Skip to main content
Log in

Electrical Stimulation-Mediated Differentiation of Neural Cells on Conductive Carbon Nanofiller-Based Scaffold

  • Review
  • Published:
Biomedical Materials & Devices Aims and scope Submit manuscript

Abstract

An important strategy in neural tissue engineering involves imparting electrical properties to the regenerative template to encourage cell proliferation and differentiation. Several clinical studies have confirmed that direct or indirect electrical stimulation therapy greatly impacts the treatment of peripheral and central nerve injury. Nerve regeneration can be accelerated by the application of electrical stimulations of different methods and with varying parameters. For a long period, electrical stimulation along with conventional conductive polymers have played an important role in nerve tissue regeneration, due to their conductivity. However, the low biocompatibility of these materials has brought attention toward the need for the alternative of the conductive polymers. Carbon nanofillers (graphene, nanotubes, and their derivatives) have been showing promising results in bioimaging, biosensing, and composites, simultaneously, proving themselves as a prospective biomaterial in neural tissue repair and regeneration due to their excellent electrical and mechanical properties, alongside, biocompatibility. Therefore, carbon nanofiller-based scaffolds synchronized with electrical stimulation may lead to a breakthrough in the treatment of nerve injury. This review article focuses on the influence of the electrical properties of carbon-based material on nerve tissue engineering. In this article, we explicitly focus on the different methods to deliver electrical stimulation and the pathways involved in the differentiation of neuronal cells. Emphasis is given to the analysis of the suitable fabrication strategies of carbon-based neural scaffold and the way its interfaces interact with neurons for promoting neuronal differentiation. Furthermore, this review summarizes the ongoing advancements to augment the conductivity and biological activities (cell adhesion, proliferation, neural differentiation, neurite outgrowth), as well as to reduce the potential toxicity in conductive carbon nanofiller-based scaffolds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Reproduced with permission from Ref. [98]

Fig. 4

Reproduced with permission from Ref. [117], c synaptic bridge formed between two MWNT bundles and the soma of the neuron is located along the edge of the MWNT. Reproduced with permission from Ref. [118] and d Schematic representation of the interacting mechanism of absorbed ECM proteins with CNT multilayers that controls NSCs biological processes Reproduced with permission from Ref. [137]

Fig. 5

Similar content being viewed by others

References

  1. M. Nadi, R. Midha, Management of peripheral nerve injuries, 4th edn. (Elsevier, Philadelphia, 2018). https://doi.org/10.1016/B978-0-323-43140-8.00061-5

    Book  Google Scholar 

  2. T. Yang, Y.J. Dai, G. Chen, S. Sen Cui, Dissecting the dual role of the glial scar and scar-forming astrocytes in spinal cord injury. Front. Cell. Neurosci. 14, 20 (2020). https://doi.org/10.3389/fncel.2020.00078

    Article  CAS  Google Scholar 

  3. B. Fan, Z. Wei, X. Yao, G. Shi, X. Cheng, X. Zhou, H. Zhou, G. Ning, Microenvironment imbalance of spinal cord injury. Cell Transplant. 10, 1–14 (2018). https://doi.org/10.1177/0963689718755778

    Article  Google Scholar 

  4. G. Crozier-Shaw, H. Denton, S. Morris, Management strategies in acute traumatic spinal cord injury: a narrative review. Neuroimmunol. Neuroinflamm. 7, 335–344 (2020). https://doi.org/10.20517/2347-8659.2019.005

    Article  CAS  Google Scholar 

  5. C.S. Ahuja, J.R. Wilson, S. Nori, M.R.N. Kotter, C. Druschel, A. Curt, M.G. Fehlings, Traumatic spinal cord injury. Nat. Rev. Dis. Prim. (2017). https://doi.org/10.1038/nrdp.2017.18

    Article  Google Scholar 

  6. C. Rouanet, D. Reges, E. Rocha, V. Gagliardi, G. SampaioSilva, Traumatic spinal cord injury: current concepts and treatment update. Traumatismo raquimedular (2017). https://doi.org/10.1590/0004-282X20170048

    Article  Google Scholar 

  7. R. López-Cebral, J. Silva-Correia, R.L. Reis, T.H. Silva, J.M. Oliveira, Peripheral nerve injury: current challenges, conventional treatment approaches, and new trends in biomaterials-based regenerative strategies. ACS Biomater. Sci. Eng. 3, 3098–3122 (2017). https://doi.org/10.1021/acsbiomaterials.7b00655

    Article  CAS  Google Scholar 

  8. N.G. Simon, R.J. Spinner, D.G. Kline, M. Kliot, Advances in the neurological and neurosurgical management of peripheral nerve trauma. J. Neurol. Neurosurg. Psychiatry. 87, 198–208 (2016). https://doi.org/10.1136/jnnp-2014-310175

    Article  Google Scholar 

  9. G.H. Han, J. Peng, P. Liu, X. Ding, S. Wei, S. Lu, Y. Wang, Therapeutic strategies for peripheral nerve injury: decellularized nerve conduits and Schwann cell transplantation. Neural Regen. Res. 14, 1343–1351 (2019). https://doi.org/10.4103/1673-5374.253511

    Article  CAS  Google Scholar 

  10. Y. Sun, X. Liu, M.N. George, S. Park, B. Gaihre, A. Terzic, L. Lu, Enhanced nerve cell proliferation and differentiation on electrically conductive scaffolds embedded with graphene and carbon nanotubes. J. Biomed. Mater. Res. - Part A. 109, 193–206 (2021). https://doi.org/10.1002/jbm.a.37016

    Article  CAS  Google Scholar 

  11. R.P. Trueman, A.S. Ahlawat, J.B. Phillips, A shock to the (nervous) system: bioelectricity within peripheral nerve tissue engineering. Tissue Eng. Part B Rev. (2022). https://doi.org/10.1089/ten.teb.2021.0159

    Article  Google Scholar 

  12. K. Pawar, G. Welzel, C. Haynl, S. Schuster, T. Scheibel, Recombinant spider silk and collagen-based nerve guidance conduits support neuronal cell differentiation and functionality in vitro. ACS Appl. Bio Mater. 2, 4872–4880 (2019). https://doi.org/10.1021/acsabm.9b00628

    Article  CAS  Google Scholar 

  13. A. Binnetoglu, B. Demir, D. Akakin, E. Kervancioglu Demirci, C. Batman, Bacterial cellulose tubes as a nerve conduit for repairing complete facial nerve transection in a rat model. Eur. Arch. Oto-Rhino-Laryngol. 277, 277–283 (2020). https://doi.org/10.1007/s00405-019-05637-9

    Article  Google Scholar 

  14. H. Fujimaki, H. Matsumine, H. Osaki, Y. Ueta, W. Kamei, M. Shimizu, K. Hashimoto, K. Fujii, T. Kazama, T. Matsumoto, Y. Niimi, M. Miyata, H. Sakurai, Dedifferentiated fat cells in polyglycolic acid-collagen nerve conduits promote rat facial nerve regeneration. Regen. Ther. 11, 240–248 (2019). https://doi.org/10.1016/j.reth.2019.08.004

