Advertisement

Oxidative Stress and Neurodegeneration

  • Juana M. PasquiniEmail author
  • Laura A. Pasquini
  • Hector R. Quintá
Chapter
Part of the Advances in Biochemistry in Health and Disease book series (ABHD, volume 16)

Abstract

Multiple sclerosis, a highly disseminated chronic inflammatory demyelinating disease, entails progressive neuroaxonal degeneration and is one of the most common causes of progressive disability affecting young people. The mechanisms involved in oxidative stress-mediated neurodegeneration in MS patients include free radical production from different sources: (a) mitochondria forced to produce high levels of energy for axonal transport upon myelin sheath loss, (b) immune cells activated upon demyelination and neurodegeneration, and (c) myelin deficiencies in producing ATP synthesis outside mitochondria. In addition, oxidative stress is amplified by iron released into the extracellular space from myelin breakdown and degenerated macrophages and microglia. The normal neuronal polarization and development in each region of the central nervous system depend on the normal function of actin cytoskeleton dynamics. This dynamics is primarily affected when there is a deregulation in the intraneuronal production of reactive oxygen species. These reactive oxygen species promote oxidation of filamentous actin (cytoskeleton depolymerization) and, therefore, axonal collapse. In summary, preventing oxidative stress is crucial to maintain the normal function of the central nervous system.

Keywords

Demyelination Neurodegeneration Microglia Oxidative stress Oligodendrocytes Mical Hydrogen peroxide Semaphorin 3A 

References

  1. 1.
    Bjartmar C, Kinkel PR, Kidd G et al (2001) Axonal loss in normal-appearing white matter in a patient with acute MS. Neurology 57:1248–1252PubMedCrossRefGoogle Scholar
  2. 2.
    Tallantyre EC, Bo L, Al-Rawashdeh O et al (2009) Greater loss of axons in primary progressive multiple sclerosis plaques compared to secondary progressive disease. Brain 132:1190–1199PubMedCrossRefGoogle Scholar
  3. 3.
    Kuhlmann T, Lingfeld G, Bitsch A et al (2002) Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 125:2202–2212PubMedCrossRefGoogle Scholar
  4. 4.
    Funfschilling U et al (2012) Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:517–521PubMedPubMedCentralGoogle Scholar
  5. 5.
    Lee Y, Morrison BM, Li Y et al (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443–448PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Frischer JM, Bramow S, Dal-Bianco A et al (2009) The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132:1175–1189PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Kornek B, Storch MK, Weissert R et al (2000) Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 157:267–276PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Kutzelnigg A, Lucchinetti CF, Stadelmann C et al (2005) Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 128:2705–2712PubMedCrossRefGoogle Scholar
  9. 9.
    DeLuca GC, Ebers GC, Esiri MM (2004) Axonal loss in multiple sclerosis: a pathological survey of the corticospinal and sensory tracts. Brain 127:1009–1018PubMedCrossRefGoogle Scholar
  10. 10.
    Bitsch A, Schuchardt J, Bunkowski S et al (2000) Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. Brain 123:1174–1183PubMedCrossRefGoogle Scholar
  11. 11.
    DeLuca GC, Williams K, Evangelou N et al (2006) The contribution of demyelination to axonal loss in multiple sclerosis. Brain 129:1507–1516PubMedCrossRefGoogle Scholar
  12. 12.
    Smith KJ, Lassmann H (2002) The role of nitric oxide in multiple sclerosis. Lancet Neurol 1:232–241PubMedCrossRefGoogle Scholar
  13. 13.
    Koch MW, Ramsaransing GSM, Arutjunyan AV et al (2006) Oxidative stress in serum and peripheral blood leukocytes in patients with different disease courses of multiple sclerosis. J Neurol 253:483–487PubMedCrossRefGoogle Scholar
  14. 14.
    Vladimirova O, O’Connor J, Cahill A et al (1998) Oxidative damage to DNA in plaques of MS brains. Mult Scler 4:413–418PubMedCrossRefGoogle Scholar
  15. 15.
    Hammann KP, Hopf HC (1986) Monocytes constitute the only peripheral blood cell population showing an increased burst activity in multiple sclerosis patients. Int Arch Allergy Applied Immunol 81:230–234CrossRefGoogle Scholar
  16. 16.
