An aligned composite film was fabricated via the deposition of carboxylic graphene oxide (C-GO) and polypyrrole (PPy) nanoparticles on aligned poly(L-lactic acid) (PLLA) fiber-films (named as C-GO/PPy/PLLA), which has the core (PLLA)–sheath (C-GO/PPy) structure, and the composition of C-GO (~4.8 wt.% of PPy sheath) significantly enhanced the tensile strength and the conductivity of the PPy/PLLA film. Especially, after 4 weeks of immersion in the PBS solution, the conductivity and the tensile strength of C-GO/PPy/PLLA films still remained ~6.10 S/cm and 28.9 MPa, respectively, which could meet the need of the sustained electrical stimulation (ES) therapy for nerve repair. Moreover, the neurite length and the neurite alignment were significantly increased through exerting ES on C-GO/PPy/PLLA films due to their sustained conductivity in the fluid of cell culture. These results indicated that C-GO/PPy/PLLA with sustained conductivity and mechanical property possessed great potential of nerve repair by exerting lasting-ES.
J Song, B Sun, S Liu, et al.. Polymerizing pyrrole coated poly (l-lactic acid-co-e-caprolactone) (PLCL) conductive nanofibrous conduit combined with electric stimulation for long-range peripheral nerve regeneration. Frontiers in Molecular Neuroscience, 2016, 9: 117 (13 pages) https://doi.org/10.3389/fnmol.2016.00117
pmid: 27877111
3
M Asplund, M Nilsson, A Jacobsson, et al.. Incidence of traumatic peripheral nerve injuries and amputations in Sweden between 1998 and 2006. Neuroepidemiology, 2009, 32(3): 217–228 https://doi.org/10.1159/000197900
pmid: 19174611
4
D Liu, D Mi, T Zhang, et al.. Tubulation repair mitigates misdirection of regenerating motor axons across a sciatic nerve gap in rats. Scientific Reports, 2018, 8(1): 3443 PMID:29311619 https://doi.org/10.1038/s41598-018-21652-y
G R D Evans. Peripheral nerve injury: a review and approach to tissue engineered constructs. The Anatomical Record, 2001, 263(4): 396–404 https://doi.org/10.1002/ar.1120
pmid: 11500817
9
C Cunha, S Panseri, S Antonini. Emerging nanotechnology approaches in tissue engineering for peripheral nerve regeneration. Nanomedicine: Nanotechnology, Biology, and Medicine, 2011, 7(1): 50–59 https://doi.org/10.1016/j.nano.2010.07.004
pmid: 20692373
10
M F Meek, J H Coert. US Food and Drug Administration/Conformit Europe-approved absorbable nerve conduits for clinical repair of peripheral and cranial nerves. Annals of Plastic Surgery, 2008, 60(1): 110–116 https://doi.org/10.1097/SAP.0b013e31804d441c
pmid: 18437784
11
M Ikeda, T Uemura, K Takamatsu, et al.. Acceleration of peripheral nerve regeneration using nerve conduits in combination with induced pluripotent stem cell technology and a basic fibroblast growth factor drug delivery system. Journal of Biomedical Materials Research Part A, 2014, 102(5): 1370–1378 https://doi.org/10.1002/jbm.a.34816
pmid: 23733515
12
Y Wu, L Wang, B Guo, et al.. Electroactive biodegradable polyurethane significantly enhanced Schwann cells myelin gene expression and neurotrophin secretion for peripheral nerve tissue engineering. Biomaterials, 2016, 87: 18–31 https://doi.org/10.1016/j.biomaterials.2016.02.010
pmid: 26897537
13
L Wang, Y Wu, B Guo, et al.. Nanofiber yarn/hydrogel core‒shell scaffolds mimicking native skeletal muscle tissue for guiding 3D myoblast alignment, elongation, and differentiation. ACS Nano, 2015, 9(9): 9167–9179 https://doi.org/10.1021/acsnano.5b03644
pmid: 26280983
14
A F Quigley, J M Razal, B C Thompson, et al.. A conducting-polymer platform with biodegradable fibers for stimulation and guidance of axonal growth. Advanced Materials, 2009, 21(43): 4393‒4397 doi:10.1002/adma.200901165
15
R A Green, P B Matteucci, R T Hassarati, et al.. Performance of conducting polymer electrodes for stimulating neuroprosthetics. Journal of Neural Engineering, 2013, 10(1): 016009 https://doi.org/10.1088/1741-2560/10/1/016009
pmid: 23283391
16
T Yao, T Cui, X Fang, et al.. Preparation of yolk/shell Fe3O4@polypyrrole composites and their applications as catalyst supports. Chemical Engineering Journal, 2013, 225(6): 230–236 https://doi.org/10.1016/j.cej.2013.02.026
17
W Jing, Q Ao, L Wang, et al.. Constructing conductive conduit with conductive fibrous infilling for peripheral nerve regeneration. Chemical Engineering Journal, 2018, 345: 566–577 doi:10.1016/j.cej.2018.04.044
M Vivó, A Puigdemasa, L Casals, et al.. Immediate electrical stimulation enhances regeneration and reinnervation and modulates spinal plastic changes after sciatic nerve injury and repair. Experimental Neurology, 2008, 211(1): 180–193 https://doi.org/10.1016/j.expneurol.2008.01.020
pmid: 18316076
20
L Li, Y H El-Hayek, B Liu, et al.. Direct-current electrical field guides neuronal stem/progenitor cell migration. Stem Cells, 2008, 26(8): 2193–2200 https://doi.org/10.1634/stemcells.2007-1022
pmid: 18556511
21
N M Geremia, T Gordon, T M Brushart, et al.. Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression. Experimental Neurology, 2007, 205(2): 347–359 https://doi.org/10.1016/j.expneurol.2007.01.040
pmid: 17428474
22
M Umana, J Waller. Protein-modified electrodes. The glucose oxidase/polypyrrole system. Analytical Chemistry, 1986, 58(14): 2979–2983 https://doi.org/10.1021/ac00127a018
23
J Y Wong, R Langer, D E Ingber. Electrically conducting polymers can noninvasively control the shape and growth of mammalian cells. Proceedings of the National Academy of Sciences of the United States of America, 1994, 91(8): 3201–3204 https://doi.org/10.1073/pnas.91.8.3201
pmid: 8159724
24
G Shi, M Rouabhia, Z Wang, et al.. A novel electrically conductive and biodegradable composite made of polypyrrole nanoparticles and polylactide. Biomaterials, 2004, 25(13): 2477–2488 https://doi.org/10.1016/j.biomaterials.2003.09.032
pmid: 14751732
S Y Park, J Park, S H Sim, et al.. Enhanced differentiation of human neural stem cells into neurons on graphene. Advanced Materials, 2011, 23(36): H263–H267 https://doi.org/10.1002/adma.201101503
pmid: 21823178
28
J S Lee, A Lipatov, L Ha, et al.. Graphene substrate for inducing neurite outgrowth. Biochemical and Biophysical Research Communications, 2015, 460(2): 267–273 https://doi.org/10.1016/j.bbrc.2015.03.023
pmid: 25778866
29
O Akhavan, E Ghaderi, E Abouei, et al.. Accelerated differentiation of neural stem cells into neurons on ginseng-reduced graphene oxide sheets. Carbon, 2014, 66(1): 395–406 https://doi.org/10.1016/j.carbon.2013.09.015
30
O Akhavan, E Ghaderi. The use of graphene in the self-organized differentiation of human neural stem cells into neurons under pulsed laser stimulation. Journal of Materials Chemistry B: Materials for Biology and Medicine, 2014, 2(34): 5602–5611 https://doi.org/10.1039/C4TB00668B
31
P Dubey, A Kumar, R Prakash. Non-covalent functionalization of graphene oxide by polyindole and subsequent incorporation of Ag nanoparticles for electrochemical applications. Applied Surface Science, 2015, 355: 262–267 https://doi.org/10.1016/j.apsusc.2015.07.079
32
S P Mukherjee, A R Gliga, B Lazzaretto, et al.. Graphene oxide is degraded by neutrophils and the degradation products are non-genotoxic. Nanoscale, 2018, 10(3): 1180–1188 doi:10.1039/C7NR03552G
pmid: 29271441
T Lammel, P Boisseaux, M L Fernández-Cruz, et al.. Internalization and cytotoxicity of graphene oxide and carboxyl graphene nanoplatelets in the human hepatocellular carcinoma cell line Hep G2. Particle and Fibre Toxicology, 2013, 10: 27 (21 pages) https://doi.org/10.1186/1743-8977-10-27
pmid: 23849434
35
M Wang, G Mi, D Shi, et al.. Nanotechnology and nanomaterials for improving neural interfaces. Advanced Functional Materials, 2017, 28(12): 1700905 doi:10.1002/adfm.201700905
36
S J Lee, W Zhu, M Nowicki, et al.. 3D printing nano conductive multi-walled carbon nanotube scaffolds for nerve regeneration. Journal of Neural Engineering, 2018, 15(1): 016018 https://doi.org/10.1088/1741-2552/aa95a5
pmid: 29064377
37
