Skip to main content

Advertisement

SpringerLink
Log in

The Role of Direct Current Electric Field-Guided Stem Cell Migration in Neural Regeneration

  • Published:
Stem Cell Reviews and Reports Aims and scope Submit manuscript

Abstract

Effective directional axonal growth and neural cell migration are crucial in the neural regeneration of the central nervous system (CNS). Endogenous currents have been detected in many developing nervous systems. Experiments have demonstrated that applied direct current (DC) electric fields (EFs) can guide axonal growth in vitro, and attempts have been made to enhance the regrowth of damaged spinal cord axons using DC EFs in in vivo experiments. Recent work has revealed that the migration of stem cells and stem cell-derived neural cells can be guided by DC EFs. These studies have raised the possibility that endogenous and applied DC EFs can be used to direct neural tissue regeneration. Although the mechanism of EF-directed axonal growth and cell migration has not been fully understood, studies have shown that the polarization of cell membrane proteins and the activation of intracellular signaling molecules are involved in the process. The application of EFs is a promising biotechnology for regeneration of the CNS.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Gould, E., & Tanapat, P. (1997). Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience, 80, 427–436.

    Article  CAS  PubMed  Google Scholar 

  2. Fallon, J., Reid, S., Kinyamu, R., Opole, I., Opole, R., Baratta, J., et al. (2000). In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proceedings of the National Academy of Sciences of the United States of America, 97, 14686–14691.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Yoshimura, N., Seki, S., Novakovic, S. D., Tzoumaka, E., Erickson, V. L., Erickson, K. A., et al. (2001). The involvement of the tetrodotoxin-resistant sodium channel Na(v)1.8 (PN3/SNS) in a rat model of visceral pain. The Journal of Neuroscience, 21, 8690–8696.

    CAS  PubMed  Google Scholar 

  4. Yamamoto, S., Nagao, M., Sugimori, M., Kosako, H., Nakatomi, H., Yamamoto, N., et al. (2001). Transcription factor expression and Notch-dependent regulation of neural progenitors in the adult rat spinal cord. The Journal of Neuroscience, 21, 9814–9823.

    CAS  PubMed  Google Scholar 

  5. Madhavan, L., Daley, B. F., Paumier, K. L., & Collier, T. J. (2009). Transplantation of subventricular zone neural precursors induces an endogenous precursor cell response in a rat model of Parkinson’s disease. Journal of Comparative Neurology, 515, 102–115.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Elliott, R. C., Miles, M. F., & Lowenstein, D. H. (2003). Overlapping microarray profiles of dentate gyrus gene expression during development- and epilepsy-associated neurogenesis and axon outgrowth. The Journal of Neuroscience, 23, 2218–2227.

    CAS  PubMed  Google Scholar 

  7. Englund, U., Bjorklund, A., Wictorin, K., Lindvall, O., & Kokaia, M. (2002). Grafted neural stem cells develop into func-tional pyramidal neurons and integrate into host cortical circuitry. Proceedings of the National Academy of Sciences of the United States of America, 99, 17089–17094.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Martino, G., & Pluchino, S. (2006). The therapeutic potential of neural stem cells. Nature Reviews Neuroscience, 7, 395–406.

    Article  CAS  PubMed  Google Scholar 

  9. Nomura, H., Zahir, T., Kim, H., Katayama, Y., Kulbatski, I., Morshead, C. M., et al. (2008). Extramedullary chitosan channels promote survival of transplanted neural stem and progenitor cells and create a tissue bridge after complete spinal cord transection. Tissue Engineering, 14, 649–665.

    Article  CAS  PubMed  Google Scholar 

  10. Du, B. L., Xiong, Y., Zeng, C. G., He, L. M., Zhang, W., Quan, D. P., et al. (2011). Transplantation of artificial neural construct partly improved spinal tissue repair and functional recovery in rats with spinal cord transection. Brain Research, 1400, 87–98.

