17β-Estradiol attenuates blood-brain barrier disruption induced by cerebral ischemia-reperfusion injury in female rats

Brain Research

Volumn 1060, Issue 1-2, 2005, Pages 55-61

  Liu, Ran ^a   Wen, Yi ^a   Perez, Evelyn ^a   Wang, Xiaofei ^a   Day, Arthur L ^b   Simpkins, James W ^a   Yang, Shao Hua ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Blood brain barrier; Cerebral ischemia; Estrogen; Matrix metalloproteinase; Neuroprotection; Reperfusion injury

Indexed keywords

ESTRADIOL; EVANS BLUE; GELATINASE A; GELATINASE B; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRAVASATION; FEMALE; FLUORESCENCE; IMMUNOBLAST; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; ANIMAL; BRAIN; ENZYMOLOGY; METABOLISM; PATHOLOGY; TRANSIENT ISCHEMIC ATTACK; WESTERN BLOTTING;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; ENZYME ACTIVATION; ESTRADIOL; FEMALE; ISCHEMIC ATTACK, TRANSIENT; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NEUROPROTECTIVE AGENTS; RATS; REPERFUSION INJURY;

EID: 26944469603     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2005.08.048     Document Type: Article

References (42)

1. N.J. Alkayed, I. Harukuni, A.S. Kimes, E.D. London, R.J. Traystman, and P.D. Hurn Gender-linked brain injury in experimental stroke Stroke 29 1998 159 165 (discussion 166)
2. S. Bake, and F. Sohrabji 17Beta-estradiol differentially regulates blood-brain barrier permeability in young and aging female rats Endocrinology 145 2004 5471 5475
3. P. Ballabh, A. Braun, and M. Nedergaard The blood-brain barrier: an overview: structure, regulation, and clinical implications Neurobiol. Dis. 16 2004 1 13
4. B. Beekman, J.W. Drijfhout, W. Bloemhoff, H.K. Ronday, P.P. Tak, and J.M. te Koppele Convenient fluorometric assay for matrix metalloproteinase activity and its application in biological media FEBS Lett. 390 1996 221 225
5. L. Belayev, R. Busto, W. Zhao, and M.D. Ginsberg Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats Brain Res. 739 1996 88 96
6. J. Bishop, and J.W. Simpkins Estradiol treatment increases viability of glioma and neuroblastoma cells in vitro Mol. Cell. Neurosci. 5 1994 303 308
7. R.C. Brown, and T.P. Davis Calcium modulation of adherens and tight junction function: a potential mechanism for blood-brain barrier disruption after stroke Stroke 33 2002 1706 1711
8. O.Z. Chi, X. Liu, and H.R. Weiss Effects of 17beta-estradiol on blood-brain barrier disruption during focal ischemia in rats Horm. Metab. Res. 34 2002 530 534
9. O.Z. Chi, S. Barsoum, Y. Wen, X. Liu, and H.R. Weiss 17Beta-estradiol prevents blood-brain barrier disruption induced by VEGF Horm. Metab. Res. 36 2004 272 276
10. A.W. Clark, C.A. Krekoski, S.S. Bou, K.R. Chapman, and D.R. Edwards Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia Neurosci. Lett. 238 1997 53 56
11. H.E. de Vries, M.C. Blom-Roosemalen, M. van Oosten, A.G. de Boer, T.J. van Berkel, D.D. Breimer, and J. Kuiper The influence of cytokines on the integrity of the blood-brain barrier in vitro J. Neuroimmunol. 64 1996 37 43
12. K. Dhandapani, and D. Brann Neuroprotective effects of estrogen and tamoxifen in vitro: a facilitative role for glia? Endocrine 21 2003 59 66
13. D.B. Dubal, M.L. Kashon, L.C. Pettigrew, J.M. Ren, S.P. Finklestein, S.W. Rau, and P.M. Wise Estradiol protects against ischemic injury J. Cereb. Blood Flow Metab. 18 1998 1253 1258
14. T. Fan, S.H. Yang, E. Johnson, B. Osteen, R. Hayes, A.L. Day, and J.W. Simpkins 17Beta-estradiol extends ischemic thresholds and exerts neuroprotective effects in cerebral subcortex against transient focal cerebral ischemia in rats Brain Res. 993 2003 10 17
15. K. Fukuda, H. Yao, S. Ibayashi, T. Nakahara, H. Uchimura, M. Fujishima, and E.D. Hall Ovariectomy exacerbates and estrogen replacement attenuates photothrombotic focal ischemic brain injury in rats Stroke 31 2000 155 160
16. S. Fukuda, C.A. Fini, T. Mabuchi, J.A. Koziol, L.L. Eggleston Jr., and G.J. del Zoppo Focal cerebral ischemia induces active proteases that degrade microvascular matrix Stroke 35 2004 998 1004
17. Y. Gasche, M. Fujimura, Y. Morita-Fujimura, J.C. Copin, M. Kawase, J. Massengale, and P.H. Chan 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. 19 1999 1020 1028
18. P.S. Green, and J.W. Simpkins Neuroprotective effects of estrogens: potential mechanisms of action Int. J. Dev. Neurosci. 18 2000 347 358
19. K.A. Harkness, P. Adamson, J.D. Sussman, G.A. Davies-Jones, J. Greenwood, and M.N. Woodroofe Dexamethasone regulation of matrix metalloproteinase expression in CNS vascular endothelium Brain 123 Pt.4 2000 698 709
20. T. Jover, H. Tanaka, A. Calderone, K. Oguro, M.V. Bennett, A.M. Etgen, and R.S. Zukin Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1 J. Neurosci. 22 2002 2115 2124
21. W.J. Lee, C.Y. Shin, B.K. Yoo, J.R. Ryu, E.Y. Choi, J.H. Cheong, J.H. Ryu, and K.H. Ko Induction of matrix metalloproteinase-9 (MMP-9) in lipopolysaccharide-stimulated primary astrocytes is mediated by extracellular signal-regulated protein kinase 1/2 (Erk1/2) Glia 41 2003 15 24
22. S.R. Lee, K. Tsuji, and E.H. Lo Role of matrix metalloproteinases in delayed neuronal damage after transient global cerebral ischemia J. Neurosci. 24 2004 671 678
23. R. Liu, S.H. Yang, E. Perez, K.D. Yi, S.S. Wu, K. Eberst, L. Prokai, K. Prokai-Tatrai, Z.Y. Cai, D.F. Covey, A.L. Day, and J.W. Simpkins Neuroprotective effects of a novel non-receptor-binding estrogen analogue: in vitro and in vivo analysis Stroke 33 2002 2485 2491
24. A. Lu, R.Q. Ran, J. Clark, M. Reilly, A. Nee, and F.R. Sharp 17-Beta-estradiol induces heat shock proteins in brain arteries and potentiates ischemic heat shock protein induction in glia and neurons J. Cereb. Blood Flow Metab. 22 2002 183 195
25. M.F. McCarty Up-regulation of endothelial nitric oxide activity as a central strategy for prevention of ischemic stroke-just say NO to stroke! Med. Hypotheses 55 2000 386 403
26. S. Mun-Bryce, and G.A. Rosenberg Gelatinase B modulates selective opening of the blood-brain barrier during inflammation Am. J. Physiol. 274 1998 R1203 R1211
27. S. Mun-Bryce, and G.A. Rosenberg Matrix metalloproteinases in cerebrovascular disease J. Cereb. Blood Flow Metab. 18 1998 1163 1172
28. M.E. O'Donnell, L. Tran, T.I. Lam, X.B. Liu, and S.E. Anderson Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke J. Cereb. Blood Flow Metab. 24 2004 1046 1056
29. J.A. Ospina, H.N. Brevig, D.N. Krause, and S.P. Duckles Estrogen suppresses IL-1beta-mediated induction of COX-2 pathway in rat cerebral blood vessels Am. J. Physiol.: Heart Circ. Physiol. 286 2004 H2010 H2019
30. W.M. Pardridge Blood-brain barrier drug targeting enables neuroprotection in brain ischemia following delayed intravenous administration of neurotrophins Adv. Exp. Med. Biol. 513 2002 397 430
31. S.W. Rau, D.B. Dubal, M. Bottner, L.M. Gerhold, and P.M. Wise Estradiol attenuates programmed cell death after stroke-like injury J. Neurosci. 23 2003 11420 11426
32. M. Razandi, A. Pedram, and E.R. Levin Estrogen signals to the preservation of endothelial cell form and function J. Biol. Chem. 275 2000 38540 38546
33. S. Rivera, C. Ogier, J. Jourquin, S. Timsit, A.W. Szklarczyk, K. Miller, A.J. Gearing, L. Kaczmarek, and M. Khrestchatisky Gelatinase B and TIMP-1 are regulated in a cell- and time-dependent manner in association with neuronal death and glial reactivity after global forebrain ischemia Eur. J. Neurosci. 15 2002 19 32
34. G.A. Rosenberg Matrix metalloproteinases in neuroinflammation Glia 39 2002 279 291
35. G.A. Rosenberg, E.Y. Estrada, and J.E. Dencoff Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain Stroke 29 1998 2189 2195
36. J. Shi, J.D. Bui, S.H. Yang, Z. He, T.H. Lucas, D.L. Buckley, S.J. Blackband, M.A. King, A.L. Day, and J.W. Simpkins Estrogens decrease reperfusion-associated cortical ischemic damage: an MRI analysis in a transient focal ischemia model Stroke 32 2001 987 992
37. J.W. Simpkins, G. Rajakumar, Y.Q. Zhang, C.E. Simpkins, D. Greenwald, C.J. Yu, N. Bodor, and A.L. Day Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat J. Neurosurg. 87 1997 724 730
38. E. Vegeto, C. Bonincontro, G. Pollio, A. Sala, S. Viappiani, F. Nardi, A. Brusadelli, B. Viviani, P. Ciana, and A. Maggi Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia J. Neurosci. 21 2001 1809 1818
39. Y. Wen, S. Yang, R. Liu, E. Perez, K.D. Yi, P. Koulen, and J.W. Simpkins Estrogen attenuates nuclear factor-kappa B activation induced by transient cerebral ischemia Brain Res. 1008 2004 147 154
40. S.H. Yang, E. Perez, J. Cutright, R. Liu, Z. He, A.L. Day, and J.W. Simpkins Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model J. Appl. Physiol. 92 2002 195 201
41. S.H. Yang, R. Liu, E.J. Perez, X. Wang, and J.W. Simpkins Estrogens as protectants of the neurovascular unit against ischemic stroke Curr. Drug Targets. CNS Neurol. Disord. 4 2005 169 177
42. V.W. Yong, C. Power, P. Forsyth, and D.R. Edwards Metalloproteinases in biology and pathology of the nervous system Nat. Rev., Neurosci. 2 2001 502 511