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
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

13233

Subventions

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

Auteurs

M G Peng (MG)

Department of Ophthalmology, Keck School of Medicine, USC Roski Eye Institute, University of Southern California, Los Angeles, CA, USA.

E Iseri (E)

Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA.

A Simonyan (A)

Department of Ophthalmology, Keck School of Medicine, USC Roski Eye Institute, University of Southern California, Los Angeles, CA, USA.

P Lam (P)

Department of Ophthalmology, Keck School of Medicine, USC Roski Eye Institute, University of Southern California, Los Angeles, CA, USA.

T Kim (T)

Department of Ophthalmology, Keck School of Medicine, USC Roski Eye Institute, University of Southern California, Los Angeles, CA, USA.

S Medvidovic (S)

Department of Ophthalmology, Keck School of Medicine, USC Roski Eye Institute, University of Southern California, Los Angeles, CA, USA.

J Paknahad (J)

Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA.

M Machnoor (M)

Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA.

G Lazzi (G)

Department of Ophthalmology, Keck School of Medicine, USC Roski Eye Institute, University of Southern California, Los Angeles, CA, USA.
Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA.

K K Gokoffski (KK)

Department of Ophthalmology, Keck School of Medicine, USC Roski Eye Institute, University of Southern California, Los Angeles, CA, USA. kimberly.gokoffski@med.us.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH