Neural stem cell differentiation by electrical stimulation using a cross-linked PEDOT substrate: Expanding the use of biocompatible conjugated conductive polymers for neural tissue engineering

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 6, 2015, Pages 1158-1168

  Pires, Filipa ^a,b,c   Ferreira, Quirina ^a   Rodrigues, Carlos A V ^b,c   Morgado, Jorge ^a,b   Ferreira, Frederico Castelo ^b,c  

^a INSTITUTO DE TELECOMUNICAÇÕES   (Portugal)

^b INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^c Instituto de Biotecnologia e Bioengenharia Lisboa   (Portugal)

Author keywords

Conjugated conductive polymer; Cross linked PEDOT:PSS; Electrical stimulation; Human neural stem cell; Neuron

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; LAMININ; POLY(3,4 ETHYLENEDIOXYTHIOPHENE); POLYMER; POLYSTYRENESULFONIC ACID; THIOPHENE DERIVATIVE; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; BIOMATERIAL; CROSS LINKING REAGENT; POLY(3,4-ETHYLENEDIOXYTHIOPHENE)-POLY(STYRENESULFONATE); POLYSTYRENE DERIVATIVE;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CELL DIFFERENTIATION; CELL FATE; CELL POPULATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; CYTOTOXICITY; ELECTROSTIMULATION; HUMAN; HUMAN CELL; L929 CELL LINE; NERVE FIBER GROWTH; NEURAL STEM CELL; PRIORITY JOURNAL; TISSUE ENGINEERING; CELL LINE; CELL LINEAGE; CHEMISTRY; ELECTRIC CONDUCTIVITY; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; PROCEDURES; SURFACE PROPERTY; TIME; TISSUE SCAFFOLD;

BIOCOMPATIBLE MATERIALS; BIOMARKERS; CELL LINE; CELL LINEAGE; CROSS-LINKING REAGENTS; ELECTRIC CONDUCTIVITY; ELECTRIC STIMULATION; HUMANS; MICROSCOPY, ATOMIC FORCE; NEURAL STEM CELLS; NEUROGENESIS; POLYSTYRENES; SURFACE PROPERTIES; THIOPHENES; TIME FACTORS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84923313720     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.01.020     Document Type: Article

References (131)

1. J.Y. Wong, R. Langer, and D.E. Ingber Electrically conducting polymers can noninvasively control the shape and growth of mammalian cells Proc. Natl. Acad. Sci. 91 1994 3201 3204
2. R. Ravichandran, S. Sundarrajan, J.R. Venugopal, S. Mukherjee, and S. Ramakrishna Applications of conducting polymers and their issues in biomedical engineering J. R. Soc. Interface 7 2010 S559 S579
3. N.K. Guimard, N. Gomez, and C.E. Schmidt Conducting polymers in biomedical engineering Prog. Polym. Sci. 32 2007 876 921
4. K. Aboody, A. Capela, N. Niazi, J.H. Stern, and S. Temple Translating stem cell studies to the clinic for CNS repair: current state of the art and the need for a Rosetta Stone Neuron 70 2011 597 613
5. T. Gorba, and L. Conti Neural stem cells as tools for drug discovery: novel platforms and approaches Expert Opin. Drug Discov. 8 2013 1083 1094
6. Z. Kokaia, G. Martino, M. Schwartz, and O. Lindvall Cross-talk between neural stem cells and immune cells: the key to better brain repair [quest] Nat. Neurosci. 15 2012 1078 1087
7. J.E. Collazos-Castro, J.L. Polo, G.R. Hernández-Labrado, V. Padial-Cañete, and C. García-Rama Bioelectrochemical control of neural cell development on conducting polymers Biomaterials 31 2010 9244 9255
8. A. Subramanian, U.M. Krishnan, and S. Sethuraman Development of biomaterial scaffold for nerve tissue engineering: biomaterial mediated neural regeneration J. Biomed. Sci. 16 2009 108
