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Published in: Metabolic Brain Disease 1/2018

01-02-2018 | Original Article

Alpha-lipoic acid mitigates toxic-induced demyelination in the corpus callosum by lessening of oxidative stress and stimulation of polydendrocytes proliferation

Authors: Nima Sanadgol, Fereshteh Golab, Hassan Askari, Fatemeh Moradi, Marziyeh Ajdary, Mehdi Mehdizadeh

Published in: Metabolic Brain Disease | Issue 1/2018

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Abstract

Multiple Sclerosis (MS), is a disease that degenerates myelin in central nervous system (CNS). Reactive oxygen species (ROSs) are toxic metabolites, and accumulating data indicate that ROSs-mediated apoptosis of oligodendrocytes (OLGs) plays a major role in the pathogenesis of MS under oxidative stress conditions. In this study, we investigated the role of endogenous antioxidant alpha-lipoic acid (ALA) as ROSs scavenger in the OLGs loss and myelin degeneration during cuprizone (cup)-induced demyelination in the experimental model of MS. Our results have shown that ALA treatment significantly increased population of mature OLGs (MOG+ cells), as well as decreased oxidative stress (ROSs, COX-2 and PGE2) and apoptosis mediators (caspase-3 and Bax/Bcl2 ratio) in corpus callosum (CC). Surprisingly, ALA significantly stimulates population of NG2 chondroitin sulfate proteoglycan positive glia (NG2+ cells or polydendrocytes), from week 4 afterward. Accordingly ALA could prevents apoptosis, delays demyelination and recruits OLGs survival and regeneration mechanisms in CC. We conclude that ALA has protective effects against toxic demyelination via reduction of redox signaling, and alleviation of polydendrocytes vulnerability to excitotoxic challenge.
Literature
go back to reference Albrecht S, Hagemeier K, Ehrlich M, Kemming C, Trotter J, Kuhlmann T (2016) Recovery from Toxic-Induced Demyelination Does Not Require the NG2 Proteoglycan. PLoS One 11(10):e0163841CrossRefPubMedPubMedCentral Albrecht S, Hagemeier K, Ehrlich M, Kemming C, Trotter J, Kuhlmann T (2016) Recovery from Toxic-Induced Demyelination Does Not Require the NG2 Proteoglycan. PLoS One 11(10):e0163841CrossRefPubMedPubMedCentral
go back to reference Ahmed MA, El-Awdan SA (2015) Lipoic acid and pentoxifylline mitigate nandrolone decanoate-induced neurobehavioral perturbations in rats via re-balance of brain neurotransmitters, up-regulation of Nrf2/HO-1 pathway, and down-regulation of TNFR1 expression. Horm Behav 73:186–199CrossRefPubMed Ahmed MA, El-Awdan SA (2015) Lipoic acid and pentoxifylline mitigate nandrolone decanoate-induced neurobehavioral perturbations in rats via re-balance of brain neurotransmitters, up-regulation of Nrf2/HO-1 pathway, and down-regulation of TNFR1 expression. Horm Behav 73:186–199CrossRefPubMed
go back to reference Baarine M, Andreoletti P, Athias A, Nury T, Zarrouk A, Ragot K et al (2012) Evidence of oxidative stress in very long chain fatty acid–treated oligodendrocytes and potentialization of ROS production using RNA interference-directed knockdown of ABCD1 and ACOX1 peroxisomal proteins. Neuroscience 213:1–18CrossRefPubMed Baarine M, Andreoletti P, Athias A, Nury T, Zarrouk A, Ragot K et al (2012) Evidence of oxidative stress in very long chain fatty acid–treated oligodendrocytes and potentialization of ROS production using RNA interference-directed knockdown of ABCD1 and ACOX1 peroxisomal proteins. Neuroscience 213:1–18CrossRefPubMed
