Table of Contents Author Guidelines Submit a Manuscript
Journal of Nanomaterials
Volume 2013, Article ID 251063, 10 pages
http://dx.doi.org/10.1155/2013/251063
Research Article

Enhanced Ca2+ Entry and Tyrosine Phosphorylation Mediate Nanostructure-Induced Endothelial Proliferation

1Institute of Biophysics, Medical University Graz, 8010 Graz, Austria
2Department of Cell Biology, Histology and Embryology, Core Facility Ultrastructure Analysis, Center for Medical Research, Medical University Graz, 8010 Graz, Austria
3Institute of Molecular Biosciences, University of Graz, 8010 Graz, Austria
4Institute of Applied Physics, Johannes Kepler University Linz, 4040 Linz, Austria
5Institute of Molecular Biology and Biochemistry, Medical University Graz, 8010 Graz, Austria

Received 23 August 2013; Accepted 6 October 2013

Academic Editor: Krasimir Vasilev

Copyright © 2013 Michaela Schernthaner 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. E. Martínez, A. Lagunas, C. A. Mills et al., “Stem cell differentiation by functionalized micro- and nanostructured surfaces,” Nanomedicine, vol. 4, no. 1, pp. 65–82, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Kruss, T. Wolfram, R. Martin, S. Neubauer, H. Kessler, and J. P. Spatz, “Stimulation of cell adhesion at nanostructured teflon interfaces,” Advanced Materials, vol. 22, no. 48, pp. 5499–5506, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Ventre, F. Causa, and P. A. Netti, “Determinants of cell-material crosstalk at the interface: towards engineering of cell instructive materials,” Journal of the Royal Society, Interface/the Royal Society, vol. 9, no. 74, pp. 2017–2032, 2012. View at Google Scholar
  4. S. Pernagallo, O. Tura, M. Wu et al., “Novel biopolymers to enhance endothelialisation of intra-vascular devices,” Advanced Healthcare Materials, vol. 1, no. 5, pp. 646–656, 2012. View at Google Scholar
  5. M. Schernthaner, B. Reisinger, H. Wolinski et al., “Nanopatterned polymer substrates promote endothelial proliferation by initiation of β-catenin transcriptional signaling,” Acta Biomaterialia, vol. 8, no. 8, pp. 2953–2962, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. F. H. Brembeck, M. Rosário, and W. Birchmeier, “Balancing cell adhesion and Wnt signaling, the key role of β-catenin,” Current Opinion in Genetics and Development, vol. 16, no. 1, pp. 51–59, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. T. J. C. Harris and M. Peifer, “Decisions, decisions: β-catenin chooses between adhesion and transcription,” Trends in Cell Biology, vol. 15, no. 5, pp. 234–237, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. F. H. Brembeck, T. Schwarz-Romond, J. Bakkers, S. Wilhelm, M. Hammerschmidt, and W. Birchmeier, “Essential role of BCL9-2 in the switch between β-catenin's adhesive and transcriptional functions,” Genes and Development, vol. 18, no. 18, pp. 2225–2230, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. C. J. Gottardi and B. M. Gumbiner, “Distinct molecular forms of β-catenin are targeted to adhesive or transcriptional complexes,” The Journal of Cell Biology, vol. 167, no. 2, pp. 339–349, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. T. P. Rao and M. Kühl, “An updated overview on wnt signaling pathways: a prelude for more,” Circulation Research, vol. 106, no. 12, pp. 1798–1806, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Valenta, G. Hausmann, and K. Basler, “The many faces and functions of beta-catenin,” The EMBO Journal, vol. 31, no. 12, pp. 2714–2736, 2012. View at Google Scholar
  12. G. E. Hannigan, C. Leung-Hagesteijn, L. Fitz-Gibbon et al., “Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase,” Nature, vol. 379, no. 6560, pp. 91–96, 1996. View at Publisher · View at Google Scholar · View at Scopus
  13. S. K. Hanks, M. B. Calalb, M. C. Harper, and S. K. Patel, “Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 18, pp. 8487–8491, 1992. View at Google Scholar · View at Scopus
  14. Y. Wang, G. Jin, H. Miao, J. Y.-S. Li, S. Usami, and S. Chien, “Integrins regulate VE-cadherin and catenins: dependence of this regulation on Src, but not on Ras,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 6, pp. 1774–1779, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Huveneers and E. H. J. Danen, “Adhesion signaling—crosstalk between integrins, Src and Rho,” Journal of Cell Science, vol. 122, part 8, pp. 1059–1069, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Lilien and J. Balsamo, “The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of β-catenin,” Current Opinion in Cell Biology, vol. 17, no. 5, pp. 459–465, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Chen, J. Nam, C. Jean et al., “VEGF-induced vascular permeability is mediated by FAK,” Developmental Cell, vol. 22, no. 1, pp. 146–157, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Bertocchi, M. V. Rao, and R. Zaidel-Bar, “Regulation of adherens junction dynamics by phosphorylation switches,” Journal of Signal Transduction, vol. 2012, Article ID 125295, 14 pages, 2012. View at Publisher · View at Google Scholar
  19. H. Rangaswami, R. Schwappacher, T. Tran et al., “Protein kinase G and focal adhesion kinase converge on Src/Akt/beta-catenin signaling module in osteoblast mechanotransduction,” The Journal of Biological Chemistry, vol. 287, no. 25, pp. 21509–21519, 2012. View at Google Scholar
  20. H. S. Lee, S. J. Millward-Sadler, M. O. Wright, G. Nuki, and D. M. Salter, “Integrin and mechanosensitive ion channel-dependent tyrosine phosphorylation of focal adhesion proteins and β-catenin in human articular chondrocytes after mechanical stimulation,” Journal of Bone and Mineral Research, vol. 15, no. 8, pp. 1501–1509, 2000. View at Google Scholar · View at Scopus
  21. S. Katz, R. Boland, and G. Santillán, “Modulation of ERK 1/2 and p38 MAPK signaling pathways by ATP in osteoblasts: Involvement of mechanical stress-activated calcium influx, PKC and Src activation,” International Journal of Biochemistry and Cell Biology, vol. 38, no. 12, pp. 2082–2091, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. E. W. Ades, F. J. Candal, R. A. Swerlick et al., “HMEC-1: establishment of an immortalized human microvascular endothelial cell line,” Journal of Investigative Dermatology, vol. 99, no. 6, pp. 683–690, 1992. View at Google Scholar · View at Scopus
  23. A. Graziani, M. Poteser, W. Heupel et al., “Cell-cell contact formation governs Ca2+ signaling by TRPC4 in the vascular endothelium: evidence for a regulatory TRPC4-β-catenin interaction,” The Journal of Biological Chemistry, vol. 285, no. 6, pp. 4213–4223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Bain, L. Plater, M. Elliott et al., “The selectivity of protein kinase inhibitors: a further update,” Biochemical Journal, vol. 408, no. 3, pp. 297–315, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Maydan, P. C. McDonald, J. Sanghera et al., “Integrin-linked kinase is a functional Mn2+-dependent protein kinase that regulates glycogen synthase kinase-3β (gsk-3β) phosphorylation,” PLoS ONE, vol. 5, no. 8, Article ID e12356, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Michels, M. Trautmann, E. Sievers et al., “SRC signaling is crucial in the growth of synovial sarcoma cells,” Cancer Research, vol. 73, no. 8, pp. 2518–2528, 2013. View at Google Scholar
  27. N. P. Shah, C. Tran, F. Y. Lee, P. Chen, D. Norris, and C. L. Sawyers, “Overriding imatinib resistance with a novel ABL kinase inhibitor,” Science, vol. 305, no. 5682, pp. 399–401, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. M. J. Mauro and B. J. Druker, “STI571: targeting BCR-ABL as therapy for CML,” Oncologist, vol. 6, no. 3, pp. 233–238, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. Z. Xie, P. A. Singleton, L. Y. W. Bourguignon, and D. D. Bikle, “Calcium-induced human keratinocyte differentiation requires src- and fyn-mediated phosphatidylinositol 3-kinase-dependent activation of phospholipase C-γ1,” Molecular Biology of the Cell, vol. 16, no. 7, pp. 3236–3246, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. G. A. Moore, D. J. McConkey, G. E. N. Kass, P. J. O'Brien, and S. Orrenius, “2,5-Di(tert-butyl)-1,4-benzohydroquinone—a novel inhibitor of liver microsomal Ca2+ sequestration,” FEBS Letters, vol. 224, no. 2, pp. 331–336, 1987. View at Publisher · View at Google Scholar · View at Scopus
