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The Scientific World Journal
Volume 2012, Article ID 793823, 14 pages
http://dx.doi.org/10.1100/2012/793823
Review Article

Mechanisms Underlying the Osteo- and Adipo-Differentiation of Human Mesenchymal Stem Cells

Department of Natural Sciences, Bonn-Rhine-Sieg University of Applied Sciences, von-Liebig-Straße 20, 53359 Rheinbach, Germany

Received 31 August 2011; Accepted 15 October 2011

Academic Editors: J.-T. Cheng, J. M. Nesland, and V. Pistoia

Copyright © 2012 Yu Zhang 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. J. A. Thomson, J. Itskovitz-Eldor, S. S. Shapiro et al., “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Google Scholar
  2. 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
  3. D. C. Ding, W. C. Shyu, and S. Z. Lin, “Mesenchymal stem cells,” Cell Transplant, vol. 20, pp. 5–14, 2011. View at Google Scholar
  4. M. Ogawa, “Differentiation and proliferation of hematopoietic stem cells,” Blood, vol. 81, no. 11, pp. 2844–2853, 1993. View at Google Scholar · View at Scopus
  5. D. Metcalf, “On hematopoietic stem cell fate,” Immunity, vol. 26, no. 6, pp. 669–673, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. 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 PubMed · View at Scopus
  8. M. Wernig, A. Meissner, R. Foreman et al., “In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state,” Nature, vol. 448, no. 7151, pp. 318–324, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. 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 PubMed · View at Scopus
  10. J. B. Kim, B. Greber, M. J. Arazo-Bravo et al., “Direct reprogramming of human neural stem cells by OCT4,” Nature, vol. 461, no. 7264, pp. 649–653, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. S. Eminli, A. Foudi, M. Stadtfeld et al., “Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells,” Nature Genetics, vol. 41, no. 9, pp. 968–976, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. P. S. Knoepfler, “Deconstructing stem cell tumorigenicity: a roadmap to safe regenerative medicine,” Stem Cells, vol. 27, no. 5, pp. 1050–1056, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. 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 PubMed
  14. A. J. Nauta and W. E. Fibbe, “Immunomodulatory properties of mesenchymal stromal cells,” Blood, vol. 110, no. 10, pp. 3499–3506, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. E. B. Maria, L. Franco, and E. F. Willem, “Mesenchymal stromal cells: a novel treatment modality for tissue repair,” Annals of the New York Academy of Sciences, vol. 1176, pp. 101–117, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. H. K. Salem and C. Thiemermann, “Mesenchymal stromal cells: current understanding and clinical status,” Stem Cells, vol. 28, no. 3, pp. 585–596, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. L. Jackson, D. Jones, P. Scotting, and V. Sottile, “Adult mesenchymal stem cells: differentiation potential and therapeutic applications,” Journal of Postgraduate Medicine, vol. 53, no. 2, pp. 121–127, 2007. View at Google Scholar · View at Scopus
  18. M. Breitbach, T. Bostani, W. Roell et al., “Potential risks of bone marrow cell transplantation into infarcted hearts,” Blood, vol. 110, no. 4, pp. 1362–1369, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. P. Bianco, P. G. Robey, and P. J. Simmons, “Mesenchymal stem cells: revisiting history, concepts, and assays,” Cell Stem Cell, vol. 2, no. 4, pp. 313–319, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. Y. Jiang, B. N. Jahagirdar, R. L. Reinhardt et al., “Pluripotency of mesenchymal stem cells derived from adult marrow,” Nature, vol. 418, no. 7146, pp. 41–49, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. W. Wagner and A. D. Ho, “Mesenchymal stem cell preparations—comparing apples and oranges,” Stem Cell Reviews, vol. 3, no. 4, pp. 239–248, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. Y. Zhang and E. Tobiasch, “The role of purinergic receptors in stem cells in their derived consecutive tissues,” in Adult Stem Cell Standardization, P. di Nardo, Ed., pp. 73–98, River Publishers, 2011. View at Google Scholar
  23. 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
