Table of Contents Author Guidelines Submit a Manuscript
Journal of Ophthalmology
Volume 2016, Article ID 2371021, 13 pages
http://dx.doi.org/10.1155/2016/2371021
Research Article

Properties of Retinal Precursor Cells Grown on Vertically Aligned Multiwalled Carbon Nanotubes Generated for the Modification of Retinal Implant-Embedded Microelectrode Arrays

1Department of Ophthalmology, University Hospital RWTH Aachen, Pauwelsstraße 30, 52074 Aachen, Germany
2Fraunhofer Institute for Ceramic Technologies and Systems, Winterbergstraße 28, 01277 Dresden, Germany
3Institute for Materials in Electrical Engineering 1, RWTH Aachen University, Sommerfeldstraße 24, 52074 Aachen, Germany

Received 8 January 2016; Accepted 4 April 2016

Academic Editor: Wai T. Wong

Copyright © 2016 Sandra Johnen 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. T. Lenarz, H.-W. Pau, and G. Paasche, “Cochlear implants,” Current Pharmaceutical Biotechnology, vol. 14, no. 1, pp. 112–123, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. C.-H. Sung and J.-Z. Chuang, “The cell biology of vision,” Journal of Cell Biology, vol. 190, no. 6, pp. 953–963, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. S. P. Daiger, S. J. Bowne, and L. S. Sullivan, “Perspective on genes and mutations causing retinitis pigmentosa,” Archives of Ophthalmology, vol. 125, no. 2, pp. 151–158, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. A. F. Wright, C. F. Chakarova, M. M. Abd El-Aziz, and S. S. Bhattacharya, “Photoreceptor degeneration: genetic and mechanistic dissection of a complex trait,” Nature Reviews Genetics, vol. 11, no. 4, pp. 273–284, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Stingl, K. U. Bartz-Schmidt, D. Besch et al., “Artificial vision with wirelessly powered subretinal electronic implant alpha-IMS,” Proceedings of the Royal Society B, vol. 280, no. 1757, Article ID 20130077, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Wilke, V.-P. Gabel, H. Sachs et al., “Spatial resolution and perception of patterns mediated by a subretinal 16-electrode array in patients blinded by hereditary retinal dystrophies,” Investigative Ophthalmology and Visual Science, vol. 52, no. 8, pp. 5995–6003, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. L. N. Ayton, P. J. Blamey, R. H. Guymer et al., “First-in-human trial of a novel suprachoroidal retinal prosthesis,” PLoS ONE, vol. 9, no. 12, Article ID e115239, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Fujikado, M. Kamei, H. Sakaguchi et al., “Testing of semichronically implanted retinal prosthesis by suprachoroidal-transretinal stimulation in patients with retinitis pigmentosa,” Investigative Ophthalmology and Visual Science, vol. 52, no. 7, pp. 4726–4733, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Da Cruz, B. F. Coley, J. Dorn et al., “The Argus II epiretinal prosthesis system allows letter and word reading and long-term function in patients with profound vision loss,” British Journal of Ophthalmology, vol. 97, no. 5, pp. 632–636, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Menzel-Severing, T. Laube, C. Brockmann et al., “Implantation and explantation of an active epiretinal visual prosthesis: 2-year follow-up data from the EPIRET3 prospective clinical trial,” Eye, vol. 26, no. 4, pp. 501–509, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Roessler, T. Laube, C. Brockmann et al., “Implantation and explantation of a wireless epiretinal retina implant device: observations during the EPIRET3 prospective clinical trial,” Investigative Ophthalmology and Visual Science, vol. 50, no. 6, pp. 3003–3008, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Waschkowski, S. Hesse, A. C. Rieck et al., “Development of very large electrode arrays for epiretinal stimulation (VLARS),” BioMedical Engineering Online, vol. 13, no. 1, article 11, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Winkin and W. Mokwa, “Flexible multi-electrode array with integrated bendable CMOS-chip for implantable systems,” in Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC '12), pp. 3882–3885, San Diego, Calif, USA, August 2012. View at Publisher · View at Google Scholar
