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Molecular Neurobiology

, Volume 51, Issue 3, pp 1395–1416 | Cite as

Bisphenol-A Impairs Myelination Potential During Development in the Hippocampus of the Rat Brain

  • Shashi Kant Tiwari
  • Swati Agarwal
  • Lalit Kumar Singh Chauhan
  • Vijay Nath Mishra
  • Rajnish Kumar ChaturvediEmail author
Article

Abstract

Myelin is the functional implication of oligodendrocytes (OLs), which is involved in insulation of axons and promoting rapid propagation of action potential in the brain. OLs are derived from oligodendrocyte progenitor cells (OPCs), which proliferate, differentiate, and migrate throughout the central nervous system. Defects in myelination process lead to the onset of several neurological and neurodegenerative disorders. Exposure to synthetic xenoestrogen bisphenol-A (BPA) causes cognitive dysfunction, impairs hippocampal neurogenesis, and causes onset of neurodevelopmental disorders. However, the effects of BPA on OPC proliferation, differentiation and myelination, and associated cellular and molecular mechanism(s) in the hippocampus of the rat brain are still largely unknown. We found that BPA significantly decreased bromodeoxyuridine (BrdU)-positive cell proliferation and number and size of oligospheres. We observed reduced co-localization of BrdU with myelination markers CNPase and platelet-derived growth factor receptor-α (PDGFR-α), suggesting impaired proliferation and differentiation of OPCs by BPA in culture. We studied the effects of BPA exposure during prenatal and postnatal periods on cellular and molecular alteration(s) in the myelination process in the hippocampus region of the rat brain at postnatal day 21 and 90. BPA exposure both in vitro and in vivo altered proliferation and differentiation potential of OPCs and decreased the expression of genes and levels of proteins that are involved in myelination. Ultrastructural electron microscopy analysis revealed that BPA exposure caused decompaction of myelinated axons and altered g-ratio at both the developmental periods as compared to control. These results suggest that BPA exposure both during prenatal and postnatal periods alters myelination in the hippocampus of the rat brain leading to cognitive deficits.

Keywords

Bisphenol-A Xenoestrogen Neurotoxicity Developmental toxicity Myelin Hippocampus Neural stem cells Oligodendrocyte progenitor cells 

Abbreviations

BPA

Bisphenol-A

NPCs

Neural progenitor cells

PND

Postnatal day

GD

Gestational day

NSCs

Neural stem cells

OPCs

Oligodendrocyte progenitor cells

TEM

Transmission electron microscopy

Notes

Acknowledgments

This work was supported by the Indian Council of Medical Research (ICMR) project grant GAP-244 to R.K.C. S.K.T. and S.A. are recipients of a Senior Research Fellowship from University Grants Commission and Council of Scientific and Industrial Research, New Delhi, respectively. CSIR-IITR Manuscript Communication Number is 3228.

Conflict of Interest

The authors declare no competing financial interest.

Supplementary material

12035_2014_8817_MOESM1_ESM.docx (13 kb)
Table S1 (DOCX 13 kb)
12035_2014_8817_MOESM2_ESM.docx (1.7 mb)
Fig. S1 (DOCX 1753 kb)
12035_2014_8817_MOESM3_ESM.docx (1.2 mb)
Fig. S2 (DOCX 1247 kb)

References

  1. 1.
    MacLusky NJ, Hajszan T, Leranth C (2005) The environmental estrogen bisphenol a inhibits estradiol-induced hippocampal synaptogenesis. Environmental health perspectives 113(6):675–679CrossRefPubMedCentralPubMedGoogle Scholar
  2. 2.
    Welshons WV, Nagel SC, vom Saal FS (2006) Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol a at levels of human exposure. Endocrinology 147(6):56–69CrossRefGoogle Scholar
  3. 3.
    Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC (2009) Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocrine reviews 30(4):293–342CrossRefPubMedCentralPubMedGoogle Scholar
  4. 4.
    Itoh K, Yaoi T, Fushiki S (2012) Bisphenol A, an endocrine-disrupting chemical, and brain development. Neuropathology 32(4):447–457CrossRefPubMedGoogle Scholar
  5. 5.
    Yeo M, Berglund K, Hanna M, Guo JU, Kittur J, Torres MD, Abramowitz J, Busciglio J, Gao Y, Birnbaumer L, Liedtke WB (2013) Bisphenol A delays the perinatal chloride shift in cortical neurons by epigenetic effects on the Kcc2 promoter. Proceedings of the National Academy of Sciences of the United States of America 110(11):4315–4320CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    Michalowicz J (2014) Bisphenol A—sources, toxicity and biotransformation. Environmental toxicology and pharmacology 37(2):738–758CrossRefPubMedGoogle Scholar
  7. 7.
    Rochester JR (2013) Bisphenol A and human health: a review of the literature. Reproductive Toxicology 42:132–155CrossRefPubMedGoogle Scholar
  8. 8.
    Masuo Y, Ishido M (2011) Neurotoxicity of endocrine disruptors: possible involvement in brain development and neurodegeneration. J Toxicol Environ Health B Crit Rev 14(5–7):346–369CrossRefPubMedGoogle Scholar
  9. 9.
    Fudvoye J, Bourguignon JP, Parent AS (2014) Endocrine-disrupting chemicals and human growth and maturation: a focus on early critical windows of exposure. Vitamins and Hormones 94:1–25CrossRefPubMedGoogle Scholar
  10. 10.
    Jurewicz J, Polanska K, Hanke W (2013) Exposure to widespread environmental toxicants and children’s cognitive development and behavioral problems. International journal of occupational medicine and environmental health 26(2):185–204CrossRefPubMedGoogle Scholar
  11. 11.
    Kuehn BM (2007) Expert panels weigh bisphenol-A risks. Jama 298(13):1499–1503PubMedGoogle Scholar
  12. 12.
    Nagao T, Kawachi K, Kagawa N, Komada M (2014) Neurobehavioral evaluation of mouse newborns exposed prenatally to low-dose bisphenol A. The Journal of toxicological sciences 39(2):231–235CrossRefPubMedGoogle Scholar
  13. 13.
    Stump DG, Beck MJ, Radovsky A, Garman RH, Freshwater LL, Sheets LP, Marty MS, Waechter JM Jr, Dimond SS, Van Miller JP, Shiotsuka RN, Beyer D, Chappelle AH, Hentges SG (2010) Developmental neurotoxicity study of dietary bisphenol A in Sprague-Dawley rats. Toxicol Sci 115(1):167–182CrossRefPubMedCentralPubMedGoogle Scholar
  14. 14.
    Eilam-Stock T, Serrano P, Frankfurt M, Luine V (2012) Bisphenol-A impairs memory and reduces dendritic spine density in adult male rats. Behavioral neuroscience 126(1):175–185CrossRefPubMedCentralPubMedGoogle Scholar
  15. 15.
    Yeo M, Patisaul H, Liedtke W (2013) Decoding the language of epigenetics during neural development is key for understanding development as well as developmental neurotoxicity. Epigenetics 8(11):1128–1132CrossRefPubMedGoogle Scholar
  16. 16.
    Hajszan T, Leranth C (2010) Bisphenol A interferes with synaptic remodeling. Frontiers in neuroendocrinology 31(4):519–530CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Kim K, Son TG, Kim SJ, Kim HS, Kim TS, Han SY, Lee J (2007) Suppressive effects of bisphenol A on the proliferation of neural progenitor cells. Journal of toxicology and environmental health 70(15–16):1288–1295CrossRefPubMedGoogle Scholar
  18. 18.
    Liu R, Xing L, Kong D, Jiang J, Shang L, Hao W (2013) Bisphenol A inhibits proliferation and induces apoptosis in micromass cultures of rat embryonic midbrain cells through the JNK, CREB and p53 signaling pathways. Food Chem Toxicol 52:76–82CrossRefPubMedGoogle Scholar
  19. 19.
    Seiwa C, Nakahara J, Komiyama T, Katsu Y, Iguchi T, Asou H (2004) Bisphenol A exerts thyroid-hormone-like effects on mouse oligodendrocyte precursor cells. Neuroendocrinology 80(1):21–30CrossRefPubMedGoogle Scholar
  20. 20.
    Yang Y, Lewis R, Miller RH (2011) Interactions between oligodendrocyte precursors control the onset of CNS myelination. Developmental biology 350(1):127–138CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Barateiro A, Fernandes A (2014) Temporal oligodendrocyte lineage progression: in vitro models of proliferation, differentiation and myelination. Biochimica et biophysica actaGoogle Scholar
  22. 22.
    Keirstead HS, Blakemore WF (1999) The role of oligodendrocytes and oligodendrocyte progenitors in CNS remyelination. Advances in experimental medicine and biology 468:183–197CrossRefPubMedGoogle Scholar
  23. 23.
    Bradl M, Lassmann H (2010) Oligodendrocytes: biology and pathology. Acta neuropathologica 119(1):37–53CrossRefPubMedCentralPubMedGoogle Scholar
  24. 24.
    Uchida N, Chen K, Dohse M, Hansen KD, Dean J, Buser JR, Riddle A, Beardsley DJ, Wan Y, Gong X, Nguyen T, Cummings BJ, Anderson AJ, Tamaki SJ, Tsukamoto A, Weissman IL, Matsumoto SG, Sherman LS, Kroenke CD, Back SA (2012) Human neural stem cells induce functional myelination in mice with severe dysmyelination. Science translational medicine 4 (155):155ra136Google Scholar
  25. 25.
    Grade S, Bernardino L, Malva JO (2013) Oligodendrogenesis from neural stem cells: perspectives for remyelinating strategies. Int J Dev Neurosci 31(7):692–700CrossRefPubMedGoogle Scholar
  26. 26.
    Lavenex P, Banta Lavenex P, Favre G (2014) What animals can teach clinicians about the hippocampus. Frontiers of neurology and neuroscience 34:36–50CrossRefPubMedGoogle Scholar
  27. 27.
    Hitti FL, Siegelbaum SA (2014) The hippocampal CA2 region is essential for social memory. Nature 508(7494):88–92CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Chambers JS, Perrone-Bizzozero NI (2004) Altered myelination of the hippocampal formation in subjects with schizophrenia and bipolar disorder. Neurochemical research 29(12):2293–2302CrossRefPubMedGoogle Scholar
  29. 29.
    Benes FM (1989) Myelination of cortical-hippocampal relays during late adolescence. Schizophrenia bulletin 15(4):585–593CrossRefPubMedGoogle Scholar
  30. 30.
    Dutta R, Chang A, Doud MK, Kidd GJ, Ribaudo MV, Young EA, Fox RJ, Staugaitis SM, Trapp BD (2011) Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients. Annals of neurology 69(3):445–454CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Noble M (2004) The possible role of myelin destruction as a precipitating event in Alzheimer’s disease. Neurobiology of aging 25(1):25–31CrossRefPubMedGoogle Scholar
  32. 32.
    Lee DH, Jeong JY, Kim YS, Kim JS, Cho YW, Roh GS, Kim HJ, Kang SS, Cho GJ, Choi WS (2010) Ethanol down regulates the expression of myelin proteolipid protein in the rat hippocampus. Anatomy & cell biology 43(3):194–200CrossRefGoogle Scholar
  33. 33.
    Pons-Vazquez S, Gallego-Pinazo R, Galbis-Estrada C, Zanon-Moreno V, Garcia-Medina JJ, Vila-Bou V, Sanz-Solana P, Pinazo-Duran MD (2011) Combined pre- and postnatal ethanol exposure in rats disturbs the myelination of optic axons. Alcohol and alcoholism (Oxford, Oxfordshire) 46(5):514–522CrossRefGoogle Scholar
  34. 34.
    Fernandez M, Paradisi M, D’Intino G, Del Vecchio G, Sivilia S, Giardino L, Calza L (2010) A single prenatal exposure to the endocrine disruptor 2,3,7,8-tetrachlorodibenzo-p-dioxin alters developmental myelination and remyelination potential in the rat brain. Journal of neurochemistry 115(4):897–909CrossRefPubMedGoogle Scholar
  35. 35.
    Brubaker CJ, Schmithorst VJ, Haynes EN, Dietrich KN, Egelhoff JC, Lindquist DM, Lanphear BP, Cecil KM (2009) Altered myelination and axonal integrity in adults with childhood lead exposure: a diffusion tensor imaging study. Neurotoxicology 30(6):867–875CrossRefPubMedCentralPubMedGoogle Scholar
  36. 36.
    Rai NK, Ashok A, Rai A, Tripathi S, Nagar GK, Mitra K, Bandyopadhyay S (2013) Exposure to As, Cd and Pb-mixture impairs myelin and axon development in rat brain, optic nerve and retina. Toxicology and applied pharmacology 273(2):242–258CrossRefPubMedGoogle Scholar
  37. 37.
    Zarazua S, Rios R, Delgado JM, Santoyo ME, Ortiz-Perez D, Jimenez-Capdeville ME (2010) Decreased arginine methylation and myelin alterations in arsenic exposed rats. Neurotoxicology 31(1):94–100CrossRefPubMedGoogle Scholar
  38. 38.
    Zawia NH, Harry GJ (1995) Exposure to lead-acetate modulates the developmental expression of myelin genes in the rat frontal lobe. Int J Dev Neurosci 13(6):639–644CrossRefPubMedGoogle Scholar
  39. 39.
    Isaacson LG, Spohler SA, Taylor DH (1990) Trichloroethylene affects learning and decreases myelin in the rat hippocampus. Neurotoxicology and teratology 12(4):375–381CrossRefPubMedGoogle Scholar
  40. 40.
    Fan Y, Ding S, Ye X, Manyande A, He D, Zhao N, Yang H, Jin X, Liu J, Tian C, Xu S, Ying C (2013) Does preconception paternal exposure to a physiologically relevant level of bisphenol A alter spatial memory in an adult rat? Hormones and behavior 64(4):598–604CrossRefPubMedGoogle Scholar
  41. 41.
    Ferguson SA, Law CD, Abshire JS (2012) Developmental treatment with bisphenol A causes few alterations on measures of postweaning activity and learning. Neurotoxicology and teratology 34(6):598–606CrossRefPubMedGoogle Scholar
  42. 42.
    Golub MS, Wu KL, Kaufman FL, Li LH, Moran-Messen F, Zeise L, Alexeeff GV, Donald JM (2010) Bisphenol A: developmental toxicity from early prenatal exposure. Birth defects research 89(6):441–466CrossRefPubMedGoogle Scholar
  43. 43.
    Inagaki T, Frankfurt M, Luine V (2012) Estrogen-induced memory enhancements are blocked by acute bisphenol A in adult female rats: role of dendritic spines. Endocrinology 153(7):3357–3367CrossRefPubMedCentralPubMedGoogle Scholar
  44. 44.
    Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environmental health perspectives 108(3):511–533CrossRefPubMedCentralPubMedGoogle Scholar
  45. 45.
    Mishra D, Tiwari SK, Agarwal S, Sharma VP, Chaturvedi RK (2012) Prenatal carbofuran exposure inhibits hippocampal neurogenesis and causes learning and memory deficits in offspring. Toxicol Sci 127(1):84–100CrossRefPubMedGoogle Scholar
  46. 46.
    Tiwari SK, Agarwal S, Seth B, Yadav A, Nair S, Bhatnagar P, Karmakar M, Kumari M, Chauhan LK, Patel DK, Srivastava V, Singh D, Gupta SK, Tripathi A, Chaturvedi RK, Gupta KC (2014) Curcumin-loaded nanoparticles potently induce adult neurogenesis and reverse cognitive deficits in Alzheimer’s disease model via canonical Wnt/beta-catenin pathway. ACS nano 8(1):76–103CrossRefPubMedGoogle Scholar
  47. 47.
    Preston M, Gong X, Su W, Matsumoto SG, Banine F, Winkler C, Foster S, Xing R, Struve J, Dean J, Baggenstoss B, Weigel PH, Montine TJ, Back SA, Sherman LS (2013) Digestion products of the PH20 hyaluronidase inhibit remyelination. Annals of neurology 73(2):266–280CrossRefPubMedCentralPubMedGoogle Scholar
  48. 48.
    Tiwari MN, Agarwal S, Bhatnagar P, Singhal NK, Tiwari SK, Kumar P, Chauhan LK, Patel DK, Chaturvedi RK, Singh MP, Gupta KC (2013) Nicotine-encapsulated poly(lactic-co-glycolic) acid nanoparticles improve neuroprotective efficacy against MPTP-induced parkinsonism. Free radical biology & medicine 65:704–718CrossRefGoogle Scholar
  49. 49.
    Vitry S, Avellana-Adalid V, Hardy R, Lachapelle F, Baron-Van Evercooren A (1999) Mouse oligospheres: from pre-progenitors to functional oligodendrocytes. Journal of neuroscience research 58(6):735–751CrossRefPubMedGoogle Scholar
  50. 50.
    Zhang SC, Lipsitz D, Duncan ID (1998) Self-renewing canine oligodendroglial progenitor expanded as oligospheres. Journal of neuroscience research 54(2):181–190CrossRefPubMedGoogle Scholar
  51. 51.
    Liu J, Dietz K, DeLoyht JM, Pedre X, Kelkar D, Kaur J, Vialou V, Lobo MK, Dietz DM, Nestler EJ, Dupree J, Casaccia P (2012) Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nature neuroscience 15(12):1621–1623CrossRefPubMedCentralPubMedGoogle Scholar
  52. 52.
    Ligon KL, Fancy SP, Franklin RJ, Rowitch DH (2006) Olig gene function in CNS development and disease. Glia 54(1):1–10CrossRefPubMedGoogle Scholar
  53. 53.
    Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006) Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26(30):7907–7918CrossRefPubMedGoogle Scholar
  54. 54.
    Butt AM, Hornby MF, Ibrahim M, Kirvell S, Graham A, Berry M (1997) PDGF-alpha receptor and myelin basic protein mRNAs are not coexpressed by oligodendrocytes in vivo: a double in situ hybridization study in the anterior medullary velum of the neonatal rat. Molecular and cellular neurosciences 8(5):311–322CrossRefPubMedGoogle Scholar
  55. 55.
    Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiological reviews 81(2):871–927PubMedGoogle Scholar
  56. 56.
    Wegner M (2001) Expression of transcription factors during oligodendroglial development. Microscopy research and technique 52(6):746–752CrossRefPubMedGoogle Scholar
  57. 57.
    Xin M, Yue T, Ma Z, Wu FF, Gow A, Lu QR (2005) Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. J Neurosci 25(6):1354–1365CrossRefPubMedGoogle Scholar
  58. 58.
    Koenning M, Jackson S, Hay CM, Faux C, Kilpatrick TJ, Willingham M, Emery B (2012) Myelin gene regulatory factor is required for maintenance of myelin and mature oligodendrocyte identity in the adult CNS. J Neurosci 32(36):12528–12542CrossRefPubMedCentralPubMedGoogle Scholar
  59. 59.
    Emery B, Agalliu D, Cahoy JD, Watkins TA, Dugas JC, Mulinyawe SB, Ibrahim A, Ligon KL, Rowitch DH, Barres BA (2009) Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 138(1):172–185CrossRefPubMedCentralPubMedGoogle Scholar
  60. 60.
    Chomiak T, Hu B (2009) What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? A theoretical approach. PloS one 4(11):e7754CrossRefPubMedCentralPubMedGoogle Scholar
  61. 61.
    Fenichel P, Chevalier N, Brucker-Davis F (2013) Bisphenol A: an endocrine and metabolic disruptor. Annales d’endocrinologie 74(3):211–220CrossRefPubMedGoogle Scholar
  62. 62.
    Lee S, Suk K, Kim IK, Jang IS, Park JW, Johnson VJ, Kwon TK, Choi BJ, Kim SH (2008) Signaling pathways of bisphenol A-induced apoptosis in hippocampal neuronal cells: role of calcium-induced reactive oxygen species, mitogen-activated protein kinases, and nuclear factor-kappaB. Journal of neuroscience research 86(13):2932–2942CrossRefPubMedGoogle Scholar
  63. 63.
    Kim ME, Park HR, Gong EJ, Choi SY, Kim HS, Lee J (2011) Exposure to bisphenol A appears to impair hippocampal neurogenesis and spatial learning and memory. Food Chem Toxicol 49(12):3383–3389CrossRefPubMedGoogle Scholar
  64. 64.
    Palanza P, Gioiosa L, vom Saal FS, Parmigiani S (2008) Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environmental research 108(2):150–157CrossRefPubMedGoogle Scholar
  65. 65.
    Akers KG, Martinez-Canabal A, Restivo L, Yiu AP, De Cristofaro A, Hsiang HL, Wheeler AL, Guskjolen A, Niibori Y, Shoji H, Ohira K, Richards BA, Miyakawa T, Josselyn SA, Frankland PW (2014) Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344(6184):598–602CrossRefPubMedGoogle Scholar
  66. 66.
    Albani SH, McHail DG, Dumas TC (2014) Developmental studies of the hippocampus and hippocampal-dependent behaviors: insights from interdisciplinary studies and tips for new investigators. Neuroscience and biobehavioral reviews 43:183–190CrossRefPubMedGoogle Scholar
  67. 67.
    White R, Kramer-Albers EM (2014) Axon-glia interaction and membrane traffic in myelin formation. Frontiers in cellular neuroscience 7:284CrossRefPubMedCentralPubMedGoogle Scholar
  68. 68.
    Arnold SE, Trojanowski JQ (1996) Human fetal hippocampal development: I. Cytoarchitecture, myeloarchitecture, and neuronal morphologic features. The Journal of comparative neurology 367(2):274–292CrossRefPubMedGoogle Scholar
  69. 69.
    Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, Haroutunian V, Fienberg AA (2001) Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 98(8):4746–4751CrossRefPubMedCentralPubMedGoogle Scholar
  70. 70.
    Brown JS Jr (2009) Effects of bisphenol-A and other endocrine disruptors compared with abnormalities of schizophrenia: an endocrine-disruption theory of schizophrenia. Schizophrenia bulletin 35(1):256–278CrossRefPubMedCentralPubMedGoogle Scholar
  71. 71.
    Zuccaro E, Arlotta P (2013) The quest for myelin in the adult brain. Nature cell biology 15(6):572–575CrossRefPubMedGoogle Scholar
  72. 72.
    Doretto S, Malerba M, Ramos M, Ikrar T, Kinoshita C, De Mei C, Tirotta E, Xu X, Borrelli E (2011) Oligodendrocytes as regulators of neuronal networks during early postnatal development. PloS one 6(5):e19849CrossRefPubMedCentralPubMedGoogle Scholar
  73. 73.
    Downes N, Mullins P (2013) The development of myelin in the brain of the juvenile rat. Toxicologic pathologyGoogle Scholar
  74. 74.
    Wang H, Li C, Wang H, Mei F, Liu Z, Shen HY, Xiao L (2013) Cuprizone-induced demyelination in mice: age-related vulnerability and exploratory behavior deficit. Neuroscience bulletin 29(2):251–259CrossRefPubMedGoogle Scholar
  75. 75.
    Fulton D, Paez PM, Campagnoni AT (2010) The multiple roles of myelin protein genes during the development of the oligodendrocyte. ASN neuro 2(1):e00027CrossRefPubMedCentralPubMedGoogle Scholar
  76. 76.
    Bongarzone ER, Pasquini JM, Soto EF (1995) Oxidative damage to proteins and lipids of CNS myelin produced by in vitro generated reactive oxygen species. Journal of neuroscience research 41(2):213–221CrossRefPubMedGoogle Scholar
  77. 77.
    Geurts JJ, Bo L, Roosendaal SD, Hazes T, Daniels R, Barkhof F, Witter MP, Huitinga I, van der Valk P (2007) Extensive hippocampal demyelination in multiple sclerosis. Journal of neuropathology and experimental neurology 66(9):819–827CrossRefPubMedGoogle Scholar
  78. 78.
    Roussos P, Haroutunian V (2014) Schizophrenia: susceptibility genes and oligodendroglial and myelin related abnormalities. Frontiers in cellular neuroscience 8:5CrossRefPubMedCentralPubMedGoogle Scholar
  79. 79.
    Naule L, Picot M, Martini M, Parmentier C, Hardin-Pouzet H, Keller M, Franceschini I, Mhaouty-Kodja S (2014) Neuroendocrine and behavioral effects of maternal exposure to oral bisphenol A in female mice. The Journal of endocrinology 220(3):375–388CrossRefPubMedGoogle Scholar
  80. 80.
    Zhang Z, Cerghet M, Mullins C, Williamson M, Bessert D, Skoff R (2004) Comparison of in vivo and in vitro subcellular localization of estrogen receptors alpha and beta in oligodendrocytes. Journal of neurochemistry 89(3):674–684CrossRefPubMedGoogle Scholar
  81. 81.
    Calza L, Fernandez M, Giardino L (2010) Cellular approaches to central nervous system remyelination stimulation: thyroid hormone to promote myelin repair via endogenous stem and precursor cells. Journal of molecular endocrinology 44(1):13–23CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Shashi Kant Tiwari
    • 1
    • 2
  • Swati Agarwal
    • 1
    • 2
  • Lalit Kumar Singh Chauhan
    • 1
  • Vijay Nath Mishra
    • 3
  • Rajnish Kumar Chaturvedi
    • 1
    • 2
    Email author
  1. 1.Developmental Toxicology Division, Systems Toxicology GroupCSIR-Indian Institute of Toxicology Research (CSIR-IITR)LucknowIndia
  2. 2.Academy of Scientific and Innovative Research (AcSIR)New DelhiIndia
  3. 3.Department of Neurology, Institute of Medical SciencesBanaras Hindu UniversityVaranasiIndia

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