  24. M. Kassem and B. M. Abdallah, “Human bone-marrow-derived mesenchymal stem cells: biological characteristics and potential role in therapy of degenerative diseases,” Cell and Tissue Research, vol. 331, no. 1, pp. 157–163, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. 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 PubMed · View at Scopus
  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 PubMed · View at Scopus
  27. U. Nöth, A. M. Osyczka, R. Tuli, N. J. Hickok, K. G. Danielson, and R. S. Tuan, “Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells,” Journal of Orthopaedic Research, vol. 20, no. 5, pp. 1060–1069, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. E. Tobiasch, “Adult human mesenchymal stem cells as source for future tissue engineering,” in Forschungsspitzen und Spitzenforschung, C. Zacharias, K. W. Ter Horst, K.-U. Witt et al., Eds., Springverlag, 2008. View at Google Scholar
  29. 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 PubMed · View at Scopus
  30. G. Kögler, S. Sensken, J. A. Airey et al., “A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential,” Journal of Experimental Medicine, vol. 200, no. 2, pp. 123–135, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. R. Hass, C. Kasper, S. Bohm, and R. Jacobs, “Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC,” Cell Communication and Signaling, vol. 9, p. 12, 2011. View at Publisher · View at Google Scholar · View at PubMed
  32. K. Mareschi, E. Biasin, W. Piacibello, M. Aglietta, E. Madon, and F. Fagioli, “Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood,” Haematologica, vol. 86, no. 10, pp. 1099–1100, 2001. 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 PubMed · View at Scopus
  34. N. Zippel, M. Schulze, and E. Tobiasch, “Biomaterials and mesenchymal stem cells for regenerative medicine,” Recent Patents on Biotechnology, vol. 4, no. 1, pp. 1–22, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Zippel, C. A. Limbach, and N. Ratajski, “Purinergic receptorsinfluence the differentiation of human mesenchymal stem cells,” Stem Cells and Development. In press. View at Publisher · View at Google Scholar · View at PubMed
  36. G. Brooke, H. Tong, J. P. Levesque, and K. Atkinson, “Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta,” Stem Cells and Development, vol. 17, no. 5, pp. 929–940, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. S. Barlow, G. Brooke, K. Chatterjee et al., “Comparison of human placenta- and bone marrow-derived multipotent mesenchymal stem cells,” Stem Cells and Development, vol. 17, no. 6, pp. 1095–1107, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. S. Kern, H. Eichler, J. Stoeve, H. Klüter, and K. Bieback, “Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue,” Stem Cells, vol. 24, no. 5, pp. 1294–1301, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. P. Shetty, K. Cooper, and C. Viswanathan, “Comparison of proliferative and multilineage differentiation potentials of cord matrix, cord blood, and bone marrow mesenchymal stem cells,” Asian Journal of Transfusion Science, vol. 4, pp. 14–24, 2010. View at Google Scholar
  40. D. Baksh, L. Song, and R. S. Tuan, “Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy,” Journal of Cellular and Molecular Medicine, vol. 8, no. 3, pp. 301–316, 2004. View at Google Scholar · View at Scopus
  41. L. L. Lu, Y. J. Liu, S. G. Yang et al., “Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials,” Haematologica, vol. 91, no. 8, pp. 1017–1028, 2006. View at Google Scholar · View at Scopus
  42. L. Peng, Z. Jia, X. Yin et al., “Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue,” Stem Cells and Development, vol. 17, no. 4, pp. 761–773, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. B. M. Schipper, K. G. Marra, W. Zhang, A. D. Donnenberg, and J. P. Rubin, “Regional anatomic and age effects on cell function of human adipose-derived stem cells,” Annals of Plastic Surgery, vol. 60, no. 5, pp. 538–544, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. Y. Y. Shi, R. P. Nacamuli, A. Salim, and M. T. Longaker, “The osteogenic potential of adipose-derived mesenchmal cells is maintained with aging,” Plastic and Reconstructive Surgery, vol. 116, no. 6, pp. 1686–1696, 2005. View at Publisher · View at Google Scholar
  45. V. van Harmelen, K. Röhrig, and H. Hauner, “Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjects,” Metabolism, vol. 53, no. 5, pp. 632–637, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Li, X. A. Zhang, H. Wang et al., “Comparative proteomic analysis of mesenchymal stem cells derived from human bone marrow, umbilical cord, and placenta: implication in the migration,” Proteomics, vol. 9, no. 1, pp. 20–30, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. D. Baksh, R. Yao, and R. S. Tuan, “Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow,” Stem Cells, vol. 25, no. 6, pp. 1384–1392, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. T. Deuse, M. Stubbendorff, K. Tang-Quan et al., “Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells,” Cell Transplantation, vol. 20, no. 5, pp. 655–667, 2011. View at Publisher · View at Google Scholar · View at PubMed
  49. Y. Kitagawa, M. Kobori, K. Toriyama, Y. Kamei, and S. Torii, “History of discovery of human adipose-derived stem cells and their clinical application,” Japanese Journal of Plastic and Reconstructive Surgery, vol. 49, no. 10, pp. 1097–1104, 2006. View at Google Scholar · View at Scopus
  50. D. A. De Ugarte, K. Morizono, A. Elbarbary et al., “Comparison of multi-lineage cells from human adipose tissue and bone marrow,” Cells Tissues Organs, vol. 174, no. 3, pp. 101–109, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. R. H. Lee, B. Kim, I. Choi et al., “Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue,” Cellular Physiology and Biochemistry, vol. 14, no. 4-6, pp. 311–324, 2004. View at Publisher · View at Google Scholar · View at PubMed
  52. D. A. De Ugarte, Z. Alfonso, P. A. Zuk et al., “Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow,” Immunology Letters, vol. 89, no. 2-3, pp. 267–270, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. N. Ahmadian kia, A. R. Bahrami, M. Ebrahimi et al., “Comparative analysis of chemokine receptor's expression in mesenchymal stem cells derived from human bone marrow and adipose tissue,” Journal of Molecular Neuroscience, vol. 4, pp. 178–185, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. 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 PubMed · View at Scopus
  55. S. M. Mueller and J. Glowacki, “Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges,” Journal of Cellular Biochemistry, vol. 82, no. 4, pp. 583–590, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. K. Stenderup, J. Justesen, C. Clausen, and M. Kassem, “Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells,” Bone, vol. 33, no. 6, pp. 919–926, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. J. K. Fraser, I. Wulur, Z. Alfonso, and M. H. Hedrick, “Fat tissue: an underappreciated source of stem cells for biotechnology,” Trends in Biotechnology, vol. 24, no. 4, pp. 150–154, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. G. Ferrari, G. Cusella-De Angelis, M. Coletta et al., “Muscle regeneration by bone marrow-derived myogenic progenitors,” Science, vol. 279, no. 5356, pp. 1528–1530, 1998. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Gronthos, D. M. Franklin, H. A. Leddy et al., “Surface protein characterization of human adipose tissue-derived stromal cells,” Journal of Cellular Physiology, vol. 189, no. 1, pp. 54–63, 2001. View at Publisher · View at Google Scholar · View at PubMed
  60. S. Wakitani, T. Saito, and A. I. Caplan, “Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine,” Muscle and Nerve, vol. 18, no. 12, pp. 1417–1426, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. S. Heydarkhan-Hagvall, K. Schenke-Layland, J. Q. Yang et al., “Human adipose stem cells: a potential cell source for cardiovascular tissue engineering,” Cells Tissues Organs, vol. 187, no. 4, pp. 263–274, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. W. C. Lee, J. P. Rubin, and K. G. Marra, “Regulation of α-smooth muscle actin protein expression in adipose-derived stem cells,” Cells Tissues Organs, vol. 183, no. 2, pp. 80–86, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. L. V. Rodríguez, Z. Alfonso, R. Zhang, J. Leung, B. Wu, and L. J. Ignarro, “Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 32, pp. 12167–12172, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. V. Planat-Bénard, C. Menard, M. André et al., “Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells,” Circulation Research, vol. 94, no. 2, pp. 223–229, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. E. Pacary, H. Legros, S. Valable et al., “Synergistic effects of CoCl(2) and ROCK inhibition on mesenchymal stem cell differentiation into neuron-like cells,” Journal of Cell Science, vol. 119, no. 13, pp. 2667–2678, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. A. Scuteri, M. Miloso, D. Foudah, M. Orciani, G. Cavaletti, and G. Tredici, “Mesenchymal stem cells neuronal differentiation ability: a real perspective for nervous system repair?” Current Stem Cell Research and Therapy, vol. 6, no. 2, pp. 82–92, 2011. View at Publisher · View at Google Scholar
