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BioMed Research International
Volume 2014 (2014), Article ID 316803, 18 pages
http://dx.doi.org/10.1155/2014/316803
Research Article

Synergistic Effects of Orbital Shear Stress on In Vitro Growth and Osteogenic Differentiation of Human Alveolar Bone-Derived Mesenchymal Stem Cells

1Department of Biosystems & Biomaterials Science and Engineering, Seoul National University, Seoul 151-921, Republic of Korea
2Department of Oral and Maxillofacial Surgery and Dental Research Institute, School of Dentistry, Seoul National University, Seoul 110-744, Republic of Korea
3Tooth Bioengineering National Research Laboratory of Post BK21, School of Dentistry, Seoul National University, Seoul 110-744, Republic of Korea
4Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea

Received 19 April 2013; Revised 18 July 2013; Accepted 30 September 2013; Published 14 January 2014

Academic Editor: Jun Liao

Copyright © 2014 Ki Taek Lim 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. A. Chakraborty, Fluid dynamic analysis of flow in orbiting dishes and the effects of flow on shear stress and endothelial cellular responses [Dissertation], University of Louisville, 2011.
  2. A. Dardik, L. Chen, J. Frattini et al., “Differential effects of orbital and laminar shear stress on endothelial cells,” Journal of Vascular Surgery, vol. 41, no. 5, pp. 869–880, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. L. R. Trump, Cell-cell Communication in three dimensional microenvironments [Dissertation], University of Illinois, Champaign, Ill, USA, 2011.
  4. J. Al-Sukhun, C. Lindqvist, and R. Kontio, “Modelling of orbital deformation using finite-element analysis,” Journal of the Royal Society Interface, vol. 3, no. 7, pp. 255–262, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. C. W. Lo, “Role of gap junctions in cardiac conduction and development: insights from the connexin knockout mice,” Circulation Research, vol. 87, no. 5, pp. 346–348, 2000. View at Scopus
  6. C. M. Potter, M. H. Lundberg, L. S. Harrington et al., “Role of shear stress in endothelial cell morphology and expression of cyclooxygenase isoforms,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 2, pp. 384–391, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Asada, J. Paszkowiak, D. Teso et al., “Sustained orbital shear stress stimulates smooth muscle cell proliferation via the extracellular signal-regulated protein kinase 1/2 pathway,” Journal of Vascular Surgery, vol. 42, no. 4, pp. 772–780, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Yamane, M. Mitsumata, N. Yamaguchi et al., “Laminar high shear stress up-regulates type IV collagen synthesis and down-regulates MMP-2 secretion in endothelium. A quantitative analysis,” Cell and Tissue Research, vol. 340, no. 3, pp. 471–479, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Gramsch, H.-D. Gabriel, M. Wiemann et al., “Enhancement of connexin 43 expression increases proliferation and differentiation of an osteoblast-like cell line,” Experimental Cell Research, vol. 264, no. 2, pp. 397–407, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Civitelli, “Cell-cell communication in the osteoblast/osteocyte lineage,” Archives of Biochemistry and Biophysics, vol. 473, no. 2, pp. 188–192, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. K. T. Lim, J. Kim, H. Seonwoo et al., “Enhanced osteogenesis of human alveolar bone-derived mesenchymal stem cells for tooth tissue engineering using fluid shear stress in a rocking culture method,” Tissue Engineering C, vol. 9, no. 2, pp. 128–145, 2013.
  12. H. L. Holtorf, J. A. Jansen, and A. G. Mikos, “Flow perfusion culture induces the osteoblastic differentiation of marrow stromal cell-scaffold constructs in the absence of dexamethasone,” Journal of Biomedical Materials Research A, vol. 72, no. 3, pp. 326–334, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. D. A. Goodenough, J. A. Goliger, and D. L. Paul, “Connexins, connexons, and intercellular communication,” Annual Review of Biochemistry, vol. 65, pp. 475–502, 1996. View at Scopus
  14. M. Grellier, L. Bordenave, and J. Amédée, “Cell-to-cell communication between osteogenic and endothelial lineages: implications for tissue engineering,” Trends in Biotechnology, vol. 27, no. 10, pp. 562–571, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. D. L. Paul, “New functions for gap junctions,” Current Opinion in Cell Biology, vol. 7, no. 5, pp. 665–672, 1995. View at Publisher · View at Google Scholar · View at Scopus
  16. R. A. Rossello and D. H. Kohn, “Cell communication and tissue engineering,” Communicative and Integrative Biology, vol. 3, no. 1, pp. 53–56, 2010.
  17. K. Ley, E. Lundgren, E. Berger, and K.-E. Arfors, “Shear-dependent inhibition of granulocyte adhesion to cultured endothelium by dextran sulfate,” Blood, vol. 73, no. 5, pp. 1324–1330, 1989. View at Scopus
  18. R. E. Berson, M. R. Purcell, and M. K. Sharp, “Computationally determined shear on cells grown in orbiting culture dishes,” Advances in Experimental Medicine and Biology, vol. 614, pp. 189–198, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. M. M. Salek, P. Sattari, and R. J. Martinuzzi, “Analysis of fluid flow and wall shear stress patterns inside partially filled agitated culture well plates,” Annals of Biomedical Engineering, vol. 40, no. 3, pp. 707–728, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. D. C. Williams, G. B. Boder, R. E. Toomey, D. C. Paul, C. C. Hillman, and K. L. King, “Mineralization and metabolic response in serially passaged adult rat bone cells,” Calcified Tissue International, vol. 30, no. 3, pp. 233–246, 1980. View at Scopus
  21. S. B. Doty, “Morphological evidence of gap junctions between bone cells,” Calcified Tissue International, vol. 33, no. 5, pp. 509–512, 1981. View at Scopus
  22. N. N. Bowman, H. J. Donahue, and H. P. Ehrlich, “Gap junctional intercellular communication contributes to the contraction of rat osteoblast populated collagen lattices,” Journal of Bone and Mineral Research, vol. 13, no. 11, pp. 1700–1706, 1998. View at Publisher · View at Google Scholar · View at Scopus
  23. H. J. Donahue, “Gap junctional intercellular communication in bone: a cellular basis for the mechanostat set point,” Calcified Tissue International, vol. 62, no. 2, pp. 85–88, 1998. View at Scopus
  24. R. L. Duncan and C. H. Turner, “Mechanotransduction and the functional response of bone to mechanical strain,” Calcified Tissue International, vol. 57, no. 5, pp. 344–358, 1995. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Tanaka, I. Morimoto, Y. Nakano et al., “Osteoblasts are regulated by the cellular adhesion through ICAM-1 and VCAM-1,” Journal of Bone and Mineral Research, vol. 10, no. 10, pp. 1462–1469, 1995. View at Scopus
  26. R. Civitelli, K. Ziambaras, P. M. Warlow et al., “Regulation of connexin43 expression and function by prostaglandin E2 (PGE2) and parathyroid hormone (PTH) in osteoblastic cells,” Journal of Cellular Biochemistry, vol. 68, no. 8, 1998.
  27. M. A. V. Molen, C. T. Rubin, K. J. McLeod, L. K. McCauley, and H. J. Donahue, “Gap junctional intercellular communication contributes to hormonal responsiveness in osteoblastic networks,” Journal of Biological Chemistry, vol. 271, no. 21, pp. 12165–12171, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Civitelli, E. C. Beyer, P. M. Warlow, A. J. Robertson, S. T. Geist, and T. H. Steinberg, “Connexin43 mediates direct intercellular communication in human osteoblastic cell networks,” Journal of Clinical Investigation, vol. 91, no. 5, pp. 1888–1896, 1993. View at Scopus
  29. H. J. Donahue, K. J. McLeod, C. T. Rubin et al., “Cell-to-cell communication in osteoblastic networks: cell line-dependent hormonal regulation of gap junction function,” Journal of Bone and Mineral Research, vol. 10, no. 6, pp. 881–889, 1995. View at Scopus
  30. K. Schirrmacher, I. Schmitz, E. Winterhager et al., “Characterization of gap junctions between osteoblast-like cells in culture,” Calcified Tissue International, vol. 51, no. 4, pp. 285–290, 1992. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Lecanda, D. A. Towler, K. Ziambaras et al., “Gap junctional communication modulates gene expression in osteoblastic cells,” Molecular Biology of the Cell, vol. 9, no. 8, pp. 2249–2258, 1998. View at Scopus
  32. G. S. Stein, J. B. Lian, and T. A. Owen, “Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation,” The FASEB Journal, vol. 4, no. 13, pp. 3111–3123, 1990. View at Scopus
  33. J. E. Aubin, F. Lui, L. Malaval, and A. K. Gupta, “Osteoblast and chondroblast differentiation,” Bone, vol. 17, no. 2, supplement 1, pp. S77–S83, 1995. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Maniatopoulos, J. Sodek, and A. H. Melcher, “Bone formation in vitro by stromal cells obtained from bone marrow of young adult rats,” Cell and Tissue Research, vol. 254, no. 2, pp. 317–330, 1988. View at Scopus
  35. P. J. Ter Brugge and J. A. Jansen, “In vitro osteogenic differentiation of rat bone marrow cells subcultured with and without dexamethasone,” Tissue Engineering, vol. 8, no. 2, pp. 321–331, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. D. J. Rickard, T. A. Sullivan, B. J. Shenker, P. S. Leboy, and I. Kazhdan, “Induction of rapid osteoblast differentiation in rat bone marrow stromal cell cultures by dexamethasone and BMP-2,” Developmental Biology, vol. 161, no. 1, pp. 218–228, 1994. View at Publisher · View at Google Scholar · View at Scopus
  37. S. J. Peter, C. R. Liang, D. J. Kim, M. S. Widmer, and A. G. Mikos, “Osteoblastic phenotype of rat marrow stromal cells cultured in the presence of dexamethasone, glycerolphosphate, and L-ascorbic acid,” Journal of Cellular Biochemistry, vol. 71, no. 1, pp. 55–62, 1998.
  38. R. A. Terkeltaub, “Inorganic pyrophosphate generation and disposition in pathophysiology,” The American Journal of Physiology, vol. 281, no. 1, pp. C1–C11, 2001. View at Scopus
  39. H. Atmani, C. Audrain, L. Mercier, D. Chappard, and M. F. Basle, “Phenotypic effects of continuous or discontinuous treatment with dexamethasone and/or calcitriol on osteoblasts differentiated from rat bone marrow stromal cells,” Journal of Cellular Biochemistry, vol. 85, no. 3, pp. 640–650, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. R. M. Porter, W. R. Huckle, and A. S. Goldstein, “Effect of dexamethasone withdrawal on osteoblastic differentiation of bone marrow stromal cells,” Journal of Cellular Biochemistry, vol. 90, no. 1, pp. 13–22, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Rochier, A. Nixon, N. Yamashita et al., “Laminar shear, but not orbital shear, has a synergistic effect with thrombin stimulation on tissue factor expression in human umbilical vein endothelial cells,” Journal of Vascular Surgery, vol. 54, no. 2, pp. 480–488, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Chakraborty, S. Chakraborty, V. R. Jala, B. Haribabu, M. K. Sharp, and R. E. Berson, “Effects of biaxial oscillatory shear stress on endothelial cell proliferation and morphology,” Biotechnology and Bioengineering, vol. 109, no. 3, pp. 695–707, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. J. M. Thomas, A. Chakraborty, M. K. Sharp, and R. E. Berson, “Spatial and temporal resolution of shear in an orbiting petri dish,” Biotechnology Progress, vol. 27, no. 2, pp. 460–465, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Bai, J. S. Bee, J. G. Biddlecombe, Q. Chen, and W. T. Leach, “Computational fluid dynamics (CFD) insights into agitation stress methods in biopharmaceutical development,” International Journal of Pharmaceutics, vol. 423, no. 2, pp. 264–280, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. R. A. Rossello and D. H. Kohn, “Gap junction intercellular communication: a review of a potential platform to modulate craniofacial tissue engineering,” Journal of Biomedical Materials Research B, vol. 88, no. 2, pp. 509–518, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. C. G. Bevans, M. Kordel, S. K. Rhee, and A. L. Harris, “Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules,” Journal of Biological Chemistry, vol. 273, no. 5, pp. 2808–2816, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. D. I. Vaney, J. C. Nelson, and D. V. Pow, “Neurotransmitter coupling through gap junctions in the retina,” Journal of Neuroscience, vol. 18, no. 24, pp. 10594–10602, 1998. View at Scopus
  48. L. E. Wyatt, C. Y. Chung, B. Carlsen et al., “Bone morphogenetic protein-2 (BMP-2) and transforming growth factor-beta1 (TGF-beta1) alter connexin 43 phosphorylation in MC3T3-E1 Cells,” BMC Cell Biology, vol. 2, no. 1, p. 14, 2001. View at Scopus
  49. J. X. Jiang, A. J. Siller-Jackson, and S. Burra, “Roles of gap junctions and hemichannels in bone cell functions and in signal transmission of mechanical stress,” Frontiers in Bioscience, vol. 12, no. 4, pp. 1450–1462, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. M. M. Thi, T. Kojima, S. C. Cowin, S. Weinbaum, and D. C. Spray, “Fluid shear stress remodels expression and function of junctional proteins in cultured bone cells,” The American Journal of Physiology, vol. 284, no. 2, pp. C389–C403, 2003. View at Scopus
  51. P. P. Cherian, A. J. Siller-Jackson, S. Gu et al., “Mechanical strain opens connexin 43 hemichannels in osteocytes: a novel mechanism for the release of prostaglandin,” Molecular Biology of the Cell, vol. 16, no. 7, pp. 3100–3106, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Romanello and P. D'Andrea, “Dual mechanism of intercellular communication in HOBIT osteoblastic cells: a role for gap-junctional hemichannels,” Journal of Bone and Mineral Research, vol. 16, no. 8, pp. 1465–1476, 2001. View at Scopus
  53. M. M. Saunders, J. You, J. E. Trosko et al., “Gap junctions and fluid flow response in MC3T3-E1 cells,” The American Journal of Physiology, vol. 281, no. 6, pp. C1917–C1925, 2001. View at Scopus
  54. M. M. Saunders, J. You, Z. Zhou et al., “Fluid flow-induced prostaglandin E2 response of osteoblastic ROS 17/2.8 cells is gap junction-mediated and independent of cytosolic calcium,” Bone, vol. 32, no. 4, pp. 350–356, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Guilak, D. L. Butler, S. A. Goldstein, and D. J. Mooney, Eds., Functional Tissue Engineering, Springer, New York, NY, USA, 2003.
  56. J. Farhadi, C. Jaquiery, A. Barbero et al., “Differentiation-dependent up-regulation of BMP-2, TGF-β1, and VEGF expression by FGF-2 in human bone marrow stromal cells,” Plastic and Reconstructive Surgery, vol. 116, no. 5, pp. 1379–1386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Kanczler and R. Oreffo, “Osteogenesis and angiogenesis: the potential for engineering bone,” European Cells and Materials, vol. 15, pp. 100–114, 2008. View at Scopus
  58. Y.-C. Huang, D. Kaigler, K. G. Rice, P. H. Krebsbach, and D. J. Mooney, “Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell—driven bone regeneration,” Journal of Bone and Mineral Research, vol. 20, no. 5, pp. 848–857, 2005. View at Publisher · View at Google Scholar · View at Scopus