    Article  CAS  PubMed  Google Scholar 

  11. All, A. H., Gharibani, P., Gupta, S., Bazley, F. A., Pashai, N., Chou, B. K., et al. (2015). Early intervention for spinal cord injury with human induced pluripotent stem cells oligodendrocyte progenitors. PLoS One, 10, e0116933.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Jaffe, L. F., & Nuccitelli, R. (1974). An ultrasensitive vibrating probe for measuring steady extracellular currents. Journal of Cell Biology, 63, 614–628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Robinson, K. R. (1979). Electrical currents through full-grown and maturing Xenopus oocytes. Proceedings of the National Academy of Sciences of the United States of America, 76, 837–841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Jaffe, L. F., & Stern, C. D. (1979). Strong electrical currents leave the primitive streak of chick embryos. Science, 206, 569–571.

    Article  CAS  PubMed  Google Scholar 

  15. Robinson, K. R. (1983). Endogenous electrical current leaves the limb and pre-limb region of the Xenopus embryo. Developmental Biology, 97, 203–211.

    Article  CAS  PubMed  Google Scholar 

  16. Hotary, K. B., & Robinson, K. R. (1990). Endogenous electrical currents and the resultant voltage gradients in the chick embryo. Developmental Biology, 140, 149–160.

    Article  CAS  PubMed  Google Scholar 

  17. Hotary, K. B., & Robinson, K. R. (1991). The neural tube of the Xenopus embryo maintains a potential difference across itself. Developmental Brain Research, 59, 65–73.

    Article  CAS  PubMed  Google Scholar 

  18. Robinson, K.R., & Messerli, M.A. (1996). Electric embryos: the embryonic epithelium as a generator of developmental information. In: McCaig CD, Editor, Nerve Growth and Nerve Guidance, Portland Press 131–150.

  19. Ingvar, S. (1920). Reactions of cells to the galvanic current in tissue culture. Proceedings of the Society for Experimental Biology and Medicine, 17, 198–199.

    Article  Google Scholar 

  20. Hotary, K. B., & Robinson, K. R. (1992). Evidence for a role for endogenous electrical fields in chick embryo development. Development, 114, 985–996.

    CAS  PubMed  Google Scholar 

  21. Hotary, K. B., & Robinson, K. B. (1994). Endogenous electrical currents and voltage gradients in Xenopus embryos and the consequences of their disruption. Developmental Biology, 166, 789–800.

    Article  CAS  PubMed  Google Scholar 

  22. Borgens, R. B., & Shi, R. (1995). Uncoupling histogenesis from morphogenesis in the vertebrate embryo by collapse of the transneural tube potential. Developmental Dynamics, 203, 456–467.

    Article  CAS  PubMed  Google Scholar 

  23. Metcalf, M. E., & Borgens, R. B. (1994). Weak applied voltages interfere with amphibian morphogenesis and pattern. Journal of Experimental Zoology, 268, 322–338.

    Google Scholar 

  24. Jaffe, L. F., & Poo, M. M. (1979). Neurites grow faster towards the cathode than the anode in a steady field. Journal of Experimental Zoology, 209, 115–128.

    Article  CAS  PubMed  Google Scholar 

  25. Yao, L., Shanley, L., McCaig, C., & Zhao, M. (2008). Small applied electric fields guide migration of hippocampal neurons. Journal of Cellular Physiology, 216, 527–535.

    Article  CAS  PubMed  Google Scholar 

  26. Feng, J. F., Liu, J., Zhang, X. Z., Zhang, L., Jiang, J. Y., Nolta, J., et al. (2012). Guided migration of neural stem cells derived from human embryonic stem cells by an electric field. Stem Cells, 30, 349–355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Tessier-Lavigne, M., & Goodman, C. (1996). The molecular biology of axon guidance. Science, 274, 1123–1133.

    Article  CAS  PubMed  Google Scholar 

  28. Bentley, D., & O’Connor, T. P. (1994). Cytoskeletal events in growth cone steering. Current Opinion in Neurobiology, 4, 43–48.

    Article  CAS  PubMed  Google Scholar 

  29. Tanaka, E., & Sabry, J. (1995). Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell, 83, 171–176.

    Article  CAS  PubMed  Google Scholar 

  30. Suter, D. M., & Forscher, P. (2000). Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. Journal of Neurobiology, 44, 97–113.

    Article  CAS  PubMed  Google Scholar 

  31. Song, H., & Poo, M. (2001). The cell biology of neuronal navigation. Nature Cell Biology, 3, E81–8.

    Article  CAS  PubMed  Google Scholar 

  32. Catalano, S. M., & Shatz, C. J. (1998). Activity-dependent cortical target selection by thalamic axons. Science, 281, 559–562.

    Article  CAS  PubMed  Google Scholar 

  33. Dantzker, J. L., & Callaway, E. M. (1998). The development of local, layer-specific visual cortical axons in the absence of extrinsic influences and intrinsic activity. The Journal of Neuroscience, 18, 4145–4154.

    CAS  PubMed  Google Scholar 

  34. McCaig, C. D. (1987). Spinal neurite reabsorption and regrowth in vitro depend on the polarity of an applied electric field. Development, 100, 31–41.

    CAS  PubMed  Google Scholar 

  35. McCaig, C. D. (1986). Dynamic aspects of amphibian neurite growth and the effects of an applied electric field. The Journal of Physiology, 375, 55–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hinkle, L., McCaig, C. D., & Robinson, K. R. (1981). The direction of growth of differentiating neurones and myoblasts from frog embryos in an applied electric field. The Journal of Physiology, 314, 121–135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Caroni, P. (1998). Driving the growth cone. Science, 281, 1465–1466.

    Article  CAS  PubMed  Google Scholar 

  38. Ming, G. L., Henley, J., Tessier-Lavigne, M., Song, H. J., & Poo, M. M. (2001). Electric activity modulates growth cone guidance by diffusible factors. Neuron, 29, 441–452.

    Article  CAS  PubMed  Google Scholar 

  39. Rajnicek, A. M., Foubister, L. E., & McCaig, C. D. (2006). Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric field. Journal of Cell Science, 119, 1723–1735.

    Article  CAS  PubMed  Google Scholar 

  40. Nuccitelli, R. (2003). A role for endogenous electric fields in wound healing. Current Topics in Developmental Biology, 58, 1–26.

    Article  PubMed  Google Scholar 

  41. Cortese, B., Palamà, I. E., D’Amone, S., & Gigli, G. (2014). Influence of electrotaxis on cell behaviour. Integrative Biology (Camb), 6, 817–30.

    Article  CAS  Google Scholar 

  42. Chang, P. C., Sulik, G. I., Soong, H. K., & Parkinson, W. C. (1996). Galvanotropic and galvanotaxic responses of corneal endothelial cells. Journal of the Formosan Medical Association, 95, 623–7.

    CAS  PubMed  Google Scholar 

  43. Zhao, M., Bai, H., Wang, E., Forrester, J. V., & McCaig, C. D. (2004). Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signaling through VEGF receptors. Journal of Cell Science, 117, 397–405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Li, X., & Kolega, J. (2002). Effects of direct current electric fields on cell migration and actin filament distribution in bovine vascular endothelial cells. Journal of Vascular Research, 39, 391–404.

    Article  CAS  PubMed  Google Scholar 

  45. Yao, L., McCaig, C. D., & Zhao, M. (2009). Electrical signals polarize neuronal organelles, direct neuron migration, and orient cell division. Hippocampus, 19, 855–68.

    Article  CAS  PubMed  Google Scholar 

  46. Almad, A., Sahinkaya, F. R., & McTigue, D. M. (2011). Oligodendrocyte fate after spinal cord injury. Neurotherapeutics, 8, 262–273.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Wang, S., Sdrulla, A. D., DiSibio, G., Bush, G., Nofziger, D., Hicks, C., et al. (1998). Notch receptor activation inhibits oligodendrocyte differentiation. Neuron, 21, 63–75.

    Article  PubMed  Google Scholar 

  48. Cao, Q., He, Q., Wang, Y., Cheng, X., Howard, R. M., Zhang, Y., et al. (2010). Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. The Journal of Neuroscience, 30, 2989–3001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Jeffery, N. D., Crang, A. J., O’leary, M. T., Hodge, S. J., & Blakemore, W. F. (1999). Behavioural consequences of oligodendrocyte progenitor cell transplantation into experimental demyelinating lesions in the rat spinal cord. European Journal of Neuroscience, 11, 1508–1514.

    Article  CAS  PubMed  Google Scholar 

  50. Lee, K. H., Yoon, D. H., Park, Y. G., & Lee, B. H. (2005). Effects of glial transplantation on functional recovery following acute spinal cord injury. Journal of Neurotrauma, 22, 575–589.