  14. S. F. Cogan, A. A. Guzelian, W. F. Agnew, T. G. H. Yuen, and D. B. McCreery, “Over-pulsing degrades activated iridium oxide films used for intracortical neural stimulation,” Journal of Neuroscience Methods, vol. 137, no. 2, pp. 141–150, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Harnack, C. Winter, W. Meissner, T. Reum, A. Kupsch, and R. Morgenstern, “The effects of electrode material, charge density and stimulation duration on the safety of high-frequency stimulation of the subthalamic nucleus in rats,” Journal of Neuroscience Methods, vol. 138, no. 1-2, pp. 207–216, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. D. B. McCreery, W. F. Agnew, T. G. H. Yuen, and L. Bullara, “Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation,” IEEE Transactions on Biomedical Engineering, vol. 37, no. 10, pp. 996–1001, 1990. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Stice, A. Gilletti, A. Panitch, and J. Muthuswamy, “Thin microelectrodes reduce GFAP expression in the implant site in rodent somatosensory cortex,” Journal of Neural Engineering, vol. 4, no. 2, pp. 42–53, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Minnikanti, M. G. A. G. Pereira, S. Jaraiedi et al., “In vivo electrochemical characterization and inflammatory response of multiwalled carbon nanotube-based electrodes in rat hippocampus,” Journal of Neural Engineering, vol. 7, no. 1, Article ID 016002, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Wang, H. A. Fishman, H. Dai, and J. S. Harris, “Neural stimulation with a carbon nanotube microelectrode array,” Nano Letters, vol. 6, no. 9, pp. 2043–2048, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Cellot, F. M. Toma, Z. K. Varley et al., “Carbon nanotube scaffolds tune synaptic strength in cultured neural circuits: novel frontiers in nanomaterial-tissue interactions,” Journal of Neuroscience, vol. 31, no. 36, pp. 12945–12953, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. G.-Z. Jin, M. Kim, U. S. Shin, and H.-W. Kim, “Neurite outgrowth of dorsal root ganglia neurons is enhanced on aligned nanofibrous biopolymer scaffold with carbon nanotube coating,” Neuroscience Letters, vol. 501, no. 1, pp. 10–14, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. V. Lovat, D. Pantarotto, L. Lagostena et al., “Carbon nanotube substrates boost neuronal electrical signaling,” Nano Letters, vol. 5, no. 6, pp. 1107–1110, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. A. I. Aria and M. Gharib, “Dry oxidation and vacuum annealing treatments for tuning the wetting properties of carbon nanotube arrays,” Journal of Visualized Experiments, no. 74, Article ID 50378, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Gołda, M. Brzychczy-Włoch, M. Faryna, K. Engvall, and A. Kotarba, “Oxygen plasma functionalization of parylene C coating for implants surface: nanotopography and active sites for drug anchoring,” Materials Science and Engineering C, vol. 33, no. 7, pp. 4221–4227, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. J.-C. Park, B. J. Park, D. H. Lee, H. Suh, D.-G. Kim, and O.-H. Kwon, “Evaluation of the cytotoxicity of polyetherurethane (PU) film containing zinc diethyldithiocarbamate (ZDEC) on various cell lines,” Yonsei Medical Journal, vol. 43, no. 4, pp. 518–526, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. G. M. Seigel, W. Sun, J. Wang, D. H. Hershberger, L. M. Campbell, and R. J. Salvi, “Neuronal gene expression and function in the growth-stimulated R28 retinal precursor cell line,” Current Eye Research, vol. 28, no. 4, pp. 257–269, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. G. M. Seigel, “Establishment of an E1A-immortalized retinal cell culture,” In Vitro Cellular & Developmental Biology—Animal, vol. 32, no. 2, pp. 66–68, 1996. View at Google Scholar · View at Scopus
  28. T. D. Schmittgen and K. J. Livak, “Analyzing real-time PCR data by the comparative CT method,” Nature Protocols, vol. 3, no. 6, pp. 1101–1108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. S. F. Cogan, “Neural stimulation and recording electrodes,” Annual Review of Biomedical Engineering, vol. 10, pp. 275–309, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. E. S. Ereifej, S. Khan, G. Newaz, J. Zhang, G. W. Auner, and P. J. Vandevord, “Comparative assessment of iridium oxide and platinum alloy wires using an in vitro glial scar assay,” Biomedical Microdevices, vol. 15, no. 6, pp. 917–924, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Thanawala, O. Palyvoda, D. G. Georgiev et al., “A neural cell culture study on thin film electrode materials,” Journal of Materials Science: Materials in Medicine, vol. 18, no. 9, pp. 1745–1752, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. R. V. Shannon, “A model of safe levels for electrical stimulation,” IEEE Transactions on Biomedical Engineering, vol. 39, no. 4, pp. 424–426, 1992. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Butterwick, A. Vankov, P. Huie, Y. Freyvert, and D. Palanker, “Tissue damage by pulsed electrical stimulation,” IEEE Transactions on Biomedical Engineering, vol. 54, no. 12, pp. 2261–2267, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Musa, D. R. Rand, D. J. Cott et al., “Bottom-up SiO2 embedded carbon nanotube electrodes with superior performance for integration in implantable neural microsystems,” ACS Nano, vol. 6, no. 6, pp. 4615–4628, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Patan, T. Shah, and M. Sahin, “Charge injection capacity of TiN electrodes for an extended voltage range,” Engineering in Medicine and Biology Society, vol. 1, pp. 890–892, 2006. View at Google Scholar
