Blood-brain barrier breakdown involves four distinct stages of vascular damage in various models of experimental focal cerebral ischemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 2, 2015, Pages 292-303

  Krueger, Martin ^a   Bechmann, Ingo ^a   Immig, Kerstin ^a   Reichenbach, Andreas ^a   Härtig, Wolfgang ^a   Michalski, Dominik ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

blood brain barrier; brain ischemia; focal ischemia; intracerebral hemorrhage; neurovascular unit

Indexed keywords

CLAUDIN 3; CLAUDIN 5; FLUORESCEIN ISOTHIOCYANATE; ISOLECTIN B4; PROTEIN ZO1; VASCULAR ENDOTHELIAL CADHERIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BLOOD VESSEL INJURY; CELL JUNCTION; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; TRANSIENT ISCHEMIC ATTACK; ANIMAL; BRAIN ISCHEMIA; CAPILLARY PERMEABILITY; CEREBROVASCULAR ACCIDENT; DISEASE MODEL; PATHOLOGY; PATHOPHYSIOLOGY; RAT; THROMBOEMBOLISM; VASCULAR ENDOTHELIUM; WISTAR RAT;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; MICE; RATS; RATS, WISTAR; STROKE; THROMBOEMBOLISM;

EID: 84922337429     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.199     Document Type: Article

References (40)

1. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999; 22: 391-397.
2. Endres M, Engelhardt B, Koistinaho J, Lindvall O, Meairs S, Mohr JP et al. Improving outcome after stroke: overcoming the translational roadblock. Cerebrovasc Dis 2008; 25: 268-278.
3. Donnan GA, Fisher M, Macleod M, Davis SM. Stroke. Lancet 2008; 371: 1612-1623.
4. del Zoppo GJ. The neurovascular unit in the setting of stroke. J Intern Med 2010; 267: 156-171.
5. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008; 57: 178-201.
6. Reese TS, Karnovsky MJ. Fine structural localization of a blood-brain barrier to exogenous peroxidase. J Cell Biol 1967; 34: 207-217.
7. Bechmann I, Galea I, Perry VH. What is the blood-brain barrier (not)? Trends Immunol 2007; 28: 5-11.
8. Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the blood-brain barrier. Nat Med 2013; 19: 1584-1596.
9. Wolburg H, Lippoldt A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 2002; 38: 323-337.
10. Fischer S, Wobben M, Kleinstück J, Renz D, Schaper W. Effect of astroglial cells on hypoxia-induced permeability in PBMEC cells. Am J Physiol Cell Physiol 2000; 279: 935-944.
11. Sandoval KE, Witt KA. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 2008; 32: 200-219.
12. Jiao H, Wang Z, Liu Y, Wang P, Xue Y. Specific role of tight junction proteins claudin-5, occludin, and ZO-1 of the blood-brain barrier in a focal cerebral ischemic insult. J Mol Neurosci 2011; 44: 130-139.
13. Liu J, Jin X, Liu KJ, Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to bloodbrain barrier damage in early ischemic stroke stage. J Neurosci 2012; 32: 3044-3057.
14. Krueger M, Härtig W, Reichenbach A, Bechmann I, Michalski D. Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions. PLoS ONE 2013; 8: e56419.
15. De Bock M, Culot M, Wang N, Bol M, Decrock E, De Vuyst E et al. Connexin channels provide a target to manipulate brain endothelial calcium dynamics and blood-brain barrier permeability. J Cereb Blood Flow Metab 2011; 31: 1942-1957.
16. Danesh-Meyer HV, Kerr NM, Zhang J, Eady EK, O'Carroll SJ, Nicholson LF et al. Connexin43 mimetic peptide reduces vascular leak and retinal ganglion cell death following retinal ischaemia. Brain 2012; 135: 506-520.
17. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008; 359: 1317-1329.
18. Meairs S, Wahlgren N, Dirnagl U, Lindvall O, Rothwell P, Baron JC et al. Stroke research priorities for the next decade - a representative view of the European scientific community. Cerebrovasc Dis 2006; 22: 75-82.
19. Dávalos A, Toni D, Iweins F, Lesaffre E, Bastianello S, Castillo J. Neurological deterioration in acute ischemic stroke: potential predictors and associated factors in the European cooperative acute stroke study (ECASS) I. Stroke 1999; 30: 2631-2636.
20. Pundik S, Xu K, Sundararajan S. Reperfusion brain injury: focus on cellular bioenergetics. Neurology 2012; 79: 44-51.
21. Whiteley WN, Thompson D, Murray G, Cohen G, Lindley RI, Wardlaw J et al. Targeting recombinant tissue-type plasminogen activator in acute ischemic stroke based on risk of intracranial hemorrhage or poor functional outcome: an analysis of the third international stroke trial. Stroke 2014; 45: 1000-1006.
22. Bulkley GB. Free radical-mediated reperfusion injury: a selective review. Br J Cancer 1987; 8: 66-73.
23. Francis JW, Ren J, Warren L, Brown RH, Jr, Finklestein SP. Postischemic infusion of Cu/Zn superoxide dismutase or SOD:Tet451 reduces cerebral infarction following focal ischemia/reperfusion in rats. Exp Neurol 1997; 146: 435-443.
24. Menzies SA, Hoff JT, Betz AL. Middle cerebral artery occlusion in rats: a neurological and pathological evaluation of a reproducible model. Neurosurgery 1992; 31: 100-106.
25. Michalski D, Grosche J, Pelz J, Schneider D, Weise C, Bauer U et al. A novel quantification of blood-brain barrier damage and histochemical typing after embolic stroke in rats. Brain Res 2010; 1359: 186-200.
26. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20: 84-91.
27. Michalski D, Härtig W, Krügel K, Edwards RH, Böddener M, Böhme L et al. Regionspecific expression of vesicular glutamate and GABA transporters under various ischaemic conditions in mouse forebrain and retina. Neuroscience 2013; 231: 328-344.
28. Sixt M, Engelhardt B, Pausch F, Hallmann R, Wendler O, Sorokin LM. Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J Cell Biol 2001; 153: 933-946.
29. Bauer AT, Bürgers HF, Rabie T, Marti HH. Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J Cereb Blood Flow Metab 2010; 30: 837-848.
30. Steiner E, Enzmann GU, Lyck R, Lin S, Rüegg MA, Kröger S, Engelhardt B. The heparan sulfate proteoglycan agrin contributes to barrier properties of mouse brain endothelial cells by stabilizing adherens junctions. Cell Tissue Res 2014; 358: 465-479.
31. Sharp FR, Lu A, Tang Y, Millhorn DE. Multiple molecular penumbras after focal cerebral ischemia. J Cereb Blood Flow Metab 2000; 20: 1011-1032.
32. Dawson DA, Hallenbeck JM. Acute focal ischemia-induced alterations in MAP2 immunostaining: description of temporal changes and utilization as a marker for volumetric assessment of acute brain injury. J Cereb Blood Flow Metab 1996; 16: 170-174.
33. Albers GW, Goldstein LB, Hess DC, Wechsler LR, Furie KL, Gorelick PB et al. Stroke Treatment Academic Industry Roundtable (STAIR) recommendations for maximizing the use of intravenous thrombolytics and expanding treatment options with intra-arterial and neuroprotective therapies. Stroke 2011; 42: 2645-2650.
34. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009; 40: 2244-2250.
35. Yu H, Wang P, An P, Yixue X. Recombinant human angiopoietin-1 ameliorates the expressions of ZO-1, occludin, VE-cadherin, and PKC? signaling after focal cerebral ischemia/reperfusion in rats. J Mol Neurosci 2012; 46: 236-247.
36. Ito U, Ohno K, Yamaguchi T, Takei H, Tomita H, Inaba Y. Effect of hypertension on blood-brain barrier. Change after restoration of blood flow in post-ischemic gerbil brains. An electronmicroscopic study. Stroke 1980; 11: 606-611.
37. Dietrich WD, Busto R, Watson BD, Scheinberg P, Ginsberg MD. Photochemically induced cerebral infarction. II. Edema and blood-brain barrier disruption. Acta Neuropathol 1987; 72: 326-334.
38. Lin WY, Chang YC, Ho CJ, Huang CC. Ischemic preconditioning reduces neurovascular damage after hypoxia-ischemia via the cellular inhibitor of apoptosis 1 in neonatal brain. Stroke 2013; 44: 162-169.
39. Kablau M, Kreisel SH, Sauer T, Binder J, Szabo K, Hennerici MG et al. Predictors a nd early outcome of hemorrhagic transformation after acute ischemic stroke. Cerebrovasc Dis 2011; 32: 334-341.
40. Rosenberg GA, Estrada EY, Dencoff JE. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998; 29: 2189-2195.