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Stem Cells International
Volume 2018, Article ID 9079538, 22 pages
https://doi.org/10.1155/2018/9079538
Review Article

Stem Cells for Cartilage Repair: Preclinical Studies and Insights in Translational Animal Models and Outcome Measures

1Department of Morphology, Biomedical Research Institute, Faculty of Medicine and Life Sciences, Hasselt University, Campus Diepenbeek, 3590 Diepenbeek, Belgium
2Department of Veterinary Medicine, Integrated Veterinary Research Unit-Namur Research Institute for Life Science (IVRU-NARILIS), Faculty of Sciences, University of Namur, 5000 Namur, Belgium
3Department of Musculoskeletal Biology, Faculty of Health and Life Sciences, University of Liverpool, Leahurst Campus, Neston CH64 7TE, UK

Correspondence should be addressed to Melissa Lo Monaco; eb.tlessahu@ocanomol.assilem

Received 27 July 2017; Revised 29 November 2017; Accepted 10 December 2017; Published 5 February 2018

Academic Editor: Celeste Scotti

Copyright © 2018 Melissa Lo Monaco 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. N. Tsumaki, M. Okada, and A. Yamashita, “iPS cell technologies and cartilage regeneration,” Bone, vol. 70, pp. 48–54, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. A. J. Sophia Fox, A. Bedi, and S. A. Rodeo, “The basic science of articular cartilage: structure, composition, and function,” Sports Health: A Multidisciplinary Approach, vol. 1, no. 6, pp. 461–468, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. J. W. Alford and B. J. Cole, “Cartilage restoration, part 1: basic science, historical perspective, patient evaluation, and treatment options,” The American Journal of Sports Medicine, vol. 33, no. 2, pp. 295–306, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. M. Cottom and J. M. Maker, “Cartilage allograft techniques and materials,” Clinics in Podiatric Medicine and Surgery, vol. 32, no. 1, pp. 93–98, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Filardo, H. Madry, M. Jelic, A. Roffi, M. Cucchiarini, and E. Kon, “Mesenchymal stem cells for the treatment of cartilage lesions: from preclinical findings to clinical application in orthopaedics,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 21, no. 8, pp. 1717–1729, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. A. M. Lubis and V. K. Lubis, “Adult bone marrow stem cells in cartilage therapy,” Acta Medica Indonesiana, vol. 44, no. 1, pp. 62–68, 2012. View at Google Scholar
  7. W. S. Toh, C. B. Foldager, M. Pei, and J. H. Hui, “Advances in mesenchymal stem cell-based strategies for cartilage repair and regeneration,” Stem Cell Reviews and Reports, vol. 10, no. 5, pp. 686–696, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. R. C. Lawrence, D. T. Felson, C. G. Helmick et al., “Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II,” Arthritis & Rheumatology, vol. 58, no. 1, pp. 26–35, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. C. R. Chu, M. Szczodry, and S. Bruno, “Animal models for cartilage regeneration and repair,” Tissue Engineering Part B: Reviews, vol. 16, no. 1, pp. 105–115, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. A. M. Alshami, “Knee osteoarthritis related pain: a narrative review of diagnosis and treatment,” International Journal Health Sciences, vol. 8, no. 1, pp. 85–104, 2014. View at Publisher · View at Google Scholar
  11. E. A. Makris, A. H. Gomoll, K. N. Malizos, H. JC, and K. A. Athanasiou, “Repair and tissue engineering techniques for articular cartilage,” Nature Reviews Rheumatology, vol. 11, no. 1, pp. 21–34, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Gopal, H. A. Amirhamed, and T. Kamarul, “Advances of human bone marrow-derived mesenchymal stem cells in the treatment of cartilage defects: a systematic review,” Experimental Biology and Medicine, vol. 239, no. 6, pp. 663–669, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Withrow, C. Murphy, Y. Liu, M. Hunter, S. Fulzele, and M. W. Hamrick, “Extracellular vesicles in the pathogenesis of rheumatoid arthritis and osteoarthritis,” Arthritis Research & Therapy, vol. 18, no. 1, p. 286, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Y. Ko, K. I. Kim, S. Park, and G. I. Im, “In vitro chondrogenesis and in vivo repair of osteochondral defect with human induced pluripotent stem cells,” Biomaterials, vol. 35, no. 11, pp. 3571–3581, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Li and M. Pei, “Cell senescence: a challenge in cartilage engineering and regeneration,” Tissue Engineering Part B: Reviews, vol. 18, no. 4, pp. 270–287, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Goldberg, K. Mitchell, J. Soans, L. Kim, and R. Zaidi, “The use of mesenchymal stem cells for cartilage repair and regeneration: a systematic review,” Journal of Orthopaedic Surgery and Research, vol. 12, no. 1, p. 39, 2017. View at Publisher · View at Google Scholar · View at Scopus
  17. R. S. Tuan, A. F. Chen, and B. A. Klatt, “Cartilage regeneration,” Journal of the American Academy of Orthopaedic Surgeons, vol. 21, no. 5, pp. 303–311, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Koga, L. Engebretsen, J. E. Brinchmann, T. Muneta, and I. Sekiya, “Mesenchymal stem cell-based therapy for cartilage repair: a review,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 17, no. 11, pp. 1289–1297, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. A. M. Mackay, S. C. Beck, J. M. Murphy, F. P. Barry, C. O. Chichester, and M. F. Pittenger, “Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow,” Tissue Engineering, vol. 4, no. 4, pp. 415–428, 1998. View at Publisher · View at Google Scholar
  20. C. Qu, K. A. Puttonen, H. Lindeberg et al., “Chondrogenic differentiation of human pluripotent stem cells in chondrocyte co-culture,” The International Journal of Biochemistry & Cell Biology, vol. 45, no. 8, pp. 1802–1812, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. S. P. Medvedev, E. V. Grigor'eva, A. I. Shevchenko et al., “Human induced pluripotent stem cells derived from fetal neural stem cells successfully undergo directed differentiation into cartilage,” Stem Cells and Development, vol. 20, no. 6, pp. 1099–1112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Steck, H. Bertram, R. Abel, B. Chen, A. Winter, and W. Richter, “Induction of intervertebral disc-like cells from adult mesenchymal stem cells,” Stem Cells, vol. 23, no. 3, pp. 403–411, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Nam, Y. A. Rim, S. M. Jung, and J. H. Ju, “Cord blood cell-derived iPSCs as a new candidate for chondrogenic differentiation and cartilage regeneration,” Stem Cell Research & Therapy, vol. 8, no. 1, p. 16, 2017. View at Publisher · View at Google Scholar · View at Scopus
  24. C. M. Digirolamo, D. Stokes, D. Colter, D. G. Phinney, R. Class, and D. J. Prockop, “Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate,” British Journal Haematology, vol. 107, no. 2, pp. 275–281, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. A. J. Friedenstein, I. I. Piatetzky-Shapiro, and K. V. Petrakova, “Osteogenesis in transplants of bone marrow cells,” Journal of Embryology and Experimental Morphology, vol. 16, no. 3, pp. 181–190, 1966. View at Google Scholar
  26. 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
  27. K. Igura, X. Zhang, K. Takahashi, A. Mitsuru, S. Yamaguchi, and T. A. Takashi, “Isolation and characterization of mesenchymal progenitor cells from chorionic villi of human placenta,” Cytotherapy, vol. 6, no. 6, pp. 543–553, 2004. View at Publisher · View at Google Scholar
  28. T. Nagamura-Inoue and H. He, “Umbilical cord-derived mesenchymal stem cells: their advantages and potential clinical utility,” World Journal of Stem Cells, vol. 6, no. 2, pp. 195–202, 2014. View at Publisher · View at Google Scholar
  29. S. Gronthos, M. Mankani, J. Brahim, P. G. Robey, and S. Shi, “Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 25, pp. 13625–13630, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Hilkens, P. Gervois, Y. Fanton et al., “Effect of isolation methodology on stem cell properties and multilineage differentiation potential of human dental pulp stem cells,” Cell and Tissue Research, vol. 353, no. 1, pp. 65–78, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. I. Kassis, L. Zangi, R. Rivkin et al., “Isolation of mesenchymal stem cells from G-CSF-mobilized human peripheral blood using fibrin microbeads,” Bone Marrow Transplantation, vol. 37, no. 10, pp. 967–976, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. C. De Bari, F. Dell'Accio, P. Tylzanowski, and F. P. Luyten, “Multipotent mesenchymal stem cells from adult human synovial membrane,” Arthritis & Rheumatology, vol. 44, no. 8, pp. 1928–1942, 2001. View at Publisher · View at Google Scholar
  33. 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
  34. S. Aggarwal and M. F. Pittenger, “Human mesenchymal stem cells modulate allogeneic immune cell responses,” Blood, vol. 105, no. 4, pp. 1815–1822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. 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
  36. J. U. Yoo, T. S. Barthel, K. Nishimura et al., “The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells,” The Journal of Bone & Joint Surgery, vol. 80, no. 12, pp. 1745–1757, 1998. View at Publisher · View at Google Scholar
  37. E. J. Kubosch, E. Heidt, A. Bernstein, K. Böttiger, and H. Schmal, “The trans-well coculture of human synovial mesenchymal stem cells with chondrocytes leads to self-organization, chondrogenic differentiation, and secretion of TGFβ,” Stem Cell Research & Therapy, vol. 7, no. 1, p. 64, 2016. View at Publisher · View at Google Scholar · View at Scopus
