Antenatal bacterial endotoxin sensitizes the immature rat brain to postnatal excitotoxic injury

Journal of Neuropathology and Experimental Neurology

Volumn 67, Issue 10, 2008, Pages 994-1000

  Rousset, Catherine I ^a,b   Kassem, Jinane ^a   Olivier, Paul ^a,c   Chalon, Sylvie ^a,b   Gressens, Pierre ^a,c,d   Saliba, Elie ^a,b,e  

^a INSERM   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d HÔPITAL ROBERT DEBRÉ   (France)

^e Centre de Pediatrie Clocheville   (France)

Author keywords

Brain development; Cerebral palsy; Excitotoxicity; Ibotenate; Lipopolysaccharide; Periventricular leukomalacia; White matter injury

Indexed keywords

ENDOTOXIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IBOTENIC ACID; AMINO ACID RECEPTOR STIMULATING AGENT; CD11B ANTIGEN; ENDOTOXIN, ESCHERICHIA COLI; GLIAL FIBRILLARY ACIDIC PROTEIN; LIPOPOLYSACCHARIDE; MYELIN BASIC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOSIS; BRAIN CORTEX LESION; BRAIN INJURY; CENTRAL NERVOUS SYSTEM; CEREBRAL PALSY; CONTROLLED STUDY; ENCEPHALITIS; EXCITOTOXICITY; EXPOSURE; FEMALE; HEMISPHERE; IMMUNITY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROGLIA; MYELINATION; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PERINATAL PERIOD; PREGNANCY; PREMATURITY; PRENATAL DEVELOPMENT; PRENATAL PERIOD; PRIORITY JOURNAL; PROGENY; RAT; STAINING; WHITE MATTER; ANIMAL; BRAIN; DRUG EFFECT; GLIOSIS; METABOLISM; MYELIN SHEATH; NERVE FIBER; PATHOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD11B; BRAIN; ENDOTOXINS; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; IBOTENIC ACID; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; MICROGLIA; MYELIN BASIC PROTEINS; MYELIN SHEATH; NERVE FIBERS; PREGNANCY; RATS; RATS, WISTAR;

EID: 54449086624     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31818894a1     Document Type: Article

References (40)

1. Yoon BH, Romero R, Kim CJ, et al. High expression of tumor necrosis factor-alpha and interleukin-6 in periventricular leukomalacia. Am J Obstet Gynecol 1997;177:406-411
2. Yoon BH, Romero R, Yang SH, et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 1996;174:1433-1440
3. Khadim H, Tabarki B, Verellen G, et al. Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology 2001;56: 1278-1284
4. Cai Z, Pan ZI, Pang Y, et al. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res 2000;47:64-72
5. Debillon T, Gras-Leguen C, Verielle V, et al. Intrauterine infection induces programmed cell death in rabbit periventricular white matter. Pediatr Res 2000;47:736-742
6. Mallard C, Welin AK, Peebles D, et al. White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res 2003;28:215-223
7. Rousset CI, Chalon S, Cantagrel S, et al. Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 2006;59: 428-433
8. Wang X, Rousset CI, Hagberg H, et al. Lipopolysaccharide-induced inflammation and perinatal brain injury. Semin Fetal Neonatal Med 2006;11:343-353
9. Marret S, Mukendi R, Gadisseux JF, et al. Effect of ibotenate on brain development: An excitotoxic mouse model of microgyria and post-hypoxic-like lesions. J Neuropathol Exp Neurol 1995;54:358-370
10. Loeliger M, Watson CS, Reynolds JD, et al. Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep. Neurosci 2003; 116:705-714
11. Chao CC, Hu S. Tumor necrosis factor-alpha potentiates glutamate neurotoxicity in human fetal brain cell cultures. Dev Neurosci 1994;16:172-179
12. Dommergues MA, Patkai J, Renauld JC, et al. Proinflammatory cytokines and interleukin-9 exacerbate excitotoxic lesions of the newborn murine neopallium. Ann Neurol 2000;47:53-63
13. Oakden E, Chiswick M, Rothwell N, et al. The influence of litter size on brain damage caused by hypoxic-ischemic injury in the neonatal rat. Pediatr Res 2002;52:692-696
14. Husson I, Mesples B, Bac P, et al. Melatoninergic neuroprotection of the murine periventricular white matter against neonatal excitotoxic challenge. Ann Neurol 2002;51:82-92
15. Paxinos G, Watson G. The Rat Brain in Stereotaxis Coordinates. New York, NY: Academic Press, 1986
16. Raisman-Vozari R, Hirsch E, Javoy-Agid F, et al. Quantitative auto-radiography of tyrosine hydroxylase immunoreactivity in the rat brain. J Neurochem 1991;57:1212-1222
17. Billiards SS, Haynes RI, Folkerth RD, et al. Development of microglia in the cerebral white matter of the human fetus and infant. J Comp Neurol 2006;497:199-208
18. Tilleux S, Hermans E. Neuroinflammation and regulation of glial glutamate uptake in neurological disorders. J Neurosci Res 2007;85: 2059-2070
19. Tanaka S, Ide M, Shibutani T, et al. Lipopolysaccharide-induced microglial activation induces learning and memory deficits without neuronal cell death in rats. J Neurosci Res 2006;83:557-566
20. Willard LB, Hauss-Wegrzyniak B, Danysz W, et al. The cytotoxicity of chronic neuroinflammation upon basal forebrain cholinergic neurons of rats can be attenuated by glutamatergic antagonism or cyclooxygenase-2 inhibition. Exp Brain Res 2000;134:58-65
21. Lehnardt S, Massillon L, Follett P, et al. Activation of innate immunity in the CNS triggers neurodegeneration through a toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 2003;100: 8514-8519
22. Persson M, Brantefjord M, Hansson E, et al. Lipopolysaccharide increases microglial GLT-1 expression and glutamate uptake capacity in vitro by a mechanism dependent on TNF->. Glia 2005;51:111-120
23. Saliba E, Marret S. Cerebral white matter damage in the preterm infant: Pathophysiology and risk factors. Semin Neonatol 2001;6:121-133
24. Mesplès B, Plaisant F, Fontaine RH, et al. Pathophysiology of neonatal brain lesions: Lessons from animal models of excitotoxicity. Acta Paediatr 2005;94:185-190
25. Tahraoui SL, Marret S, Bodenant C, et al. Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 2001;11:56-71
26. Dommergues MA, Plaisant F, Verney C, et al. Early microglial activation following neonatal excitotoxic brain damage in mice: A potential target for neuroprotection. Neuroscience 2003;121:619-628
27. Piani D, Spranger M, Frei K, et al. Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur J Immunol 1992;22:2429-2436
28. Wood PL. Microglia as a unique cellular target in the treatment of stroke: Potential neurotoxic mediators produced by activated microglia. Neurol Res 1995;17:242-248
29. Sen E, Levison SW. Astrocytes and developmental white matter disorders. MRDD Res Rev 2006;132:97-104
30. Deguchi K, Oguchi K, Takashima S. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr Neurol 1997; 16:296-300
31. Gilles FH, Murphy SF. Perinatal telencephalic leucoencephalopathy. J Neurol Neurosurg Psychiatry 1969;32:404-413
32. 2+ influx at a key point in white matter development. J Neuropathol Exp Neurol 2004; 63:856-871
33. Wilke S, Thomas R, Allcock N, et al. Mechanism of acute ischemic injury of oligodendroglia in early myelinating white matter: The importance of astrocyte injury and glutamate release. J Neuropathol Exp Neurol 2004;63:872-881
34. Fern R. Intracellular calcium and cell death during ischemia in neonatal rat white matter astrocytes in situ. J Neurosci 1998;18:7232-7243
35. Back SA, Luo NL, Mallinson RA, et al. Selective vulnerability of preterm white matter to oxidative damage defined by F2-isoprostanes. Ann Neurol 2005;58:108-120
36. Merill JE. Effects of interleukin-1 and tumor necrosis factor-alpha on astrocytes, microglia, oligodendrocytes, and glial precursors in vitro. Dev Neurosci 1991;13:130-137
37. Vartanian T, Li Y, Zhao M, et al. Interferon-gamma-induced oligoden-drocyte cell death: Implications for the pathogenesis of multiple sclerosis. Mol Med 1995;1:732-743
38. Back SA, Gan X, Li Y, et al. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 1998;18:6241-6253
39. Itoh T, Beesley J, Itoh A, et al. AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 2002;81:390-402
40. Salter MG, Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 2005;438: 1167-1171