    Article  Google Scholar 

  15. A.J. Reid, A.C. de Luca, A. Faroni, S. Downes, M. Sun, G. Terenghi, P.J. Kingham, Long term peripheral nerve regeneration using a novel PCL nerve conduit. Neurosci. Lett. 544, 125–130 (2013). https://doi.org/10.1016/j.neulet.2013.04.001

    Article  CAS  Google Scholar 

  16. L. Zhu, S. Jia, T. Liu, L. Yan, D. Huang, Z. Wang, S. Chen, Z. Zhang, W. Zeng, Y. Zhang, H. Yang, D. Hao, Aligned PCL fiber conduits immobilized with nerve growth factor gradients enhance and direct sciatic nerve regeneration. Adv. Funct. Mater. (2020). https://doi.org/10.1002/adfm.202002610

    Article  Google Scholar 

  17. H. Amani, H. Kazerooni, H. Hassanpoor, A. Akbarzadeh, H. Pazoki-Toroudi, Tailoring synthetic polymeric biomaterials towards nerve tissue engineering: a review. Artif. Cells Nanomed. Biotechnol. 47, 3524–3539 (2019). https://doi.org/10.1080/21691401.2019.1639723

    Article  CAS  Google Scholar 

  18. J. Du, H. Chen, L. Qing, X. Yang, X. Jia, Biomimetic neural scaffolds: a crucial step towards optimal peripheral nerve regeneration. Biomater. Sci. 6, 1299–1311 (2018). https://doi.org/10.1039/c8bm00260f

    Article  CAS  Google Scholar 

  19. S. Ghosh, S. Haldar, S. Gupta, A. Bisht, S. Chauhan, V. Kumar, P. Roy, D. Lahiri, An anisotropically conductive biodegradable scaffold with co-axially aligned carbon nanotubes for directional regeneration of peripheral nerves. Appl. Bio Mater. 3(9), 5796–5812 (2020). https://doi.org/10.1021/acsabm.0c00534

  20. S. Haldar, S. Ghosh, V. Kumar, P. Roy, D. Lahiri, The evolving neural tissue engineering landscape of India, Appl. Bio Mater. 2(12), 5446–5459 (2019). https://doi.org/10.1021/acsabm.9b00567

  21. S. Ghosh, P. Roy, D. Lahiri, Polymer matrix-based carbon nanocomposites for neural tissue engineering, Trans. Ind. Nat. Acad. Eng. 7, 93–114 (2022). https://doi.org/10.1007/s41403-021-00291-2

  22. S. Ghosh, A. Shrivastava, P. Jha, P. Roy, D. Lahiri, Analysis of neural cell behaviour on anisotropic electrically conductive polymeric biodegradable scaffolds reinforced with carbon nanotubes. Med. Dev. & Sens. 4(1), e10152 (2021). https://doi.org/10.1002/mds3.10152

  23. A. Magaz, A. Faroni, J.E. Gough, A.J. Reid, X. Li, J.J. Blaker, Bioactive silk-based nerve guidance conduits for augmenting peripheral nerve repair. Adv. Healthc. Mater. (2018). https://doi.org/10.1002/adhm.201800308

    Article  Google Scholar 

  24. O.S. Manoukian, J.T. Baker, S. Rudraiah, M.R. Arul, A.T. Vella, A.J. Domb, S.G. Kumbar, Functional polymeric nerve guidance conduits and drug delivery strategies for peripheral nerve repair and regeneration. J. Control. Release. 317, 78–95 (2020). https://doi.org/10.1016/j.jconrel.2019.11.021

    Article  CAS  Google Scholar 

  25. B.A. Karamian, N. Siegel, B. Nourie, M.D. Serruya, R.F. Heary, J.S. Harrop, A.R. Vaccaro, The role of electrical stimulation for rehabilitation and regeneration after spinal cord injury. J. Orthop. Traumatol. (2022). https://doi.org/10.1186/s10195-021-00623-6

    Article  Google Scholar 

  26. K. Haastert-Talini, R. Schmitte, N. Korte, D. Klode, A. Ratzka, C. Grothe, Electrical stimulation accelerates axonal and functional peripheral nerve regeneration across long gaps. J. Neurotrauma. 28, 661–674 (2011). https://doi.org/10.1089/neu.2010.1637

    Article  Google Scholar 

  27. J. Huang, L. Lu, X. Hu, Z. Ye, Y. Peng, X. Yan, D. Geng, Z. Luo, Electrical stimulation accelerates motor functional recovery in the rat model of 15-mm sciatic nerve gap bridged by scaffolds with longitudinally oriented microchannels. Neurorehabil. Neural Repair. 24, 736–745 (2010). https://doi.org/10.1177/1545968310368686

    Article  Google Scholar 

  28. H. Xu, J.M. Holzwarth, Y. Yan, P. Xu, H. Zheng, Y. Yin, S. Li, P.X. Ma, Conductive PPY/PDLLA conduit for peripheral nerve regeneration. Biomaterials 35, 225–235 (2014). https://doi.org/10.1016/j.biomaterials.2013.10.002

    Article  CAS  Google Scholar 

  29. Y. Bu, H.X. Xu, X. Li, W.J. Xu, Y.X. Yin, H.L. Dai, X. Bin Wang, Z.J. Huang, P.H. Xu, A conductive sodium alginate and carboxymethyl chitosan hydrogel doped with polypyrrole for peripheral nerve regeneration. RSC Adv. 8, 10806–10817 (2018). https://doi.org/10.1039/c8ra01059e

    Article  CAS  Google Scholar 

  30. M. Nune, S. Manchineella, T. Govindaraju, K.S. Narayan, Melanin incorporated electroactive and antioxidant silk fibroin nanofibrous scaffolds for nerve tissue engineering. Mater. Sci. Eng. C. 94, 17–25 (2019). https://doi.org/10.1016/j.msec.2018.09.014

    Article  CAS  Google Scholar 

  31. L. Sordini, F.F.F. Garrudo, C.A.V. Rodrigues, R.J. Linhardt, J.M.S. Cabral, F.C. Ferreira, J. Morgado, Effect of electrical stimulation conditions on neural stem cells differentiation on cross-linked PEDOT:PSS films. Front. Bioeng. Biotechnol. 9, 1–13 (2021). https://doi.org/10.3389/fbioe.2021.591838

    Article  Google Scholar 

  32. F.F.F. Garrudo, D.E.S. Nogueira, C.A.V. Rodrigues, F.A. Ferreira, P. Paradiso, R. Colaço, A.C. Marques, J.M.S. Cabral, J. Morgado, R.J. Linhardt, F.C. Ferreira, Electrical stimulation of neural-differentiating iPSCs on novel coaxial electroconductive nanofibers. Biomater. Sci. 9, 5359–5382 (2021). https://doi.org/10.1039/d1bm00503k

    Article  CAS  Google Scholar 

  33. C. Chen, X. Bai, Y. Ding, I.S. Lee, Electrical stimulation as a novel tool for regulating cell behavior in tissue engineering. Biomater. Res. 23, 1–12 (2019). https://doi.org/10.1186/s40824-019-0176-8