  38. X. Li, L. Duan, Y. Liang, W. Zhu, J. Xiong, and D. Wang, “Human umbilical cord blood-derived mesenchymal stem cells contribute to chondrogenesis in coculture with chondrocytes,” BioMed Research International, vol. 2016, Article ID 3827057, 2 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Acharya, A. Adesida, P. Zajac et al., “Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation,” Journal of Cellular Physiology, vol. 227, no. 1, pp. 88–97, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Fukumoto, J. W. Sperling, A. Sanyal et al., “Combined effects of insulin-like growth factor-1 and transforming growth factor-β1 on periosteal mesenchymal cells during chondrogenesis in vitro,” Osteoarthritis and Cartilage, vol. 11, no. 1, pp. 55–64, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. L. A. Solchaga, K. Penick, J. D. Porter, V. M. Goldberg, A. I. Caplan, and J. F. Welter, “FGF-2 enhances the mitotic and chondrogenic potentials of human adult bone marrow-derived mesenchymal stem cells,” Journal of Cellular Physiology, vol. 203, no. 2, pp. 398–409, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. H. J. Kim, Y. J. Kim, and G. I. Im, “Is continuous treatment with transforming growth factor-beta necessary to induce chondrogenic differentiation in mesenchymal stem cells?” Cells, Tissues, Organs, vol. 190, no. 1, pp. 1–10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. I. Sekiya, B. L. Larson, J. T. Vuoristo, R. L. Reger, and D. J. Prockop, “Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma,” Cell and Tissue Research, vol. 320, no. 2, pp. 269–276, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Xu, Z. Gechtman, A. Hughes et al., “Potential involvement of BMP receptor type IB activation in a synergistic effect of chondrogenic promotion between rhTGFβ3 and rhGDF5 or rhBMP7 in human mesenchymal stem cells,” Growth Factors, vol. 24, no. 4, pp. 268–278, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Gomez-Leduc, M. Hervieu, F. Legendre et al., “Chondrogenic commitment of human umbilical cord blood-derived mesenchymal stem cells in collagen matrices for cartilage engineering,” Scientific Reports, vol. 6, no. 1, article 32786, 2016. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Arslan, M. O. Guler, and A. B. Tekinay, “Glycosaminoglycan-mimetic signals direct the osteo/chondrogenic differentiation of mesenchymal stem cells in a three-dimensional peptide nanofiber extracellular matrix mimetic environment,” Biomacromolecules, vol. 17, no. 4, pp. 1280–1291, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Y. Fong, A. Subramanian, K. Gauthaman et al., “Human umbilical cord Wharton’s jelly stem cells undergo enhanced chondrogenic differentiation when grown on nanofibrous scaffolds and in a sequential two-stage culture medium environment,” Stem Cell Reviews and Reports, vol. 8, no. 1, pp. 195–209, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. W. J. Li, R. Tuli, C. Okafor et al., “A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells,” Biomaterials, vol. 26, no. 6, pp. 599–609, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Bosnakovski, M. Mizuno, G. Kim, S. Takagi, M. Okumura, and T. Fujinaga, “Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: influence of collagen type II extracellular matrix on MSC chondrogenesis,” Biotechnology and Bioengineering, vol. 93, no. 6, pp. 1152–1163, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Yao, J. Xue, Q. Wang et al., “Glucosamine-modified polyethylene glycol hydrogel-mediated chondrogenic differentiation of human mesenchymal stem cells,” Materials Science and Engineering: C, vol. 79, pp. 661–670, 2017. View at Publisher · View at Google Scholar · View at Scopus
  51. W. Wang, B. Li, Y. Li, Y. Jiang, H. Ouyang, and C. Gao, “In vivo restoration of full-thickness cartilage defects by poly(lactide-co-glycolide) sponges filled with fibrin gel, bone marrow mesenchymal stem cells and DNA complexes,” Biomaterials, vol. 31, no. 23, pp. 5953–5965, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Liu, Y. Jia, M. Yuan et al., “Repair of osteochondral defects using human umbilical cord Wharton’s jelly-derived mesenchymal stem cells in a rabbit model,” BioMed Research International, vol. 2017, Article ID 8760383, 12 pages, 2017. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Leijten, N. Georgi, L. Moreira Teixeira, C. A. van Blitterswijk, J. N. Post, and M. Karperien, “Metabolic programming of mesenchymal stromal cells by oxygen tension directs chondrogenic cell fate,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 38, pp. 13954–13959, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. M. E. Bernardo, J. A. Emons, M. Karperien et al., “Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources,” Connective Tissue Research, vol. 48, no. 3, pp. 132–140, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. G. I. Im, Y. W. Shin, and K. B. Lee, “Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells?” Osteoarthritis and Cartilage, vol. 13, no. 10, pp. 845–853, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. Ľ. Danišovič, M. Boháč, R. Zamborský et al., “Comparative analysis of mesenchymal stromal cells from different tissue sources in respect to articular cartilage tissue engineering,” General Physiology and Biophysics, vol. 35, no. 02, pp. 207–214, 2016. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Hennig, H. Lorenz, A. Thiel et al., “Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFβ receptor and BMP profile and is overcome by BMP-6,” Journal of Cellular Physiology, vol. 211, no. 3, pp. 682–691, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. H. J. Kim and G. I. Im, “Chondrogenic differentiation of adipose tissue-derived mesenchymal stem cells: greater doses of growth factor are necessary,” Journal of Orthopaedic Research, vol. 27, no. 5, pp. 612–619, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. K. Pelttari, A. Winter, E. Steck et al., “Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice,” Arthritis & Rheumatology, vol. 54, no. 10, pp. 3254–3266, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. J. M. Murphy, K. Dixon, S. Beck, D. Fabian, A. Feldman, and F. Barry, “Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis,” Arthritis & Rheumatology, vol. 46, no. 3, pp. 704–713, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. J. D. Kretlow, Y. Q. Jin, W. Liu et al., “Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells,” BMC Cell Biology, vol. 9, no. 1, p. 60, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. A. C. Bakker, F. A. van de Loo, H. M. van Beuningen et al., “Overexpression of active TGF-beta-1 in the murine knee joint: evidence for synovial-layer-dependent chondro-osteophyte formation,” Osteoarthritis and Cartilage, vol. 9, no. 2, pp. 128–136, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Scharstuhl, E. L. Vitters, P. M. van der Kraan, and W. B. van den Berg, “Reduction of osteophyte formation and synovial thickening by adenoviral overexpression of transforming growth factor β/bone morphogenetic protein inhibitors during experimental osteoarthritis,” Arthritis & Rheumatology, vol. 48, no. 12, pp. 3442–3451, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Li, T. Liu, N. Van Halm-Lutterodt, J. Chen, Q. Su, and Y. Hai, “Reprogramming of blood cells into induced pluripotent stem cells as a new cell source for cartilage repair,” Stem Cell Research & Therapy, vol. 7, no. 1, p. 31, 2016. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Wei, W. Zeng, R. Wan et al., “Chondrogenic differentiation of induced pluripotent stem cells from osteoarthritic chondrocytes in alginate matrix,” European Cells and Materials, vol. 23, pp. 1–12, 2012. View at Publisher · View at Google Scholar
  66. R. M. Guzzo, V. Scanlon, A. Sanjay, X. RH, and H. Drissi, “Establishment of human cell type-specific iPS cells with enhanced chondrogenic potential,” Stem Cell Reviews and Reports, vol. 10, no. 6, pp. 820–829, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. K. Kim, R. Zhao, A. Doi et al., “Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells,” Nature Biotechnology, vol. 29, no. 12, pp. 1117–1119, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. R. M. Guzzo, J. Gibson, X. RH, F. Y. Lee, and H. Drissi, “Efficient differentiation of human iPSC-derived mesenchymal stem cells to chondroprogenitor cells,” Journal of Cellular Biochemistry, vol. 114, no. 2, pp. 480–490, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Nejadnik, S. Diecke, O. D. Lenkov et al., “Improved approach for chondrogenic differentiation of human induced pluripotent stem cells,” Stem Cell Reviews and Reports, vol. 11, no. 2, pp. 242–253, 2015. View at Publisher · View at Google Scholar · View at Scopus
  70. N. Koyama, M. Miura, K. Nakao et al., “Human induced pluripotent stem cells differentiated into chondrogenic lineage via generation of mesenchymal progenitor cells,” Stem Cells and Development, vol. 22, no. 1, pp. 102–113, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Liu, H. Nie, Z. Xu et al., “The effect of 3D nanofibrous scaffolds on the chondrogenesis of induced pluripotent stem cells and their application in restoration of cartilage defects,” PLoS One, vol. 9, no. 11, article e111566, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Kang, Y. Zhou, S. Tan et al., “Mesenchymal stem cells derived from human induced pluripotent stem cells retain adequate osteogenicity and chondrogenicity but less adipogenicity,” Stem Cell Research & Therapy, vol. 6, no. 1, p. 144, 2015. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Zhao, Z. N. Zhang, Z. Rong, and Y. Xu, “Immunogenicity of induced pluripotent stem cells,” Nature, vol. 474, no. 7350, pp. 212–215, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Saito, F. Yano, D. Mori et al., “Hyaline cartilage formation and tumorigenesis of implanted tissues derived from human induced pluripotent stem cells,” Biomedical Research, vol. 36, no. 3, pp. 179–186, 2015. View at Publisher · View at Google Scholar
  75. A. S. Lee, C. Tang, M. S. Rao, I. L. Weissman, and J. C. Wu, “Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies,” Nature Medicine, vol. 19, no. 8, pp. 998–1004, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. K. Okita, T. Ichisaka, and S. Yamanaka, “Generation of germline-competent induced pluripotent stem cells,” Nature, vol. 448, no. 7151, pp. 313–317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Nakagawa, M. Koyanagi, K. Tanabe et al., “Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts,” Nature Biotechnology, vol. 26, no. 1, pp. 101–106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Fusaki, H. Ban, A. Nishiyama, K. Saeki, and M. Hasegawa, “Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome,” Proceedings of the Japan Academy, Series B, vol. 85, no. 8, pp. 348–362, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. G. Itakura, S. Kawabata, M. Ando et al., “Fail-safe system against potential tumorigenicity after transplantation of iPSC derivatives,” Stem Cell Reports, vol. 8, no. 3, pp. 673–684, 2017. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Wu, Y. Wu, X. Zhang, and M. R. Capecchi, “Efficient germ-line transmission obtained with transgene-free induced pluripotent stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 29, pp. 10678–10683, 2014. View at Publisher · View at Google Scholar · View at Scopus
  81. M. Schuldiner, J. Itskovitz-Eldor, and N. Benvenisty, “Selective ablation of human embryonic stem cells expressing a “suicide” gene,” Stem Cells, vol. 21, no. 3, pp. 257–265, 2003. View at Publisher · View at Google Scholar
  82. C. Leten, V. D. Roobrouck, T. Struys et al., “Controlling and monitoring stem cell safety in vivo in an experimental rodent model,” Stem Cells, vol. 32, no. 11, pp. 2833–2844, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. B. Sadlik, G. Jaroslawski, D. Gladysz et al., “Knee cartilage regeneration with umbilical cord mesenchymal stem cells embedded in collagen scaffold using dry arthroscopy technique,” Advances in Experimental Medicine and Biology, vol. 1020, pp. 113–122, 2017. View at Publisher · View at Google Scholar
  84. J. Mak, C. L. Jablonski, C. A. Leonard et al., “Intra-articular injection of synovial mesenchymal stem cells improves cartilage repair in a mouse injury model,” Scientific Reports, vol. 6, no. 1, article 23076, 2016. View at Publisher · View at Google Scholar · View at Scopus
  85. 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
  86. F. P. Barry and J. M. Murphy, “Mesenchymal stem cells: clinical applications and biological characterization,” The International Journal of Biochemistry & Cell Biology, vol. 36, no. 4, pp. 568–584, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. F. Barry, R. E. Boynton, B. Liu, and J. M. Murphy, “Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components,” Experimental Cell Research, vol. 268, no. 2, pp. 189–200, 2001. View at Publisher · View at Google Scholar · View at Scopus
  88. Y. Zhu, X. Wu, Y. Liang et al., “Repair of cartilage defects in osteoarthritis rats with induced pluripotent stem cell derived chondrocytes,” BMC Biotechnology, vol. 16, no. 1, p. 78, 2016. View at Publisher · View at Google Scholar · View at Scopus
  89. J. M. Murphy, D. J. Fink, E. B. Hunziker, and F. P. Barry, “Stem cell therapy in a caprine model of osteoarthritis,” Arthritis & Rheumatology, vol. 48, no. 12, pp. 3464–3474, 2003. View at Publisher · View at Google Scholar · View at Scopus
  90. S. M. Richardson, G. Kalamegam, P. N. Pushparaj et al., “Mesenchymal stem cells in regenerative medicine: focus on articular cartilage and intervertebral disc regeneration,” Methods, vol. 99, pp. 69–80, 2016. View at Publisher · View at Google Scholar · View at Scopus
  91. J. L. Spees, R. H. Lee, and C. A. Gregory, “Mechanisms of mesenchymal stem/stromal cell function,” Stem Cell Research & Therapy, vol. 7, no. 1, p. 125, 2016. View at Publisher · View at Google Scholar · View at Scopus
  92. B. E. Bobick, F. H. Chen, A. M. Le, and R. S. Tuan, “Regulation of the chondrogenic phenotype in culture,” Birth Defects Research Part C, Embryo Today: Reviews, vol. 87, no. 4, pp. 351–371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. K. Kuroda, T. Kabata, K. Hayashi et al., “The paracrine effect of adipose-derived stem cells inhibits osteoarthritis progression,” BMC Musculoskeletal Disorders, vol. 16, no. 1, p. 236, 2015. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Zhang, W. C. Chu, R. C. Lai, S. K. Lim, J. H. Hui, and W. S. Toh, “Exosomes derived from human embryonic mesenchymal stem cells promote osteochondral regeneration,” Osteoarthritis and Cartilage, vol. 24, no. 12, pp. 2135–2140, 2016. View at Publisher · View at Google Scholar · View at Scopus
  95. S. C. Tao, T. Yuan, Y. L. Zhang, W. J. Yin, S. C. Guo, and C. Q. Zhang, “Exosomes derived from miR-140-5p-overexpressing human synovial mesenchymal stem cells enhance cartilage tissue regeneration and prevent osteoarthritis of the knee in a rat model,” Theranostics, vol. 7, no. 1, pp. 180–195, 2017. View at Publisher · View at Google Scholar · View at Scopus
  96. U. T. Arasu, R. Karna, K. Harkonen et al., “Human mesenchymal stem cells secrete hyaluronan-coated extracellular vesicles,” Matrix Biology, vol. 64, pp. 54–68, 2017. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Uccelli, L. Moretta, and V. Pistoia, “Mesenchymal stem cells in health and disease,” Nature Reviews Immunology, vol. 8, no. 9, pp. 726–736, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. G. Chamberlain, J. Fox, B. Ashton, and J. Middleton, “Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing,” Stem Cells, vol. 25, no. 11, pp. 2739–2749, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. M. Pers, M. Ruiz, D. Noel, and C. Jorgensen, “Mesenchymal stem cells for the management of inflammation in osteoarthritis: state of the art and perspectives,” Osteoarthritis and Cartilage, vol. 23, no. 11, pp. 2027–2035, 2015. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Glennie, I. Soeiro, P. J. Dyson, E. W. Lam, and F. Dazzi, “Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells,” Blood, vol. 105, no. 7, pp. 2821–2827, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. A. Del Fattore, R. Luciano, L. Pascucci et al., “Immunoregulatory effects of mesenchymal stem cell-derived extracellular vesicles on T lymphocytes,” Cell Transplantation, vol. 24, no. 12, pp. 2615–2627, 2015. View at Publisher · View at Google Scholar · View at Scopus
  102. K. Akiyama, C. Chen, D. Wang et al., “Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis,” Cell Stem Cell, vol. 10, no. 5, pp. 544–555, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Meisel, A. Zibert, M. Laryea, U. Gobel, W. Daubener, and D. Dilloo, “Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation,” Blood, vol. 103, no. 12, pp. 4619–4621, 2004. View at Publisher · View at Google Scholar · View at Scopus
  104. W. Ge, J. Jiang, J. Arp, W. Liu, B. Garcia, and H. Wang, “Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression,” Transplantation, vol. 90, no. 12, pp. 1312–1320, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. G. M. Spaggiari, A. Capobianco, H. Abdelrazik, F. Becchetti, M. C. Mingari, and L. Moretta, “Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2,” Blood, vol. 111, no. 3, pp. 1327–1333, 2008. View at Publisher · View at Google Scholar · View at Scopus
  106. L. Pierdomenico, L. Bonsi, M. Calvitti et al., “Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp,” Transplantation, vol. 80, no. 6, pp. 836–842, 2005. View at Publisher · View at Google Scholar · View at Scopus
  107. P. C. Demircan, A. E. Sariboyaci, Z. S. Unal, G. Gacar, C. Subasi, and E. Karaoz, “Immunoregulatory effects of human dental pulp-derived stem cells on T cells: comparison of transwell co-culture and mixed lymphocyte reaction systems,” Cytotherapy, vol. 13, no. 10, pp. 1205–1220, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. R. Ramasamy, H. Fazekasova, E. W. Lam, I. Soeiro, G. Lombardi, and F. Dazzi, “Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle,” Transplantation, vol. 83, no. 1, pp. 71–76, 2007. View at Publisher · View at Google Scholar · View at Scopus
  109. A. J. Nauta, A. B. Kruisselbrink, E. Lurvink, R. Willemze, and W. E. Fibbe, “Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells,” The Journal of Immunology, vol. 177, no. 4, pp. 2080–2087, 2006. View at Publisher · View at Google Scholar
  110. S. Jose, S. W. Tan, Y. Y. Ooi, R. Ramasamy, and S. Vidyadaran, “Mesenchymal stem cells exert anti-proliferative effect on lipopolysaccharide-stimulated BV2 microglia by reducing tumour necrosis factor-α levels,” Journal of Neuroinflammation, vol. 11, no. 1, p. 149, 2014. View at Publisher · View at Google Scholar · View at Scopus
  111. Z. Rahmat, S. Jose, R. Ramasamy, and S. Vidyadaran, “Reciprocal interactions of mouse bone marrow-derived mesenchymal stem cells and BV2 microglia after lipopolysaccharide stimulation,” Stem Cell Research & Therapy, vol. 4, no. 1, p. 12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  112. B. Zhang, R. Liu, D. Shi et al., “Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2-dependent regulatory dendritic cell population,” Blood, vol. 113, no. 1, pp. 46–57, 2009. View at Publisher · View at Google Scholar · View at Scopus