  67. G. C. Kopen, D. J. Prockop, and D. G. Phinney, “Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 19, pp. 10711–10716, 1999. View at Publisher · View at Google Scholar · View at Scopus
  68. M. J. Seo, S. Y. Suh, Y. C. Bae, and J. S. Jung, “Differentiation of human adipose stromal cells into hepatic lineage In vitro and in vivo,” Biochemical and Biophysical Research Communications, vol. 328, no. 1, pp. 258–264, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. B. Pournasr, M. Mohamadnejad, M. Bagheri et al., “In vitro differentiation of human bone marrow mesenchymal stem cells into hepatocyte-like cells,” Archives Of Iranian Medicine, pp. 244–249, 14. View at Google Scholar
  70. M. Wosnitza, K. Hemmrich, A. Groger, S. Gräber, and N. Pallua, “Plasticity of human adipose stem cells to perform adipogenic and endothelial differentiation,” Differentiation, vol. 75, no. 1, pp. 12–23, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  71. C. Limbert and J. Seufert, “In vitro (re)programming of human bone marrow stromal cells toward insulin-producing phenotypes,” Pediatric Diabetes, vol. 10, no. 6, pp. 413–419, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. O. Karnieli, Y. Izhar-Prato, S. Bulvik, and S. Efrat, “Generation of insulin-producing cells from human bone marrow mesenchymal stem cells by genetic manipulation,” Stem Cells, vol. 25, no. 11, pp. 2837–2844, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. W. B. Slayton and G. J. Spangrude, “Adult stem cell plasticity,” in Adult Stem Cells, K. Turksen, Ed., pp. 1–3, Humana Press, NJ, USA, 2004. View at Google Scholar
  74. F. Guilak, D. M. Cohen, B. T. Estes, J. M. Gimble, W. Liedtke, and C. S. Chen, “Control of stem cell fate by physical interactions with the extracellular matrix,” Cell Stem Cell, vol. 5, no. 1, pp. 17–26, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  75. A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, “Matrix elasticity directs stem cell lineage specification,” Cell, vol. 126, no. 4, pp. 677–689, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. D. E. Discher, D. J. Mooney, and P. W. Zandstra, “Growth factors, matrices, and forces combine and control stem cells,” Science, vol. 324, no. 5935, pp. 1673–1677, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. R. S. Tuan, G. Boland, and R. Tuli, “Adult mesenchymal stem cells and cell-based tissue engineering,” Arthritis Research and Therapy, vol. 5, no. 1, pp. 32–45, 2003. View at Google Scholar · View at Scopus
  78. N. Tremain, J. Korkko, D. Ibberson, G. C. Kopen, C. DiGirolamo, and D. G. Phinney, “MicroSAGE analysis of 2,353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAS of multiple cell lineages,” Stem Cells, vol. 19, no. 5, pp. 408–418, 2001. View at Google Scholar · View at Scopus
  79. G. Yourek, S. M. McCormick, J. J. Mao, and G. C. Reilly, “Shear stress induces osteogenic differentiation of human mesenchymal stem cells,” Regenerative Medicine, vol. 5, no. 5, pp. 713–724, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. J. H. W. Jansen, O. P. Van Der Jagt, B. J. Punt et al., “Stimulation of osteogenic differentiation in human osteoprogenitor cells by pulsed electromagnetic fields: an in vitro study,” BMC Musculoskeletal Disorders, vol. 11, pp. 188–199, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. R. Hess, T. Douglas, K. A. Myers et al., “Hydrostatic pressure stimulation of human mesenchymal stem cells seeded on collagen-based artificial extracellular matrices,” Journal of Biomechanical Engineering, vol. 132, no. 2, pp. 1–6, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  82. M. Igarashi, N. Kamiya, M. Hasegawa, T. Kasuya, T. Takahashi, and M. Takagi, “Inductive effects of dexamethasone on the gene expression of Cbfa1, Osterix and bone matrix proteins during differentiation of cultured primary rat osteoblasts,” Journal of Molecular Histology, vol. 35, no. 1, pp. 3–10, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Gupta, D. T. Leong, H. F. Bai, S. B. Singh, T. C. Lim, and D. W. Hutmacher, “Osteomaturation of adipose-derived stem cells required the combined action of vitamin D3, beta-glycerophosphate, and ascorbic acid,” Biochemical and Biophysical Research Communications, vol. 362, pp. 17–24, 2007. View at Google Scholar
