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Stem Cells International
Volume 2010, Article ID 519028, 14 pages
http://dx.doi.org/10.4061/2010/519028
Review Article

Mesenchymal Progenitor Cells and Their Orthopedic Applications: Forging a Path towards Clinical Trials

1Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, 5841 South Maryland Avenue, MC3079, Chicago, IL 60637, USA
2Key Laboratory of Diagnostic Medicine Designated by Chinese Ministry of Education, The Affiliated Hospitals of Chongqing Medical University, Chongqing 400016, China
3Stem Cell Biology and Therapy Laboratory, The Children's Hospital of Chongqing Medical University, Chongqing 400014, China
4School of Bioengineering, Chongqing University, Chongqing 400030, China
5Department of Geriatrics, Xinhua Hospital of Shanghai Jiatong University, Shanghai 400092, China
6Department of Cell Biology, The Third Military Medical University, Chongqing 400042, China

Received 17 May 2010; Revised 7 July 2010; Accepted 28 September 2010

Academic Editor: Jin Sup Jung

Copyright © 2010 Deana S. Shenaq 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. H. E. Young, “Existence of reserve quiescent stem cells in adults, from amphibians to humans,” Current Topics in Microbiology and Immunology, vol. 280, pp. 71–109, 2003. View at Google Scholar · View at Scopus
  2. M. Buehr, S. Meek, K. Blair et al., “Capture of authentic embryonic stem cells from rat blastocysts,” Cell, vol. 135, no. 7, pp. 1287–1298, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. J. A. Thomson, “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Google Scholar · View at Scopus
  4. M. Cho, E. J. Lee, H. Nam et al., “Human feeder layer system derived from umbilical cord stromal cells for human embryonic stem cells,” Fertility and Sterility, vol. 93, no. 8, pp. 2525–2531, 2010. View at Publisher · View at Google Scholar
  5. L. Gepstein, “Derivation and potential applications of human embryonic stem cells,” Circulation Research, vol. 91, no. 10, pp. 866–876, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. A. S. Lee, C. Tang, F. Cao et al., “Effects of cell number on teratoma formation by human embryonic stem cells,” Cell Cycle, vol. 8, no. 16, pp. 2608–2612, 2009. View at Google Scholar · View at Scopus
  7. B. Hamilton, Q. Feng, M. Ye, and G. G. Welstead, “Generation of induced pluripotent stem cells by reprogramming mouse embryonic fibroblasts with a four transcription factor, doxycycline inducible lentiviral transduction system,” Journal of Visualized Experiments, no. 33, 2009. View at Google Scholar
  8. I.-H. Park, R. Zhao, J. A. West et al., “Reprogramming of human somatic cells to pluripotency with defined factors,” Nature, vol. 451, no. 7175, pp. 141–146, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. C. A. Sommer, M. Stadtfeld, G. J. Murphy, K. Hochedlinger, D. N. Kotton, and G. Mostoslavsky, “Induced pluripotent stem cell generation using a single lentiviral stem cell cassette,” Stem Cells, vol. 27, no. 3, pp. 543–549, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Yu, M. A. Vodyanik, K. Smuga-Otto et al., “Induced pluripotent stem cell lines derived from human somatic cells,” Science, vol. 318, no. 5858, pp. 1917–1920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. C. J. Lengner, “IPS cell technology in regenerative medicine,” Annals of the New York Academy of Sciences, vol. 1192, no. 1, pp. 38–44, 2010. View at Publisher · View at Google Scholar
  13. A. P. D .N. deBarros, C. M. Takiya, L. R. Garzoni et al., “Osteoblasts and bone marrow mesenchymal stromal cells control hematopoietic stem cell migration and proliferation in 3D in vitro model,” PLoS ONE, vol. 5, no. 2, Article ID e9093, 2010. View at Publisher · View at Google Scholar
