How microglia kill neurons

Brain Research

Volumn 1628, Issue , 2015, Pages 288-297

  Brown, Guy C ^a   Vilalta, Anna ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cell death; Inflammation; Neurodegeneration; Neurotoxicity; Nitric oxide; Phagocytosis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 8; CATHEPSIN B; GLUTAMIC ACID; GLUTAMINASE; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MATRIX METALLOPROTEINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITROUS OXIDE; OXIDIZING AGENT; PEROXYNITRITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SOMATOMEDIN C; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ARTICLE; CELL ACTIVATION; CELL HYPOXIA; CELL STRESS; CYTOKINE RELEASE; ENZYME RELEASE; EXCITOTOXICITY; GLIA; HUMAN; MICROGLIA; MITOCHONDRIAL RESPIRATION; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CELL DEATH; MACROPHAGE; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; CELL DEATH; CYTOKINES; HUMANS; MACROPHAGES; MICROGLIA; NEURONS;

EID: 84952637264     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.08.031     Document Type: Article

References (87)

1. V. Annese, M.T. Herrero, M. Di Pentima, A. Gomez, L. Lombardi, C.M. Ros, V. De Pablos, E. Fernandez Villalba, and M.E. De-Stefano Metalloproteinase-9 contributes to inflammatory glia activation and nigro-striatal pathway degeneration in both mouse and monkey models of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced Parkinsonism Brain Struct. Funct. 220 2015 703 727
2. A. Bal-Price, and G.C. Brown Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity J. Neurosci. 21 2001 6480 6491
3. A. Bal-Price, A. Matthias, and G.C. Brown Stimulation of the NADPH oxidase in activated rat microglia removes nitric oxide but induces peroxynitrite production J. Neurochem. 80 2002 73 80
4. A. Bal-Price, Z. Moneer, and G.C. Brown Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes Glia 40 2002 312 323
5. C. Barcia, and et al. ROCK/Cdc42-mediated microglial motility and gliapse formation lead to phagocytosis of degenerating dopaminergic neurons in vivo Sci. Rep. 2 2012 809
6. K. Biber, T. Owens, and E. Boddeke What is microglia neurotoxicity (Not)? Glia 62 2014 841 854
7. M.L. Block, L. Zecca, and J.S. Hong Microglia-mediated neurotoxicity: uncovering the molecular mechanisms Nat. Rev. Neurosci. 8 2007 57 69
8. D. Boche, V.H. Perry, and J.A. Nicoll Review: activation patterns of microglia and their identification in the human brain Neuropathol. Appl. Neurobiol. 39 2013 3 18
9. G.C. Brown Nitric oxide and neuronal death Nitric Oxide 23 2010 153 165
10. G.C. Brown, and A. Bal-Price Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria Mol. Neurobiol. 27 2003 325 355
11. G.C. Brown, and C.E. Cooper Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase FEBS Lett. 356 1994 295 298
12. G.C. Brown, and J.J. Neher Eaten alive! Cell death by primary phagocytosis: phagoptosis Trends Biochem. Sci. 37 2012 325 332
13. G.C. Brown, and J.J. Neher Microglial phagocytosis of live neurons Nat. Rev. Neurosci. 15 2014 209 216
14. M.J. Brzozowski, P. Jenner, and S. Rose Inhibition of i-NOS but not n-NOS protects rat primary cell cultures against MPP-induced neuronal toxicity J. Neural. Transm. 2014
15. C.C. Chao, S. Hu, L. Ehrlich, and P.K. Peterson Interleukin-1 and tumor necrosis factor-alpha synergistically mediate neurotoxicity: involvement of nitric oxide and of N-methyl-d-aspartate receptors Brain Behav. Immun. 9 1995 355 365
16. C.J. Chen, and et al. Glutamate released by Japanese encephalitis virus-infected microglia involves TNF-alpha signaling and contributes to neuronal death Glia 60 2012 487 501
17. C. Cheret, and et al. Neurotoxic activation of microglia is promoted by a nox1-dependent NADPH oxidase J. Neurosci. 28 2008 12039 12051
18. V. Chhor, and et al. Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro Brain Behav. Immun. 32 2013 70 85
