Lipopolysaccharide-activated microglia induce death of oligodendrocyte progenitor cells and impede their development

Neuroscience

Volumn 166, Issue 2, 2010, Pages 464-475

  Pang, Y ^a   Campbell, L ^a   Zheng, B ^a   Fan, L ^a   Cai, Z ^a   Rhodes, P ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokine; Myelin; Nitric oxide; Reactive oxygen species; TNF

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CYTOKINE; LIPOPOLYSACCHARIDE; MYELIN BASIC PROTEIN; N(G) NITROARGININE METHYL ESTER; NERVE GROWTH FACTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DAMAGE; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; MICROGLIA; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; WHITE MATTER; ANALYSIS OF VARIANCE; ANIMAL; CELL CULTURE; CELL LINEAGE; CELL SURVIVAL; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; MYELINATED NERVE; STEM CELL; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; CELL SURVIVAL; CELLS, CULTURED; CILIARY NEUROTROPHIC FACTOR; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR I; LIPOPOLYSACCHARIDES; MICROGLIA; NERVE FIBERS, MYELINATED; NERVE GROWTH FACTOR; NITRIC OXIDE; OLIGODENDROGLIA; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; STEM CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77951930197     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.12.040     Document Type: Article

References (36)

1. Bal-Price A, Brown GC (2001) Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and exicitotoxicity. J Neurosci 21:6480-6491.
2. Barger SW, Basile AS (2001) Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J Neurochem 76:846-854.
3. Barres BA, Schmid R, Sendnter M, Raff MC (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118:283-295.
4. Baud O, Li J, Zhang Y, Neve RL, Volpe JJ, Rosenberg PA (2004) Nitric oxide-induced cell death in developing oligodendrocytes is associated with mitochondrial dysfunction and apoptosis-inducing factor translocation. Eur J Neurosci 20:1713-1726.
5. Billiards SS, Haynes RL, Folkerth RD, Borenstein NS, Trachtenberg FL, Rowitch DH, Ligon KL, Volpe JJ, Kinney HC (2008) Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia. Brain Pathol 18:153-163.
6. Cai Z, Pan ZL, Pang Y, Evans OB, Rhodes PG (2000) Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res 47: 64-72.
7. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758.
8. Domercq M, Sánchez-Gómez MV, Sherwin C, Etxebarria E, Fern R, Matute C (2007) System xc- and glutamate transporter inhibition mediates microglial toxicity to oligodendrocytes. J Immunol 178:6549-6556.
9. Facchinetti F, Del Giudice E, Furegato S, Passarotto M, Leon A (2003) Cannabinoids ablate release of TNF-alpha in rat microglial cells stimulated with lipopolysaccharide. Glia 41:161-168.
10. Follett PL, Deng W, Dai W, Talos DM, Massillon LJ, Rosenberg PA, Volpe JJ, Jensen FE (2004) Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci 24:4412-4420.
11. Fragoso G, Martínez-Bermúdez AK, Liu HN, Khorchid A, Chemtob S, Mushynski WE, Almazan G (2004) Developmental differences in HO-induced oligodendrocyte cell death: role of glutathione, mitogen-activated protein kinases and caspase 3. J Neurochem 90:392-404.
12. Gilles FH, Leviton A, Kerr CS (1976) Endotoxin leucoencephalopathy in the telencephalon of the newborn kitten. J Neurol Sci 27:183-191.
13. Grether JK, Nelson KB (1997) Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 278:207-211.
14. Haynes RL, Folkerth RD, Keefe RJ, Sung I, Swzeda LI, Rosenberg PA, Volpe JJ, Kinney HC (2003) Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 62:441-450.
15. Horiuchi M, Itoh A, Pleasure D, Itoh T (2006) MEK-ERK signaling is involved in interferon-gamma-induced death of oligodendroglial progenitor cells. J Biol Chem 281:20095-20106.