  84. M. T. Tsai, W. J. Li, R. S. Tuan, and W. H. Chang, “Modulation of osteogenesis in human mesenchymal stem cells by specific pulsed electromagnetic field stimulation,” Journal of Orthopaedic Research, vol. 27, no. 9, pp. 1169–1174, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. P. Diniz, K. Shomura, K. Soejima, and G. Ito, “Effects of pulsed electromagnetic field (PEMF) stimulation on bone tissue like formation are dependent on the maturation stages of the osteoblasts,” Bioelectromagnetics, vol. 23, no. 5, pp. 398–405, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. M. T. Tsai, W. H. S. Chang, K. Chang, R. J. Hou, and T. W. Wu, “Pulsed electromagnetic fields affect osteoblast proliferation and differentiation in bone tissue engineering,” Bioelectromagnetics, vol. 28, no. 7, pp. 519–528, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  87. L. Fassina, L. Visai, F. Benazzo et al., “Effects of electromagnetic stimulation on calcified matrix production by SAOS-2 cells over a polyurethane porous scaffold,” Tissue Engineering, vol. 12, no. 7, pp. 1985–1999, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. R. M. Salasznyk, W. A. Williams, A. Boskey, A. Batorsky, and G. E. Plopper, “Adhesion to vitronectin and collagen I promotes osteogenic differentiation of human mesenchymal stem cells,” Journal of Biomedicine and Biotechnology, vol. 2004, no. 1, pp. 24–34, 2004. View at Publisher · View at Google Scholar · View at PubMed
  89. M. Mizuno and Y. Kuboki, “Osteoblast-related gene expression of bone marrow cells during the osteoblastic differentiation induced by type I collagen,” Journal of Biochemistry, vol. 129, no. 1, pp. 133–138, 2001. View at Google Scholar · View at Scopus
  90. A. K. Kundu and A. J. Putnam, “Vitronectin and collagen I differentially regulate osteogenesis in mesenchymal stem cells,” Biochemical and Biophysical Research Communications, vol. 347, no. 1, pp. 347–357, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. S. Vukicevic, H. K. Kleinman, F. P. Luyten, A. B. Roberts, N. S. Roche, and A. H. Reddi, “Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components,” Experimental Cell Research, vol. 202, no. 1, pp. 1–8, 1992. View at Publisher · View at Google Scholar · View at Scopus
  92. M. B. Eslaminejad, F. Bagheri, and E. Zomorodian, “Matrigel Enhances In vitro Bone Differentiation of Human Marrow-derived Mesenchymal Stem Cells,” Iranian Journal of Basic Medical Sciences, vol. 13, pp. 187–194, 2009. View at Google Scholar
  93. R. D. Sumanasinghe, S. H. Bernacki, and E. G. Loboa, “Osteogenic differentiation of human mesenchymal stem cells in collagen matrices: effect of uniaxial cyclic tensile strain on bone morphogenetic protein (BMP-2) mRNA expression,” Tissue Engineering, vol. 12, no. 12, pp. 3459–3465, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  94. J. F. Heubach, E. M. Graf, J. Leutheuser et al., “Electrophysiological properties of human mesenchymal stem cells,” Journal of Physiology, vol. 554, no. 3, pp. 659–672, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  95. T. Cho, J. H. Bae, H. B. Choi et al., “Human neural stem cells: electrophysiological properties of voltage-gated ion channels,” NeuroReport, vol. 13, no. 11, pp. 1447–1452, 2002. View at Google Scholar · View at Scopus
  96. S. Konig, V. Hinard, S. Arnaudeau et al., “Membrane hyperpolarization triggers myogenin and myocyte enhancer factor-2 expression during human myoblast differentiation,” Journal of Biological Chemistry, vol. 279, no. 27, pp. 28187–28196, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  97. S. Sundelacruz, M. Levin, and D. L. Kaplan, “Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells,” PLoS ONE, vol. 3, no. 11, Article ID e3737, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  98. P. Ducy and G. Karsenty, “Genetic control of cell differentiation in the skeleton,” Current Opinion in Cell Biology, vol. 10, no. 5, pp. 614–619, 1998. View at Publisher · View at Google Scholar · View at Scopus
