Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-30T07:35:23.688Z Has data issue: false hasContentIssue false
  • English
  • Français

A living electrode construct for incorporation of cells into bionic devices

Published online by Cambridge University Press:  27 June 2017

Josef Goding ,
Aaron Gilmour ,
Ulises Aregueta Robles ,
Laura Poole-Warren ,
Nigel Lovell ,
Penny Martens  and
Rylie Green
Josef Goding
Affiliation:
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia Department of Bioengineering, Imperial College London, London, UK
Aaron Gilmour
Affiliation:
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia
Ulises Aregueta Robles
Affiliation:
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia
Laura Poole-Warren
Affiliation:
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia
Nigel Lovell
Affiliation:
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia
Penny Martens
Affiliation:
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia
Rylie Green*
Affiliation:
Graduate School of Biomedical Engineering, University of New South Wales, Sydney, Australia Department of Bioengineering, Imperial College London, London, UK
*
Address all correspondence to Rylie Green at [email protected]
Get access

Abstract

A living electrode construct that enables integration of cells within bionic devices has been developed. The layered construct uses a combination of non-degradable conductive hydrogel and degradable biosynthetic hydrogel to support cell encapsulation at device surfaces. In this study, the material system is designed and analyzed to understand the impact of the cell carrying component on electrode characteristics. The cell carrying layer is shown to provide a soft interface that supports extracellular matrix development within the electrode while not significantly reducing the charge transfer characteristics. The living layer was shown to degrade over 21 days with minimal swelling upon implantation.