  31. D. A. Murtazina, D. Chung, A. Ulloa, E. Bryan, H. L. Galan, and B. M. Sanborn, “TRPC1, STIM1, and ORAI influence signal-regulated intracellular and endoplasmic reticulum calcium dynamics in human myometrial cells,” Biology of Reproduction, vol. 85, no. 2, pp. 315–326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. O. P. Hamill and D. W. Mcbride Jr., “The pharmacology of mechanogated membrane ion channels,” Pharmacological Reviews, vol. 48, no. 2, pp. 231–252, 1996. View at Google Scholar · View at Scopus
  33. A. I. Teixeira, G. A. Abrams, P. J. Bertics, C. J. Murphy, and P. F. Nealey, “Epithelial contact guidance on well-defined micro- and nanostructured substrates,” Journal of Cell Science, vol. 116, part 10, pp. 1881–1892, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. P. T. Ohara and R. C. Buck, “Contact guidance in vitro. A light, transmission, and scanning electron microscopic study,” Experimental Cell Research, vol. 121, no. 2, pp. 235–249, 1979. View at Google Scholar · View at Scopus
  35. A. Oloumi, S. Syam, and S. Dedhar, “Modulation of Wnt3a-mediated nuclear β-catenin accumulation and activation by integrin-linked kinase in mammalian cells,” Oncogene, vol. 25, no. 59, pp. 7747–7757, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Xing, Z. Zhang, H. Mao, R. G. Schnellmann, and S. Zhuang, “Src regulates cell cycle protein expression and renal epithelial cell proliferation via PI3K/Akt signaling-dependent and -independent mechanisms,” American Journal of Physiology—Renal Physiology, vol. 295, no. 1, pp. F145–F152, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. X. Liu, L. Du, and R. Feng, “c-Src regulates cell cycle proteins expression through protein kinase B/glycogen synthase kinase 3 beta and extracellular signal-regulated kinases 1/2 pathways in MCF-7 cells,” Acta Biochimica et Biophysica Sinica, vol. 45, no. 7, pp. 586–592, 2013. View at Google Scholar
  38. D. Riley, N. O. Carragher, M. C. Frame, and J. A. Wyke, “The mechanism of cell cycle regulation by v-Src,” Oncogene, vol. 20, no. 42, pp. 5941–5950, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Babnigg, S. R. Bowersox, and M. L. Villereal, “The role of pp60(c-src) in the regulation of calcium entry via store-operated calcium channels,” The Journal of Biological Chemistry, vol. 272, no. 47, pp. 29434–29437, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. J. A. Rosado, D. Graves, and S. O. Sage, “Tyrosine kinases activate store-mediated Ca2+ entry in human platelets through the reorganization of the actin cytoskeleton,” Biochemical Journal, vol. 351, part 2, pp. 429–437, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. J. A. Rosado and S. O. Sage, “Regulation of plasma membrane Ca2+-ATPase by small GTPases and phosphoinositides in human platelets,” The Journal of Biological Chemistry, vol. 275, no. 26, pp. 19529–19535, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. I. F. Abdullaev, J. M. Bisaillon, M. Potier, J. C. Gonzalez, R. K. Motiani, and M. Trebak, “Stim1 and orai1 mediate crac currents and store-operated calcium entry important for endothelial cell proliferation,” Circulation Research, vol. 103, no. 11, pp. 1289–1299, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. W. F. Graier, W. R. Kukovetz, and K. Groschner, “Cyclic AMP enhances agonist-induced Ca2+ entry into endothelial cells by activation of potassium channels and membrane hyperpolarization,” Biochemical Journal, vol. 291, part 1, pp. 263–267, 1993. View at Google Scholar · View at Scopus
  44. I. Bogeski, M. Bozem, L. Sternfeld, H. W. Hofer, and I. Schulz, “Inhibition of protein tyrosine phosphatase 1B by reactive oxygen species leads to maintenance of Ca2+ influx following store depletion in HEK 293 cells,” Cell Calcium, vol. 40, no. 1, pp. 1–10, 2006. View at Publisher · View at Google Scholar · View at Scopus