Combination effects of mesenchymal stem cells transplantation and anodal transcranial direct current stimulation on a cuprizone-induced mouse model of multiple sclerosis.


Journal

Journal of molecular histology
ISSN: 1567-2387
Titre abrégé: J Mol Histol
Pays: Netherlands
ID NLM: 101193653

Informations de publication

Date de publication:
Oct 2022
Historique:
received: 27 01 2022
accepted: 20 07 2022
pubmed: 11 8 2022
medline: 14 9 2022
entrez: 10 8 2022
Statut: ppublish

Résumé

Multiple sclerosis (MS) has no absolute treatment, and researchers are still exploring to introduce promising therapy for MS. Transcranial direct current stimulation (tDCS), is a safe, non-invasive procedure for brain stimulating which can enhance working memory, cognitive neurohabitation and motor recovery. Here, we evaluated the effects of tDCS treatment and Mesenchymal stem cells (MSCs) transplantation on remyelination ability of a Cuprizone (CPZ)-induced demyelination mouse model. tDCS significantly increased the motor coordination and balance abilities in CPZ + tDCS and CPZ + tDCS + MSCs mice in comparison to the CPZ mice. Luxol fast blue (LFB) staining showed that tDCS and MSCs transplantation could increase remyelination capacity in CPZ + tDCS and CPZ + MSCs mice compared to the CPZ mice. But, the effect of tDCS with MSCs transplantation on remyelination process was larger than each of treatment alone. Immunofluorescence technique indicated that the numbers of Olig2

Identifiants

pubmed: 35947228
doi: 10.1007/s10735-022-10092-8
pii: 10.1007/s10735-022-10092-8
doi:

Substances chimiques

Cuprizone 5N16U7E0AO

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

817-831

Subventions

Organisme : Baqyiatallah University of Medical Sciences
ID : Grant No. 98000512

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Ahn SM, Jung DH, Lee HJ, Pak ME, Jung YJ, Shin Y-I, Shin HK, Choi BT (2020) Contralesional application of transcranial direct current stimulation on functional improvement in ischemic stroke mice. Stroke 51:2208–2218
pubmed: 32521221
Baba T, Kameda M, Yasuhara T, Morimoto T, Kondo A, Shingo T, Tajiri N, Wang F, Miyoshi Y, Borlongan CV (2009) Electrical stimulation of the cerebral cortex exerts antiapoptotic, angiogenic, and anti-inflammatory effects in ischemic stroke rats through phosphoinositide 3-kinase/Akt signaling pathway. Stroke 40:e598–e605
pubmed: 19762690
Barati S, Kashani IR, Tahmasebi F, Mehrabi S, Joghataei MT (2019) Effect of mesenchymal stem cells on glial cells population in cuprizone induced demyelination model. Neuropeptides 75:75–84
pubmed: 31030907
Barati S, Tahmasebi F, Faghihi F (2020) Effects of mesenchymal stem cells transplantation on multiple sclerosis patients. Neuropeptides 8:102095
Bornheim S, Croisier J-L, Maquet P, Kaux J-F (2020) Transcranial direct current stimulation associated with physical-therapy in acute stroke patients-A randomized, triple blind, sham-controlled study. Brain Stimul 13:329–336
pubmed: 31735645
Bourdillon P, Hermann B, Sitt JD, Naccache L (2019) Electromagnetic brain stimulation in patients with disorders of consciousness. Front Neurosci 13:223
pubmed: 30936822 pmcid: 6432925
Braun R, Klein R, Walter HL, Ohren M, Freudenmacher L, Getachew K, Ladwig A, Luelling J, Neumaier B, Endepols H (2016) Transcranial direct current stimulation accelerates recovery of function, induces neurogenesis and recruits oligodendrocyte precursors in a rat model of stroke. Exp Neurol 279:127–136
pubmed: 26923911
Cruz-Martinez P, González-Granero S, Molina-Navarro MM, Pacheco-Torres J, Garcia-Verdugo JM, Geijo-Barrientos E, Jones J, Martinez S (2016) Intraventricular injections of mesenchymal stem cells activate endogenous functional remyelination in a chronic demyelinating murine model. Cell Death Dis 7:e2223–e2223
pubmed: 27171265 pmcid: 4917663
Cullen CL, Young KM (2016) How does transcranial magnetic stimulation influence glial cells in the central nervous system? Front Neural Circuits 10:26
pubmed: 27092058 pmcid: 4820444
Dewar D, Underhill SM, Goldberg MP (2003) Oligodendrocytes and ischemic brain injury. J Cereb Blood Flow Metab 23:263–274
pubmed: 12621301
Ferrucci R, Vergari M, Cogiamanian F, Bocci T, Ciocca M, Tomasini E, De Riz M, Scarpini E, Priori A (2014) Transcranial direct current stimulation (tDCS) for fatigue in multiple sclerosis. NeuroRehabilitation 34:121–127
pubmed: 24284464
Fregni F, Boggio PS, Santos MC, Lima M, Vieira AL, Rigonatti SP, Silva MTA, Barbosa ER, Nitsche MA, Pascual-Leone A (2006) Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov Disord 21:1693–1702
pubmed: 16817194
Gholami M, Nami M, Shamsi F, Jaberi KR, Kateb B, Jaberi AR (2021) Effects of transcranial direct current stimulation on cognitive dysfunction in multiple sclerosis. Neurophysiol Clin 51(4):319–328
pubmed: 34088588
Greenberg ME, Xu B, Lu B, Hempstead BL (2009) New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 29:12764–12767
pubmed: 19828787 pmcid: 3091387
Gutiérrez-Fernández M, Rodríguez-Frutos B, Ramos-Cejudo J, Otero-Ortega L, Fuentes B, Vallejo-Cremades MT, Sanz-Cuesta BE, Díez-Tejedor E (2015) Comparison between xenogeneic and allogeneic adipose mesenchymal stem cells in the treatment of acute cerebral infarct: proof of concept in rats. J Transl Med 13:1–10
Hsu W-Y, Cheng C-H, Zanto TP, Gazzaley A, Bove RM (2021) Effects of transcranial direct current stimulation on cognition, mood, pain, and fatigue in multiple sclerosis: a systematic review and meta-analysis. Front Neurol 12:276
Huang Y, Li Y, Chen J, Zhou H, Tan S (2015) Electrical stimulation elicits neural stem cells activation: new perspectives in CNS repair. Front Hum Neurosci 9:586
pubmed: 26539102 pmcid: 4610200
Kashani IR, Chavoshi H, Pasbakhsh P, Hassani M, Omidi A, Mahmoudi R, Beyer C, Zendedel A (2017) Protective effects of erythropoietin against cuprizone-induced oxidative stress and demyelination in the mouse corpus callosum. Iran J Basic Med Sci 20:886
pubmed: 29085580 pmcid: 5651474
Keuters MH, Aswendt M, Tennstaedt A, Wiedermann D, Pikhovych A, Rotthues S, Fink GR, Schroeter M, Hoehn M, Rueger MA (2015) Transcranial direct current stimulation promotes the mobility of engrafted NSCs in the rat brain. NMR Biomed 28:231–239
pubmed: 25521600