    Article  PubMed  Google Scholar 

  51. Guest, J. D., Hiester, E. D., & Bunge, R. P. (2005). Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Experimental Neurology, 192, 384–393.

    Article  CAS  PubMed  Google Scholar 

  52. Thuret, S., Moon, L. D., & Gage, F. H. (2006). Therapeutic interventions after spinal cord injury. Nature Reviews Neuroscience, 7, 628–643.

    Article  CAS  PubMed  Google Scholar 

  53. Iannotti, C., Li, H., Yan, P., Lu, X., Wirthlin, L., & Xu, X. M. (2003). Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Experimental Neurology, 183, 379–393.

    Article  CAS  PubMed  Google Scholar 

  54. Liu, G., Wang, X., Shao, G., & Liu, Q. (2014). Genetically modified Schwann cells producing glial cell line-derived neurotrophic factor inhibit neuronal apoptosis in rat spinal cord injury. Molecular Medicine Reports, 9, 1305–1312.

    CAS  PubMed  Google Scholar 

  55. Yao, L., Li, Y., Knapp, J., & Smith, P. (2015). Exploration of molecular pathways mediating electric field-directed Schwann cell migration by RNA-Seq. Journal of Cellular Physiology, 230, 1515–1524.

    Article  CAS  PubMed  Google Scholar 

  56. Li, Y., Wang, X., & Yao, L. (2015). Directional migration and transcriptional analysis of oligodendrocyte precursors subjected to stimulation of electrical signal. American Journal of Physiology. Cell Physiology, 309, C532–540.

    Article  PubMed  Google Scholar 

  57. Meng, X., Arocena, M., Penninger, J., Gage, F. H., Zhao, M., & Song, B. (2011). PI3K mediated electrotaxis of embryonic and adult neural progenitor cells in the presence of growth factors. Experimental Neurology, 227, 210–217.

    Article  CAS  PubMed  Google Scholar 

  58. Nishino, H., Hida, H., Takei, N., Kumazaki, M., Nakajima, K., & Baba, H. (2000). Mesencephalic neural stem (progenitor) cells develop to dopaminergic neurons more strongly in dopamine-depleted striatum than in intact striatum. Experimental Neurology, 164, 209–14.

    Article  CAS  PubMed  Google Scholar 

  59. Shim, J. W., Park, C. H., Bae, Y. C., Bae, J. Y., Chung, S., Chang, M. Y., et al. (2007). Generation of functional dopamine neurons from neural precursor cells isolated from the subventricular zone and white matter of the adult rat brain using Nurr1 overexpression. Stem Cells, 25, 1252–62.

    Article  CAS  PubMed  Google Scholar 

  60. Liu, J., Zhu, B., Zhang, G., Wang, J., Tian, W., Ju, G., et al. (2015). Electric signals regulate directional migration of ventral midbrain derived dopaminergic neural progenitor cells via Wnt/GSK3β signaling. Experimental Neurology, 263, 113–121.

    Article  CAS  PubMed  Google Scholar 

  61. Grade, S., Agasse, F., Bernardino, L., & Malva, J. O. (2012). Functional identification of neural stem cell-derived oligodendrocytes. Methods in Molecular Biology, 879, 165–178.

    Article  CAS  PubMed  Google Scholar 

  62. Broughton, S. K., Chen, H., Riddle, A., Kuhn, S. E., Nagalla, S., Roberts, C. T., Jr., et al. (2007). Large-scale generation of highly enriched neural stem-cell-derived oligodendroglial cultures: maturation-dependent differences in insulin-like growth factor-mediated signal transduction. Journal of Neurochemistry, 100, 628–638.

    Article  CAS  PubMed  Google Scholar 

  63. Li, Y., Wang, P. S., Lucas, G., Li, R., & Yao, L. (2015). ARP2/3 complex is required for directional migration of neural stem cell-derived oligodendrocyte precursors in electric fields. Stem Cell Research & Therapy, 2015(6), 41.