  14. Y. Jiang, B. N. Jahagirdar, R. L. Reinhardt et al., “Pluripotency of mesenchymal stem cells derived from adult marrow,” Nature, vol. 418, no. 6893, pp. 41–49, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Steinhardt, H. Aslan, E. Regev et al., “Maxillofacial-derived stem cells regenerate critical mandibular bone defect,” Tissue Engineering—Part A, vol. 14, no. 11, pp. 1763–1773, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. I. Bab, B. A. Ashton, D. Gazit, G. Marx, M. C. Williamson, and M. E. Owen, “Kinetics and differentiation of marrow stromal cells in diffusion chambers in vivo,” Journal of Cell Science, vol. 84, pp. 139–151, 1986. View at Google Scholar · View at Scopus
  17. H. Castro-Malaspina, R. E. Gay, and G. Resnick, “Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny,” Blood, vol. 56, no. 2, pp. 289–301, 1980. View at Google Scholar · View at Scopus
  18. J. E. Dennis and P. Charbord, “Origin and differentiation of human and murine stroma,” Stem Cells, vol. 20, no. 3, pp. 205–214, 2002. View at Google Scholar · View at Scopus
  19. M. Kassem, M. Kristiansen, and B. M. Abdallah, “Mesenchymal stem cells: cell biology and potential use in therapy,” Basic and Clinical Pharmacology and Toxicology, vol. 95, no. 5, pp. 209–214, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. 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
  21. W. Wagner, F. Wein, A. Seckinger et al., “Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood,” Experimental Hematology, vol. 33, no. 11, pp. 1402–1416, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. A. J. Friedenstein, K. V. Petrakova, A. I. Kurolesova, and G. P. Frolova, “Heterotopic of bone marrow.Analysis of precursor cells for osteogenic and hematopoietic tissues,” Transplantation, vol. 6, no. 2, pp. 230–247, 1968. View at Google Scholar · View at Scopus
  23. S. A. Kuznetsov, M. H. Mankani, P. Bianco, and P. G. Robey, “Enumeration of the colony-forming units-fibroblast from mouse and human bone marrow in normal and pathological conditions,” Stem Cell Research, vol. 2, no. 1, pp. 83–94, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. Z.-L. Deng, K. A. Sharff, N. Tang et al., “Regulation of osteogenic differentiation during skeletal development,” Frontiers in Bioscience, vol. 13, no. 6, pp. 2001–2021, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. H. H. Luu, W.-X. Song, X. Luo et al., “Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells,” Journal of Orthopaedic Research, vol. 25, no. 5, pp. 665–677, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Igura, X. Zhang, K. Takahashi, A. Mitsuru, S. Yamaguchi, and T. A. Takahashi, “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 · View at Scopus
  27. A. Briquet, S. Dubois, S. Bekaert, M. Dolhet, Y. Beguin, and A. Gothot, “Prolonged ex vivo culture of human bone marrow mesenchymal stem cells influences their supportive activity toward NOD/SCID-repopulating cells and committed progenitor cells of B lymphoid and myeloid lineages,” Haematologica, vol. 95, no. 1, pp. 47–56, 2010. View at Publisher · View at Google Scholar
  28. M. H. Mankani, S. A. Kuznetsov, and P. G. Robey, “Formation of hematopoietic territories and bone by transplanted human bone marrow stromal cells requires a critical cell density,” Experimental hematology, vol. 35, no. 6, pp. 995–1004, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Götherström, O. Ringdén, C. Tammik, E. Zetterberg, M. Westgren, and K. Le Blanc, “Immunologic properties of human fetal mesenchymal stem cells,” American Journal of Obstetrics and Gynecology, vol. 190, no. 1, pp. 239–245, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Le Blanc, F. Frassoni, L. Ball et al., “Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study,” The Lancet, vol. 371, no. 9624, pp. 1579–1586, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Le Blanc, C. Tammik, K. Rosendahl, E. Zetterberg, and O. Ringdén, “HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells,” Experimental Hematology, vol. 31, no. 10, pp. 890–896, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. A. J. Nauta, G. Westerhuis, A. B. Kruisselbrink, E. G. A. Lurvink, R. Willemze, and W. E. Fibbe, “Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting,” Blood, vol. 108, no. 6, pp. 2114–2120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  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. A. Sorrentino, M. Ferracin, G. Castelli et