Table of Contents Author Guidelines Submit a Manuscript
Bone Marrow Research
Volume 2013, Article ID 803450, 13 pages
http://dx.doi.org/10.1155/2013/803450
Clinical Study

High-Frequency Vibration Treatment of Human Bone Marrow Stromal Cells Increases Differentiation toward Bone Tissue

1Department of Industrial and Information Sciences, University of Pavia, Via Ferrata 1, 27100 Pavia, Italy
2Center for Tissue Engineering, University of Pavia, Via Ferrata 1, 27100 Pavia, Italy
3Department of Public Health, Experimental Medicine and Forensics, University of Pavia, Via Forlanini, 8, 27100 Pavia, Italy
4Department of Molecular Medicine and UdR INSTM, University of Pavia, Viale Forlanini 6, 27100 Pavia, Italy
5Laboratory of Nanotechnology, Salvatore Maugeri Foundation IRCCS, Via S. Maugeri 4, 27100 Pavia, Italy

Received 3 December 2012; Accepted 20 February 2013

Academic Editor: David A. Rizzieri

Copyright © 2013 D. Prè 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. C. M. Korstjens, P. A. Nolte, E. H. Burger et al., “Stimulation of bone cell differentiation by low-intensity ultrasound—a histomorphometric in vitro study,” Journal of Orthopaedic Research, vol. 22, no. 3, pp. 495–500, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Fassina, E. Saino, M. G. Cusella De Angelis, G. Magenes, F. Benazzo, and L. Visai, “Low-power ultrasounds as a tool to culture human osteoblasts inside cancellous hydroxyapatite,” Bioinorganic Chemistry and Applications, vol. 2010, Article ID 456240, 8 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Diniz, K. Shomura, K. Soejima, and G. Ito, “Effects of periodic pulsed electromagnetic field stimulation on proliferation, differentiation and bone-like matrix mineralization in osteoblasts in different maturational stages,” Bone, vol. 28, no. 5, article S155, 2001. View at Google Scholar
  4. 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 Scopus
  5. 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 Scopus
  6. L. Fassina, L. Visai, L. Asti et al., “Calcified matrix production by SAOS-2 cells inside a polyurethane porous scaffold, using a perfusion bioreactor,” Tissue Engineering, vol. 11, no. 5-6, pp. 685–700, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Ignatius, H. Blessing, A. Liedert et al., “Tissue engineering of bone: effects of mechanical strain on osteoblastic cells in type I collagen matrices,” Biomaterials, vol. 26, no. 3, pp. 311–318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. M. E. Gomes, R. L. Reis, and A. G. Mikos, “Bone tissue engineering constructs based on starch scaffolds and bone marrow cells cultured in a flow perfusion bioreactor,” Materials Science Forum, vol. 514–516, no. 2, pp. 980–984, 2006. View at Google Scholar · View at Scopus
  9. S. Kimoto, M. Matsuzawa, T. Onishi, N. Uchimura, T. Kawase, and S. Saito, “Effect of mechanical stress on osteoblast-like cells derived from alveolar bone,” Journal of Dental Research, vol. 75, article 583, 1996. View at Google Scholar
  10. R. Smalt, F. T. Mitchell, R. L. Howard, and T. J. Chambers, “Mechanical strain versus wall shear stress as the stimulus to bone cells in mechanical loading,” Journal of Bone and Mineral Research, vol. 11, article M336, 1996. View at Google Scholar
  11. C. H. Lee, H. J. Shin, I. H. Cho et al., “Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast,” Biomaterials, vol. 26, no. 11, pp. 1261–1270, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. G. P. Thomas and A. J. El Haj, “Bone marrow stromal cells are load responsive in vitro,” Calcified Tissue International, vol. 58, no. 2, pp. 101–108, 1996. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Chiquet, M. Matthisson, M. Koch, M. Tannheimer, and R. Chiquet-Ehrismann, “Regulation of extracellular matrix synthesis by mechanical stress,” Biochemistry and Cell Biology, vol. 74, no. 6, pp. 737–744, 1996. View at Google Scholar · View at Scopus
  14. E. Ruoslahti, “Stretching is good for a cell,” Science, vol. 276, no. 5317, pp. 1345–1346, 1997. View at Publisher · View at Google Scholar · View at Scopus
