Early ischemic blood brain barrier damage: A potential indicator for hemorrhagic transformation following tissue plasminogen activator (tpa) thrombolysis?

Current Neurovascular Research

Volumn 11, Issue 3, 2014, Pages 254-262

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

^a THE SECOND AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^b TONGJI HOSPITAL OF TONGJI UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF SHENZHEN UNIVERSITY   (China)

Author keywords

Blood brain barrier; Hemorrhage transformation; Ischemia stroke; Matrix metalloproteinase; Thrombolysis; Tight junction proteins; Tissue plasminogen activator

Indexed keywords

CAVEOLIN 1; CLAUDIN 5; GELATINASE A; OCCLUDIN; TISSUE PLASMINOGEN ACTIVATOR; ALTEPLASE; COUMARIN DERIVATIVE; IMM H 004; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BLOOD BRAIN BARRIER INJURY; BLOOD CLOT LYSIS; BRAIN BLOOD FLOW; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN ISCHEMIA; DISEASE SEVERITY; EVOLUTION; FIBRINOLYTIC THERAPY; HUMAN; NEUROIMAGING; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; ACUTE PHASE RESPONSE; BLOOD BRAIN BARRIER; BLOOD COMPONENT; BRAIN CAPILLARY; BRAIN DAMAGE; COMPUTER ASSISTED TOMOGRAPHY; DRUG EFFICACY; DRUG SAFETY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSTTHROMBOSIS SYNDROME; REPERFUSION INJURY; SPATIOTEMPORAL ANALYSIS;

EID: 84906849284     PISSN: 15672026     EISSN: 18755739     Source Type: Journal    
DOI: 10.2174/1567202611666140530145643     Document Type: Article

References (88)