    Article  CAS  Google Scholar 

  34. W. Zhu, T. Ye, S.J. Lee, H. Cui, S. Miao, X. Zhou, D. Shuai, L.G. Zhang, Enhanced neural stem cell functions in conductive annealed carbon nanofibrous scaffolds with electrical stimulation, nanomedicine nanotechnology. Biol. Med. 14, 2485–2494 (2018). https://doi.org/10.1016/j.nano.2017.03.018

    Article  CAS  Google Scholar 

  35. C. Fu, S. Pan, Y. Ma, W. Kong, Z. Qi, X. Yang, Effect of electrical stimulation combined with graphene-oxide-based membranes on neural stem cell proliferation and differentiation. Artif. Cells Nanomed. Biotechnol. 47, 1867–1876 (2019). https://doi.org/10.1080/21691401.2019.1613422

    Article  CAS  Google Scholar 

  36. A. Vashist, A. Kaushik, A. Vashist, V. Sagar, A. Ghosal, Y.K. Gupta, S. Ahmad, M. Nair, Advances in carbon nanotubes-hydrogel hybrids in nanomedicine for therapeutics. Adv. Healthc. Mater. 7, 1–21 (2018). https://doi.org/10.1002/adhm.201701213

    Article  CAS  Google Scholar 

  37. S. Houshyar, M.M. Pillai, T. Saha, G. Sathish-Kumar, C. Dekiwadia, S.R. Sarker, R. Sivasubramanian, R.A. Shanks, A. Bhattacharyya, Three-dimensional directional nerve guide conduits fabricated by dopamine-functionalized conductive carbon nanofibre-based nanocomposite ink printing. RSC Adv. 10, 40351–40364 (2020). https://doi.org/10.1039/d0ra06556k

    Article  CAS  Google Scholar 

  38. M. Aleemardani, P. Zare, A. Seifalian, Z. Bagher, A.M. Seifalian, Graphene-based materials prove to be a promising candidate for nerve regeneration following peripheral nerve injury. Biomedicines. 10, 1–23 (2022). https://doi.org/10.3390/biomedicines10010073

    Article  CAS  Google Scholar 

  39. R.R. Llinás, Intrinsic electrical properties of mammalian neurons and CNS function: a historical perspective. Front. Cell. Neurosci. 8, 1–14 (2014). https://doi.org/10.3389/fncel.2014.00320

    Article  Google Scholar 

  40. P. Xiao Feng, Z. Hong Juan, J. jiang, N. Yin Jia, The mechanism of generation of nerve impulse and its features of propagation along the nerve fiber cells in living systems, J. Appl. Biotechnol. Bioeng. 5 (2018) 260–268. https://doi.org/10.15406/jabb.2018.05.00147.

  41. A. Potentials, B.Y.A.F. Huxley, and action potentials of single myelinated nerve fibres by A. F. Huxley and R. Stampfli from the physiological laboratory, University of Cambridge, and the Physiological Institute, University of Berne in the preceding paper Huxley & Stampfli, 195, (1951) 496–508.

  42. R. Splinter, Ultrashort phenomena in biochemistry and biological signalling. J. Phys. Conf. Ser. (2014). https://doi.org/10.1088/1742-6596/548/1/012008

    Article  Google Scholar 

  43. B.F. Sisken, J. Walker, M. Orgel, Prospects on clinical applications of electrical stimulation for nerve regeneration. J. Cell. Biochem. 51, 404–409 (1993). https://doi.org/10.1002/jcb.2400510404

    Article  CAS  Google Scholar 

  44. M. Hu, L. Hong, C. Liu, S. Hong, S. He, M. Zhou, G. Huang, Q. Chen, Electrical stimulation enhances neuronal cell activity mediated by Schwann cell derived exosomes. Sci. Rep. (2019). https://doi.org/10.1038/s41598-019-41007-5

    Article  Google Scholar 

  45. K.M. Chan, M.W.T. Curran, T. Gordon, The use of brief post-surgical low frequency electrical stimulation to enhance nerve regeneration in clinical practice. J. Physiol. 594, 3553–3559 (2016). https://doi.org/10.1113/JP270892

    Article  CAS  Google Scholar 

  46. B.F. Sisken, M. Kanje, G. Lundborg, E. Herbst, W. Kurtz, Stimulation of rat sciatic nerve regeneration with pulsed electromagnetic fields. Brain Res. 485, 309–316 (1989). https://doi.org/10.1016/0006-8993(89)90575-1

    Article  CAS  Google Scholar 

  47. M.I. Weintraub, D.N. Herrmann, A.G. Smith, M.M. Backonja, S.P. Cole, Pulsed electromagnetic fields to reduce diabetic neuropathic pain and stimulate neuronal repair: a randomized controlled trial. Arch. Phys. Med. Rehabil. 90, 1102–1109 (2009). https://doi.org/10.1016/j.apmr.2009.01.019

    Article  Google Scholar 

  48. M.J. Crowe, Z.P. Sun, J.H. Battocletti, M.Y. Macias, F.A. Pintar, D.J. Maiman, Exposure to pulsed magnetic fields enhances motor recovery in cats after spinal cord injury. Spine (Phila Pa. 1976) 28(2003), 2660–2666 (2003). https://doi.org/10.1097/01.BRS.0000099385.46102.0D

    Article  Google Scholar 

  49. C. Redondo-Gómez, R. Leandro-Mora, D. Blanch-Bermúdez, C. Espinoza-Araya, D. Hidalgo-Barrantes, J. Vega-Baudrit, Recent advances in carbon nanotubes for nervous tissue regeneration. Adv. Polym. Technol. 2020, 1–16 (2020). https://doi.org/10.1155/2020/6861205

    Article  CAS  Google Scholar 

  50. D. Bitounis, H. Ali-Boucetta, B.H. Hong, D. Min, K. Kostarelos, Prospects and challenges of graphene in biomedical applications. Adv. Mater. 25, 2258–2268 (2013)

    Article  CAS  Google Scholar 

  51. T. Aydin, C. Gurcan, H. Taheri, A. Yilmazer, Graphene based materials in neural tissue regeneration. Cell Biol. Transl. Med. 3, 129–142 (2018)

    Google Scholar 

  52. J.-H. Chen, C. Jang, S. Xiao, M. Ishigami, M.S. Fuhrer, Intrinsic and extrinsic performance limits of graphene devices on SiO2. Nat. Nanotechnol. 3, 206–209 (2008)

    Article  CAS  Google Scholar 

  53. D.R. Cooper, B. D’Anjou, N. Ghattamaneni, B. Harack, M. Hilke, A. Horth, N. Majlis, M. Massicotte, L. Vandsburger, E. Whiteway, V. Yu, Experimental review of graphene. ISRN Condens. Matter Phys. (2012). https://doi.org/10.5402/2012/501686

    Article  Google Scholar 

  54. K.S. Novoselov, A.K. Geim, S.V. Morozov, D. Jiang, M.I. Katsnelson, I.V. Grigorieva, S.V. Dubonos, A.A. Firsov, Two-dimensional gas of massless Dirac fermions in graphene. Nature 438, 197–200 (2005). https://doi.org/10.1038/nature04233

