Moderate hypoxia followed by reoxygenation results in blood-brain barrier breakdown via oxidative stress-dependent tight-junction protein disruption

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Zehendner, Christoph M ^a   Librizzi, Laura ^b   Hedrich, Jana ^a   Bauer, Nina M ^a   Angamo, Eskedar A ^c   De Curtis, Marco ^b   Luhmann, Heiko J ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 5; PROTEIN ZO1; REACTIVE OXYGEN METABOLITE; TIGHT JUNCTION PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; BRAIN HYPOXIA; CELL HYPOXIA; CELL MEMBRANE PERMEABILITY; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; ELECTRIC RESISTANCE; ENZYME ACTIVITY; GUINEA PIG; IMMUNOHISTOCHEMISTRY; MACROMOLECULE; NONHUMAN; OXIDATIVE STRESS; PROTEIN FUNCTION; REOXYGENATION; REPERFUSION; TRANSENDOTHELIAL ELECTRICAL RESISTANCE; UPREGULATION; YOUNG ADULT;

ANIMALS; ANOXIA; BLOOD-BRAIN BARRIER; CELL MEMBRANE; CLAUDIN-5; ENDOTHELIAL CELLS; GUINEA PIGS; MICROVESSELS; MITOCHONDRIA; OXIDATIVE STRESS; PERMEABILITY; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; TIGHT JUNCTION PROTEINS; TIGHT JUNCTIONS; TYROSINE; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84891952619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082823     Document Type: Article

References (63)

1. Zlokovic BV (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57:178-201. doi:10.1016/j.neuron. 2008.01.003. PubMed: 18215617.
2. Yang Y, Rosenberg GA (2011) Blood-brain barrier breakdown in acute and chronic cerebrovascular disease. Stroke 42:3323-3328. doi: 10.1161/STROKEAHA. 110.608257. PubMed: 21940972.
3. Coisne C, Engelhardt B (2011) Tight Junctions in Brain Barriers during CNS. Inflammation - Antioxidants and Redox Signalling: 110306091003087. doi:10.1089/ars.2011.3929.
4. Kahles T, Luedike P, Endres M, Galla H-J, Steinmetz H et al. (2007) NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke 38:3000-3006. doi:10.1161/STROKEAHA. 107.489765. PubMed: 17916764. (Pubitemid 350035696)
5. Miller AA, Dusting GJ, Roulston CL, Sobey CG (2006) NADPH-oxidase activity is elevated in penumbral and non-ischemic cerebral arteries following stroke. Brain Res 1111:111-116. doi:10.1016/j.brainres. 2006.06.082. PubMed: 16879806. (Pubitemid 44331177)
6. Fraser PA (2011) The role of free radical generation in increasing cerebrovascular permeability. Free Radic Biol Med 51:967-977. doi: 10.1016/j.freeradbiomed.2011.06.003. PubMed: 21712087.
7. Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K et al. (2009) Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med 15:1031-1037. doi:10.1038/nm.2022. PubMed: 19718040.
8. Jian Liu K, Rosenberg GA (2005) Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radic Biol Med 39:71-80. doi: 10.1016/j.freeradbiomed.2005.03.033. PubMed: 15925279. (Pubitemid 40733117)
9. Rosenberg GA, Yang Y (2007) Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus 22:E4. PubMed: 17613235.
10. Sandoval KE, Witt KA (2008) Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 32:200-219. doi: 10.1016/j.nbd.2008.08.005. PubMed: 18790057.
11. Rosenberg GA (1999) Ischemic brain edema. Prog Cardiovasc Dis 42:209-216. doi:10.1016/S0033-0620 (99) 70003-4. PubMed: 10598921.
12. Hansel CM, Zeiner CA, Santelli CM, Webb SM (2012) Mn (II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction. Proc Natl Acad Sci U S A 109:12621-12625. doi:10.1073/pnas. 1203885109. PubMed: 22802654.
13. Riganti C, Costamagna C, Bosia A, Ghigo D (2006) The NADPH oxidase inhibitor apocynin (acetovanillone) induces oxidative stress. Toxicol Appl Pharmacol 212:179-187. doi:10.1016/j.taap. 2005.07.011. PubMed: 16120450.
14. Riganti C, Costamagna C, Doublier S, Miraglia E, Polimeni M et al. (2008) The NADPH oxidase inhibitor apocynin induces nitric oxide synthesis via oxidative stress. Toxicol Appl Pharmacol 228:277-285. doi:10.1016/j.taap. 2007.12.013. PubMed: 18234259.
15. Thal SC, Luh C, Schaible E-V, Timaru-Kast R, Hedrich J et al. (2012) Volatile Anesthetics Influence Blood-Brain Barrier Integrity by Modulation of Tight Junction Protein Expression in Traumatic Brain. Injury - PLOS ONE 7:e50752. doi:10.1371/journal.pone.0050752.
16. Astrup J, Symon L, Branston NM, Lassen NA (1977) Cortical evoked potential and extracellular K+ and H+ at critical levels of brain ischemia. Stroke 8:51-57. doi:10.1161/01. STR.8.1.51. PubMed: 13521.
17. De Curtis M, Biella G, Buccellati C, Folco G (1998) Simultaneous investigation of the neuronal and vascular compartments in the guinea pig brain isolated in vitro. Brain Res Brain Res Protoc 3:221-228. doi: 10.1016/S1385-299X (98) 00044-0. PubMed: 9813340. (Pubitemid 28527104)
18. Librizzi L, Janigro D, De Biasi S, de Curtis M (2001) Blood-brain barrier preservation in the in vitro isolated guinea pig brain preparation. J Neurosci Res 66:289-297. doi:10.1002/jnr.1223. PubMed: 11592126. (Pubitemid 32912298)
19. Mazzetti S, Librizzi L, Frigerio S, de Curtis M, Vitellaro-Zuccarello L (2004) Molecular anatomy of the cerebral microvessels in the isolated guinea-pig brain. Brain Res 999:81-90. doi:10.1016/j.brainres. 2003.11.032. PubMed: 14746924. (Pubitemid 38121453)
20. Matsuzawa T, Fujiwara E, Washi Y (2013) Autophagy activation by interferon-γ via the p38 MAPK signalling pathway is involved in macrophage bactericidal activity. Immunology: ([MedlinePgn:]) doi: 10.1111/imm.12168. PubMed: 24032631.
21. Wind S, Beuerlein K, Eucker T, Müller H, Scheurer P et al. (2010) Comparative pharmacology of chemically distinct NADPH oxidase inhibitors. Br J Pharmacol 161:885-898. doi:10.1111/j. 1476-5381.2010.00920.x. PubMed: 20860666.
22. Gladden JD, Zelickson BR, Guichard J, Ahmed MI, Yancey DM et al. (2013) Xanthine Oxidase Inhibition Preserves Left Ventricular Systolic but not Diastolic Function in Cardiac Volume Overload. Am J Physiol Heart Circ Physiol. doi:10.1152/ajpheart.00007.2013.
23. Terrisse AD, Puech N, Allart S, Gourdy P, Xuereb JM et al. (2010) Internalization of microparticles by endothelial cells promotes platelet/endothelial cell interaction under flow: Internalization of microparticles by endothelial cells. Journal of Thrombosis and Haemostasis 8:2810-2819. doi:10.1111/j.1538-7836.2010.04088.x. PubMed: 21029362.
24. Kuhlmann CRW, Trümper JRFC, Abdallah Y, Wiebke Lüdders D, Schaefer CA et al. (2004) The K+-channel opener NS1619 increases endothelial NO-synthesis involving p42/p44 MAP-kinase. Thromb Haemost 92:1099-1107. doi:10.1267/THRO04051099. PubMed: 15543339. (Pubitemid 39545535)
25. Kuhlmann CRW, Gerigk M, Bender B, Closhen D, Lessmann V et al. (2008) Fluvastatin prevents glutamate-induced blood-brain-barrier disruption in vitro. Life Sci 82:1281-1287. doi:10.1016/j.lfs. 2008.04.017. PubMed: 18534629.
26. Manaenko A, Chen H, Kammer J, Zhang JH, Tang J (2011) Comparison Evans Blue injection routes: Intravenous versus intraperitoneal, for measurement of blood-brain barrier in a mice hemorrhage model. J Neurosci Methods 195:206-210. doi:10.1016/j.jneumeth.2010.12.013. PubMed: 21168441.
27. Zehendner CM, Luhmann HJ, Kuhlmann CR (2009) Studying the neurovascular unit: an improved blood-brain barrier model. J Cereb Blood Flow Metab 29:1879-1884. doi:10.1038/jcbfm.2009.103. PubMed: 19638997.
28. Bauer AT, Bürgers HF, Rabie T, Marti HH (2010) Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. Journal of Cerebral Blood Flow and Metabolism 30:837-848. doi:10.1038/jcbfm.2009.248. PubMed: 19997118.
29. Daneman R, Zhou L, Kebede AA, Barres BA (2010) Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468:562-566. doi:10.1038/nature09513. PubMed: 20944625.
30. Kitagawa K, Matsumoto M, Niinobe M, Mikoshiba K, Hata R et al. (1989) Microtubule-associated protein 2 as a sensitive marker for cerebral ischemic damage-Immunohistochemical investigation of dendritic damage. Neuroscience 31:401-411. doi: 10.1016/0306-4522 (89) 90383-7. PubMed: 2797444. (Pubitemid 19238646)
31. Breschi GL, Mastropietro A, Zucca I, Librizzi L, de Curtis M (2012) Penumbra region excitability is not enhanced acutely after cerebral ischemia in the in vitro isolated guinea pig brain. Epilepsia 53:448-458. doi:10.1111/j.1528-1167.2011.03356.x. PubMed: 22191769.
32. Shi H, Liu KJ (2007) Cerebral tissue oxygenation and oxidative brain injury during ischemia and reperfusion. Front Biosci 12:1318-1328. doi:10.2741/2150. PubMed: 17127384. (Pubitemid 46846837)
33. Betzen C, White R, Zehendner CM, Pietrowski E, Bender B et al. (2009) Oxidative stress upregulates the NMDA receptor on cerebrovascular endothelium. Free Radic Biol Med 47:1212-1220. doi: 10.1016/j.freeradbiomed.2009.07.034. PubMed: 19660541.
34. Del Zoppo GJ, Sharp FR, Heiss W-D, Albers GW (2011) Heterogeneity in the penumbra. J Cereb Blood Flow Metab 31:1836-1851. doi: 10.1038/jcbfm.2011.93. PubMed: 21731034.
35. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A et al. (2008) Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 359:1317-1329. doi:10.1056/NEJMoa0804656. PubMed: 18815396.
36. Molina CA, Saver JL (2005) Extending reperfusion therapy for acute ischemic stroke: emerging pharmacological, mechanical, and imaging strategies. Stroke 36:2311-2320. doi:10.1161/01. STR. 0000182100.65262.46. PubMed: 16179577. (Pubitemid 41429268)
37. Caso V, Hacke W (2002) The very acute stroke treatment: fibrinolysis and after. Clin Exp Hypertens 24:595-602. doi:10.1081/CEH-120015335. PubMed: 12450234. (Pubitemid 35415773)
38. Liu S, Shi H, Liu W, Furuichi T, Timmins GS et al. (2004) Interstitial pO2 in ischemic penumbra and core are differentially affected following transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 24:343-349. doi:10.1097/01. WCB.0000110047.43905.01. PubMed: 15091115. (Pubitemid 38314590)
39. Kuhlmann CRW, Zehendner CM, Gerigk M, Closhen D, Bender B et al. (2009) MK801 blocks hypoxic blood-brain-barrier disruption and leukocyte adhesion. Neurosci Lett 449:168-172. doi:10.1016/j.neulet. 2008.10.096. PubMed: 18996441.
40. Gu Y, Zheng G, Xu M, Li Y, Chen X et al. (2012) Caveolin-1 regulates nitric oxide-mediated matrix metalloproteinases activity and blood-brain barrier permeability in focal cerebral ischemia and reperfusion injury. J Neurochem 120:147-156. doi:10.1111/j.1471-4159.2011.07542.x. PubMed: 22007835.
41. Al-Mehdi AB, Zhao G, Dodia C, Tozawa K, Costa K, et al. (1998) Endothelial NADPH oxidase as the source of oxidants in lungs exposed to ischemia or high K+. Circ Res 83:730-737 (Pubitemid 28462787)
42. Brandes RP, Kreuzer J (2005) Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 65:16-27. doi:10.1016/j.cardiores.2004. 08.007. PubMed: 15621030. (Pubitemid 40038475)
43. Itoh Y, Takaoka R, Ohira M, Abe T, Tanahashi N et al. (2006) Reactive oxygen species generated by mitochondrial injury in human brain microvessel endothelial cells. Clin Hemorheol Microcirc 34:163-168. PubMed: 16543632. (Pubitemid 43351025)
44. Kleikers PWM, Wingler K, Hermans JJR, Diebold I, Altenhöfer S et al. (2012) NADPH oxidases as a source of oxidative stress and molecular target in ischemia/reperfusion injury. J Mol Med 90:1391-1406. doi: 10.1007/s00109-012- 0963-3. PubMed: 23090009.
45. Förstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. Eur Heart J 33:829-837, 837a-837d doi:10.1093/eurheartj/ehr304.
46. Fisher M, Albers GW (2013) Advanced imaging to extend the therapeutic time window of acute ischemic stroke. Ann Neurol 73:4-9. doi:10.1002/ana.23744. PubMed: 23378323.
47. Barber PA (2013) Magnetic resonance imaging of ischemia viability thresholds and the neurovascular unit. Sensors (Basel) 13:6981-7003. doi:10.3390/s130606981. PubMed: 23711462.
48. Deli MA, Abrahám CS, Kataoka Y, Niwa M (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell Mol Neurobiol 25:59-127. doi:10.1007/s10571-004-1377-8. PubMed: 15962509. (Pubitemid 40558585)
49. Harhaj NS, Antonetti DA (2004) Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol 36:1206-1237. doi:10.1016/j.biocel.2003.08.007. PubMed: 15109567. (Pubitemid 38519069)
50. Zehendner CM, Librizzi L, de Curtis M, Kuhlmann CRW, Luhmann HJ (2011) Caspase-3 contributes to ZO-1 and Cl-5 tight-junction disruption in rapid anoxic neurovascular unit damage. PLOS ONE 6:e16760. doi: 10.1371/journal.pone. 0016760. PubMed: 21364989.
51. Campbell M, Hanrahan F, Gobbo OL, Kelly ME, Kiang A-S et al. (2012) Targeted suppression of claudin-5 decreases cerebral oedema and improves cognitive outcome following traumatic brain injury. Nat Commun 3:849. doi:10.1038/ncomms1852. PubMed: 22617289.
52. Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R et al. (2009) Pivotal role of cerebral interleukin-17-producing γδT cells in the delayed phase of ischemic brain injury. Nat Med 15:946-950. doi: 10.1038/nm.1999. PubMed: 19648929.
53. Mühlethaler M, Curtis M, Walton K, Llinás R (1993) The Isolated and Perfused Brain of the Guinea-pig. In Vitro - European Journal of Neuroscience 5:915-926. doi:10.1111/j.1460-9568.1993.tb00942.x.
54. Librizzi L, Folco G, de Curtis M (2000) Nitric oxide synthase inhibitors unmask acetylcholine-mediated constriction of cerebral vessels in the in vitro isolated guinea-pig brain. Neuroscience 101:283-287. doi: 10.1016/S0306-4522 (00) 00365-1. PubMed: 11074151.
55. Schulz E, Wenzel P, Münzel T, Daiber A (2012) Mitochondrial Redox Signaling: Interaction of Mitochondrial Reactive Oxygen Species with Other Sources of Oxidative. Stress - Antioxidants and Redox Signalling. doi:10.1089/ars.2012.4609.
56. Sena LA, Chandel NS (2012) Physiological roles of mitochondrial reactive oxygen species. Mol Cell 48:158-167. doi:10.1016/j.molcel. 2012.09.025. PubMed: 23102266.
57. Octavia Y, Brunner-La Rocca HP, Moens AL (2012) NADPH oxidasedependent oxidative stress in the failing heart: From pathogenic roles to therapeutic approach. Free Radic Biol Med 52:291-297. doi:10.1016/j.freeradbiomed.2011.10. 482. PubMed: 22080085.
58. Okuno Y, Nakamura-Ishizu A, Otsu K, Suda T, Kubota Y (2012) Pathological neoangiogenesis depends on oxidative stress regulation by ATM. Nat Med 18:1208-1216. doi:10.1038/nm.2846. PubMed: 22797809.
59. Mangan PR, O'Quinn D, Harrington L, Bonder CS, Kubes P et al. (2005) Both Th1 and Th2 cells require P-selectin glycoprotein ligand-1 for optimal rolling on inflamed endothelium. Am J Pathol 167:1661-1675. doi:10.1016/S0002-9440 (10) 61249-7. PubMed: 16314478. (Pubitemid 41713318)
60. Brown RC, Morris AP, O'Neil RG (2007) Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells. Brain Res 1130:17-30. doi:10.1016/j.brainres.2006.10.083. PubMed: 17169347. (Pubitemid 46053886)
61. Patrick Schenck L, Hirota SA, Hirota CL, Boasquevisque P, Tulk SE et al. (2013) Attenuation of Clostridium difficile toxin-induced damage to epithelial barrier by ecto-5'-nucleotidase (CD73) and adenosine receptor signaling. Neurogastroenterology and Motility 25:e441-e453. doi:10.1111/nmo.12139.
62. Movahedan A, Afsharkhamseh N, Sagha HM, Shah JR, Milani BY et al. (2013) Loss of Notch1 Disrupts the Barrier Repair in the Corneal Epithelium. PLOS ONE 8:e69113. doi:10.1371/journal.pone.0069113. PubMed: 23874882.
63. D'Agostino RB, Pearson ES (1990). Testing for Departures from Normality. 44:31 21.