al., “Isolation and characterization of CD146+ multipotent mesenchymal stromal cells,” Experimental Hematology, vol. 36, no. 8, pp. 1035–1046, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. B. Sacchetti, A. Funari, S. Michienzi et al., “Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment,” Cell, vol. 131, no. 2, pp. 324–336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Dazzi, R. Ramasamy, S. Glennie, S. P. Jones, and I. Roberts, “The role of mesenchymal stem cells in haemopoiesis,” Blood Reviews, vol. 20, no. 3, pp. 161–171, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Kadiyala, R. G. Young, M. A. Thiede, and S. P. Bruder, “Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro,” Cell Transplantation, vol. 6, no. 2, pp. 125–134, 1997. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Dos Santos, P. Z. Andrade, J. S. Boura, M. M. Abecasis, C. L. Da Silva, and J. M.S. Cabral, “Ex vivo expansion of human mesenchymal stem cells: a more effective cell proliferation kinetics and metabolism under hypoxia,” Journal of Cellular Physiology, vol. 223, no. 1, pp. 27–35, 2010. View at Publisher · View at Google Scholar
  39. A. K. Prahalad and J. M. Hock, “Proteomic characteristics of ex vvo-enriched adult human bone marrow mononuclear cells in continuous perfusion cultures,” Journal of Proteome Research, vol. 8, no. 4, pp. 2079–2089, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Hernigou, G. Mathieu, A. Poignard, O. Manicom, F. Beaujean, and H. Rouard, “Percutaneous autologous bone-marrow grafting for nonunions. Surgical technique,” The Journal of Bone and Joint Surgery A, vol. 88, supplement, part 2, pp. 322–327, 2006. View at Google Scholar · View at Scopus
  41. PH. Hernigou, A. Poignard, F. Beaujean, and H. Rouard, “Percutaneous autologous bone-marrow grafting for nonunions: influence of the number and concentration of progenitor cells,” Journal of Bone and Joint Surgery A, vol. 87, no. 7, pp. 1430–1437, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. F. H. Seeger, T. Tonn, N. Krzossok, A. M. Zeiher, and S. Dimmeler, “Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction,” European Heart Journal, vol. 28, no. 6, pp. 766–772, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. D. J. Prockop, “Marrow stromal cells as stem cells for nonhematopoietic tissues,” Science, vol. 276, no. 5309, pp. 71–74, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Tondreau, L. Lagneaux, M. Dejeneffe et al., “Isolation of BM mesenchymal stem cells by plastic adhesion or negative selection: phenotype, proliferation kinetics and differentiation potential,” Cytotherapy, vol. 6, no. 4, pp. 372–379, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Aslan, Y. Zilberman, L. Kandel et al., “Osteogenic differentiation of noncultured immunoisolated bone marrow-derived CD105+ cells,” Stem Cells, vol. 24, no. 7, pp. 1728–1737, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Gronthos and A. C. W. Zannettino, “A method to isolate and purify human bone marrow stromal stem cells,” Methods in Molecular Biology, vol. 449, pp. 45–57, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. P. J. Psaltis, S. Paton, F. See et al., “Enrichment for STRO-1 expression enhances the cardiovascular paracrine activity of human bone marrow-derived mesenchymal cell populations,” Journal of Cellular Physiology, vol. 223, no. 2, pp. 530–540, 2010. View at Publisher · View at Google Scholar
  48. G. F. Muschler and R. J. Midura, “Connective tissue progenitors: practical concepts for clinical applications,” Clinical Orthopaedics and Related Research, no. 395, pp. 66–80, 2002. View at Google Scholar · View at Scopus