    Article  CAS  Google Scholar 

  55. R.S. Edwards, K.S. Coleman, Graphene synthesis: relationship to applications. Nanoscale 5, 38–51 (2013)

    Article  CAS  Google Scholar 

  56. K. Manna, H.-N. Huang, W.-T. Li, Y.-H. Ho, W.-H. Chiang, Toward understanding the efficient exfoliation of layered materials by water-assisted cosolvent liquid-phase exfoliation. Chem. Mater. 28, 7586–7593 (2016)

    Article  CAS  Google Scholar 

  57. K.S. Subrahmanyam, L.S. Panchakarla, A. Govindaraj, C.N.R. Rao, Simple method of preparing graphene flakes by an arc-discharge method. J. Phys. Chem. C. 113, 4257–4259 (2009)

    Article  CAS  Google Scholar 

  58. T. Zhang, J. Liu, C. Wang, X. Leng, Y. Xiao, L. Fu, Synthesis of graphene and related two-dimensional materials for bioelectronics devices. Biosens. Bioelectron. 89, 28–42 (2017)

    Article  CAS  Google Scholar 

  59. Q. Zhang, Z. Wu, N. Li, Y. Pu, B. Wang, T. Zhang, J. Tao, Advanced review of graphene-based nanomaterials in drug delivery systems: synthesis, modification, toxicity and application. Mater. Sci. Eng. C. 77, 1363–1375 (2017). https://doi.org/10.1016/j.msec.2017.03.196

    Article  CAS  Google Scholar 

  60. Y. Qian, X. Wang, J. Song, W. Chen, S. Chen, Y. Jin, Y. Ouyang, W.E. Yuan, C. Fan, Preclinical assessment on neuronal regeneration in the injury-related microenvironment of graphene-based scaffolds. NPJ Regen. Med. 6, 1–8 (2021). https://doi.org/10.1038/s41536-021-00142-2

    Article  CAS  Google Scholar 

  61. A.C. Jachak, M. Creighton, Y. Qiu, A.B. Kane, R.H. Hurt, Biological interactions and safety of graphene materials. MRS Bull. 37, 1307–1313 (2012)

    Article  CAS  Google Scholar 

  62. S. Sayyar, D.L. Officer, G.G. Wallace, Fabrication of 3D structures from graphene-based biocomposites. J. Mater. Chem. B. 5, 3462–3482 (2017)

    Article  CAS  Google Scholar 

  63. R. Cai, J. Wu, L. Sun, Y. Liu, T. Fang, S. Zhu, S. Li, Y. Wang, L. Guo, C. Zhao, 3D graphene/ZnO composite with enhanced photocatalytic activity. Mater. Des. 90, 839–844 (2016)

    Article  CAS  Google Scholar 

  64. C. Heo, J. Yoo, S. Lee, A. Jo, S. Jung, H. Yoo, Y. Hee, M. Suh, The control of neural cell-to-cell interactions through non-contact electrical field stimulation using graphene electrodes. Biomaterials 32, 19–27 (2011). https://doi.org/10.1016/j.biomaterials.2010.08.095

    Article  CAS  Google Scholar 

  65. C. Chen, T. Zhang, Q. Zhang, X. Chen, Biointerface by cell growth on graphene oxide doped bacterial biointerface by cell growth on graphene oxide doped bacterial cellulose / poly (3, 4-ethylenedioxythiophene ) nanofibers. ACS Appl. Mater. Interfaces. 8, 10183–10192 (2016). https://doi.org/10.1021/acsami.6b01243

    Article  CAS  Google Scholar 

  66. C.-H. Chen, C.-T. Lin, W.-L. Hsu, Y.-C. Chang, S.-R. Yeh, L.-J. Li, D.-J. Yao, A flexible hydrophilic-modified graphene microprobe for neural and cardiac recording, nanomedicine nanotechnology. Biol. Med. 9, 600–604 (2013)

    CAS  Google Scholar 

  67. W. Guo, S. Wang, X. Yu, J. Qiu, J. Li, W. Tang, Z. Li, X. Mou, H. Liu, Z. Wang, Construction of a 3D rGO–collagen hybrid scaffold for enhancement of the neural differentiation of mesenchymal stem cells. Nanoscale 8, 1897–1904 (2016)

    Article  CAS  Google Scholar 

  68. N. Abzan, M. Kharaziha, S. Labbaf, Development of three-dimensional piezoelectric polyvinylidene fluoride-graphene oxide scaffold by non-solvent induced phase separation method for nerve tissue engineering. Mater. Des. (2019). https://doi.org/10.1016/j.matdes.2019.107636

    Article  Google Scholar 

  69. C. Dong, F. Qiao, W. Hou, L. Yang, Y. Lv, Graphene-based conductive fibrous scaffold boosts sciatic nerve regeneration and functional recovery upon electrical stimulation. Appl. Mater. Today. 21, 100870 (2020)

    Article  Google Scholar 

  70. Y. Zhao, J. Gong, C. Niu, Z. Wei, J. Shi, G. Li, Y. Yang, H. Wang, A new electrospun graphene-silk fibroin composite scaffolds for guiding Schwann cells. J. Biomater. Sci. Polym. Ed. 28, 2171–2185 (2017). https://doi.org/10.1080/09205063.2017.1386835

    Article  CAS  Google Scholar 

  71. C. Zhu, T. Han, E.B. Duoss, A.M. Golobic, J.D. Kuntz, C.M. Spadaccini, M.A. Worsley, Highly compressible 3D periodic graphene aerogel microlattices. Nat. Commun. 6, 1–8 (2015)

    Article  Google Scholar 

  72. A. Farzan, S. Borandeh, J. Seppälä, Conductive polyurethane/PEGylated graphene oxide composite for 3D-printed nerve guidance conduits. Eur. Polym. J. (2022). https://doi.org/10.1016/j.eurpolymj.2022.111068

    Article  Google Scholar 

  73. E. Cattaneo, R. McKay, Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347, 762–765 (1990). https://doi.org/10.1038/347762a0

    Article  CAS  Google Scholar 

  74. C. Vicario-Abejón, K.K. Johe, T.G. Hazel, D. Collazo, R.D.G. McKay, Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15, 105–114 (1995). https://doi.org/10.1016/0896-6273(95)90068-3

    Article  Google Scholar 

  75. A. Schanzer, F. Wachs, D. Wilhelm, T. Acker, C. Cooper-Kuhn, B. H, J. Winkler, L. Aigner, K.H. Plate, H.G. Kuhn, Direct stimulation of adult neural stem cells by vascular endothelial growth factor. Brain Pathol. 14, 237–248 (2004)

    Article  Google Scholar 

  76. E.K.F. Yim, S.W. Pang, K.W. Leong, Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp. Cell Res. 313, 1820–1829 (2007). https://doi.org/10.1016/j.yexcr.2007.02.031

    Article  CAS  Google Scholar 

  77. F. Yang, R. Murugan, S. Wang, S. Ramakrishna, Electrospinning of nano/micro scale poly(l-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 26, 2603–2610 (2005). https://doi.org/10.1016/j.biomaterials.2004.06.051

    Article  CAS  Google Scholar 

  78. A.J. Engler, S. Sen, H.L. Sweeney, D.E. Discher, Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006). https://doi.org/10.1016/j.cell.2006.06.044

    Article  CAS  Google Scholar 

  79. N.D. Leipzig, M.S. Shoichet, Biomaterials the effect of substrate stiffness on adult neural stem cell behavior. Biomaterials 30, 6867–6878 (2009). https://doi.org/10.1016/j.biomaterials.2009.09.002

    Article  CAS  Google Scholar 

  80. K.A. Chang, J.W. Kim, J.A. Kim, S. Lee, S. Kim, W.H. Suh, H.S. Kim, S. Kwon, S.J. Kim, Y.H. Suh, Biphasic electrical currents stimulation promotes both proliferation and differentiation of fetal neural stem cells. PLoS ONE. (2011). https://doi.org/10.1371/journal.pone.0018738

    Article  Google Scholar 

  81. M.P. Prabhakaran, L. Ghasemi-mobarakeh, G. Jin, S. Ramakrishna, Electrospun conducting polymer nanofibers and electrical stimulation of nerve stem cells. JBIOSC. 112, 501–507 (2011). https://doi.org/10.1016/j.jbiosc.2011.07.010

    Article  CAS  Google Scholar 

  82. N. Wong, S. Kam, E. Jan, N.A. Kotov, Electrical stimulation of neural stem cells mediated by humanized carbon nanotube composite made with extracellular matrix protein (2009)

  83. R. Balint, S.H. Cartmell, Electrical stimulation: a novel tool. Tissue Eng. Part B 19, 48–57 (2013). https://doi.org/10.1089/ten.teb.2012.0183

    Article  CAS  Google Scholar 

  84. X. Yuan, D.E. Arkonac, P.H.G. Chao, G. Vunjak-Novakovic, Electrical stimulation enhances cell migration and integrative repair in the meniscus. Sci. Rep. 4, 1–12 (2015). https://doi.org/10.1038/srep03674

    Article  CAS  Google Scholar 

  85. B.C. Thompson, E. Murray, G.G. Wallace, Graphite oxide to graphene. Biomaterials to bionics. Adv. Mater. 27, 7563–82 (2015). https://doi.org/10.1002/adma.201500411

    Article  CAS  Google Scholar 

  86. M. Zhao, Electrical fields in wound healing—an overriding signal that directs cell migration. Semin. Cell Dev. Biol. 20, 674–682 (2009). https://doi.org/10.1016/j.semcdb.2008.12.009

    Article  CAS  Google Scholar 

  87. T. Gordon, Electrical stimulation for improving nerve regeneration: where do we stand?, 1st edn. (Elsevier, Philadelphia, 2009)

    Google Scholar 

  88. M. Lu, C. Ho, S. Hsu, H. Lee, J. Lin, C. Yao, Y. Chen, Effects of electrical stimulation at different frequencies on regeneration of transected peripheral nerve. Neurorehabil. Neural Repair. 22, 367–373 (2008). https://doi.org/10.1177/1545968307313507

    Article  Google Scholar 

  89. L.H. Hess, C. Becker-freyseng, M.S. Wismer, B.M. Blaschke, M. Lottner, F. Rolf, M. Seifert, J.A. Garrido, Electrical coupling between cells and graphene transistors. Small (2014). https://doi.org/10.1002/smll.201402225

    Article  Google Scholar 

  90. J.A. Fairfield, Nanostructured materials for neural electrical interfaces. Adv. Funct. Mater. 1701145, 1–12 (2017). https://doi.org/10.1002/adfm.201701145

    Article  CAS  Google Scholar 

  91. S.Y. Park, J. Park, S.H. Sim, M.G. Sung, K.S. Kim, B.H. Hong, S. Hong, Enhanced differentiation of human neural stem cells into neurons on graphene. Adv. Mater. 23, 263–267 (2011). https://doi.org/10.1002/adma.201101503

    Article  CAS  Google Scholar 

  92. M. Tang, Q. Song, N. Li, Z. Jiang, R. Huang, G. Cheng, Enhancement of electrical signaling in neural networks on graphene films. Biomaterials 34, 6402–6411 (2013). https://doi.org/10.1016/j.biomaterials.2013.05.024

    Article  CAS  Google Scholar 

  93. S. Meng, Nerve cell differentiation using constant and programmed electrical stimulation through conductive non-functional graphene nanosheets film. Tissue Eng. Regen. Med. 11, 274–283 (2014). https://doi.org/10.1007/s13770-014-0011-1

    Article  CAS  Google Scholar 

  94. D.A. Balikov, B. Fang, Y.W. Chun, S.W. Crowder, D. Prasai, J.B. Lee, K.I. Bolotin, H. Sung, Directing lineage specification of human mesenchymal stem cells by decoupling electrical stimulation and physical patterning on unmodified. Nanoscale. 8, 13730 (2016). https://doi.org/10.1039/c6nr04400j

    Article  CAS  Google Scholar 

  95. S.R. Das, M. Uz, S. Ding, M.T. Lentner, J.A. Hondred, A.A. Cargill, D.S. Sakaguchi, S. Mallapragada, J.C. Claussen, Electrical differentiation of mesenchymal stem cells into Schwann-cell-like phenotypes using inkjet-printed graphene circuits. Adv. Healthcare Mater. (2017). https://doi.org/10.1002/adhm.201601087

    Article  Google Scholar 

  96. O. Akhavan, E. Ghaderi, S.A. Shirazian, R. Rahighi, Rolled graphene oxide foams as three-dimensional scaffolds for growth of neural fibers using electrical stimulation of stem cells. Carbon N. Y. 97, 71–77 (2016). https://doi.org/10.1016/j.carbon.2015.06.079

    Article  CAS  Google Scholar 

  97. Z.Q. Feng, T. Wang, B. Zhao, J. Li, L. Jin, Soft graphene nanofibers designed for the acceleration of nerve growth and development. Adv. Mater. 27, 6462–6468 (2015). https://doi.org/10.1002/adma.201503319

    Article  CAS  Google Scholar 

  98. S. Aznar-cervantes, A. Pagán, J.G. Martínez, T.F. Otero, L. Meseguer-olmo, I. Paredes, J.L. Cenis, Electrospun silk fibroin scaffolds coated with reduced graphene promote neurite outgrowth of PC-12 cells under electrical stimulation. Mater. Sci. Eng. C. 79, 315–325 (2017). https://doi.org/10.1016/j.msec.2017.05.055

    Article  CAS  Google Scholar 

  99. W. Guo, X. Zhang, X. Yu, S. Wang, J. Qiu, W. Tang, L. Li, H. Liu, Z.L. Wang, W. Guo, X. Zhang, X. Yu, S. Wang, J. Qiu, W. Tang, L. Li, H. Liu, Z.L. Wang (2016) https://doi.org/10.1021/acsnano.6b00200

  100. M.S. Kang, J.H. Lee, S.-J. Song, D.-M. Shin, J.-H. Jang, S.-H. Hyon, S.W. Hong, J.H. Lee, D.-W. Han, Graphene oxide-functionalized nanofibre composite matrices to enhance differentiation of hippocampal neuronal cells. Mater. Adv. 1, 3496–3506 (2020). https://doi.org/10.1039/D0MA00733A