9. X. Wang Evaluation of biocompatibility of polypyrrole in vitro and in vivo J. Biomed. Mater. Res. A 68 2004 411 422
10. P.M. George Fabrication and biocompatibility of polypyrrole implants suitable for neural prosthetics Biomaterials 26 2005 3511 3519
11. S. Bhadra, D. Khastgir, N.K. Singha, and J.H. Lee Progress in preparation, processing and applications of polyaniline Prog. Polym. Sci. 34 2009 783 810
12. W.-S. Huang, B.D. Humphrey, and A.G. MacDiarmid Polyaniline, a novel conducting polymer. Morphology and chemistry of its oxidation and reduction in aqueous electrolytes J. Chem. Soc. Faraday Trans.1: Phys. Chem. Condens. Phases 82 1986 2385 2400
13. M. Mattioli-Belmonte Tailoring biomaterial compatibility: in vivo tissue response versus in vitro cell behavior Int. J. Artif. Organs 26 2003 1077 1085
14. M. Asplund Toxicity evaluation of PEDOT/biomolecular composites intended for neural communication electrodes Biomed. Mater. 4 2009 045009
15. D. Kumar, and R. Sharma Advances in conductive polymers Eur. Polym. J. 34 1998 1053 1060
16. A. Kotwal, and C.E. Schmidt Electrical stimulation alters protein adsorption and nerve cell interactions with electrically conducting biomaterials Biomaterials 22 2001 1055 1064
17. V. Lundin, A. Herland, M. Berggren, E.W. Jager, and A.I. Teixeira Control of neural stem cell survival by electroactive polymer substrates PLoS One 6 2011 e18624
18. Y. Li, K.G. Neoh, and E.-T. Kang Plasma protein adsorption and thrombus formation on surface functionalized polypyrrole with and without electrical stimulation J. Colloid Interface Sci. 275 2004 488 495
19. X. Cui, J. Wiler, M. Dzaman, R.A. Altschuler, and D.C. Martin In vivo studies of polypyrrole/peptide coated neural probes Biomaterials 24 2003 777 787
20. E. Ostrakhovitch, J. Byers, K. O'Neil, and O. Semenikhin Directed differentiation of embryonic P19 cells and neural stem cells into neural lineage on conducting PEDOT-PEG and ITO glass substrates Arch. Biochem. Biophys. 528 2012 21 31
21. H. Castano, E.A. O'Rear, P.S. McFetridge, and V.I. Sikavitsas Polypyrrole thin films formed by admicellar polymerization support the osteogenic differentiation of mesenchymal stem cells Macromol. Biosci. 4 2004 785 794
22. L. Zhang, W.R. Stauffer, E.P. Jane, P.J. Sammak, and X.T. Cui Enhanced differentiation of embryonic and neural stem cells to neuronal fates on laminin peptides doped polypyrrole Macromol. Biosci. 10 2010 1456 1464
23. G. Shi, M. Rouabhia, Z. Wang, L.H. Dao, and Z. Zhang A novel electrically conductive and biodegradable composite made of polypyrrole nanoparticles and polylactide Biomaterials 25 2004 2477 2488
24. C. Thomas, K. Zong, P. Schottland, and J. Reynolds Poly (3, 4-alkylenedioxypyrrole) s as highly stable aqueous-compatible conducting polymers with biomedical implications Adv. Mater. 12 2000 222 225
25. X. Cui, J.F. Hetke, J.A. Wiler, D.J. Anderson, and D.C. Martin Electrochemical deposition and characterization of conducting polymer polypyrrole/PSS on multichannel neural probes Sensors Actuators A Phys. 93 2001 8 18
26. X. Cui Surface modification of neural recording electrodes with conducting polymer/biomolecule blends J. Biomed. Mater. Res. 56 2001 261 272
27. X. Cui, and D.C. Martin Electrochemical deposition and characterization of poly (3, 4-ethylenedioxythiophene) on neural microelectrode arrays Sensors Actuators B Chem. 89 2003 92 102