  15. B. Tian, K. Lessan, J. Kahm, J. Kleidon, and C. Henke, “β1 integrin regulates fibroblast viability during collagen matrix contraction through a phosphatidylinositol 3-kinase/Akt/protein kinase B signaling pathway,” Journal of Biological Chemistry, vol. 277, no. 27, pp. 24667–24675, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. R. G. Bacabac, T. H. Smit, J. J. W. A. Van Loon, B. Z. Doulabi, M. Helder, and J. Klein-Nulend, “Bone cell responses to high-frequency vibration stress: does the nucleus oscillate within the cytoplasm?” FASEB Journal, vol. 20, no. 7, pp. 858–864, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. H. F. Shi, W. H. Cheung, L. Qin, A. H. C. Leung, and K. S. Leung, “Low-magnitude high-frequency vibration treatment augments fracture healing in ovariectomy-induced osteoporotic bone,” Bone, vol. 46, no. 5, pp. 1299–1305, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Lau, S. Al-Dujaili, A. Guenther, D. Liu, L. Wang, and L. You, “Effect of low-magnitude, high-frequency vibration on osteocytes in the regulation of osteoclasts,” Bone, vol. 46, no. 6, pp. 1508–1515, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Prè, G. Ceccarelli, L. Benedetti, G. Magenes, and M. G. C. De Angelis, “Effects of low-amplitude, high-frequency vibrations on proliferation and differentiation of SAOS-2 Human osteogenic cell line,” Tissue Engineering Part C, vol. 15, no. 4, pp. 669–679, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Prè, G. Ceccarelli, G. Gastaldi et al., “The differentiation of human adipose-derived stem cells (hASCs) into osteoblasts is promoted by low amplitude, high frequency vibration treatment,” Bone, vol. 49, no. 2, pp. 295–303, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Marui, C. Niyibizi, H. I. Georgescu et al., “Effect of growth factors on matrix synthesis by ligament fibroblasts,” Journal of Orthopaedic Research, vol. 15, no. 1, pp. 18–23, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. J. E. Moreau, J. Chen, R. L. Horan, D. L. Kaplan, and G. H. Altman, “Sequential growth factor application in bone marrow stromal cell ligament engineering,” Tissue Engineering, vol. 11, no. 11-12, pp. 1887–1897, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. F. J. Hughes and C. A. G. McCulloch, “Stimulation of the differentiation of osteogenic rat bone marrow stromal cells by osteoblast cultures,” Laboratory Investigation, vol. 64, no. 5, pp. 617–622, 1991. View at Google Scholar · View at Scopus
  24. Z. Li, S. J. Yao, M. Alini, and M. J. Stoddart, “Chondrogenesis of human bone marrow mesenchymal stem cells in fibrin-polyurethane composites is modulated by frequency and amplitude of dynamic compression and shear stress,” Tissue Engineering Part A, vol. 16, no. 2, pp. 575–584, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. U. Nöth, L. Rackwitz, A. Heymer et al., “Chondrogenic differentiation of human mesenchymal stem cells in collagen type I hydrogels,” Journal of Biomedical Materials Research Part A, vol. 83, no. 3, pp. 626–635, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Burlacu, A. M. Rosca, H. Maniu et al., “Promoting effect of 5-azacytidine on the myogenic differentiation of bone marrow stromal cells,” European Journal of Cell Biology, vol. 87, no. 3, pp. 173–184, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Tian, S. Bharadwaj, Y. Liu et al., “Myogenic differentiation of human bone marrow mesenchymal stem cells on a 3D nano fibrous scaffold for bladder tissue engineering,” Biomaterials, vol. 31, no. 5, pp. 870–877, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Scintu, C. Reali, R. Pillai et al., “Differentiation of human bone marrow stem cells into cells with a neural phenotype: diverse effects of two specific treatments,” BMC Neuroscience, vol. 7, article 14, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. M. M. Yaghoobi and M. T. Mahani, “NGF and BDNF expression drop off in neurally differentiated bone marrow stromal stem cells,” Brain Research, vol. 1203, pp. 26–31, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Wang, B. A. Bunnell, R. G. Painter et al., “Adult stem cells from bone marrow stroma differentiate into airway epithelial cells: potential therapy for cystic fibrosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 1, pp. 186–191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Xu, X. Liu, J. Chen et al., “Simvastatin enhances bone marrow stromal cell differentiation into endothelial cells via notch signaling pathway,” American Journal of Physiology, vol. 296, no. 3, pp. C535–C543, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. N. Saulnier, W. Lattanzi, M. A. Puglisi et al., “Mesenchymal stromal cells multipotency and plasticity: induction toward the hepatic lineage,” European Review for Medical and Pharmacological Sciences, vol. 13, no. 1, supplement, pp. 71–78, 2009. View at Google Scholar · View at Scopus
