Estrogen-receptor-mediated protection of cerebral endothelial cell viability and mitochondrial function after ischemic insult in vitro

Journal of Cerebral Blood Flow and Metabolism

Volumn 30, Issue 3, 2010, Pages 545-554

  Guo, Jiabin ^a,b   Krause, Diana N ^b   Horne, James ^b   Weiss, John H ^b   Li, Xuejun ^a   Duckles, Sue P ^b  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cerebral ischemia and or reperfusion; Estradiol; Estrogen protection

Indexed keywords

ADENOSINE TRIPHOSPHATE; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; GLUCOSE; OXYGEN; SUPEROXIDE;

ANIMAL CELL; ARTICLE; BRAIN BLOOD VESSEL; BRAIN CELL; BRAIN ISCHEMIA; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY;

ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; BRAIN ISCHEMIA; CELL LINE; CELL SURVIVAL; ENDOTHELIAL CELLS; ESTROGENS; GLUCOSE; HYPOXIA, BRAIN; L-LACTATE DEHYDROGENASE; MEMBRANE POTENTIALS; MICE; MITOCHONDRIA; RECEPTORS, ESTROGEN; REPERFUSION INJURY; SUPEROXIDES;

EID: 77649275015     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2009.226     Document Type: Article

References (43)

1. Adam-Vizi V (2005) Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid Redox Signal 7:1140-1149
2. Alonso de Leciñana M, Egido JA (2006) Estrogens asneur-oprotectants against ischemic stroke. Cerebrovasc Dis 21:48-53
3. Andjelkovic AV, Stamatovic SM, Keep RF (2003) The protective effects of preconditioning on cerebral en-dothelial cells in vitro. J Cereb Blood Flow Metab 23:1348-1355
4. Araújo GW, Beyer C, Arnold S (2008) Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes. J Neuroendocrinol 20:930-941
5. Bastide M, Ouk T, Plaisier F, Petrault O, Stolc S, Bordet R (2007) Neurogliovascular unit after cerebral ischemia: is the vascular wall a pharmacological target. Psychoneur-oendocrinology 32:s36-9
6. 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
7. Bushnell CD, Hurn P, Colton C, Miller VM, del Zoppo G, Elkin MSV, Stern B, Herrington D, Ford-Lynch G, Gorelick P, James A, Brown CM, Choi E, Bray P, Newby LK, Goldstein LB, Simpkins J (2006) Advancing the study of stroke in women. Stroke 37:2387-2399
8. del Zoppo GJ, Mabuchi T (2003) Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab 23:879-894
9. Davidson SM, Duchen MR (2007) Endothelial mitochondria: contributing to vascular function and disease. Circ Res 100:1128-1141
10. Dhandapani KM, Brann DW (2007) Role of astrocytes in estrogen-mediated neuroprotection. Exp Gerontol 42:70-75
11. Dubal DB, Rau SW, Shughrue PJ, Zhu H, Yu J, Cashion AB, Suzuki S, Gerhold LM, Bottner MB, Dubal SB, Merchanthaler I, Kindy MS, Wise PM (2006) Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERalpha in estradiol-mediated protection against delayed cell death. Endocrinology 147:3076-3084
12. Duckles SP, Krause DN, Stirone C Procaccio V (2006) Estrogen and mitochondria: a new paradigm for vascular protection? Mol Interv 6:26-35
13. Fiskum G, Rosenthal RE, Vereczki V, Martin E, Hoffman GE, Chinopoulos C, Kowaltowski A (2004) Protection against ischemic brain injury by inhibition of mitochon-drial oxidative stress. J Bioenerg Biomembr 36:347-352 (Pubitemid 39619839)
14. Flynn JM, Dimitrijevich SD, Younes M, Skliris G, Murphy LC, Cammarata PR (2008) Role of wild-type estrogen receptor-beta in mitochondrial cytoprotection of cultured normalmaleand femalehuman lens epithelial cells. Am J Physiol Endocrinol Metab 295:E637-47
15. Gibson CL, Gray LJ, Murphy SP, Bath PMW (2006) Estrogens and experimental ischemic stroke: a systematic review. J Cereb Blood Flow Metab 26:1103-1113
16. Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenel-lenbogen JA, Katzenellenbogen BS (2003) Activities of estrogen receptor alpha-and beta-selective ligands at diverse estrogen responsive gene sites mediating trans-activation or transrepression. Mol Cell Endocrinol 206:13-22
17. Hawkins BT, Davis TP (2005) The blood-brain barrier/ neurovascular unit in health and disease. Pharmacol Rev 57:173-185
18. Iadecola C, Goldman SS, Harder DR, Heistad DD, Katusic ZS, Moskowitz MA, Simard JM, Sloan MA, Traystman RJ, Velletri PA (2006) Recommendations of the National Heart, Lung, and Blood Institute working group on cerebrovascular biology and disease. Stroke 37:1578-1581
19. Irwin RW, Yao J, Hamilton RT, Cadenas E, Brinton RD, Nilsen J (2008) Progesterone and estrogen regulate oxidative metabolism in brain mitochondria. Endocrinology 149:3167-3175
20. Koopman WJ, Distelmaier F, Esseling JJ, Smeitink JA, Willems PH (2008) Computer-assisted live cell analysis of mitochondrial membrane potential, morphology and calcium handling. Methods 46:304-311
21. Krause DK, Duckles SP, Pelligrino DA (2006) Influence of sex steroid hormones on cerebrovascular function. J Appl Physiol 101:1252-1261
22. Liu F, Yuan R, Benashski SE, McCullough LD (2009) Changes in experimental stroke outcome across the life span. J Cereb Blood Flow Metab 29:792-802
23. Liu R, Wen Y, Perez E, Wang X, Day AL, Simpkins JW, Yang SH (2005) 17beta-Estradiol attenuates blood-brain barrier disruption induced by cerebral ischemia-reperfu-sion injury in female rats. Brain Res 1060:55-61
24. Miller VM, Duckles SP (2008) Vascular actions of estrogens: functional implications. Pharmacol Rev 60:210-241
25. Nilsen J, Chen S, Irwin RW, Iwamoto S, Brinton RD (2006) Estrogen protects neuronal cells from amyloid beta-induced apoptosis via regulation of mitochondrial proteins and function. BMC Neurosci 7:74
26. Noppens RR, Kofler J, Grafe MR, Hurn PD, Traystman RJ (2009) Estradiol after cardiac arrest and cardiopulmon-ary resuscitation is neuroprotective and mediated through estrogen receptor-beta. J Cereb Blood Flow Metab 29:277-286
27. Odenlund M, Ekblad E, Nilsson BO (2008) Stimulation of oestrogen receptor-expressing endothelial cells with oestrogen reduces proliferation of cocultured vascular smooth muscle cells. Clin Exp Pharmacol Physiol 35:245-248
28. Oldendorf WH, Cornford ME, Brown WJ (1977) The large apparent work capability of the blood-brain barrier: a study of the mitochondrial content of capillary en-dothelial cells in brain and other tissues of the rat. Ann Neurol 1:409-417
29. Omidi Y, Campbell L, Barar J, Connell D, Akhtar S, Gumbleton M (2003) Evaluation of the immortalised mouse brain capillary endothelial cell line, b.End3, asan in vitro blood-brain barrier model for drug uptake transport studies. Brain Res 990:95-112
30. Prokai L, Prokai-Tatrai K, Perjesi P, Zharikova Ad, Perez EJ, Liu R, Simpkins JW (2003) Quinol-based cyclic anti-oxidant mechanism in estrogen neuroprotection. Proc Natl Acad Sci USA 100:11741-11746
31. Ramsauer M, Kuntz J, Krause D, Dermietzel R (1998) Regulation of a blood-brain barrier-specific enzyme expressed by cerebral pericytes (pericytic aminopepti-dase N/pAPN) under cell culture conditions. J Cereb Blood Flow Metab 18:1270-1281
32. Raval AP, Bramlett H, Perez-Pinzon MA (2006) Estrogen preconditioning protects the hippocampal CA1 against ischemia. Neuroscience 141:1721-1730
33. Razmara A, Duckles SP, Krause DN, Procaccio V (2007) Estrogen suppresses brain mitochondrial oxidative stress in female and male rats. Brain Res 1176:71-81
34. Razmara A, Sunday L, Stirone C, Wang XB, Krause DN, Duckles SP, Procaccio V (2008) Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain endothelial cells. J Pharmacol Exp Ther 325: 782-790
35. Santizo RA, Anderson S, Ye S, Koenig HM, Pelligrino DA (2000) Effects of estrogen on leukocyte adhesion after transient forebrain ischemia. Stroke 31:2231-2235
36. Simpkins JW, Dykens JA (2008) Mitochondrial mechanisms of estrogen neuroprotection. Brain Res Rev 57: 421-430
37. Sims NR, Anderson MF (2002) Mitochondrial contributions to tissue damage in stroke. Neurochem Int 40: 511-526
38. Stirone C, Duckles SP, Krause DN (2003) Multiple forms of estrogen receptor-alpha in cerebral blood vessels: regulation by estrogen. Am J Physiol 284:E184-92
39. Stirone C, Duckles SP, Krause DN, Procaccio V (2005) Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral vessels. Mol Pharmacol 68:959-965
40. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359-407
41. Wilson ME, Dubal DB, Wise PM (2000) Estradiol protects against injury-induced cell death in cortical explants cultures: a role for estrogen receptors. Brain Res 873:235-242
42. Yang SH, Sarkar SN, Liu R, Perez EJ, Wang X, Wen Y, Yan LJ, Simpkins JW (2009) Estrogen receptor beta as a mitochondrial vulnerability factor. J Biol Chem 284:9540-9548
43. Zhang Y, Park TS, Gidday JM (2007) Hypoxic preconditioning protects human brain endothelium from is-chemic apoptosis by Akt-dependent surviving activation. Am J Physiol Heart Circ Physiol 292: H2573-81