    Greco A, Minghetti L, Sette G et al (1999) Cerebrospinal fluid isoprostane shows oxidative stress in patients with multiple sclerosis. Neurology 53:1876–1879PubMedCrossRefGoogle Scholar
  17. 17.
    Nikic I, Merkler D, Sorbara C et al (2011) A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 17:495–499PubMedCrossRefGoogle Scholar
  18. 18.
    van Horssen J, Witte ME, Schreibelt G, de Vries HE (2011) Radical changes in multiple sclerosis pathogenesis. Biochim Biophys Acta 1812:141–150PubMedCrossRefGoogle Scholar
  19. 19.
    van Horssen J, Schreibelt G, Drexhage J et al (2008) Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 45:1729–1737PubMedCrossRefGoogle Scholar
  20. 20.
    Haider L, Fischer MT, Frischer JM et al (2011) Oxidative damage in multiple sclerosis lesions. Brain 134:1914–1924PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Campbell GR, Mahad DJ (2011) Mitochondria as crucial players in demyelinated axons: lessons from neuropathology and experimental demyelination. Autoimmune Dis 2011:262847. doi: 10.4061/2011/262847 PubMedPubMedCentralGoogle Scholar
  22. 22.
    Fünfschilling U, Supplie LM, Mahad D et al (2012) Glycolytic oligodendrocytes maintain myelin and longterm axonal integrity. Nature 485:517–521PubMedPubMedCentralGoogle Scholar
  23. 23.
    Andrews H, White K, Thomson C et al (2006) Increased axonal mitochondrial activity as an adaptation to myelin deficiency in the shiverer mouse. J Neurosci Res 83:1533–1539PubMedCrossRefGoogle Scholar
  24. 24.
    Hogan V, White K, Edgar J et al (2009) Increase in mitochondrial density within axons and supporting cells in response to demyelination in the Plp1 mouse model. J Neurosci Res 87:452–459PubMedCrossRefGoogle Scholar
  25. 25.
    Sathornsumetee S, McGavern DB, Ure DR, Rodriguez M (2000) Quantitative ultrastructural analysis of a single spinal cord demyelinated lesion predicts total lesion load, axonal loss, and neurological dysfunction in a murine model of multiple sclerosis. Am J Pathol 157:1365–1376PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Zambonin JL, Zhao C, Ohno N et al (2011) Increased mitochondrial content in remyelinated axons: implications for multiple sclerosis. Brain 134:1901–1913PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Dutta R, McDonough J, Yin X et al (2006) Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 59:478–489PubMedCrossRefGoogle Scholar
  28. 28.
    Kalman B (2006) Role of mitochondria in multiple sclerosis. Curr Neurol Neurosci Rep 6:244–252PubMedCrossRefGoogle Scholar
  29. 29.
    Smith KJ, McDonald WI (1999) The pathophysiology of multiple sclerosis: the mechanisms underlying the production of symptoms and the natural history of the disease. Philos Trans R Soc Lond B Biol Sci 354:1649–1673PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Mahad DJ, Ziabreva I, Campbell G et al (2009) Mitochondrial changes within axons in multiple sclerosis. Brain 132:1161–1174PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Ohno N, Kidd GJ, Mahad D et al (2011) Myelination and axonal electrical activity modulate the distribution and motility of mitochondria at CNS nodes of Ranvier. J Neurosci 31:7249–7258PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Larsson NG (2010) Somatic mitochondrial DNA mutations in mammalian aging. Ann Rev Biochem 79:683–706PubMedCrossRefGoogle Scholar
  33. 33.
    Howarth C, Gleeson P, Attwell D (2012) Updated energy budgets for neural computation in the neocortex and cerebellum. J Cereb Blood Flow Metab 32:1222–1232PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Smith KJ (2007) Sodium channels and multiple sclerosis: roles in symptom production, damage and therapy. Brain Pathol 17:230–242PubMedCrossRefGoogle Scholar
  35. 35.
    Tsutsui S, Stys PK (2013) Metabolic injury to axons and myelin. Exp Neurol 246:26–34PubMedCrossRefGoogle Scholar
  36. 36.
    Waxman SG (2006) Ions, energy and axonal injury: towards a molecular neurology of multiple sclerosis. Trends Mol Med 12:192–195PubMedCrossRefGoogle Scholar
  37. 37.
    Graham R, Campbell J, Worrall T, Mahad DJ (2014) The central role of mitochondria in axonal degeneration in multiple sclerosis. Multiple Sclerosis J 20:1806–1813CrossRefGoogle Scholar
  38. 38.
    Babior BM (2004) NADPH oxidase. Curr Opin Immunol 16:42–47PubMedCrossRefGoogle Scholar
  39. 39.
    Zeis T, Probst A, Steck AJ et al (2009) Molecular changes in white matter adjacent to an active demyelinating lesion in early multiple sclerosis. Brain Pathol 19:459–466PubMedCrossRefGoogle Scholar
  40. 40.
    Nikić I, Merkler D, Sorbara C et al (2011) A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 17:495–499PubMedCrossRefGoogle Scholar
  41. 41.
    Jekabsone A, Neher JJ, Borutaite V, Brown GC (2007) Nitric oxide from neuronal nitric oxide synthase sensitises neurons to hypoxia-induced death via competitive inhibition of cytochrome oxidase. J Neurochem 103:346–356PubMedGoogle Scholar
  42. 42.
    Haider L (2015) Inflammation, iron, energy failure and oxidative stress in the pathogenesis of multiple sclerosis. Oxid Med Cell Longev 2015:725370. doi: 10.1155/2015/725370 PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    DiMauro S, Schon EA, Carelli V, Hirano M (2013) The clinical maze of mitochondrial neurology. Nat Rev Neurol 9:429–444PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Yakes FM, VanHouten B (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 94:514–519PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Witte ME, Geurts JJG, de Vries HE et al (2010) Mitochondrial dysfunction: a potential link between neuroinflammation and neurodegeneration? Mitochondrion 10:411–418PubMedCrossRefGoogle Scholar
  46. 46.
    Panfoli I, Calzia D, Bianchini P et al (2009) Evidence for aerobic metabolism in retinal rod outer segment disks. Int J Biochem Cell Biol 41:2555–2565PubMedCrossRefGoogle Scholar
  47. 47.
    Ravera S, Panfoli I, Calzia D et al (2009) Evidence for aerobic ATP synthesis in isolated myelin vesicles. Int J Biochem Cell Biol 41:1581–1591PubMedCrossRefGoogle Scholar
  48. 48.
    Ravera S, Panfoli I, Aluigi MG et al (2011) Characterization of myelin sheath F0-F1-ATP synthase and its regulation by IF. Cell Biochem Biophys 59:63–70PubMedCrossRefGoogle Scholar
  49. 49.
    Ravera S, Bartolucci M, Calzia D et al (2013) Tricarboxylic acid cycle-sustained oxidative phosphorylation in isolated myelin vesicles. Biochimie 95:1991–1998PubMedCrossRefGoogle Scholar
  50. 50.
    Ravera S, Nobbio L, Visigalli D et al (2013) Oxydative phosphorylation in sciatic nerve myelin and its impairment in a model of dysmyelinating peripheral neuropathy. J Neurochem 126:82–92PubMedCrossRefGoogle Scholar
  51. 51.
    Bartolucci M, Ravera S, Garbarino G et al (2015) functional expression of electron transport chain and FoF1-ATP synthase in optic nerve myelin sheath. Neurochem Res 40(11):2230–2241PubMedCrossRefGoogle Scholar
  52. 52.
    Ravera S, Bartolucci M, Cuccarolo P et al (2015) Oxidative stress in myelin sheath: the other face of the extramitochondrial oxidative phosphorylation ability. Free Radic Res 49:1156–1164PubMedCrossRefGoogle Scholar
  53. 53.
    Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18:685–716PubMedCrossRefGoogle Scholar
  54. 54.
    Hulet SW, Hess EJ, Debinski W et al (1999) Characterization and distribution of ferritin binding sites in the adult mouse brain. J Neurochem 72:868–874PubMedCrossRefGoogle Scholar
  55. 55.
