Large enhancement in neurite outgrowth on a cell membrane-mimicking conducting polymer

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zhu, Bo ^a,b   Luo, Shyh Chyang ^a,c   Zhao, Haichao ^a   Lin, Hsing An ^a,d   Sekine, Jun ^a   Nakao, Aiko ^a   Chen, Chi ^e   Yamashita, Yoshiro ^d   Yu, Hsiao Hua ^a,f  

^a RIKEN   (Japan)

^b DONGHUA UNIVERSITY   (China)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^e RESEARCH CENTER FOR APPLIED SCIENCES   (Taiwan)

^f INSTITUTE OF CHEMISTRY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETIC MATERIAL; BIOPOLYMER; CELL ENZYME; POLY(3,4 ETHYLENEDIOXYTHIOPHENE); UNCLASSIFIED DRUG; BIOMATERIAL; NERVE GROWTH FACTOR; PEPTIDE; POLYMER;

ELECTRICAL POWER; ENZYME ACTIVITY; GROWTH RATE; OPTIMIZATION; POLYMER;

ANIMAL CELL; ARTICLE; BIOENERGY; CELL COMMUNICATION; CELL FUNCTION; CELL SPECIFICITY; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME BINDING; MICROELECTRODE; NERVE FIBER GROWTH; NERVE FIBER MEMBRANE CONDUCTANCE; NONHUMAN; POLYMERIZATION; PROTEIN INTERACTION; PROTEIN SECRETION; RAT; RESPONSE TIME; 3T3 CELL LINE; ANIMAL; CELL ADHESION; CHEMISTRY; ELECTRIC CONDUCTIVITY; EQUIPMENT DESIGN; MOUSE; NERVE CELL; NEURITE; PC12 CELL LINE; PHYSIOLOGY; SCHWANN CELL; SECRETION (PROCESS);

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOMIMETIC MATERIALS; CELL ADHESION; ELECTRIC CONDUCTIVITY; ELECTRIC STIMULATION; EQUIPMENT DESIGN; MICE; NERVE GROWTH FACTOR; NEURITES; NEURONS; NIH 3T3 CELLS; PC12 CELLS; PEPTIDES; POLYMERS; RATS; SCHWANN CELLS;

EID: 84905024378     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5523     Document Type: Article

References (69)

