Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage

Journal of Neuroscience

Volumn 32, Issue 9, 2012, Pages 3044-3057

  Liu, Jie ^a,b   Jin, Xinchun ^b   Liu, Ke J ^b,c   Liu, Wenlan ^b  

^a Medicial School NanHua University   (China)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CLAUDIN 5; GELATINASE A; GELATINASE B; OCCLUDIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER DAMAGE; BRAIN DAMAGE; BRAIN ISCHEMIA; CELL FRACTIONATION; CONTROLLED STUDY; ENDOTHELIUM CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; ISCHEMIC PRECONDITIONING; MALE; MICRODIALYSIS; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; OXYGEN GLUCOSE DEPRIVATION; PERMEABILITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIGHT JUNCTION; WESTERN BLOTTING; ZYMOGRAPHY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CAVEOLIN 1; CELL LINE, TUMOR; CELLS, CULTURED; CLAUDINS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MATRIX METALLOPROTEINASE 2; MEMBRANE PROTEINS; MICE; RATS; RATS, SPRAGUE-DAWLEY; STROKE;

EID: 84863230646     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6409-11.2012     Document Type: Article

References (88)

1. Alberts MJ (1998) tPA in acute ischemic stroke: United States experience and issues for the future. Neurology 51:S53-S55.
2. András IE, Pu H, Deli MA, Nath A, Hennig B, Toborek M (2003) HIV-1 Tat protein alters tight junction protein expression and distribution in cultured brain endothelial cells. J Neurosci Res 74:255-265.
3. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, Fini ME, Lo EH (2001) Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21:7724-7732.
4. Aviv RI, d'Esterre CD, Murphy BD, Hopyan JJ, Buck B, Mallia G, Li V, Zhang L, Symons SP, Lee TY (2009) Hemorrhagic transformation of ischemic stroke: prediction with CT perfusion. Radiology 250:867-877.
5. Bang OY, Buck BH, Saver JL, Alger JR, Yoon SR, Starkman S, Ovbiagele B, Kim D, Ali LK, Sanossian N, Jahan R, Duckwiler GR, Viñuela F, Salamon N, Villablanca JP, Liebeskind DS (2007) Prediction of hemorrhagic transformation after recanalization therapy using T2*-permeability magnetic resonance imaging. Ann Neurol 62:170-176.
6. Benchenane K, Berezowski V, Fernández-Monreal M, Brillault J, Valable S, Dehouck MP, Cecchelli R, Vivien D, Touzani O, Ali C (2005) Oxygen glucose deprivation switches the transport of tPA across the blood-brain barrier from an LRP-dependent to an increased LRP-independent process. Stroke 36:1065-1070.
7. Brown S, Bernardo MM, Li ZH, Kotra LP, Tanaka Y, Fridman R, Mobashery S, Sabatini DM (2000) Potent and selective mechanism-based inhibition of gelatinases. J Am Chem Soc 122:6799-6800.
8. Butcher SP, Bullock R, Graham DI, McCulloch J (1990) Correlation between amino acid release and neuropathologic outcome in rat brain following middle cerebral artery occlusion. Stroke 21:1727-1733.
9. Chen B, Friedman B, Cheng Q, Tsai P, Schim E, Kleinfeld D, Lyden PD (2009) Severe blood-brain barrier disruption and surrounding tissue injury. Stroke 40:e666-e674.
10. Date I, Takagi N, Takagi K, Tanonaka K, Funakoshi H, Matsumoto K, Nakamura T, Takeo S (2006) Hepatocyte growth factor attenuates cerebral ischemia-induced increase in permeability of the blood-brain barrier and decreases in expression of tight junctional proteins in cerebral vessels. Neurosci Lett 407:141-145.
11. De Becker A, Van Hummelen P, Bakkus M, Vande Broek I, De Wever J, De Waele M, Van Riet I (2007) Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3. Haematologica 92:440-449.
12. del Zoppo GJ, von Kummer R, Hamann GF (1998) Ischaemic damage of brain microvessels: inherent risks for thrombolytic treatment in stroke. J Neurol Neurosurg Psychiatry 65:1-9.
