Microglia potentiate damage to blood-brain barrier constituents: Improvement by minocycline in vivo and in vitro

Stroke

Volumn 37, Issue 4, 2006, Pages 1087-1093

  Yenari, Midori A ^b,c   Xu, Lijun ^a   Xian, Nan Tang ^a,b   Qiao, Yanli ^a   Giffard, Rona G ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Blood brain barrier; Inflammation; Ischemia; Microglia

Indexed keywords

APOCYNIN; GLUCOSE; MINOCYCLINE; OXYGEN; ACETOPHENONE DERIVATIVE; ANTIOXIDANT; HYDROGEN PEROXIDE; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INFARCTION SIZE; BRAIN PROTECTION; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBRINOLYSIS; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; STROKE; ANIMAL; ANOXIA; BRAIN; BRAIN INFARCTION; BRAIN ISCHEMIA; C57BL MOUSE; CELL CULTURE; CELL DEATH; DRUG EFFECT; METABOLISM; NEUROLOGIC DISEASE; PATHOLOGY; PATHOPHYSIOLOGY;

ACETOPHENONES; ANIMALS; ANOXIA; ANTIOXIDANTS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; BRAIN ISCHEMIA; CELL DEATH; CELLS, CULTURED; CEREBRAL HEMORRHAGE; CEREBRAL INFARCTION; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; GLUCOSE; HYDROGEN PEROXIDE; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; MINOCYCLINE; NERVOUS SYSTEM DISEASES; SUPEROXIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33645799230     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.STR.0000206281.77178.ac     Document Type: Article

References (41)

1. Gehrmann J, Matsumoto Y, Kreutzberg GW. Microglia: intrinsic immuneffector cell of the brain. Brain Res Brain Res Rev. 1995;20:269-287.
2. Stoll G, Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol. 1999;58:233-247.
3. Flavin MP, Ho LT. Propentofylline protects neurons in culture from death triggered by macrophage or microglial secretory products. J Neurosci Res. 1999;56:54-59.
4. Flavin MP, Coughlin K, Ho LT. Soluble macrophage factors trigger apoptosis in cultured hippocampal neurons. Neuroscience. 1997;80:437-448.
5. Lyons SA, Kettenmann H. Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J Cereb Blood Flow Metab. 1998;18:521-530.
6. Yenari MA, Giffard RG. Ischemic vulnerability of primary murine microglial cultures. Neurosci Lett. 2001;298:5-8.
7. Sankarapandi S, Zweier JL, Mukherjee G, Quinn MT, Huso DL. Measurement and characterization of superoxide generation in microglial cells: Evidence for an NADPH oxidase-dependent pathway. Arch Biochem Biophys. 1998;353:312-321.
8. Xu J, He L, Ahmed SH, Chen SW, Goldberg MP, Beckman JS, Hsu CY. Oxygen-glucose deprivation induces inducible nitric oxide synthase and nitrotyrosine expression in cerebral endothelial cells. Stroke. 2000;31:1744-1751.
9. Gobbel GT, Chan TY, Gregory GA, Chan PH. Response of cerebral endothelial cells to hypoxia: modification by fructose-1,6-bisphosphate but not glutamate receptor antagonists. Brain Res. 1994;653:23-30.
10. Dugan LL, Bruno VM, Amagasu SM, Giffard RG. Glia modulate the response of murine cortical neurons to excitotoxicity: glia exacerbate AMPA neurotoxicity. J Neurosci. 1995;15:4545-4555.
11. Papadopoulos MC, Koumenis IL, Yuan TY, Giffard RG. Increasing vulnerability of astrocytes to oxidative injury with age despite constant antioxidant defenses. Neuroscience. 1998;82:915-925.
12. Lee JE, Yenari MA, Sun GH, Xu L, Emond MR, Cheng D, Steinberg GK, Giffard RG. Differential neuroprotection from human heat shock protein 70 overexpression in in vitro and in vivo models of ischemia and ischemia-like conditions. Exp Neurol. 2001;170:129-139.
13. Koh JY, Choi DW. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods. 1987;20:83-90.
14. Papadopoulos MC, Koumenis IL, Xu L, Giffard RG. Potentiation of murine astrocyte antioxidant defence by bcl-2: protection in part reflects elevated glutathione levels. Eur J Neurosci. 1998;10:1252-1260.
15. Qiao Y, Ouyang YB, Giffard RG. Overexpression of hdj-2 protects astrocytes from ischemia-like injury and reduces redistribution of ubiquitin staining in vitro. J Cereb Blood Flow Metab. 2003;23:1113-1116.
16. Wang GJ, Deng HY, Maier CM, Sun GH, Yenari MA. Mild hypothermia reduces ICAM-1 expression, neutrophil infiltration and microglia/monocyte accumulation following experimental stroke. Neuroscience. 2002;114:1081-1090.
17. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci U S A. 1999;96:13496-13500.
18. Yrjanheikki J, Keinänen R, Pellikka M, Hökfelt T, Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A. 1998;95:15769-15774.
19. Maier CM, Sun GH, Kunis D, Yenari MA, Steinberg GK. Delayed induction and long-term effects of mild hypothermia in a focal model of transient cerebral ischemia: Neurological outcome and infarct size. J Neurosurg. 2001;94:90-96.
20. Yang G, Chan PH, Chen J, Carlson E, Chen SF, Weinstein P, Epstein CJ, Kamii H. Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke. 1994;25:165-170.
21. Yenari MA, de Crespigny A, Palmer JT, Roberts S, Schrier SL, Albers GW, Moseley ME, Steinberg GK. Improved perfusion with rt-pa and hirulog in a rabbit model of embolic stroke. J Cereb Blood Flow Metab. 1997;17:401-411.
22. Belayev L, Busto R, Zhao W, Ginsberg MD. Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res. 1996;739:88-96.
23. Imaizumi S, Kondo T, Deli MA, Gobbel G, Joo F, Epstein CJ, Yoshimoto T, Chan PH. The influence of oxygen free radicals on the permeability of the monolayer of cultured brain endothelial cells. Neurochem Int. 1996;29:205-211.
24. Fischer S, Wobben M, Kleinstuck J, Renz D, Schaper W. Effect of astroglial cells on hypoxia-induced permeability in PBMEC cells. Am J Physiol Cell Physiol. 2000;279:C935-C944.
25. Kondo T, Kinouchi H, Kawase M, Yoshimoto T. Astroglial cells inhibit the increasing permeability of brain endothelial cell monolayer following hypoxia/reoxygenation. Neurosci Lett. 1996;208:101-104.
26. Gaillard PJ, Voorwinden LH, Nielsen JL, Ivanov A, Atsumi R, Engman H, Ringbom C, de Boer AG, Breimer DD. Establishment and functional characterization of an in vitro model of the blood-brain barrier, comprising a coculture of brain capillary endothelial cells and astrocytes. Eur J Pharm Sci. 2001;12:215-222.
27. Morioka T, Kalehua AN, Streit WJ. Characterization of microglial reaction after middle cerebral artery occlusion in rat brain. J Comp Neurol. 1993;327:123-132.
28. Davies CA, Loddick SA, Stroemer RP, Hunt J, Rothwell NJ. An integrated analysis of the progression of cell responses induced by permanent focal middle cerebral artery occlusion in the rat. Exp Neurol. 1998;154:199-212.
29. Flavin MP, Zhao G, Ho LT. Microglial tissue plasminogen activator (tpa) triggers neuronal apoptosis in vitro. Glia. 2000;29:347-354.
30. Han HS, Qiao Y, Karabiyikoglu M, Giffard RG, Yenari MA. Influence of mild hypothermia on inducible nitric oxide synthase expression and reactive nitrogen production in experimental stroke and inflammation. J Neurosci. 2002;22:3921-3928.
31. Lynch NJ, Willis CL, Nolan CC, Roscher S, Fowler MJ, Weihe E, Ray DE, Schwaeble WJ. Microglial activation and increased synthesis of complement component clq precedes blood-brain barrier dysfunction in rats. Mol Immunol. 2004;40:709-716.
32. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci. 2001;21:2580-2588.
33. Tomas-Camardiel M, Rite I, Herrera AJ, de Pablos RM, Cano J, Machado A, Venero JL. Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system. Neurobiol Dis. 2004;16:190-201.
34. Power C, Henry S, Del Bigio MR, Larsen PH, Corbett D, Imai Y, Yong VW, Peeling J. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol. 2003;53:731-742.
35. Tikka TM, Koistinaho JE. Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol. 2001;166:7527-7533.
36. Koistinaho M, Malm TM, Kettunen MI, Goldsteins G, Starckx S, Kauppinen RA, Opdenakker G, Koistinaho J. Minocycline protects against permanent cerebral ischemia in wild type but not in matrix metalloprotease-9-deficient mice. J Cereb Blood Flow Metab. 2005;25:460-467.
37. Friedlander RM. Apoptosis and caspases in neurodegenerative diseases. N Engl J Med. 2003;348:1365-1375.
38. Green SP, Cairns B, Rae J, Errett-Baroncini C, Hongo JA, Erickson RW, Curnutte JT. Induction of gp91-phox, a component of the phagocyte NADPH oxidase, in microglial cells during central nervous system inflammation. J Cereb Blood Flow Metab. 2001;21:374-384.
39. Noh KM, Koh JY. Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. J Neurosci. 2000;20:RC111.
40. Hori O, Matsumoto M, Maeda Y, Ueda H, Ohtsuki T, Stern DM, Kinoshita T, Ogawa S, Kamada T. Metabolic and biosynthetic alterations in cultured astrocytes exposed to hypoxia/reoxygenation. J Neurochem. 1994;62:1489-1495.
41. Morgenstern LB, Staub L, Chan W, Wein TH, Bartholomew LK, King M, Felberg RA, Burgin WS, Groff J, Hickenbottom SL, Saldin K, Demchuk AM, Kalra A, Dhingra A, Grotta JC. Improving delivery of acute stroke therapy: the TLL Temple Foundation Stroke Project Stroke. 2002;33:160-166.