go back to reference Burg MA, Nishiyama A, Stallcup WB (1997) A central segment of the NG2 proteoglycan is critical for the ability of glioma cells to bind and migrate toward type VI collagen. Exp Cell Res 235(1):254–264CrossRefPubMed Burg MA, Nishiyama A, Stallcup WB (1997) A central segment of the NG2 proteoglycan is critical for the ability of glioma cells to bind and migrate toward type VI collagen. Exp Cell Res 235(1):254–264CrossRefPubMed
go back to reference Chaudhary P, Marracci G, Galipeau D, Pocius E, Morris B, Bourdette D (2015a) Lipoic acid reduces inflammation in a mouse focal cortical experimental autoimmune encephalomyelitis model. J Neuroimmunol 289:68–74CrossRefPubMedPubMedCentral Chaudhary P, Marracci G, Galipeau D, Pocius E, Morris B, Bourdette D (2015a) Lipoic acid reduces inflammation in a mouse focal cortical experimental autoimmune encephalomyelitis model. J Neuroimmunol 289:68–74CrossRefPubMedPubMedCentral
go back to reference Chaudhary P, Marracci G, Galipeau D, Pocius E, Morris B, Bourdette D (2015b) Lipoic acid reduces inflammation in a mouse focal cortical experimental autoimmune encephalomyelitis model. J Neuroimmunol 289:68–74CrossRefPubMedPubMedCentral Chaudhary P, Marracci G, Galipeau D, Pocius E, Morris B, Bourdette D (2015b) Lipoic acid reduces inflammation in a mouse focal cortical experimental autoimmune encephalomyelitis model. J Neuroimmunol 289:68–74CrossRefPubMedPubMedCentral
go back to reference Chekenya M, Rooprai H, Davies D, Levine J, Butt A, Pilkington G (1999) The NG2 chondoitin sulfate proteoglycan: role in malignant progression of human brain tumours. Int J Dev Neurosci 17(5):421–435CrossRefPubMed Chekenya M, Rooprai H, Davies D, Levine J, Butt A, Pilkington G (1999) The NG2 chondoitin sulfate proteoglycan: role in malignant progression of human brain tumours. Int J Dev Neurosci 17(5):421–435CrossRefPubMed
go back to reference Choi KH, Park MS, Kim HS, Kim KT, Kim HS, Kim JT et al (2015) Alpha-lipoic acid treatment is neurorestorative and promotes functional recovery after stroke in rats. Mol Brain 11(8):9CrossRef Choi KH, Park MS, Kim HS, Kim KT, Kim HS, Kim JT et al (2015) Alpha-lipoic acid treatment is neurorestorative and promotes functional recovery after stroke in rats. Mol Brain 11(8):9CrossRef
go back to reference Deng H, Zuo X, Zhang J, Liu X, Liu L, Xu Q, Wu Z, Ji A (2015) Α-lipoic acid protects against cerebral ischemia/reperfusion-induced injury in rats. Mol Med Rep 11(5):3659–3665CrossRefPubMed Deng H, Zuo X, Zhang J, Liu X, Liu L, Xu Q, Wu Z, Ji A (2015) Α-lipoic acid protects against cerebral ischemia/reperfusion-induced injury in rats. Mol Med Rep 11(5):3659–3665CrossRefPubMed
go back to reference Dong, Y., Wang, H., & Chen, Z. (2015). Alpha-lipoic acid attenuates cerebral ischemia and reperfusion injury via insulin receptor and PI3K/Akt-dependent inhibition of NADPH oxidase. International journal of endocrinology, 2015 Dong, Y., Wang, H., & Chen, Z. (2015). Alpha-lipoic acid attenuates cerebral ischemia and reperfusion injury via insulin receptor and PI3K/Akt-dependent inhibition of NADPH oxidase. International journal of endocrinology, 2015
go back to reference Font-Nieves M, Sans-Fons MG, Gorina R, Bonfill-Teixidor E, Salas-Pérdomo A, Márquez-Kisinousky L, Santalucia T, Planas AM (2012) Induction of COX-2 enzyme and down-regulation of COX-1 expression by lipopolysaccharide (LPS) control prostaglandin E2 production in astrocytes. J Biol Chem 287(9):6454–6468CrossRefPubMedPubMedCentral Font-Nieves M, Sans-Fons MG, Gorina R, Bonfill-Teixidor E, Salas-Pérdomo A, Márquez-Kisinousky L, Santalucia T, Planas AM (2012) Induction of COX-2 enzyme and down-regulation of COX-1 expression by lipopolysaccharide (LPS) control prostaglandin E2 production in astrocytes. J Biol Chem 287(9):6454–6468CrossRefPubMedPubMedCentral
