Rat cerebellar slice cultures exposed to bilirubin evidence reactive gliosis, excitotoxicity and impaired myelinogenesis that is prevented by AMPA and TNF-α inhibitors

Molecular Neurobiology

Volumn 49, Issue 1, 2014, Pages 424-439

  Barateiro, Andreia ^a   Domingues, Helena Sofia ^b   Fernandes, Adelaide ^a   Relvas, João Bettencourt ^b   Brites, Dora ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

Astrocytes; Cerebellar slice culture; Microglia; Myelination; Oligodendrocytes; Unconjugated bilirubin

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; BILIRUBIN; GLUTAMIC ACID; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MYELIN BASIC PROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 1; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN S100B; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ASTROCYTE; ASTROCYTOSIS; BRAIN SLICE; CELL MATURATION; CEREBELLUM; CONTROLLED STUDY; CYTOKINE RELEASE; ENCEPHALITIS; EXCITOTOXICITY; EXPOSURE; GENE EXPRESSION; GLIA CELL; GLIOSIS; HYPERBILIRUBINEMIA; MICROGLIA; MYELINATED NERVE; MYELINATION; NEUROTRANSMITTER RELEASE; NEWBORN JAUNDICE; NONHUMAN; OLIGODENDROGLIA; RAT; REVIEW;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; BILIRUBIN; CELL DIFFERENTIATION; CEREBELLUM; GLIOSIS; MYELIN SHEATH; NERVE FIBERS, MYELINATED; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, AMPA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84894373448     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8530-7     Document Type: Review

References (94)

1. Cohen RS, Wong RJ, Stevenson DK (2010) Understanding neonatal jaundice: a perspective on causation. Pediatr Neonatol 51(3):143-148. doi: 10.1016/S1875-9572(10)60027-7
2. Kaplan M, Muraca M, Hammerman C, Rubaltelli FF, Vilei MT, Vreman HJ, Stevenson DK (2002) Imbalance between production and conjugation of bilirubin: a fundamental concept in the mechanism of neonatal jaundice. Pediatrics 110(4):e47
3. Bratlid D (1990) How bilirubin gets into the brain. Clin Perinatol 17(2):449-465
4. Brites D (2012) The evolving landscape of neurotoxicity by unconjugated bilirubin: role of glial cells and inflammation. Front Pharmacol 3:88. doi: 10.3389/fphar.2012.00088
5. Hansen TW (2000) Pioneers in the scientific study of neonatal jaundice and kernicterus. Pediatrics 106(2):E15
6. Ahdab-Barmada M, Moossy J (1984) The neuropathology of kernicterus in the premature neonate: diagnostic problems. J Neuropathol Exp Neurol 43(1):45-56
7. Brito MA, Zurolo E, Pereira P, Barroso C, Aronica E, Brites D (2011) Cerebellar axon/myelin loss, angiogenic sprouting, and neuronal increase of vascular endothelial growth factor in a preterm infant with kernicterus. J Child Neurol. doi: 10.1177/0883073811423975
8. Gkoltsiou K, Tzoufi M, Counsell S, Rutherford M, Cowan F (2008) Serial brain MRI and ultrasound findings: relation to gestational age, bilirubin level, neonatal neurologic status and neurodevelopmental outcome in infants at risk of kernicterus. Early Hum Dev 84(12):829-838. doi: 10.1016/j.earlhumdev.2008.09. 008
9. Hanko E, Hansen TW, Almaas R, Paulsen R, Rootwelt T (2006) Synergistic protection of a general caspase inhibitor and MK-801 in bilirubin-induced cell death in human NT2-N neurons. Pediatr Res 59(1):72-77. doi: 10.1203/01.pdr. 0000191135.63586.08