  49. J. T. Vilquin and P. Rosset, “Mesenchymal stem cells in bone and cartilage repair: current status,” Regenerative medicine, vol. 1, no. 4, pp. 589–604, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. M. H. Mankani, S. A. Kuznetsov, G. W. Marshall, and P. G. Robey, “Creation of new bone by the percutaneous injection of human bone marrow stromal cell and HA/TCP suspensions,” Tissue Engineering—Part A, vol. 14, no. 12, pp. 1949–1958, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. S. S. Tseng, M. A. Lee, and A. H. Reddi, “Nonunions and the potential of stem cells in fracture-healing,” Journal of Bone and Joint Surgery A, vol. 90, supplement 1, pp. 92–98, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Gundle, C. J. Joyner, and J. T. Triffitt, “Human bone tissue formation in diffusion chamber culture in vivo by bone-derived cells and marrow stromal fibroblastic cells,” Bone, vol. 16, no. 6, pp. 597–601, 1995. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Bostrom, J. M. Lane, E. Tomin et al., “Use of bone morphogenetic protein-2 in the rabbit ulnar nonunion model,” Clinical Orthopaedics and Related Research, no. 327, pp. 272–282, 1996. View at Google Scholar · View at Scopus
  54. E. Kon, A. Muraglia, A. Corsi et al., “Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones,” Journal of Biomedical Materials Research, vol. 49, no. 3, pp. 328–337, 2000. View at Publisher · View at Google Scholar · View at Scopus
  55. T. L. Arinzeh, S. J. Peter, M. P. Archambault et al., “Allogeneic mesenchymal stem cells regenerate bone in a critical-sized canine segmental defect,” Journal of Bone and Joint Surgery A, vol. 85, no. 10, pp. 1927–1935, 2003. View at Google Scholar · View at Scopus
  56. S. A. Kuznetsov, K. E. Huang, G. W. Marshall, P. G. Robey, and M. H. Mankani, “Long-term stable canine mandibular augmentation using autologous bone marrow stromal cells and hydroxyapatite/tricalcium phosphate,” Biomaterials, vol. 29, no. 31, pp. 4211–4216, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. M. H. Mankani, S. A. Kuznetsov, R. M. Wolfe, G. W. Marshall, and P. G. Robey, “In vivo bone formation by human bone marrow stromal cells: reconstruction of the mouse calvarium and mandible,” Stem Cells, vol. 24, no. 9, pp. 2140–2149, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. M. H. Mankani, S. A. Kuznetsov, B. Shannon et al., “Canine cranial reconstruction using autologous bone marrow stromal cells,” American Journal of Pathology, vol. 168, no. 2, pp. 542–550, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Quarto, M. Mastrogiacomo, R. Cancedda et al., “Repair of large bone defects with the use of autologous bone marrow stromal cells,” New England Journal of Medicine, vol. 344, no. 5, pp. 385–386, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Marcacci, E. Kon, V. Moukhachev et al., “Stem cells associated with macroporous bioceramics for long bone repair: 6- To 7-year outcome of a pilot clinical study,” Tissue Engineering, vol. 13, no. 5, pp. 947–955, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Ohgushi, J. Miyake, T. Tateishi, and W. , “Mesenchymal stem cells and bioceramics: strategies to regenerate the skeleton,” Novartis Foundation Symposium, vol. 249, pp. 118–132, 2003. View at Google Scholar · View at Scopus
  62. C. A. Vacanti, L. J. Bonassar, M. P. Vacanti, and J. Shufflebarger, “Replacement of an avulsed phalanx with tissue-engineered bone,” New England Journal of Medicine, vol. 344, no. 20, pp. 1511–1514, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Lendeckel, A. Jödicke, P. Christophis et al., “Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report,” Journal of Cranio-Maxillofacial Surgery, vol. 32, no. 6, pp. 370–373, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Hibi, Y. Yamada, H. Kagami, and M. Ueda, “Distraction osteogenesis assisted by tissue engineering in an irradiated mandible: a case report,” International Journal of Oral and Maxillofacial Implants, vol. 21, no. 1, pp. 141–147, 2006. View at Google Scholar · View at Scopus
  65. H. Kitoh, T. Kitakoji, H. Tsuchiya et al., “Transplantation of marrow-derived mesenchymal stem cells and platelet-rich plasma during distraction osteogenesis—a preliminary result of three cases,” Bone, vol. 35, no. 4, pp. 892–898, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Ueda, Y. Yamada, R. Ozawa, and Y. Okazaki, “Clinical case reports of injectable tissue-engineered bone for alveolar augmentation with simultaneous implant placement,” International Journal of Periodontics and Restorative Dentistry, vol. 25, no. 2, pp. 129–137, 2005. View at Google Scholar · View at Scopus
