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Stem Cell Reviews and Reports

, Volume 13, Issue 5, pp 575–586 | Cite as

Mesenchymal Stem/Progenitor Cells Derived from Articular Cartilage, Synovial Membrane and Synovial Fluid for Cartilage Regeneration: Current Status and Future Perspectives

Article

Abstract

Large articular cartilage defects remain an immense challenge in the field of regenerative medicine because of their poor intrinsic repair capacity. Currently, the available medical interventions can relieve clinical symptoms to some extent, but fail to repair the cartilaginous injuries with authentic hyaline cartilage. There has been a surge of interest in developing cell-based therapies, focused particularly on the use of mesenchymal stem/progenitor cells with or without scaffolds. Mesenchymal stem/progenitor cells are promising graft cells for tissue regeneration, but the most suitable source of cells for cartilage repair remains controversial. The tissue origin of mesenchymal stem/progenitor cells notably influences the biological properties and therapeutic potential. It is well known that mesenchymal stem/progenitor cells derived from synovial joint tissues exhibit superior chondrogenic ability compared with those derived from non-joint tissues; thus, these cell populations are considered ideal sources for cartilage regeneration. In addition to the progress in research and promising preclinical results, many important research questions must be answered before widespread success in cartilage regeneration is achieved. This review outlines the biology of stem/progenitor cells derived from the articular cartilage, the synovial membrane, and the synovial fluid, including their tissue distribution, function and biological characteristics. Furthermore, preclinical and clinical trials focusing on their applications for cartilage regeneration are summarized, and future research perspectives are discussed.

Keywords

Mesenchymal stem cells progenitors Synovial joint Synovial membrane Synovial fluid Articular cartilage Regenerative medicine 

Notes

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 31600792, U1613224 and 31570970).

Compliance with Ethical Standards

Disclosures

The authors declare no conflicts of interest.