    Article  CAS  Google Scholar 

  64. Babona-Pilipos, R., Droujinine, I. A., Popovic, M. R., & Morshead, C. M. (2011). Adult subependymal neural precursors, but not differentiated cells, undergo rapid cathodal migration in the presence of direct current electric fields. PLoS One, 6, e23808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Li, Y., Weiss, M., & Yao, L. (2014). Directed migration of embryonic stem cell derived motor neuron in an applied electric field. Stem Cell Reviews and Reports, 10, 653–662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Zhang, J., Calafiore, M., Zeng, Q., Zhang, X., Huang, Y., Li, R. A., et al. (2011). Electrically guiding migration of human induced pluripotent stem cells. Stem Cell Reviews and Reports, 7, 987–996.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Ozdemir, M., Attar, A., Kuzu, I., Ayten, M., Ozgencil, E., Bozkurt, M., et al. (2012). Stem cell therapy in spinal cord injury: in vivo and postmortem tracking of bone marrow mononuclear or mesenchymal stem cells. Stem Cell Reviews, 8, 953–962.

    Article  CAS  PubMed  Google Scholar 

  68. Quertainmont, R., Cantinieaux, D., Botman, O., Sid, S., Schoenan, J., & Franzen, R. (2012). Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro-angiogenic actions. PLoS ONE, 7, e39500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zhao, Z., Watt, C., Karystinou, A., Roelofs, A. J., McCaig, C. D., Gibson, I. R., et al. (2011). Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. European Cells & Materials, 22, 344–358.

    CAS  Google Scholar 

  70. Jaffe, L. F. (1977). Electrophoresis along cell membranes. Nature, 265, 600–602.

    Article  CAS  PubMed  Google Scholar 

  71. Poo, M., & Robinson, K. R. (1977). Electrophoresis of concanavalin a receptors along embryonic muscle cell membrane. Nature, 265, 602–5.

    Article  CAS  PubMed  Google Scholar 

  72. Orida, N., & Poo, M. M. (1978). Electrophoretic movement and localisation of acetylcholine receptors in the embryonic muscle cell membrane. Nature, 275, 31–5.

    Article  CAS  PubMed  Google Scholar 

  73. McLaughlin, S., & Poo, M. M. (1981). The role of electro-osmosis in the electric-field-induced movement of charged macromolecules on the surfaces of cells. Biophysical Journal, 34, 85–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Poo, M. (1981). In situ electrophoresis of membrane components. Annual Review of Biophysics and Bioengineering Journal, 10, 245–276.

    Article  CAS  Google Scholar 

  75. Nishimura, K. Y., Isseroff, R. R., & Nuccitelli, R. (1996). Human keratinocytes migrate to the negative pole in direct current electric fields comparable to those measured in mammalian wounds. Journal of Cell Science, 109, 199–207.

    CAS  PubMed  Google Scholar 

  76. Brust-Mascher, I., & Webb, W. W. (1998). Calcium waves induced by large voltage pulses in fish keratocytes. Biophysical Journal, 75, 1669–1678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Onuma, E. K., & Hui, S. W. (1988). Electric field-directed cell shape changes, displacement, and cytoskeletal reorganization are calcium dependent. The Journal of Cell Biology, 106, 2067–2075.

    Article  CAS  PubMed  Google Scholar 

  78. Chan, A. Y., Raft, S., Bailly, M., Wyckoff, J. B., Segall, J. E., & Condeelis, J. S. (1998). EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells. Journal of Cell Science, 111, 199–211.

    CAS  PubMed  Google Scholar 

  79. Svitkina, T. M., Neyfakh, A. A., & Bershadsky, A. D. (1986). Actin cytoskeleton of spread fibroblasts appears to assemble at the cell edges. Journal of Cell Science, 82, 235–248.

    CAS  PubMed  Google Scholar 

  80. Zhao, M., Pu, J., Forrester, J. V., & McCaig, C. D. (2002). Membrane lipids, EGF receptors, and intracellular signals colocalize and are polarized in epithelial cells moving directionally in a physiological electric field. The FASEB Journal, 16, 857–859.

    CAS  PubMed  Google Scholar 

  81. Mycielska, M. E., & Djamgoz, M. B. (2004). Cellular mechanisms of direct-current electric field effects: galvanotaxis and metastatic disease. Journal of Cell Science, 117, 1631–1639.

    Article  CAS  PubMed  Google Scholar 

  82. Zhao, M., Song, B., Pu, J., Wada, T., Reid, B., Tai, G., et al. (2006). Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature, 442, 457–460.

    Article  CAS  PubMed  Google Scholar 

  83. Li, L., El-Hayek, Y. H., Liu, B., Chen, Y., Gomez, E., Wu, X., et al. (2008). Direct-current electrical field guides neuronal stem/progenitor cell migration. Stem Cells, 26, 2193–2200.

    Article  CAS  PubMed  Google Scholar 

  84. Rajnicek, A. M., Foubister, L. E., & McCaig, C. D. (2006). Growth cone steering by a physiological electric field requires dynamic microtubules, microfilaments and Rac-mediated filopodial asymmetry. Journal of Cell Science, 119, 1736–1745.

    Article  CAS  PubMed  Google Scholar 

  85. Pullar, C. E., Baier, B. S., Kariya, Y., Russell, A. J., Horst, B. A., Marinkovich, M. P., et al. (2006). beta4 integrin and epidermal growth factor coordinately regulate electric field-mediated directional migration via Rac1. Molecular Biology of the Cell, 17, 4925–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Tsai, C. H., Lin, B. J., & Chao, P. H. (2013). α2β1 integrin and RhoA mediates electric field-induced ligament fibroblast migration directionality. Journal of Orthopaedic Research, 31, 322–7.

    Article  CAS  PubMed  Google Scholar 

  87. Sato, H., Ishii, Y., Yamamoto, S., Azuma, E., Takahashi, Y., Hamashima, T., et al. (2015). PDGFR-β plays a key role in the ectopic migration of neuroblasts in cerebral stroke. Stem Cells. doi:10.1002/stem.2212.

    PubMed  Google Scholar 

  88. Nakada, M., Nambu, E., Furuyama, N., Yoshida, Y., Takino, T., Hayashi, Y., et al. (2013). Integrin α3 is overexpressed in glioma stem-like cells and promotes invasion. British Journal of Cancer, 108, 2516–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Song, B., Zhao, M., Forrester, J., & McCaig, C. D. (2004). Nerve regeneration and wound healing are stimulated and directed by an endogenous electrical field in vivo. Journal of Cell Science, 117, 4681–4690.

    Article  CAS  PubMed  Google Scholar 

  90. Mendonca, A. C., Barbieri, C. H., & Mazzer, N. (2003). Directly applied low intensity direct electric current enhances peripheral nerve regeneration in rats. Journal of Neuroscience Methods, 129, 183–90.

    Article  PubMed  Google Scholar 

  91. Al-Majed, A. A., Brushart, T. M., & Gordon, T. (2000). Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. The European Journal of Neuroscience, 12, 4381–90.

    CAS  PubMed  Google Scholar 

  92. Brushart, T. M., Hoffman, P. N., Royall, R. M., Murinson, B. B., Witzel, C., & Gordon, T. (2002). Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. The Journal of Neuroscience, 22, 6631–8.

    CAS  PubMed  Google Scholar 

  93. Huang, J., Lu, L., Zhang, J., Hu, X., Zhang, Y., Liang, W., et al. (2012). Electrical stimulation to conductive scaffold promotes axonal regeneration and remyelination in a rat model of large nerve defect. PLoS One, 7, e39526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Borgens, R. B., Roederer, E., & Cohen, M. J. (1981). Enhanced spinal cord regeneration in lamprey by applied electric fields. Science, 213, 611–617.

    Article  CAS  PubMed  Google Scholar 

  95. Borgens, R. B., Blight, A. R., & McGinnis, M. E. (1987). Behavioral recovery induced by applied electric fields after spinal cord hemisection in guinea pig. Science, 238, 366–369.

    Article  CAS  PubMed  Google Scholar 

  96. Fehlings, M. G., Tator, C. H., & Linden, R. D. (1988). The effect of direct current field on recovery from experimental spinal cord injury. Journal of Neurosurgery, 68, 781–792.

    Article  CAS  PubMed  Google Scholar 

  97. Borgens, R. B., Blight, A. R., Murphy, D. J., & Stewart, L. (1986). Transected dorsal column axons within the guinea pig spinal cord regenerate in the presence of an applied electric field. Journal of Comparative Neurology, 250, 168–180.

    Article  CAS  PubMed  Google Scholar 

  98. Shapiro, S. (2014). A review of oscillating field stimulation to treat human spinal cord injury. World Neurosurgery, 81, 830–5.

    Article  PubMed  Google Scholar 

  99. Cao, L., Wei, D., Reid, B., Zhao, S., Pu, J., Pan, T., et al. (2013). Endogenous electric currents might guide rostral migration of neuroblasts. EMBO Reports, 14, 184–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Song, B., Zhao, M., Forrester, J. V., & McCaig, C. D. (2002). Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo. Proceedings of the National Academy of Sciences of the United States of America, 99, 13577–13582.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Chiang, M., Cragoe, E. J., & Vanable, J. W. (1991). Intrinsic electric fields promote epithelisation of wounds in the newt, Notophthalmus viridescens. Developmental Biology, 146, 377–385.

    Article  CAS  PubMed  Google Scholar 

  102. Chiang, M., Robinson, K. R., & Vanable, J. W. (1992). Electric fields in the vicinity of epithelial wounds in the isolated bovine eye. Experimental Eye Research, 54, 999–1003.

    Article  CAS  PubMed  Google Scholar 

  103. Sta Iglesia, D. D., Cragoe, E. J., Jr., & Vanable, J. W., Jr. (1996). Electric field strength and epithelization in the newt (Notophthalmus viridescens). Journal of Experimental Zoology, 274, 56–62.

    Article  CAS  PubMed  Google Scholar 

  104. Zhao, M., McCaig, C. D., Agius-Fernandez, A., Forrester, J. V., & Araki-Sasaki, K. (1997). Human corneal epithelial cells reorient and migrate cathodally in a small applied electric field. Current Eye Research, 16, 973–984.

    Article  CAS  PubMed  Google Scholar 

  105. Reid, B., Song, B., McCaig, C. D., & Zhao, M. (2005). Wound healing in rat cornea: the role of electric currents. FASEB Journal, 19, 379–386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Fitch, M. T., & Silver, J. (2008). CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Experimental Neurology, 209, 294–301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Kawano, H., Kimura-Kuroda, J., Komuta, Y., Yoshioka, N., Li, H. P., Kawamura, K., et al. (2012). Role of the lesion scar in the response to damage and repair of the central nervous system. Cell and Tissue Research, 349, 169–80.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., et al. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nature Cell Biology, 9, 893–904.

    Article  CAS  PubMed  Google Scholar 

  109. Beadle, C., Assanah, M. C., Monzo, P., Vallee, R., Rosenfeld, S. S., & Canoll, P. (2008). The role of myosin II in glioma invasion of the brain. Molecular Biology of the Cell, 19, 3357–3368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Wolf, K., Müller, R., Borgmann, S., Bröcker, E. B., & Friedl, P. (2003). Amoeboid shape change and contact guidance: Tlymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood, 102, 3262–3269.

    Article  CAS  PubMed  Google Scholar 

  111. Wagenaar-Miller, R. A., Engelholm, L. H., Gavard, J., Yamada, S. S., Gutkind, J. S., Behrendt, N., et al. (2007). Complementary roles of intracellular and pericellular collagen degradation pathways in vivo. Molecular and Cellular Biology, 27, 6309–6322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Mohamed, M. M., & Sloane, B. F. (2006). Cysteine cathepsins: multifunctional enzymes in cancer. Nature Reviews Cancer, 6, 764–775.

    Article  CAS  PubMed  Google Scholar 

  113. Bradbury, E. J., Moon, L. D., Popat, R. J., King, V. R., Bennett, G. S., Patel, P. N., et al. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature, 11(416), 636–40.

    Article  Google Scholar 

  114. Hyatt, A. J., Wang, D., Kwok, J. C., Fawcett, J. W., & Martin, K. R. (2010). Controlled release of chondroitinase ABC from fibrin gel reduces the level of inhibitory glycosaminoglycan chains in lesioned spinal cord. Journal of Controlled Release, 2010(147), 24–9.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Wichita State University, Wichita, KS, 67260, USA

    Li Yao & Yongchao Li

Authors
  1. Li Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongchao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Li Yao.

Ethics declarations

Conflict of Interest

The authors indicate no potential conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yao, L., Li, Y. The Role of Direct Current Electric Field-Guided Stem Cell Migration in Neural Regeneration. Stem Cell Rev and Rep 12, 365–375 (2016). https://doi.org/10.1007/s12015-016-9654-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12015-016-9654-8

Keywords

Search

Navigation