  67. D. Marsh, “Concepts of fracture union, delayed union, and nonunion,” Clinical Orthopaedics and Related Research, vol. 355, supplement, pp. S22–S30, 1998. View at Google Scholar · View at Scopus
  68. T. A. Einhorn, “Enhancement of fracture-healing,” Journal of Bone and Joint Surgery A, vol. 77, no. 6, pp. 940–956, 1995. View at Google Scholar · View at Scopus
  69. R. Salama and S. L. Weissman, “The clinical use of combined xenografts of bone and autologous red marrow. A preliminary report,” Journal of Bone and Joint Surgery B, vol. 60, no. 1, pp. 111–115, 1978. View at Google Scholar · View at Scopus
  70. J. F. Connolly, R. Guse, J. Tiedeman, and R. Dehne, “Autologous marrow injection as a substitute for operative grafting of tibial nonunions,” Clinical Orthopaedics and Related Research, no. 266, pp. 259–270, 1991. View at Google Scholar · View at Scopus
  71. J. F. Connolly, “Injectable bone marrow preparations to stimulate osteogenic repair,” Clinical Orthopaedics and Related Research, no. 313, pp. 8–18, 1995. View at Google Scholar · View at Scopus
  72. N. K. Garg, S. Gaur, and S. Sharma, “Percutaneous autogenous bone marrow grafting in 20 cases of ununited fracture,” Acta Orthopaedica Scandinavica, vol. 64, no. 6, pp. 671–672, 1993. View at Google Scholar · View at Scopus
  73. A. Goel, S. S. Sangwan, R. C. Siwach, and A. M. Ali, “Percutaneous bone marrow grafting for the treatment of tibial non-union,” Injury, vol. 36, no. 1, pp. 203–206, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Maneerit, S. Meknavin, and S. Hanpanitkitkan, “Percutaneous versus open bone grafting in the treatment of tibial fractures: a randomized prospective trial,” Journal of the Medical Association of Thailand, vol. 87, no. 9, pp. 1034–1040, 2004. View at Google Scholar · View at Scopus
  75. S. Wakitani, M. Nawata, K. Tensho, T. Okabe, H. Machida, and H. Ohgushi, “Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mesenchymal cell transplantation: three case reports involving nine defects in five knees,” Journal of Tissue Engineering and Regenerative Medicine, vol. 1, no. 1, pp. 74–79, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Wakitani, K. Imoto, T. Yamamoto, M. Saito, N. Murata, and M. Yoneda, “Human autologous culture expanded bone marrow-mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees,” Osteoarthritis and Cartilage, vol. 10, no. 3, pp. 199–206, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. K. Le Blanc, C. Götherström, O. Ringdén et al., “Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta,” Transplantation, vol. 79, no. 11, pp. 1607–1614, 2005. View at Publisher · View at Google Scholar
  78. E. M. Horwitz, P. L. Gordon, W. K. K. Koo et al., “Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 13, pp. 8932–8937, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. D. C. Flanigan, J. D. Harris, T. Q. Trinh, R. A. Siston, and R. H. Brophy, “Prevalence of chondral defects in athletes' knees—a systematic review,” Medicine & Science in Sports & Exercise, vol. 42, no. 10, pp. 1795–1801, 2010. View at Google Scholar
  80. B. P. O'Hara, J. P. G. Urban, and A. Maroudas, “Influence of cyclic loading on the nutrition of articular cartilage,” Annals of the Rheumatic Diseases, vol. 49, no. 7, pp. 536–539, 1990. View at Google Scholar · View at Scopus
  81. A. Bedi, B. T. Feeley, and R. J. Williams 3rd., “Management of articular cartilage defects of the knee,” The Journal of Bone and Joint Surgery A, vol. 92, no. 4, pp. 994–1009, 2010. View at Publisher · View at Google Scholar
  82. M. Brittberg, “Autologous chondrocyte implantation-Technique and long-term follow-up,” Injury, vol. 39, supplement 1, pp. 40–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. T. Minas, “Autologous chondrocyte implantation for focal chondral defects of the knee,” Clinical Orthopaedics and Related Research, no. 391, supplement, pp. S349–S361, 2001. View at Google Scholar · View at Scopus