16. Huleihel M, Golan H, Hallak M (2004) Intrauterine infection/inflammation during pregnancy and offspring brain damages: possible mechanisms involved. Reprod Biol Endocrinol 2:17.
17. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, Rosenberg PA, Volpe JJ, Vartanian T (2002) The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 22:2478-2486.
18. Leviton A, Gilles F (1996) Ventriculomegaly, delayed myelination, white matter hypoplasia, and "periventricular" leukomalacia: how are they related? Pediatr Neurol 15:127-136
19. Li J, Baud O, Vartanian T, Volpe JJ, Rosenberg PA (2005) Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc Natl Acad Sci U S A 102:9936-9941.
20. Miller BA, Crum JM, Tovar CA, Ferguson AR, Bresnahan JC, Beattie MS (2007) Developmental stage of oligodendrocytes determines their response to activated microglia in vitro. J Neuroinflammation 4:28.
21. Minghetti L (2005) Role of inflammation in neurodegenerative diseases. Curr Opin Neurol 18:315-321.
22. Nakajima K, Kohsaka S (2004) Microglia: neuroprotective and neurotrophic cells in the central nervous system. Curr Drug Targets Cardiovasc Haematol Disord 4:65-84.
23. Nakamura Y, Si QS, Kataoka K (1999) Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci Res 35:95-100.
24. Palacios N, Sánchez-Franco F, Fernández M, Sánchez I, Cacicedo L (2005) Intracellular events mediating insulin-like growth factor I-induced oligodendrocyte development: modulation by cyclic AMP. J Neurochem 95:1091-1107.
25. Pang Y, Cai Z, Rhodes PG (2000) Effects of lipopolysaccharide on oligodendrocyte progenitor cells are mediated by astrocytes and microglia. J Neurosci Res 62:510-520.
26. 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 140:205-214.
27. Pang Y, Cai Z, Rhodes G (2005) Effect of tumor necrosis factor-alpha on developing optic nerve oligodendrocyte in culture. J Neurosci Res 15:226-234.
28. Petratos S, Gonzales MF, Azari MF, Marriott M, Minichiello RA, Shipham KA, Profyris C, Nicolaou A, Boyle K, Cheema SS, Kilpatrick TJ (2004) Expression of the low-affinity neurotrophin receptor, p75(NTR), is upregulated by oligodendroglial progenitors adjacent to the subventricular zone in response to demyelination. Glia 48:64-75.
29. Rezaie P, Dean A (2002) Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology 22:106-132.
30. Sanvicens N, Gómez-Vicente V, Messeguer A, Cotter TG (2006) The radical scavenger CR-6 protects SH-SY5Y neuroblastoma cells from oxidative stress-induced apoptosis: effect on survival pathways. J Neurochem 98:735-747.
31. Scurlock B, Dawson G (1999) Differential responses of oligodendrocytes to tumor necrosis factor and other pro-apoptotic agents: role of ceramide in apoptosis. J Neurosci Res 55:514-522.
32. 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 63:520-530.
33. Sherwin C, Fern R (2005) Acute lipopolysaccharide-mediated injury in neonatal white matter glia: role of TNF-alpha, IL-1beta, and calcium. J Immunol 175:155-161.
34. Talbott JF, Cao Q, Bertram J, Nkansah M, Benton RL, Lavik E, Whittemore SR (2007) CNTF promotes the survival and differentiation of adult spinal cord-derived oligodendrocyte precursor cells in vitro but fails to promote remyelination in vivo. Exp Neurol 204:485-489.
35. Uehara T, Kikuchi Y, Nomura Y (1999) Caspase activation accompanying cytochrome c release from mitochondria is possibly involved in nitric oxide-induced neuronal apoptosis in SH-SY5Y cells. J Neurochem 72:196-205.
36. Yune TY, Lee JY, Jung GY, Kim SJ, Jiang MH, Kim YC, Oh YJ, Markelonis GJ, Oh TH (2007) Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J Neurosci 27: 7751-7761.