  99. K. S. Lee, H. J. Kim, Q. L. Li et al., “Runx2 is a common target of transforming growth factor β1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12,” Molecular and Cellular Biology, vol. 20, no. 23, pp. 8783–8792, 2000. View at Publisher · View at Google Scholar · View at Scopus
  100. M. H. Lee, Y. J. Kim, H. J. Kim et al., “BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-β1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression,” Journal of Biological Chemistry, vol. 278, no. 36, pp. 34387–34394, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  101. M. H. Lee, T. -G. Kwon, H. -S. Park, J. M. Wozney, and H.-M. Ryoo, “BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2,” Biochemical and Biophysical Research Communications, vol. 309, no. 3, pp. 689–694, 2003. View at Publisher · View at Google Scholar
  102. T. Gaur, C. J. Lengner, H. Hovhannisyan et al., “Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression,” Journal of Biological Chemistry, vol. 280, no. 39, pp. 33132–33140, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  103. H. Enomoto, T. Furuichi, A. Zanma et al., “Runx2 deficiency in chondrocytes causes adipogenic changes in vitro,” Journal of Cell Science, vol. 117, no. 3, pp. 417–425, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  104. T. Matsubara, K. Kida, A. Yamaguchi et al., “BMP2 regulates osterix through Msx2 and Runx2 during osteoblast differentiation,” Journal of Biological Chemistry, vol. 283, no. 43, pp. 29119–29125, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  105. S. I. Harada and G. A. Rodan, “Control of osteoblast function and regulation of bone mass,” Nature, vol. 423, no. 6937, pp. 349–355, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  106. T. Komori, “Regulation of osteoblast differentiation by transcription factors,” Journal of Cellular Biochemistry, vol. 99, no. 5, pp. 1233–1239, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  107. W. Liu, S. Toyosawa, T. Furuichi et al., “Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures,” Journal of Cell Biology, vol. 155, no. 1, pp. 157–166, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  108. K. Nakashima, X. Zhou, G. Kunkel et al., “The novel zinc finger-containing transcription factor Osterix is required for osteoblast differentiation and bone formation,” Cell, vol. 108, no. 1, pp. 17–29, 2002. View at Publisher · View at Google Scholar · View at Scopus
  109. J. E. Aubin and F. Liu, “The osteoblast lineage,” in Principles of Bone Biology, J. P. Bilezikian, L. G. Raisz, and G. A. Rodan, Eds., pp. 51–68, Academic, San Diego, calif, USA, 1996. View at Google Scholar
  110. D. Pavlin, S. B. Dove, R. Zadro, and J. Gluhak-Heinrich, “Mechanical loading stimulates differentiation of periodontal osteoblasts in a mouse osteoinduction model: effect on type I collagen and alkaline phosphatase genes,” Calcified Tissue International, vol. 67, no. 2, pp. 163–172, 2000. View at Google Scholar · View at Scopus
  111. D. Pavlin, R. Zadro, and J. Gluhak-Heinrich, “Temporal pattern of stimulation of osteoblast-associated genes during mechanically-induced osteogenesis in vivo: early responses of osteocalcin and type I collagen,” Connective Tissue Research, vol. 42, no. 2, pp. 135–148, 2001. View at Google Scholar · View at Scopus
  112. S. Yamasaki, T. Nakashima, A. Kawakami et al., “Cytokines regulate fibroblast-like synovial cell differentiation to adipocyte-like cells,” Rheumatology, vol. 43, no. 4, pp. 448–452, 2004. View at Publisher · View at Google Scholar · View at PubMed
  113. E. Tobiasch, “Differentiation potential of adult human mesenchymal stem cells,” in Stem Cell Engineering, G.M. Artmann, J. Hescheler, and S. Minger, Eds., Springer, 2010. View at Google Scholar
  114. A. E. Grigoriadis, J. N. M. Heersche, and J. E. Aubin, “Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bone-derived clonal cell population: effect of dexamethasone,” Journal of Cell Biology, vol. 106, no. 6, pp. 2139–2151, 1988. View at Google Scholar · View at Scopus
  115. J. M. Lehmann, J. M. Lenhard, B. B. Oliver, G. M. Ringold, and S. A. Kliewer, “Peroxisome proliferator-activated receptors α and γ are activated by indomethacin and other non-steroidal anti-inflammatory drugs,” Journal of Biological Chemistry, vol. 272, no. 6, pp. 3406–3410, 1997. View at Publisher · View at Google Scholar · View at Scopus
  116. S. Kim and N. Moustaid-Moussa, “Secretory, endocrine and autocrine/paracrine function of the adipocyte,” Journal of Nutrition, vol. 130, no. 12, pp. 3110–3115, 2000. View at Google Scholar · View at Scopus
  117. E. D. Rosen and O. A. MacDougald, “Adipocyte differentiation from the inside out,” Nature Reviews Molecular Cell Biology, vol. 7, no. 12, pp. 885–896, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  118. P. J. Smith, L. S. Wise, R. Berkowitz, C. Wan, and C. S. Rubin, “Insulin-like growth factor-I is an essential regulator of the differentiation of 3T3-L1 adipocytes,” Journal of Biological Chemistry, vol. 263, no. 19, pp. 9402–9408, 1988. View at Google Scholar · View at Scopus
  119. G. M. Leinninger, C. Backus, M. D. Uhler, S. I. Lentz, and E. L. Feldman, “Phosphatidylinositol 3-kinase and Akt effectors mediate insulin-like growth factor-I neuroprotection in dorsal root ganglia neurons,” FASEB Journal, vol. 18, no. 13, pp. 1544–1572, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  120. R. J. Southgate, C. R. Bruce, A. L. Carey et al., “PGC-1α gene expression is down-regulated by Akt-mediated phosphorylation and nuclear exclusion of FoxO1 in insulin-stimulated skeletal muscle,” FASEB Journal, vol. 19, no. 14, pp. 2072–2074, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  121. R. Menghini, V. Marchetti, M. Cardellini et al., “Phosphorylation of GATA2 by akt increases adipose tissue differentiation and reduces adipose tissue-related inflammation: a novel pathway linking obesity to atherosclerosis,” Circulation, vol. 111, no. 15, pp. 1946–1953, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  122. T. C. Otto and M. D. Lane, “Adipose development: from stem cell to adipocyte,” Critical Reviews in Biochemistry and Molecular Biology, vol. 40, no. 4, pp. 229–242, 2005. View at Publisher · View at Google Scholar · View at PubMed
  123. Y. Oishi, I. Manabe, K. Tobe et al., “Krüppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation,” Cell Metabolism, vol. 1, no. 1, pp. 27–39, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  124. E. D. Rosen, C. H. Hsu, X. Wang et al., “C/EBPα induces adipogenesis through PPARγ: a unified pathway,” Genes and Development, vol. 16, no. 1, pp. 22–26, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  125. E. D. Rosen, C. J. Walkey, P. Puigserver, and B. M. Spiegelman, “Transcriptional regulation of adipogenesis,” Genes and Development, vol. 14, no. 11, pp. 1293–1307, 2000. View at Google Scholar · View at Scopus
  126. Y. Tamori, J. Masugi, N. Nishino, and M. Kasuga, “Role of peroxisome proliferator-activated receptor-γ in maintenance of the characteristics of mature 3T3-L1 adipocytes,” Diabetes, vol. 51, no. 7, pp. 2045–2055, 2002. View at Google Scholar · View at Scopus
  127. Q. Tong, G. Dalgin, H. Xu, C. N. Ting, J. M. Leiden, and G. S. Hotamisligil, “Function of GATA transcription factors in preadipocyte-adipocyte transition,” Science, vol. 290, no. 5489, pp. 134–138, 2000. View at Publisher · View at Google Scholar · View at Scopus
  128. F. M. Gregoire, C. M. Smas, and H. S. Sul, “Understanding adipocyte differentiation,” Physiological Reviews, vol. 78, no. 3, pp. 783–809, 1998. View at Google Scholar · View at Scopus
  129. J. M. Gimble, S. Zvonic, Z. E. Floyd, M. Kassem, and M. E. Nuttall, “Playing with bone and fat,” Journal of Cellular Biochemistry, vol. 98, no. 2, pp. 251–266, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  130. J. N. Beresford, J. H. Bennett, C. Devlin, P. S. Leboy, and M. E. Owen, “Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures,” Journal of Cell Science, vol. 102, no. 2, pp. 341–351, 1992. View at Google Scholar · View at Scopus
  131. D. Falconi, K. Oizumi, and J. E. Aubin, “Leukemia inhibitory factor influences the fate choice of mesenchymal progenitor cells,” Stem Cells, vol. 25, no. 2, pp. 305–312, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  132. J. M. Gimble, C. Morgan, K. Kelly et al., “Bone morphogenetic proteins inhibit adipocyte differentiation by bone marrow stromal cells,” Journal of Cellular Biochemistry, vol. 58, no. 3, pp. 393–402, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  133. S. Kang, C. N. Bennett, I. Gerin, L. A. Rapp, K. D. Hankenson, and O. A. MacDougald, “Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein α and peroxisome proliferator-activated receptor γ,” Journal of Biological Chemistry, vol. 282, no. 19, pp. 14515–14524, 2007. View at Publisher · View at Google Scholar · View at PubMed
  134. B. M. Abdallah and M. Kassem, “New factors controlling the balance between osteoblastogenesis and adipogenesis,” Bone. In press. View at Publisher · View at Google Scholar · View at PubMed
  135. R. McBeath, D. M. Pirone, C. M. Nelson, K. Bhadriraju, and C. S. Chen, “Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment,” Developmental Cell, vol. 6, no. 4, pp. 483–495, 2004. View at Publisher · View at Google Scholar · View at Scopus
  136. B. A. J. Roelen and P. Ten Dijke, “Controlling mesenchymal stem cell differentiation by TGFβ family members,” Journal of Orthopaedic Science, vol. 8, no. 5, pp. 740–748, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  137. T. Watabe and K. Miyazono, “Roles of TGF-β family signaling in stem cell renewal and differentiation,” Cell Research, vol. 19, no. 1, pp. 103–115, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  138. F. Ng, S. Boucher, S. Koh et al., “PDGF, tgf-2. And FGF signaling is important for differentiation and growth of mesenchymal stem cells (mscs): transcriptional profiling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages,” Blood, vol. 112, no. 2, pp. 295–307, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  139. J. S. Park, J. S. Chu, A. D. Tsou et al., “The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-β,” Biomaterials, vol. 32, no. 16, pp. 3921–3930, 2011. View at Publisher · View at Google Scholar · View at PubMed
  140. M. Schulze and E. Tobiasch, “Artificial scaffolds and mesenchymal stem cells for hard tissue,” Advances in Biochemical Engineering Biotechnology. In press.
  141. G. Pattappa, H. K. Heywood, J. D. de Bruijn, and D. A. Lee, “The metabolism of human mesenchymal stem cells during proliferation and differentiation,” Journal of Cellular Physiology, vol. 226, pp. 2562–2570, 2010. View at Google Scholar
  142. G. B. Adams, K. T. Chabner, I. R. Alley et al., “Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor,” Nature, vol. 439, no. 7076, pp. 599–603, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  143. T. A. Mcadams, W. M. Miller, and E. T. Papoutsakis, “Variations in culture pH affect the cloning efficiency and differentiation of progenitor cells in ex vivo haemopoiesis,” British Journal of Haematology, vol. 97, no. 4, pp. 889–895, 1997. View at Google Scholar · View at Scopus
  144. 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 PubMed · View at Scopus
  145. A. Pansky, B. Roitzheim, and E. Tobiasch, “Differentiation potential of adult human mesenchymal stem cells,” Clinical Laboratory, vol. 53, no. 1-2, pp. 81–84, 2007. View at Google Scholar · View at Scopus
  146. D. I. Jung, J. Ha, B. T. Kang et al., “A comparison of autologous and allogenic bone marrow-derived mesenchymal stem cell transplantation in canine spinal cord injury,” Journal of the Neurological Sciences, vol. 285, no. 1-2, pp. 67–77, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  147. 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 PubMed · View at Scopus
  148. J. F. Liu, B. W. Wang, H. F. Hung, H. Chang, and K. G. Shyu, “Human mesenchymal stem cells improve myocardial performance in a splenectomized rat model of chronic myocardial infarction,” Journal of the Formosan Medical Association, vol. 107, no. 2, pp. 165–174, 2008. View at Publisher · View at Google Scholar · View at Scopus
  149. J. M. Hare, J. H. Traverse, T. D. Henry et al., “A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (Prochymal) after acute myocardial infarction,” Journal of the American College of Cardiology, vol. 54, no. 24, pp. 2277–2286, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  150. H. Mizuno, “Adipose-derived stem and stromal cells for cell-based therapy: current status of preclinical studies and clinical trials,” Current Opinion in Molecular Therapeutics, vol. 12, no. 4, pp. 442–449, 2010. View at Google Scholar · View at Scopus