  36. J. H. Shin, G. B. Kim, E. J. Lee et al., “Carbon-nanotube-modified electrodes for highly efficient acute neural recording,” Advanced Healthcare Materials, vol. 3, no. 2, pp. 245–252, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. R. A. Parker, S. Negi, T. Davis et al., “The use of a novel carbon nanotube coated microelectrode array for chronic intracortical recording and microstimulation,” Engineering in Medicine and Biology Society, vol. 2012, pp. 791–794, 2012. View at Google Scholar
  38. P. Nymark, P. Wijshoff, R. Cavill et al., “Extensive temporal transcriptome and microRNA analyses identify molecular mechanisms underlying mitochondrial dysfunction induced by multi-walled carbon nanotubes in human lung cells,” Nanotoxicology, vol. 9, no. 5, pp. 624–635, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Vardharajula, S. Z. Ali, P. M. Tiwari et al., “Functionalized carbon nanotubes: biomedical applications,” International Journal of Nanomedicine, vol. 7, pp. 5361–5374, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. K. M. Gladwin, R. L. D. Whitby, S. V. Mikhalovsky, P. Tomlins, and J. Adu, “In vitro biocompatibility of multiwalled carbon nanotubes with sensory neurons,” Advanced Healthcare Materials, vol. 2, no. 5, pp. 728–735, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Li, H. Wang, Y. Qi et al., “Assessment of nanomaterial cytotoxicity with SOLiD sequencing-based microRNA expression profiling,” Biomaterials, vol. 32, no. 34, pp. 9021–9030, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. V. G. Walker, Z. Li, T. Hulderman, D. Schwegler-Berry, M. L. Kashon, and P. P. Simeonova, “Potential in vitro effects of carbon nanotubes on human aortic endothelial cells,” Toxicology and Applied Pharmacology, vol. 236, no. 3, pp. 319–328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. X. Cheng, C. Li, L. Rao, H. Zhou, T. Li, and Y. Duan, “Platinum wire implants coated with PEDOT/carbon nanotube conducting polymer films in the brain of rats: a histological evaluation,” Journal Wuhan University of Technology, vol. 27, no. 6, pp. 1053–1057, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. S. C. Tilton, N. J. Karin, A. Tolic et al., “Three human cell types respond to multi-walled carbon nanotubes and titanium dioxide nanobelts with cell-specific transcriptomic and proteomic expression patterns,” Nanotoxicology, vol. 8, no. 5, pp. 533–548, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. I. I. Bobrinetskii, R. A. Morozov, A. S. Seleznev, R. Y. Podchernyaeva, and O. A. Lopatina, “Proliferative activity and viability of fibroblast and glioblastoma cell on various types of carbon nanotubes,” Bulletin of Experimental Biology and Medicine, vol. 153, no. 2, pp. 259–262, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. K. N. Pielarski, B. van Stegen, A. Andreyeva et al., “Asymmetric N-cadherin expression results in synapse dysfunction, synapse elimination, and axon retraction in cultured mouse neurons,” PLoS ONE, vol. 8, no. 1, Article ID e54105, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. Z.-J. Liu, T. Ueda, T. Miyazaki et al., “A critical role for cyclin C in promotion of the hematopoietic cell cycle by cooperation with c-Myc,” Molecular and Cellular Biology, vol. 18, no. 6, pp. 3445–3454, 1998. View at Publisher · View at Google Scholar · View at Scopus
  48. R. E. Marc, B. W. Jones, C. B. Watt, and E. Strettoi, “Neural remodeling in retinal degeneration,” Progress in Retinal and Eye Research, vol. 22, no. 5, pp. 607–655, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. G. M. Seigel, A. L. Mutchler, and E. L. Imperato, “Expression of glial markers in a retinal precursor cell line,” Molecular Vision, vol. 2, article 2, 1996. View at Google Scholar
  50. D. Cocchia, J. M. Polak, G. Terenghi et al., “Localization of S-100 protein in Müller cells of the retina—2. Electron microscopical immunocytochemistry,” Investigative Ophthalmology & Visual Science, vol. 24, no. 7, pp. 980–984, 1983. View at Google Scholar
  51. F. Ghosh, “Müller cells in long-term full-thickness retinal transplants,” Glia, vol. 37, no. 1, pp. 76–82, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Kaempf, P. Walter, A. K. Salz, and G. Thumann, “Novel organotypic culture model of adult mammalian neurosensory retina in co-culture with retinal pigment epithelium,” Journal of Neuroscience Methods, vol. 173, no. 1, pp. 47–58, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Rösch, S. Johnen, A. Mataruga, F. Müller, C. Pfarrer, and P. Walter, “Selective photoreceptor degeneration by intravitreal injection of N-methyl-N-nitrosourea,” Investigative Ophthalmology and Visual Science, vol. 55, no. 3, pp. 1711–1723, 2014. View at Publisher · View at Google Scholar · View at Scopus