  113. Q. Z. Zhang, W. R. Su, S. H. Shi et al., “Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing,” Stem Cells, vol. 28, no. 10, pp. 1856–1868, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. A. B. Vasandan, S. Jahnavi, C. Shashank, P. Prasad, A. Kumar, and S. J. Prasanna, “Human mesenchymal stem cells program macrophage plasticity by altering their metabolic status via a PGE2-dependent mechanism,” Scientific Reports, vol. 6, no. 1, article 38308, 2016. View at Publisher · View at Google Scholar · View at Scopus
  115. C. Lo Sicco, D. Reverberi, C. Balbi et al., “Mesenchymal stem cell-derived extracellular vesicles as mediators of anti-inflammatory effects: endorsement of macrophage polarization,” Stem Cells Translational Medicine, vol. 6, no. 3, pp. 1018–1028, 2017. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Corcione, F. Benvenuto, E. Ferretti et al., “Human mesenchymal stem cells modulate B-cell functions,” Blood, vol. 107, no. 1, pp. 367–372, 2006. View at Publisher · View at Google Scholar · View at Scopus
  117. M. Franquesa, M. J. Hoogduijn, O. Bestard, and J. M. Grinyo, “Immunomodulatory effect of mesenchymal stem cells on B cells,” Frontiers in Immunology, vol. 3, p. 212, 2012. View at Publisher · View at Google Scholar · View at Scopus
  118. L. V. Schnabel, C. M. Abratte, J. C. Schimenti et al., “Induced pluripotent stem cells have similar immunogenic and more potent immunomodulatory properties compared with bone marrow-derived stromal cells in vitro,” Regenerative Medicine, vol. 9, no. 5, pp. 621–635, 2014. View at Publisher · View at Google Scholar · View at Scopus
  119. B. L. Yen, C. J. Chang, K. J. Liu et al., “Brief report—human embryonic stem cell-derived mesenchymal progenitors possess strong immunosuppressive effects toward natural killer cells as well as T lymphocytes,” Stem Cells, vol. 27, no. 2, pp. 451–456, 2009. View at Publisher · View at Google Scholar · View at Scopus
  120. Z. Tan, Z. Y. Su, R. R. Wu et al., “Immunomodulative effects of mesenchymal stem cells derived from human embryonic stem cells in vivo and in vitro,” Journal of Zhejiang University Science B, vol. 12, no. 1, pp. 18–27, 2011. View at Publisher · View at Google Scholar · View at Scopus
  121. Q. L. Fu, Y. Y. Chow, S. J. Sun et al., “Mesenchymal stem cells derived from human induced pluripotent stem cells modulate T-cell phenotypes in allergic rhinitis,” Allergy, vol. 67, no. 10, pp. 1215–1222, 2012. View at Publisher · View at Google Scholar
  122. H. K. Tam, A. Srivastava, C. W. Colwell, and D. D. D'Lima, “In vitro model of full-thickness cartilage defect healing,” Journal of Orthopaedic Research, vol. 25, no. 9, pp. 1136–1144, 2007. View at Publisher · View at Google Scholar · View at Scopus
  123. K. W. Ng, F. Wanivenhaus, T. Chen et al., “A novel macroporous polyvinyl alcohol scaffold promotes chondrocyte migration and interface formation in an in vitro cartilage defect model,” Tissue Engineering Part A, vol. 18, no. 11-12, pp. 1273–1281, 2012. View at Publisher · View at Google Scholar · View at Scopus
  124. C. J. Moran, A. Ramesh, P. A. Brama, J. M. O'Byrne, F. J. O'Brien, and T. J. Levingstone, “The benefits and limitations of animal models for translational research in cartilage repair,” Journal of Experimental Orthopaedics, vol. 3, no. 1, p. 1, 2016. View at Publisher · View at Google Scholar
  125. J. L. Cook, C. T. Hung, K. Kuroki et al., “Animal models of cartilage repair,” Bone & Joint Research, vol. 3, no. 4, pp. 89–94, 2014. View at Publisher · View at Google Scholar · View at Scopus
  126. J. D. Gibson, M. B. O'Sullivan, F. Alaee et al., “Regeneration of articular cartilage by human ESC-derived mesenchymal progenitors treated sequentially with BMP-2 and Wnt5a,” Stem Cells Translational Medicine, vol. 6, no. 1, pp. 40–50, 2017. View at Publisher · View at Google Scholar · View at Scopus
  127. Y. Oshima, N. Watanabe, K. Matsuda, S. Takai, M. Kawata, and T. Kubo, “Behavior of transplanted bone marrow-derived GFP mesenchymal cells in osteochondral defect as a simulation of autologous transplantation,” Journal of Histochemistry & Cytochemistry, vol. 53, no. 2, pp. 207–216, 2005. View at Publisher · View at Google Scholar · View at Scopus
  128. M. Ferretti, K. G. Marra, K. Kobayashi, A. J. Defail, and C. R. Chu, “Controlled in vivo degradation of genipin crosslinked polyethylene glycol hydrogels within osteochondral defects,” Tissue Engineering, vol. 12, no. 9, pp. 2657–2663, 2006. View at Publisher · View at Google Scholar · View at Scopus
  129. P. E. Lammi, M. J. Lammi, R. H. Tammi, H. J. Helminen, and M. M. Espanha, “Strong hyaluronan expression in the full-thickness rat articular cartilage repair tissue,” Histochemistry and Cell Biology, vol. 115, no. 4, pp. 301–308, 2001. View at Publisher · View at Google Scholar
  130. M. Karakaplan, N. Elmalı, E. Mirel, N. Şahin, E. Ergen, and C. Elmalı, “Effect of microfracture and autologous-conditioned plasma application in the focal full-thickness chondral defect of the knee: an experimental study on rabbits,” Journal of Orthopaedic Surgery and Research, vol. 10, no. 1, p. 110, 2015. View at Publisher · View at Google Scholar · View at Scopus
  131. R. Vayas, R. Reyes, M. Rodríguez-Évora, C. Del Rosario, A. Delgado, and C. Évora, “Evaluation of the effectiveness of a bMSC and BMP-2 polymeric trilayer system in cartilage repair,” Biomedical Materials, vol. 12, no. 4, article 045001, 2017. View at Publisher · View at Google Scholar
  132. X. Xu, D. Shi, Y. Liu et al., “In vivo repair of full-thickness cartilage defect with human iPSC-derived mesenchymal progenitor cells in a rabbit model,” Experimental and Therapeutic Medicine, vol. 14, no. 1, pp. 239–245, 2017. View at Publisher · View at Google Scholar
  133. D. D. Frisbie, M. W. Cross, and C. W. McIlwraith, “A comparative study of articular cartilage thickness in the stifle of animal species used in human pre-clinical studies compared to articular cartilage thickness in the human knee,” Veterinary and Comparative Orthopaedics and Traumatology, vol. 19, no. 3, pp. 142–146, 2006. View at Google Scholar
  134. J. Malda, J. C. de Grauw, K. E. Benders et al., “Of mice, men and elephants: the relation between articular cartilage thickness and body mass,” PLoS One, vol. 8, no. 2, article e57683, 2013. View at Publisher · View at Google Scholar · View at Scopus
  135. D. L. Gushue, J. Houck, and A. L. Lerner, “Rabbit knee joint biomechanics: motion analysis and modeling of forces during hopping,” Journal of Orthopaedic Research, vol. 23, no. 4, pp. 735–742, 2005. View at Publisher · View at Google Scholar · View at Scopus
  136. A. Chevrier, A. S. Kouao, G. Picard, M. B. Hurtig, and M. D. Buschmann, “Interspecies comparison of subchondral bone properties important for cartilage repair,” Journal of Orthopaedic Research, vol. 33, no. 1, pp. 63–70, 2015. View at Publisher · View at Google Scholar · View at Scopus
  137. X. Wei, J. Gao, and K. Messner, “Maturation-dependent repair of untreated osteochondral defects in the rabbit knee joint,” Journal of Biomedical Materials Research, vol. 34, no. 1, pp. 63–72, 1997. View at Publisher · View at Google Scholar
  138. T. Möller, M. Amoroso, D. Hägg et al., “In vivo chondrogenesis in 3D bioprinted human cell-laden hydrogel constructs,” Plastic and Reconstructive Surgery - Global Open, vol. 5, no. 2, article e1227, 2017. View at Publisher · View at Google Scholar
  139. A. Haisch, A. Gröger, C. Radke et al., “Macroencapsulation of human cartilage implants: pilot study with polyelectrolyte complex membrane encapsulation,” Biomaterials, vol. 21, no. 15, pp. 1561–1566, 2000. View at Publisher · View at Google Scholar · View at Scopus
  140. T. Matsumoto, S. Kubo, L. B. Meszaros et al., “The influence of sex on the chondrogenic potential of muscle-derived stem cells: implications for cartilage regeneration and repair,” Arthritis & Rheumatology, vol. 58, no. 12, pp. 3809–3819, 2008. View at Publisher · View at Google Scholar · View at Scopus
  141. C. W. McIlwraith, D. D. Frisbie, W. G. Rodkey et al., “Evaluation of intra-articular mesenchymal stem cells to augment healing of microfractured chondral defects,” Arthroscopy, vol. 27, no. 11, pp. 1552–1561, 2011. View at Publisher · View at Google Scholar · View at Scopus
  142. M. M. Wilke, D. V. Nydam, and A. J. Nixon, “Enhanced early chondrogenesis in articular defects following arthroscopic mesenchymal stem cell implantation in an equine model,” Journal Orthopaedic Research, vol. 25, no. 7, pp. 913–925, 2007. View at Publisher · View at Google Scholar · View at Scopus
  143. D. D. Frisbie, H. E. McCarthy, C. W. Archer, M. F. Barrett, and C. W. McIlwraith, “Evaluation of articular cartilage progenitor cells for the repair of articular defects in an equine model,” The Journal of Bone and Joint Surgery, vol. 97, no. 6, pp. 484–493, 2015. View at Publisher · View at Google Scholar · View at Scopus
  144. D. Kazemi, K. Shams Asenjan, N. Dehdilani, and H. Parsa, “Canine articular cartilage regeneration using mesenchymal stem cells seeded on platelet rich fibrin: macroscopic and histological assessments,” Bone & Joint Research, vol. 6, no. 2, pp. 98–107, 2017. View at Publisher · View at Google Scholar · View at Scopus
  145. C. D. Hoemann, M. Hurtig, E. Rossomacha et al., “Chitosan-glycerol phosphate/blood implants improve hyaline cartilage repair in ovine microfracture defects,” The Journal of Bone and Joint Surgery. American Volume, vol. 87, no. 12, pp. 2671–2686, 2005. View at Publisher · View at Google Scholar · View at Scopus
  146. N. Hopper, J. Wardale, R. Brooks, J. Power, N. Rushton, and F. Henson, “Peripheral blood mononuclear cells enhance cartilage repair in in vivo osteochondral defect model,” PLoS One, vol. 10, no. 8, article e0133937, 2015. View at Publisher · View at Google Scholar · View at Scopus
  147. P. Orth, H. L. Meyer, L. Goebel et al., “Improved repair of chondral and osteochondral defects in the ovine trochlea compared with the medial condyle,” Journal of Orthopaedic Research, vol. 31, no. 11, pp. 1772–1779, 2013. View at Publisher · View at Google Scholar · View at Scopus
  148. A. R. Zorzi, E. M. Amstalden, A. M. Plepis et al., “Effect of human adipose tissue mesenchymal stem cells on the regeneration of ovine articular cartilage,” International Journal of Molecular Sciences, vol. 16, no. 11, pp. 26813–26831, 2015. View at Publisher · View at Google Scholar · View at Scopus
  149. A. F. Manunta, P. Zedde, S. Pilicchi et al., “The use of embryonic cells in the treatment of osteochondral defects of the knee: an ovine in vivo study,” Joints, vol. 04, no. 02, pp. 070–079, 2016. View at Publisher · View at Google Scholar · View at Scopus
  150. H. Y. Nam, P. Karunanithi, W. C. Loo et al., “The effects of staged intra-articular injection of cultured autologous mesenchymal stromal cells on the repair of damaged cartilage: a pilot study in caprine model,” Arthritis Research & Therapy, vol. 15, no. 5, article R129, 2013. View at Publisher · View at Google Scholar · View at Scopus
  151. T. J. Levingstone, A. Ramesh, R. T. Brady et al., “Cell-free multi-layered collagen-based scaffolds demonstrate layer specific regeneration of functional osteochondral tissue in caprine joints,” Biomaterials, vol. 87, pp. 69–81, 2016. View at Publisher · View at Google Scholar · View at Scopus
  152. B. B. Christensen, C. B. Foldager, M. L. Olesen et al., “Experimental articular cartilage repair in the Göttingen minipig: the influence of multiple defects per knee,” Journal of Experimental Orthopaedics, vol. 2, no. 1, p. 13, 2015. View at Publisher · View at Google Scholar
  153. T. Gotterbarm, S. J. Breusch, U. Schneider, and M. Jung, “The minipig model for experimental chondral and osteochondral defect repair in tissue engineering: retrospective analysis of 180 defects,” Laboratory Animals, vol. 42, no. 1, pp. 71–82, 2008. View at Publisher · View at Google Scholar · View at Scopus
  154. M. B. Fisher, N. S. Belkin, A. H. Milby et al., “Effects of mesenchymal stem cell and growth factor delivery on cartilage repair in a mini-pig model,” Cartilage, vol. 7, no. 2, pp. 174–184, 2016. View at Publisher · View at Google Scholar · View at Scopus
  155. C. W. Ha, Y. B. Park, J. Y. Chung, and Y. G. Park, “Cartilage repair using composites of human umbilical cord blood-derived mesenchymal stem cells and hyaluronic acid hydrogel in a minipig model,” Stem Cells Translational Medicine, vol. 4, no. 9, pp. 1044–1051, 2015. View at Publisher · View at Google Scholar · View at Scopus
  156. B. L. Proffen, M. McElfresh, B. C. Fleming, and M. M. Murray, “A comparative anatomical study of the human knee and six animal species,” The Knee, vol. 19, no. 4, pp. 493–499, 2012. View at Publisher · View at Google Scholar · View at Scopus
  157. J. M. Vandeweerd, N. Kirschvink, B. Muylkens et al., “A study of the anatomy and injection techniques of the ovine stifle by positive contrast arthrography, computed tomography arthrography and gross anatomical dissection,” The Veterinary Journal, vol. 193, no. 2, pp. 426–432, 2012. View at Publisher · View at Google Scholar · View at Scopus
  158. G. Osterhoff, S. Löffler, H. Steinke, C. Feja, C. Josten, and P. Hepp, “Comparative anatomical measurements of osseous structures in the ovine and human knee,” The Knee, vol. 18, no. 2, pp. 98–103, 2011. View at Publisher · View at Google Scholar · View at Scopus
  159. B. J. Ahern, J. Parvizi, R. Boston, and T. P. Schaer, “Preclinical animal models in single site cartilage defect testing: a systematic review,” Osteoarthritis and Cartilage, vol. 17, no. 6, pp. 705–713, 2009. View at Publisher · View at Google Scholar · View at Scopus
  160. H. Madry, M. Ochi, M. Cucchiarini, D. Pape, and R. Seil, “Large animal models in experimental knee sports surgery: focus on clinical translation,” Journal of Experimental Orthopaedics, vol. 2, no. 1, p. 9, 2015. View at Publisher · View at Google Scholar
  161. C. W. McIlwraith, L. A. Fortier, D. D. Frisbie, and A. J. Nixon, “Equine models of articular cartilage repair,” Cartilage, vol. 2, no. 4, pp. 317–326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  162. S. Patil, N. Steklov, L. Song, W. C. Bae, and D. D. D'Lima, “Comparative biomechanical analysis of human and caprine knee articular cartilage,” The Knee, vol. 21, no. 1, pp. 119–125, 2014. View at Publisher · View at Google Scholar · View at Scopus
  163. J. Malda, K. E. Benders, T. J. Klein et al., “Comparative study of depth-dependent characteristics of equine and human osteochondral tissue from the medial and lateral femoral condyles,” Osteoarthritis and Cartilage, vol. 20, no. 10, pp. 1147–1151, 2012. View at Publisher · View at Google Scholar · View at Scopus
  164. B. von Rechenberg, M. K. Akens, D. Nadler et al., “Changes in subchondral bone in cartilage resurfacing—an experimental study in sheep using different types of osteochondral grafts,” Osteoarthritis and Cartilage, vol. 11, no. 4, pp. 265–277, 2003. View at Publisher · View at Google Scholar · View at Scopus
  165. D. W. Jackson, P. A. Lalor, H. M. Aberman, and T. M. Simon, “Spontaneous repair of full-thickness defects of articular cartilage in a goat model. A preliminary study,” The Journal of Bone and Joint Surgery American Volume, vol. 83-A, no. 1, pp. 53–64, 2001. View at Google Scholar
  166. M. B. Hurtig, M. D. Buschmann, L. A. Fortier et al., “Preclinical studies for cartilage repair: recommendations from the international cartilage repair society,” Cartilage, vol. 2, no. 2, pp. 137–152, 2011. View at Publisher · View at Google Scholar · View at Scopus
  167. J. M. Vandeweerd, F. Hontoir, N. Kirschvink et al., “Prevalence of naturally occurring cartilage defects in the ovine knee,” Osteoarthritis and Cartilage, vol. 21, no. 8, pp. 1125–1131, 2013. View at Publisher · View at Google Scholar · View at Scopus
  168. H. Katagiri, L. F. Mendes, and F. P. Luyten, “Definition of a critical size osteochondral knee defect and its negative effect on the surrounding articular cartilage in the rat,” Osteoarthritis and Cartilage, vol. 25, no. 9, pp. 1531–1540, 2017. View at Publisher · View at Google Scholar · View at Scopus
  169. X. Wei and K. Messner, “Maturation-dependent durability of spontaneous cartilage repair in rabbit knee joint,” Journal of Biomedical Materials Research, vol. 46, no. 4, pp. 539–548, 1999. View at Publisher · View at Google Scholar
  170. A. I. Vasara, M. M. Hyttinen, O. Pulliainen et al., “Immature porcine knee cartilage lesions show good healing with or without autologous chondrocyte transplantation,” Osteoarthritis and Cartilage, vol. 14, no. 10, pp. 1066–1074, 2006. View at Publisher · View at Google Scholar · View at Scopus
  171. B. D. Boyan, L. L. Tosi, R. D. Coutts et al., “Addressing the gaps: sex differences in osteoarthritis of the knee,” Biology of Sex Differences, vol. 4, no. 1, p. 4, 2013. View at Publisher · View at Google Scholar · View at Scopus
  172. A. S. Turner, K. A. Athanasiou, C. F. Zhu, M. R. Alvis, and H. U. Bryant, “Biochemical effects of estrogen on articular cartilage in ovariectomized sheep,” Osteoarthritis and Cartilage, vol. 5, no. 1, pp. 63–69, 1997. View at Publisher · View at Google Scholar · View at Scopus
  173. H. Huang, J. D. Skelly, D. C. Ayers, and J. Song, “Age-dependent changes in the articular cartilage and subchondral bone of C57BL/6 mice after surgical destabilization of medial meniscus,” Scientific Reports, vol. 7, no. 1, article 42294, p. 17603, 2017. View at Publisher · View at Google Scholar
  174. H. L. Ma, T. J. Blanchet, D. Peluso, B. Hopkins, E. A. Morris, and S. S. Glasson, “Osteoarthritis severity is sex dependent in a surgical mouse model,” Osteoarthritis and Cartilage, vol. 15, no. 6, pp. 695–700, 2007. View at Publisher · View at Google Scholar · View at Scopus
  175. S. C. Faber, F. Eckstein, S. Lukasz et al., “Gender differences in knee joint cartilage thickness, volume and articular surface areas: assessment with quantitative three-dimensional MR imaging,” Skeletal Radiology, vol. 30, no. 3, pp. 144–150, 2001. View at Publisher · View at Google Scholar · View at Scopus
  176. D. Kumar, R. B. Souza, K. Subburaj et al., “Are there sex differences in knee cartilage composition and walking mechanics in healthy and osteoarthritis populations?” Clinical Orthopaedics and Related Research, vol. 473, no. 8, pp. 2548–2558, 2015. View at Publisher · View at Google Scholar · View at Scopus
  177. P. C. Kreuz, S. Muller, C. Erggelet et al., “Is gender influencing the biomechanical results after autologous chondrocyte implantation?” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 22, no. 1, pp. 72–79, 2014. View at Publisher · View at Google Scholar · View at Scopus
  178. J. E. Trachtenberg, T. N. Vo, and A. G. Mikos, “Pre-clinical characterization of tissue engineering constructs for bone and cartilage regeneration,” Annals of Biomedical Engineering, vol. 43, no. 3, pp. 681–696, 2015. View at Publisher · View at Google Scholar · View at Scopus
  179. F. Hontoir, P. Clegg, J. F. Nisolle, S. Tew, and J. M. Vandeweerd, “Magnetic resonance compositional imaging of articular cartilage: what can we expect in veterinary medicine?” The Veterinary Journal, vol. 205, no. 1, pp. 11–20, 2015. View at Publisher · View at Google Scholar · View at Scopus
  180. J. F. Nisolle, B. Bihin, N. Kirschvink et al., “Prevalence of age-related changes in ovine lumbar intervertebral discs during computed tomography and magnetic resonance imaging,” Comperative Medicine, vol. 66, no. 4, pp. 300–307, 2016. View at Google Scholar
  181. P. Orth, D. Zurakowski, M. Alini, M. Cucchiarini, and H. Madry, “Reduction of sample size requirements by bilateral versus unilateral research designs in animal models for cartilage tissue engineering,” Tissue Engineering Part C: Methods, vol. 19, no. 11, pp. 885–891, 2013. View at Publisher · View at Google Scholar · View at Scopus
  182. M. Masri, G. Lombardero, C. Velasquillo et al., “Matrix-encapsulation cell-seeding technique to prevent cell detachment during arthroscopic implantation of matrix-induced autologous chondrocytes,” Arthroscopy, vol. 23, no. 8, pp. 877–883, 2007. View at Publisher · View at Google Scholar · View at Scopus
  183. R. H. Neundorf, M. B. Lowerison, A. M. Cruz, J. J. Thomason, B. J. McEwen, and M. B. Hurtig, “Determination of the prevalence and severity of metacarpophalangeal joint osteoarthritis in thoroughbred racehorses via quantitative macroscopic evaluation,” American Journal of Veterinary Research, vol. 71, no. 11, pp. 1284–1293, 2010. View at Publisher · View at Google Scholar · View at Scopus
  184. L. E. Craig and A. Reed, “Age-associated cartilage degeneration of the canine humeral head,” Veterinary Pathology, vol. 50, no. 2, pp. 264–268, 2013. View at Publisher · View at Google Scholar · View at Scopus
  185. F. Hontoir, P. Clegg, V. Simon, N. Kirschvink, J. F. Nisolle, and J. M. Vandeweerd, “Accuracy of computed tomographic arthrography for assessment of articular cartilage defects in the ovine stifle,” Veterinary Radiology & Ultrasound, vol. 58, no. 5, pp. 512–523, 2017. View at Publisher · View at Google Scholar · View at Scopus
  186. C. A. McGibbon and C. A. Trahan, “Measurement accuracy of focal cartilage defects from MRI and correlation of MRI graded lesions with histology: a preliminary study,” Osteoarthritis and Cartilage, vol. 11, no. 7, pp. 483–493, 2003. View at Publisher · View at Google Scholar · View at Scopus
  187. T. M. Link, J. Neumann, and X. Li, “Prestructural cartilage assessment using MRI,” Journal of Magnetic Resonance Imaging, vol. 45, no. 4, pp. 949–965, 2017. View at Publisher · View at Google Scholar · View at Scopus
  188. P. M. Jungmann, T. Baum, J. S. Bauer et al., “Cartilage repair surgery: outcome evaluation by using noninvasive cartilage biomarkers based on quantitative MRI techniques?” BioMed Research International, vol. 2014, Article ID 840170, 17 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  189. F. Hontoir, J. F. Nisolle, H. Meurisse et al., “A comparison of 3-T magnetic resonance imaging and computed tomography arthrography to identify structural cartilage defects of the fetlock joint in the horse,” The Veterinary Journal, vol. 199, no. 1, pp. 115–122, 2014. View at Publisher · View at Google Scholar · View at Scopus
  190. E. H. Oei, J. van Tiel, W. H. Robinson, and G. E. Gold, “Quantitative radiologic imaging techniques for articular cartilage composition: toward early diagnosis and development of disease-modifying therapeutics for osteoarthritis,” Arthritis Care & Research, vol. 66, no. 8, pp. 1129–1141, 2014. View at Publisher · View at Google Scholar · View at Scopus
  191. M. Shahabpour, M. Kichouh, E. Laridon, J. L. Gielen, and J. De Mey, “The effectiveness of diagnostic imaging methods for the assessment of soft tissue and articular disorders of the shoulder and elbow,” European Journal of Radiology, vol. 65, no. 2, pp. 194–200, 2008. View at Publisher · View at Google Scholar · View at Scopus
  192. J. E. Kurkijarvi, L. Mattila, R. O. Ojala et al., “Evaluation of cartilage repair in the distal femur after autologous chondrocyte transplantation using T2 relaxation time and dGEMRIC,” Osteoarthritis and Cartilage, vol. 15, no. 4, pp. 372–378, 2007. View at Publisher · View at Google Scholar · View at Scopus
  193. S. J. Matzat, F. Kogan, G. W. Fong, and G. E. Gold, “Imaging strategies for assessing cartilage composition in osteoarthritis,” Current Rheumatology Reports, vol. 16, no. 11, p. 462, 2014. View at Publisher · View at Google Scholar · View at Scopus
  194. J. Endo, A. Watanabe, T. Sasho et al., “Utility of T2 mapping and dGEMRIC for evaluation of cartilage repair after allograft chondrocyte implantation in a rabbit model,” Osteoarthritis and Cartilage, vol. 23, no. 2, pp. 280–288, 2015. View at Publisher · View at Google Scholar · View at Scopus
  195. A. Watanabe, C. Boesch, S. E. Anderson, W. Brehm, and P. Mainil Varlet, “Ability of dGEMRIC and T2 mapping to evaluate cartilage repair after microfracture: a goat study,” Osteoarthritis and Cartilage, vol. 17, no. 10, pp. 1341–1349, 2009. View at Publisher · View at Google Scholar · View at Scopus
  196. J. van Tiel, G. Kotek, M. Reijman et al., “Is T1ρ mapping an alternative to delayed gadolinium-enhanced MR imaging of cartilage in the assessment of sulphated glycosaminoglycan content in human osteoarthritic knees? An in vivo validation study,” Radiology, vol. 279, no. 2, pp. 523–531, 2016. View at Publisher · View at Google Scholar · View at Scopus
  197. J. Chen, F. Wang, Y. Zhang et al., “In vivo tracking of superparamagnetic iron oxide nanoparticle labeled chondrocytes in large animal model,” Annals of Biomedical Engineering, vol. 40, no. 12, pp. 2568–2578, 2012. View at Publisher · View at Google Scholar · View at Scopus
  198. S. Ramaswamy, J. B. Greco, M. C. Uluer, Z. Zhang, K. W. Fishbein, and R. G. Spencer, “Magnetic resonance imaging of chondrocytes labeled with superparamagnetic iron oxide nanoparticles in tissue-engineered cartilage,” Tissue Engineering Part A, vol. 15, no. 12, pp. 3899–3910, 2009. View at Publisher · View at Google Scholar · View at Scopus
  199. J. W. Bulte, “In vivo MRI cell tracking: clinical studies,” American Journal of Roentgenology, vol. 193, no. 2, pp. 314–325, 2009. View at Publisher · View at Google Scholar · View at Scopus
  200. H. J. Je, M. G. Kim, and H. J. Kwon, “Bioluminescence assays for monitoring chondrogenic differentiation and cartilage regeneration,” Sensors, vol. 17, no. 6, 2017. View at Publisher · View at Google Scholar
  201. M. Vilalta, C. Jorgensen, I. R. Dégano et al., “Dual luciferase labelling for non-invasive bioluminescence imaging of mesenchymal stromal cell chondrogenic differentiation in demineralized bone matrix scaffolds,” Biomaterials, vol. 30, no. 28, pp. 4986–4995, 2009. View at Publisher · View at Google Scholar · View at Scopus
  202. M. H. Vandsburger, M. Radoul, B. Cohen, and M. Neeman, “MRI reporter genes: applications for imaging of cell survival, proliferation, migration and differentiation,” NMR in Biomedicine, vol. 26, no. 7, pp. 872–884, 2013. View at Publisher · View at Google Scholar · View at Scopus
  203. J. Kaler, G. J. Wassink, and L. E. Green, “The inter- and intra-observer reliability of a locomotion scoring scale for sheep,” The Veterinary Journal, vol. 180, no. 2, pp. 189–194, 2009. View at Publisher · View at Google Scholar · View at Scopus
  204. H. L. Shafford, P. W. Hellyer, and A. S. Turner, “Intra-articular lidocaine plus bupivacaine in sheep undergoing stifle arthrotomy,” Veterinary Anaesthesia and Analgesia, vol. 31, no. 1, pp. 20–26, 2004. View at Publisher · View at Google Scholar · View at Scopus
  205. R. Poole, S. Blake, M. Buschmann et al., “Recommendations for the use of preclinical models in the study and treatment of osteoarthritis,” Osteoarthritis and Cartilage, vol. 18, Supplement 3, pp. S10–S16, 2010. View at Publisher · View at Google Scholar · View at Scopus
  206. E. Teeple, G. D. Jay, K. A. Elsaid, and B. C. Fleming, “Animal models of osteoarthritis: challenges of model selection and analysis,” The AAPS Journal, vol. 15, no. 2, pp. 438–446, 2013. View at Publisher · View at Google Scholar · View at Scopus
  207. U. Maninchedda, O. M. Lepage, M. Gangl et al., “Development of an equine groove model to induce metacarpophalangeal osteoarthritis: a pilot study on 6 horses,” PLoS One, vol. 10, no. 2, article e0115089, 2015. View at Publisher · View at Google Scholar · View at Scopus
  208. V. G. Cuellar, J. M. Cuellar, T. Kirsch, and E. J. Strauss, “Correlation of synovial fluid biomarkers with cartilage pathology and associated outcomes in knee arthroscopy,” Arthroscopy, vol. 32, no. 3, pp. 475–485, 2016. View at Publisher · View at Google Scholar · View at Scopus
  209. L. T. Nguyen, A. R. Sharma, C. Chakraborty, B. Saibaba, M. E. Ahn, and S. S. Lee, “Review of prospects of biological fluid biomarkers in osteoarthritis,” International Journal of Molecular Sciences, vol. 18, no. 3, 2017. View at Publisher · View at Google Scholar · View at Scopus
  210. C. L. Blaker, E. C. Clarke, and C. B. Little, “Using mouse models to investigate the pathophysiology, treatment, and prevention of post-traumatic osteoarthritis,” Journal of Orthopaedic Research, vol. 35, no. 3, pp. 424–439, 2017. View at Publisher · View at Google Scholar · View at Scopus
  211. D. R. Seifer, B. D. Furman, F. Guilak, S. A. Olson, S. C. Brooks 3rd, and V. B. Kraus, “Novel synovial fluid recovery method allows for quantification of a marker of arthritis in mice,” Osteoarthritis and Cartilage, vol. 16, no. 12, pp. 1532–1538, 2008. View at Publisher · View at Google Scholar · View at Scopus
  212. L. Goebel, D. Zurakowski, A. Müller, D. Pape, M. Cucchiarini, and H. Madry, “2D and 3D MOCART scoring systems assessed by 9.4 T high-field MRI correlate with elementary and complex histological scoring systems in a translational model of osteochondral repair,” Osteoarthritis and Cartilage, vol. 22, no. 10, pp. 1386–1395, 2014. View at Publisher · View at Google Scholar · View at Scopus
  213. L. Goebel, A. Müller, A. Bücker, and H. Madry, “High resolution MRI imaging at 9.4 tesla of the osteochondral unit in a translational model of articular cartilage repair,” BMC Musculoskeletal Disorders, vol. 16, no. 1, p. 91, 2015. View at Publisher · View at Google Scholar · View at Scopus
  214. P. Orth, C. Peifer, L. Goebel, M. Cucchiarini, and H. Madry, “Comprehensive analysis of translational osteochondral repair: focus on the histological assessment,” Progress in Histochemistry and Cytochemistry, vol. 50, no. 3, pp. 19–36, 2015. View at Publisher · View at Google Scholar · View at Scopus
  215. C. B. Little, M. M. Smith, M. A. Cake, R. A. Read, M. J. Murphy, and F. P. Barry, “The OARSI histopathology initiative - recommendations for histological assessments of osteoarthritis in sheep and goats,” Osteoarthritis and Cartilage, vol. 18, Supplement 3, pp. S80–S92, 2010. View at Publisher · View at Google Scholar · View at Scopus
  216. A. Changoor, N. Tran-Khanh, S. Méthot et al., “A polarized light microscopy method for accurate and reliable grading of collagen organization in cartilage repair,” Osteoarthritis and Cartilage, vol. 19, no. 1, pp. 126–135, 2011. View at Publisher · View at Google Scholar · View at Scopus
  217. C. Hoemann, R. Kandel, S. Roberts et al., “International cartilage repair society (ICRS) recommended guidelines for histological endpoints for cartilage repair studies in animal models and clinical trials,” Cartilage, vol. 2, no. 2, pp. 153–172, 2011. View at Publisher · View at Google Scholar · View at Scopus
  218. M. P. van den Borne, N. J. Raijmakers, J. Vanlauwe et al., “International cartilage repair society (ICRS) and Oswestry macroscopic cartilage evaluation scores validated for use in autologous chondrocyte implantation (ACI) and microfracture,” Osteoarthritis and Cartilage, vol. 15, no. 12, pp. 1397–1402, 2007. View at Publisher · View at Google Scholar · View at Scopus
  219. M. Rutgers, M. J. van Pelt, W. J. Dhert, L. B. Creemers, and D. B. Saris, “Evaluation of histological scoring systems for tissue-engineered, repaired and osteoarthritic cartilage,” Osteoarthritis and Cartilage, vol. 18, no. 1, pp. 12–23, 2010. View at Publisher · View at Google Scholar · View at Scopus
  220. P. Orth, D. Zurakowski, D. Wincheringer, and H. Madry, “Reliability, reproducibility, and validation of five major histological scoring systems for experimental articular cartilage repair in the rabbit model,” Tissue Engineering Part C: Methods, vol. 18, no. 5, pp. 329–339, 2012. View at Publisher · View at Google Scholar · View at Scopus
  221. P. Kiviranta, E. Lammentausta, J. Töyräs, I. Kiviranta, and J. S. Jurvelin, “Indentation diagnostics of cartilage degeneration,” Osteoarthritis and Cartilage, vol. 16, no. 7, pp. 796–804, 2008. View at Publisher · View at Google Scholar · View at Scopus
  222. C. D. Hoemann, J. Sun, V. Chrzanowski, and M. D. Buschmann, “A multivalent assay to detect glycosaminoglycan, protein, collagen, RNA, and DNA content in milligram samples of cartilage or hydrogel-based repair cartilage,” Analytical Biochemistry, vol. 300, no. 1, pp. 1–10, 2002. View at Publisher · View at Google Scholar · View at Scopus
  223. G. P. Dowthwaite, J. C. Bishop, S. N. Redman et al., “The surface of articular cartilage contains a progenitor cell population,” Journal of Cell Science, vol. 117, pp. 889–897, 2004. View at Publisher · View at Google Scholar · View at Scopus
  224. R. Williams, I. M. Khan, K. Richardson et al., “Identification and clonal characterisation of a progenitor cell sub-population in normal human articular cartilage,” PLoS One, vol. 5, no. 10, article e13246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  225. Y. Yu, H. Zheng, J. A. Buckwalter, and J. A. Martin, “Single cell sorting identifies progenitor cell population from full thickness bovine articular cartilage,” Osteoarthritis and Cartilage, vol. 22, no. 9, pp. 1318–1326, 2014. View at Publisher · View at Google Scholar · View at Scopus
  226. M. Imaizumi, Y. Nomoto, Y. Sato et al., “Evaluation of the use of induced pluripotent stem cells (iPSCs) for the regeneration of tracheal cartilage,” Cell Transplantation, vol. 22, no. 2, pp. 341–353, 2013. View at Publisher · View at Google Scholar · View at Scopus
  227. T. D. Bornes, A. B. Adesida, and N. M. Jomha, “Mesenchymal stem cells in the treatment of traumatic articular cartilage defects: a comprehensive review,” Arthritis Research & Therapy, vol. 16, no. 5, p. 432, 2014. View at Publisher · View at Google Scholar · View at Scopus
  228. Z. Z. Zhang, S. J. Wang, J. Y. Zhang et al., “3D-printed poly(ε-caprolactone) scaffold augmented with mesenchymal stem cells for total meniscal substitution: a 12- and 24-week animal study in a rabbit model,” The American Journal of Sports Medicine, vol. 45, no. 7, pp. 1497–1511, 2017. View at Publisher · View at Google Scholar · View at Scopus
  229. B. Sridharan, A. D. Laflin, M. A. Holtz, D. M. Pacicca, N. K. Wischmeier, and M. S. Detamore, “In vivo evaluation of stem cell aggregates on osteochondral regeneration,” Journal of Orthopaedic Research, vol. 35, no. 8, pp. 1606–1616, 2016. View at Publisher · View at Google Scholar · View at Scopus
  230. M. Itokazu, S. Wakitani, H. Mera et al., “Transplantation of scaffold-free cartilage-like cell-sheets made from human bone marrow mesenchymal stem cells for cartilage repair: a preclinical study,” Cartilage, vol. 7, no. 4, pp. 361–372, 2016. View at Publisher · View at Google Scholar · View at Scopus
  231. O. H. Jeon and J. Elisseeff, “Orthopedic tissue regeneration: cells, scaffolds, and small molecules,” Drug Delivery and Translational Research, vol. 6, no. 2, pp. 105–120, 2016. View at Publisher · View at Google Scholar · View at Scopus
  232. P. Vanhelleputte, K. Nijs, M. Delforge, G. Evers, and S. Vanderschueren, “Pain during bone marrow aspiration: prevalence and prevention,” Journal of Pain and Symptom Management, vol. 26, no. 3, pp. 860–866, 2003. View at Publisher · View at Google Scholar · View at Scopus
  233. 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
  234. D. Mehrabani, M. Babazadeh, N. Tanideh et al., “The healing effect of adipose-derived mesenchymal stem cells in full-thickness femoral articular cartilage defects of rabbit,” International Journal of Organ Transplantation Medicine, vol. 6, no. 4, pp. 165–175, 2015. View at Google Scholar
  235. 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 Surgery and Research, vol. 10, no. 1, p. 35, 2015. View at Publisher · View at Google Scholar · View at Scopus
  236. S. Portron, C. Merceron, O. Gauthier et al., “Effects of in vitro low oxygen tension preconditioning of adipose stromal cells on their in vivo chondrogenic potential: application in cartilage tissue repair,” PLoS One, vol. 8, no. 4, article e62368, 2013. View at Publisher · View at Google Scholar · View at Scopus
  237. P. Van Pham, K. H. Bui, D. Q. Ngo et al., “Activated platelet-rich plasma improves adipose-derived stem cell transplantation efficiency in injured articular cartilage,” Stem Cell Research & Therapy, vol. 4, no. 4, p. 91, 2013. View at Publisher · View at Google Scholar · View at Scopus
  238. H. Koga, T. Muneta, T. Nagase et al., “Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit,” Cell and Tissue Research, vol. 333, no. 2, pp. 207–215, 2008. View at Publisher · View at Google Scholar · View at Scopus
  239. X. Xie, Y. Wang, C. Zhao et al., “Comparative evaluation of MSCs from bone marrow and adipose tissue seeded in PRP-derived scaffold for cartilage regeneration,” Biomaterials, vol. 33, no. 29, pp. 7008–7018, 2012. View at Publisher · View at Google Scholar · View at Scopus
  240. Q. Li, J. Tang, R. Wang et al., “Comparing the chondrogenic potential in vivo of autogeneic mesenchymal stem cells derived from different tissues,” Artificial Cells, Blood Substitutes, and Immobilization Biotechnology, vol. 39, no. 1, pp. 31–38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  241. J. C. Lee, H. J. Min, H. J. Park, S. Lee, S. C. Seong, and M. C. Lee, “Synovial membrane-derived mesenchymal stem cells supported by platelet-rich plasma can repair osteochondral defects in a rabbit model,” Arthroscopy, vol. 29, no. 6, pp. 1034–1046, 2013. View at Publisher · View at Google Scholar · View at Scopus
  242. J. C. Lee, S. Y. Lee, H. J. Min et al., “Synovium-derived mesenchymal stem cells encapsulated in a novel injectable gel can repair osteochondral defects in a rabbit model,” Tissue Engineering Part A, vol. 18, no. 19-20, pp. 2173–2186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  243. T. Nakamura, I. Sekiya, T. Muneta et al., “Arthroscopic, histological and MRI analyses of cartilage repair after a minimally invasive method of transplantation of allogeneic synovial mesenchymal stromal cells into cartilage defects in pigs,” Cytotherapy, vol. 14, no. 3, pp. 327–338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  244. S. Meirelles Lda, A. M. Fontes, D. T. Covas, and A. I. Caplan, “Mechanisms involved in the therapeutic properties of mesenchymal stem cells,” Cytokine & Growth Factor Reviews, vol. 20, no. 5-6, pp. 419–427, 2009. View at Publisher · View at Google Scholar · View at Scopus
  245. Y. Zhang, S. Liu, W. Guo et al., “Co-culture systems-based strategies for articular cartilage tissue engineering,” Journal of Cellular Physiology, vol. 233, no. 3, pp. 1940–1951, 2018. View at Publisher · View at Google Scholar
  246. M. A. Sabatino, R. Santoro, S. Gueven et al., “Cartilage graft engineering by co-culturing primary human articular chondrocytes with human bone marrow stromal cells,” Journal of Tissue Engineering and Regenerative Medicine, vol. 9, no. 12, pp. 1394–1403, 2015. View at Publisher · View at Google Scholar · View at Scopus
  247. Z. Cai, B. Pan, H. Jiang, and L. Zhang, “Chondrogenesis of human adipose-derived stem cells by in vivo co-graft with auricular chondrocytes from microtia,” Aesthetic Plastic Surgery, vol. 39, no. 3, pp. 431–439, 2015. View at Publisher · View at Google Scholar · View at Scopus
  248. L. Moradi, M. Vasei, M. M. Dehghan, M. Majidi, S. Farzad Mohajeri, and S. Bonakdar, “Regeneration of meniscus tissue using adipose mesenchymal stem cells-chondrocytes co-culture on a hybrid scaffold: in vivo study,” Biomaterials, vol. 126, pp. 18–30, 2017. View at Publisher · View at Google Scholar · View at Scopus
  249. K. B. Lee, J. H. Hui, I. C. Song, L. Ardany, and E. H. Lee, “Injectable mesenchymal stem cell therapy for large cartilage defects—a porcine model,” Stem Cells, vol. 25, no. 11, pp. 2964–2971, 2007. View at Publisher · View at Google Scholar · View at Scopus
  250. H. Koga, M. Shimaya, T. Muneta et al., “Local adherent technique for transplanting mesenchymal stem cells as a potential treatment of cartilage defect,” Arthritis Research & Therapy, vol. 10, no. 4, p. R84, 2008. View at Publisher · View at Google Scholar · View at Scopus
  251. Y. Yasui, W. Ando, K. Shimomura et al., “Scaffold-free, stem cell-based cartilage repair,” Journal of Clinical Orthopaedics and Trauma, vol. 7, no. 3, pp. 157–163, 2016. View at Publisher · View at Google Scholar · View at Scopus
  252. J. Xue, A. He, Y. Zhu et al., “Repair of articular cartilage defects with acellular cartilage sheets in a swine model,” Biomedical Materials, 2017. View at Publisher · View at Google Scholar
  253. Z. J. Wang, R. Z. An, J. Y. Zhao et al., “Repair of articular cartilage defects by tissue-engineered cartilage constructed with adipose-derived stem cells and acellular cartilaginous matrix in rabbits,” Genetics and Molecular Research, vol. 13, no. 2, pp. 4599–4606, 2014. View at Publisher · View at Google Scholar · View at Scopus
  254. I. L. Kim, R. L. Mauck, and J. A. Burdick, “Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid,” Biomaterials, vol. 32, no. 34, pp. 8771–8782, 2011. View at Publisher · View at Google Scholar · View at Scopus
  255. S. Kazemnejad, M. Khanmohammadi, N. Baheiraei, and S. Arasteh, “Current state of cartilage tissue engineering using nanofibrous scaffolds and stem cells,” Avicenna Journal of Medical Biotechnology, vol. 9, no. 2, pp. 50–65, 2017. View at Google Scholar
  256. D. Nguyen, D. A. Hagg, A. Forsman et al., “Cartilage tissue engineering by the 3D bioprinting of iPS cells in a nanocellulose/alginate bioink,” Scientific Reports, vol. 7, no. 1, p. 658, 2017. View at Publisher · View at Google Scholar · View at Scopus
  257. C. McKee, Y. Hong, D. Yao, and G. R. Chaudhry, “Compression induced chondrogenic differentiation of embryonic stem cells in three-dimensional polydimethylsiloxane scaffolds,” Tissue Engineering Part A, vol. 23, no. 9-10, pp. 426–435, 2017. View at Publisher · View at Google Scholar · View at Scopus
  258. 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
  259. M. Liu, X. Zeng, C. Ma et al., “Injectable hydrogels for cartilage and bone tissue engineering,” Bone Research, vol. 5, article 17014, 2017. View at Publisher · View at Google Scholar · View at Scopus
  260. M. Mata, L. Milian, M. Oliver et al., “In vivo articular cartilage regeneration using human dental pulp stem cells cultured in an alginate scaffold: a preliminary study,” Stem Cells International, vol. 2017, Article ID 8309256, 9 pages, 2017. View at Publisher · View at Google Scholar
  261. C. Chung and J. A. Burdick, “Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis,” Tissue Engineering Part A, vol. 15, no. 2, pp. 243–254, 2009. View at Publisher · View at Google Scholar · View at Scopus
  262. J. Y. Chung, M. Song, C. W. Ha, J. A. Kim, C. H. Lee, and Y. B. Park, “Comparison of articular cartilage repair with different hydrogel-human umbilical cord blood-derived mesenchymal stem cell composites in a rat model,” Stem Cell Research & Therapy, vol. 5, no. 2, p. 39, 2014. View at Publisher · View at Google Scholar · View at Scopus
  263. D. Eyrich, F. Brandl, B. Appel et al., “Long-term stable fibrin gels for cartilage engineering,” Biomaterials, vol. 28, no. 1, pp. 55–65, 2007. View at Publisher · View at Google Scholar · View at Scopus
  264. W. Swieszkowski, B. H. Tuan, K. J. Kurzydlowski, and D. W. Hutmacher, “Repair and regeneration of osteochondral defects in the articular joints,” Biomolecular Engineering, vol. 24, no. 5, pp. 489–495, 2007. View at Publisher · View at Google Scholar · View at Scopus
  265. C. H. Chang, T. F. Kuo, F. H. Lin et al., “Tissue engineering-based cartilage repair with mesenchymal stem cells in a porcine model,” Journal of Orthopaedic Research, vol. 29, no. 12, pp. 1874–1880, 2011. View at Publisher · View at Google Scholar · View at Scopus
  266. M. Lazarini, P. Bordeaux-Rego, R. Giardini-Rosa et al., “Natural type II collagen hydrogel, fibrin sealant, and adipose-derived stem cells as a promising combination for articular cartilage repair,” Cartilage, vol. 8, no. 4, pp. 439–443, 2017. View at Publisher · View at Google Scholar
  267. P. Gentile, V. Chiono, I. Carmagnola, and P. V. Hatton, “An overview of poly(lactic-co-glycolic) acid (PLGA)-based biomaterials for bone tissue engineering,” International Journal of Molecular Sciences, vol. 15, no. 3, pp. 3640–3659, 2014. View at Publisher · View at Google Scholar · View at Scopus
  268. F. Yin, J. Cai, W. Zen et al., “Cartilage regeneration of adipose-derived stem cells in the TGF-β1-immobilized PLGA-gelatin scaffold,” Stem Cell Reviews and Reports, vol. 11, no. 3, pp. 453–459, 2015. View at Publisher · View at Google Scholar · View at Scopus
  269. S. Zhu, B. Zhang, C. Man, Y. Ma, X. Liu, and J. Hu, “Combined effects of connective tissue growth factor-modified bone marrow-derived mesenchymal stem cells and NaOH-treated PLGA scaffolds on the repair of articular cartilage defect in rabbits,” Cell Transplantation, vol. 23, no. 6, pp. 715–727, 2014. View at Publisher · View at Google Scholar · View at Scopus
  270. M. Caminal, X. Moll, D. Codina et al., “Transitory improvement of articular cartilage characteristics after implantation of polylactide:polyglycolic acid (PLGA) scaffolds seeded with autologous mesenchymal stromal cells in a sheep model of critical-sized chondral defect,” Biotechnology Letters, vol. 36, no. 10, pp. 2143–2153, 2014. View at Publisher · View at Google Scholar · View at Scopus
  271. M. Li, X. Luo, X. Lv et al., “In vivo human adipose-derived mesenchymal stem cell tracking after intra-articular delivery in a rat osteoarthritis model,” Stem Cell Research & Therapy, vol. 7, no. 1, p. 160, 2016. View at Publisher · View at Google Scholar · View at Scopus
  272. L. S. Tseng, S. H. Chen, M. T. Lin, and Y. C. Lin, “Transplantation of human dental pulp-derived stem cells protects against heatstroke in mice,” Cell Transplantation, vol. 24, no. 5, pp. 921–937, 2015. View at Publisher · View at Google Scholar · View at Scopus
  273. I. Kerkis, C. E. Ambrosio, A. Kerkis et al., “Early transplantation of human immature dental pulp stem cells from baby teeth to golden retriever muscular dystrophy (GRMD) dogs: local or systemic?” Journal of Translational Medicine, vol. 6, no. 1, p. 35, 2008. View at Publisher · View at Google Scholar · View at Scopus
  274. F. Wei, T. Song, G. Ding et al., “Functional tooth restoration by allogeneic mesenchymal stem cell-based bio-root regeneration in swine,” Stem Cells and Development, vol. 22, no. 12, pp. 1752–1762, 2013. View at Publisher · View at Google Scholar · View at Scopus
  275. V. Dayan, V. Sotelo, V. Delfina et al., “Human mesenchymal stromal cells improve cardiac perfusion in an ovine immunocompetent animal model,” Journal of Investigative Surgery, vol. 29, no. 4, pp. 218–225, 2016. View at Publisher · View at Google Scholar · View at Scopus
  276. J. Harding, R. M. Roberts, and O. Mirochnitchenko, “Large animal models for stem cell therapy,” Stem Cell Research & Therapy, vol. 4, no. 2, p. 23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  277. J. Ogorevc, S. Orehek, and P. Dovc, “Cellular reprogramming in farm animals: an overview of iPSC generation in the mammalian farm animal species,” Journal of Animal Science and Biotechnology, vol. 7, no. 1, p. 10, 2016. View at Publisher · View at Google Scholar · View at Scopus
  278. C. Madeira, A. Santhagunam, J. B. Salgueiro, and J. M. Cabral, “Advanced cell therapies for articular cartilage regeneration,” Trends in Biotechnology, vol. 33, no. 1, pp. 35–42, 2015. View at Publisher · View at Google Scholar · View at Scopus
  279. O. S. Beane, V. C. Fonseca, L. L. Cooper, G. Koren, and E. M. Darling, “Impact of aging on the regenerative properties of bone marrow-, muscle-, and adipose-derived mesenchymal stem/stromal cells,” PLoS One, vol. 9, no. 12, article e115963, 2014. View at Publisher · View at Google Scholar · View at Scopus
  280. Y. J. Kim, H. J. Kim, and G. I. Im, “PTHrP promotes chondrogenesis and suppresses hypertrophy from both bone marrow-derived and adipose tissue-derived MSCs,” Biochemical and Biophysical Research Communications, vol. 373, no. 1, pp. 104–108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  281. C. J. Moran, C. Pascual-Garrido, S. Chubinskaya et al., “Restoration of articular cartilage,” The Journal of Bone & Joint Surgery, vol. 96, no. 4, pp. 336–344, 2014. View at Publisher · View at Google Scholar · View at Scopus