  84. U. Horas, D. Pelinkovic, G. Herr, T. Aigner, and R. Schnettler, “Autologous chondrocyte implantation and osteochondral cylinder transplantation in cartilage repair of the knee joint. A prospective, comparative trial,” Journal of Bone and Joint Surgery A, vol. 85, no. 2, pp. 185–192, 2003. View at Google Scholar · View at Scopus
  85. C. Erggelet, P. C. Kreuz, E. H. Mrosek et al., “Autologous chondrocyte implantation versus ACI using 3D-bioresorbable graft for the treatment of large full-thickness cartilage lesions of the knee,” Archives of Orthopaedic and Trauma Surgery, pp. 1–8, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. P. C. Kreuz, S. Müller, C. Ossendorf, C. Kaps, and C. Erggelet, “Treatment of focal degenerative cartilage defects with polymer-based autologous chondrocyte grafts: four-year clinical results,” Arthritis Research and Therapy, vol. 11, no. 2, article R33, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. C. Ossendorf, C. Kaps, P. C. Kreuz, G. R. Burmester, M. Sittinger, and C. Erggelet, “Treatment of posttraumatic and focal osteoarthritic cartilage defects of the knee with autologous polymer-based three-dimensional chondrocyte grafts: 2-year clinical results,” Arthritis Research and Therapy, vol. 9, article R41, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Manfredini, F. Zerbinati, A. Gildone, and R. Faccini, “Autologous chondrocyte implantation: a comparison between an open periosteal-covered and an arthroscopic matrix-guided technique,” Acta Orthopaedica Belgica, vol. 73, no. 2, pp. 207–218, 2007. View at Google Scholar · View at Scopus
  89. B. A. Ashton, T. D. Allen, C. R. Howlett, C. C. Eaglesom, A. Hattori, and M. Owen, “Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vivo,” Clinical Orthopaedics and Related Research, no. 151, pp. 294–307, 1980. View at Google Scholar · View at Scopus
  90. R. Kuroda, A. Usas, S. Kubo et al., “Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells,” Arthritis and Rheumatism, vol. 54, no. 2, pp. 433–442, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. E. G. Meyer, C. T. Buckley, S. D. Thorpe, and D. J. Kelly, “Low oxygen tension is a more potent promoter of chondrogenic differentiation than dynamic compression,” Journal of Biomechanics, vol. 43, no. 13, pp. 2516–2523, 2010. View at Publisher · View at Google Scholar
  92. T. Vinardell, S. D. Thorpe, C. T. Buckley, and D. J. Kelly, “Chondrogenesis and integration of mesenchymal stem cells within an in vitro cartilage defect repair model,” Annals of Biomedical Engineering, vol. 37, no. 12, pp. 2556–2565, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Wakitani, T. Mitsuoka, N. Nakamura, Y. Toritsuka, Y. Nakamura, and S. Horibe, “Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: two case reports,” Cell Transplantation, vol. 13, no. 5, pp. 595–600, 2004. View at Google Scholar · View at Scopus
  94. L. L. Black, J. Gaynor, D. Gahring et al., “Effect of adipose-derived mesenchymal stem and regenerative cells on lameness in dogs with chronic osteoarthritis of the coxofemoral joints: a randomized, double-blinded, multicenter, controlled trial,” Veterinary Therapeutics, vol. 8, no. 4, pp. 272–284, 2007. View at Google Scholar · View at Scopus
  95. J. M. Murphy, D. J. Fink, E. B. Hunziker, and F. P. Barry, “Stem cell therapy in a caprine model of osteoarthritis,” Arthritis and Rheumatism, vol. 48, no. 12, pp. 3464–3474, 2003. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Erices, P. Conget, and J. J. Minguell, “Mesenchymal progenitor cells in human umbilical cord blood,” British Journal of Haematology, vol. 109, no. 1, pp. 235–242, 2000. View at Publisher · View at Google Scholar · View at Scopus
  97. O. K. Lee, T. K. Kuo, W.-M. Chen, K.-D. Lee, S.-L. Hsieh, and T.-H. Chen, “Isolation of multipotent mesenchymal stem cells from umbilical cord blood,” Blood, vol. 103, no. 5, pp. 1669–1675, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Lee, C. K. Chan, N. Patil, and S. B. Goodman, “Cell therapy for bone regeneration-bench to bedside,” Journal of Biomedical Materials Research - Part B Applied Biomaterials, vol. 89, no. 1, pp. 252–263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. P. Hernigou, F. Bernaudin, P. Reinert, M. Kuentz, and J. P. Vernant, “Bone-marrow transplantation in sickle-cell disease. Effect on osteonecrosis: a case report with a four-year follow-up,” Journal of Bone and Joint Surgery A, vol. 79, no. 11, pp. 1726–1730, 1997. View at Google Scholar · View at Scopus
