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Journal for Biophysical Chemistry

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Optimizing interfacial features to regulate neural progenitor cells using polyelectrolyte multilayers and brain derived neurotrophic factor

Biointerphases volume 6, pages 189–199 (2011)Cite this article

Abstract

The development of biomaterials with controllable interfacial features which have the capability to instruct cellular behavior are required to produce functional scaffolds for the treatment of spinal cord injury (SCI). Here, poly-ε-caprolactone surfaces were biofunctionalized via layer-by-layer (LbL) deposition. The polyelectrolytes employed in this LbL technique were heparin and poly-L-lysine (PLL), the latter being chosen to improve cell adhesion and the subsequent cellular function of in vitrocultured neural progenitor cells. Material characterization results confirmed the deposition of well structured multilayers. Cell culture studies revealed significant differences in the cellular response to these adhesive/nonadhesive (PLL/heparin) polyelectrolyte multilayer (PEM)surfaces, with neurite outgrowth being significantly promoted on the PLL terminating layers. In addition, brain derived neurotrophic factor (BDNF) was adsorbed onto the LbL surfaces. This combined chemical and biological effect was then characterized in terms of neurite length along with the full length/truncated isoform 1 tyrosine kinase receptor (TrkB-FL/TrkB-T1) and growth associated protein-43 mRNA levels. Here, the authors report the differential effect of adsorbed and soluble BDNF of different concentrations. Adsorbed BDNF promoted neurite outgrowth and led to elevated, sustained TrkB mRNA levels. These findings highlight the potential of PEM biofunctionalized surfaces with integrated chemical and neurotrophin supportive cues to overcome SCI inhibitory environments and to promote regeneration.

References

  1. M. T. Fitch and J. Silver, Exp. Neurol. 209, 294 (2008).

    Article  CAS  Google Scholar 

  2. V. Kottis, P. Thibault, D. Mikol, Z.-C. Xiao, R. Zhang, P. Dergham, and P. E. Braun, J. Neurochem. 82, 1566 (2002).

    Article  CAS  Google Scholar 

  3. J. W. Fawcett, Spinal Cord 36, 811 (1998).

    Article  CAS  Google Scholar 

  4. S. M. Willerth and S. E. Sakiyama-Elbert, Adv. Drug Delivery Rev. 60, 263 (2008).

    Article  CAS  Google Scholar 

  5. F. M. Bareyre, J. Neurol. Sci. 265, 63 (2008).

    Article  CAS  Google Scholar 

  6. H. Tabesh, G. Amoabediny, N. S. Nik, M. Heydari, M. Yosefifard, S. O. R. Siadat, and K. Mottaghy, Neurochem. Int. 54, 73 (2009).

    Article  CAS  Google Scholar 

  7. D. R. Nisbet, S. Pattanawong, N. E. Ritchie, W. Shen, D. I. Finkelstein, M. K. Horne, and J. S. Forsythe, J. Neural Eng. 4, 35 (2007).

    Article  CAS  Google Scholar 

  8. D. R. Nisbet, K. E. Crompton, M. K. Horne, D. I. Finkelstein, and J. S. Forsythe, J. Biomed. Mater. Res., Part B: Appl. Biomater. 87B, 251 (2008).

    Article  CAS  Google Scholar 

  9. S. Woerly, E. Pinet, L. de Robertis, D. Van Diep, and M. Bousmina, Biomaterials 22, 1095 (2001).

    Article  CAS  Google Scholar 

  10. D. R. Nisbet, L. M. Y. Yu, T. Zahir, J. S. Forsythe, and M. S. Shoichet, J. Biomater. Sci., Polym. Ed. 19, 623 (2008).

    Article  CAS  Google Scholar 

  11. H. Nomura, C. H. Tator, and M. S. Shoichet, J. Neurotrauma 23, 496 (2006).

    Article  Google Scholar 

  12. C. Boura, P. Menu, E. Payan, C. Picart, J. C. Voegel, S. Muller, and J. F. L. Richert, P. Lavalle, E. Payan, X. Z. Shu, G. D. Prestwich, J. F. Stoltz, P. Schaaf, J. C. Voegel, and C. Picart, Langmuir 20, 448 (2004).