1. Kozai, T. D. Y. et al. Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat. Mater. 11, 1065-1073 (2012).
2. Grill, W. M., Norman, S. E. & Bellamkonda, R. V. Implanted neural interfaces: biochallenges and engineered solutions. Annu. Rev. Biomed. Eng. 11, 1-24 (2009).
3. Subbaroyan, J., Martin, D. C. & Kipke, D. R. A finite-element model of the mechanical effects of implantable microelectrodes in the cerebral cortex. J. Neural Eng. 2, 103-113 (2005). (Pubitemid 41740528)
4. Lee, H., Bellamkonda, R. V., Sun, W. & Levenston, M. E. Biomechanical analysis of silicon microelectrode-induced strain in the brain. J. Neural Eng. 2, 81-89 (2005). (Pubitemid 41740525)
5. Rousche, P. J. & Normann, R. A. Chronic recording capability of the Utah Intracortical Electrode Array in cat sensory cortex. J. Neurosci. Methods 82, 1-15 (1998). (Pubitemid 28335467)
6. Biran, R., Martin, D. C. & Tresco, P. A. Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp. Neurol. 195, 115-126 (2005). (Pubitemid 41116819)
7. Ward, M. P., Rajdev, P., Ellison, C. & Irazoqui, P. P. Toward a comparison of microelectrodes for acute and chronic recordings. Brain Res. 1282, 183-200 (2009).
8. Cogan, S. F. Neural stimulation and recording electrodes. Annu. Rev. Biomed. Eng. 10, 275-309 (2008).
9. Rose, T. L. & Robblee, L. S. Electrical stimulation with Pt electrodes. VIII. Electrochemically safe charge injection limits with 0.2 ms pulses (neuronal application). IEEE Trans. Biomed. Eng. 37, 1118-1120 (1990).
10. Gawad, S. et al. Substrate arrays of iridium oxide microelectrodes for in vitro neuronal interfacing. Front. Neuroeng. 2, 1 (2009).
11. Green, R. A. et al. Performance of conducting polymer electrodes for stimulating neuroprosthetics. J. Neural Eng. 10, 016009 (2013).
12. Discher, D. E., Janmey, P. & Wang, Y.-L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139 (2005).
13. Mitragotri, S. & Lahann, J. Physical approaches to biomaterial design. Nat. Mater. 8, 15-23 (2009).
14. Otero, T. F., Martinez, J. G. & Arias-Pardilla, J. Biomimetic electrochemistry from conducting polymers. A review: artificial muscles, smart membranes, smart drug delivery and computer/neuron interfaces. Electrochim. Acta 84, 112-128 (2012).
15. Ludwig, K. A., Uram, J. D., Yang, J., Martin, D. C. & Kipke, D. R. Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film. J. Neural Eng. 3, 59-70 (2006). (Pubitemid 43332372)
16. Cui, X. T. & Zhou, D. D. Poly(3,4-ethylenedioxythiophene) for chronic neural stimulation. IEEE Trans. Neural Syst. Rehabil. Eng. 15, 502-508 (2007). (Pubitemid 350274180)
17. Wallace, G. G., Moulton, S. E. & Clark, G. M. Electrode-cellular interface. Science 324, 185-186 (2009).
18. Guimard, N. K., Gomez, N. & Schmidt, C. E. Conducting polymers in biomedical engineering. Prog. Polym. Sci. 32, 876-921 (2007). (Pubitemid 47198288)
19. Asplund, M., Nyberg, T. & Inganäs, O. Electroactive polymers for neural interfaces. Polym. Chem. 1, 1374-1391 (2010).
20. Ghasemi-Mobarakeh, L. et al. Application of conductive polymers, scaffolds and electrical stimulation for nerve tissue engineering. J. Tissue Eng. Regen. M 5, e17-e35 (2011).
21. Thompson, B. C., Moulton, S. E., Richardson, R. T. & Wallace, G. G. Effect of the dopant anion in polypyrrole on nerve growth and release of a neurotrophic protein. Biomaterials 32, 3822-3831 (2011).
22. Richardson-Burns, S. M. et al. Polymerization of the conducting polymer poly(3,4-ethylenedioxythiophene) (PEDOT) around living neural cells. Biomaterials 28, 1539-1552 (2007). (Pubitemid 46027252)
23. Huang, L. et al. Synthesis and characterization of electroactive and biodegradable ABA block copolymer of polylactide and aniline pentamer. Biomaterials 28, 1741-1751 (2007). (Pubitemid 46123544)
24. Schmidt, C. E., Shastri, V. R., Vacanti, J. P. & Langer, R. Stimulation of neurite outgrowth using an electrically conducting polymer. Proc. Natl Acad. Sci. USA 94, 8948-8953 (1997). (Pubitemid 27357762)
25. Cui, X. & Martin, D. C. Electrochemical deposition and characterization of poly(3,4-ethylenedioxythiophene) on neural microelectrode arrays. Sensor Actuat. B Chem. 89, 92-102 (2003).