    Article  CAS  Google Scholar 

  101. R. Vajtai, Springer handbook of nanomaterials (Springer, Berlin, 2013)

    Book  Google Scholar 

  102. P. Avouris, J. Appenzeller, R. Martel, S.J. Wind, Carbon nanotube electronics. Proc. IEEE. 91, 1772–1784 (2003)

    Article  CAS  Google Scholar 

  103. Marc et al., Strongly correlated electron behavior in carbon nanotubes. EPJ Web Conf. 23, 19 (2012). https://doi.org/10.1051/epjconf/20122300019

    Article  CAS  Google Scholar 

  104. Q. Cao, Q. Yu, D.W. Connell, G. Yu, Titania/carbon nanotube composite (TiO2/CNT) and its application for removal of organic pollutants. Clean Technol. Environ. Policy 15, 871–880 (2013)

    Article  CAS  Google Scholar 

  105. W.-H. Chiang, D.N. Futaba, M. Yumura, K. Hata, Growth control of single-walled, double-walled, and triple-walled carbon nanotube forests by a priori electrical resistance measurement of catalyst films. Carbon N. Y. 49, 4368–4375 (2011)

    Article  CAS  Google Scholar 

  106. T. Guo, P. Nikolaev, A. Thess, D.T. Colbert, R.E. Smalley, Catalytic growth of single-walled manotubes by laser vaporization. Chem. Phys. Lett. 243, 49–54 (1995)

    Article  CAS  Google Scholar 

  107. W.-H. Chiang, R. Mohan Sankaran, Linking catalyst composition to chirality distributions of as-grown single-walled carbon nanotubes by tuning NixFe1− x nanoparticles. Nat. Mater. 8, 882–886 (2009)

    Article  CAS  Google Scholar 

  108. M. Baldrighi, M. Trusel, R. Tonini, S. Giordani, Carbon nanomaterials interfacing with neurons: an in vivo perspective. Front. Neurosci. 10, 1–27 (2016). https://doi.org/10.3389/fnins.2016.00250

    Article  Google Scholar 

  109. A. Kavosi, S. Hosseini Ghale Noei, S. Madani, S. Khalighfard, S. Khodayari, H. Khodayari, M. Mirzaei, M.R. Kalhori, M. Yavarian, A.M. Alizadeh, M. Falahati, The toxicity and therapeutic effects of single-and multi-wall carbon nanotubes on mice breast cancer. Sci. Rep. 8, 8375 (2018). https://doi.org/10.1038/s41598-018-26790-x

    Article  CAS  Google Scholar 

  110. C.M. Voge, J.P. Stegemann, Carbon nanotubes in neural interfacing applications. J. Neural Eng. (2011). https://doi.org/10.1088/1741-2560/8/1/011001

    Article  Google Scholar 

  111. J.-Y. Hwang, U.S. Shin, W.-C. Jang, J.K. Hyun, I.B. Wall, H.-W. Kim, Biofunctionalized carbon nanotubes in neural regeneration: a mini-review. Nanoscale 5, 487–497 (2013)

    Article  CAS  Google Scholar 

  112. K. Matsumoto, C. Sato, Y. Naka, R. Whitby, N. Shimizu, Stimulation of neuronal neurite outgrowth using functionalized carbon nanotubes. Nanotechnology 21, 1–9 (2010). https://doi.org/10.1088/0957-4484/21/11/115101

    Article  CAS  Google Scholar 

  113. S.J. Lee et al., 3D printing nano conductive multi-walled carbon nanotube scaffolds for nerve regeneration. J. Neural Eng. 15, 1–29 (2018)

    Article  Google Scholar 

  114. H.-S. Ahn, J.-Y. Hwang, M.S. Kim, J.-Y. Lee, J.-W. Kim, H.-S. Kim, U.S. Shin, J.C. Knowles, H.-W. Kim, J.K. Hyun, Carbon-nanotube-interfaced glass fiber scaffold for regeneration of transected sciatic nerve. Acta Biomater. 13, 324–334 (2015)

    Article  CAS  Google Scholar 

  115. S. Wu, B. Duan, A. Lu, Y. Wang, Q. Ye, L. Zhang, Biocompatible chitin/carbon nanotubes composite hydrogels as neuronal growth substrates. Carbohydr. Polym. 174, 830–840 (2017). https://doi.org/10.1016/j.carbpol.2017.06.101

    Article  CAS  Google Scholar 

  116. S.R. Shin, H. Bae, J.M. Cha, J.Y. Mun, Y.-C. Chen, H. Tekin, H. Shin, S. Zarabi, M.R. Dokmeci, S. Tang, Carbon nanotube reinforced hybrid microgels as scaffold materials for cell encapsulation. ACS Nano 6, 362–372 (2011)

    Article  Google Scholar 

  117. A.N. Koppes, K.W. Keating, A.L. McGregor, R.A. Koppes, K.R. Kearns, A.M. Ziemba, C.A. McKay, J.M. Zuidema, C.J. Rivet, R.J. Gilbert, D.M. Thompson, Robust neurite extension following exogenous electrical stimulation within single walled carbon nanotube-composite hydrogels. Acta Biomater. 39, 34–43 (2016). https://doi.org/10.1016/j.actbio.2016.05.014

    Article  CAS  Google Scholar 

  118. X. Zhang, S. Prasad, S. Niyogi, A. Morgan, M. Ozkan, C.S. Ozkan, Guided neurite growth on patterned carbon nanotubes. Sensors Actuators B Chem. 106, 843–850 (2005). https://doi.org/10.1016/j.snb.2004.10.039

    Article  CAS  Google Scholar 

  119. G.-Z. Jin, M. Kim, U.S. Shin, H.-W. Kim, Neurite outgrowth of dorsal root ganglia neurons is enhanced on aligned nanofibrous biopolymer scaffold with carbon nanotube coating. Neurosci. Lett. 501, 10–14 (2011). https://doi.org/10.1016/j.neulet.2011.06.023

    Article  CAS  Google Scholar 

  120. G.S. Lorite, L. Ylä-Outinen, L. Janssen, O. Pitkänen, T. Joki, J.T. Koivisto, M. Kellomäki, R. Vajtai, S. Narkilahti, K. Kordas, Carbon nanotube micropillars trigger guided growth of complex human neural stem cells networks. Nano Res. 12, 2894–2899 (2019). https://doi.org/10.1007/s12274-019-2533-2

    Article  CAS  Google Scholar 

  121. X. Chen, C. Liu, Z. Huang, X. Pu, L. Shang, G. Yin, C. Xue, Preparation of carboxylic graphene oxide-composited polypyrrole conduits and their effect on sciatic nerve repair under electrical stimulation. J. Biomed. Mater. Res. Part A. 107, 2784–2795 (2019)

    Article  CAS  Google Scholar 

  122. J.V. Veetil, K. Ye, Tailored carbon nanotubes for tissue engineering applications. Biotechnol. Prog. 25, 709–721 (2009). https://doi.org/10.1002/btpr.165