1. Lakhan SE, Kirchgessner A, Tepper D, Leonard A. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke. Front Neurol 2013; 4: 32
2. Chapman SN, Mehndiratta P, Johansen MC, McMurry TL, Johnston KC, Southerland AM. Current perspectives on the use of intravenous recombinant tissue plasminogen activator (tPA) for treatment of acute ischemic stroke. Vasc Health Risk Manag 2014; 10: 75-87
3. Wardlaw JM, Murray V, Berge E, et al. Recombinant tissue plasminogen activator for acute ischaemic stroke: An updated systematic review and meta-Analysis. Lancet 2012; 379(9834): 2364-72
4. Foley LM, Hitchens TK, Barbe B, et al. Quantitative Temporal Profiles of Penumbra and Infarction During Permanent Middle Cerebral Artery Occlusion in Rats. Transl Stroke Res 2010; 1(3): 220-29
5. Merino JG, Warach S. Imaging of acute stroke. Nat Rev Neurol 2010; 6(10): 560-71
6. Jung JE, Kim GS, Chen H, et al. Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection. Mol Neurobiol 2010; 41(2-3): 172-9
7. Bang OY, Buck BH, Saver JL, et al. Prediction of hemorrhagic transformation after recanalization therapy using T2.*-permeability magnetic resonance imaging. Ann Neurol 2007; 62(2): 170-6
8. Hjort N, Wu O, Ashkanian M. et al. MRI detection of early bloodbrain barrier disruption: parenchymal enhancement predicts focal hemorrhagic transformation after thrombolysis. Stroke 2008; 39(3): 1025-8
9. Hom J, Dankbaar JW, Soares BP, et al. Blood-brain barrier permeability assessed by perfusion CT predicts symptomatic hemorrhagic transformation and malignant edema in acute ischemic stroke. AJNR Am J Neuroradiol 2011; 32(1): 41-8
10. Kassner A, Roberts TP, Moran B, Silver FL, Mikulis DJ. Recombinant tissue plasminogen activator increases blood-brain barrier disruption in acute ischemic stroke: An MR imaging permeability study. AJNR Am J Neuroradiol 2009; 30(10): 1864-9
11. Sun L, Zhou W, Mueller C, et al. Oxygen therapy reduces secondary hemorrhage after thrombolysis in thromboembolic cerebral ischemia. J Cereb Blood Flow Metab 2010; 30(9): 1651-60
12. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005; 57(2): 173-85
13. del Zoppo GJ. Plasminogen activators and ischemic stroke: conditions for acute delivery. Semin Thromb Hemost 2013; 39(4): 406-25
14. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V. Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 2007; 6(3): 258-68
15. Liu KJ, Rosenberg GA. Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radic Biol Med 2005; 39(1): 71-80
16. Rodrigo R, Fernandez-Gajardo R, Gutierrez R, et al. Oxidative stress and pathophysiology of ischemic stroke: novel therapeutic opportunities. CNS Neurol Disord Drug Targets 2013; 12(5): 698-714
17. O'Sullivan S, Medina C, Ledwidge M, Radomski MW, Gilmer JF. Nitric oxide-matrix metaloproteinase-9 interactions: biological and pharmacological significance-NO and MMP-9 interactions. Biochim Biophys Acta 2014; 1843(3): 603-17
18. Schofield ZV, Woodruff TM, Halai R, Wu MC, Cooper MA. Neutrophils-A key component of ischemia-reperfusion injury. Shock 2013; 40(6): 463-70
19. Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010; 67(2): 181-98
20. Rosenberg GA, Yang Y. Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus 2007; 22(5): E4
21. Pillai DR, Dittmar MS, Baldaranov D, et al. Cerebral ischemiareperfusion injury in rats-A 3 T MRI study on biphasic blood-brain barrier opening and the dynamics of edema formation. J Cereb Blood Flow Metab 2009; 29(11): 1846-55
22. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA. 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 2007; 27(4): 697-709
23. Strbian D, Durukan A, Pitkonen M, et al. The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience 2008; 153(1): 175-81
24. Durukan A, Marinkovic I, Strbian D, et al. Post-ischemic bloodbrain barrier leakage in rats: one-week follow-up by MRI. Brain Res 2009; 1280: 158-65
25. Gerriets T, Walberer M, Ritschel N, et al. Edema formation in the hyperacute phase of ischemic stroke. Laboratory investigation. J Neurosurg 2009; 111(5): 1036-42
26. DiNapoli VA, Huber JD, Houser K, Li X, Rosen CL. Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats. Neurobiol Aging 2008; 29(5): 753-64
27. Chen B, Friedman B, Cheng Q, et al. Severe blood-brain barrier disruption and surrounding tissue injury. Stroke 2009; 40(12): E666-74
28. 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(1-2): 88-96
29. Betz AL, Coester HC. Effect of steroids on edema and sodium uptake of the brain during focal ischemia in rats. Stroke 1990; 21(8): 1199-204
30. Menzies SA, Betz AL, Hoff JT. Contributions of ions and albumin to the formation and resolution of ischemic brain edema. J Neurosurg 1993; 78(2): 257-66
31. Del Zoppo GJ, Saver JL, Jauch EC, Adams HP, Jr. 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 2009; 40(8): 2945-8
32. Hacke W, Kaste M, Bluhmki E, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008; 359(13): 1317-29
33. Latour LL, Kang DW, Ezzeddine MA, Chalela JA, Warach S. Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol 2004; 56(4): 468-77
34. Warach S, Latour LL. 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 2004; 35(11 Suppl 1): 2659-61
35. Liu W, Hendren J, Qin XJ, Liu KJ. Normobaric hyperoxia reduces the neurovascular complications associated with delayed tissue plasminogen activator treatment in a rat model of focal cerebral ischemia. Stroke 2009; 40(7): 2526-31
36. Liu W, Hendren J, Qin XJ, Shen J, Liu KJ. Normobaric hyperoxia attenuates early blood-brain barrier disruption by inhibiting MMP- 9-mediated occludin degradation in focal cerebral ischemia. J Neurochem 2009; 108(3): 811-20
37. Kastrup A, Groschel K, Ringer TM, et al. Early disruption of the blood-brain barrier after thrombolytic therapy predicts hemorrhage in patients with acute stroke. Stroke 2008; 39(8): 2385-7
38. Wu L, Shen Y, Liu X, et al. The 1425G/A SNP in PRKCH is associated with ischemic stroke and cerebral hemorrhage in a Chinese population. Stroke 2009; 40(9): 2973-6
39. Aviv RI, d'Esterre CD, Murphy BD, et al. Hemorrhagic transformation of ischemic stroke: prediction with CT perfusion. Radiology 2009; 250(3): 867-77
40. Jin X, Liu J, Yang Y, Liu KJ, Liu W. Spatiotemporal evolution of blood brain barrier damage and tissue infarction within the first 3h after ischemia onset. Neurobiol Dis 2012; 48(3): 309-16
41. Nagaraja TN, Keenan KA, Fenstermacher JD, Knight RA. Acute leakage patterns of fluorescent plasma flow markers after transient focal cerebral ischemia suggest large openings in blood-brain barrier. Microcirculation 2008; 15(1): 1-14
42. Michalski D, Grosche J, Pelz J, et al. A novel quantification of blood-brain barrier damage and histochemical typing after embolic stroke in rats. Brain Res 2010
43. Jalal FY, Yang Y, Thompson J, Lopez AC, Rosenberg GA. Myelin loss associated with neuroinflammation in hypertensive rats. Stroke 2012; 43(4): 1115-22
44. Liu S, Shi H, Liu W, Furuichi T, Timmins GS, Liu KJ. Interstitial pO2 in ischemic penumbra and core are differentially affected following transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 2004; 24(3): 343-9
45. Yang GY, Betz AL. Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke 1994; 25(8): 1658-64; discussion 64-5
46. Giebel SJ, Menicucci G, McGuire PG, Das A. Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab Invest 2005; 85(5): 597-607
47. McColl BW, Rothwell NJ, Allan SM. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 2008; 28(38): 9451-62
48. McCaffrey G, Staatz WD, Quigley CA, et al. Tight junctions contain oligomeric protein assembly critical for maintaining bloodbrain barrier integrity in vivo. J Neurochem 2007; 103(6): 2540-55
49. Caron A, Desrosiers RR, Beliveau R. Ischemia injury alters endothelial cell properties of kidney cortex: stimulation of MMP-9. Exp Cell Res 2005; 310(1): 105-16
50. Egashira Y, Suzuki Y, Azuma Y, et al. The growth factor progranulin attenuates neuronal injury induced by cerebral ischemia-reperfusion through the suppression of neutrophil recruitment. J Neuroinflammation 2013; 10: 105
51. Garcia-Bonilla L, Sosti V, Campos M, et al. Effects of acute posttreatment with dipyridamole in a rat model of focal cerebral ischemia. Brain Res 2011; 1373: 211-20
52. Cheng T, Petraglia AL, Li Z, et al. Activated protein C inhibits tissue plasminogen activator-induced brain hemorrhage. Nat Med 2006; 12(11): 1278-85
53. Gu Y, Zheng G, Xu M, et al. Caveolin-1 regulates nitric oxidemediated matrix metalloproteinases activity and blood-brain barrier permeability in focal cerebral ischemia and reperfusion injury. J Neurochem 2011; 120(1): 147-56
54. Tarin C, Lavin B, Gomez M, Saura M, Diez-Juan A, Zaragoza C. The extracellular matrix metalloproteinase inducer EMMPRIN is a target of nitric oxide in myocardial ischemia/reperfusion. Free Radic Biol Med 2011; 51(2): 387-95
55. Slevin M, Krupinski J, Rovira N, et al. Identification of proangiogenic markers in blood vessels from stroked-Affected brain tissue using laser-capture microdissection. BMC Genomics 2009; 10: 113
56. Yang MZ, Mun CH, Choi YJ, et al. Agmatine inhibits matrix metalloproteinase-9 via endothelial nitric oxide synthase in cerebral endothelial cells. Neurol Res 2007; 29(7): 749-54
57. Candela ME, Geraci F, Turturici G, Taverna S, Albanese I, Sconzo G. Membrane vesicles containing matrix metalloproteinase-9 and fibroblast growth factor-2 are released into the extracellular space from mouse mesoangioblast stem cells. J Cell Physiol 2010; 224(1): 144-51
58. Sbai O, Ferhat L, Bernard A, et al. Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells. Mol Cell Neurosci 2008; 39(4): 549-68
59. Liu J, Jin X, Liu KJ, Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. J Neurosci 2012; 32(9): 3044-57
60. Liu W, Furuichi T, Miyake M, Rosenberg GA, Liu KJ. Differential expression of tissue inhibitor of metalloproteinases-3 in cultured astrocytes and neurons regulates the activation of matrix metalloproteinase-2. J Neurosci Res 2007; 85(4): 829-36
61. Yong VW, Krekoski CA, Forsyth PA, Bell R, Edwards DR. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 1998; 21(2): 75-80
62. Lischper M, Beuck S, Thanabalasundaram G, Pieper C, Galla HJ. Metalloproteinase mediated occludin cleavage in the cerebral microcapillary endothelium under pathological conditions. Brain Res 2010; 1326: 114-27
63. Song L, Ge S, Pachter JS. Caveolin-1 regulates expression of junction-Associated proteins in brain microvascular endothelial cells. Blood 2007; 109(4): 1515-23
64. Andras IE, Pu H, Deli MA, Nath A, Hennig B, Toborek M. HIV-1 Tat protein alters tight junction protein expression and distribution in cultured brain endothelial cells. J Neurosci Res 2003; 74(2): 255-65
65. Kondo N, Ogawa M, Wada H, Nishikawa S. Thrombin induces rapid disassembly of claudin-5 from the tight junction of endothelial cells. Exp Cell Res 2009; 315(17): 2879-87
66. Larson J, Schomberg S, Schroeder W, Carpenter TC. Endothelial EphA receptor stimulation increases lung vascular permeability. Am J Physiol Lung Cell Mol Physiol 2008; 295(3): L431-9
67. Chidlow JH, Jr., Sessa WC. Caveolae, caveolins, and cavins: complex control of cellular signalling and inflammation. Cardiovasc Res 2010; 86(2): 219-25
68. Kong MM, Hasbi A, Mattocks M, Fan T, O'Dowd BF, George SR. Regulation of D1 dopamine receptor trafficking and signaling by caveolin-1. Mol Pharmacol 2007; 72(5): 1157-70
69. Nag S, Venugopalan R, Stewart DJ. Increased caveolin-1 expression precedes decreased expression of occludin and claudin- 5 during blood-brain barrier breakdown. Acta Neuropathol 2007; 114(5): 459-69
70. Stamatovic SM, Keep RF, Wang MM, Jankovic I, Andjelkovic AV. Caveolae-mediated internalization of occludin and claudin-5 during CCL2-induced tight junction remodeling in brain endothelial cells. J Biol Chem 2009; 284(28): 19053-66
71. Zehendner CM, Librizzi L, de Curtis M, Kuhlmann CR, Luhmann HJ. Caspase-3 contributes to ZO-1 and Cl-5 tight-junction disruption in rapid anoxic neurovascular unit damage. PLoS One 2011; 6(2): E16760
72. Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke. The NINDS t-PA Stroke Study Group. Stroke 1997; 28(11): 2109-18
73. Weintraub MI. Thrombolysis (tissue plasminogen activator) in stroke: A medicolegal quagmire. Stroke 2006; 37(7): 1917-22
74. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, Lawrence DA. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 2003; 112(10): 1533-40
75. Hoffmann A, Zhu G, Wintermark M. Advanced neuroimaging in stroke patients: prediction of tissue fate and hemorrhagic transformation. Expert Rev Cardiovasc Ther 2012; 10(4): 515-24
76. Zhu G, Michel P, Aghaebrahim A, et al. Computed tomography workup of patients suspected of acute ischemic stroke: perfusion computed tomography adds value compared with clinical evaluation, noncontrast computed tomography, and computed tomography angiogram in terms of predicting outcome. Stroke 2013; 44(4): 1049-55
77. Rouchaud A, Pistocchi S, Blanc R, Engrand N, Bartolini B, Piotin M. Predictive value of flat-panel CT for haemorrhagic transformations in patients with acute stroke treated with thrombectomy. J Neurointerv Surg 2013; 6(2): 139-43
78. Thornhill RE, Chen S, Rammo W, Mikulis DJ, Kassner A. Contrast-enhanced MR imaging in acute ischemic stroke: T2.* measures of blood-brain barrier permeability and their relationship to T1 estimates and hemorrhagic transformation. AJNR Am J Neuroradiol 2010; 31(6): 1015-22
79. Nguyen GT, Coulthard A, Wong A, et al. Measurement of bloodbrain barrier permeability in acute ischemic stroke using standard first-pass perfusion CT data. Neuroimage Clin 2013; 2: 658-62
80. Kuntz M, Mysiorek C, Petrault O, et al. Stroke-induced brain parenchymal injury drives blood-brain barrier early leakage kinetics: A combined in vivo/in vitro study. J Cereb Blood Flow Metab 2014; 34(1): 95-107
81. Fisher M, Albers GW. Advanced imaging to extend the therapeutic time window of acute ischemic stroke. Ann Neurol 2013; 73(1): 4-9
82. Kudo K, Christensen S, Sasaki M, et al. Accuracy and reliability assessment of CT and MR perfusion analysis software using a digital phantom. Radiology 2014; 267(1): 201-11
83. O'Collins VE, Macleod MR, Donnan GA, Howells DW. Evaluation of combination therapy in animal models of cerebral ischemia. J Cereb Blood Flow Metab 2012; 32(4): 585-97
84. Jin X, Liu J, Liu KJ, Rosenberg GA, Yang Y, Liu W. Normobaric hyperoxia combined with minocycline provides greater neuroprotection than either alone in transient focal cerebral ischemia. Exp Neurol 2013; 240: 9-16
85. Zuo W, Chen J, Zhang S, et al. IMM-H004 prevents toxicity induced by delayed treatment of tPA in a rat model of focal cerebral ischemia involving PKA-And PI3K-dependent Akt activation. Eur J Neurosci 2014; 39(12): 2107-18
86. Houng AK, Wang D, Reed GL. Reversing the deleterious effects of alpha2-Antiplasmin on tissue plasminogen activator therapy improves outcomes in experimental ischemic stroke. Exp Neurol 2014; 255: 56-62
87. Michalski D, Hobohm C, Weise C, et al. Interrelations between blood-brain barrier permeability and matrix metalloproteinases are differently affected by tissue plasminogen activator and hyperoxia in a rat model of embolic stroke. Med Gas Res 2012; 2(1): 2
88. Michalski D, Kuppers-Tiedt L, Weise C, et al. Long-term functional and neurological outcome after simultaneous treatment with tissue-plasminogen activator and hyperbaric oxygen in e phase of embolic stroke in rats. Brain Res 2009; 1303: 161-8