28. X.T. Cui, and D.D. Zhou Poly (3, 4-ethylenedioxythiophene) for chronic neural stimulation IEEE Trans. Neural Syst. Rehabil. Eng. 15 2007 502 508
29. J. Albuquerque A simple method to estimate the oxidation state of polyanilines Synth. Met. 113 2000 19 22
30. N.V. Blinova, J. Stejskal, M. Trchová, and J. Prokeš Control of polyaniline conductivity and contact angles by partial protonation Polym. Int. 57 2008 66 69
31. T. Lindfors, and L. Harju Determination of the protonation constants of electrochemically polymerized poly (aniline) and poly (< i>o -methylaniline) films Synth. Met. 158 2008 233 241
32. P. Bober, T. Lindfors, M. Pesonen, and J. Stejskal Enhanced pH stability of conducting polyaniline by reprotonation with perfluorooctanesulfonic acid Synth. Met. 178 2013 52 55
33. J. Stejskal, and R. Gilbert Polyaniline. Preparation of a conducting polymer (IUPAC technical report) Pure Appl. Chem. 74 2002 857 867
34. J. Huang Investigation of the effects of doping and post-deposition treatments on the conductivity, morphology, and work function of poly (3, 4-ethylenedioxythiophene)/poly (styrene sulfonate) films Adv. Funct. Mater. 15 2005 290 296
35. F. Louwet PEDOT/PSS: synthesis, characterization, properties and applications Synth. Met. 135 2003 115 117
36. S.J. Wilks, S.M. Richardson-Burns, J.L. Hendricks, D.C. Martin, and K.J. Otto Poly (3, 4-ethylenedioxythiophene) as a micro-neural interface material for electrostimulation Front. Neuroeng. 2 2009
37. M.R. Abidian, and D.C. Martin Experimental and theoretical characterization of implantable neural microelectrodes modified with conducting polymer nanotubes Biomaterials 29 2008 1273 1283
38. K.A. Ludwig, J.D. Uram, J. Yang, D.C. Martin, and D.R. Kipke Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly (3, 4-ethylenedioxythiophene)(PEDOT) film J. Neural Eng. 3 2006 59
39. T. Nyberg, A. Shimada, and K. Torimitsu Ion conducting polymer microelectrodes for interfacing with neural networks J. Neurosci. Methods 160 2007 16 25
40. Y. Furukawa, A. Shimada, K. Kato, H. Iwata, and K. Torimitsu Monitoring neural stem differentiation using PEDOT-PSS based MEA Biochim. Biophys. Acta Gen. Subj. 1830 2013 4329 4333
41. M.H. Bolin Nano-fiber scaffold electrodes based on PEDOT for cell stimulation Sensors Actuators B Chem. 142 2009 451 456
42. N. Srivastava Neuronal differentiation of embryonic stem cell derived neuronal progenitors can be regulated by stretchable conducting polymers Tissue Eng. A 19 2013 1984 1993
43. D. Esrafilzadeh, J.M. Razal, S.E. Moulton, E.M. Stewart, and G.G. Wallace Multifunctional conducting fibres with electrically controlled release of ciprofloxacin J. Control. Release 169 2013 313 320
44. L. Jin A facile approach for the fabrication of core-shell PEDOT nanofiber mats with superior mechanical properties and biocompatibility J. Mater. Chem. B 1 2013 1818 1825
45. A. Townsend-Nicholson, and S.N. Jayasinghe Cell electrospinning: a unique biotechnique for encapsulating living organisms for generating active biological microthreads/scaffolds Biomacromolecules 7 2006 3364 3369
46. S.N. Jayasinghe Cell electrospinning: a novel tool for functionalising fibres, scaffolds and membranes with living cells and other advanced materials for regenerative biology and medicine Analyst 138 2013 2215 2223
