Asymmetric charge balanced waveforms direct retinal ganglion cell axon growth.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 08 2023
14 08 2023
Historique:
received:
13
02
2023
accepted:
04
08
2023
medline:
16
8
2023
pubmed:
15
8
2023
entrez:
14
8
2023
Statut:
epublish
Résumé
Failure to direct axon regeneration to appropriate targets is a major barrier to restoring function after nerve injury. Development of strategies that can direct targeted regeneration of neurons such as retinal ganglion cells (RGCs) are needed to delay or reverse blindness in diseases like glaucoma. Here, we demonstrate that a new class of asymmetric, charge balanced (ACB) waveforms are effective at directing RGC axon growth, in vitro, without compromising cell viability. Unlike previously proposed direct current (DC) stimulation approaches, charge neutrality of ACB waveforms ensures the safety of stimulation while asymmetry ensures its efficacy. Furthermore, we demonstrate the relative influence of pulse amplitude and pulse width on the overall effectiveness of stimulation. This work can serve as a practical guideline for the potential deployment of electrical stimulation as a treatment strategy for nerve injury.
Identifiants
pubmed: 37580344
doi: 10.1038/s41598-023-40097-6
pii: 10.1038/s41598-023-40097-6
pmc: PMC10425404
doi:
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
13233Subventions
Organisme : NEI NIH HHS
ID : K08 EY031797
Pays : United States
Organisme : NEI NIH HHS
ID : P30 EY029220
Pays : United States
Informations de copyright
© 2023. Springer Nature Limited.
Références
Sharf, T., Kalakuntala, T. & Gokoffski, K. K. Electrical devices for visual restoration. Surv. Ophthalmol. 67, 793–800. https://doi.org/10.1016/j.survophthal.2021.08.008 (2022).
doi: 10.1016/j.survophthal.2021.08.008
pubmed: 34487742
Ingvar, S. Reaction of cells to the galvanic current in tissue cultures. Exp. Biol. Med. 17, 198–199 (1920).
doi: 10.3181/00379727-17-105
Yamashita, M. Electric axon guidance in embryonic retina: Galvanotropism revisited. Biochem. Biophys. Res. Commun. 431, 280–283. https://doi.org/10.1016/j.bbrc.2012.12.115 (2013).
doi: 10.1016/j.bbrc.2012.12.115
pubmed: 23291175
McCaig, C. D., Rajnicek, A. M., Song, B. & Zhao, M. Controlling cell behavior electrically: Current views and future potential. Physiol. Rev. 85, 943–978. https://doi.org/10.1152/physrev.00020.2004 (2005).
doi: 10.1152/physrev.00020.2004
pubmed: 15987799
Morimoto, T. et al. Transcorneal electrical stimulation rescues axotomized retinal ganglion cells by activating endogenous retinal IGF-1 system. Invest. Ophthalmol. Vis. Sci. 46, 2147–2155. https://doi.org/10.1167/iovs.04-1339 (2005).
doi: 10.1167/iovs.04-1339
pubmed: 15914636
Goldberg, J. L. et al. Retinal ganglion cells do not extend axons by default: Promotion by neurotrophic signaling and electrical activity. Neuron 33, 689–702 (2002).
doi: 10.1016/S0896-6273(02)00602-5
pubmed: 11879647
Gokoffski, K. K., Jia, X., Shvarts, D., Xia, G. & Zhao, M. Physiologic electrical fields direct retinal ganglion cell axon growth in vitro. Invest. Ophthalmol. Vis. Sci. 60, 3659–3668. https://doi.org/10.1167/iovs.18-25118 (2019).
doi: 10.1167/iovs.18-25118
pubmed: 31469406
pmcid: 6716951
Merrill, D. R., Bikson, M. & Jefferys, J. G. Electrical stimulation of excitable tissue: Design of efficacious and safe protocols. J. Neurosci. Methods 141, 171–198. https://doi.org/10.1016/j.jneumeth.2004.10.020 (2005).
doi: 10.1016/j.jneumeth.2004.10.020
pubmed: 15661300
Gall, C. et al. Alternating current stimulation for vision restoration after optic nerve damage: A randomized clinical trial. PLoS ONE 11, e0156134. https://doi.org/10.1371/journal.pone.0156134 (2005).
doi: 10.1371/journal.pone.0156134
Kloth, L. C. Electrical stimulation for wound healing: A review of evidence from in vitro studies, animal experiments, and clinical trials. Int. J. Low Extrem. Wounds 4, 23–44. https://doi.org/10.1177/1534734605275733 (2005).
doi: 10.1177/1534734605275733
pubmed: 15860450
Percie du Sert, N. et al. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. BMJ Open Sci. 4, e100115. https://doi.org/10.1177/1534734605275733 (2020).
doi: 10.1177/1534734605275733
pubmed: 34095516
pmcid: 7610906
Huang, X., Wu, D. Y., Chen, G., Manji, H. & Chen, D. F. Support of retinal ganglion cell survival and axon regeneration by lithium through a Bcl-2-dependent mechanism. Invest. Ophthalmol. Vis. Sci. 44, 347–354 (2003).
doi: 10.1167/iovs.02-0198
pubmed: 12506095
Gao, F. et al. Comparative analysis of three purification protocols for retinal ganglion cells from rat. Mol. Vis. 22, 387–400 (2016).
pubmed: 27122968
pmcid: 4844924
Rajnicek, A. M., Foubister, L. E. & McCaig, C. D. 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. https://doi.org/10.1242/jcs.02896 (2006).
doi: 10.1242/jcs.02896
pubmed: 16595546
Feng, J. F. et al. Electrical guidance of human stem cells in the rat brain. Stem Cell Rep. 9, 177–189. https://doi.org/10.1016/j.stemcr.2017.05.035 (2017).
doi: 10.1016/j.stemcr.2017.05.035
Hadjinicolaou, A. E. et al. Optimizing the electrical stimulation of retinal ganglion cells. IEEE Trans. Neural Syst. Rehabil. Eng. 23, 169–178. https://doi.org/10.1109/TNSRE.2014.2361900 (2015).
doi: 10.1109/TNSRE.2014.2361900
pubmed: 25343761
Babona-Pilipos, R., Droujinine, I. A., Popovic, M. R. & Morshead, C. M. Adult subependymal neural precursors, but not differentiated cells, undergo rapid cathodal migration in the presence of direct current electric fields. PLoS ONE 6, e23808. https://doi.org/10.1371/journal.pone.0023808 (2011).
doi: 10.1371/journal.pone.0023808
pubmed: 21909360
pmcid: 3166127
Babona-Pilipos, R., Pritchard-Oh, A., Popovic, M. R. & Morshead, C. M. Biphasic monopolar electrical stimulation induces rapid and directed galvanotaxis in adult subependymal neural precursors. Stem Cell Res. Ther. 6, 67. https://doi.org/10.1186/s13287-015-0049-6 (2015).
doi: 10.1186/s13287-015-0049-6
pubmed: 25888848
pmcid: 4413998
Wang, E., Zhao, M., Forrester, J. V. & MCCaig, C. D. Re-orientation and faster, directed migration of lens epithelial cells in a physiological electric field. Exp. Eye Res. 71, 91–98. https://doi.org/10.1006/exer.2000.0858 (2000).
doi: 10.1006/exer.2000.0858
pubmed: 10880279