go back to reference Gilgun-Sherki Y, Melamed E, Offen D (2004) The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J Neurol 251(3):261–268CrossRefPubMed Gilgun-Sherki Y, Melamed E, Offen D (2004) The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J Neurol 251(3):261–268CrossRefPubMed
go back to reference Goldberg J, Clarner T, Beyer C, Kipp M (2015) Anatomical distribution of cuprizone-induced lesions in C57BL6 mice. J Mol Neurosci 57(2):166–175CrossRefPubMed Goldberg J, Clarner T, Beyer C, Kipp M (2015) Anatomical distribution of cuprizone-induced lesions in C57BL6 mice. J Mol Neurosci 57(2):166–175CrossRefPubMed
go back to reference Hatanaka Y, Yan Z, Torigoe M, Yoshiaki K, Murakami F (2016) From migration to settlement: the pathways, migration modes and dynamics of neurons in the developing brain. Proc Japan Acad Ser B, Phys Biol Sci 92(1):1CrossRef Hatanaka Y, Yan Z, Torigoe M, Yoshiaki K, Murakami F (2016) From migration to settlement: the pathways, migration modes and dynamics of neurons in the developing brain. Proc Japan Acad Ser B, Phys Biol Sci 92(1):1CrossRef
go back to reference Huang YP, Jin HY, Yu HP (2017) Inhibitory effects of alpha-lipoic acid on oxidative stress in the rostral ventrolateral medulla in rats with salt-induced hypertension. Int J Mol Med 39(2):430–436CrossRefPubMed Huang YP, Jin HY, Yu HP (2017) Inhibitory effects of alpha-lipoic acid on oxidative stress in the rostral ventrolateral medulla in rats with salt-induced hypertension. Int J Mol Med 39(2):430–436CrossRefPubMed
go back to reference Hohlfeld R, Dornmair K, Meinl E, Wekerle H (2016) The search for the target antigens of multiple sclerosis, part 1: autoreactive CD4+ T lymphocytes as pathogenic effectors and therapeutic targets. Lancet Neurol 15(2):198–209CrossRefPubMed Hohlfeld R, Dornmair K, Meinl E, Wekerle H (2016) The search for the target antigens of multiple sclerosis, part 1: autoreactive CD4+ T lymphocytes as pathogenic effectors and therapeutic targets. Lancet Neurol 15(2):198–209CrossRefPubMed
go back to reference Jang Y-S, Lee M-H, Lee S-H, Bae K (2011) Cu/Zn superoxide dismutase is differentially regulated in period gene-mutant mice. Biochem Biophys Res Commun 409(1):22–27CrossRefPubMed Jang Y-S, Lee M-H, Lee S-H, Bae K (2011) Cu/Zn superoxide dismutase is differentially regulated in period gene-mutant mice. Biochem Biophys Res Commun 409(1):22–27CrossRefPubMed
go back to reference Khani M, Amani D, Taheripanah R, Sanadgol N, Feizollahzadeh S, Rahmani Z (2015) Transforming growth factor beta-1 (TGF-β1) gene single nucleotide polymorphisms (SNPs) and susceptibility to pre-eclampsia in Iranian women: A case–control study. Pregnan Hyperten: Int J Women's Cardiovasc Health 5(4):267–272CrossRef Khani M, Amani D, Taheripanah R, Sanadgol N, Feizollahzadeh S, Rahmani Z (2015) Transforming growth factor beta-1 (TGF-β1) gene single nucleotide polymorphisms (SNPs) and susceptibility to pre-eclampsia in Iranian women: A case–control study. Pregnan Hyperten: Int J Women's Cardiovasc Health 5(4):267–272CrossRef
go back to reference Kucharova K, Stallcup WB (2010) The NG2 proteoglycan promotes oligodendrocyte progenitor proliferation and developmental myelination. Neuroscience 166(1):185–194CrossRefPubMed Kucharova K, Stallcup WB (2010) The NG2 proteoglycan promotes oligodendrocyte progenitor proliferation and developmental myelination. Neuroscience 166(1):185–194CrossRefPubMed