J Zeng, Z Huang, G Yin, et al.. Fabrication of conductive NGF-conjugated polypyrrole-poly(l-lactic acid) fibers and their effect on neurite outgrowth. Colloids and Surfaces B: Biointerfaces, 2013, 110(10): 450–457 https://doi.org/10.1016/j.colsurfb.2013.05.012
pmid: 23759386
38
C E Schmidt, V R Shastri, J P Vacanti, et al.. Stimulation of neurite outgrowth using an electrically conducting polymer. Proceedings of the National Academy of Sciences of the United States of America, 1997, 94(17): 8948–8953 https://doi.org/10.1073/pnas.94.17.8948
pmid: 9256415
39
A Yang, Z Huang, G Yin, et al.. Fabrication of aligned, porous and conductive fibers and their effects on cell adhesion and guidance. Colloids and Surfaces B: Biointerfaces, 2015, 134: 469–474 https://doi.org/10.1016/j.colsurfb.2015.07.028
pmid: 26258750
N V Bhat, A P Gadre, V A Bambole. Investigation of electropolymerized polypyrrole composite film: Characterization and application to gas sensors. Journal of Applied Polymer Science, 2003, 88(1): 22–29 https://doi.org/10.1002/app.11641
42
J Tabaciarova, M Micusik, P Fedorko, et al.. Study of polypyrrole aging by XPS, FTIR and conductivity measurements. Polymer Degradation and Stability, 2015, 120: 392–401 https://doi.org/10.1016/j.polymdegradstab.2015.07.021
43
G Kister, G Cassanas, M Vert. Effects of morphology, conformation and configuration on the IR and Raman spectra of various poly(lactic acid)s. Polymer, 1998, 39(2): 267–273 https://doi.org/10.1016/S0032-3861(97)00229-2
44
M Acik, G Lee, C Mattevi, et al.. Unusual infrared-absorption mechanism in thermally reduced graphene oxide. Nature Materials, 2010, 9(10): 840–845 https://doi.org/10.1038/nmat2858
pmid: 20852618
45
S Bose, T Kuila, M E Uddin, et al.. In-situ synthesis and characterization of electrically conductive polypyrrole/graphene nanocomposites. Polymer, 2010, 51(25): 5921–5928 https://doi.org/10.1016/j.polymer.2010.10.014
D Zhang, X Zhang, Y Chen, et al.. Enhanced capacitance and rate capability of graphene/polypyrrole composite as electrode material for supercapacitors. Journal of Power Sources, 2011, 196(14): 5990–5996 https://doi.org/10.1016/j.jpowsour.2011.02.090
48
W Wu, L Yang, S Chen, et al.. Core‒shell nanospherical polypyrrole/graphene oxide composites for high performance supercapacitors. RSC Advances, 2015, 5(111): 91645–91653 https://doi.org/10.1039/C5RA17036B
49
M J McAllister, J L Li, D H Adamson, et al.. Single sheet functionalized graphene by oxidation and thermal expansion of graphite. Chemistry of Materials, 2007, 19(18): 4396–4404 https://doi.org/10.1021/cm0630800
50
S Yang, C Shen, Y Liang, et al.. Graphene nanosheets-polypyrrole hybrid material as a highly active catalyst support for formic acid electro-oxidation. Nanoscale, 2011, 3(8): 3277–3284 https://doi.org/10.1039/c1nr10371g
pmid: 21713273
51
A Xie, F Tao, P Chen, et al.. Synthesis and supercapacitive properties of carboxylated graphene oxide‒polyaniline/polypyrrole nanocomposites. Journal of the Electrochemical Society, 2018, 165(7): H291–H299 https://doi.org/10.1149/2.0211807jes
52
C E Dumont, W Born. Stimulation of neurite outgrowth in a human nerve scaffold designed for peripheral nerve reconstruction. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 2005, 73B(1): 194–202 https://doi.org/10.1002/jbm.b.30202
pmid: 15660444
53
M Gu, Y Liu, T Chen, et al.. Is graphene a promising nano-material for promoting surface modification of implants or scaffold materials in bone tissue engineering? Tissue Engineering Part B: Reviews, 2014, 20(5): 477–491 https://doi.org/10.1089/ten.teb.2013.0638
pmid: 24447041
54
R D Fields, P B Guthrie, J T Russell, et al.. Accommodation of mouse DRG growth cones to electrically induced collapse: kinetic analysis of calcium transients and set-point theory. Journal of Neurobiology, 1993, 24(8): 1080–1098 https://doi.org/10.1002/neu.480240807
pmid: 8409969
L Yao, C D McCaig, M Zhao. Electrical signals polarize neuronal organelles, direct neuron migration, and orient cell division. Hippocampus, 2009, 19(9): 855–868 https://doi.org/10.1002/hipo.20569
pmid: 19280605