References

  1. 1.
    Yamamoto, T., Wakitani, S., Imoto, K., et al. (2004). Fibroblast growth factor-2 promotes the repair of partial thickness defects of articular cartilage in immature rabbits but not in mature rabbits. Osteoarthritis and Cartilage, 12(8), 636–641.PubMedCrossRefGoogle Scholar
  2. 2.
    Hembry, R. M., Dyce, J., Driesang, I., et al. (2001). Immunolocalization of matrix metalloproteinases in partial-thickness defects in pig articular cartilage. A preliminary report. Journal of Bone & Joint Surgery, American, 83-A(6), 826–838.CrossRefGoogle Scholar
  3. 3.
    Masahiko, T., Damle, S., Penmatsa, M., et al. (2012). Temporal changes in collagen cross-links in spontaneous articular cartilage repair. Cartilage, 3(3), 278–287.PubMedCrossRefGoogle Scholar
  4. 4.
    Sellers, R. S., Zhang, R., Glasson, S. S., et al. (2000). Repair of articular cartilage defects one year after treatment with recombinant human bone morphogenetic protein-2 (rhBMP-2). Journal of Bone & Joint Surgery, American, 82(2), 151–160.CrossRefGoogle Scholar
  5. 5.
    Mithoefer, K., McAdams, T., Williams, R. J., Kreuz, P. C., & Mandelbaum, B. R. (2009). Clinical efficacy of the microfracture technique for articular cartilage repair in the knee: an evidence-based systematic analysis. The American Journal of Sports Medicine, 37(10), 2053–2063.PubMedCrossRefGoogle Scholar
  6. 6.
    Case, J. M., & Scopp, J. M. (2016). Treatment of articular cartilage defects of the knee with microfracture and enhanced microfracture techniques. Sports Medicine & Arthroscopy Review, 24(2), 63–68.CrossRefGoogle Scholar
  7. 7.
    Richter, D. L., Schenck Jr., R. C., Wascher, D. C., & Treme, G. (2016). Knee Articular Cartilage Repair and Restoration Techniques: A Review of the Literature. Sports Health, 8(2), 153–160.PubMedCrossRefGoogle Scholar
  8. 8.
    Brittberg, M., Lindahl, A., Nilsson, A., Ohlsson, C., Isaksson, O., & Peterson, L. (1994). Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. The New England Journal of Medicine, 331(14), 889–895.PubMedCrossRefGoogle Scholar
  9. 9.
    Brittberg, M. (2008). Autologous chondrocyte implantation--technique and long-term follow-up. Injury, 39(Suppl 1), S40–S49.PubMedCrossRefGoogle Scholar
  10. 10.
    Schnabel, M., Marlovits, S., Eckhoff, G., et al. (2002). Dedifferentiation-associated changes in morphology and gene expression in primary human articular chondrocytes in cell culture. Osteoarthritis and Cartilage, 10(1), 62–70.PubMedCrossRefGoogle Scholar
  11. 11.
    Darling, E. M., & Athanasiou, K. A. (2005). Rapid phenotypic changes in passaged articular chondrocyte subpopulations. Journal of Orthopaedic Research, 23(2), 425–432.PubMedCrossRefGoogle Scholar
  12. 12.
    Dell'Accio, F., De Bari, C., & Luyten, F. P. (2001). Molecular markers predictive of the capacity of expanded human articular chondrocytes to form stable cartilage in vivo. Arthritis & Rheumatology, 44(7), 1608–1619.CrossRefGoogle Scholar
  13. 13.
    Dell'Accio, F., De Bari, C., & Luyten, F. P. (2003). Microenvironment and phenotypic stability specify tissue formation by human articular cartilage-derived cells in vivo. Experimental Cell Research, 287(1), 16–27.PubMedCrossRefGoogle Scholar
  14. 14.
    Rackwitz, L., Djouad, F., Janjanin, S., Nöth, U., & Tuan, R. S. (2014). Functional cartilage repair capacity of de-differentiated, chondrocyte- and mesenchymal stem cell-laden hydrogels in vitro. Osteoarthritis and Cartilage, 22(8), 1148–1157.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Dominici, M., Le Blanc, K., Mueller, I., et al. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8(4), 315–317.PubMedCrossRefGoogle Scholar
  16. 16.
    Chen, J. Y., Mou, X. Z., Du, X. C., & Xiang, C. (2015). Comparative analysis of biological characteristics of adult mesenchymal stem cells with different tissue origins. Asian Pacific Journal of Tropical Medicine, 8(9), 739–746.PubMedCrossRefGoogle Scholar
  17. 17.
    Somal, A., Bhat, I. A., B, I., et al. (2016). A comparative study of growth kinetics, in vitro differentiation potential and molecular characterization of fetal adnexa derived caprine mesenchymal stem cells. PloS One, 11(6), e0156821.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Liu, R., Chang, W., Wei, H., & Zhang, K. (2016). Comparison of the Biological Characteristics of Mesenchymal Stem Cells Derived from Bone Marrow and Skin. Stem Cells International, 2016, 3658798.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Li, C. Y., Wu, X. Y., Tong, J. B., et al. (2015). Comparative analysis of human mesenchymal stem cells from bone marrow and adipose tissue under xeno-free conditions for cell therapy. Stem Cell Research & Therapy, 6, 55.CrossRefGoogle Scholar
  20. 20.
    Islam, A., Hansen, A. K., Mennan, C., & Martinez-Zubiaurre, I. (2016). Mesenchymal stromal cells from human umbilical cords display poor chondrogenic potential in scaffold-free three dimensional cultures. European Cells & Materials Journal, 31, 407–424.CrossRefGoogle Scholar
  21. 21.
    Bernardo, M. E., Emons, J. A., Karperien, M., et al. (2007). Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources. Connective Tissue Research, 48(3), 132–140.PubMedCrossRefGoogle Scholar
  22. 22.
    Huang, Y. C., Zhu, H. M., Cai, J. Q., et al. (2012). Hypoxia inhibited the spontaneous calcification of bone marrow derived mesenchymal stem cells. Journal of Cellular Biochemistry, 113(4), 1407–1415.PubMedCrossRefGoogle Scholar
  23. 23.
    Farrell, E., Both, S. K., Odörfer, K. I., et al. (2011). In-vivo generation of bone via endochondral ossification by in-vitro chondrogenic priming of adult human and rat mesenchymal stem cells. BMC Musculoskeletal Disorders, 12, 31.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Pelttari, K., Winter, A., Steck, E., et al. (2006). 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, 54(10), 3254–3266.CrossRefGoogle Scholar
  25. 25.
    Yang, W., Both, S. K., van Osch, G. J., Wang, Y., Jansen, J. A., & Yang, F. (2015). Effects of in vitro chondrogenic priming time of bone-marrow-derived mesenchymal stromal cells on in vivo endochondral bone formation. Acta Biomaterialia, 13, 254–265.PubMedCrossRefGoogle Scholar
  26. 26.
    Serafini, M., Sacchetti, B., Pievani, A., et al. (2014). Establishment of bone marrow and hematopoietic niches in vivo by reversion of chondrocyte differentiation of human bone marrow stromal cells. Stem Cell Research, 12(3), 659–672.PubMedCrossRefGoogle Scholar
  27. 27.
    Van der Stok, J., Koolen, M. K., Jahr, H., et al. (2014). Chondrogenically differentiated mesenchymal stromal cell pellets stimulate endochondral bone regeneration in critical-sized bone defects. European Cells & Materials Journal, 27, 137–148.CrossRefGoogle Scholar
  28. 28.
    Su, X., Zuo, W., Wu, Z., et al. (2015). CD146 as a new marker for an increased chondroprogenitor cell sub-population in the later stages of osteoarthritis. Journal of Orthopaedic Research, 33(1), 84–91.PubMedCrossRefGoogle Scholar
  29. 29.
    Ando, W., Kutcher, J. J., Krawetz, R., et al. (2014). Clonal analysis of synovial fluid stem cells to characterize and identify stable mesenchymal stromal cell/mesenchymal progenitor cell phenotypes in a porcine model: a cell source with enhanced commitment to the chondrogenic lineage. Cytotherapy, 16(6), 776–788.PubMedCrossRefGoogle Scholar
  30. 30.
    Ohlsson, C., Nilsson, A., Isaksson, O., & Lindahl, A. (1992). Growth hormone induces multiplication of the slowly cycling germinal cells of the rat tibial growth plate. Proceedings of the National Academy of Sciences of the United States of America, 89(20), 9826–9830.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Karlsson, C., Thornemo, M., Henriksson, H. B., & Lindahl, A. (2009). Identification of a stem cell niche in the zone of Ranvier within the knee joint. Journal of Anatomy, 215(3), 355–363.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Candela, M. E., Cantley, L., Yasuaha, R., Iwamoto, M., Pacifici, M., & Enomoto-Iwamoto, M. (2014). Distribution of slow-cycling cells in epiphyseal cartilage and requirement of β-catenin signaling for their maintenance in growth plate. Journal of Orthopaedic Research, 32(5), 661–668.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Kozhemyakina, E., Zhang, M., Ionescu, A., et al. (2015). Identification of a Prg4-expressing articular cartilage progenitor cell population in mice. Arthritis & Rheumatology, 67(5), 1261–1273.CrossRefGoogle Scholar
  34. 34.
    Pretzel, D., Linss, S., Rochler, S., et al. (2011). Relative percentage and zonal distribution of mesenchymal progenitor cells in human osteoarthritic and normal cartilage. Arthritis Research & Therapy, 13(2), R64.CrossRefGoogle Scholar
  35. 35.
    Ustunel, I., Ozenci, A. M., Sahin, Z., et al. (2008). The immunohistochemical localization of notch receptors and ligands in human articular cartilage, chondroprogenitor culture and ultrastructural characteristics of these progenitor cells. Acta Histochemica, 110(5), 397–407.PubMedCrossRefGoogle Scholar
  36. 36.
    Ozbey, O., Sahin, Z., Acar, N., et al. (2014). Characterization of colony-forming cells in adult human articular cartilage. Acta Histochemica, 116(5), 763–770.PubMedCrossRefGoogle Scholar
  37. 37.
    Grogan, S. P., Miyaki, S., Asahara, H., D'Lima, D. D., & Lotz, M. K. (2009). Mesenchymal progenitor cell markers in human articular cartilage: normal distribution and changes in osteoarthritis. Arthritis Research & Therapy, 11(3), R85.CrossRefGoogle Scholar
  38. 38.
    Giurea, A., Rüger, B. M., Hollemann, D., Yanagida, G., Kotz, R., & Fischer, M. B. (2006). STRO-1+ mesenchymal precursor cells located in synovial surface projections of patients with osteoarthritis. Osteoarthritis and Cartilage, 14(9), 938–943.PubMedCrossRefGoogle Scholar
  39. 39.
    Klein, T. J., Malda, J., Sah, R. L., & Hutmacher, D. W. (2009). Tissue engineering of articular cartilage with biomimetic zones. Tissue Engineering Part B Reviews, 15(2), 143–157.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Hayes, A. J., MacPherson, S., Morrison, H., Dowthwaite, G., & Archer, C. W. (2001). The development of articular cartilage: evidence for an appositional growth mechanism. Anatomy and Embryology (Berlin), 203(6), 469–479.CrossRefGoogle Scholar
  41. 41.
    Bartok, B., & Firestein, G. S. (2010). Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunological Reviews, 233(1), 233–255.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Vandenabeele, F., De Bari, C., Moreels, M., et al. (2003). Morphological and immunocytochemical characterization of cultured fibroblast-like cells derived from adult human synovial membrane. Archives of Histology and Cytology, 66(2), 145–153.PubMedCrossRefGoogle Scholar
  43. 43.
    Kurth, T. B., Dell'accio, F., Crouch, V., Augello, A., Sharpe, P. T., & De Bari, C. (2011). Functional mesenchymal stem cell niches in adult mouse knee joint synovium in vivo. Arthritis & Rheumatology, 63(5), 1289–1300.CrossRefGoogle Scholar
  44. 44.
    Hermida-Gómez, T., Fuentes-Boquete, I., Gimeno-Longas, M. J., et al. (2011). Quantification of cells expressing mesenchymal stem cell markers in healthy and osteoarthritic synovial membranes. The Journal of Rheumatology, 38(2), 339–349.PubMedCrossRefGoogle Scholar
  45. 45.
    Chen, C., Fingerhut, J. M., & Yamashita, Y. M. (2016). The ins(ide) and outs(ide) of asymmetric stem cell division. Current Opinion in Cell Biology, 43, 1–6.PubMedCrossRefGoogle Scholar
  46. 46.
    Mukoyama, S., Sasho, T., Akatsu, Y., et al. (2015). Spontaneous repair of partial thickness linear cartilage injuries in immature rats. Cell and Tissue Research, 359(2), 513–520.PubMedCrossRefGoogle Scholar
  47. 47.
    Zhang, K., Shi, J., Li, Y., et al. (2016). Chondrogenic cells respond to partial-thickness defects of articular cartilage in adult rats: an in vivo study. Journal of Molecular Histology, 47(3), 249–258.PubMedCrossRefGoogle Scholar
  48. 48.
    Hunziker, E. B., & Rosenberg, L. C. (1996). Repair of partial-thickness defects in articular cartilage: cell recruitment from the synovial membrane. Journal of Bone & Joint Surgery, American, 78(5), 721–733.CrossRefGoogle Scholar
  49. 49.
    Hunziker, E. B. (2001). Growth-factor-induced healing of partial-thickness defects in adult articular cartilage. Osteoarthritis and Cartilage, 9(1), 22–32.PubMedCrossRefGoogle Scholar
  50. 50.
    Morito, T., Muneta, T., Hara, K., et al. (2008). Synovial fluid-derived mesenchymal stem cells increase after intra-articular ligament injury in humans. Rheumatology (Oxford, England), 47(8), 1137–1143.CrossRefGoogle Scholar
  51. 51.
    Matsukura, Y., Muneta, T., Tsuji, K., Koga, H., & Sekiya, I. (2014). Mesenchymal stem cells in synovial fluid increase after meniscus injury. Clinical Orthopaedics and Related Research, 472(5), 1357–1364.PubMedCrossRefGoogle Scholar
  52. 52.
    Anraku, Y., Mizuta, H., Sei, A., et al. (2009). Analyses of early events during chondrogenic repair in rat full-thickness articular cartilage defects. Journal of Bone and Mineral Metabolism, 27(3), 272–286.PubMedCrossRefGoogle Scholar
  53. 53.
    Chuma, H., Mizuta, H., Kudo, S., Takagi, K., & Hiraki, Y. (2004). One day exposure to FGF-2 was sufficient for the regenerative repair of full-thickness defects of articular cartilage in rabbits. Osteoarthritis and Cartilage, 12(10), 834–842.PubMedCrossRefGoogle Scholar
  54. 54.
    Swan, A., Amer, H., & Dieppe, P. (2002). The value of synovial fluid assays in the diagnosis of joint disease: a literature survey. Annals of the Rheumatic Diseases, 61(6), 493–498.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Delling, U., Brehm, W., Metzger, M., Ludewig, E., Winter, K., & Jülke, H. (2015). In vivo tracking and fate of intra-articularly injected superparamagnetic iron oxide particle-labeled multipotent stromal cells in an ovine model of osteoarthritis. Cell Transplantation, 24(11), 2379–2390.PubMedCrossRefGoogle Scholar
  56. 56.
    Skagen, P. S., Kruse, H. A., & Horn, T. (2014). Repair Mechanisms in Articular Cartilage—A Porcine in Vitro Study. Microscopy Research, 2(2), 67–80.CrossRefGoogle Scholar
  57. 57.
    Seol, D., McCabe, D. J., Choe, H., et al. (2012). Chondrogenic progenitor cells respond to cartilage injury. Arthritis & Rheumatology, 64(11), 3626–3637.CrossRefGoogle Scholar
  58. 58.
    Yu, Y., Brouillette, M. J., Seol, D., Zheng, H., Buckwalter, J. A., & Martin, J. A. (2015). Use of recombinant human stromal cell-derived factor 1α-loaded fibrin/hyaluronic acid hydrogel networks to achieve functional repair of full-thickness bovine articular cartilage via homing of chondrogenic progenitor cells. Arthritis & Rheumatology, 67(5), 1274–1285.CrossRefGoogle Scholar
  59. 59.
    Bos, P. K., Kops, N., Verhaar, J. A., & van Osch, G. J. (2008). Cellular origin of neocartilage formed at wound edges of articular cartilage in a tissue culture experiment. Osteoarthritis and Cartilage, 16(2), 204–211.PubMedCrossRefGoogle Scholar
  60. 60.
    Dowthwaite, G. P., Bishop, J. C., Redman, S. N., Thomson, B., & Archer, C. W. (2002). Characterisation of articular cartilage progenitor cells. European Cells & Materials Journal, 4, 35–36.Google Scholar
  61. 61.
    Dowthwaite, G. P., Bishop, J. C., Redman, S. N., et al. (2004). The surface of articular cartilage contains a progenitor cell population. Journal of Cell Science, 117(Pt 6), 889–897.PubMedCrossRefGoogle Scholar
  62. 62.
    Nelson, L., McCarthy, H. E., Fairclough, J., Williams, R., & Archer, C. W. (2014). Evidence of a Viable Pool of Stem Cells within Human Osteoarthritic Cartilage. Cartilage, 5(4), 203–214.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Choi, W. H., Kim, H. R., Lee, S. J., et al. (2016). Fetal cartilage-derived cells have stem cell properties and are a highly potent cell source for cartilage regeneration. Cell Transplantation, 25(3), 449–461.PubMedCrossRefGoogle Scholar
  64. 64.
    Salamon, A., Jonitz-Heincke, A., Adam, S., et al. (2013). Articular cartilage-derived cells hold a strong osteogenic differentiation potential in comparison to mesenchymal stem cells in vitro. Experimental Cell Research, 319(18), 2856–2865.PubMedCrossRefGoogle Scholar
  65. 65.
    Li, Y., Zhou, J., Yang, X., Jiang, Y., & Gui, J. (2016). Intermittent hydrostatic pressure maintains and enhances the chondrogenic differentiation of cartilage progenitor cells cultivated in alginate beads. Development Growth & Differentiation, 58(2), 180–193.CrossRefGoogle Scholar
  66. 66.
    Williams, R., Khan, I. M., Richardson, K., et al. (2010). Identification and clonal characterisation of a progenitor cell sub-population in normal human articular cartilage. PloS One, 5(10), e13246.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    McCarthy, H. E., Bara, J. J., Brakspear, K., Singhrao, S. K., & Archer, C. W. (2012). The comparison of equine articular cartilage progenitor cells and bone marrow-derived stromal cells as potential cell sources for cartilage repair in the horse. The Veterinary Journal, 192(3), 345–351.PubMedCrossRefGoogle Scholar
  68. 68.
    Fickert, S., Fiedler, J., & Brenner, R. E. (2003). Identification, quantification and isolation of mesenchymal progenitor cells from osteoarthritic synovium by fluorescence automated cell sorting. Osteoarthritis and Cartilage, 11(11), 790–800.PubMedCrossRefGoogle Scholar
  69. 69.
    Li, J., Campbell, D. D., Bal, G. K., & Pei, M. (2014). Can arthroscopically harvested synovial stem cells be preferentially sorted using stage-specific embryonic antigen 4 antibody for cartilage, bone, and adipose regeneration? Arthroscopy: The Journal of Arthroscopic & Related Surgery, 30(3), 352–361.CrossRefGoogle Scholar
  70. 70.
    De Bari, C., Dell'Accio, F., Tylzanowski, P., & Luyten, F. P. (2001). Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis & Rheumatology, 44(8), 1928–1942.CrossRefGoogle Scholar
  71. 71.
    Sakaguchi, Y., Sekiya, I., Yagishita, K., & Muneta, T. (2005). Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis & Rheumatology, 52(8), 2521–2529.CrossRefGoogle Scholar
  72. 72.
    Yoshimura, H., Muneta, T., Nimura, A., Yokoyama, A., Koga, H., & Sekiya, I. (2007). Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell and Tissue Research, 327(3), 449–462.PubMedCrossRefGoogle Scholar
  73. 73.
    Mochizuki, T., Muneta, T., Sakaguchi, Y., et al. (2006). Higher chondrogenic potential of fibrous synovium- and adipose synovium-derived cells compared with subcutaneous fat-derived cells: distinguishing properties of mesenchymal stem cells in humans. Arthritis & Rheumatology, 54(3), 843–853.CrossRefGoogle Scholar
  74. 74.
    Segawa, Y., Muneta, T., Makino, H., et al. (2009). Mesenchymal stem cells derived from synovium, meniscus, anterior cruciate ligament, and articular chondrocytes share similar gene expression profiles. Journal of Orthopaedic Research, 27(4), 435–441.PubMedCrossRefGoogle Scholar
  75. 75.
    Karystinou, A., Dell'Accio, F., Kurth, T. B., et al. (2009). Distinct mesenchymal progenitor cell subsets in the adult human synovium. Rheumatology (Oxford, England), 48(9), 1057–1064.CrossRefGoogle Scholar
  76. 76.
    Bilgen, B., Ren, Y., Pei, M., Aaron, R. K., & Ciombor, D. M. (2009). CD14-negative isolation enhances chondrogenesis in synovial fibroblasts. Tissue Engineering Part A, 15(11), 3261–3270.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Gullo, F., & De Bari, C. (2013). Prospective purification of a subpopulation of human synovial mesenchymal stem cells with enhanced chondro-osteogenic potency. Rheumatology (Oxford, England), 52(10), 1758–1768.CrossRefGoogle Scholar
  78. 78.
    Jones, E. A., Crawford, A., English, A., et al. (2008). Synovial fluid mesenchymal stem cells in health and early osteoarthritis: detection and functional evaluation at the single-cell level. Arthritis & Rheumatology, 58(6), 1731–1740.CrossRefGoogle Scholar
  79. 79.
    Lee, W. J., Hah, Y. S., Ock, S. A., et al. (2015). Cell source-dependent in vivo immunosuppressive properties of mesenchymal stem cells derived from the bone marrow and synovial fluid of minipigs. Experimental Cell Research, 333(2), 273–288.PubMedCrossRefGoogle Scholar
  80. 80.
    Kim, Y. S., Lee, H. J., Yeo, J. E., Kim, Y. I., Choi, Y. J., & Koh, Y. G. (2015). Isolation and characterization of human mesenchymal stem cells derived from synovial fluid in patients with osteochondral lesion of the talus. The American Journal of Sports Medicine, 43(2), 399–406.PubMedCrossRefGoogle Scholar
  81. 81.
    Krawetz, R. J., Wu, Y. E., Martin, L., Rattner, J. B., Matyas, J. R., & Hart, D. A. (2012). Synovial fluid progenitors expressing CD90+ from normal but not osteoarthritic joints undergo chondrogenic differentiation without micro-mass culture. PloS One, 7(8), e43616.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Marcus, P., De Bari, C., Dell'Accio, F., & Archer, C. W. (2014). Articular chondroprogenitor cells maintain chondrogenic potential but fail to form a functional matrix when implanted into muscles of SCID mice. Cartilage, 5(4), 231–240.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Frisbie, D. D., McCarthy, H. E., Archer, C. W., Barrett, M. F., & McIlwraith, C. W. (2015). Evaluation of articular cartilage progenitor cells for the repair of articular defects in an equine model. Journal of Bone & Joint Surgery, American, 97(6), 484–493.CrossRefGoogle Scholar
  84. 84.
    De Bari, C., Dell'Accio, F., & Luyten, F. P. (2004). Failure of in vitro-differentiated mesenchymal stem cells from the synovial membrane to form ectopic stable cartilage in vivo. Arthritis & Rheumatology, 50(1), 142–150.CrossRefGoogle Scholar
  85. 85.
    Vinardell, T., Sheehy, E. J., Buckley, C. T., & Kelly, D. J. (2012). A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources. Tissue Engineering Part A, 18(11–12), 1161–1170.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Hori, J., Deie, M., Kobayashi, T., Yasunaga, Y., Kawamata, S., & Ochi, M. (2011). Articular cartilage repair using an intra-articular magnet and synovium-derived cells. Journal of Orthopaedic Research, 29(4), 531–538.PubMedCrossRefGoogle Scholar
  87. 87.
    Koga, H., Muneta, T., Ju, Y. J., et al. (2007). Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells, 25(3), 689–696.PubMedCrossRefGoogle Scholar
  88. 88.
    Pei, M., He, F., Boyce, B. M., & Kish, V. L. (2009). Repair of full-thickness femoral condyle cartilage defects using allogeneic synovial cell-engineered tissue constructs. Osteoarthritis and Cartilage, 17(6), 714–722.PubMedCrossRefGoogle Scholar
  89. 89.
    Suzuki, S., Muneta, T., Tsuji, K., et al. (2012). Properties and usefulness of aggregates of synovial mesenchymal stem cells as a source for cartilage regeneration. Arthritis Research & Therapy, 14(3), R136.CrossRefGoogle Scholar
  90. 90.
    Lee, J. C., Min, H. J., Park, H. J., Lee, S., Seong, S. C., & Lee, M. C. (2013). Synovial membrane-derived mesenchymal stem cells supported by platelet-rich plasma can repair osteochondral defects in a rabbit model. Arthroscopy: The Journal of Arthroscopic & Related Surgery, 29(6), 1034–1046.CrossRefGoogle Scholar
  91. 91.
    Koga, H., Shimaya, M., Muneta, T., et al. (2008). Local adherent technique for transplanting mesenchymal stem cells as a potential treatment of cartilage defect. Arthritis Research & Therapy, 10(4), R84.CrossRefGoogle Scholar
  92. 92.
    Nakamura, T., Sekiya, I., Muneta, T., et al. (2012). 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, 14(3), 327–338.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Lee, J. C., Min, H. J., Lee, S., Seong, S. C., & Lee, M. C. (2013). Effect of chondroitinase ABC on adhesion and behavior of synovial membrane-derived mesenchymal stem cells in rabbit partial-thickness chondral defects. Journal of Orthopaedic Research, 31(8), 1293–1301.PubMedCrossRefGoogle Scholar
  94. 94.
    Ando, W., Tateishi, K., Hart, D. A., et al. (2007). Cartilage repair using an in vitro generated scaffold-free tissue-engineered construct derived from porcine synovial mesenchymal stem cells. Biomaterials, 28(36), 5462–5470.PubMedCrossRefGoogle Scholar
  95. 95.
    Shimomura, K., Ando, W., Tateishi, K., et al. (2010). The influence of skeletal maturity on allogenic synovial mesenchymal stem cell-based repair of cartilage in a large animal model. Biomaterials, 31(31), 8004–8011.PubMedCrossRefGoogle Scholar
  96. 96.
    Fujie, H., Nansai, R., Ando, W., et al. (2015). Zone-specific integrated cartilage repair using a scaffold-free tissue engineered construct derived from allogenic synovial mesenchymal stem cells: Biomechanical and histological assessments. Journal of Biomechanics, 48(15), 4101–4108.PubMedCrossRefGoogle Scholar
  97. 97.
    Ando, W., Fujie, H., Moriguchi, Y., et al. (2012). Detection of abnormalities in the superficial zone of cartilage repaired using a tissue engineered construct derived from synovial stem cells. European Cells & Materials Journal, 24, 292–307.CrossRefGoogle Scholar