47. C.E. Schmidt, V.R. Shastri, J.P. Vacanti, and R. Langer Stimulation of neurite outgrowth using an electrically conducting polymer Proc. Natl. Acad. Sci. 94 1997 8948 8953
48. E. Stewart Electrical stimulation using conductive polymer polypyrrole promotes differentiation of human neural stem cells: a biocompatible platform for translational neural tissue engineering Tissue Eng. 2014 10.1089/ten.tec.2014.0338 [ahead of print]
49. B.C. Thompson Conducting polymers, dual neurotrophins and pulsed electrical stimulation - dramatic effects on neurite outgrowth J. Control. Release 141 2010 161 167
50. J. Xie Conductive core-sheath nanofibers and their potential application in neural tissue engineering Adv. Funct. Mater. 19 2009 2312 2318
51. J. Serra Moreno, M.G. Sabbieti, D. Agas, L. Marchetti, and S. Panero Polysaccharides immobilized in polypyrrole matrices are able to induce osteogenic differentiation in mouse mesenchymal stem cells J. Tissue Eng. Regen. Med. 8 2012 989 999
52. J.-W. Lee, F. Serna, J. Nickels, and C.E. Schmidt Carboxylic acid-functionalized conductive polypyrrole as a bioactive platform for cell adhesion Biomacromolecules 7 2006 1692 1695
53. H.-K. Song, B. Toste, K. Ahmann, D. Hoffman-Kim, and G. Palmore Micropatterns of positive guidance cues anchored to polypyrrole doped with polyglutamic acid: a new platform for characterizing neurite extension in complex environments Biomaterials 27 2006 473 484
54. D.H. Kim, M. Abidian, and D.C. Martin Conducting polymers grown in hydrogel scaffolds coated on neural prosthetic devices J. Biomed. Mater. Res. A 71 2004 577 585
55. D. Cheng, H. Xia, and H.S. Chan Synthesis and characterization of surface-functionalized conducting polyaniline-chitosan nanocomposite J. Nanosci. Nanotechnol. 5 2005 466 473
56. M. Gizdavic-Nikolaidis, S. Ray, J.R. Bennett, A.J. Easteal, and R.P. Cooney Electrospun functionalized polyaniline copolymer-based nanofibers with potential application in tissue engineering Macromol. Biosci. 10 2010 1424 1431
57. M. Li, Y. Guo, Y. Wei, A.G. MacDiarmid, and P.I. Lelkes Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications Biomaterials 27 2006 2705 2715
58. T. Sergeyeva, N. Lavrik, S. Piletsky, A. Rachkov, and A. El'Skaya Polyaniline label-based conductometric sensor for IgG detection Sensors Actuators B Chem. 34 1996 283 288
59. M. Tahhan, V.-T. Truong, G.M. Spinks, and G.G. Wallace Carbon nanotube and polyaniline composite actuators∗ Smart Mater. Struct. 12 2003 626
60. G.M. Spinks, B. Xi, V.-T. Truong, and G.G. Wallace Actuation behaviour of layered composites of polyaniline, carbon nanotubes and polypyrrole Synth. Met. 151 2005 85 91
61. G.M. Spinks, V. Mottaghitalab, M. Bahrami-Samani, P.G. Whitten, and G.G. Wallace Carbon-nanotube-reinforced polyaniline fibers for high-strength artificial muscles Adv. Mater. 18 2006 637 640
62. S.M. Richardson-Burns Polymerization of the conducting polymer poly (3, 4-ethylenedioxythiophene)(PEDOT) around living neural cells Biomaterials 28 2007 1539 1552
63. N. Martino A Polymer Optoelectronic Interface Restores Light Sensitivity in Blind Rat Retinas 2013
64. M. Manceau, A. Rivaton, J.-L. Gardette, S. Guillerez, and N. Lemaître The mechanism of photo-and thermooxidation of poly (3-hexylthiophene)(P3HT) reconsidered Polym. Degrad. Stab. 94 2009 898 907
65. R. Rodrigues, Q. Ferreira, A.L. Mendonça, and J. Morgado Template role of polyhexylthiophene nanowires on efficient bilayer photovoltaic cells Synth. Met. 190 2014 72 78