13. Del Zoppo GJ, Saver JL, Jauch EC, Adams HP Jr; American Heart Association Stroke Council (2009) Expansion of the time window for treatment of acute ischemic stroke with intravenous tissue plasminogen activator: a science advisory from the American Heart Association/American Stroke Association. Stroke 40:2945-2948.
14. Derex L, Nighoghossian N (2008) Intracerebral haemorrhage after thrombolysis for acute ischaemic stroke: an update. J Neurol Neurosurg Psychiatry 79:1093-1099.
15. DiNapoli VA, Huber JD, Houser K, Li X, Rosen CL (2008) Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats. Neurobiol Aging 29:753-764.
16. Eckle T, Faigle M, Grenz A, Laucher S, Thompson LF, Eltzschig HK (2008) A2B adenosine receptor dampens hypoxia-induced vascular leak. Blood 111:2024-2035.
17. ElAli A, Doeppner TR, Zechariah A, Hermann DM (2011) Increased bloodbrain barrier permeability and brain edema after focal cerebral ischemia induced by hyperlipidemia: role of lipid peroxidation and calpain-1/2, matrix metalloproteinase-2/9, and RhoA overactivation. Stroke 42:3238-3244.
18. Ellison JA, Barone FC, Feuerstein GZ (1999) Matrix remodeling after stroke. De novo expression of matrix proteins and integrin receptors. Ann N Y Acad Sci 890:204-222.
19. Floyd RA (1999) Neuroinflammatory processes are important in neurodegenerative diseases: an hypothesis to explain the increased formation of reactive oxygen and nitrogen species as major factors involved in neurodegenerative disease development. Free Radic Biol Med 26:1346-1355.
20. Förster C (2008) Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130:55-70.
21. Furuichi T, Liu W, Shi H, Miyake M, Liu KJ (2005) Generation of hydrogen peroxide during brief oxygen-glucose deprivation induces preconditioning neuronal protection in primary cultured neurons. J Neurosci Res 79:816-824.
22. Gasche Y, Soccal PM, Kanemitsu M, Copin JC (2006) Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain. Front Biosci 11:1289-1301.
23. Gerriets T, Walberer M, Ritschel N, Tschernatsch M, Mueller C, Bachmann G, Schoenburg M, Kaps M, Nedelmann M (2009) Edema formation in the hyperacute phase of ischemic stroke. Laboratory investigation. J Neurosurg 111:1036-1042.
24. Giebel SJ, Menicucci G, McGuire PG, Das A (2005) Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab Invest 85:597-607.
25. Gong Y, Hart E, Shchurin A, Hoover-Plow J (2008) Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest 118:3012-3024.
26. Grabovac V, Bernkop-Schnürch A (2006) Improvement of the intestinal membrane permeability of low molecular weight heparin by complexation with stem bromelain. Int J Pharm 326:153-159.
27. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D, Larrue V, Lees KR, Medeghri Z, Machnig T, Schneider D, von Kummer R, Wahlgren N, Toni D; ECASS Investigators (2008) Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 359:1317-1329.
28. Hallenbeck JM, Dutka AJ (1990) Background review and current concepts of reperfusion injury. Arch Neurol 47:1245-1254.
29. Hawkins BT, Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173-185.
30. Heo JH, Lucero J, Abumiya T, Koziol JA, Copeland BR, del Zoppo GJ (1999) Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab 19:624-633.
31. Hjort N, Wu O, Ashkanian M, Sølling C, Mouridsen K, Christensen S, Gyldensted C, Andersen G, Østergaard L (2008) MRI detection of early blood-brain barrier disruption: parenchymal enhancement predicts focal hemorrhagic transformation after thrombolysis. Stroke 39:1025-1028.
32. Jian Liu K, Rosenberg GA (2005) Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radic Biol Med 39:71-80.
33. Jin R, Yang G, Li G (2010) Molecular insights and therapeutic targets for blood-brain barrier disruption in ischemic stroke: critical role of matrix metalloproteinases and tissue-type plasminogen activator. Neurobiol Dis 38:376-385.
34. Jung JE, Kim GS, Chen H, Maier CM, Narasimhan P, Song YS, Niizuma K, Katsu M, Okami N, Yoshioka H, Sakata H, Goeders CE, Chan PH (2010) Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection. Mol Neurobiol 41:172-179.