  98. 98.
    Chiang, C. W., Chen, W. C., Liu, H. W., & Chen, C. H. (2014). Application of synovial fluid mesenchymal stem cells: platelet-rich plasma hydrogel for focal cartilage defect. Journal of Experimental & Clinical Medicine, 6(4), 118–124.CrossRefGoogle Scholar
  99. 99.
    Jiang, Y., Cai, Y., Zhang, W., et al. (2016). Human cartilage-derived progenitor cells from committed chondrocytes for efficient cartilage repair and regeneration. Stem Cells Translational Medicine, 5(6), 733–744.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Sekiya, I., Muneta, T., Horie, M., & Koga, H. (2015). Arthroscopic transplantation of synovial stem cells improves clinical outcomes in knees with cartilage defects. Clinical Orthopaedics and Related Research, 473(7), 2316–2326.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Alsalameh, S., Amin, R., Gemba, T., & Lotz, M. (2004). Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage. Arthritis & Rheumatology, 50(5), 1522–1532.CrossRefGoogle Scholar
  102. 102.
    Fickert, S., Fiedler, J., & Brenner, R. E. (2004). Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Research & Therapy, 6(5), R422–R432.CrossRefGoogle Scholar
  103. 103.
    Hattori, S., Oxford, C., & Reddi, A. H. (2007). Identification of superficial zone articular chondrocyte stem/progenitor cells. Biochemical and Biophysical Research Communications, 358(1), 99–103.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Yu, Y., Zheng, H., Buckwalter, J. A., & Martin, J. A. (2014). Single cell sorting identifies progenitor cell population from full thickness bovine articular cartilage. Osteoarthritis and Cartilage, 22(9), 1318–1326.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Fu, C., Yan, Z., Xu, H., et al. (2015). Isolation, identification and differentiation of human embryonic cartilage stem cells. Cell Biology International, 39(7), 777–787.PubMedCrossRefGoogle Scholar
  106. 106.
    Djouad, F., Bony, C., Häupl, T., et al. (2005). Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Research & Therapy, 7(6), R1304–R1315.CrossRefGoogle Scholar
  107. 107.
    Prado, A. A., Favaron, P. O., da Silva, L. C., Baccarin, R. Y., Miglino, M. A., & Maria, D. A. (2015). Characterization of mesenchymal stem cells derived from the equine synovial fluid and membrane. BMC Veterinary Research, 11, 281.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Godoy, R. F., Alves, A. L., Gibson, A. J., Lima, E. M., & Goodship, A. E. (2014). Do progenitor cells from different tissue have the same phenotype? Research in Veterinary Science, 96(3), 454–459.PubMedCrossRefGoogle Scholar
  109. 109.
    Teramura, T., Fukuda, K., Kurashimo, S., et al. (2008). Isolation and characterization of side population stem cells in articular synovial tissue. BMC Musculoskeletal Disorders, 9, 86.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Jones, E. A., English, A., Henshaw, K., et al. (2004). Enumeration and phenotypic characterization of synovial fluid multipotential mesenchymal progenitor cells in inflammatory and degenerative arthritis. Arthritis & Rheumatology, 50(3), 817–827.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Laboratory of Stem Cell and Tissue Engineering, West China HospitalSichuan UniversityChengduChina
  2. 2.Centro di Ricerca E. MenniFondazione Poliambulanza-Istituto OspedalieroBresciaItaly
  3. 3.Istituto di Anatomia Umana e Biologia CellulareUniversità Cattolica del Sacro Cuore Facoltà di Medicina e ChirurgiaRomeItaly
  4. 4.Shenzhen Engineering Laboratory of Orthopaedic Regenerative Technologies, Orthopaedic Research CenterPeking University Shenzhen HospitalShenzhenChina
  5. 5.Shenzhen Key Laboratory of Spine Surgery, Department of Spine SurgeryPeking University Shenzhen HospitalShenzhenChina
  6. 6.Department of Orthopaedics and TraumatologyThe University of Hong KongHong KongChina
  7. 7.Beijing Key Laboratory for Genetic Research of Bone and Joint Disease, Central Laboratory, Peking Union Medical College HospitalPeking Union Medical College and Chinese Academy of Medical SciencesBeijingChina

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