19. S. Cho, and et al. Obligatory role of inducible nitric oxide synthase in ischemic preconditioning J. Cereb. Blood Flow. Metab. 25 2005 493 501
20. S.H. Choi, S. Aid, H.W. Kim, S.H. Jackson, and F. Bosetti Inhibition of NADPH oxidase promotes alternative and anti-inflammatory microglial activation during neuroinflammation J. Neurochem. 120 2012 292 301
21. D.E. Christofferson, Y. Li, and J. Yuan Control of life-or-death decisions by RIP1 kinase Annu. Rev. Physiol. 76 2014 129 150
22. D.J. Clarke, and R.L. Branton A role for tumor necrosis factor alpha in death of dopaminergic neurons following neural transplantation Exp. Neurol. 176 2002 154 162
23. J. Claude, B. Linnartz-Gerlach, A.P. Kudin, W.S. Kunz, and H. Neumann Microglial CD33-related Siglec-E inhibits neurotoxicity by preventing the phagocytosis-associated oxidative burst J. Neurosci. 33 2013 18270 18276
24. C.L. Cunningham, V. Martinez-Cerdeno, and S.C. Noctor Microglia regulate the number of neural precursor cells in the developing cerebral cortex J. Neurosci. 33 2013 4216 4233
25. B. Engelhardt, and R.M. Ransohoff The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms Trends Immunol. 26 2005 485 495
26. N. Erdmann, and et al. In vitro glutaminase regulation and mechanisms of glutamate generation in HIV-1-infected macrophage J. Neurochem. 109 2009 551 561
27. M. Fricker, and et al. MFG-E8 mediates primary phagocytosis of viable neurons during neuroinflammation J. Neurosci. 32 2012 2657 2666
28. L. Gan, and et al. Identification of cathepsin B as a mediator of neuronal death induced by Abeta-activated microglial cells using a functional genomics approach J. Biol. Chem. 279 2004 5565 5572
29. C.K. Glass, K. Saijo, B. Winner, M.C. Marchetto, and F.H. Gage Mechanisms underlying inflammation in neurodegeneration Cell 140 2010 918 934
30. S. Golde, S. Chandran, G.C. Brown, and A. Compston Different pathways for iNOS-mediated toxicity in vitro dependent on neuronal maturation and NMDA receptor expression J. Neurochem. 82 2002 269 282
31. H.S. Han, Y. Qiao, M. Karabiyikoglu, R.G. Giffard, and M.A. Yenari Influence of mild hypothermia on inducible nitric oxide synthase expression and reactive nitrogen production in experimental stroke and inflammation J. Neurosci. 22 2002 3921 3928
32. U.K. Hanisch, and H. Kettenmann Microglia: active sensor and versatile effector cells in the normal and pathologic brain Nat. Neurosci. 10 2007 1387 1394
33. M.S. Hernandes, and et al. Microglial cells are involved in the susceptibility of NADPH oxidase knockout mice to 6-hydroxy-dopamine-induced neurodegeneration PLoS ONE 8 2013 e75532
34. T.C. Hornik, U. Neniskyte, and G.C. Brown Inflammation induces multinucleation of Microglia via PKC inhibition of cytokinesis, generating highly phagocytic multinucleated giant cells J. Neurochem. 128 2014 650 661
35. Y. Huang, and et al. Glutaminase dysregulation in HIV-1-infected human microglia mediates neurotoxicity: relevant to HIV-1-associated neurocognitive disorders J. Neurosci. 31 2011 15195 15204
36. A. Jekabsone, P.K. Mander, A. Tickler, M. Sharpe, and G.C. Brown Fibrillar beta-amyloid peptide Abeta1-40 activates microglial proliferation via stimulating TNF-alpha release and H2O2 derived from NADPH oxidase: a cell culture study J. Neuroinflamm. 3 2006 24
37. A. Jekabsone, J.J. Neher, V. Borutaite, and G.C. Brown Nitric oxide from neuronal nitric oxide synthase sensitises neurons to hypoxia-induced death via competitive inhibition of cytochrome oxidase J. Neurochem. 103 2007 346 356
38. A.W. Kao, and et al. A neurodegenerative disease mutation that accelerates the clearance of apoptotic cells Proc. Natl. Acad. Sci. USA 108 2011 4441 4446
39. S. Kim, and et al. Neurotoxicity of microglial cathepsin D revealed by secretome analysis J. Neurochem. 103 2007 2640 2650
40. P.J. Kingham, and J.M. Pocock Microglial secreted cathepsin B induces neuronal apoptosis J. Neurochem. 76 2001 1475 1484
41. A. Kinsner, and et al. Highly purified lipoteichoic acid induced pro-inflammatory signalling in primary culture of rat microglia through Toll-like receptor 2: selective potentiation of nitric oxide production by muramyl dipeptide J. Neurochem. 99 2006 596 607
42. A. Klegeris, E.G. McGeer, and P.L. McGeer Therapeutic approaches to inflammation in neurodegenerative disease Curr. Opin. Neurol. 20 2007 351 357
43. A.D. Kraft, C.A. McPherson, and G.J. Harry Heterogeneity of microglia and TNF signaling as determinants for neuronal death or survival Neurotoxicology 30 2009 785 793
44. C.C. Leonardo, A.A. Hall, L.A. Collier, P.E. Gottschall, and K.R. Pennypacker Inhibition of gelatinase activity reduces neural injury in an ex vivo model of hypoxia-ischemia Neuroscience 160 2009 755 766
45. G. Liu, and et al. Neuronal phagocytosis by inflammatory macrophages in ALS spinal cord: inhibition of inflammation by resolvin D1 Am. J. Neurodegener. Dis. 1 2012 60 74
46. S. Liu, and et al. Necroptosis mediates TNF-induced toxicity of hippocampal neurons Biomed. Res. Int. 2014 2014 290182
47. S.M. Lucas, N.J. Rothwell, and R.M. Gibson The role of inflammation in CNS injury and disease Br. J. Pharmacol. 147 Suppl. 1 2006 S232 S240
48. I. Maezawa, and L.W. Jin Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate J. Neurosci. 30 2010 5346 5356
49. P. Mander, and G.C. Brown Activation of microglial NADPH oxidase is synergistic with glial iNOS expression in inducing neuronal death: a dual-key mechanism of inflammatory neurodegeneration J. Neuroinflamm. 2 2005 20
50. P. Mander, V. Borutaite, S. Moncada, and G.C. Brown Nitric oxide from inflammatory-activated glia synergizes with hypoxia to induce neuronal death J. Neurosci. Res. 79 2005 208 215
51. P.K. Mander, A. Jekabsone, and G.C. Brown Microglia proliferation is regulated by hydrogen peroxide from NADPH oxidase J. Immunol. 176 2006 1046 1052
52. J.L. Marin-Teva, and et al. Microglia promote the death of developing Purkinje cells Neuron 41 2004 535 547
53. D.F. Marker, and et al. LRRK2 kinase inhibition prevents pathological microglial phagocytosis in response to HIV-1 Tat protein J. Neuroinflamm. 9 2012 261
54. F.O. Martinez, and S. Gordon The M1 and M2 paradigm of macrophage activation: time for reassessment F1000Prime Rep. 6 2014 13
55. M.K. McCoy, and M.G. Tansey TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease J. Neuroinflamm. 5 2008 45
56. S.O. McGuire, and et al. Tumor necrosis factor alpha is toxic to embryonic mesencephalic dopamine neurons Exp. Neurol. 169 2001 219 230
57. E.N. McNamee, K.M. Ryan, D. Kilroy, and T.J. Connor Noradrenaline induces IL-1ra and IL-1 type II receptor expression in primary glial cells and protects against IL-1beta-induced neurotoxicity Eur. J. Pharmacol. 626 2010 219 228
58. K.S. McNaught, and G.C. Brown Nitric oxide causes glutamate release from brain synaptosomes J. Neurochem. 70 1998 1541 1546
59. S. Murphy Production of nitric oxide by glial cells: regulation and potential roles in the CNS Glia 29 2000 1 13
60. J.J. Neher, and et al. Inhibition of microglial phagocytosis is sufficient to prevent inflammatory neuronal death J. Immunol. 186 2011 4973 4983
61. J.J. Neher, and et al. Phagocytosis executes delayed neuronal death after focal brain ischemia Proc. Natl. Acad. Sci. USA 110 2013 E4098 E4107
62. U. Neniskyte, and G.C. Brown Lactadherin/MFG-E8 is essential for microglia-mediated neuronal loss and phagoptosis induced by amyloid beta J. Neurochem. 126 2013 312 317
63. U. Neniskyte, J.J. Neher, and G.C. Brown Neuronal death induced by nanomolar amyloid beta is mediated by primary phagocytosis of neurons by microglia J. Biol. Chem. 286 2011 39904 39913
64. U. Neniskyte, A. Vilalta, and G.C. Brown Tumour necrosis factor alpha-induced neuronal loss is mediated by microglial phagocytosis FEBS Lett. 588 2014 2952 2956