  100. P. Hernigou and F. Beaujean, “Treatment of osteonecrosis with autologous bone marrow grafting,” Clinical Orthopaedics and Related Research, no. 405, pp. 14–23, 2002. View at Google Scholar · View at Scopus
  101. W. A. Cabral, S. Milgrom, A. D. Letocha, E. Moriarty, and J. C. Marini, “Biochemical screening of type I collagen in osteogenesis imperfecta: detection of glycine substitutions in the amino end of the alpha chains requires supplementation by molecular analysis,” Journal of Medical Genetics, vol. 43, no. 8, pp. 685–690, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. A. Galicka, S. Wolczynski, and A. Gindzienski, “Comparative studies of osteoblast and fibroblast type I collagen in a patient with osteogenesis imperfecta type IV,” Journal of Pathology, vol. 196, no. 2, pp. 235–237, 2002. View at Publisher · View at Google Scholar · View at Scopus
  103. A. P. Sarafova, H. Choi, A. Forlino et al., “Three novel type I collagen mutations in osteogenesis imperfecta type IV probands are associated with discrepancies between electrophoretic migration of osteoblast and fibroblast collagen,” Human Mutation, vol. 11, no. 5, pp. 395–403, 1998. View at Publisher · View at Google Scholar · View at Scopus
  104. J. R. Shapiro and P. D. Sponsellor, “Osteogenesis imperfecta: questions and answers,” Current Opinion in Pediatrics, vol. 21, no. 6, pp. 709–716, 2009. View at Publisher · View at Google Scholar
  105. F. H. Glorieux, N. J. Bishop, H. Plotkin, G. Chabot, G. Lanoue, and R. Travers, “Cyclic administration of pamidronate in children with severe osteogenesis imperfecta,” New England Journal of Medicine, vol. 339, no. 14, pp. 947–952, 1998. View at Publisher · View at Google Scholar · View at Scopus
  106. E. J. A. Roldán, T. Pasqualini, and L. Plantalech, “Bisphosphonates in children with osteogenesis imperfecta may improve bone mineralization but not bone strength. Report of two patients,” Journal of Pediatric Endocrinology and Metabolism, vol. 12, no. 4, pp. 555–559, 1999. View at Google Scholar · View at Scopus
  107. R. F. Pereira, M. D. O'Hara, A. V. Laptev et al., “Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 3, pp. 1142–1147, 1998. View at Publisher · View at Google Scholar · View at Scopus
  108. E. M. Horwitz, D. J. Prockop, P. L. Gordon et al., “Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta,” Blood, vol. 97, no. 5, pp. 1227–1231, 2001. View at Publisher · View at Google Scholar · View at Scopus
  109. R. G. Young, D. L. Butler, W. Weber, A. I. Caplan, S. L. Gordon, and D. J. Fink, “Use of mesenchymal stem cells in a collagen matrix for achilles tendon repair,” Journal of Orthopaedic Research, vol. 16, no. 4, pp. 406–413, 1998. View at Publisher · View at Google Scholar · View at Scopus
  110. A. Crovace, L. Lacitignola, R. deSiena, G. Rossi, and E. Francioso, “Cell therapy for tendon repair in horses: an experimental study,” Veterinary Research Communications, vol. 31, supplement 1, pp. 281–283, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. H. W. Ouyang, J. C. H. Goh, A. Thambyah, S. H. Teoh, and E. H. Lee, “Knitted poly-lactide-co-glycolidescaffold loaded with bone marrow stromal cells in repair and regeneration of rabbit achilles tendon,” Tissue Engineering, vol. 9, no. 3, pp. 431–439, 2003. View at Publisher · View at Google Scholar · View at Scopus
  112. M. T. Harris, D. L. Butler, G. P. Boivin, J. B. Florer, E. J. Schantz, and R. J. Wenstrup, “Mesenchymal stem cells used for rabbit tendon repair can form ectopic bone and express alkaline phosphatase activity in constructs,” Journal of Orthopaedic Research, vol. 22, no. 5, pp. 998–1003, 2004. View at Publisher · View at Google Scholar · View at Scopus