  33. Y. Yang, B. Qu, J. H. Huo, S. L. Wu, M. Y. Zhang, and Z. R. Wang, “Serum from radiofrequency-injured livers induces differentiation of bone marrow stem cells into hepatocyte-like cells,” Journal of Surgical Research, vol. 155, no. 1, pp. 18–24, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Gronthos, A. C. W. Zannettino, S. J. Hay et al., “Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow,” Journal of Cell Science, vol. 116, no. 9, pp. 1827–1835, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. I. Tognarini, S. Sorace, R. Zonefrati et al., “In vitro differentiation of human mesenchymal stem cells on Ti6Al4V surfaces,” Biomaterials, vol. 29, no. 7, pp. 809–824, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. S. L. Cheng, J. W. Yang, L. Rifas, S. F. Zhang, and L. V. Avioli, “Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone,” Endocrinology, vol. 134, no. 1, pp. 277–286, 1994. View at Publisher · View at Google Scholar · View at Scopus
  37. M. E. Bernardo, A. Cometa, R. Villa et al., “Human bone marrow-derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms,” Blood, vol. 110, no. 11, article 367A, 2007. View at Google Scholar
  38. D. Prè, G. Magenes, G. Ceccarelli, and M. G. Cusella De Angelis, “A high frequency vibrating system to stimulate cells in bone tissue engineering,” in Proceedings of the 2nd International Conference on Bioinformatics and Biomedical Engineering (iCBBE '08), pp. 884–887, May 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Bosco, R. Colli, E. Introini et al., “Adaptive responses of human skeletal muscle to vibration exposure,” Clinical Physiology, vol. 19, no. 2, pp. 183–187, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Cardinale, J. Leiper, P. Farajian, and M. Heer, “Whole-body vibration can reduce calciuria induced by high protein intakes and may counteract bone resorption: a preliminary study,” Journal of Sports Sciences, vol. 25, no. 1, pp. 111–119, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. L. V. Hale, Y. F. Ma, and R. F. Santerre, “Semi-quantitative fluorescence analysis of calcein binding as a measurement of in vitro mineralization,” Calcified Tissue International, vol. 67, no. 1, pp. 80–84, 2000. View at Google Scholar · View at Scopus
  42. A. K. Majors, C. A. Boehm, H. Nitto, R. J. Midura, and G. F. Muschler, “Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation,” Journal of Orthopaedic Research, vol. 15, no. 4, pp. 546–557, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Komori, “Regulation of osteoblast differentiation by runx2,” Advances in Experimental Medicine and Biology, vol. 658, pp. 43–49, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Owen and A. J. Friedenstein, “Stromal stem cells: marrow-derived osteogenic precursors,” Ciba Foundation Symposium, vol. 136, pp. 42–60, 1988. View at Google Scholar · View at Scopus
  45. D. T. Denhardt and X. Guo, “Osteopontin: a protein with diverse functions,” FASEB Journal, vol. 7, no. 15, pp. 1475–1482, 1993. View at Google Scholar · View at Scopus
  46. F. Azari, H. Vali, J. L. Guerquin-Kern et al., “Intracellular precipitation of hydroxyapatite mineral and implications for pathologic calcification,” Journal of Structural Biology, vol. 162, no. 3, pp. 468–479, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. J. A. R. Gordon, C. E. Tye, A. V. Sampaio, T. M. Underhill, G. K. Hunter, and H. A. Goldberg, “Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro,” Bone, vol. 41, no. 3, pp. 462–473, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Yamaguchi, T. Komori, and T. Suda, “Regulation of osteoblast differentiation mediated by bone morphogenetic proteins, hedgehogs, and Cbfa1,” Endocrine Reviews, vol. 21, no. 4, pp. 393–411, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Z. Xing, L. Zhu, J. A. Jackson et al., “Dynamic monitoring of cytotoxicity on microelectronic sensors,” Chemical Research in Toxicology, vol. 18, no. 2, pp. 154–161, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. N. W. Roehm, G. H. Rodgers, S. M. Hatfield, and A. L. Glasebrook, “An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT,” Journal of Immunological Methods, vol. 142, no. 2, pp. 257–265, 1991. View at Publisher · View at Google Scholar · View at Scopus
  51. N. J. Marshall, C. J. Goodwin, and S. J. Holt, “A critical assessment of the use of microculture tetrazolium assays to measure cell growth and function,” Growth Regulation, vol. 5, no. 2, pp. 69–84, 1995. View at Google Scholar · View at Scopus
  52. E. Saino, S. Grandi, E. Quartarone et al., “In vitro calcified matrix deposition by human osteoblasts onto a zinc-containing bioactive glass,” European Cells and Materials, vol. 21, pp. 59–72, 2011. View at Google Scholar · View at Scopus
  53. C. T. Rubin, R. Recker, D. Cullen, J. Ryaby, J. McCabe, and K. McLeod, “Prevention of postmenopausal bone loss by a low-magnitude, high-frequency mechanical stimuli: a clinical trial assessing compliance, efficacy, and safety,” Journal of Bone and Mineral Research, vol. 19, no. 3, pp. 343–351, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Rietschel, S. Van Koningsbruggen, O. Fricke, O. Semler, and E. Schoenau, “Whole body vibration: a new therapeutic approach to improve muscle function in cystic fibrosis?” International Journal of Rehabilitation Research, vol. 31, no. 3, pp. 253–256, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Trans, J. Aaboe, M. Henriksen, R. Christensen, H. Bliddal, and H. Lund, “Effect of whole body vibration exercise on muscle strength and proprioception in females with knee osteoarthritis,” Knee, vol. 16, no. 4, pp. 256–261, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. R. W. K. Lau, T. Teo, F. Yu, R. C. K. Chung, and M. Y. C. Pang, “Effects of whole-body vibration on sensorimotor performance in people with parkinson disease: a systematic review,” Physical Therapy, vol. 91, no. 2, pp. 198–209, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Howard, L. D. Buttery, K. M. Shakesheff, and S. J. Roberts, “Tissue engineering: strategies, stem cells and scaffolds,” Journal of Anatomy, vol. 213, no. 1, pp. 66–72, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. W. R. Otto and J. Rao, “Tomorrow's skeleton staff: mesenchymal stem cells and the repair of bone and cartilage,” Cell Proliferation, vol. 37, no. 1, pp. 97–110, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. I. S. Kim, Y. M. Song, T. H. Cho et al., “In vitro response of primary human bone marrow stromal cells to recombinant human bone morphogenic protein-2 in the early and late stages of osteoblast differentiation,” Development Growth and Differentiation, vol. 50, no. 7, pp. 553–564, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Potier, J. Noailly, and K. Ito, “Directing bone marrow-derived stromal cell function with mechanics,” Journal of Biomechanics, vol. 43, no. 5, pp. 807–817, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. C. Zhang, J. Li, L. Zhang et al., “Effects of mechanical vibration on proliferation and osteogenic differentiation of human periodontal ligament stem cells,” Archives of Oral Biology, vol. 57, no. 10, pp. 1395–1407, 2012. View at Google Scholar
  62. Y. Zhou, X. Guan, Z. Zhu et al., “Osteogenic differentiation of bone marrow-derived mesenchymal stromal cells on bone-derived scaffolds: effect of microvibration and role of ERK1/2 activation,” European Cells and Materials, vol. 22, pp. 12–25, 2011. View at Google Scholar · View at Scopus
  63. S. H. Kim, J. Turnbull, and S. Guimond, “Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor,” Journal of Endocrinology, vol. 209, no. 2, pp. 139–151, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. C. S. Chen, “Mechanotransduction—a field pulling together?” Journal of Cell Science, vol. 121, no. 20, pp. 3285–3292, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. D. E. Jaalouk and J. Lammerding, “Mechanotransduction gone awry,” Nature Reviews Molecular Cell Biology, vol. 10, no. 1, pp. 63–73, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. S. I. Deliloglu-Gurhan, H. S. Vatansever, F. Ozdal-Kurt, and I. Tuglu, “Characterization of osteoblasts derived from bone marrow stromal cells in a modified cell culture system,” Acta Histochemica, vol. 108, no. 1, pp. 49–57, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. T. A. Owen, M. Aronow, V. Shalhoub et al., “Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix,” Journal of Cellular Physiology, vol. 143, no. 3, pp. 420–430, 1990. View at Publisher · View at Google Scholar · View at Scopus
  68. J. E. Aubin and F. Liu, “The osteoblast lineage,” in Principles of Bone Biology, J. P. Bilezkian, L. G. Raisz, and G. A. Rodan, Eds., pp. 51–67, Academic Press, San Diego, Calif, USA, 1996. View at Google Scholar
  69. P. Bornstein and E. H. Sage, “Matricellular proteins: extracellular modulators of cell function,” Current Opinion in Cell Biology, vol. 14, no. 5, pp. 608–616, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Long and H. J. Rack, “Titanium alloys in total joint replacement—a materials science perspective,” Biomaterials, vol. 19, no. 18, pp. 1621–1639, 1998. View at Publisher · View at Google Scholar · View at Scopus
  71. S. L. Manske, C. A. Good, R. F. Zernicke, and S. K. Boyd, “High-frequency, low-magnitude vibration does not prevent bone loss resulting from muscle disuse in mice following botulinum toxin injection,” PLoS ONE, vol. 7, no. 5, Article ID e36486, 2012. View at Google Scholar
  72. G. M. Pagnotti, B. J. Adler, D. E. Green et al., “Low magnitude mechanical signals mitigate osteopenia without compromising longevity in an aged murine model of spontaneous granulosa cell ovarian cancer,” Bone, vol. 51, no. 3, pp. 570–577, 2012. View at Google Scholar