26. Nyberg, T., Inganäs, O. & Jerregård, H. Polymer hydrogel microelectrodes for neural communication. Biomed. Microdevices 4, 43-52 (2002). (Pubitemid 34240363)
27. Lee, J. Y., Bashur, C. A., Goldstein, A. S. & Schmidt, C. E. Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. Biomaterials 30, 4325-4335 (2009).
28. Moroder, P. et al. Material properties and electrical stimulation regimens of polycaprolactone fumarate-polypyrrole scaffolds as potential conductive nerve conduits. Acta Biomater. 7, 944-953 (2011).
29. Gomez, N. & Schmidt, C. E. Nerve growth factor-immobilized polypyrrole: Bioactive electrically conducting polymer for enhanced neurite extension. J. Biomed. Mater. Res. A 81A, 135-149 (2007). (Pubitemid 46435461)
30. Lee, J. Y. et al. Nerve growth factor-immobilized electrically conducting fibrous scaffolds for potential use in neural engineering applications. IEEE Trans. Nanobioscience 11, 15-21 (2012).
31. Liu, X., Yue, Z., Higgins, M. J. & Wallace, G. G. Conducting polymers with immobilised fibrillar collagen for enhanced neural interfacing. Biomaterials 32, 7309-7317 (2011).
32. Yamato, H., Ohwa, M. & Wernet, W. Stability of polypyrrole and poly(3,4-ethylenedioxythiophene) for biosensor application. J. Electroanal. Chem. 397, 163-170 (1995).
33. Green, R. A., Lovell, N. H. & Poole-Warren, L. A. Cell attachment functionality of bioactive conducting polymers for neural interfaces. Biomaterials 30, 3637-3644 (2009).
34. Venkatraman, S. et al. in Proceedings of the 4th International IEEE EMBS Conference on Neural Engineering 383-386 (Antalya, 2009).
35. Moulton, S. E., Higgins, M. J., Kapsa, R. M. I. & Wallace, G. G. Organic bionics: a new dimension in neural communications. Adv. Funct. Mater. 2, 2003-2014 (2012).
36. Simon, D. T. et al. Organic electronics for precise delivery of neurotransmitters to modulate mammalian sensory function. Nat. Mater. 8, 742-746 (2009).
37. Yang, S. Y. et al. Detection of transmitter release from single living cells using conducting polymer microelectrodes. Adv. Mater. 23, H184-H188 (2011).
38. Lin, P., Yan, F., Yu, J., Chan, H. L. W. & Yang, M. The application of organic electrochemical transistors in cell-based biosensors. Adv. Mater. 22, 3655-3660 (2010).
39. Chikar, J. A. et al. The use of a dual PEDOT and RGD-functionalized alginate hydrogel coating to provide sustained drug delivery and improved cochlear implant function. Biomaterials 33, 1982-1990 (2012).
40. Abidian, M. R., Ludwig, K. A., Marzullo, T. C., Martin, D. C. & Kipke, D. R. Interfacing conducting polymer nanotubes with the central nervous system: chronic neural recording using poly(3,4-ethylenedioxythiophene) nanotubes. Adv. Mater. 21, 3764-3770 (2009).
41. Harris, A. R. et al. Conducting polymer coated neural recording electrodes. J. Neural Eng. 10, 16004 (2013).
42. Asplund, M. et al. Toxicity evaluation of PEDOT/biomolecular composites intended for neural communication electrodes. Biomed. Mater. 4, 045009 (2009).
43. Polikov, V. S., Tresco, P. A. & Reichert, W. M. Response of brain tissue to chronically implanted neural electrodes. J. Neurosci. Meth. 148, 1-18 (2005). (Pubitemid 41423453)
44. Moxon, K. A. et al. Long-term recordings of multiple, single-neurons for clinical applications: the emerging role of the bioactive microelectrode. Materials 2, 1762-1794 (2009).
45. Povlich, L. K. et al. Synthesis, copolymerization and peptide-modification of carboxylic acid-functionalized 3,4- ethylenedioxythiophene (EDOTacid) for neural electrode interfaces. Biochim. Biophys. Acta 1830, 4288-4293 (2012).
46. Cui, X., Wiler, J., Dzaman, M., Altschuler, R. & Martin, D. In vivo studies of polypyrrole/peptide coated neural probes. Biomaterials 24, 777-787 (2003). (Pubitemid 35449830)
47. Wadhwa, R., Lagenaur, C. & Cui, X. Electrochemically controlled release of dexamethasone from conducting polymer polypyrrole coated electrode. J. Control Release 110, 531-541 (2006). (Pubitemid 43163443)
48. Fang, J. et al. Conjugated zwitterionic polyelectrolyte as the charge injection layer for high-performance polymer light-emitting diodes. J. Am. Chem. Soc. 133, 683-685 (2011).
49. Cardoso, J., Huanosta, A. & Manero, O. Ionic conductivity studies on salt-polyzwitterion systems. Macromolecules 24, 2890-2895 (1991). (Pubitemid 21653238)
50. Singer, S. J. & Nicolson, G. L. The fluid mosaic model of the structure of cell membranes. Science 175, 720-731 (1972).
51. Bangham, A. D. A correlation between surface charge and coagulant action of phospholipids. Nature 192, 1197-1198 (1961).
52. Zwaal, R. F. A., Comfurius, P. & van Deenen, L. L. M. Membrane asymmetry and blood coagulation. Nature 268, 358-360 (1977). (Pubitemid 8142006)
53. Hayward, J. A. & Chapman, D. Biomembrane surfaces as models for polymer design: the potential for haemocompatibility. Biomaterials 5, 135-142 (1984). (Pubitemid 14116173)
54. Chen, S., Zheng, J., Li, L. & Jiang, S. Strong resistance of phosphorylcholine selfassembled monolayers to protein adsorption: insights into nonfouling properties of zwitterionic materials. J. Am. Chem. Soc. 127, 14473-14478 (2005). (Pubitemid 41457607)
55. Moro, T. et al. Surface grafting of artificial joints with a biocompatible polymer for preventing periprosthetic osteolysis. Nat. Mater. 3, 829-836 (2004).
56. Holmlin, R. E., Chen, X., Chapman, R. G., Takayama, S. & Whitesides, G. M. Zwitterionic SAMs that resist nonspecific adsorption of protein from aqueous buffer. Langmuir 17, 2841-2850 (2001). (Pubitemid 35330542)
57. Ishihara, K., Ueda, T. & Nakabayashi, N. Preparation of phospholipid polymers and their properties as polymer hydrogel membranes. Polym. J. 22, 355-360 (1990). (Pubitemid 20719572)
58. Gorin, G., Martic, P. A. & Doughty, G. Kinetics of the reaction of N-ethylmaleimide with cysteine and some congeners. Arch. Biochem. Biophys. 115, 593-597 (1966).
59. Rana, D. & Matsuura, T. Surface modifications for antifouling membranes. Chem. Rev. 110, 2448-2471 (2010).
60. Tashiro, K. et al. A synthetic peptide containing the IKVAV sequence from the A chain of laminin mediates cell attachment, migration, and neurite outgrowth. J. Biol. Chem. 264, 16174-16182 (1989). (Pubitemid 19238381)
61. Silva, G. A. et al. Selective differentiation of neural progenitor cells by highepitope density nanofibers. Science 303, 1352-1355 (2004). (Pubitemid 38269424)
62. Bhatheja, K. & Field, J. Schwann cells: origins and role in axonal maintenance and regeneration. Int. J. Biochem. Cell B 38, 1995-1999 (2006). (Pubitemid 44397614)
63. Wan, L., Zhang, S., Xia, R. & Ding, W. Short-term low-frequency electrical stimulation enhanced remyelination of injured peripheral nerves by inducing the promyelination effect of brain-derived neurotrophic factor on Schwann cell polarization. J. Neurosci. Res. 88, 2578-2587 (2010).
64. Huang, J., Ye, Z., Hu, X., Lu, L. & Luo, Z. Electrical stimulation induces calcium-dependent release of NGF from cultured Schwann cells. Glia 58, 622-631 (2010).
65. Hunag, J. et al. Electrical regulation of Schwann cells using conductive polypyrrole/chitosan polymers. J. Biomed. Mater. Res. 93A, 164-174 (2010).
66. Lima, A., Schottland, P., Sadki, S. & Chevrot, C. Electropolymerization of 3,4-ethylenedioxythiophene and 3,4- ethylenedioxythiophene methanol in the presence of dodecylbenzenesulfonate. Synth. Met. 93, 33-41 (1998). (Pubitemid 128393551)
67. Akoudad, S. & Roncali, J. Modification of the electrochemical and electronic properties of electrogenerated poly(3,4-ethylenedioxythiophene) by hydroxymethyl and oligo(oxyethylene) substituents. Electrochem. Commun. 2, 72-76 (2000).
68. Mohamed Ali, E., Kantchev, E. A. B., Yu, H.-h. & Ying, J. Y. Conductivity shift of polyethylenedioxythiophenes (PEDOTs) in aqueous solutions from side-chain charge perturbation. Macromolecules 40, 6025-6027 (2007). (Pubitemid 47329042)
69. Luo, S.-C. et al. PEDOT nanobiointerfaces: thin, ultrasmooth, and functionalized poly(3,4-ethylenedioxythiophene) films with in vitro and in vivo biocompatibility. Langmuir. 24, 8071-8077 (2008).