35. Kamada H, Yu F, Nito C, Chan PH (2007) Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction. Stroke 38:1044-1049.
36. Kassner A, Roberts TP, Moran B, Silver FL, Mikulis DJ (2009) Recombinant tissue plasminogen activator increases blood-brain barrier disruption in acute ischemic stroke: an MR imaging permeability study. AJNR Am J Neuroradiol 30:1864-1869.
37. Kastrup A, Gröschel K, Ringer TM, Redecker C, Cordesmeyer R, Witte OW, Terborg C (2008) Early disruption of the blood-brain barrier after thrombolytic therapy predicts hemorrhage in patients with acute stroke. Stroke 39:2385-2387.
38. Kolev K, Skopál J, Simon L, Csonka E, Machovich R, Nagy Z (2003) Matrix metalloproteinase-9 expression in post-hypoxic human brain capillary endothelial cells: H2O2 as a trigger and NF-kappaB as a signal transducer. Thromb Haemost 90:528-537.
39. Kondo N, Ogawa M, Wada H, Nishikawa S (2009) Thrombin induces rapid disassembly of claudin-5 from the tight junction of endothelial cells. Exp Cell Res 315:2879-2887.
40. Larson J, Schomberg S, Schroeder W, Carpenter TC (2008) Endothelial EphA receptor stimulation increases lung vascular permeability. Am J Physiol Lung Cell Mol Physiol 295:L431-L439.
41. Latour LL, Kang DW, Ezzeddine MA, Chalela JA, Warach S (2004) Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol 56:468-477.
42. Lisanti MP, Scherer PE, Tang Z, Sargiacomo M (1994) Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis. Trends Cell Biol 4:231-235.
43. Lischper M, Beuck S, Thanabalasundaram G, Pieper C, Galla HJ (2010) Metalloproteinasemediated occludin cleavage in the cerebral microcapillary endothelium under pathological conditions. Brain Res 1326:114-127.
44. Liu S, Liu M, Peterson S, Miyake M, Vallyathan V, Liu KJ (2003) Hydroxyl radical formation is greater in striatal core than in penumbra in a rat model of ischemic stroke. J Neurosci Res 71:882-888.
45. Liu W, Furuichi T, Miyake M, Rosenberg GA, Liu KJ (2007) Differential expression of tissue inhibitor of metalloproteinases-3 in cultured astrocytes and neurons regulates the activation of matrix metalloproteinase-2. J Neurosci Res 85:829-836.
46. Liu W, Sood R, Chen Q, Sakoglu U, Hendren J, Cetin O, Miyake M, Liu KJ (2008) Normobaric hyperoxia inhibits NADPH oxidase-mediated matrix metalloproteinase-9 induction in cerebral microvessels in experimental stroke. J Neurochem 107:1196-1205.
47. Liu W, Hendren J, Qin XJ, Shen J, Liu KJ (2009a) Normobaric hyperoxia attenuates early blood-brain barrier disruption by inhibiting MMP-9-mediated occludin degradation in focal cerebral ischemia. J Neurochem 108:811-820.
48. Liu W, Hendren J, Qin XJ, Liu KJ (2009b) Normobaric hyperoxia reduces the neurovascular complications associated with delayed tissue plasminogen activator treatment in a rat model of focal cerebral ischemia. Stroke 40:2526-2531.
49. Lo AC, Chen AY, Hung VK, Yaw LP, Fung MK, Ho MC, Tsang MC, Chung SS, Chung SK (2005) Endothelin-1 overexpression leads to further water accumulation and brain edema after middle cerebral artery occlusion via aquaporin 4 expression in astrocytic end-feet. J Cereb Blood Flow Metab 25:998-1011.
50. Mattila OS, Strbian D, Saksi J, Pikkarainen TO, Rantanen V, Tatlisumak T, Lindsberg PJ (2011) Cerebral mast cells mediate blood-brain barrier disruption in acute experimental ischemic stroke through perivascular gelatinase activation. Stroke 42:3600-3605.