go back to reference Makagiansar IT, Williams S, Mustelin T, Stallcup WB (2007) Differential phosphorylation of NG2 proteoglycan by ERK and PKCα helps balance cell proliferation and migration. J Cell Biol 178(1):155–165CrossRefPubMedPubMedCentral Makagiansar IT, Williams S, Mustelin T, Stallcup WB (2007) Differential phosphorylation of NG2 proteoglycan by ERK and PKCα helps balance cell proliferation and migration. J Cell Biol 178(1):155–165CrossRefPubMedPubMedCentral
go back to reference Ma R, Wang X, Peng P, Xiong J, Dong H, Wang L, Ding Z (2016) Alpha-lipoic acid inhibits sevoflurane-induced neuronal apoptosis through PI3K/Akt signalling pathway. Cell Biochem Funct 34(1):42–47CrossRefPubMed Ma R, Wang X, Peng P, Xiong J, Dong H, Wang L, Ding Z (2016) Alpha-lipoic acid inhibits sevoflurane-induced neuronal apoptosis through PI3K/Akt signalling pathway. Cell Biochem Funct 34(1):42–47CrossRefPubMed
go back to reference Ming X, Li W, Maeda Y, Blumberg B, Raval S, Cook SD, Dowling PC (2002) Caspase-1 expression in multiple sclerosis plaques and cultured glial cells. J Neurol Sci 197(1):9–18CrossRefPubMed Ming X, Li W, Maeda Y, Blumberg B, Raval S, Cook SD, Dowling PC (2002) Caspase-1 expression in multiple sclerosis plaques and cultured glial cells. J Neurol Sci 197(1):9–18CrossRefPubMed
go back to reference Mirshafiey A, Mohsenzadegan M (2009a) Antioxidant therapy in multiple sclerosis. Immunopharmacol Immunotoxicol 31(1):13–29CrossRefPubMed Mirshafiey A, Mohsenzadegan M (2009a) Antioxidant therapy in multiple sclerosis. Immunopharmacol Immunotoxicol 31(1):13–29CrossRefPubMed
go back to reference Ortiz, G. G., Pacheco-Moisés, F. P., Bitzer-Quintero, O. K., Ramírez-Anguiano, A. C., Flores-Alvarado, L. J., Ramírez-Ramírez, V., . . . Torres-Sánchez, E. D. (2013). Immunology and oxidative stress in multiple sclerosis: clinical and basic approach. Clinical and Developmental Immunology, 2013 Ortiz, G. G., Pacheco-Moisés, F. P., Bitzer-Quintero, O. K., Ramírez-Anguiano, A. C., Flores-Alvarado, L. J., Ramírez-Ramírez, V., . . . Torres-Sánchez, E. D. (2013). Immunology and oxidative stress in multiple sclerosis: clinical and basic approach. Clinical and Developmental Immunology, 2013
go back to reference Pfeifenbring S, Nessler S, Wegner C, Stadelmann C, Brück W (2015) Remyelination After Cuprizone-Induced Demyelination Is Accelerated in Juvenile Mice. J Neuropathol Exp Neurol 74(8):756–766CrossRefPubMed Pfeifenbring S, Nessler S, Wegner C, Stadelmann C, Brück W (2015) Remyelination After Cuprizone-Induced Demyelination Is Accelerated in Juvenile Mice. J Neuropathol Exp Neurol 74(8):756–766CrossRefPubMed
go back to reference Pu, Y., Zhang, S., Zhou, R., Huang, N., Li, H., Wei, W., . . . Li, Z. (2015). IL-17A up-regulates expression of endothelial tissue factor in liver cirrhosis via the ROS/p38 signal pathway. Biochemical and biophysical research communications Pu, Y., Zhang, S., Zhou, R., Huang, N., Li, H., Wei, W., . . . Li, Z. (2015). IL-17A up-regulates expression of endothelial tissue factor in liver cirrhosis via the ROS/p38 signal pathway. Biochemical and biophysical research communications
go back to reference Ramroodi N, Khani M, Ganjali Z, Javan MR, Sanadgol N, Khalseh R et al (2015) Prophylactic effect of BIO-1211 small-molecule antagonist of VLA-4 in the EAE mouse model of multiple sclerosis. Immunol Investig 44(7):694–712CrossRef Ramroodi N, Khani M, Ganjali Z, Javan MR, Sanadgol N, Khalseh R et al (2015) Prophylactic effect of BIO-1211 small-molecule antagonist of VLA-4 in the EAE mouse model of multiple sclerosis. Immunol Investig 44(7):694–712CrossRef