66. G. Brotas Synthesis, characterization, and applications in photovoltaic cells of oxetane-functionalized P3HT derivatives J. Polym. Sci. A Polym. Chem. 52 2014 652 663
67. G. Brotas, J. Farinhas, Q. Ferreira, J. Morgado, and A. Charas Nanostructured layers of a new cross-linkable poly (3-hexylthiophene) in organic photovoltaic cells Synth. Met. 162 2012 2052 2058
68. N. Martino, D. Ghezzi, F. Benfenati, G. Lanzani, and M.R. Antognazza Organic semiconductors for artificial vision J. Mater. Chem. B 1 2013 3768 3780
69. D. Ghezzi A hybrid bioorganic interface for neuronal photoactivation Nat. Commun. 2 2011 166
70. R.F.A. Rodrigues, A. Charas, J. Morgado, and A.N. Maçanita Self-organization and excited-state dynamics of a fluorene-bithiophene copolymer (F8T2) in solution Macromolecules 43 2009 765 771
71. G. Bernardo Synergistic effect on the efficiency of polymer light-emitting diodes upon blending of two green-emitting polymers J. Appl. Phys. 108 2010 014503
72. Z. Liu, H. Li, Z. Qiu, S.L. Zhang, and Z.B. Zhang SMALL-hysteresis thin-film transistors achieved by facile dip-coating of nanotube/polymer composite Adv. Mater. 24 2012 3633 3638
73. 2 J. Mater. Chem. 18 2008 654 659
74. J. Farinhas Nanostructured donor/acceptor interfaces in photovoltaic cells using columnar-grain films of a cross-linked poly (fluorene-alt-bithiophene) J. Mater. Chem. 21 2011 12511 12519
75. Z.-S. Kim, S.C. Lim, S.H. Kim, Y.S. Yang, and D.-H. Hwang Biotin-functionalized semiconducting polymer in an organic field effect transistor and application as a biosensor Sensors 12 2012 11238 11248
76. M. Ates, T. Karazehir, and A.S. Sarac Conducting polymers and their applications Curr. Phys. Chem. 2 2012 224 240
77. Z. Matharu, S.K. Arya, S. Singh, V. Gupta, and B. Malhotra Langmuir-Blodgett film based on MEH-PPV for cholesterol biosensor Anal. Chim. Acta 634 2009 243 249
78. Van den Bogaert, R. (Google Patents, 2005).
79. L.H. Jimison Measurement of barrier tissue integrity with an organic electrochemical transistor Adv. Mater. 24 2012 5919 5923
80. P.A. Levermore, R. Jin, X. Wang, J.C. de Mello, and D.D. Bradley Organic light-emitting diodes based on poly (9, 9-dioctylfluorene-co-bithiophene)(F8T2) Adv. Funct. Mater. 19 2009 950 957
81. R. Donato Differential development of neuronal physiological responsiveness in two human neural stem cell lines BMC Neurosci. 8 2007 36
82. E. Stavrinidou Direct measurement of ion mobility in a conducting polymer Adv. Mater. 25 2013 4488 4493
83. R. Hoffrogge 2-DE proteome analysis of a proliferating and differentiating human neuronal stem cell line (ReNcell VM) Proteomics 6 2006 1833 1847
84. W. Strober Trypan blue exclusion test of cell viability Curr. Protoc. Immunol. A 3B. 1-A. 3B. 2 2001
85. S. Casarosa, J. Zasso, and L. Conti Systems for ex-vivo Isolation and Culturing of Neural Stem Cells 2013
86. J.C. Conover, and R.Q. Notti The neural stem cell niche Cell Tissue Res. 331 2008 211 224
87. P. Hall, J. Lathia, and M. Caldwell Laminin enhances the growth of human neural stem cells in defined culture media BMC Neurosci. 9 2008 71
88. M. Lampin, R. Warocquier-Clérout, C. Legris, M. Degrange, and M. Sigot-Luizard Correlation between substratum roughness and wettability, cell adhesion, and cell migration J. Biomed. Mater. Res. 36 1997 99 108
89. A. Thapa, T.J. Webster, and K.M. Haberstroh Polymers with nano-dimensional surface features enhance bladder smooth muscle cell adhesion J. Biomed. Mater. Res. A 67 2003 1374 1383
90. A.-S. Andersson Nanoscale features influence epithelial cell morphology and cytokine production Biomaterials 24 2003 3427 3436
91. F. Yang, C. Xu, M. Kotaki, S. Wang, and S. Ramakrishna Characterization of neural stem cells on electrospun poly (l-lactic acid) nanofibrous scaffold J. Biomater. Sci. Polym. Ed. 15 2004 1483 1497
92. Q. Ferreira, G. Bernardo, A. Charas, L.S. Alcácer, and J. Morgado Polymer light-emitting diode interlayers' formation studied by current-sensing atomic force microscopy and scaling laws J. Phys. Chem. C 114 2009 572 579
93. C. Ionescu-Zanetti, A. Mechler, S.A. Carter, and R. Lal Semiconductive polymer blends: correlating structure with transport properties at the nanoscale Adv. Mater. 16 2004 385 389
94. X. Li, and J. Kolega Effects of direct current electric fields on cell migration and actin filament distribution in bovine vascular endothelial cells J. Vasc. Res. 39 2002 391 404
95. A.Y. Chan EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells J. Cell Sci. 111 1998 199 211
96. J. Settleman Tension precedes commitment - even for a stem cell Mol. Cell 14 2004 148 150
97. R. McBeath, D.M. Pirone, C.M. Nelson, K. Bhadriraju, and C.S. Chen Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell 6 2004 483 495
98. A.M. Rajnicek, L.E. Foubister, and C.D. McCaig Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric field J. Cell Sci. 119 2006 1723 1735
99. M.D. Treiser Cytoskeleton-based forecasting of stem cell lineage fates Proc. Natl. Acad. Sci. 107 2010 610 615
100. G. Thrivikraman, G. Madras, and B. Basu Intermittent electrical stimuli for guidance of human mesenchymal stem cell lineage commitment towards neural-like cells on electroconductive substrates Biomaterials 35 2014 6219 6235
101. X. Yao, R. Peng, and J. Ding Effects of aspect ratios of stem cells on lineage commitments with and without induction media Biomaterials 34 2013 930 939
102. Y.-J. Chang, C.-J. Tsai, F.-G. Tseng, T.-J. Chen, and T.-W. Wang Micropatterned stretching system for the investigation of mechanical tension on neural stem cells behavior Nanomed.: Nanotechnol., Biol. Med. 9 2013 345 355
103. M.R. Cho, H.S. Thatte, R.C. Lee, and D. Golan Reorganization of microfilament structure induced by ac electric fields FASEB J. 10 1996 1552 1558
104. I. Titushkin, and M. Cho Regulation of cell cytoskeleton and membrane mechanics by electric field: role of linker proteins Biophys. J. 96 2009 717 728
105. M.R. Cho, H. Thatte, R. Lee, and D. Golan Induced redistribution of cell surface receptors by alternating current electric fields FASEB J. 8 1994 771 776
106. M. Zhao, A. Dick, J.V. Forrester, and C.D. McCaig Electric field-directed cell motility involves up-regulated expression and asymmetric redistribution of the epidermal growth factor receptors and is enhanced by fibronectin and laminin Mol. Biol. Cell 10 1999 1259 1276
107. M.S. Lord, M. Foss, and F. Besenbacher Influence of nanoscale surface topography on protein adsorption and cellular response Nano Today 5 2010 66 78
108. H.T. Nguyen Electric field stimulation through a substrate influences Schwann cell and extracellular matrix structure J. Neural Eng. 10 2013 046011
