NADPH oxidase mediates TNF-α-evoked in vitro brain barrier dysfunction: Roles of apoptosis and time

Molecular and Cellular Neuroscience

Volumn 61, Issue , 2014, Pages 72-84

  Abdullah, Zuraidah ^a   Bayraktutan, Ulvi ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Blood brain barrier; Cytoskeleton; MMP; NADPH oxidase; TNF

Indexed keywords

CASPASE 3; CASPASE 7; CATALASE; CLAUDIN 5; COPPER ZINC SUPEROXIDE DISMUTASE; GELATINASE A; GELATINASE B; OCCLUDIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TUMOR NECROSIS FACTOR ALPHA; ACETOPHENONE DERIVATIVE; APOCYNIN; CATION; CYTOCHROME C; DIPHENYLIODONIUM SALT; ENZYME INHIBITOR; OXYGEN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

APOPTOSIS; ARTICLE; ASTROCYTE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; COCULTURE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIGHT JUNCTION; DRUG EFFECTS; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; IMPEDANCE; METABOLISM; TIME;

ACETOPHENONES; APOPTOSIS; ASTROCYTES; CATALASE; COCULTURE TECHNIQUES; CYTOCHROMES C; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HUMANS; IN VITRO TECHNIQUES; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NADPH OXIDASE; ONIUM COMPOUNDS; OXYGEN; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84902291024     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.06.002     Document Type: Article

References (39)

1. Allen C.L., Bayraktutan U. Antioxidants attenuate hyperglycaemia-mediated brain endothelial cell dysfunction and blood-brain barrier hyperpermeability. Diabetes Obes. Metab. 2009, 11:480-490.
2. Allen C., Srivastava K., Bayraktutan U. Small GTPase RhoA and its effector rho kinase mediate oxygen glucose deprivation-evoked in vitro cerebral barrier dysfunction. Stroke 2010, 41:2056-2063.
3. Armstead W.M., Mirro R., Thelin O.P., Shibata M., Zuckerman S.L., Shanklin D.R., Busija D.W., Leffler C.W. Polyethylene glycol superoxide dismutase and catalase attenuate increased blood-brain barrier permeability after ischemia in piglets. Stroke 1992, 23:755-762.
4. Balcerczyk A., Soszynski M.a, Rybaczek D., Przygodzki T., Karowicz-Bilinska A., Maszewski J., Bartosz G. Induction of apoptosis and modulation of production of reactive oxygen species in human endothelial cells by diphenyleneiodonium. Biochem. Pharmacol. 2005, 69:1263-1273.
5. Barone F.C., Arvin B., White R.F., Miller A., Webb C.L., Willette R.N., Lysko P.G., Feuerstein G.Z. Tumor necrosis factor-α: a mediator of focal ischemic brain injury. Stroke 1997, 28:1233-1244.
6. Basuroy S., Bhattacharya S., Tcheranova D., Qu Y., Regan R.F., Leffler C.W., Parfenova H. HO-2 provides endogenous protection against oxidative stress and apoptosis caused by TNF-α in cerebral vascular endothelial cells. Am. J. Physiol. Cell Physiol. 2006, 291:C897-C908.
7. Basuroy S., Bhattacharya S., Leffler C.W., Parfenova H. Nox4 NADPH oxidase mediates oxidative stress and apoptosis caused by TNF-α in cerebral vascular endothelial cells. Am. J. Physiol. Cell Physiol. 2009, 296:C422-C432.
8. Bayraktutan U. Free radicals, diabetes and endothelial dysfunction. Diabetes Obes. Metab. 2002, 4:224-238.
9. Bayraktutan U. Reactive oxygen species, nitric oxide and hypertensive endothelial dysfunction. Curr. Hypertens. Rev. 2005, 1:201-215.
10. Bresgen N., Jaksch H., Bauer H.-C., Eckl P., Krizbai I., Tempfer H. Astrocytes are more resistant than cerebral endothelial cells toward geno- and cytotoxicity mediated by short-term oxidative stress. J. Neurosci. Res. 2006, 84:1821-1828.
11. Burek M., Förster C.Y. Cloning and characterization of the murine claudin-5 promoter. Mol. Cell. Endocrinol. 2009, 298:19-24.
12. Chen H., Song Y.S., Chan P.H. Inhibition of NADPH oxidase is neuroprotective after ischemia-reperfusion. J. Cereb. Blood Flow Metab. 2009, 29:1262-1272.
13. Crocker S.J., Frausto R.F., Whitton J.L., Milner R. A novel method to establish microglia-free astrocyte cultures: comparison of matrix metalloproteinase expression profiles in pure cultures of astrocytes and microglia. Glia 2008, 56:1187-1198.
14. de Vries H.E., Blom-Roosemalen M.C.M., Oosten M.v, de Boer A.G., van Berkel T.J.C., Breimer D.D., Kuiper J. The influence of cytokines on the integrity of the blood-brain barrier in vitro. J. Neuroimmunol. 1996, 64:37-43.
15. Dejana E. Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 2004, 5:261-270.
16. Denes A., Ferenczi S., Halasz J., Kornyei Z., Kovacs K.J. Role of CX3CR1 in brain damage and inflammation induced by focal cerebral ischemia in mouse. J. Cereb. Blood Flow Metab. 2008, 28:1707-1721.
17. Förster C., Burek M., Romero I.A., Weksler B., Couraud P.-O., Drenckhahn D. Differential effects of hydrocortisone and TNFα on tight junction proteins in an in vitro model of the human blood-brain barrier. J. Physiol. 2008, 586:1937-1949.
18. Gasche Y., Fujimura M., Morita-Fujimura Y., Copin J.-C., Kawase M., Massengale J., Chan P.H. Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction. J. Cereb. Blood Flow Metab. 1999, 19:1020-1028.
19. Gu X., Zhang J., Brann D.W., Yu F.-S.X. Brain and retinal vascular endothelial cells with extended life span established by ectopic expression of telomerase. Invest. Ophthalmol. Vis. Sci. 2003, 44:3219-3225.
20. Gu Y., Zheng G., Xu M., Li Y., Chen X., Zhu W., Tong Y., Chung S.K., Liu K.J., Shen J. Caveolin-1 regulates nitric oxide-mediated matrix metalloproteinases activity and blood-brain barrier permeability in focal cerebral ischemia and reperfusion injury. J. Neurochem. 2012, 120:147-156.
21. Hosomi N., Ban C.R., Naya T., Takahashi T., Guo P., Song X.Y., Kohno M. Tumor necrosis factor-alpha neutralization reduced cerebral edema through inhibition of matrix metalloproteinase production after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2005, 25:959-967.
22. Hurwitz A.A., Berman J.W., Rashbaum W.K., Lyman W.D. Human fetal astrocytes induce the expression of blood-brain barrier specific proteins by autologous endothelial cells. Brain Res. 1993, 625:238-243.
23. Kahles T., Luedike P., Endres M., Galla H.-J., Steinmetz H., Busse R., Neumann-Haefelin T., Brandes R.P. NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke 2007, 38:3000-3006.
24. Kim J.A., Tran N.D., Wang S.-J., Fisher M.J. Astrocyte regulation of human brain capillary endothelial fibrinolysis. Thromb. Res. 2003, 112:159-165.
25. Kobayashi N., DeLano F.A., Schmid-Schönbein G.W. Oxidative stress promotes endothelial cell apoptosis and loss of microvessels in the spontaneously hypertensive rats. Arterioscler. Thromb. Vasc. 2005, 25:2114-2121.
26. Li Y., Zhu H., Kuppusamy P., Roubaud V., Zweier J.L., Trush M.A. Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J. Biol. Chem. 1998, 273:2015-2023.
27. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., Robinson J.P. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 2003, 278:8516-8525.
28. Lopez-Ramirez M.A., Fischer R., Torres-Badillo C.C., Davies H.A., Logan K., Pfizenmaier K., Male D.K., Sharrack B., Romero I.A. Role of caspases in cytokine-induced barrier breakdown in human brain endothelial cells. J. Immunol. 2012, 189:3130-3139.
29. McKenzie J.A.G., Ridley A.J. Roles of Rho/ROCK and MLCK in TNF-α-induced changes in endothelial morphology and permeability. J. Cell. Physiol. 2007, 213:221-228.
30. Megyeri P., Abraham C.s, Temesvari P., Kovacs J., Vas T., Speer C.P. Recombinant human tumor necrosis factor alpha constricts pial arterioles and increases blood-brain barrier permeability in newborn piglets. Neurosci. Lett. 1992, 148:137-140.
31. Parks W.C., Wilson C.L., Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 2004, 4:617-629.
32. Petrache I., Verin A.D., Crow M.T., Birukova A., Liu F., Garcia J.G.N. Differential effect of MLC kinase in TNF-α-induced endothelial cell apoptosis and barrier dysfunction. Am. J. Physiol. Lung Cell 2001, 280:L1168-L1178.
33. Ramesh G., MacLean A.G., Philipp M.T. Cytokines and chemokines at the crossroads of neuroinflammation, neurodegeneration, and neuropathic pain. Mediat. Inflamm. 2013, 2013:20. (Aug 12). 10.1155/2013/480739.2013.
34. Rosenberg G.A., Estrada E.Y., Dencoff J.E., Stetler-Stevenson W.G. Tumor necrosis factor-α-induced gelatinase B causes delayed opening of the blood-brain barrier: an expanded therapeutic window. Brain Res. 1995, 703:151-155.
35. Rosenberg G.A., Estrada E.Y., Dencoff J.E., Hsu C.Y. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998, 29:2189-2195. Editorial Comment.
36. Shao B., Bayraktutan U. Hyperglycaemia promotes cerebral barrier dysfunction through activation of protein kinase C-β. Diabetes Obes. Metab. 2013, 15:993-999.
37. Ülker S., McMaster D., McKeown P.P., Bayraktutan U. Antioxidant vitamins C and E ameliorate hyperglycaemia-induced oxidative stress in coronary endothelial cells. Diabetes Obes. Metab. 2004, 6:442-451.
38. Wang Q., Tang X.N., Yenari M.A. The inflammatory response in stroke. J. Neuroimmunol. 2007, 184:53-68.
39. Zhang H.-S., Wang S.-Q. Salvianolic acid B from Salvia miltiorrhiza inhibits tumor necrosis factor-α (TNF-α)-induced MMP-2 upregulation in human aortic smooth muscle cells via suppression of NAD(P)H oxidase-derived reactive oxygen species. J. Mol. Cell. Cardiol. 2006, 41:138-148.