  113. H. Schliephake, H. A. Weich, C. Dullin, R. Gruber, and S. Frahse, “Mandibular bone repair by implantation of rhBMP-2 in a slow release carrier of polylactic acid-an experimental study in rats,” Biomaterials, vol. 29, no. 1, pp. 103–110, 2008. View at Publisher · View at Google Scholar · View at Scopus
  114. J. Luo et al., “Gene therapy for bone regeneration,” Current Gene Therapy, vol. 5, no. 2, pp. 167–179, 2005. View at Google Scholar · View at Scopus
  115. B. Breyer, W. Jiang, H. Cheng et al., “Adenoviral vector-mediated gene transfer for human gene therapy,” Current gene therapy, vol. 1, no. 2, pp. 149–162, 2001. View at Google Scholar · View at Scopus
  116. S. S. Ghosh, P. Gopinath, and A. Ramesh, “Adenoviral vectors: a promising tool for gene therapy,” Applied Biochemistry and Biotechnology, vol. 133, no. 1, pp. 9–29, 2006. View at Publisher · View at Google Scholar · View at Scopus
  117. A. W. A. Baltzer, C. Lattermann, J. D. Whalen et al., “Genetic enhancement of fracture repair: healing of an experimental segmental defect by adenoviral transfer of the BMP-2 gene,” Gene Therapy, vol. 7, no. 9, pp. 734–739, 2000. View at Publisher · View at Google Scholar · View at Scopus
  118. J. Park, J. Ries, K. Gelse et al., “Bone regeneration in critical size defects by cell-mediated BMP-2 gene transfer: a comparison of adenoviral vectors and liposomes,” Gene Therapy, vol. 10, no. 13, pp. 1089–1098, 2003. View at Publisher · View at Google Scholar · View at Scopus
  119. N. Tang, W.-X. Song, J. Luo et al., “BMP-9-induced osteogenic differentiation of mesenchymal progenitors requires functional canonical Wnt/β-catenin signalling,” Journal of Cellular and Molecular Medicine, vol. 13, no. 8 B, pp. 2448–2464, 2009. View at Publisher · View at Google Scholar
  120. M. Lind and C. Bünger, “Orthopaedic applications of gene therapy,” International Orthopaedics, vol. 29, no. 4, pp. 205–209, 2005. View at Publisher · View at Google Scholar · View at Scopus
  121. I. V. Balyasnikova, R. Franco-Gou, J. Michael Mathis, and M. S. Lesniak, “Genetic modification of mesenchymal stem cells to express a single-chain antibody against EGFRvIII on the cell surface,” Journal of Tissue Engineering and Regenerative Medicine, vol. 4, no. 4, pp. 247–258, 2010. View at Publisher · View at Google Scholar
  122. G. P. Duffy, S. D'Arcy, T. Ahsan, R. M. Nerem, T. O'Brien, and F. Barry, “Mesenchymal stem cells overexpressing ephrin-B2 rapidly adopt an early endothelial phenotype with simultaneous reduction of osteogenic potential,” Tissue Engineering—Part A, vol. 16, no. 9, pp. 2755–2768, 2010. View at Publisher · View at Google Scholar
  123. D. Sheyn, G. Pelled, Y. Zilberman et al., “Nonvirally engineered porcine adipose tissue-derived stem cells: use in posterior spinal fusion,” Stem Cells, vol. 26, no. 4, pp. 1056–1064, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. Y. Gheisari, M. Soleimani, K. Azadmanesh, and S. Zeinali, “Multipotent mesenchymal stromal cells: optimization and comparison of five cationic polymer-based gene delivery methods,” Cytotherapy, vol. 10, no. 8, pp. 815–823, 2008. View at Publisher · View at Google Scholar · View at Scopus
  125. A. Hoffmann, G. Pelled, G. Turgeman et al., “Neotendon formation induced by manipulation of the Smad8 signalling pathway in mesenchymal stem cells,” Journal of Clinical Investigation, vol. 116, no. 4, pp. 940–952, 2006. View at Publisher · View at Google Scholar · View at Scopus
  126. L. B. Jacobsen, S. A. Calvin, K. E. Colvin, and M. Wright, “FuGENE 6 transfection reagent: the gentle power,” Methods, vol. 33, no. 2, pp. 104–112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  127. A. Hoffmann, S. Czichos, C. Kaps et al., “The T-box transcription factor Brachyury mediates cartilage development in mesenchymal stem cell line C3H10T1/2,” Journal of Cell Science, vol. 115, part 4, pp. 769–781, 2002. View at Google Scholar · View at Scopus
  128. B. J. Slater, M. D. Kwan, D. M. Gupta, N. J. Panetta, and M. T. Longaker, “Mesenchymal cells for skeletal tissue engineering,” Expert Opinion on Biological Therapy, vol. 8, no. 7, pp. 885–893, 2008. View at Publisher · View at Google Scholar · View at Scopus