    Article  CAS  Google Scholar 

  123. J.R. Lee, S. Ryu, S. Kim, B.S. Kim, Behaviors of stem cells on carbon nanotube. Biomater. Res. 19, 19–24 (2015). https://doi.org/10.1186/s40824-014-0024-9

    Article  CAS  Google Scholar 

  124. G.A. Posypanova, I.A. Gayduchenko, E.Y. Moskaleva, G.E. Fedorov, Neuronal differentiation of PC12 cells and mouse neural stem cells on carbon nanotube films. Cell Tissue Biol. 10, 194–201 (2016). https://doi.org/10.1134/S1990519X16030111

    Article  Google Scholar 

  125. Morris et al., 基因的改变NIH public access. Gerontology 61, 515–525 (2015). https://doi.org/10.1002/adhm.201400042.Carbon

    Article  CAS  Google Scholar 

  126. W. Seok Lee, B.E. Yoon, The brain cells on the carbon nanotubes: morphological and functional changes in neurons and glia (J. Mol. Nanotechnol. Nanomater., 2018). https://doi.org/10.4172/2324-8777.1000241

    Book  Google Scholar 

  127. Z. Zhou, X. Liu, W. Wu, S. Park, A.L. Miller, A. Terzic, L. Lu, Effective nerve cell modulation by electrical stimulation of carbon nanotube embedded conductive polymeric scaffolds. Biomater. Sci. 6, 2375–2385 (2018). https://doi.org/10.1039/c8bm00553b

    Article  CAS  Google Scholar 

  128. S.Y. Park, D.S. Choi, H.J. Jin, J. Park, K.E. Byun, K.B. Lee, S. Hong, Polarization-controlled differentiation of human neural stem cells using synergistic cues from the patterns of carbon nanotube monolayer coating. ACS Nano 5, 4704–4711 (2011). https://doi.org/10.1021/nn2006128

    Article  CAS  Google Scholar 

  129. X. Li, W. Yang, H. Xie, J. Wang, L. Zhang, Z. Wang, L. Wang, CNT/sericin conductive nerve guidance conduit promotes functional recovery of transected peripheral nerve injury in a rat model. ACS Appl. Mater. Interfaces. 12, 36860–36872 (2020). https://doi.org/10.1021/acsami.0c08457

    Article  CAS  Google Scholar 

  130. J.H. Lee, J.Y. Lee, S.H. Yang, E.J. Lee, H.W. Kim, Carbon nanotube-collagen three-dimensional culture of mesenchymal stem cells promotes expression of neural phenotypes and secretion of neurotrophic factors. Acta Biomater. 10, 4425–4436 (2014). https://doi.org/10.1016/j.actbio.2014.06.023

    Article  CAS  Google Scholar 

  131. H. Hu, Y. Ni, S.K. Mandal, V. Montana, B. Zhao, R.C. Haddon, V. Parpura, Polyethyleneimine functionalized single-walled carbon nanotubes as a substrate for neuronal growth. J. Phys. Chem. B. 109, 4285–4289 (2005). https://doi.org/10.1021/jp0441137

    Article  CAS  Google Scholar 

  132. Y.C. Huang, S.H. Hsu, W.C. Kuo, C.L. Chang-Chien, H. Cheng, Y.Y. Huang, Effects of laminin-coated carbon nanotube/chitosan fibers on guided neurite growth. J. Biomed. Mater. Res. Part A. 99, 86–93 (2011). https://doi.org/10.1002/jbm.a.33164

    Article  CAS  Google Scholar 

  133. K. Shah, D. Vasileva, A. Karadaghy, S.P. Zustiak, Development and characterization of polyethylene glycol-carbon nanotube hydrogel composite. J. Mater. Chem. B. 3, 7950–7962 (2015). https://doi.org/10.1039/c5tb01047k

    Article  CAS  Google Scholar 

  134. N. Nazeri, R. Karimi, H. Ghanbari, The effect of surface modification of poly-lactide-co-glycolide/carbon nanotube nanofibrous scaffolds by laminin protein on nerve tissue engineering. J. Biomed. Mater. Res. - Part A. 109, 159–169 (2021). https://doi.org/10.1002/jbm.a.37013

    Article  CAS  Google Scholar 

  135. H. Hu, Y. Ni, V. Montana, R.C. Haddon, V. Parpura, Chemically functionalized carbon nanotubes as substrates for neuronal growth. Nano Lett. 4, 507–511 (2004). https://doi.org/10.1021/nl035193d

    Article  CAS  Google Scholar 

  136. N. Vicentini, T. Gatti, M. Salerno, Y.S. Hernandez Gomez, M. Bellon, S. Gallio, C. Marega, F. Filippini, E. Menna, Effect of different functionalized carbon nanostructures as fillers on the physical properties of biocompatible poly(L-lactic acid) composites. Mater. Chem. Phys. 214, 265–276 (2018). https://doi.org/10.1016/j.matchemphys.2018.04.042

    Article  CAS  Google Scholar 

  137. H. Shao, T. Li, R. Zhu, X. Xu, J. Yu, S. Chen, L. Song, S. Ramakrishna, Z. Lei, Y. Ruan, L. He, Carbon nanotube multilayered nanocomposites as multifunctional substrates for actuating neuronal differentiation and functions of neural stem cells. Biomaterials 175, 93–109 (2018). https://doi.org/10.1016/j.biomaterials.2018.05.028

    Article  CAS  Google Scholar 

  138. E. Mirzaei, J. Ai, S. Ebrahimi-Barough, J. Verdi, H. Ghanbari, R. Faridi-Majidi, The differentiation of human endometrial stem cells into neuron-like cells on electrospun PAN-derived carbon nanofibers with random and aligned topographies. Mol. Neurobiol. 53, 4798–4808 (2016)

    Article  CAS  Google Scholar 

  139. V. Brunetti, G. Maiorano, L. Rizzello, B. Sorce, S. Sabella, R. Cingolani, P.P. Pompa, Neurons sense nanoscale roughness with nanometer sensitivity. Proc. Natl. Acad. Sci. USA 107, 6264–6269 (2010). https://doi.org/10.1073/pnas.0914456107

    Article  Google Scholar 

  140. Z. Zhou, X. Liu, W. Wu, S. Park, A.L.M. Ii, A. Terzic, L. Lu, Effective nerve cell modulation by electrical stimulation of carbon nanotube embedded conductive polymeric scaffold. Biomater. Sci. 6, 2375–2385 (2018). https://doi.org/10.1039/c8bm00553b

    Article  CAS  Google Scholar 

  141. M. Imaninezhad, K. Pemberton, F. Xu, K. Kalinowski, R. Bera, S.P. Zustiak, Directed and enhanced neurite outgrowth following exogenous electrical stimulation on carbon nanotube-hydrogel composites. J. Neural Eng. 15, 56034 (2018). https://doi.org/10.1088/1741-2552/aad65b

    Article  Google Scholar 

  142. J. Wang, L. Tian, N. Chen, S. Ramakrishna, X. Mo, The cellular response of nerve cells on poly-l-lysine coated PLGA-MWCNTs aligned nanofibers under electrical stimulation. Mater. Sci. Eng. C. 91, 715–726 (2018)

    Article  CAS  Google Scholar 

  143. J. Zhang, X. Zhang, C. Wang, F. Li, Z. Qiao, L. Zeng, Z. Wang, H. Liu, J. Ding, H. Yang, Conductive composite fiber with optimized alignment guides neural regeneration under electrical stimulation. Adv. Healthc. Mater. (2021). https://doi.org/10.1002/adhm.202000604

    Article  Google Scholar 

  144. L. Cao, C.D. Mccaig, J. Pu, Extracellular electric signals regulate neuroblast behaviours in adult brain. Arch. Stem Cell Res. 2, 1010 (2015)

    Google Scholar 

  145. H. Cheng, Y. Huang, H. Yue, Y. Fan, Electrical stimulation promotes stem cell neural differentiation in tissue engineering. Stem Cells Int. (2021). https://doi.org/10.1155/2021/6697574

    Article  Google Scholar 

  146. X. Meng, M. Arocena, J. Penninger, F.H. Gage, M. Zhao, B. Song, PI3K mediated electrotaxis of embryonic and adult neural progenitor cells in the presence of growth factors. Exp. Neurol. 227, 210–217 (2011). https://doi.org/10.1016/j.expneurol.2010.11.002

    Article  CAS  Google Scholar 

  147. C. Yang, L. Wang, W. Weng, S. Wang, Y. Ma, Q. Mao, G. Gao, R. Chen, J. Feng, Steered migration and changed morphology of human astrocytes by an applied electric field. Exp. Cell Res. 374, 282–289 (2019). https://doi.org/10.1016/j.yexcr.2018.11.029

    Article  CAS  Google Scholar 

  148. M. Arocena, M. Zhao, J.M. Collinson, 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, 3267–3274 (2010). https://doi.org/10.1002/jnr.22502

    Article  CAS  Google Scholar 

  149. Z. Dong, Z. Pei, Y. Wang, Z. Li, A. Khan, X. Meng, Ascl1 regulates electric field-induced neuronal differentiation through PI3K/Akt pathway. Neuroscience. 404, 141–152 (2019). https://doi.org/10.1016/j.neuroscience.2019.02.004

    Article  CAS  Google Scholar 

  150. A.M. Rajnicek, L.E. Foubister, 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, 1723–1735 (2006). https://doi.org/10.1242/jcs.02896

    Article  CAS  Google Scholar 

  151. J. Zhang, M. Calafiore, Q. Zeng, X. Zhang, Y. Huang, R.A. Li, W. Deng, M. Zhao, Electrically guiding migration of human induced pluripotent stem cells. Stem Cell Rev. Rep. 7, 987–996 (2011). https://doi.org/10.1007/s12015-011-9247-5

    Article  Google Scholar 

  152. M. Wang, P. Li, M. Liu, W. Song, Q. Wu, Y. Fan, Potential protective effect of biphasic electrical stimulation against growth factor-deprived apoptosis on olfactory bulb neural progenitor cells through the brain-derived neurotrophic factor-phosphatidylinositol 3′-kinase/Akt pathway. Exp. Biol. Med. 238, 951–959 (2013). https://doi.org/10.1177/1535370213494635

    Article  CAS  Google Scholar 

  153. Y.J. Chang, C.M. Hsu, C.H. Lin, M.S.C. Lu, L. Chen, Electrical stimulation promotes nerve growth factor-induced neurite outgrowth and signaling. Biochim. Biophys. Acta - Gen. Subj. 2013, 4130–4136 (1830). https://doi.org/10.1016/j.bbagen.2013.04.007

    Article  CAS  Google Scholar 

  154. G.L. Ming, J. Henley, M. Tessier-Lavigne, H.J. Song, M.M. Poo, Electrical activity modulates growth cone guidance by diffusible factors. Neuron 29, 441–452 (2001). https://doi.org/10.1016/S0896-6273(01)00217-3

    Article  CAS  Google Scholar 

  155. M. Yamada, K. Tanemura, S. Okada, A. Iwanami, M. Nakamura, H. Mizuno, M. Ozawa, R. Ohyama-Goto, N. Kitamura, M. Kawano, K. Tan-Takeuchi, C. Ohtsuka, A. Miyawaki, A. Takashima, M. Ogawa, Y. Toyama, H. Okano, T. Kondo, Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem Cells. 25, 562–570 (2007). https://doi.org/10.1634/stemcells.2006-0011

    Article  CAS  Google Scholar 

  156. M.L. Baer, S.C. Henderson, R.J. Colello, Elucidating the role of injury-induced electric fields (EFs) in regulating the astrocytic response to injury in the mammalian central nervous system. PLoS ONE 10, 1–29 (2015). https://doi.org/10.1371/journal.pone.0142740

    Article  CAS  Google Scholar 

  157. J.F. Feng, J. Liu, L. Zhang, J.Y. Jiang, M. Russell, B.G. Lyeth, J.A. Nolta, M. Zhao, Electrical guidance of human stem cells in the rat brain. Stem Cell Rep. 9, 177–189 (2017). https://doi.org/10.1016/j.stemcr.2017.05.035

    Article  Google Scholar 

  158. T. Yasuda, P.F. Bartlett, D.J. Adams, Kir and Kv channels regulate electrical properties and proliferation of adult neural precursor cells. Mol. Cell. Neurosci. 37, 284–297 (2008). https://doi.org/10.1016/j.mcn.2007.10.003

    Article  CAS  Google Scholar 

  159. L. Yao, C.D. McCaig, M. Zhao, Electrical signals polarize neuronal organelles, direct neuron migration, and orient cell division. Hippocampus 19, 855–868 (2009). https://doi.org/10.1002/hipo.20569

    Article  CAS  Google Scholar 

  160. S. Ghosh, P. Roy, D. Lahiri, Enhanced neurogenic differentiation on anisotropically conductive carbon nanotube reinforced polycaprolactone- collagen scaffold by applying direct coupling electrical stimulation. Int. J. Biol. Macromol. (2022). https://doi.org/10.1016/j.ijbiomac.2022.07.087

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the financial funding provided by the Indian Council of Medical Research (ICMR) grant no. (5/3/8/293/2015-ITR) and Intensification of Research in High Priority Areas (IRHPA) grant no. (IPA/2020/000025). The authors are sincerely thankful to the Indian Institute of Technology, Roorkee for providing the infrastructure and facilities for this study. The authors would like to express gratitude to support for all the personnel from, Department of Biosciences & Bioengineering, Department of Metallurgical and Materials Engineering and Centre for Nanotechnology.

Funding

Financial support was received from ICMR (5/3/8/293/2015-ITR) and IRHPA (IPA/2020/000025).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Debrupa Lahiri.

Ethics declarations

Conflict of interest

The authors have no competing interests that are relevant to the content to this article.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaushik, G., Khatua, C., Ghosh, S. et al. Electrical Stimulation-Mediated Differentiation of Neural Cells on Conductive Carbon Nanofiller-Based Scaffold. Biomedical Materials & Devices 1, 301–318 (2023). https://doi.org/10.1007/s44174-022-00011-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s44174-022-00011-6

Keywords

Navigation