go back to reference Ramroodi N, Niazi AA, Sanadgol N, Ganjali Z, Sarabandi V (2013) Evaluation of reactive Epstein–Barr Virus (EBV) in Iranian patient with different subtypes of multiple sclerosis (MS). Braz J Infect Dis 17(2):156–163CrossRefPubMed Ramroodi N, Niazi AA, Sanadgol N, Ganjali Z, Sarabandi V (2013) Evaluation of reactive Epstein–Barr Virus (EBV) in Iranian patient with different subtypes of multiple sclerosis (MS). Braz J Infect Dis 17(2):156–163CrossRefPubMed
go back to reference Sanadgol N, Golab F, Mostafaie A, Mehdizadeh M, Abdollahi M, Sharifzadeh M, Ravan H (2016) Ellagic acid ameliorates cuprizone-induced acute CNS inflammation via restriction of microgliosis and down-regulation of CCL2 and CCL3 pro-inflammatory chemokines. Cell Molec Biol (Noisy-le-Grand, France) 62(12):24 Sanadgol N, Golab F, Mostafaie A, Mehdizadeh M, Abdollahi M, Sharifzadeh M, Ravan H (2016) Ellagic acid ameliorates cuprizone-induced acute CNS inflammation via restriction of microgliosis and down-regulation of CCL2 and CCL3 pro-inflammatory chemokines. Cell Molec Biol (Noisy-le-Grand, France) 62(12):24
go back to reference Sanadgol N, Golab F, Tashakkor Z, Taki N, Moradi Kouchi S, Mostafaie A, Mehdizadeh M, Abdollahi M, Taghizadeh G, Sharifzadeh M (2017) Neuroprotective effects of ellagic acid on cuprizone-induced acute demyelination through limitation of microgliosis, adjustment of CXCL12/IL-17/IL-11 axis and restriction of mature oligodendrocytes apoptosis. Pharm Biol 55(1):1679–1687CrossRefPubMed Sanadgol N, Golab F, Tashakkor Z, Taki N, Moradi Kouchi S, Mostafaie A, Mehdizadeh M, Abdollahi M, Taghizadeh G, Sharifzadeh M (2017) Neuroprotective effects of ellagic acid on cuprizone-induced acute demyelination through limitation of microgliosis, adjustment of CXCL12/IL-17/IL-11 axis and restriction of mature oligodendrocytes apoptosis. Pharm Biol 55(1):1679–1687CrossRefPubMed
go back to reference Sanchooli J, Ramroodi N, Sanadgol N, Sarabandi V, Ravan H, Rad RS (2014) Relationship between metalloproteinase 2 and 9 concentrations and soluble CD154 expression in Iranian patients with multiple sclerosis. Kaohsiung J Med Sci 30(5):235–242CrossRefPubMed Sanchooli J, Ramroodi N, Sanadgol N, Sarabandi V, Ravan H, Rad RS (2014) Relationship between metalloproteinase 2 and 9 concentrations and soluble CD154 expression in Iranian patients with multiple sclerosis. Kaohsiung J Med Sci 30(5):235–242CrossRefPubMed
go back to reference Sarvandi SS, Joghataei MT, Parivar K, Khosravi M, Sarveazad A, Sanadgol N (2015) In vitro differentiation of rat mesenchymal stem cells to hepatocyte lineage. Iran J Basic Med Sci 18(1):89PubMedPubMedCentral Sarvandi SS, Joghataei MT, Parivar K, Khosravi M, Sarveazad A, Sanadgol N (2015) In vitro differentiation of rat mesenchymal stem cells to hepatocyte lineage. Iran J Basic Med Sci 18(1):89PubMedPubMedCentral
go back to reference Shinto L, Quinn J, Montine T, Dodge HH, Woodward W, Baldauf-Wagner S et al (2014) A randomized placebo-controlled pilot trial of omega-3 fatty acids and alpha lipoic acid in Alzheimer's disease. J Alzheimers Dis 38(1):111–120PubMed Shinto L, Quinn J, Montine T, Dodge HH, Woodward W, Baldauf-Wagner S et al (2014) A randomized placebo-controlled pilot trial of omega-3 fatty acids and alpha lipoic acid in Alzheimer's disease. J Alzheimers Dis 38(1):111–120PubMed
go back to reference Silva MCC, de Sousa CNS, Gomes PXL, de Oliveira GV, Araújo FYR, Ximenes NC et al (2016) Evidence for protective effect of lipoic acid and desvenlafaxine on oxidative stress in a model depression in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 64:142–148CrossRef Silva MCC, de Sousa CNS, Gomes PXL, de Oliveira GV, Araújo FYR, Ximenes NC et al (2016) Evidence for protective effect of lipoic acid and desvenlafaxine on oxidative stress in a model depression in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 64:142–148CrossRef