65. A. Novelli, J.A. Reilly, P.G. Lysko, and R.C. Henneberry Glutamate becomes neurotoxic via the N-methyl-d-aspartate receptor when intracellular energy levels are reduced Brain Res. 451 1988 205 212
66. R.C. Paolicelli, and et al. Synaptic pruning by microglia is necessary for normal brain development Science 333 2011 1456 1458
67. K.W. Park, H.H. Baik, and B.K. Jin Interleukin-4-induced oxidative stress via microglial NADPH oxidase contributes to the death of hippocampal neurons in vivo Curr. Aging Sci. 1 2008 192 201
68. S. Pawate, Q. Shen, F. Fan, and N.R. Bhat Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma J. Neurosci. Res. 77 2004 540 551
69. V.H. Perry, and C. Holmes Microglial priming in neurodegenerative disease Nat. Rev. Neurol. 10 2014 217 224
70. R.M. Ransohoff, and V.H. Perry Microglial physiology: unique stimuli, specialized responses Annu. Rev. Immunol. 27 2009 119 145
71. F.S. Shie, K.S. Montine, R.M. Breyer, and T.J. Montine Microglial EP2 is critical to neurotoxicity from activated cerebral innate immunity Glia 52 2005 70 77
72. Y. Shigemoto-Mogami, K. Hoshikawa, J.E. Goldman, Y. Sekino, and K. Sato Microglia enhance neurogenesis and oligodendrogenesis in the early postnatal subventricular zone J. Neurosci. 34 2014 2231 2243
73. V.C. Stewart, A.J. Heslegrave, G.C. Brown, J.B. Clark, and S.J. Heales Nitric oxide-dependent damage to neuronal mitochondria involves the NMDA receptor Eur. J. Neurosci. 15 2002 458 464
74. K. Takuma, and et al. Anti-apoptotic effect of cGMP in cultured astrocytes: inhibition by cGMP-dependent protein kinase of mitochondrial permeable transition pore J. Biol. Chem. 276 2001 48093 48099
75. W.Y. Tam, and C.H. Ma Bipolar/rod-shaped microglia are proliferating microglia with distinct M1/M2 phenotypes Sci. Rep. 4 2014 7279
76. D.L. Taylor, F. Jones, E.S. Kubota, and J.M. Pocock Stimulation of microglial metabotropic glutamate receptor mGlu2 triggers tumor necrosis factor alpha-induced neurotoxicity in concert with microglial-derived Fas ligand J. Neurosci. 25 2005 2952 2964
77. A. Valencia, and et al. Elevated NADPH oxidase activity contributes to oxidative stress and cell death in Huntington's disease Hum. Mol. Genet. 22 2013 1112 1131
78. A. Vilalta, and et al. Moderate and severe traumatic brain injury induce early overexpression of systemic and brain gelatinases Intensiv. Care Med. 34 2008 1384 1392
79. A. Vilalta, and et al. Brain contusions induce a strong local overexpression of MMP-9. Results of a pilot study Acta Neurochir. Suppl. 102 2008 415 419
80. S. Wakselman, and et al. Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor J. Neurosci. 28 2008 8138 8143
81. T. Wyss-Coray Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat. Med. 12 2006 1005 1015
82. L. Ye, and et al. IL-1beta and TNF-alpha induce neurotoxicity through glutamate production: a potential role for neuronal glutaminase J. Neurochem. 125 2013 897 908
83. H. Yoshioka, and et al. NADPH oxidase mediates striatal neuronal injury after transient global cerebral ischemia J. Cereb. Blood Flow Metab. 31 2011 868 880
84. H. Zeng, M. Ding, X.X. Chen, and Q. Lu Microglial NADPH oxidase activation mediates rod cell death in the retinal degeneration in rd mice Neuroscience 275 2014 54 61
85. L. Zhao, M.K. Zabel, X. Wang, W. Ma, P. Shah, R.N. Fariss, H. Qian, C.N. Parkhurst, W.B. Gan, and W.T. Wong Microglial phagocytosis of living photoreceptors contributes to inherited retinal degeneration EMBO Mol Med. 7 2015 1179 1197
86. F. Zipp, and O. Aktas The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases Trends Neurosci. 29 2006 518 527
87. G.J. del Zoppo, and et al. Microglial cell activation is a source of metalloproteinase generation during hemorrhagic transformation J. Cereb. Blood Flow Metab. 32 2012 919 932