Research, vol. 25, no. 2, pp. 152–163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. English, E. A. Jones, D. Corscadden et al., “A comparative assessment of cartilage and joint fat pad as a potential source of cells for autologous therapy development in knee osteoarthritis,” Rheumatology, vol. 46, no. 11, pp. 1676–1683, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Liu, C. T. Buckley, R. Downey, K. J. Mulhall, and D. J. Kelly, “The role of environmental factors in regulating the development of cartilaginous grafts engineered using osteoarthritic human infrapatellar fat pad-derived stem cells,” Tissue Engineering Part A, vol. 18, no. 15-16, pp. 1531–1541, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Vinardell, E. J. Sheehy, C. T. Buckley, and D. J. Kelly, “A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources,” Tissue Engineering—Part A, vol. 18, no. 11-12, pp. 1161–1170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Lopa, A. Colombini, D. Stanco, L. de Girolamo, V. Sansone, and M. Moretti, “Donor-matched mesenchymal stem cells from knee infrapatellar and subcutaneous adipose tissue of osteoarthritic donors display differential chondrogenic and osteogenic commitment,” European Cells and Materials, vol. 27, pp. 298–311, 2014. View at Google Scholar · View at Scopus
  39. L. Lodewyckx, F. Cailotto, S. Thysen, F. P. Luyten, and R. J. Lories, “Tight regulation of wingless-type signaling in the articular cartilage—subchondral bone biomechanical unit: transcriptomics in Frzb-knockout mice,” Arthritis Research and Therapy, vol. 14, article R16, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Stenberg, T. S. de Windt, J. Synnergren et al., “Clinical outcome 3 years after autologous chondrocyte implantation does not correlate with the expression of a predefined gene marker set in chondrocytes prior to implantation but is associated with critical signaling pathways,” Orthopaedic Journal of Sports Medicine, vol. 2, no. 9, 2014. View at Publisher · View at Google Scholar
  41. A. J. Cote, C. M. McLeod, M. J. Farrell et al., “Single-cell differences in matrix gene expression do not predict matrix deposition,” Nature Communications, vol. 7, p. 10865, 2016. View at Publisher · View at Google Scholar