51. McCaffrey G, Staatz WD, Quigley CA, Nametz N, Seelbach MJ, Campos CR, Brooks TA, Egleton RD, Davis TP (2007) Tight junctions contain oligomeric protein assembly critical for maintaining blood-brain barrier integrity in vivo. J Neurochem 103:2540-2555.
52. McColl BW, Rothwell NJ, Allan SM (2008) Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 28:9451-9462.
53. Min D, Lyons JG, Jia J, Lo L, McLennan SV (2006) 2-Methoxy-2,4-diphenyl-3(2H)-furanone-labeled gelatin zymography and reverse zymography: a rapid real-time method for quantification of matrix metalloproteinases-2 and-9 and tissue inhibitors of metalloproteinases. Electrophoresis 27:357-364.
54. Nag S, Venugopalan R, Stewart DJ (2007) Increased caveolin-1 expression precedes decreased expression of occludin and claudin-5 during bloodbrain barrier breakdown. Acta Neuropathol 114:459-469.
55. Nagaraja TN, Ewing JR, Karki K, Jacobs PE, Divine GW, Fenstermacher JD, Patlak CS, Knight RA (2011) MRI and quantitative autoradiographic studies following bolus injections of unlabeled and 14C-labeled gadolinium-diethylenetriaminepentaacetic acid in a rat model of stroke yield similar distribution volumes and blood-to-brain influx rate constants. NMR Biomed 24:547-558.
56. Nakamuta M, Kotoh K, Enjoji M, Nawata H (2005) Effects of fibril-or fixed-collagen on matrix metalloproteinase-1 and tissue inhibitor of matrix metalloproteinase-1 production in the human hepatocyte cell line HLE. World J Gastroenterol 11:2264-2268.
57. Nilsson UW, Dabrosin C (2006) Estradiol and tamoxifen regulate endostatin generation via matrix metalloproteinase activity in breast cancer in vivo. Cancer Res 66:4789-4794.
58. Okamoto T, Schlegel A, Scherer PE, Lisanti MP (1998) Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273:5419-5422.
59. Romanic AM, White RF, Arleth AJ, Ohlstein EH, Barone FC (1998) Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29:1020-1030.
60. Rosenberg GA, Mun-Bryce S (2004) Matrix metalloproteinases in neuroinflammation and cerebral ischemia. Ernst Schering Res Found Workshop 2004:1-16.
61. Rosenberg GA, Estrada EY, Dencoff JE (1998) Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 29:2189-2195.
62. Sbai O, Ferhat L, Bernard A, Gueye Y, Ould-Yahoui A, Thiolloy S, Charrat E, Charton G, Tremblay E, Risso JJ, Chauvin JP, Arsanto JP, Rivera S, Khrestchatisky M (2008) Vesicular trafficking and secretion of matrix metalloproteinases-2,-9 and tissue inhibitor of metalloproteinases-1 in neuronal cells. Mol Cell Neurosci 39:549-568.
63. Sbai O, Ould-Yahoui A, Ferhat L, Gueye Y, Bernard A, Charrat E, Mehanna A, Risso JJ, Chauvin JP, Fenouillet E, Rivera S, Khrestchatisky M (2010) Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes. Glia 58:344-366.
64. Schnaeker EM, Ossig R, Ludwig T, Dreier R, Oberleithner H, Wilhelmi M, Schneider SW (2004) Microtubule-dependent matrix metalloproteinase-2/matrix metalloproteinase-9 exocytosis: prerequisite in human melanoma cell invasion. Cancer Res 64:8924-8931.
65. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V (2007) Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 6:258-268.
66. Slevin M, Krupinski J, Rovira N, Turu M, Luque A, Baldellou M, Sanfeliu C, de Vera N, Badimon L (2009) Identification of pro-angiogenic markers in blood vessels from stroked-affected brain tissue using laser-capture microdissection. BMC Genomics 10:113.
67. Smart EJ, Graf GA, McNiven MA, Sessa WC, Engelman JA, Scherer PE, Okamoto T, Lisanti MP (1999) Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 19:7289-7304.
68. Song L, Ge S, Pachter JS (2007) Caveolin-1 regulates expression of junctionassociated proteins in brain microvascular endothelial cells. Blood 109:1515-1523.
69. Stamatovic SM, Keep RF, Wang MM, Jankovic I, Andjelkovic AV (2009) Caveolae-mediated internalization of occludin and claudin-5 during CCL2-induced tight junction remodeling in brain endothelial cells. J Biol Chem 284:19053-19066.
70. Sun L, Zhou W, Mueller C, Sommer C, Heiland S, Bauer AT, Marti HH, Veltkamp R (2010) Oxygen therapy reduces secondary hemorrhage after thrombolysis in thromboembolic cerebral ischemia. J Cereb Blood Flow Metab 30:1651-1660.
71. Tanne D (2008) Imaging blood-brain barrier disruption: an evolving tool for assessing the risk of hemorrhage after thrombolysis. Nat Clin Pract Neurol 4:644-645.
72. Taraboletti G, D'Ascenzo S, Giusti I, Marchetti D, Borsotti P, Millimaggi D, Giavazzi R, Pavan A, Dolo V (2006) Bioavailability of VEGF in tumorshed vesicles depends on vesicle burst induced by acidic pH. Neoplasia 8:96-103.
73. Vorbrodt AW, Dobrogowska DH (2004) Molecular anatomy of interendothelial junctions in human blood-brain barrier microvessels. Folia Histochem Cytobiol 42:67-75.
74. Wang X, Lo EH (2003) Triggers and mediators of hemorrhagic transformation in cerebral ischemia. Mol Neurobiol 28:229-244.
75. Wang X, Lee SR, Arai K, Lee SR, Tsuji K, Rebeck GW, Lo EH (2003) Lipoproteinreceptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat Med 9:1313-1317.
76. Wang Y, Zagorevski DV, Lennartz MR, Loegering DJ, Stenken JA (2009) Detection of in vivo matrix metalloproteinase activity using microdialysis sampling and liquid chromatography/mass spectrometry. Anal Chem 81:9961-9971.
77. Wang Z, Leng Y, Tsai LK, Leeds P, Chuang DM (2011) Valproic acid attenuates blood-brain barrier disruption in a rat model of transient focal cerebral ischemia: the roles of HDAC and MMP-9 inhibition. J Cereb Blood Flow Metab 31:52-57.
78. Warach S, Latour LL (2004) Evidence of reperfusion injury, exacerbated by thrombolytic therapy, in human focal brain ischemia using a novel imaging marker of early blood-brain barrier disruption. Stroke 35:2659-2661.
79. Wen X, Li Y, Liu Y (2010) Opposite action of peroxisome proliferatoractivated receptor-γ in regulating renal inflammation: functional switch by its ligand. J Biol Chem 285:29981-29988.
80. Wolburg H, Lippoldt A (2002) Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 38:323-337.
81. Yang MZ, Mun CH, Choi YJ, Baik JH, Park KA, Lee WT, Lee JE (2007) Agmatine inhibits matrix metalloproteinase-9 via endothelial nitric oxide synthase in cerebral endothelial cells. Neurol Res 29:749-754.
82. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA (2007) Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 27:697-709.
83. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, Lawrence DA (2003) Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 112:1533-1540.
84. Yong VW, Krekoski CA, Forsyth PA, Bell R, Edwards DR (1998) Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 21:75-80.
85. Zehendner CM, Librizzi L, de Curtis M, Kuhlmann CR, 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.
86. Zhang C, An J, Haile WB, Echeverry R, Strickland DK, Yepes M (2009) Microglial low-density lipoprotein receptor-related protein 1mediates the effect of tissue-type plasminogen activator on matrix metalloproteinase-9 activity in the ischemic brain. J Cereb Blood Flow Metab 29:1946-1954.
87. Zhu D, Wang Y, Singh I, Bell RD, Deane R, Zhong Z, Sagare A, Winkler EA, Zlokovic BV (2010) Protein S controls hypoxic/ischemic blood-brain barrier disruption through the TAM receptor Tyro3 and sphingosine 1-phosphate receptor. Blood 115:4963-4972.
88. Zozulya A, Weidenfeller C, Galla HJ (2008) Pericyte-endothelial cell interaction increases MMP-9 secretion at the blood-brain barrier in vitro. Brain Res 1189:1-11.