Tamoxifen mediated estrogen receptor activation protects against early impairment of hippocampal neuron excitability in an oxygen/glucose deprivation brain slice ischemia model

Brain Research

Volumn 1247, Issue , 2009, Pages 196-211

  Zhang, Huaqiu ^a,c   Xie, Minjie ^a,c   Schools, Gary P ^a   Feustel, Paul F ^b   Wang, Wei ^c   Lei, Ting ^c   Kimelberg, Harold K ^a   Zhou, Min ^a  

^a ORDWAY RESEARCH INSTITUTE   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Acute hippocampus slice; Astrocytes; Estrogen receptor; Neuronal excitability; Neurons; Oxygen glucose deprivation; Tamoxifen

Indexed keywords

AMPA RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; GLUCOSE; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OXYGEN; PAXILLINE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN CITRATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; BRAIN OXYGEN CONSUMPTION; CELL MEMBRANE DEPOLARIZATION; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GLUCOSE BRAIN LEVEL; HIPPOCAMPUS; HORMONAL REGULATION; INTERNEURON; MALE; MEMBRANE POTENTIAL; NERVE CELL EXCITABILITY; NEUROPHYSIOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIMULATION;

ACTION POTENTIALS; ANIMALS; CYTOPROTECTION; ESTRADIOL; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MALE; NEURONS; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, ESTROGEN; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TAMOXIFEN;

RATTUS;

EID: 57549105460     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.10.015     Document Type: Article

References (47)

1. Abdullaev I.F., Rudkouskaya A., Schools G.P., Kimelberg H.K., and Mongin A.A. Pharmacological comparison of swelling-activated excitatory amino acid release and Cl- currents in cultured rat astrocytes. J. Physiol. 572 (2006) 677-689
2. Allen N.J., and Attwell D. The effect of simulated ischaemia on spontaneous GABA release in area CA1 of the juvenile rat hippocampus. J. Physiol. 561 (2004) 485-498
3. Allen N.J., Karadottir R., and Attwell D. A preferential role for glycolysis in preventing the anoxic sepolarization of rat hippocampal area CA1 pyramidal cells. J. Neurosci. 25 (2005) 848-859
4. Benhassine N., and Berger T. Homogenous distribution of large-conductance calcium-dependent potassium channels on soma and apical dendrite of rat neocortical layer 5 pyramidal neurons. Eur. J. Neurosci. 21 (2005) 914-926
5. Dhandapani K.M., and Brann D.W. Protective effects of estrogen and selective estrogen receptor modulators in the brain. Biol. Reprod. 67 (2002) 1379-1385
6. Dick G.M., Hunter A.C., and Sanders K.N. Ethylbromide tamoxifen, a membrane-impermeant antiestrogen, activates smooth muscle calcium-activated large-conductance potassium channels from the extracellular side. Mol. Pharmacol. 61 (2002) 1105-1113
7. Feustel P.J., Jin Y., and Kimelberg H.K. Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra. Stroke 35 (2004) 1164-1168
8. Fleiervish I.A., Gebhardt C., and Heinemann U. Enhance spontaneous transmitter release is the earliest consequence of neocortical hypoxia that can explain the disruption of normal circuit function. J. Neurosci. 21 (2001) 46000-46008
9. Ghatta S., Nimmagadda D., Xu X., and O'Rourke S.T. Large-conductance, calcium-activated potassium channels: structural and functional implications. Pharmacol. Ther. 110 (2006) 103-116
10. Gong L., Gao T.M., and Li X. Enhancement in activities of large conductance calcium-activated potassium channels in CA1 pyramidal neurons of rat hippocampus after transient forebrain ischemia. Brain Res. 24 (2000) 147-154
11. Gribkoff V.K., Lum-Ragan J.T., Boissard C.G., Post-Munson D.J., Meanwell N.A., Starrett Jr. J.E., Kozlowski E.S., Romine J.L., Trojnacki J.T., Mckay M.C., Zhong J., and Dworetzky S.I. Effects of channel modulators on cloned large-conductance calcium-activated potassium channels. Mol. Pharmacol. 50 (1996) 206-217
12. Gribkoff V.K., Starrett Jr. J.E., Dworetzky S.I., Hewawasam P., Boissard C.G., Cook D.A., Frantz S.W., Heman K., Hibbard J.R., Huston K., Johnson G., Krishnan B.S., Kinney G.G., Lombardo L.A., Meanwell N.A., Molinoff P.B., Myers R.A., Moon S.L., Ortiz A., Pajor L., Pieschl R.L., Post-Munson D.J., Signor L.J., Srinivas N., Taber M.T., Thalody G., Trojnacki J.T., Wiener H., Yeleswaram K., and Yeola S.W. Targeting acute ischemic stroke with a calcium-sensitive opener of maxi-K potassium channels. Nat. Med. 7 (2001) 71-477
13. Hansen A.J. Effect of anoxia on ion distribution in the brain. Physiol. Rev. 65 (1985) 101-148
14. Inoue H., and Okada Y. Roles of volume-sensitive chloride channel in excitotoxic neuronal injury. J. Neurosci. 27 (2007) 1445-1455
15. Katchman A.N., and Hershkowitz N. Early anoxia-induced vesicular glutamate release results from mobilization of calcium from intracellular stores. J. Neurophysiol. 70 (1993) 1-7
16. Katchman A.N., and Hershkowitz N. Arachidonic acid participates in the anoxia-induced increase in mEPSC frequency in CA1 neurons of the rat hippocampus. Neurosci. Lett. 28 (1994) 217-220
17. Kimelberg H.K. Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia 50 (2005) 389-397
18. Kimelberg H.K., Feustel P.J., and Jin Y. Acute treatment with tamoxifen reduces ischemic damage following middle cerebral artery occlusion. NeuroReport 11 (2000) 2675-2679
19. Kimelberg H.K., Jin Y., and Charniga C. Neuroprotective activity of tamoxifen in permanent focal ischemia. J. Neurosurg. 99 (2003) 138-142
20. Koziol J.A., and Feng A.C. On the analysis and interpretation of outcome measures in stroke clinical trials: lessons from the SAINT I study of NXY-059 for acute ischemic stroke. Stroke 37 (2006) 2644-2647
21. Kuroki Y., Fukushima K., Kanda Y., Mizuno K., and Watanabe Y. Neuroprotection by estrogen via extracellular signal-regulated kinase against quinolinic acid-induced cell death in the rat hippocampus. Eur. J. Neurosci. 13 (2001) 472-476
22. Leis J.A., Bekar L.K., and Walz W. Potassium homeostasis in the ischemic brain. Glia 50 (2005) 407-416 (review)
23. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., and Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 491 (2005) 81-95
24. Morikawa E., Ginsberg M.D., Dietrich W.D., Duncan R.C., Kraydieh S., Globus M.Y., and Busto R. The significance of brain temperature in focal cerebral ischemia: histopathological consequences of middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 12 (1992) 380-389
25. Muir K.W., and Teal P.A. Why have neuroprotectants failed? Lessons learned from stroke trails. J. Neurol. 252 (2005) 1011-1020
26. Muller M., and Somjen G.G. Na+ and K+ concentrations, extra- and intracellular voltages and the effect of TTX in hypoxic rat hippocampal slices. J. Neurophysiol. 83 (2000) 735-745
27. Nishimura I., Ui-Tei K., Saigo K., Ishii H., Sakuma Y., and Kato M. 17beta-estradiol at physiological concentrations augments Ca2+-activated K+ currents via estrogen receptor beta in the gonadotropin-releasing hormone neuronal cell line GT1-7. Endocrinol. 149 (2008) 774-782
28. Onitsuka M., Mihara S., Inokuchi H., Shigemori M., and Higashi H. Mild hypothermia protects rat hippocampal CA1 neurons from irreversible membrane dysfunction induced by experimental ischemia. Neurosci. Res. 30 (1998) 1-6
29. Osuka K., Feustel P.J., Mongin A.A., Tranmer B.I., and Kimelberg H.K. Tamoxifen inhibits nitrotyrosine formation after reversible middle cerebral artery occlusion in the rat. J. Neurochem. 76 (2001) 1842-1850
30. Plant K., Pelkey K.A., and Bortolotto Z.A. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9 (2006) 602-604
31. Quintana P., Alberi S., Hakkoum D., and Muller D. Glutamate receptor changes associated with transient anoxia/hypoglycaemia in hippocampal slice cultures. Eur. J. Neurosci. 23 (2006) 975-983
32. Raffaelli G., Saviane C., Mohajerani M.H., Pedarzani P., and Cherubini E. BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus. J Physiol. 557 Pt1 (2004) 147-157
33. Raley-Susman K.M., Kass I.S., Cottrell J.E., Newman R.B., Chambers G., and Wang J. Sodium influx blockade and hypoxic damage to CA1 pyramidal neurons in rat hippocampal slices. J. Neurophysiol. 86 (2001) 2715-2726
34. Rasband, W.S., ImageJ 1997-2004. National Institutes of Health, Bethesda, Maryland, USA, http://rsb.info.nih.gov/ij/.
35. Rossi D.J., Oshima T., and Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403 (2000) 316-332
36. Rothman S.M., and Olney J.W. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19 (1986) 105-111
37. Runden-Pran E., Hauq F.M., Storm J.F., and Ottersen O.P. BK channel activity determines the extent of cell degeneration after oxygen and glucose deprivation: a study in organotypical hippocampal slice cultures. Neuroscience 112 (2002) 277-288
38. Somogyi P., and Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 562 (2005) 9-26 (Review)
39. Sweeney M.I., Yager J.Y., Walz W., and Juurlink B.H. Cellular mechanisms involved in brain ischemia. Can. J. Physiol. Pharmacol. 73 (1995) 1525-1535
40. Taylor C.P., and Weber M.L. Effect of temperature on synaptic function after reduced oxygen and glucose in hippocampal slices. Neuroscience 52 (1993) 555-562
41. Thompson R.J., Zhou N., and MacVicar B.A. Ischemia opens neuronal gap junction hemichannels. Science 312 (2006) 924-927
42. Van Hooijdonk C.A., Glade C.P., and Van Erp P.E. TO-PRO-3 iodide: a novel HeNe laser-excitable DNA stain as an alternative for propidium iodide in multiparameter flow cytometry. Cytometry 17 (1994) 185-189
43. Wade G.N., Blaustein J.D., Gray J.M., and Mertrdith J.M. ICI 182, 780: a pure antiestrogen that affects behaviors and energy balance in rats without acting in the brain. Am. J. Physiol. 265 (1993) 1392-1398
44. Xie M.J., Wang W., Kimelberg H.K., and Zhou M. Oxygen and glucose deprivation induced changes in astrocyte membrane potential and their underlying mechanisms in acute rat hippocampal slices. J. Cereb. Blood Flow Metab. 28 (2008) 456-467
45. Zhang Y., Jin Y., Behr M.J., Feustel P.J., Morrison J.P., and Kimelberg H.K. Behavioral and histological neuroprotection by tamoxifen after reversible focal cerebral ischemia. Exp. Neurol. 196 (2005) 41-46
46. Zhang H., Schools G.P., Tin L., Wei W., Kimelberg H.K., and Zhou M. Resveratrol attenuates early pyramidal neuron excitability impairment and death in acute rat hippocampal slices caused by oxygen-glucose deprivation. Exp. Neurol. 212 (2008) 44-52
47. Zhou M., Schools G.P., and Kimelberg H.K. Development of GLAST (+) astrocytes an NG2 (+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J. Neurophysiol. 95 (2006) 134-143