Type
Biomaterials for 3D Cell Biology Research Letter
Information
MRS Communications , Volume 7 , Issue 3 , September 2017 , pp. 487 - 495
Copyright
Copyright © Materials Research Society 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Cogan, S.F.: Neural stimulation and recording electrodes. Ann. Rev. Biomed. Eng. 10, 275–309 (2008).Google Scholar
2.McCreery, D.B., Yuen, T.G., and Bullara, L.A.: Chronic microstimulation in the feline ventral cochlear nucleus: physiologic and histologic effects. Hear. Res. 149, 223–238 (2000).Google Scholar
3.Woolley, A.J., Desai, H.A., Steckbeck, M.A., Patel, N.K., and Otto, K.J.: In situ characterization of the brain–microdevice interface using device capture histology. J. Neurosci. Methods 201, 67–77 (2011).Google Scholar
4.Gilmour, A.D., Woolley, A.J., Poole-Warren, L.A., Thomson, C.E., and Green, R.A.: A critical review of cell culture strategies for modelling intracortical brain implant material reactions. Biomaterials 91, 23–43 (2016). doi: 10.1016/j.biomaterials.2016.03.011.Google Scholar
5.McCreery, D.B., Yuen, T.G., Agnew, W.F., and Bullara, L.A.: A characterization of the effects on neuronal excitability due to prolonged microstimulation with chronically implanted microelectrodes. IEEE Trans. Biomed. Eng. 44, 931–939 (1997).Google Scholar
6.Onnela, N., Takeshita, H., Kaiho, Y., Kojima, T., Kobayashi, R., Tanaka, T., and Hyttinen, J.: Comparison of electrode materials for the use of retinal prosthesis. Biomed. Mater. Eng. 21, 83–97 (2011).Google Scholar
7.Aregueta-Robles, U.A., Woolley, A.J., Poole-Warren, L.A., Lovell, N.H., and Green, R.A.: Organic electrode coatings for next-generation neural interfaces. Front. Neuroeng. 7, 15 (2014).Google Scholar
8.Ochiai, H., Shibata, H., Sawa, Y., and Katoh, T.: “Living electrode” as a long-lived photoconverter for biophotolysis of water. Proc. Natl. Acad. Sci. USA 77, 2442–2444 (1980).Google Scholar
9.Ochiai, H., Shibata, H., Sawa, Y., Shoga, M., and Ohta, S.: Properties of semiconductor electrodes coated with living films of cyanobacteria. Appl. Biochem. Biotechnol. 8, 289–303 (1983).Google Scholar
10.Campbell, T.E., Hodgson, A.J., and Wallace, G.G.: Incorporation of erythrocytes into polypyrrole to form the basis of a biosensor to screen for rhesus (D) blood groups and rhesus (D) antibodies. Electroanalysis 11, 215–222 (1999).Google Scholar
11.Richardson-Burns, S.M., Hendricks, J.L., Foster, B., Povlich, L.K., Kim, D.H., and Martin, D.C.: Polymerization of the conducting polymer poly(3,4-ethylenedioxythiophene) (PEDOT) around living neural cells. Biomaterials 28, 1539–1552 (2007).Google Scholar
12.Richardson-Burns, S.M., Hendricks, J.L., and Martin, D.C.: Electrochemical polymerization of conducting polymers in living neural tissue. J. Neural Eng. 4, L6 (2007).Google Scholar
13.Ouyang, L., Green, R., Feldman, K.E., and Martin, D.C.: Direct local polymerization of poly (3, 4-ethylenedioxythiophene) in rat cortex. In Progress in Brain Research, edited by Schouenborg, J., Garwicz, M., and Danielsen, N. (Elsevier, Oxford, UK, 194, 2011).Google Scholar
14.Mahoney, M.J. and Anseth, K.S.: Three-dimensional growth and function of neural tissue in degradable polyethylene glycol hydrogels. Biomaterials 27, 2265–2274 (2006).Google Scholar
15.Baek, S., Green, R.A., Granville, A., Martens, P., and Poole-Warren, L.A.: Thin film hydrophilic electroactive polymer coatings for bioelectrodes. J. Mater. Chem. B, Mater. Biol. Med. 1, 3803–3810 (2013).Google Scholar
16.Green, R.A., Hassarati, R.T., Goding, J.A., Baek, S., Lovell, N.H., and Martens, P.J.: Conductive hydrogels: mechanically robust hybrids for use as biomaterials. Macromol. Biosci. 12, 494–501 (2012).Google Scholar
17.Hassarati, R.T., Dueck, W.F., Tasche, C., Carter, P.M., Poole-Warren, L.A., and Green, R.A.: Improving cochlear implant properties through conductive hydrogel coatings. IEEE Trans. Neural Syst. Rehabil. Eng. 22, 411–418 (2014).Google Scholar
18.Goding, J., Gilmour, A., Martens, P., Poole-Warren, L., and Green, R.: Interpenetrating conducting hydrogel materials for neural interfacing electrodes. Adv. Healthc. Mater. 6, 1601177 (2017).Google Scholar
19.Green, R.A., Lim, K.S., Henderson, W.C., Hassarati, R.T., Martens, P.J., Lovell, N.H., and Poole-Warren, L.A.: Living electrodes: tissue engineering the neural interface. IEEE Eng. Med. Biol. Soc. Annu. Conf. 2013, 6957–6960 (2013).Google Scholar
20.Lim, K.S., Alves, M.H., Poole-Warren, L.A., and Martens, P.J.: Covalent incorporation of non-chemically modified gelatin into degradable PVA-tyramine hydrogels. Biomaterials 34, 7097–7105 (2013).Google Scholar
21.Lim, K.S., Kundu, J., Reeves, A., Poole-Warren, L.A., Kundu, S.C., and Martens, P.J.: The influence of silkworm species on cellular interactions with novel PVA/silk sericin hydrogels. Macromol. Biosci. 12, 322–332 (2012).Google Scholar
22.Aregueta-Robles, U.A., Lim, K.S., Martens, P.J., Lovell, N.H., Poole-Warren, L.A., and Green, R.A.: Producing 3D neuronal networks in hydrogels for living bionic device interfaces. In IEEE Engineering in Medicine and Biology Conf. (EMBC), IEEE: Milan, Italy, 2015.Google Scholar
23.Beebe, X. and Rose, T.L.: Charge injection limits of activated iridium oxide electrodes with 0.2 ms pulses in bicarbonate buffered saline (neurological stimulation application). IEEE Trans. Biomed. Eng. 35, 494–495 (1988).Google Scholar
24.Green, R.A., Matteucci, P.B., Dodds, C.W., Palmer, J., Dueck, W.F., Hassarati, R.T., Byrnes-Preston, P.J., Lovell, N.H., and Suaning, G.J.: Laser patterning of platinum electrodes for safe neurostimulation. J. Neural Eng. 11, 056017 (2014).Google Scholar
25.Gilmour, A., Goding, J., Poole-Warren, L.A., Thompson, C.E., and Green, R.A.: In vitro biological assessment of electrode materials for neural interfaces. In 7th IEEE EMBS Conf. on Neural Engineering, 2015.Google Scholar
26.Thomson, C.E., McCulloch, M., Sorenson, A., Barnett, S.C., Seed, B.V., Griffiths, I.R., and McLaughlin, M.: Myelinated, synapsing cultures of murine spinal cord—validation as an in vitro model of the central nervous system. Eur. J. Neurosci. 28, 1–18 (2008).Google Scholar
27.Sorensen, A., Moffat, K., Thomson, C., and Barnett, S.C.: Astrocytes, but not olfactory ensheathing cells or Schwann cells, promote myelination of CNS axons in vitro. Glia 56, 750–763 (2008).Google Scholar
28.Cheong, G.L.M., Lim, K.S., Jakubowicz, A., Martens, P.J., Poole-Warren, L.A., and Green, R.A.: Conductive hydrogels with tailored bioactivity for implantable electrode coatings. Acta Biomater. 10, 1216–1226 (2014).Google Scholar
29.Kozai, T.D., Catt, K., Li, X., Gugel, Z.V., Olafsson, V.T., Vazquez, A.L., and Cui, X.T.: Mechanical failure modes of chronically implanted planar silicon-based neural probes for laminar recording. Biomaterials 37, 25–39 (2015).Google Scholar
30.Lippert, S.A., Rang, E.M., and Grimm, M.J.: The high frequency properties of brain tissue. Biorheology 41, 681–691 (2004).Google Scholar
31.Guo, B., Finne-Wistrand, A., and Albertsson, A.-C.: Degradable and electroactive hydrogels with tunable electrical conductivity and swelling behavior. Chem. Mater. 23, 1254–1262 (2011).Google Scholar
32.De Faveri, S., Maggiolini, E., Miele, E., De Angelis, F., Cesca, F., Benfenati, F., and Fadiga, L.: Bio-inspired hybrid microelectrodes: a hybrid solution to improve long-term performance of chronic intracortical implants. Front. Neuroeng. 7, 7 (2014).Google Scholar
33.Kim, D.-H., Wiler, J.A., Anderson, D.J., Kipke, D.R., and Martin, D.C.: Conducting polymers on hydrogel-coated neural electrode provide sensitive neural recordings in auditory cortex. Acta Biomat. 6, 57–62 (2010).Google Scholar