    Article  Google Scholar 

  13. Y. Gong, Y. Zhu, Y. Liu, Z. Ma, C. Gao, and J. Shen, Acta Biomater. 3, 677 (2007).

    Article  CAS  Google Scholar 

  14. S. Ahmed, B. A. Reynolds, and S. Weiss, J. Neurosci. 15, 5765 (1995).

    CAS  Google Scholar 

  15. S. S. Shiratori and M. F. Rubner, Macromolecules 33, 4213 (2000).

    Article  CAS  Google Scholar 

  16. S. Boddohi, C. E. Killingsworth, and M. J. Kipper, Biomacromolecules 9, 2021 (2008).

    Article  CAS  Google Scholar 

  17. L. Richert, A. J. Engler, D. E. Discher, and C. Picart, Biomacromolecules 5, 1908 (2004).

    Article  CAS  Google Scholar 

  18. C. B. Bucur, Z. Sui, and J. B. Schlenoff, J. Am. Chem. Soc. 128, 13690 (2006).

    Article  CAS  Google Scholar 

  19. B. Schoeler, E. Poptoshev, and F. Caruso, Macromolecules 36, 5258 (2003).

    Article  CAS  Google Scholar 

  20. P. Bertrand, A. Jonas, A. Laschewsky, and R. Legras, Macromol. Rapid Commun. 21, 319 (2000).

    Article  CAS  Google Scholar 

  21. J. Almodovar, S. Bacon, J. Gogolski, J. D. Kisiday, and M. J. Kipper, Biomacromolecules 11, 2629 (2010).

    Article  CAS  Google Scholar 

  22. C. Picart, P. Lavalle, P. Hubert, F. J. G. Cuisinier, G. Decher, P. Schaaf, and J. C. Voegel, Langmuir 17, 7414 (2001).

    Article  CAS  Google Scholar 

  23. M. Houska, E. Brynda, and K. Bohat, J. Colloid Interface Sci. 273, 140 (2004).

    Article  CAS  Google Scholar 

  24. H. Min, E. S. Eric, T. Charlotte, T. Jasmine, and R. H. Vincent, Tissue Eng. 6, 585 (2000).

    Article  Google Scholar 

  25. D. R. Nisbet, D. Moses, T. R. Gengenbach, J. S. Forsythe, D. I. Finkelstein, and M. K. Horne, J. Biomed. Mater. Res. Part A 89A, 24 (2009).

    Article  CAS  Google Scholar 

  26. E. Young, Thromb. Res. 122, 743 (2008).

    Article  CAS  Google Scholar 

  27. D. J. Tyrrell, A. P. Horne, K. R. Holme, J. M. H. Preuss, C. P. Page, M. W. A. F. M. J. Thomas August, and T. C. Joseph, “Heparin in Inflammation: Potential Therapeutic Applications beyond Anticoagulation,” in Advances in Pharmacology (Academic, New York, 1999), p. 151.

    Google Scholar 

  28. J. Fu, J. Ji, W. Yuan, and J. Shen, Biomaterials 26, 6684 (2005).

    Article  CAS  Google Scholar 

  29. L. D. Thompson, M. W. Pantoliano, and B. A. Springer, Biochemistry 33, 3831 (1994).

    Article  CAS  Google Scholar 

  30. J. J. Yoon, H. J. Chung, H. J. Lee, and T. G. Park, J. Biomed. Mater. Res. Part A (2006).

    Google Scholar 

  31. M. Philippe, M. M. Claudia, R. W. Scott, P. B. Richard, and B. M. Bartlett, Eur. J. Neurosci. 10, 607 (1998).

    Article  Google Scholar 

  32. A. G. Rabchevsky, I. Fugaccia, A. F. Turner, D. A. Blades, M. P. Mattson, and S. W. Scheff, Exp. Neurol. 164, 280 (2000).

    Article  CAS  Google Scholar 

  33. X.-Y. Song, F. Li, F.-H. Zhang, J.-H. Zhong, and X.-F. Zhou, PLoS One 3, e1707 (2008).

    Article  Google Scholar 

  34. J. F. Poduslo and G. L. Curran, Brain Res. Mol. Brain Res. 36, 280 (1996).

    Article  CAS  Google Scholar 

  35. N. R. Kobayashi, D.-P. Fan, K. M. Giehl, A. M. Bedard, S. J. Wiegand, and W. Tetzlaff, J. Neurosci. 17, 9583 (1997).

    CAS  Google Scholar 

  36. M. Stroh, W. R. Zipfel, R. M. Williams, S. C. Ma, W. W. Webb, and W. M. Saltzman, Nature Mater. 3, 489 (2004).

    Article  CAS  Google Scholar 

  37. S. Biffo, N. Offenhauser, B. D. Carter, and Y. A. Barde, Development 121, 2461 (1995).

    CAS  Google Scholar 

  38. L. Richert, P. Lavalle, D. Vautier, B. Senger, J. F. Stoltz, P. Schaaf, J. C. Voegel, and C. Picart, Biomacromolecules 3, 1170 (2002).

    Article  CAS  Google Scholar 

  39. D. R. Nisbet, A. E. Rodda, M. K. Horne, J. S. Forsythe, and D. I. Finkelstein, Biomaterials 30, 4573 (2009).

    Article  CAS  Google Scholar 

  40. M. V. Voinova, M. Jonson, and B. Kasemo, Biosens. Bioelectron. 17, 835 (2002).

    Article  CAS  Google Scholar 

  41. D. Yoo, S. S. Shiratori, and M. F. Rubner, Macromolecules 31, 4309 (1998).

    Article  CAS  Google Scholar 

  42. I. Husson, C.-M. Rangon, V. Lelievre, A.-P. Bemelmans, P. Sachs, J. Mallet, B. E. Kosofsky, and P. Gressens, Cereb. Cortex 15, 250 (2005).

    Article  Google Scholar 

  43. J. Bilsland, M. Rigby, L. Young, and S. Harper, J. Neurosci. Methods 92, 75 (1999).

    Article  CAS  Google Scholar 

  44. E. Meijering, M. Jacob, J. C. F. Sarria, P. Steiner, H. Hirling, and M. Unser, Cytometry, Part A 58A, 167 (2004).

    Article  Google Scholar 

  45. M. Bibel, J. Richter, E. Lacroix, and Y.-A. Barde, Nat. Protoc. 2, 1034 (2007).

    Article  CAS  Google Scholar 

  46. L. Frank, R. Ventimiglia, K. Anderson, R. M. Lindsay, and J. S. Rudge, Eur. J. Neurosci. 8, 1220 (1996).

    Article  CAS  Google Scholar 

  47. C. Picart, J. Mutterer, L. Richert, Y. Luo, G. D. Prestwich, P. Schaaf, J. C. Voegel, and P. Lavalle, Proc. Natl. Acad. Sci. U.S.A. 99, 12531 (2002).

    Article  CAS  Google Scholar 

  48. Y. Zhu, C. Gao, X. Liu, and J. Shen, Biomacromolecules 3, 1312 (2002).

    Article  CAS  Google Scholar 

  49. M. Bellion, L. Santen, H. Mantz, H. Hahl, A. Quinn, A. Nagel, C. Gilow, C. Weitenberg, Y. Schmitt, and K. Jacobs, J. Phys.: Condens. Matter 20, 404226 (2008).

    Article  Google Scholar 

  50. I. C. Maier and M. E. Schwab, Philos. Trans. R. Soc. London, Ser. B 361, 1611 (2006).

    Article  CAS  Google Scholar 

  51. R. J. Tolwani, P. S. Buckmaster, S. Varma, J. M. Cosgaya, Y. Wu, C. Suri, and E. M. Shooter, Neuroscience 114, 795 (2002).

    Article  CAS  Google Scholar 

  52. B. D. Carter, U. Zirrgiebel, and Y.-A. Barde, J. Biol. Chem. 270, 21751 (1995).

    Article  CAS  Google Scholar 

  53. R. Deogracias, G. Espliguero, T. Iglesias, and A. Rodriguez-Pena, Mol. Cell. Neurosci. 26, 470 (2004).

    Article  CAS  Google Scholar 

  54. D. Cai, Y. Shen, M. De Bellard, S. Tang, and M. T. Filbin, Neuron 22, 89 (1999).

    Article  CAS  Google Scholar 

  55. A. Meyer-Franke, G. A. Wilkinson, A. Kruttgen, M. Hu, E. Munro, M. G. Hanson, L. F. Reichardt, and B. A. Barres, Neuron 21, 681 (1998).

    Article  CAS  Google Scholar 

  56. J. K. Atwal, B. Massie, F. D. Miller, and D. R. Kaplan, Neuron 27, 265 (2000).

    Article  CAS  Google Scholar 

  57. J. C. Perron and J. L. Bixby, Mol. Cell. Neurosci. 13, 362 (1999).

    Article  CAS  Google Scholar 

  58. Y. Ito, G. Chen, Y. Imanishi, T. Morooka, E. Nishida, Y. Okabayashi, and M. Kasuga, J. Biochem. (Tokyo) 129, 733 (2001).

    Article  CAS  Google Scholar 

  59. Q. Li and Y. Chau, J. Biomed. Mater. Res. Part A 94A, 688 (2010).

    CAS  Google Scholar 

  60. Y.-Z. Zhang, D. B. Moheban, B. R. Conway, A. Bhattacharyya, and R. A. Segal, J. Neurosci. 20, 5671 (2000).

    CAS  Google Scholar 

  61. Y. Gao, E. Nikulina, W. Mellado, and M. T. Filbin, J. Neurosci. 23, 11770 (2003).

    CAS  Google Scholar 

  62. L. Aigner, S. Arber, J. P. Kapfhammer, T. Laux, C. Schneider, F. Botteri, H.-R. Brenner, and P. Caroni, Cell 83, 269 (1995).

    Article  CAS  Google Scholar 

  63. K. F. Meiri, J. L. Saffell, F. S. Walsh, and P. Doherty, J. Neurosci. 18, 10429 (1998).

    CAS  Google Scholar 

  64. R. D. Jacobson, I. Virag, and J. H. Skene, J. Neurosci. 6, 1843 (1986).

    CAS  Google Scholar 

  65. A. E. Fournier, J. Beer, C. O. Arregui, C. Essagian, A. J. Aguayo, and L. McKerracher, J. Neurosci. Res. 47, 561 (1997).

    Article  CAS  Google Scholar 

  66. A. Buffo, A. J. D. G. Holtmaat, T. Savio, J. S. Verbeek, J. Oberdick, A. B. Oestreicher, W. H. Gispen, J. Verhaagen, F. Rossi, and P. Strata, J. Neurosci. 17, 8778 (1997).

    CAS  Google Scholar 

  67. P. Caroni, L. Aigner, and C. Schneider, J. Cell Biol. 136, 679 (1997).

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Materials Engineering, Monash University, VIC, 3800, Australia

    Kun Zhou & John S. Forsythe

  2. Monash Immunology and Stem Cell Laboratories, Monash University, VIC, 3800, Australia

    Kun Zhou & Gui Zhi Sun

  3. Department of Zoology, The University of Melbourne, VIC, 3010, Australia

    Claude C. Bernard & George A. Thouas

  4. ANU College of Engineering and Computer Science, The Australian National University, ACT, 0200, Australia

    David R. Nisbet

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  1. Kun Zhou
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  2. Gui Zhi Sun
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Zhou, K., Sun, G.Z., Bernard, C.C. et al. Optimizing interfacial features to regulate neural progenitor cells using polyelectrolyte multilayers and brain derived neurotrophic factor. Biointerphases 6, 189–199 (2011). https://doi.org/10.1116/1.3656249

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  • DOI: https://doi.org/10.1116/1.3656249