109. M.R. Cho A review of electrocoupling mechanisms mediating facilitated wound healing IEEE Trans. Plasma Sci. 30 2002 1504 1515
110. M. Zhao Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN Nature 442 2006 457 460
111. Y. Li Engineering cell alignment in vitro Biotechnol. Adv. 32 2013 347 365
112. M. Théry Micropatterning as a tool to decipher cell morphogenesis and functions J. Cell Sci. 123 2010 4201 4213
113. J.M. Corey, and E.L. Feldman Substrate patterning: an emerging technology for the study of neuronal behavior Exp. Neurol. 184 2003 89 96
114. M. Nikkhah, F. Edalat, S. Manoucheri, and A. Khademhosseini Engineering microscale topographies to control the cell-substrate interface Biomaterials 33 2012 5230 5246
115. L. Yao, A. Pandit, S. Yao, and C.D. McCaig Electric field-guided neuron migration: a novel approach in neurogenesis Tissue Eng. B Rev. 17 2011 143 153
116. M. Arocena, M. Zhao, J.M. Collinson, and B. Song A time-lapse and quantitative modelling analysis of neural stem cell motion in the absence of directional cues and in electric fields J. Neurosci. Res. 88 2010 3267 3274
117. C.D. McCaig, A.M. Rajnicek, B. Song, and M. Zhao Controlling cell behavior electrically: current views and future potential Physiol. Rev. 85 2005 943 978
118. C.D. McCaig, B. Song, and A.M. Rajnicek Electrical dimensions in cell science J. Cell Sci. 122 2009 4267 4276
119. J.F. Feng Guided migration of neural stem cells derived from human embryonic stem cells by an electric field Stem Cells 30 2012 349 355
120. A.K. Dubey, S.D. Gupta, and B. Basu Optimization of electrical stimulation parameters for enhanced cell proliferation on biomaterial surfaces J. Biomed. Mater. Res. B Appl. Biomater. 98 2011 18 29
121. O. Yanes Metabolic oxidation regulates embryonic stem cell differentiation Nat. Chem. Biol. 6 2010 411 417
122. M. Tsatmali, E.C. Walcott, and K.L. Crossin Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors Brain Res. 1040 2005 137 150
123. J. Smith, E. Ladi, M. Mayer-Pröschel, and M. Noble Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell Proc. Natl. Acad. Sci. 97 2000 10032 10037
124. M.J. Higgins, P.J. Molino, Z. Yue, and G.G. Wallace Organic conducting polymer-protein interactions Chem. Mater. 24 2012 828 839
125. M.E. Mycielska, and M.B. Djamgoz Cellular mechanisms of direct-current electric field effects: galvanotaxis and metastatic disease J. Cell Sci. 117 2004 1631 1639
126. C.A. Ariza The influence of electric fields on hippocampal neural progenitor cells Stem Cell Rev. Rep. 6 2010 585 600
127. L. Hinkle, C. McCaig, and K. Robinson The direction of growth of differentiating neurones and myoblasts from frog embryos in an applied electric field J. Physiol. 314 1981 121 135
128. V. Shastri, C. Schmidt, T.-H. Kim, J. Vacanti, and R. Langer MRS Proceedings vol. 414 1995 Cambridge Univ Press
129. M. Wood, and R.K. Willits Short-duration, DC electrical stimulation increases chick embryo DRG neurite outgrowth Bioelectromagnetics 27 2006 328 331
130. Z. Zhang Electrically conductive biodegradable polymer composite for nerve regeneration: electricity-stimulated neurite outgrowth and axon regeneration Artif. Organs 31 2007 13 22
131. Y.-J. Chang, C.-M. Hsu, C.-H. Lin, M.S.-C. Lu, and L. Chen Electrical stimulation promotes nerve growth factor-induced neurite outgrowth and signaling Biochim. Biophys. Acta Gen. Subj. 1830 2013 4130 4136