Accelerating bioelectric functional development of neural stem cells by graphene coupling: Implications for neural interfacing with conductive materials

Biomaterials

Volumn 106, Issue , 2016, Pages 193-204

  Guo, Rongrong ^a,b   Zhang, Shasha ^a,b   Xiao, Miao ^c   Qian, Fuping ^a,b   He, Zuhong ^a,b   Li, Dan ^a,b   Zhang, Xiaoli ^d   Li, Huawei ^e   Yang, Xiaowei ^f   Wang, Ming ^g   Chai, Renjie ^a,b   Tang, Mingliang ^a,b  

^a SOUTHEAST UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

^c SUZHOU INSTITUTE OF NANO TECH AND NANO BIONICS   (China)

^d THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

^e EYE AND ENT HOSPITAL OF FUDAN UNIVERSITY   (China)

^f TONGJI UNIVERSITY   (China)

^g University of Science and Technology of China   (China)

Author keywords

Bioelectric properties; Differentiation; Graphene; Neural stem cells

Indexed keywords

CELL ENGINEERING; CELLS; CHARACTERIZATION; CONDUCTIVE MATERIALS; CYTOLOGY; DIFFERENTIATION (CALCULUS); ELECTRIC FIELDS; ELECTROPHYSIOLOGY; MEMBRANES; STEM CELLS; SUBSTRATES; TISSUE ENGINEERING; TISSUE REGENERATION;

BIOELECTRIC PROPERTIES; ELECTRIC CHARACTERIZATION; ELECTRICAL PARAMETER; ELECTROPHYSIOLOGICAL RECORDINGS; MEMBRANE POTENTIALS; MEMBRANE PROPERTIES; METHODS AND MATERIALS; NEURAL STEM CELL;

GRAPHENE;

BIOMATERIAL; GRAPHENE; GRAPHENE FILM; PROTEIN; PROTEIN TREK 1; UNCLASSIFIED DRUG; GRAPHITE;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOENERGY; CELL FUNCTION; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOLOGY; ELECTRIC CAPACITANCE; ELECTRIC FIELD; ELECTRIC RESISTANCE; MEMBRANE STEADY POTENTIAL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPSE; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; COMPUTER SIMULATION; DEVICES; ELECTRIC CONDUCTIVITY; ELECTRODE; IMPEDANCE; MATERIALS TESTING; MEMBRANE POTENTIAL; PHYSIOLOGY; PROCEDURES; TISSUE ENGINEERING; TISSUE SCAFFOLD;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BIOCOMPATIBLE MATERIALS; CELL DIFFERENTIATION; CELLS, CULTURED; COMPUTER SIMULATION; ELECTRIC CONDUCTIVITY; ELECTRIC IMPEDANCE; ELECTRODES; GRAPHITE; MATERIALS TESTING; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; NEURAL STEM CELLS; RATS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84983552171     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2016.08.019     Document Type: Article

References (65)

1. [1] Gadsby, D.C., Ion channels versus ion pumps: the principal difference, in principle. Nat. Rev. Mol. Cell Biol. 10 (2009), 344–352.
2. [2] McCaig, C.D., Rajnicek, A.M., Song, B., Zhao, M., Controlling cell behavior electrically: current views and future potential. Physiol. Rev. 85 (2005), 943–978.
3. [3] Zhu, Y., Murali, S., Cai, W., Li, X., Suk, J.W., Potts, J.R., et al. Graphene and graphene oxide: synthesis, properties, and applications. Adv. Mater. 22 (2010), 3906–3924.
4. [4] Sun, X., Liu, Z., Welsher, K., Robinson, J.T., Goodwin, A., Zaric, S., et al. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 1 (2008), 203–212.
5. [5] Cohen-Karni, T., Qing, Q., Li, Q., Fang, Y., Lieber, C.M., Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Lett. 10 (2010), 1098–1102.
6. [6] Nayak, T.R., Andersen, H., Makam, V.S., Khaw, C., Bae, S., Xu, X., et al. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano 5 (2011), 4670–4678.
7. [7] Park, S.Y., Park, J., Sim, S.H., Sung, M.G., Kim, K.S., Hong, B.H., et al. Enhanced differentiation of human neural stem cells into neurons on graphene. Adv. Mater. 23 (2011), H263–H267.
8. [8] Yang, K., Zhang, S., Zhang, G., Sun, X., Lee, S.T., Liu, Z., Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett. 10 (2010), 3318–3323.
9. [9] Lee, J.S., Lipatov, A., Ha, L., Shekhirev, M., Andalib, M.N., Sinitskii, A., et al. Graphene substrate for inducing neurite outgrowth. Biochem. Biophys. Res. Commun. 460 (2015), 267–273.
10. [10] Hong, S.W., Lee, J.H., Kang, S.H., Hwang, E.Y., Hwang, Y.S., Lee, M.H., et al. Enhanced neural cell adhesion and neurite outgrowth on graphene-based biomimetic substrates. BioMed Res. Int., 2014, 2014, 212149.
11. [11] Tu, Q., Pang, L., Wang, L., Zhang, Y., Zhang, R., Wang, J., Biomimetic choline-like graphene oxide composites for neurite sprouting and outgrowth. ACS Appl. Mater. Interfaces 5 (2013), 13188–13197.
12. [12] Akhavan, O., Ghaderi, E., The use of graphene in the self-organized differentiation of human neural stem cells into neurons under pulsed laser stimulation. J. Mat. Chem. B 2 (2014), 5602–5611.
13. [13] Akhavan, O., Ghaderi, E., Abouei, E., Hatamie, S., Ghasemi, E., Accelerated differentiation of neural stem cells into neurons on ginseng-reduced graphene oxide sheets. Carbon 66 (2014), 395–406.
14. [14] Akhavan, O., Ghaderi, E., Shirazian, S.A., Near infrared laser stimulation of human neural stem cells into neurons on graphene nanomesh semiconductors. Colloids Surfaces B Biointerfaces 126 (2015), 313–321.
15. [15] Akhavan, O., Ghaderi, E., Shirazian, S.A., Rahighi, R., Rolled graphene oxide foams as three-dimensional scaffolds for growth of neural fibers using electrical stimulation of stem cells. Carbon 97 (2016), 71–77.
16. [16] Akhavan, O., Ghaderi, E., Flash photo stimulation of human neural stem cells on graphene/TiO2 heterojunction for differentiation into neurons. Nanoscale 5 (2013), 10316–10326.
17. [17] Crowder, S.W., Prasai, D., Rath, R., Balikov, D.A., Bae, H., Bolotin, K.I., et al. Three-dimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells. Nanoscale 5 (2013), 4171–4176.
18. [18] Kim, J., Choi, K.S., Kim, Y., Lim, K.T., Seonwoo, H., Park, Y., et al. Bioactive effects of graphene oxide cell culture substratum on structure and function of human adipose-derived stem cells. J. Biomed. Mater. Res. Part A 101 (2013), 3520–3530.
19. [19] Tatavarty, R., Ding, H., Lu, G., Taylor, R.J., Bi, X., Synergistic acceleration in the osteogenesis of human mesenchymal stem cells by graphene oxide-calcium phosphate nanocomposites. Chem. Commun. 50 (2014), 8484–8487.
20. [20] Elkhenany, H., Amelse, L., Lafont, A., Bourdo, S., Caldwell, M., Neilsen, N., et al. Graphene supports in vitro proliferation and osteogenic differentiation of goat adult mesenchymal stem cells: potential for bone tissue engineering. J. Appl. Toxicol. JAT 35 (2015), 367–374.
21. [21] Luo, Y., Shen, H., Fang, Y., Cao, Y., Huang, J., Zhang, M., et al. Enhanced proliferation and osteogenic differentiation of mesenchymal stem cells on graphene oxide-incorporated electrospun poly(lactic-co-glycolic acid) nanofibrous mats. ACS Appl. Mater. Interfaces 7 (2015), 6331–6339.
22. [22] Zhang, T., Li, N., Li, K., Gao, R., Gu, W., Wu, C., et al. Enhanced proliferation and osteogenic differentiation of human mesenchymal stem cells on biomineralized three-dimensional graphene foams. Carbon 105 (2016), 233–243.