Kidgell DJ, Daly RM, Young K, Lum J, Tooley G, Jaberzadeh S, Zoghi M, Pearce AJ (2013) Different current intensities of anodal transcranial direct current stimulation do not differentially modulate motor cortex plasticity. Neural plast 1:9
Li DC, Li Q (2017) Electrical stimulation of cortical neurons promotes oligodendrocyte development and remyelination in the injured spinal cord. Neural Regen Res 12:1613
pubmed: 29171422 pmcid: 5696838
Liu A, Vöröslakos M, Kronberg G, Henin S, Krause MR, Huang Y, Opitz A, Mehta A, Pack CC, Krekelberg B (2018) Immediate neurophysiological effects of transcranial electrical stimulation. Nat Commun 9:1–12
Ma X, Cheng O, Jiang Q, Yang J, Xiao H, Qiu H (2021) Activation of ephrinb1/EPHB2/MAP-2/NMDAR mediates hippocampal neurogenesis promoted by transcranial direct current stimulation in cerebral-ischemic mice. NeuroMol Med 23(4):521–530
Maas DA, Angulo MC (2021) Can enhancing neuronal activity improve myelin repair in multiple sclerosis? Front Cell Neurosci 15:38
Madadi S, Pasbakhsh P, Tahmasebi F, Mortezaee K, Khanehzad M, Boroujeni FB, Noorzehi G, Kashani IR (2019) Astrocyte ablation induced by La-aminoadipate (L-AAA) potentiates remyelination in a cuprizone demyelinating mouse model. Metab Brain Dis 34:593–603
pubmed: 30652255
Madhavan S, Shah B (2012) Enhancing motor skill learning with transcranial direct current stimulation–a concise review with applications to stroke. Front Psych 3:66
Mercurio S, Serra L, Nicolis SK (2019) More than just stem cells: functional roles of the transcription factor Sox2 in differentiated glia and neurons. Int J Mol Sci 20:4540
pmcid: 6769708
Miniussi C, Cappa SF, Cohen LG, Floel A, Fregni F, Nitsche MA, Oliveri M, Pascual-Leone A, Paulus W, Priori A (2008) Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation. Brain Stimul 1:326–336
pubmed: 20633391
Mirzaie J, Raoofi A, Jamalpoor Z, Nezhadi A, Golmohammadi R (2020) Protective impacts of erythropoietin on myelinization of oligodendrocytes and schwann cells in CNS and PNS following cuprizone-induced multiple sclerosis-histology, molecular, and functional studies. J Chem Neuroanat 104:101750
pubmed: 31954768
Mojaverrostami S, Pasbakhsh P, Madadi S, Nekoonam S, Zarini D, Noori L, Shiri E, Salama M, Zibara K, Kashani IR (2020) Calorie restriction promotes remyelination in a cuprizone-Induced demyelination mouse model of multiple sclerosis. Metab Brain Dis 35:1211–1224
pubmed: 32638202
Monai H, Hirase H (2018) Astrocytes as a target of transcranial direct current stimulation (tDCS) to treat depression. Neurosci Res 126:15–21
pubmed: 29079367
Monai H, Ohkura M, Tanaka M, Oe Y, Konno A, Hirai H, Mikoshiba K, Itohara S, Nakai J, Iwai Y (2016) Calcium imaging reveals glial involvement in transcranial direct current stimulation-induced plasticity in mouse brain. Nat Commun 7:1–10
Mosayebi-Samani M, Melo L, Agboada D, Nitsche MA, Kuo M-F (2020) Ca
pubmed: 32768154
Nitsche MA, Boggio PS, Fregni F, Pascual-Leone A (2009) Treatment of depression with transcranial direct current stimulation (tDCS): a review. Exp Neurol 219:14–19
pubmed: 19348793
Ortiz FC, Habermacher C, Graciarena M, Houry P-Y, Nishiyama A, Oumesmar BN, Angulo MC (2019) Neuronal activity in vivo enhances functional myelin repair. JCI Insight 4:9
Pelegri NG, Gorrie CA, Santos J (2019) Rat hippocampal neural stem cell modulation using PDGF, VEGF, PDGF/VEGF, and BDNF. Stem Cells Int. https://doi.org/10.1155/2019/4978917
doi: 10.1155/2019/4978917 pubmed: 31011333 pmcid: 6442450
Pourabdolhossein F, Hamidabadi HG, Bojnordi MN, Rostam SM (2017) Stem cell therapy: a promising therapeutic approach for multiple sclerosis. Multiple sclerosis: perspectives in treatment and pathogenesis. Exon Publications, Brisbane, pp 85–108
Rueger MA, Keuters MH, Walberer M, Braun R, Klein R, Sparing R, Fink GR, Graf R, Schroeter M (2012) Multi-session transcranial direct current stimulation (tDCS) elicits inflammatory and regenerative processes in the rat brain. PLoS ONE 7(8):e43776
pubmed: 22928032 pmcid: 3425495
Samaddar S, Vazquez K, Ponkia D, Toruno P, Sahbani K, Begum S, Abouelela A, Mekhael W, Ahmed Z (2017) Transspinal direct current stimulation modulates migration and proliferation of adult newly born spinal cells in mice. J Appl Physiol 122:339–353
pubmed: 27932680
Sherafat MA, Heibatollahi M, Mongabadi S, Moradi F, Javan M, Ahmadiani A (2012) Electromagnetic field stimulation potentiates endogenous myelin repair by recruiting subventricular neural stem cells in an experimental model of white matter demyelination. J Mol Neurosci 48:144–153
pubmed: 22588976
Sivandzade F, Cucullo L (2021) Regenerative stem cell therapy for neurodegenerative diseases: an overview. Int J Mol Sci 22:2153