10. Silva RF, Rodrigues CM, Brites D (2002) Rat cultured neuronal and glial cells respond differently to toxicity of unconjugated bilirubin. Pediatr Res 51(4):535-541
11. Brites DaB, A (2012) Bilirubin toxicity. In: Stevenson DK MM, Watchko JF (ed) Care of the jaundiced neonate. McGraw-Hill, New York, pp 115-143
12. Fernandes A, Silva RF, Falcao AS, Brito MA, Brites D (2004) Cytokine production, glutamate release and cell death in rat cultured astrocytes treated with unconjugated bilirubin and LPS. J Neuroimmunol 153(1-2):64-75. doi: 10.1016/j.jneuroim.2004.04.007
13. Falcao AS, Fernandes A, Brito MA, Silva RF, Brites D (2006) Bilirubin-induced immunostimulant effects and toxicity vary with neural cell type and maturation state. Acta Neuropathol 112(1):95-105. doi: 10.1007/s00401-006-0078-4
14. Hanko E, Hansen TW, Almaas R, Rootwelt T (2006) Recovery after short-term bilirubin exposure in human NT2-N neurons. Brain Res 1103(1):56-64. doi: 10.1016/j.brainres.2006.05.083
15. Brito MA, Vaz AR, Silva SL, Falcao AS, Fernandes A, Silva RF, Brites D (2010) N-methyl-aspartate receptor and neuronal nitric oxide synthase activation mediate bilirubin-induced neurotoxicity. Mol Med 16(9-10):372-380. doi: 10.2119/molmed.2009.00152
16. Fernandes A, Falcao AS, Silva RF, Gordo AC, Gama MJ, Brito MA, Brites D (2006) Inflammatory signalling pathways involved in astroglial activation by unconjugated bilirubin. J Neurochem 96(6):1667-1679. doi: 10.1111/j.1471-4159. 2006.03680.x
17. Gordo AC, Falcao AS, Fernandes A, Brito MA, Silva RF, Brites D (2006) Unconjugated bilirubin activates and damages microglia. J Neurosci Res 84(1):194-201. doi: 10.1002/jnr.20857
18. Silva SL, Osorio C, Vaz AR, Barateiro A, Falcao AS, Silva RF, Brites D (2011) Dynamics of neuron-glia interplay upon exposure to unconjugated bilirubin. J Neurochem 117(3):412-424. doi: 10.1111/j.1471-4159.2011.07200.x
19. Chang FY, Lee CC, Huang CC, Hsu KS (2009) Unconjugated bilirubin exposure impairs hippocampal long-term synaptic plasticity. PLoS One 4(6):e5876. doi: 10.1371/journal.pone.0005876
20. Shapiro SM (2005) Definition of the clinical spectrum of kernicterus and bilirubin-induced neurologic dysfunction (BIND). J Perinatol 25(1):54-59. doi: 10.1038/sj.jp.7211157
21. Fernandes A, Falcao AS, Abranches E, Bekman E, Henrique D, Lanier LM, Brites D (2009) Bilirubin as a determinant for altered neurogenesis, neuritogenesis, and synaptogenesis. Developmental neurobiology 69(9):568-582. doi: 10.1002/dneu.20727
22. Barateiro A, Vaz AR, Silva SL, Fernandes A, Brites D (2012) ER Stress, Mitochondrial dysfunction and calpain/JNK Activation are involved in oligodendrocyte precursor cell death by unconjugated bilirubin. Neuromolecular Med 14(4):285-302. doi: 10.1007/s12017-012-8187-9
23. Barateiro A, Miron VE, Santos SD, Relvas JB, Fernandes A, Ffrench-Constant C, Brites D (2013) Unconjugated bilirubin restricts oligodendrocyte differentiation and axonal myelination. Mol Neurobiol 47(2):632-644. doi: 10.1007/s12035-012-8364-8
24. Castonguay A, Levesque S, Robitaille R (2001) Glial cells as active partners in synaptic functions. Prog Brain Res 132:227-240. doi: 10.1016/S0079-6123(01)32079-4
25. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6(8):626-640. doi: 10.1038/nrn1722
26. Lai AY, Todd KG (2008) Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 56(3):259-270. doi: 10.1002/glia.20610
27. Ghoumari AM, Ibanez C, El-Etr M, Leclerc P, Eychenne B, O'Malley BW, Baulieu EE, Schumacher M (2003) Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum. J Neurochem 86(4):848-859
28. Kasparov S, Teschemacher AG, Paton JF (2002) Dynamic confocal imaging in acute brain slices and organotypic slice cultures using a spectral confocal microscope with single photon excitation. Exp Physiol 87(6):715-724
29. Bhutani VK, Stevenson DK (2011) The need for technologies to prevent bilirubin-induced neurologic dysfunction syndrome. Semin Perinatol 35(3):97-100. doi: 10.1053/j.semperi.2011.02.002
30. Brito MA, Zurolo E, Pereira P, Barroso C, Aronica E, Brites D (2012) Cerebellar axon/myelin loss, angiogenic sprouting, and neuronal increase of vascular endothelial growth factor in a preterm infant with kernicterus. J Child Neurol 27(5):615-624. doi: 10.1177/0883073811423975
31. Zhang H, Jarjour AA, Boyd A, Williams A (2011) Central nervous system remyelination in culture - a tool for multiple sclerosis research. Exp Neurol 230(1):138-148. doi: 10.1016/j.expneurol.2011.04.009
32. Craig A, Ling Luo N, Beardsley DJ, Wingate-Pearse N, Walker DW, Hohimer AR, Back SA (2003) Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp Neurol 181(2):231-240
33. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109(1):75-86
34. 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):1354-1365. doi: 10.1523/JNEUROSCI.3034-04.2005
35. Copray S, Balasubramaniyan V, Levenga J, de Bruijn J, Liem R, Boddeke E (2006) Olig2 overexpression induces the in vitro differentiation of neural stem cells into mature oligodendrocytes. Stem Cells 24(4):1001-1010. doi: 10.1634/stemcells.2005-0239
36. Buchet D, Baron-Van Evercooren A (2009) In search of human oligodendroglia for myelin repair. Neurosci Lett 456(3):112-119. doi: 10.1016/j.neulet.2008.09.086
37. Nave KA (2010) Myelination and the trophic support of long axons. Nat Rev Neurosci 11(4):275-283. doi: 10.1038/nrn2797
38. Deng W, Rosenberg PA, Volpe JJ, Jensen FE (2003) Calcium-permeable AMPA/kainate receptors mediate toxicity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors. Proc Natl Acad Sci U S A 100(11):6801-6806. doi: 10.1073/pnas.1136624100
39. Itoh T, Beesley J, Itoh A, Cohen AS, Kavanaugh B, Coulter DA, Grinspan JB, Pleasure D (2002) AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 81(2):390-402
40. Rosenberg PA, Dai W, Gan XD, Ali S, Fu J, Back SA, Sanchez RM, Segal MM, Follett PL, Jensen FE, Volpe JJ (2003) Mature myelin basic protein-expressing oligodendrocytes are insensitive to kainate toxicity. J Neurosci Res 71(2):237-245. doi: 10.1002/jnr.10472
41. Li S, Stys PK (2000) Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J Neurosci 20(3):1190-1198
42. De Biase LM, Kang SH, Baxi EG, Fukaya M, Pucak ML, Mishina M, Calabresi PA, Bergles DE (2011) NMDA receptor signaling in oligodendrocyte progenitors is not required for oligodendrogenesis and myelination. J Neurosci 31(35):12650-12662. doi: 10.1523/JNEUROSCI.2455-11.2011
43. McDonagh AF, Assisi F (1972) The ready isomerization of bilirubin IX- in aqueous solution. Biochem J 129(3):797-800
44. Silva SL, Vaz AR, Diogenes MJ, van Rooijen N, Sebastiao AM, Fernandes A, Silva RF, Brites D (2012) Neuritic growth impairment and cell death by unconjugated bilirubin is mediated by NO and glutamate, modulated by microglia, and prevented by glycoursodeoxycholic acid and interleukin-10. Neuropharmacology 62(7):2398-2408. doi: 10.1016/j.neuropharm.2012.02.002
45. Ostrow JD, Pascolo L, Shapiro SM, Tiribelli C (2003) New concepts in bilirubin encephalopathy. Eur J Clin Invest 33(11):988-997
46. Ostrow JD, Pascolo L, Tiribelli C (2003) Reassessment of the unbound concentrations of unconjugated bilirubin in relation to neurotoxicity in vitro. Pediatric research 54(6):926
47. Brito MA, Silva RF, Brites D (2002) Bilirubin induces loss of membrane lipids and exposure of phosphatidylserine in human erythrocytes. Cell Biol Toxicol 18(3):181-192
48. Brito MA, Brondino CD, Moura JJ, Brites D (2001) Effects of bilirubin molecular species on membrane dynamic properties of human erythrocyte membranes: a spin label electron paramagnetic resonance spectroscopy study. Arch Biochem Biophys 387(1):57-65. doi: 10.1006/abbi.2000.2210
49. Ahlfors CE, Wennberg RP, Ostrow JD, Tiribelli C (2009) Unbound (free) bilirubin: improving the paradigm for evaluating neonatal jaundice. Clin Chem 55(7):1288-1299. doi: 10.1373/clinchem.2008.121269
50. Palmela I, Sasaki H, Cardoso FL, Moutinho M, Kim KS, Brites D, Brito MA (2012) Time-dependent dual effects of high levels of unconjugated bilirubin on the human blood-brain barrier lining. Front Cell Neurosci 6:22. doi: 10.3389/fncel.2012.00022
51. Labombarda F, Gonzalez SL, Lima A, Roig P, Guennoun R, Schumacher M, de Nicola AF (2009) Effects of progesterone on oligodendrocyte progenitors, oligodendrocyte transcription factors, and myelin proteins following spinal cord injury. Glia 57(8):884-897. doi: 10.1002/glia.20814
52. Falcao AS, Silva RF, Vaz AR, Silva SL, Fernandes A, Brites D (2013) Cross-talk between neurons and astrocytes in response to bilirubin: early beneficial effects. Neurochem Res 38(3):644-659. doi: 10.1007/s11064-012-0963-2
53. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25(2):317-329
54. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109(1):61-73
55. Dugas JC, Tai YC, Speed TP, Ngai J, Barres BA (2006) Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26(43):10967-10983. doi: 10.1523/JNEUROSCI.2572-06.2006
56. Nicolay DJ, Doucette JR, Nazarali AJ (2007) Transcriptional control of oligodendrogenesis. Glia 55(13):1287-1299. doi: 10.1002/glia.20540
57. Emery B (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330(6005):779-782. doi: 10.1126/science.1190927
58. Jenkins HG, Ikeda H (1992) Tumour necrosis factor causes an increase in axonal transport of protein and demyelination in the mouse optic nerve. J Neurol Sci 108(1):99-104
59. Chen H, Kintner DB, Jones M, Matsuda T, Baba A, Kiedrowski L, Sun D (2007) AMPA-mediated excitotoxicity in oligodendrocytes: role for Na(+)-K(+)-Cl(-) co-transport and reversal of Na(+)/Ca(2+) exchanger. J Neurochem 102(6):1783-1795. doi: 10.1111/j.1471-4159.2007.04638.x
60. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511-533
61. Fields RD (2008) White matter in learning, cognition and psychiatric disorders. Trends Neurosci 31(7):361-370. doi: 10.1016/j.tins.2008.04.001
62. Yang Y, Lewis R, Miller RH (2011) Interactions between oligodendrocyte precursors control the onset of CNS myelination. Dev Biol 350(1):127-138. doi: 10.1016/j.ydbio.2010.11.028
63. Gadea A, Aguirre A, Haydar TF, Gallo V (2009) Endothelin-1 regulates oligodendrocyte development. The Journal of neuroscience: the official journal of the Society for Neuroscience 29(32):10047-10062. doi: 10.1523/JNEUROSCI.0822- 09.2009
64. Johnson L, Bhutani VK (2011) The clinical syndrome of bilirubin-induced neurologic dysfunction. Semin Perinatol 35(3):101-113. doi: 10.1053/j.semperi. 2011.02.003
65. Dean JM, Riddle A, Maire J, Hansen KD, Preston M, Barnes AP, Sherman LS, Back SA (2011) An organotypic slice culture model of chronic white matter injury with maturation arrest of oligodendrocyte progenitors. Mol Neurodegener 6:46. doi: 10.1186/1750-1326-6-46
66. Segovia KN, McClure M, Moravec M, Luo NL, Wan Y, Gong X, Riddle A, Craig A, Struve J, Sherman LS, Back SA (2008) Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury. Ann Neurol 63(4):520-530. doi: 10.1002/ana.21359
67. Cai J, Tuong CM, Zhang Y, Shields CB, Guo G, Fu H, Gozal D (2012) Mouse intermittent hypoxia mimicking apnoea of prematurity: effects on myelinogenesis and axonal maturation. J Pathol 226(3):495-508. doi: 10.1002/path.2980
68. Riddle A, Dean J, Buser JR, Gong X, Maire J, Chen K, Ahmad T, Cai V, Nguyen T, Kroenke CD, Hohimer AR, Back SA (2011) Histopathological correlates of magnetic resonance imaging-defined chronic perinatal white matter injury. Ann Neurol 70(3):493-507. doi: 10.1002/ana.22501
69. Buser JR, Maire J, Riddle A, Gong X, Nguyen T, Nelson K, Luo NL, Ren J, Struve J, Sherman LS, Miller SP, Chau V, Hendson G, Ballabh P, Grafe MR, Back SA (2012) Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 71(1):93-109. doi: 10.1002/ana.22627
70. Ligon KL, Fancy SP, Franklin RJ, Rowitch DH (2006) Olig gene function in CNS development and disease. Glia 54(1):1-10. doi: 10.1002/glia.20273
71. Niu J, Mei F, Wang L, Liu S, Tian Y, Mo W, Li H, Lu QR, Xiao L (2012) Phosphorylated olig1 localizes to the cytosol of oligodendrocytes and promotes membrane expansion and maturation. Glia. doi: 10.1002/glia.22364
72. Liu W, Tang Y, Feng J (2011) Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci 89(5-6):141-146. doi: 10.1016/j.lfs.2011.05.011
73. Biran V, Joly LM, Heron A, Vernet A, Vega C, Mariani J, Renolleau S, Charriaut-Marlangue C (2006) Glial activation in white matter following ischemia in the neonatal P7 rat brain. Exp Neurol 199(1):103-112. doi: 10.1016/j.expneurol.2006.01.037
74. Rostworowski M, Balasingam V, Chabot S, Owens T, Yong VW (1997) Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-gamma. J Neurosci 17(10):3664-3674
75. Rousset CI, Chalon S, Cantagrel S, Bodard S, Andres C, Gressens P, Saliba E (2006) Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 59(3):428-433. doi: 10.1203/01.pdr.0000199905.08848.55
76. Delcour M, Russier M, Amin M, Baud O, Paban V, Barbe MF, Coq JO (2012) Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behav Brain Res 232(1):233-244. doi: 10.1016/j.bbr.2012.03.029
77. Delcour M, Russier M, Xin DL, Massicotte VS, Barbe MF, Coq JO (2011) Mild musculoskeletal and locomotor alterations in adult rats with white matter injury following prenatal ischemia. Int J Dev Neurosci 29(6):593-607. doi: 10.1016/j.ijdevneu.2011.02.010
78. Haynes RL, Folkerth RD, Trachtenberg FL, Volpe JJ, Kinney HC (2009) Nitrosative stress and inducible nitric oxide synthase expression in periventricular leukomalacia. Acta Neuropathol 118(3):391-399. doi: 10.1007/s00401-009-0540-1
79. Kim SU, de Vellis J (2005) Microglia in health and disease. J Neurosci Res 81(3):302-313. doi: 10.1002/jnr.20562
80. Allan SM, Rothwell NJ (2001) Cytokines and acute neurodegeneration. Nat Rev Neurosci 2(10):734-744. doi: 10.1038/35094583
81. Bermpohl D, You Z, Lo EH, Kim HH, Whalen MJ (2007) TNF alpha and Fas mediate tissue damage and functional outcome after traumatic brain injury in mice. J Cereb Blood Flow Metab 27(11):1806-1818. doi: 10.1038/sj.jcbfm.9600487
82. Silva SL, Vaz AR, Barateiro A, Falcao AS, Fernandes A, Brito MA, Silva RF, Brites D (2010) Features of bilirubin-induced reactive microglia: from phagocytosis to inflammation. Neurobiol Dis 40(3):663-675. doi: 10.1016/j.nbd.2010.08.010
83. Pang Y, Zheng B, Kimberly SL, Cai Z, Rhodes PG, Lin RC (2012) Neuron-oligodendrocyte myelination co-culture derived from embryonic rat spinal cord and cerebral cortex. Brain Behav 2(1):53-67. doi: 10.1002/brb3.33
84. Pang Y, Cai Z, Rhodes PG (2003) Disturbance of oligodendrocyte development, hypomyelination and white matter injury in the neonatal rat brain after intracerebral injection of lipopolysaccharide. Brain Res Dev Brain Res 140(2):205-214
85. Huleihel M, Golan H, Hallak M (2004) Intrauterine infection/inflammation during pregnancy and offspring brain damages: possible mechanisms involved. Reprod Biol Endocrinol 2:17. doi: 10.1186/1477-7827-2-17
86. Beattie MS, Ferguson AR, Bresnahan JC (2010) AMPA-receptor trafficking and injury-induced cell death. Eur J Neurosci 32(2):290-297. doi: 10.1111/j.1460-9568.2010.07343.x
87. Bittigau P, Sifringer M, Pohl D, Stadthaus D, Ishimaru M, Shimizu H, Ikeda M, Lang D, Speer A, Olney JW, Ikonomidou C (1999) Apoptotic neurodegeneration following trauma is markedly enhanced in the immature brain. Ann Neurol 45(6):724-735
88. Silverstein FS, Buchanan K, Johnston MV (1986) Perinatal hypoxia-ischemia disrupts striatal high-affinity [3H]glutamate uptake into synaptosomes. J Neurochem 47(5):1614-1619
89. + channel block. J Neurosci 16(8):2659-2670
90. Yuan X, Eisen AM, McBain CJ, Gallo V (1998) A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125(15):2901-2914
91. Roseth S, Hansen TW, Fonnum F, Walaas SI (1998) Bilirubin inhibits transport of neurotransmitters in synaptic vesicles. Pediatr Res 44(3):312-316
92. Silva R, Mata LR, Gulbenkian S, Brito MA, Tiribelli C, Brites D (1999) Inhibition of glutamate uptake by unconjugated bilirubin in cultured cortical rat astrocytes: role of concentration and pH. Biochem Biophys Res Commun 265(1):67-72. doi: 10.1006/bbrc.1999.1646
93. Park E, Velumian AA, Fehlings MG (2004) The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J Neurotrauma 21(6):754-774. doi: 10.1089/0897715041269641
94. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE (2000) NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 20(24):9235-9241