23. [23] Chen, G.Y., Pang, D.W., Hwang, S.M., Tuan, H.Y., Hu, Y.C., A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials 33 (2012), 418–427.
24. [24] Lee, T.J., Park, S., Bhang, S.H., Yoon, J.K., Jo, I., Jeong, G.J., et al. Graphene enhances the cardiomyogenic differentiation of human embryonic stem cells. Biochem. Biophys. Res. Commun. 452 (2014), 174–180.
25. [25] Yang, D., Li, T., Xu, M., Gao, F., Yang, J., Yang, Z., et al. Graphene oxide promotes the differentiation of mouse embryonic stem cells to dopamine neurons. Nanomedicine 9 (2014), 2445–2455.
26. [26] Li, X., Cai, W., An, J., Kim, S., Nah, J., Yang, D., et al. Large-area synthesis of high-quality and uniform graphene films on copper foils. Science 324 (2009), 1312–1314.
27. [27] Graf, D., Molitor, F., Ensslin, K., Stampfer, C., Jungen, A., Hierold, C., et al. Spatially resolved Raman spectroscopy of single- and few-layer graphene. Nano Lett. 7 (2007), 238–242.
28. [28] Li, X., Zhu, Y., Cai, W., Borysiak, M., Han, B., Chen, D., et al. Transfer of large-area graphene films for high-performance transparent conductive electrodes. Nano Lett. 9 (2009), 4359–4363.
29. [29] Akhavan, O., Ghaderi, E., Differentiation of human neural stem cells into neural networks on graphene nanogrids. J. Mat. Chem. B 1 (2013), 6291–6301.
30. [30] Heo, C., Yoo, J., Lee, S., Jo, A., Jung, S., Yoo, H., et al. The control of neural cell-to-cell interactions through non-contact electrical field stimulation using graphene electrodes. Biomaterials 32 (2011), 19–27.
31. [31] Cesetti, T., Obernier, K., Bengtson, C.P., Fila, T., Mandl, C., Holzl-Wenig, G., et al. Analysis of stem cell lineage progression in the neonatal subventricular zone identifies EGFR+/NG2- cells as transit-amplifying precursors. Stem Cells 27 (2009), 1443–1454.
32. [32] Yasuda, T., Bartlett, P.F., Adams, D.J., K(ir) and K(v) channels regulate electrical properties and proliferation of adult neural precursor cells. Mol. Cell Neurosci. 37 (2008), 284–297.
33. [33] Cerbai, E., Pino, R., Sartiani, L., Mugelli, A., Influence of postnatal-development on I(f) occurrence and properties in neonatal rat ventricular myocytes. Cardiovasc. Res. 42 (1999), 416–423.
34. [34] Spitzer, N.C., Electrical activity in early neuronal development. Nature 444 (2006), 707–712.
35. [35] Ernst, C., Christie, B.R., The putative neural stem cell marker, nestin, is expressed in heterogeneous cell types in the adult rat neocortex. Neuroscience 138 (2006), 183–188.
36. [36] Wang, Y., Lee, W.C., Manga, K.K., Ang, P.K., Lu, J., Liu, Y.P., et al. Fluorinated graphene for promoting neuro-induction of stem cells. Adv. Mater. 24 (2012), 4285–4290.
37. [37] Aprea, J., Calegari, F., Bioelectric state and cell cycle control of Mammalian neural stem cells. Stem Cells Int., 2012, 2012, 816049.
38. [38] Yasuda, T., Adams, D.J., Physiological roles of ion channels in adult neural stem cells and their progeny. J. Neurochem. 114 (2010), 946–959.
39. [39] Blackiston, D.J., McLaughlin, K.A., Levin, M., Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 8 (2009), 3519–3528.
40. [40] Levin, M., Large-scale biophysics: ion flows and regeneration. Trends Cell Biol. 17 (2007), 261–270.
41. [41] Bahrey, H.L., Moody, W.J., Voltage-gated currents, dye and electrical coupling in the embryonic mouse neocortex. Cereb. Cortex 13 (2003), 239–251.
42. [42] Cai, J., Cheng, A., Luo, Y., Lu, C., Mattson, M.P., Rao, M.S., et al. Membrane properties of rat embryonic multipotent neural stem cells. J. Neurochem. 88 (2004), 212–226.
43. [43] Owens, D.F., Boyce, L.H., Davis, M.B., Kriegstein, A.R., Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16 (1996), 6414–6423.
44. [44] Franks, N.P., Honore, E., The TREK K2P channels and their role in general anaesthesia and neuroprotection. Trends Pharmacol. Sci. 25 (2004), 601–608.
45. [45] Goldstein, S.A., Bayliss, D.A., Kim, D., Lesage, F., Plant, L.D., Rajan, S., International Union of Pharmacology. LV. Nomenclature and molecular relationships of two-P potassium channels. Pharmacol. Rev. 57 (2005), 527–540.
46. [46] Lotshaw, D.P., Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K+ channels. Cell Biochem. Biophys. 47 (2007), 209–256.
47. [47] Fink, M., Duprat, F., Lesage, F., Reyes, R., Romey, G., Heurteaux, C., et al. Cloning, functional expression and brain localization of a novel unconventional outward rectifier K+ channel. EMBO J. 15 (1996), 6854–6862.
48. [48] Xi, G., Zhang, X., Zhang, L., Sui, Y., Hui, J., Liu, S., et al. Fluoxetine attenuates the inhibitory effect of glucocorticoid hormones on neurogenesis in vitro via a two-pore domain potassium channel, TREK-1. Psychopharmacol. Berl. 214 (2011), 747–759.
49. [49] Scheffler, B., Walton, N.M., Lin, D.D., Goetz, A.K., Enikolopov, G., Roper, S.N., et al. Phenotypic and functional characterization of adult brain neuropoiesis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 9353–9358.
50. [50] Nguyen, L., Malgrange, B., Belachew, S., Rogister, B., Rocher, V., Moonen, G., et al. Functional glycine receptors are expressed by postnatal nestin-positive neural stem/progenitor cells. Eur. J. Neurosci. 15 (2002), 1299–1305.
51. [51] Yoshihara, Y., De Roo, M., Muller, D., Dendritic spine formation and stabilization. Curr. Opin. Neurobiol. 19 (2009), 146–153.
52. [52] Akhavan, O., Graphene scaffolds in progressive nanotechnology/stem cell-based tissue engineering of the nervous system. J. Mat. Chem. B 4 (2016), 3169–3190.
53. [53] Boga, A., Binokay, S., Emre, M., Sertdemir, Y., The embryonic development of Xenopus laevis under a low frequency electric field. In Vitro Cell. Dev. Biol. Animal 48 (2012), 385–391.
54. [54] Corner, M.A., Spontaneous neuronal burst discharges as dependent and independent variables in the maturation of cerebral cortex tissue cultured in vitro: a review of activity-dependent studies in live 'model' systems for the development of intrinsically generated bioelectric slow-wave sleep patterns. Brain Res. Rev. 59 (2008), 221–244.
55. [55] Karja, N.W., Otoi, T., Wongsrikeao, P., Shimizu, R., Murakami, M., Agung, B., et al. Effects of electric field strengths on fusion and in vitro development of domestic cat embryos derived by somatic cell nuclear transfer. Theriogenology 66 (2006), 1237–1242.
56. [56] Gomes, P.A., Bassani, R.A., Bassani, J.W., Electric field stimulation of cardiac myocytes during postnatal development. IEEE Trans. Bio-medical Eng. 48 (2001), 630–636.
57. [57] Ramakers, G.J., Raadsheer, F.C., Corner, M.A., Ramaekers, F.C., Van Leeuwen, F.W., Development of neurons and glial cells in cerebral cortex, cultured in the presence or absence of bioelectric activity: morphological observations. Eur. J. Neurosci. 3 (1991), 140–153.
58. [58] Zhao, H., Steiger, A., Nohner, M., Ye, H., Specific intensity direct current (DC) electric field improves neural stem cell migration and enhances differentiation towards betaIII-Tubulin+ neurons. PloS one, 10, 2015, e0129625.
59. [59] Esfandiari, E., Roshankhah, S., Mardani, M., Hashemibeni, B., Naghsh, E., Kazemi, M., et al. The effect of high frequency electric field on enhancement of chondrogenesis in human adipose-derived stem cells. Iran. J. Basic Med. Sci. 17 (2014), 571–576.
60. [60] Matos, M.A., Cicerone, M.T., Alternating current electric field effects on neural stem cell viability and differentiation. Biotechnol. Prog. 26 (2010), 664–670.
61. [61] Li, Y., Weiss, M., Yao, L., Directed migration of embryonic stem cell-derived neural cells in an applied electric field. Stem Cell Rev. 10 (2014), 653–662.
62. [62] Zhao, Z., Watt, C., Karystinou, A., Roelofs, A.J., McCaig, C.D., Gibson, I.R., et al. Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. Eur. Cells Mater. 22 (2011), 344–358.
63. [63] Kuzmenko, V., Kalogeropoulos, T., Thunberg, J., Johannesson, S., Hagg, D., Enoksson, P., et al. Enhanced growth of neural networks on conductive cellulose-derived nanofibrous scaffolds. Materials science & engineering C. Mater. Biol. Appl. 58 (2016), 14–23.
64. [64] Stewart, E., Kobayashi, N.R., Higgins, M.J., Quigley, A.F., Jamali, S., Moulton, S.E., et al. Electrical stimulation using conductive polymer polypyrrole promotes differentiation of human neural stem cells: a biocompatible platform for translational neural tissue engineering. Tissue engineering Part C. Methods 21 (2015), 385–393.
65. [65] Xie, J., Macewan, M.R., Willerth, S.M., Li, X., Moran, D.W., Sakiyama-Elbert, S.E., et al. Conductive core-sheath nanofibers and their potential application in neural tissue engineering. Adv. Funct. Mater. 19 (2009), 2312–2318.