pubmed: 33671500 pmcid: 7926761
Spaas J, Van Veggel L, Schepers M, Tiane A, Van Horssen J, Wilson DM, Moya PR, Piccart E, Hellings N, Eijnde BO (2021) Oxidative stress and impaired oligodendrocyte precursor cell differentiation in neurological disorders. Cell Mol Life Sci 78(10):4615–4637
pubmed: 33751149 pmcid: 8195802
Sullivan GM, Knutsen AK, Peruzzotti-Jametti L, Korotcov A, Bosomtwi A, Dardzinski BJ, Bernstock JD, Rizzi S, Edenhofer F, Pluchino S (2020) Transplantation of induced neural stem cells (iNSCs) into chronically demyelinated corpus callosum ameliorates motor deficits. Acta Neuropathol Commun 8:1–23
Tahmasebi F, Pasbakhsh P, Barati S, Madadi S, Kashani IR (2021) The effect of microglial ablation and mesenchymal stem cell transplantation on a cuprizone-induced demyelination model. J Cell Physiol 236:3552–3564
pubmed: 32996165
Tehovnik E, Tolias A, Sultan F, Slocum W, Logothetis N (2006) Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol 96:512–521
pubmed: 16835359
Ulam F, Shelton C, Richards L, Davis L, Hunter B, Fregni F, Higgins K (2015) Cumulative effects of transcranial direct current stimulation on EEG oscillations and attention/working memory during subacute neurorehabilitation of traumatic brain injury. Clin Neurophysiol 126:486–496
pubmed: 24947595
Wachter D, Wrede A, Schulz-Schaeffer W, Taghizadeh-Waghefi A, Nitsche MA, Kutschenko A, Rohde V, Liebetanz D (2011) Transcranial direct current stimulation induces polarity-specific changes of cortical blood perfusion in the rat. Exp Neurol 227:322–327
pubmed: 21147105
Winkler C, Reis J, Hoffmann N, Gellner A-K, Münkel C, Curado MR, Furlanetti L, Garcia J, Döbrössy MD, Fritsch B (2017) Anodal transcranial direct current stimulation enhances survival and integration of dopaminergic cell transplants in a rat Parkinson model. Eneuro. https://doi.org/10.1523/ENEURO.0063-17.2017
doi: 10.1523/ENEURO.0063-17.2017 pubmed: 28966974 pmcid: 5617080
Xia Y, Khalid W, Yin Z, Huang G, Bikson M, Fu BM (2020) Modulation of solute diffusivity in brain tissue as a novel mechanism of transcranial direct current stimulation (tDCS). Sci Rep 10:1–12
Xiu Y, Cheng GH, Peng C, Wang Y, Li YD, Chao FL, Tang Y (2017) Ultrastructural abnormalities and loss of myelinated fibers in the corpus callosum of demyelinated mice induced by cuprizone. J Neurosci Res 95:1677–1689
pubmed: 27935632
Zaninotto AL, El-Hagrassy MM, Green JR, Babo M, Paglioni VM, Benute GG, Paiva WS (2019) Transcranial direct current stimulation (tDCS) effects on traumatic brain injury (TBI) recovery: a systematic review. Dement Neuropsychol 13:172–179
pubmed: 31285791 pmcid: 6601308
Zarini D, Pasbakhsh P, Nekoonam S, Mojaverrostami S, Ghasemi S, Shabani M, Kashani IR (2021) Protective features of calorie restriction on cuprizone-induced demyelination via modulating microglial phenotype. J Chem Neuroanat 116:102013
pubmed: 34391881
Zendedel A, Beyer C, Kipp M (2013) Cuprizone-induced demyelination as a tool to study remyelination and axonal protection. J Mol Neurosci 51:567–572
pubmed: 23666824
Zhang RL, Zhang ZG, Chopp M (2008) Ischemic stroke and neurogenesis in the subventricular zone. Neuropharmacology 55:345–352
pubmed: 18632119 pmcid: 2562038
Zhang C, Zhang G, Rong W, Wang A, Wu C, Huo X (2014) Oscillating field stimulation promotes spinal cord remyelination by inducing differentiation of oligodendrocyte precursor cells after spinal cord injury. Bio-Med Mater Eng 24:3629–3636
Zhang K-Y, Rui G, Zhang J-P, Guo L, An G-Z, Lin J-J, He W, Ding G-R (2020a) Cathodal tDCS exerts neuroprotective effect in rat brain after acute ischemic stroke. BMC Neurosci 21:1–13
Zhang K, Guo L, Zhang J, Rui G, An G, Zhou Y, Lin J, Xing J, Zhao T, Ding G (2020b) tDCS accelerates the rehabilitation of MCAO-induced motor function deficits via neurogenesis modulated by the Notch1 signaling pathway. Neurorehabil Neural Repair 34:640–651
pubmed: 32543269
Zilkha-Falb R, Kaushansky N, Kawakami N, Ben-Nun A (2016) Post-CNS-inflammation expression of CXCL12 promotes the endogenous myelin/neuronal repair capacity following spontaneous recovery from multiple sclerosis-like disease. J Neuroinflammation 13:1–19

Auteurs

Sina Mojaverrostami (S)

Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran.
Department of Anatomy, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran.

Farnaz Khadivi (F)

Department of Anatomy, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran.

Davood Zarini (D)

Department of Anatomy, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran.

Alireza Mohammadi (A)

Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran. ar.mohammadi@bmsu.ac.ir.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH