About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 361906, 15 pages
http://dx.doi.org/10.1155/2013/361906
Research Article

Activation of the ERK1/2 Signaling Pathway during the Osteogenic Differentiation of Mesenchymal Stem Cells Cultured on Substrates Modified with Various Chemical Groups

1Department of Prosthodontics, School of Stomatology, China Medical University, Shenyang 110001, China
2State Key Laboratory of New Ceramics and Fine Processing, Department of Materials Science and Engineering, Tsinghua University, Beijing 100084, China
3Department of Cell Biology, Key Laboratory of Cell Biology, Ministry of Public Health and Key Laboratory of Medical Cell Biology, Ministry of Education, China Medical University, Shenyang 110001, China

Received 22 April 2013; Revised 9 July 2013; Accepted 16 July 2013

Academic Editor: Kibret Mequanint

Copyright © 2013 Bing Bai 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. P. Buma, W. Schreurs, and N. Verdonschot, “Skeletal tissue engineering—from in vitro studies to large animal models,” Biomaterials, vol. 25, no. 9, pp. 1487–1495, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchy-mal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999.
  3. D. Dallari, M. Fini, C. Stagni et al., “In vivo study on the healing of bone defects treated with bone marrow stromal cells, platelet-rich plasma, and freeze-dried bone allografts, alone and in combination,” Journal of Orthopaedic Research, vol. 24, no. 5, pp. 877–888, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. M. P. Lutolf, P. M. Gilbert, and H. M. Blau, “Designing materials to direct stem-cell fate,” Nature, vol. 462, no. 7272, pp. 433–441, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Chai and K. W. Leong, “Biomaterials approach to expand and direct differentiation of stem cells,” Molecular Therapy, vol. 15, no. 3, pp. 467–480, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Saha, J. F. Pollock, D. V. Schaffer, and K. E. Healy, “Designing synthetic materials to control stem cell phenotype,” Current Opinion in Chemical Biology, vol. 11, no. 4, pp. 381–387, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Dawson, G. Mapili, K. Erickson, S. Taqvi, and K. Roy, “Biomaterials for stem cell differentiation,” Advanced Drug Delivery Reviews, vol. 60, no. 2, pp. 215–228, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. S. M. Dellatore, A. S. Garcia, and W. M. Miller, “Mimicking stem cell niches to increase stem cell expansion,” Current Opinion in Biotechnology, vol. 19, no. 5, pp. 534–540, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Little, K. E. Healy, and D. Schaffer, “Engineering biomaterials for synthetic neural stem cell microenvironments,” Chemical Reviews, vol. 108, no. 5, pp. 1787–1796, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. J. A. Burdick and G. Vunjak-Novakovic, “Engineered microenvironments for controlled stem cell differentiation,” Tissue Engineering A, vol. 15, no. 2, pp. 205–219, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. R. A. Marklein and J. A. Burdick, “Controlling stem cell fate with material design,” Advanced Materials, vol. 22, no. 2, pp. 175–189, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. B. G. Keselowsky, D. M. Collard, and A. J. García, “Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion,” Journal of Biomedical Materials Research A, vol. 66, no. 2, pp. 247–259, 2003. View at Scopus
  13. B. G. Keselowsky, D. M. Collard, and A. J. García, “Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding,” Biomaterials, vol. 25, no. 28, pp. 5947–5954, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Lan, C. A. Gersbach, K. E. Michael, B. G. Keselowsky, and A. J. García, “Myoblast proliferation and differentiation on fibronectin-coated self assembled monolayers presenting different surface chemistries,” Biomaterials, vol. 26, no. 22, pp. 4523–4531, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Xiao, D. Jiang, P. Thomas et al., “MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1,” Journal of Biological Chemistry, vol. 275, no. 6, pp. 4453–4459, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Xiao, R. Gopalakrishnan, D. Jiang, E. Reith, M. D. Benson, and R. T. Franceschi, “Bone morphogenetic proteins, extracellular matrix, and mitogen-activated protein kinase signaling pathways are required for osteoblast-specific gene expression and differentiation in MC3T3-E1 cells,” Journal of Bone and Mineral Research, vol. 17, no. 1, pp. 101–110, 2002. View at Scopus
  17. L. Chang and M. Karin, “Mammalian MAP kinase signalling cascades,” Nature, vol. 410, no. 6824, pp. 37–40, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. Q. Liu, L. Cen, H. Zhou et al., “The role of the extracellular signal-related kinase signaling pathway in osteogenic differentiation of human adipose-derived stem cells and in adipogenic transition initiated by dexamethasone,” Tissue Engineering A, vol. 15, no. 11, pp. 3487–3497, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. R. K. Jaiswal, N. Jaiswal, S. P. Bruder, G. Mbalaviele, D. R. Marshak, and M. F. Pittenger, “Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase,” Journal of Biological Chemistry, vol. 275, no. 13, pp. 9645–9652, 2000. View at Publisher · View at Google Scholar · View at Scopus
  20. E. M. Sale, P. G. P. Atkinson, and G. J. Sale, “Requirement of MAP kinase for differentiation of fibroblasts to adipocytes, for insulin activation of p90 S6 kinase and for insulin or serum stimulation of DNA synthesis,” EMBO Journal, vol. 14, no. 4, pp. 674–684, 1995. View at Scopus
  21. R. M. Salasznyk, R. F. Klees, M. K. Hughlock, and G. E. Plopper, “ERK signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells on collagen I and vitronectin,” Cell Communication and Adhesion, vol. 11, no. 5-6, pp. 137–153, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Fu, T. Tang, Y. Miao, S. Zhang, Z. Qu, and K. Dai, “Stimulation of osteogenic differentiation and inhibition of adipogenic differentiation in bone marrow stromal cells by alendronate via ERK and JNK activation,” Bone, vol. 43, no. 1, pp. 40–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Mrksich, “Using self-assembled monolayers to model the extracellular matrix,” Acta Biomaterialia, vol. 5, no. 3, pp. 832–841, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. J. M. Curran, R. Chen, and J. A. Hunt, “The guidance of human mesenchymal stem cell differentiation in vitro by controlled modifications to the cell substrate,” Biomaterials, vol. 27, no. 27, pp. 4783–4793, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. J. M. Curran, R. Chen, and J. A. Hunt, “Controlling the phenotype and function of mesenchymal stem cells in vitro by adhesion to silane-modified clean glass surfaces,” Biomaterials, vol. 26, no. 34, pp. 7057–7067, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. J. E. Phillips, T. A. Petrie, F. P. Creighton, and A. J. García, “Human mesenchymal stem cell differentiation on self-assembled monolayers presenting different surface chemistries,” Acta Biomaterialia, vol. 6, no. 1, pp. 12–20, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. Y.-J. Ren, H. Zhang, H. Huang et al., “in vitro behavior of neural stem cells in response to different chemical functional groups,” Biomaterials, vol. 30, no. 6, pp. 1036–1044, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. J. M. Curran, F. Pu, R. Chen, and J. A. Hunt, “The use of dynamic surface chemistries to control msc isolation and function,” Biomaterials, vol. 32, no. 21, pp. 4753–4760, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. X. Liu, J. He, S. Zhang, X. M. Wang, H. Y. Liu, and F. Z. Cui, “Adipose stem cells controlled by surface chemistry,” Journal of Tissue Engineering and Regenerative Medicin, vol. 7, no. 2, pp. 112–117, 2013.
  30. X.-L. Yu, B. Zhang, X.-M. Wang et al., “Cancer cell proliferation controlled by surface chemistry in its microenvironment,” Frontiers of Materials Science, vol. 5, no. 4, pp. 412–416, 2011.
  31. H. Deng, X. Wang, C. Du, X.-C. Shen, and F.-Z. Cui, “Combined effect of ion concentration and functional groups on the surface chemistry modulated CaCO3 crystallization,” CrystEngComm, vol. 20, no. 14, pp. 6647–6653, 2012.
  32. G. K. Toworfe, R. J. Composto, I. M. Shapiro, and P. Ducheyne, “Nucleation and growth of calcium phosphate on amine-, carboxyl- and hydroxyl-silane self-assembled monolayers,” Biomaterials, vol. 27, no. 4, pp. 631–642, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. C. A. Widrig, C. A. Alves, and M. D. Porter, “Scanning tunneling microscopy of ethanethiolate and n-octadecanethiolate monolayers spontaneously adsorbed at gold surfaces,” Journal of the American Chemical Society, vol. 113, no. 8, pp. 2805–2810, 1991. View at Scopus
  34. S. Lossdörfer, Z. Schwartz, C. H. Lohmann, D. C. Greenspan, D. M. Ranly, and B. D. Boyan, “Osteoblast response to bioactive glasses in vitro correlates with inorganic phosphate content,” Biomaterials, vol. 25, no. 13, pp. 2547–2555, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Otto, A. P. Thornell, T. Crompton et al., “Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development,” Cell, vol. 89, no. 5, pp. 765–771, 1997. View at Scopus
  36. G. Karsenty, “Role of Cbfa1 in osteoblast differentiation and function,” Seminars in Cell and Developmental Biology, vol. 11, no. 5, pp. 343–346, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. A. K. Kundu, C. B. Khatiwala, and A. J. Putnam, “Extracellular matrix remodeling, integrin expression, and downstream signaling pathways influence the osteogenic differentiation of mesenchymal stem cells on poly(Lactide-co-glycolide) substrates,” Tissue Engineering A, vol. 15, no. 2, pp. 273–283, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. R. O. Hynes, “Integrins: versatility, modulation, and signaling in cell adhesion,” Cell, vol. 69, no. 1, pp. 11–25, 1992. View at Publisher · View at Google Scholar · View at Scopus
  39. E. Ruoslahti, “Integrins,” Journal of Clinical Investigation, vol. 87, no. 1, pp. 1–5, 1991. View at Scopus
  40. E. A. Clark and J. S. Brugge, “Integrins and sign transduction pathways: the road taken,” Science, vol. 268, no. 5208, pp. 233–239, 1995. View at Scopus
  41. R. O. Hynes, “Integrins: bidirectional, allosteric signaling machines,” Cell, vol. 110, no. 6, pp. 673–687, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Krause, E. A. Cowles, and G. Gronowicz, “Integrin-mediated signaling in osteoblasts on titanium implant materials,” Journal of Biomedical Materials Research, vol. 52, no. 4, pp. 738–747, 2000.
  43. L. Pang, T. Sawada, S. J. Decker, and A. R. Saltiel, “Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor,” Journal of Biological Chemistry, vol. 270, no. 23, pp. 13585–13588, 1995. View at Publisher · View at Google Scholar · View at Scopus
  44. M. R. Caplan and M. M. Shah, “Translating biomaterial properties to intracellular signaling,” Cell Biochemistry and Biophysics, vol. 54, no. 1–3, pp. 1–10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. J. G. Lock, B. Wehrle-Haller, and S. Strömblad, “Cell-matrix adhesion complexes: master control machinery of cell migration,” Seminars in Cancer Biology, vol. 18, no. 1, pp. 65–76, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. I. Delon and N. H. Brown, “Integrins and the actin cytoskeleton,” Current Opinion in Cell Biology, vol. 19, no. 1, pp. 43–50, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. A. L. Berrier and K. M. Yamada, “Cell-matrix adhesion,” Journal of Cellular Physiology, vol. 213, no. 3, pp. 565–573, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. R. L. Juliano, P. Reddig, S. Alahari, M. Edin, A. Howe, and A. Aplin, “Integrin regulation of cell signalling and motility,” Biochemical Society Transactions, vol. 32, no. 3, pp. 443–446, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. F. G. Giancotti and E. Ruoslahti, “Integrin signaling,” Science, vol. 285, no. 5430, pp. 1028–1032, 1999. View at Publisher · View at Google Scholar · View at Scopus
  50. R. O. Hynes, “Integrins: a family of cell surface receptors,” Cell, vol. 48, no. 4, pp. 549–554, 1987. View at Scopus
  51. J. W. Ramos, “The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells,” International Journal of Biochemistry and Cell Biology, vol. 40, no. 12, pp. 2707–2719, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. J. P. Rodríguez, S. Ríos, M. Fernández, and J. F. Santibañez, “Differential activation of ERK1,2 MAP kinase signaling pathway in mesenchymal stem cell from control and osteoporotic postmenopausal women,” Journal of Cellular Biochemistry, vol. 92, no. 4, pp. 745–754, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. R. F. Klees, R. M. Salasznyk, K. Kingsley, W. A. Williams, A. Boskey, and G. E. Plopper, “Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway,” Molecular Biology of the Cell, vol. 16, no. 2, pp. 881–890, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Takahashi, Y. Seko, E. Noiri et al., “Vascular endothelial growth factor induces activation and subcellular translocation of focal adhesion kinase (p125(FAK)) in cultured rat cardiac myocytes,” Circulation Research, vol. 84, no. 10, pp. 1194–1202, 1999. View at Scopus
  55. S. Klein, F. G. Giancotti, M. Presta, S. M. Albelda, C. A. Buck, and D. B. Rifkin, “Basic fibroblast growth factor modulates integrin expression in microvascular endothelial cells,” Molecular Biology of the Cell, vol. 4, no. 10, pp. 973–982, 1993. View at Scopus
  56. R. F. Rotundo, T. M. Curtis, M. D. Shah et al., “TNF-α disruption of lung endothelial integrity: reduced integrin mediated adhesion to fibronectin,” American Journal of Physiology. Lung Cellular and Molecular Physiology, vol. 282, no. 2, pp. L316–L329, 2002. View at Scopus
  57. C.-H. Yeh, H.-C. Peng, and T.-F. Huang, “Cytokines modulate integrin α(v)β3-mediated human endothelial cell adhesion and calcium signaling,” Experimental Cell Research, vol. 251, no. 1, pp. 57–66, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. H.-Y. Liu, X. Liu, L.-P. Zhang, H.-J. Ai, and F.-Z. Cui, “Improvement on the performance of bone regeneration of calcium sulfate hemihydrate by adding mineralized collagen,” Tissue Engineering A, vol. 16, no. 6, pp. 2075–2084, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. C. A. Scotchford, C. P. Gilmore, E. Cooper, G. J. Leggett, and S. Downes, “Protein adsorption and human osteoblast-like cell attachment and growth on alkylthiol on gold self-assembled monolayers,” Journal of Biomedical Materials Research, vol. 59, no. 1, pp. 84–99, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Faucheux, R. Schweiss, K. Lützow, C. Werner, and T. Groth, “Self-assembled monolayers with different terminating groups as model substrates for cell adhesion studies,” Biomaterials, vol. 25, no. 14, pp. 2721–2730, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. D. E. Ingber, “Tensegrity II. How structural networks influence cellular information processing networks,” Journal of Cell Science, vol. 116, no. 8, pp. 1397–1408, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. G. Altankov, F. Grinnell, and T. Groth, “Studies on the biocompatibility of materials: fibroblast reorganization of substratum-bound fibronectin on surfaces varying in wettability,” Journal of Biomedical Materials Research, vol. 30, no. 3, pp. 385–391, 1996.
  63. S. Gronthos, P. J. Simmons, S. E. Graves, and P. G. Robey, “Integrin-mediated interactions between human bone marrow stromal precursor cells and the extracellular matrix,” Bone, vol. 28, no. 2, pp. 174–181, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Webb, V. Hlady, and P. A. Tresco, “Relationships among cell attachment, spreading, cytoskeletal organization, and migration rate for anchorage-dependent cells on model surfaces,” Journal of Biomedical Materials Research, vol. 49, no. 3, pp. 362–368, 2000.
  65. R. Zaidel-Bar, S. Itzkovitz, A. Ma'ayan, R. Iyengar, and B. Geiger, “Functional atlas of the integrin adhesome,” Nature Cell Biology, vol. 9, no. 8, pp. 858–867, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. L. B. Rosen, D. D. Ginty, M. J. Weber, and M. E. Greenberg, “Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras,” Neuron, vol. 12, no. 6, pp. 1207–1221, 1994. View at Publisher · View at Google Scholar · View at Scopus