    Hulet SW, Powers S, Connor JR (1999) Distribution of transferrin and ferritin binding in normal and multiple sclerotic human brains. J Neurol Sci 165:48–55PubMedCrossRefGoogle Scholar
  56. 56.
    Hallgren B, Sourander P (1958) The effect of age on the non haemin iron in the human brain. J Neurochem 3:41–51PubMedCrossRefGoogle Scholar
  57. 57.
    Barnett MH, Prineas JW (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 55:458–468PubMedCrossRefGoogle Scholar
  58. 58.
    Lassmann H (2011) The architecture of inflammatory demyelinating lesions: implications for studies on pathogenesis. Neuropathol Appl Neurobiol 37:698–710PubMedCrossRefGoogle Scholar
  59. 59.
    Hametner S, Wimmer I, Haider L et al (2013) Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 74:848–861PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Lopes KO, Sparks DL, Streit WJ (2008) Microglial dystrophy in the aged and Alzheimer’s disease brain is associated with ferritin immunoreactivity. Glia 56:1048–1060PubMedCrossRefGoogle Scholar
  61. 61.
    Craelius W, Migdal MW, Luessenhop CP et al (1982) Iron deposits surrounding multiple sclerosis plaques. Arch Pathol Lab Med 106:397–399PubMedGoogle Scholar
  62. 62.
    Bagnato F, Hametner S, Yao B et al (2011) Tracking iron in multiple sclerosis: a combined imaging and histopathological study at 7 Tesla. Brain 134:3599–3612PubMedCentralCrossRefGoogle Scholar
  63. 63.
    Friese MA, Schattling B, Fugger L (2014) Mechanisms of neurodegeneration and axonal dysfunction in multiple sclerosis. Nat Rev Neurol 10:225–238PubMedCrossRefGoogle Scholar
  64. 64.
    Lassmann H, Van Horssen J, Mahad D (2012) Progressive multiple sclerosis: pathology and pathogenesis. Nat Rev Neurol 8:647–656PubMedCrossRefGoogle Scholar
  65. 65.
    Acs P, Kipp M, Norkute A et al (2009) 17β-estradiol and progesterone prevent cuprizone provoked demyelination of corpus callosum in male mice. Glia 57:807–814PubMedCrossRefGoogle Scholar
  66. 66.
    Clarner T, Parabucki A, Beyer C, Kipp M (2011) Corticosteroids impair remyelination in the corpus callosum of cuprizone-treated mice. J Neuroendocrinol 23:601–611PubMedCrossRefGoogle Scholar
  67. 67.
    Kipp M, Clarner T, Dang J et al (2009) The cuprizone animal model: new insights into an old story. Acta Neuropathol 118:723–736PubMedCrossRefGoogle Scholar
  68. 68.
    Harsan LA, Steibel J, Zaremba A et al (2008) Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J Neurosci 28:14189–14201PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Mason JL, Langaman C, Morell P et al (2001) Episodic demyelination and subsequent remyelination within the murine central nervous system: changes in axonal caliber. Neuropathol Appl Neurobiol 27:50–58PubMedCrossRefGoogle Scholar
  70. 70.
    Lindner M, Fokuhl J, Linsmeier F et al (2009) Chronic toxic demyelination in the central nervous system leads to axonal damage despite remyelination. Neurosci Lett 453:120–125PubMedCrossRefGoogle Scholar
  71. 71.
    Zhang H, Zhang Y, Xu H et al (2013) Locomotor activity and anxiety status, but not spatial working memory, are affected in mice after brief exposure to cuprizone. Neurosci Bull 29:633–641PubMedCrossRefGoogle Scholar
  72. 72.
    Manrique-Hoyos N, Jürgens T, Grønborg M et al (2012) Late motor decline after accomplished remyelination: impact for progressive multiple sclerosis. Ann Neurol 71:227–244PubMedCrossRefGoogle Scholar
  73. 73.
    Pasquini LA, Calatayud CA, Bertone U et al (2007) The neurotoxic effect of cuprizone on oligodendrocytes depends on thepresence of pro-inflammatory cytokines secreted by microglia. Neurochem Res 32:279–292PubMedCrossRefGoogle Scholar
  74. 74.
    Benardais K, Kotsiari A, Skuljec J et al (2013) Cuprizone [bis(cyclohexyliden-hydrazide)] is selectively toxic for mature oligodendrocytes. Neurotoxic Res 24:244–250CrossRefGoogle Scholar
  75. 75.
    Acs P, Komoly S (2012) Selective ultrastructural vulnerability in the cuprizone-induced experimental demyelination. Ideggyogy Sz 65:266–270PubMedGoogle Scholar
  76. 76.
    Biancotti JC, Kumar S, de Vellis J (2008) Activation of inflammatory response by a combination of growth factors in cuprizone-induced demyelinated brain leads to myelin repair. Neurochem Res 33:2615–2628PubMedCrossRefGoogle Scholar
  77. 77.
    Hiremath MM, Saito Y, Knapp GW et al (1998) Microglial/macrophage accumulation during cuprizone-induced demyelinationin in C57BL/6 mice. J Neuroimmunol 92:38–49PubMedCrossRefGoogle Scholar
  78. 78.
    Asano M, Wakabayashi T, Ishikawa K, Kishimoto H (1978) Mechanism of the formation of megamitochondria by copper-chelating agents IV. Role of the fusion phenomenon in the cuprizone-induced megamitochondrial formation. Acta Pathol Jpn 28:205–213PubMedGoogle Scholar
  79. 79.
    Ludwin SK (1978) Central nervous system demyelination and remyelination in the mouse: an ultrastructural study of cuprizone toxicity. Lab Invest 39:597–612PubMedGoogle Scholar
  80. 80.
    Tandler B, Hoppel CL (1973) Division of giant mitochondria during recovery from cuprizone intoxication. J Cell Biol 56:266–272PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Wakabayashi T, Asano M, Ishikawa K, Kishimoto H (1978) Mechanism of the formation of megamitochondria by copper-chelating agents V. Further studies on isolated megamitochondria. Acta Pathol Jpn 28:215–223PubMedGoogle Scholar
  82. 82.
    Flatmark T, Kryvi H, Tangeras A (1980) Induction of megamitochondria by cuprizone (biscyclohexanone oxaldihydrazone). Evidence for an inhibition of the mitochondrial division process. Eur J Cell Biol 23:141–148PubMedGoogle Scholar
  83. 83.
    Miwa S, Lawless C, von Zglinicki T (2008) Mitochondrial turnover in liver is fast in vivo and is accelerated by dietary restriction: application of a simple dynamic model. Aging Cell 7:920–923PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Wakabayashi T, Asano M, Kurono C (1975) Mechanism of the formation of megamitochondria induced by copper-chelating agents II. Isolation and some properties of megamitochondria from the cuprizone-treated mouse liver. Acta Pathol Jpn 25:39–49PubMedGoogle Scholar
  85. 85.
    Wakabayashi T, Asano M, Ishikawa K, Kishimoto H (1977) Cuprizone induced megamitochondrial formation and membrane fusion. J Electron Microsc (Tokyo) 26:137–140Google Scholar
  86. 86.
    Tandler B, Hoppel CL (1975) The failure of supplemental dietary copper to preventcuprizone-induced alterations in mouse hepatocytes. Beitr Pathol 156:56–64PubMedCrossRefGoogle Scholar
  87. 87.
    Wagner T, Rafael J (1977) Biochemical properties of liver megamitochondria induced by chloramphenicol or cuprizone. Exp Cell Res 107:1–13Google Scholar
  88. 88.
    Kimberlin RH, Collis SC, Walker CA (1976) Profiles of brain glycosidase activity in cuprizone-fed Syrian hamsters and in scrapie-affected mice, rats, Chinese and Syrian hamsters. J Comp Pathol 86:135–142PubMedCrossRefGoogle Scholar
  89. 89.
    Millet V, Moiola CP, Pasquini JM et al (2009) Partial inhibition of proteasome activity enhances remyelination after cuprizone-induced demyelination. Exp Neurol 217:282–296PubMedCrossRefGoogle Scholar
  90. 90.
    Nelecz MJ, Wroniszewska A, Famulski KS, Wojtczak L (1982) Changes in the mitochondrial surface potential during cuprizone-induced formation of megamitochondria. Eur J Cell Biol 27:289–295PubMedGoogle Scholar
  91. 91.
    Petronilli V, Zoratti M (1990) A characterization of cuprizone-induced giant mouse liver mitochondria. J Bioenerg Biomembr 22:663–677PubMedCrossRefGoogle Scholar
  92. 92.
    Venturini G (1973) Enzymic activities and sodium, potassium and copper concentrations in mouse brain and liver after cuprizone treatment in vivo. J Neurochem 21:1147–1151PubMedCrossRefGoogle Scholar
  93. 93.
    Praet J, Guglielmetti C, Berneman Z et al (2014) Cellular and molecular neuropathology of the cuprizone mouse model: clinical relevance for multiple sclerosis. Neurosci Biobehav Rev 47:485–505PubMedCrossRefGoogle Scholar
  94. 94.
    Bernardo A, Greco A, Levi G, Minghetti L (2003) Differential lipid peroxidation, Mn-superoxide dismutase and bcl-2 expression contribute to the maturation-dependent vulnerability of oligodendrocytes to oxidative stress. J Neuropathol Exp Neurol 62:509–519PubMedCrossRefGoogle Scholar
  95. 95.
    Witherick J, Wilkins A, Scolding N, Kemp K (2010) Mechanisms of oxidative damage in multiple sclerosis and a cell therapy approach to treatment. Autoimmune Dis doi: 10.4061/2011/164608 Google Scholar
  96. 96.
    Ljutakova SG, Russanov EM (1985) Differences in the in vivo effects of cuprizone on superoxide dismutase activity in rat liver cytosol and mitochondrial intermembrane space. Acta Physiol Pharmacol Bulg 11:56–61PubMedGoogle Scholar
  97. 97.
    Russanov EM, Ljutakova SG (1980) Effect of cuprizone on copper exchange and superoxide dismutase activity in rat liver. Gen Pharmacol 11:535–538PubMedCrossRefGoogle Scholar
  98. 98.
    Zhang Y, Xu H, Jiang W et al (2008) Quetiapine alleviates the cuprizone-induced white matter pathology in the brain of C57BL/6 mouse. Schizophr Res 106:182–191PubMedCrossRefGoogle Scholar
  99. 99.
    Juurlink BH, Thorburne SK, Hertz L (1998) Peroxide-scavenging deficit underlies oligodendrocyte susceptibility to oxidative stress. Glia 22:371–378PubMedCrossRefGoogle Scholar
  100. 100.
    Marrif H, Juurlink BH (2003) Differential vulnerability of oligodendrocytes and astrocytes to hypoxic-ischemic stress. Adv Mol Cell Biol 31:857–867CrossRefGoogle Scholar
  101. 101.
    Xu H, Yang HJ, Li XM (2013) Differential effects of antipsychotics on the devel-opment of rat oligodendrocyte precursor cells exposed to cuprizone. Eur Arch Psychiatry Clin Neurosci 264:121–129PubMedCrossRefGoogle Scholar
  102. 102.
    Volpe JJ (2009) The encephalopathy of prematurity--brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 16:167–178PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Bax M, Tydeman C, Flodmark O (2006) Clinical and MRI correlates of cerebral palsy: the European Cerebral Palsy Study. JAMA 296:1602–1608PubMedCrossRefGoogle Scholar
  104. 104.
    Ferriero DM, Miller SP (2010) Imaging of selective vulnerability in the developing nervous system. J Anat 217:429–435PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Rezaie P, Dean A (2002) Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathol 22:106–132CrossRefGoogle Scholar
  106. 106.
    Haynes RL, Folkerth RD, Keefe RJ et al (2003) Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 62:441–450PubMedCrossRefGoogle Scholar
  107. 107.
    Paez PM, Marta CB, Moreno MB et al (2002) Apotransferrin decreases migration and enhances differentiation of oligodendroglial progenitor cells in an in vitro system. Dev Neurosci 24:47–58PubMedCrossRefGoogle Scholar
  108. 108.
    Paez PM, Garcia CI, Davio C et al (2004) Apotransferrin promotes the differentiation of two oligodendroglial cell lines. Glia 46:207–217PubMedCrossRefGoogle Scholar
  109. 109.
    Vannucci RC, Vannucci SJ (1997) A model of perinatal hypoxic ischemic brain damage. Ann N Y Acad Sci 835:234–249PubMedCrossRefGoogle Scholar
  110. 110.
    Vannucci RC, Vannucci SJ (2005) Perinatal hypoxic–ischemic brain damage: evolution of an animal model. Dev Neurosci 27:81–86PubMedCrossRefGoogle Scholar
  111. 111.
    Vannucci SJ (1999) Rat model of perinatal hypoxic–ischemic brain damage. J Neurosci Res 55:158–163PubMedCrossRefGoogle Scholar
  112. 112.
    Guardia-Clausi M, Pasquini LA, Soto EF, Pasquini JM (2010) Apotransferrin-induced recovery after hypoxic/ischaemic injury on myelination. ASN Neurol 19:e00048. doi: 10.1042/AN20100020 Google Scholar
  113. 113.
    Paez PM, Fulton DJ, Spreuer V et al (2009) Regulation of store-operated and voltage-operated Ca channels in the proliferation and death of oligodendrocyte precursor cells by golgi proteins. ASN Neurol 1:1–15Google Scholar
  114. 114.
    Guardia-Clausi M, Paez PM, Campagnoni AT et al (2012) Intranasal administration of Tf protects and repairs the neonatal white matter after a cerebral hypoxic-ischemic event. Glia 60:1540–1554PubMedCrossRefGoogle Scholar
  115. 115.
    Back SA, Gan X, Li Y et al (1998) Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death by glutathione depletion. J Neurosci 16:6241–6253Google Scholar
  116. 116.
    Back SA, Han BH, Luo NL et al (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia–ischemia. J Neurosci 22:455–463PubMedGoogle Scholar
  117. 117.
    Baud O, Haynes RF, Wang H et al (2004) Developmental up-regulation of MnSOD in rat oligodendrocytes confers protection against oxidative injury. Eur J Neurosci 20:29–40PubMedCrossRefGoogle Scholar
  118. 118.
    Fern R, Möller T (2000) Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J Neurosci 20:34–42PubMedGoogle Scholar
  119. 119.
    Fragoso G, Martínez-Bermúdez AK, Liu HN et al (2004) Developmental differences in HO-induced oligodendrocyte cell death: roles of glutathione, mitogen-activated protein kinases and caspase 3. J Neurochem 90:392–404PubMedCrossRefGoogle Scholar
  120. 120.
    Lin S, Rhodes PG, Lei M et al (2004) α-Phenyl-n-tert-butyl-nitrone attenuates hypoxic-ischemic white matter injury in the neonatal rat brain. Brain Res 1007:132–141PubMedCrossRefGoogle Scholar
  121. 121.
    Mronga T, Stahnke T, Goldbaum O, Richter-Landsberg C (2004) Mitochondrial pathway is involved in hydrogen peroxide induced apoptotic cell death of oligodendrocytes. Glia 46:446–455PubMedCrossRefGoogle Scholar
  122. 122.
    Sánchez-Gómez MV, Alberdi E, Ibarretxe G et al (2003) Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J Neurosci 23:9519–9528PubMedGoogle Scholar
  123. 123.
    Wang H, Li J, Follett PL et al (2004) Lipoxygenase plays a key role in cell death caused by glutathione depletion and arachidonic acid in rat oligodendrocytes. Eur J Neurosci 20:2049–2058PubMedCrossRefGoogle Scholar
  124. 124.
    Jellinger KA, Lantos PL (2010) Papp-Lantos inclusions and the pathogenesis of multiple system atrophy: an update. Acta Neuropathol 119:657–667PubMedCrossRefGoogle Scholar
  125. 125.
    Riedel M, Goldbaum O, Schwarz L et al (2010) 17-AAG induces cytoplasmic α-synuclein aggregate clearance by induction of autophagy. PLoS One 18:e8753CrossRefGoogle Scholar
  126. 126.
    Vogiatzi T, Xilouri M, Vekrellis K, Stefanis L (2008) Wild type α-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem 283:23542–23556PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Jellinger KA (2010) Neuropathology in Parkinson’s disease with mild cognitive impairment. Acta Neuropathol 120:829–830PubMedCrossRefGoogle Scholar
  128. 128.
    Pukass K, Richter-Landsberg C (2014) Oxidative stress promotes uptake, accumulation, and oligomerization of extracellular α-synuclein in oligodendrocytes. J Mol Neurosci 52:339–352PubMedCrossRefGoogle Scholar
  129. 129.
    Riedel M, Goldbaum O, Richter-Landsberg C (2009) α-Synuclein promotes the recruitment of tau to protein inclusions in oligodendroglial cells: effects of oxidative and proteolytic stress. J Mol Neurosci 39:226–234PubMedCrossRefGoogle Scholar
  130. 130.
    Bradke F, Dotti CG (1999) The role of local actin instability in axon formation. Science 283:1931–1934PubMedCrossRefGoogle Scholar
  131. 131.
    Wilson C, Nunez MT, Gonzalez-Billault C (2015) Contribution of NADPH-oxidase to the establishment of hippocampal neuronal polarity in culture. J Cell Sci 128:2989–2995PubMedCrossRefGoogle Scholar
  132. 132.
    Wilson C, Gonzalez-Billault C (2015) Regulation of cytoskeletal dynamics by redox signaling and oxidative stress: implications for neuronal development and trafficking. Front Cell Neurosci 9:381. doi: 10.3389/fncel.2015.00381 PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Morinaka A, Yamada M, Itofusa R et al (2011) Thioredoxin mediates oxidation-dependent phosphorylation of CRMP2 and growth cone collapse. Sci Signal 4(170):ra26. doi: 10.1126/scisignal.2001127 PubMedCrossRefGoogle Scholar
  134. 134.
    Casas C, Isus L, Herrando-Grabulosa M et al (2015) Network-based proteomic approaches reveal the neurodegenerative, neuroprotective and pain-related mechanisms involved after retrograde axonal damage. Sci Rep 5:9185. doi: 10.1038/srep09185 PubMedCrossRefGoogle Scholar
  135. 135.
    Quinta HR, Pasquini LA, Pasquini JM (2015) Three-dimensional reconstruction of corticospinal tract using one-photon confocal microscopy acquisition allows detection of axonal disruption in spinal cord injury. J Neurochem 133:113–124PubMedCrossRefGoogle Scholar
  136. 136.
    Pasterkamp RJ, Anderson PN, Verhaagen J (2001) Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent semaphorin 3. Eur J Neurosci 13:457–471PubMedCrossRefGoogle Scholar
  137. 137.
    Pasterkamp RJ, Giger RJ, Ruitenberg MJ et al (1999) Expression of the gene encoding the chemorepellent semaphorin 3 is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol Cell Neurosci 13:143–166PubMedCrossRefGoogle Scholar
  138. 138.
    Kolodkin AL, Matthes DJ, Goodman CS (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389–1399PubMedCrossRefGoogle Scholar
  139. 139.
    Quinta HR, Pasquini JM, Rabinovich GA, Pasquini LA (2014) Glycan-dependent binding of galectin-1 to neuropilin-1 promotes axonal regeneration after spinal cord injury. Cell Death Differ 21:941–955PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Quinta HR, Pasquini JM, Rabinovich GA, Pasquini LA (2014) Axonal regeneration in spinal cord injury: key role of galectin-1. Medicina (Buenos Aires) 74:321–325Google Scholar
  141. 141.
    De Winter F, Oudega M, Lankhorst AJ et al (2002) Injury-induced class 3 semaphorin expression in the rat spinal cord. Exp Neurol 175:61–75PubMedCrossRefGoogle Scholar
  142. 142.
    Giridharan SS, Caplan S (2014) MICAL-family proteins: complex regulators of the actin cytoskeleton. Antioxid Redox Signal 20:2059–2073PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Hung RJ, Terman JR (2011) Extracellular inhibitors, repellents, and semaphorin/plexin/MICAL-mediated actin filament disassembly. Cytoskeleton (Hoboken) 68:415–433Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Juana M. Pasquini
    • 1
    Email author
  • Laura A. Pasquini
    • 1
  • Hector R. Quintá
    • 1
  1. 1.Departamento de Química Biológica and Instituto de Química y Fisicoquímica Biológica (IQUIFIB, UBA-CONICET), Facultad de Farmacia y BioquímicaUniversidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations