Inflammatory responses are not sufficient to cause delayed neuronal death in ATP-induced acute brain injury

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Jeong, Hey Kyeong ^a   Ji, Kyung Min ^a   Kim, Beomsue ^a   Kim, Jun ^a   Jou, Ilo ^a   Joe, Eun Hye ^a  

^a Ajou University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD45 ANTIGEN; CD68 ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; IONIZED CALCIUM BINDING ADAPTER MOLECULE 1; MEMBRANE PROTEIN; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; PRIMER DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL ACTIVATION; CELL INFILTRATION; CELL STRUCTURE; CONTROLLED STUDY; DISEASE COURSE; DOPAMINERGIC NERVE CELL; ELECTRON MICROSCOPY; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFLAMMATION; MICROGLIA; MONOCYTE; NERVE CELL NECROSIS; NONHUMAN; PHAGOCYTOSIS; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEREOMETRY; SUBSTANTIA NIGRA; ANIMAL; CELL DEATH; NUCLEOTIDE SEQUENCE; PATHOLOGY;

RATTUS;

ADENOSINE TRIPHOSPHATE; ANIMALS; BASE SEQUENCE; BRAIN INJURIES; CELL DEATH; DNA PRIMERS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROSCOPY, ELECTRON; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78149456920     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013756     Document Type: Article

References (62)

1. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK (1992) Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 149: 2736-2741.
2. Giulian D, Corpuz M, Chapman S, Mansouri M, Robertson C (1993) Reactive mononuclear phagocytes release neurotoxins after ischemic and traumatic injury to the central nervous system. J Neurosci Res 36: 681-693.
3. Kitamura Y, Takahashi H, Matsuoka Y, Tooyama I, Kimura H, et al. (1996) In vivo induction of inducible nitric oxide synthase by microinjection with interferon-gamma and lipopolysaccharide in rat hippocampus. Glia 18: 233-243.
4. de Bock F, Derijard B, Dornand J, Bockaert J, Rondouin G (1998) The neuronal death induced by endotoxic shock but not that induced by excitatory amino acids requires TNF-alpha. Eur J Neurosci 10: 3107-3114.
5. Scali C, Prosperi C, Vannucchi MG, Pepeu G, Casamenti F (2000) Brain inflammatory reaction in an animal model of neuronal degeneration and its modulation by an anti-inflammatory drug: implication in Alzheimer's disease. Eur J Neurosci 12: 1900-1912.
6. Choi SH, Joe EH, Kim SU, Jin BK (2003) Thrombin-induced microglial activation produces degeneration of nigral dopaminergic neurons in vivo. J Neurosci 23: 5877-5886.
7. Ryu JK, Franciosi S, Sattayaprasert P, Kim SU, McLarnon JG (2004) Minocycline inhibits neuronal death and glial activation induced by beta-amyloid peptide in rat hippocampus. Glia 48: 85-90.
8. Kaushal V, Schlichter LC (2008) Mechanisms of microglia-mediated neurotox-icity in a new model of the stroke penumbra. J Neurosci 28: 2221-2230.
9. Hallenbeck JM, Dutka AJ, Tanishima T, Kochanek PM, Kumaroo KK, et al. (1986) Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke 17: 246-253.
10. Schoettle RJ, Kochanek PM, Magargee MJ, Uhl MW, Nemoto EM (1990) Early polymorphonuclear leukocyte accumulation correlates with the development of posttraumatic cerebral edema in rats. J Neurotrauma 7: 207-217.
11. Kochanek PM, Hallenbeck JM (1992) Polymorphonuclear leukocytes and monocytes/macrophages in the pathogenesis of cerebral ischemia and stroke. Stroke 23: 1367-1379.
12. Matsuo Y, Onodera H, Shiga Y, Nakamura M, Ninomiya M, et al. (1994) Correlation between myeloperoxidase-quantified neutrophil accumulation and ischemic brain injury in the rat. Effects of neutrophil depletion. Stroke 25: 1469-1475.
13. Zhang ZG, Chopp M, Tang WX, Jiang N, Zhang RL (1995) Postischemic treatment (2-4 h) with anti-CD11b and anti-CD18 monoclonal antibodies are neuroprotective after transient (2 h) focal cerebral ischemia in the rat. Brain Res 698: 79-85.
14. Connolly ES, Jr., Winfree CJ, Springer TA, Naka Y, Liao H, et al. (1996) Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J Clin Invest 97: 209-216.
15. del Zoppo G, Ginis I, Hallenbeck JM, Iadecola C, Wang X, et al. (2000) Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia. Brain Pathol 10: 95-112.
16. Matsumoto H, Kumon Y, Watanabe H, Ohnishi T, Shudou M, et al. (2007) Antibodies to CD11b, CD68, and lectin label neutrophils rather than microglia in traumatic and ischemic brain lesions. J Neurosci Res 85: 994-1009.
17. Ji KA, Yang MS, Jeong HK, Min KJ, Kang SH, et al. (2007) Resident microglia die and infiltrated neutrophils and monocytes become major inflammatory cells in lipopolysaccharide-injected brain. Glia 55: 1577-1588.
18. Ji KA, Eu MY, Kang SH, Gwag BJ, Jou I, et al. (2008) Differential neutrophil infiltration contributes to regional differences in brain inflammation in the substantia nigra pars compacta and cortex. Glia 56: 1039-1047.
19. Gautier S, Ouk T, Petrault O, Caron J, Bordet R (2009) Neutrophils contribute to intracerebral haemorrhages after treatment with recombinant tissue plasminogen activator following cerebral ischaemia. Br J Pharmacol 156: 673-679.
20. Malm TM, Koistinaho M, Parepalo M, Vatanen T, Ooka A, et al. (2005) Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to beta-amyloid deposition in APP/PS1 double transgenic Alzheimer mice. Neurobiol Dis 18: 134-142.
21. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S (2006) Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49: 489-502.
22. Elkabes S, DiCicco-Bloom EM, Black IB (1996) Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16: 2508-2521.
23. Lehrmann E, Kiefer R, Christensen T, Toyka KV, Zimmer J, et al. (1998) Microglia and macrophages are major sources of locally produced transforming growth factor-beta1 after transient middle cerebral artery occlusion in rats. Glia 24: 437-448.
24. Batchelor PE, Liberatore GT, Wong JY, Porritt MJ, Frerichs F, et al. (1999) Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J Neurosci 19: 1708-1716.
25. Streit WJ (2002) Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40: 133-139.
26. Streit WJ (2005) Microglia and neuroprotection: implications for Alzheimer's disease. Brain Res Brain Res Rev 48: 234-239.
27. Cavaliere F, D'Ambrosi N, Ciotti MT, Mancino G, Sancesario G, et al. (2001) Glucose deprivation and chemical hypoxia: neuroprotection by P2 receptor antagonists. Neurochem Int 38: 189-197.
28. Cavaliere F, D'Ambrosi N, Sancesario G, Bernardi G, Volonte C (2001) Hypoglycaemia-induced cell death: features of neuroprotection by the P2 receptor antagonist basilen blue. Neurochem Int 38: 199-207.
29. Kharlamov A, Jones SC, Kim DK (2002) Suramin reduces infarct volume in a model of focal brain ischemia in rats. Exp Brain Res 147: 353-359.
30. Melani A, Turchi D, Vannucchi MG, Cipriani S, Gianfriddo M, et al. (2005) ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem Int 47: 442-448.
31. Amadio S, D'Ambrosi N, Cavaliere F, Murra B, Sancesario G, et al. (2002) P2 receptor modulation and cytotoxic function in cultured CNS neurons. Neuropharmacology 42: 489-501.
32. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, et al. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752-758.
33. Hide I, Tanaka M, Inoue A, Nakajima K, Kohsaka S, et al. (2000) Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J Neurochem 75: 965-972.
34. Sanz JM, Di Virgilio F (2000) Kinetics and mechanism of ATP-dependent IL-1 beta release from microglial cells. J Immunol 164: 4893-4898.
35. Inoue K (2002) Microglial activation by purines and pyrimidines. Glia 40: 156-163.
36. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, et al. (2003) P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 278: 13309-13317.
37. Melani A, Amadio S, Gianfriddo M, Vannucchi MG, Volonte C, et al. (2006) P2X7 receptor modulation on microglial cells and reduction of brain infarct caused by middle cerebral artery occlusion in rat. J Cereb Blood Flow Metab 26: 974-982.
38. Paxinos G, Watson CR (2005) The rat brain in stereotaxic coordinates. Amsterdam; Boston: Elsevier Academic Press.;fith Edition.
39. Lehner M, Holter W (2002) Endotoxin-free purification of monocytes for dendritic cell generation via discontinuous density gradient centrifugation based on diluted Ficoll-Paque Plus. Int Arch Allergy Immunol 128: 73-76.
40. Sedgwick JD, Schwender S, Imrich H, Dorries R, Butcher GW, et al. (1991) Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci USA 88: 7438-7442.
41. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD (1995) Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J Immunol 154: 4309-4321.
42. Campanella M, Sciorati C, Tarozzo G, Beltramo M (2002) Flow cytometric analysis of inflammatory cells in ischemic rat brain. Stroke 33: 586-592.
43. Bohatschek M, Werner A, Raivich G (2001) Systemic LPS injection leads to granulocyte influx into normal and injured brain: effects of ICAM-1 deficiency. Exp Neurol 172: 137-152.
44. da Silva RP, Gordon S (1999) Phagocytosis stimulates alternative glycosylation of macrosialin (mouse CD68), a macrophage-specific endosomal protein. Biochem J 338(Pt 3): 687-694.
45. Nerlich AG, Weiler C, Zipperer J, Narozny M, Boos N (2002) Immunolocal-ization of phagocytic cells in normal and degenerated intervertebral discs. Spine (Phila Pa 1976) 27: 2484-2490.
46. Rezaie P, Corbisiero V, Male D (2005) Transient expression of MIDC-8 in the normal mouse brain. Neurosci Lett 377: 189-194.
47. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, et al. (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2: 55-67.
48. Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D, et al. (2005) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 12 Suppl 2: 1463-1467.
49. Motyl T, Gajkowska B, Zarzynska J, Gajewska M, Lamparska-Przybysz M (2006) Apoptosis and autophagy in mammary gland remodeling and breast cancer chemotherapy. J Physiol Pharmacol 57 Suppl 7: 17-32.
50. Peters A, Palay SL, Webster Hd (1991) The fine structure of the nervous system: neurons and their supporting cells. New York: Oxford University Press xviii, 494: 10-23.
51. Kirino T, Sano K (1984) Fine structural nature of delayed neuronal death following ischemia in the gerbil hippocampus. Acta Neuropathol 62: 209-218.
52. Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146: 3-15.
53. Zhao JW, Raha-Chowdhury R, Fawcett JW, Watts C (2009) Astrocytes and oligodendrocytes can be generated from NG2+ progenitors after acute brain injury: intracellular localization of oligodendrocyte transcription factor 2 is associated with their fate choice. Eur J Neurosci 29: 1853-1869.
54. Kang J, Rivest S (2007) MyD88-deficient bone marrow cells accelerate onset and reduce survival in a mouse model of amyotrophic lateral sclerosis. J Cell Biol 179: 1219-1230.
55. Napoli I, Neumann H (2010) Protective effects of microglia in multiple sclerosis. Exp Neurol 225: 24-28.
56. Ryu JK, Tran KC, McLarnon JG (2007) Depletion of neutrophils reduces neuronal degeneration and inflammatory responses induced by quinolinic acid in vivo. Glia 55: 439-451.
57. Pyo H, Yang MS, Jou I, Joe EH (2003) Wortmannin enhances lipopolysaccha-ride-induced inducible nitric oxide synthase expression in microglia in the presence of astrocytes in rats. Neurosci Lett 346: 141-144.
58. Min KJ, Yang MS, Kim SU, Jou I, Joe EH (2006) Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation. J Neurosci 26: 1880-1887.
59. Inoue K, Koizumi S, Tsuda M, Shigemoto-Mogami Y (2003) Signaling of ATP receptors in glia-neuron interaction and pain. Life Sci 74: 189-197.
60. Suzuki T, Hide I, Ido K, Kohsaka S, Inoue K, et al. (2004) Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. J Neurosci 24: 1-7.
61. Holt MP, Cheng L, Ju C (2008) Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J Leukoc Biol 84: 1410-1421.
62. Ishida Y, Gao JL, Murphy PM (2008) Chemokine receptor CX3CR1 mediates skin wound healing by promoting macrophage and fibroblast accumulation and function. J Immunol 180: 569-579.