go back to reference Steelman AJ, Zhou Y, Koito H, Kim S, Payne HR, Lu QR, Li J (2016) Activation of oligodendroglial Stat3 is required for efficient remyelination. Neurobiol Dis 91:336–346CrossRefPubMedPubMedCentral Steelman AJ, Zhou Y, Koito H, Kim S, Payne HR, Lu QR, Li J (2016) Activation of oligodendroglial Stat3 is required for efficient remyelination. Neurobiol Dis 91:336–346CrossRefPubMedPubMedCentral
go back to reference von Leden, R. E., Yauger, Y. J., Khayrullina, G., & Byrnes, K. (2016). Review: CNS Injury and NADPH Oxidase: Oxidative Stress and Therapeutic Targets. Journal of neurotrauma(ja) von Leden, R. E., Yauger, Y. J., Khayrullina, G., & Byrnes, K. (2016). Review: CNS Injury and NADPH Oxidase: Oxidative Stress and Therapeutic Targets. Journal of neurotrauma(ja)
go back to reference Wei W, Wang H, Wu Y, Ding K, Li T, Cong Z et al (2015) Alpha lipoic acid inhibits neural apoptosis via a mitochondrial pathway in rats following traumatic brain injury. Neurochem Int 87:85–91CrossRefPubMed Wei W, Wang H, Wu Y, Ding K, Li T, Cong Z et al (2015) Alpha lipoic acid inhibits neural apoptosis via a mitochondrial pathway in rats following traumatic brain injury. Neurochem Int 87:85–91CrossRefPubMed
go back to reference Wu M-H, Huang C-C, Chio C-C, Tsai K-J, Chang C-P, Lin N-K, Lin M-T (2016) Inhibition of peripheral TNF-α and downregulation of microglial activation by alpha-lipoic acid and etanercept protect rat brain against ischemic stroke. Mol Neurobiol 53(7):4961–4971CrossRefPubMed Wu M-H, Huang C-C, Chio C-C, Tsai K-J, Chang C-P, Lin N-K, Lin M-T (2016) Inhibition of peripheral TNF-α and downregulation of microglial activation by alpha-lipoic acid and etanercept protect rat brain against ischemic stroke. Mol Neurobiol 53(7):4961–4971CrossRefPubMed
go back to reference Yang T, Xu Z, Liu W, Feng S, Li H, Guo M, Deng Y, Xu B (2017) Alpha-lipoic acid reduces methylmercury-induced neuronal injury in rat cerebral cortex via antioxidation pathways. Environ Toxicol 32(3):931–943CrossRefPubMed Yang T, Xu Z, Liu W, Feng S, Li H, Guo M, Deng Y, Xu B (2017) Alpha-lipoic acid reduces methylmercury-induced neuronal injury in rat cerebral cortex via antioxidation pathways. Environ Toxicol 32(3):931–943CrossRefPubMed
go back to reference Zhang J, Zhang ZG, Lu M, Wang X, Shang X, Elias SB, Chopp M (2017) MiR-146a promotes remyelination in a cuprizone model of demyelinating injury. Neuroscience 348:252–263CrossRefPubMed Zhang J, Zhang ZG, Lu M, Wang X, Shang X, Elias SB, Chopp M (2017) MiR-146a promotes remyelination in a cuprizone model of demyelinating injury. Neuroscience 348:252–263CrossRefPubMed
go back to reference Zhu X, Zuo H, Maher BJ, Serwanski DR, LoTurco JJ, Lu QR, Nishiyama A (2012) Olig2-dependent developmental fate switch of NG2 cells. Development 139(13):2299–2307CrossRefPubMedPubMedCentral Zhu X, Zuo H, Maher BJ, Serwanski DR, LoTurco JJ, Lu QR, Nishiyama A (2012) Olig2-dependent developmental fate switch of NG2 cells. Development 139(13):2299–2307CrossRefPubMedPubMedCentral
Metadata
Title
Alpha-lipoic acid mitigates toxic-induced demyelination in the corpus callosum by lessening of oxidative stress and stimulation of polydendrocytes proliferation
Authors
Nima Sanadgol
Fereshteh Golab
Hassan Askari
Fatemeh Moradi
Marziyeh Ajdary
Mehdi Mehdizadeh
Publication date
01-02-2018
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 1/2018
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-017-0099-9

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