Neuroprotective action of raloxifene against hypoxia-induced damage in mouse hippocampal cells depends on ERα but not ERβ or GPR30 signalling

Journal of Steroid Biochemistry and Molecular Biology

Volumn 146, Issue , 2015, Pages 26-37

  Rzemieniec, J ^a   Litwa, E ^a   Wnuk, A ^a   Lason, W ^a   Golas A ^b   Krzeptowski, W ^b   Kajta, M ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

^b JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Apoptosis; Immunoblots; Primary neuronal cell cultures; SERMs; siRNAs

Indexed keywords

4 [2 PHENYL 5,7 BIS(TRIFLUOROMETHYL)PYRAZOLO[1,5,A]PYRIMIDIN 3 YL]PHENOL; ADENOSINE TRIPHOSPHATASE; CASPASE 3; ESTERASE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; G PROTEIN COUPLED RECEPTOR 30; HOE 33342; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LACTATE DEHYDROGENASE; MESSENGER RNA; METHYLPIPERIDINOPYRAZOLE; NEUROPROTECTIVE AGENT; RALOXIFENE; STEROID HORMONE RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; GPR30 PROTEIN, MOUSE; HIF1A PROTEIN, MOUSE; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN HYPOXIA; BRAIN INJURY; CELL DAMAGE; CELL HYPOXIA; CELL NUCLEUS; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; EMBRYO; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NEUROPROTECTION; NONHUMAN; PRIMARY CULTURE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; ANOXIA; CELL CULTURE; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ANOXIA; CASPASE 3; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; L-LACTATE DEHYDROGENASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NEUROPROTECTIVE AGENTS; RALOXIFENE; RECEPTORS, G-PROTEIN-COUPLED; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SIGNAL TRANSDUCTION;

EID: 84918580079     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.05.005     Document Type: Article

References (48)

1. S.J. Choi, I.J. Shin, K.H. Je, E.K. Min, E.J. Kim, H.S. Kim, S. Choe, D.E. Kim, D.K. Lee, Hypoxia antagonizes glucose deprivation on interleukin 6 expression in an Akt dependent, but HIF-1/2α independent manner, PLoS One 8 (2013) e58662, http://dx.doi.org/10.1371/journal.pone.0058662.
2. R. Tuma, The two faces of oxygen, Sci. Aging Knowledge Environ. (2001) oa5, http://dx.doi.org/10.1126/sageke.2001.1.oa.
3. A. Jose, J. Matthai, S. Paul, Correlation of EEG, CT, and MRI brain with neurological outcome at 12 months in term newborns with hypoxic ischemic encephalopathy, J. Clin. Neonatol. 2 (2013) 125-130, http://dx.doi.org/10.4103/2249-4847.119996.
4. M. El Amki, D. Lerouet, B. Coqueran, E. Curis, C. Orset, D. Vivien, M. Plotkine, C. Marchand-Leroux, I. Margaill, Experimental modeling of recombinant tissue plasminogen activator effects after ischemic stroke, Exp. Neurol. 238 (2012) 138-144, http://dx.doi.org/10.1016/j.expneurol.2012.08.005.
5. R.F. Soll, Cooling for newborns with hypoxic ischemic encephalopathy, Neonatolog 104 (2013) 260-262, http://dx.doi.org/10.1159/000353681.
6. D. Bushnell Cheryl, Stroke in women: risk and prevention throughout the lifespan, Neurol. Clin. 26 (2008) 1161-xi, http://dx.doi.org/10.1016/j.ncl.2008.05.009.
7. Y.L. Ma, P. Qin, Y. Li, L. Shen, S.Q. Wang, H.L. Dong, W.G. Hou, L.Z. Xiong, The effects of different doses of estradiol (E2) on cerebral ischemia in an in vitro model of oxygen and glucose deprivation and reperfusion and in a rat model of middle carotid artery occlusion, M BMC Neurosci. 14 (2013) 118, http://dx.doi.org/10.1186/1471-2202-14-118.
8. J. Dang, B. Mitkari, M. Kipp, C. Beyer, Gonadal steroids prevent cell damage and stimulate behavioral recovery after transient middle cerebral artery occlusion in male and female rats, Brain Behav. Immun. 25 (2011) 715-726, http://dx.doi.org/10.1016/j.bbi.2011.01.013.
9. D. Lebesgue, V. Chevaleyre, R.S. Zukin, A.M. Etgen, Estradiol rescues neurons from global ischemia-induced cell death: multiple cellular pathways of neuroprotection, Steroids 74 (2009) 555-561, http://dx.doi.org/10.1016/j.steroids.2009.01.003.
10. A.M. Billeci, M. Paciaroni, V. Caso, G. Agnelli, Hormone replacement therapy and stroke, Curr. Vasc. Pharmacol. 6 (2008) 112-123, http://dx.doi.org/10.2174/157016108783955338.
11. J.S. Lewis, V.C. Jordan, Selective estrogen receptor modulators (SERMs): mechanisms of anticarcinogenesis and drug resistance, Mutat. Res. 591 (2005) 247-263, http://dx.doi.org/10.1016/j.mrfmmm.2005.02.028.
12. J.R. Rey, E.V. Cervino, M.L. Rentero, E.C. Crespo, A.O. Alvaro, M. Casillas, Raloxifene: mechanism of action, effects on bone tissue, and applicability in clinical traumatology practice, Open Orthop. J. 3 (2009) 14-21, http://dx.doi.org/10.2174/1874325000903010014.
13. Y. Maximov Philipp, Theresa M. Lee, V. Craig Jordan, The discovery and development of selective estrogen receptor modulators (SERMs) for clinical practice, Curr. Clin. Pharmacol. 8 (2013) 135-155, http://dx.doi.org/10.2174/1574884711308020006.
14. W.C. Park, V.C. Jordan, Selective estrogen receptor modulators (SERMS) and their roles in breast cancer prevention, Trends Mol. Med. 8 (2002) 82-88, http://dx.doi.org/10.1016/S1471-4914(02)02282-7.
15. S. Benvenuti, P. Luciani, G.B. Vannelli, S. Gelmini, E. Franceschi, M. Serio, A. Peri, Estrogen and selective estrogen receptor modulators exert neuroprotective effects and stimulate the expression of selective Alzheimer's disease indicator-1, a recently discovered antiapoptotic gene, in human neuroblast long-term cell cultures, J. Clin. Endocrinol. Metab. 90 (2005) 1775-1782, http://dx.doi.org/10.1210/jc.2004-0066.
16. M. Morissette, S. Al Sweidi, S. Callier, T. Di Paolo, Estrogen and SERM neuroprotection in animal models of Parkinson's disease, Mol. Cell Endocrinol. 290 (2008) 60-69, http://dx.doi.org/10.1016/j.mce.2008.04.008.
17. A.M. Baraka, A.A. Korish, G.A. Soliman, H. Kamal, The possible role of estrogen and selective estrogen receptor modulators in a rat model of Parkinson's disease, Life Sci. 88 (2011) 879-885, http://dx.doi.org/10.1016/j.lfs.2011.03.010.
18. K. O'Neill, S. Chen, R.D. Brinton, Impact of the selective estrogen receptor modulator, raloxifene, on neuronal survival and outgrowth following toxic insults associated with aging and Alzheimer's disease, Exp. Neurol. 185 (2004) 63-80, http://dx.doi.org/10.1016/j.expneurol.2003.09.005.
19. I. Ciriza, P. Carrero, I. Azcoitia, S.G. Lundeen, L.M. Garcia-Segura, Selective estrogen receptor modulators protect hippocampal neurons from kainic acid excitotoxicity: differences with the effect of estradiol, J. Neurobiol. 61 (2004) 209-221, http://dx.doi.org/10.1002/neu.20043.
20. E. Biewenga, L. Cabell, T. Audesirk, Estradiol and raloxifene protect cultured SN4741 neurons against oxidative stress, Neurosci. Lett. 373 (2005) 179-183, http://dx.doi.org/10.1016/j.neulet.2004.09.067.
21. K.L. Hung, C.C. Wang, S.J. Wang, Cellular mechanisms of acute decrease of glutamate release induced by raloxifene in rat cerebral cortex, Neuropharmacology 61 (2011) 293-304, http://dx.doi.org/10.1016/j.neuropharm.2011.04.016.
22. R. Abdelhamid, J. Luo, L. Vandevrede, I. Kundu, B. Michalsen, V.A. Litosh, I.T. Schiefer, T. Gherezghiher, P. Yao, Z. Qin, G.R. Thatcher, Benzothiophene selective estrogen receptor modulators provide neuroprotection by a novel GPR30-dependent mechanism, ACS Chem. Neurosci. 2 (2011) 256-268, http://dx.doi.org/10.1021/cn100106a.
23. M. Kajta, A.K. Wójtowicz, M. Maćkowiak, W. Lasoń, Aryl hydrocarbon receptor-mediated apoptosis of neuronal cells: a possible interaction with estrogen receptor signaling, Neuroscience 158 (2009) 811-822, http://dx.doi.org/10.1016/j.neuroscience.2008.10.045.
24. M. Kajta, J. Rzemieniec, E. Litwa, W. Lason, M. Lenartowicz, W. Krzeptowski, A.K. Wojtowicz, The key involvement of estrogen receptor β and G-protein-coupled receptor 30 in the neuroprotective action of daidzein, Neuroscience 238 (2013) 345-360, http://dx.doi.org/10.1016/j.neuroscience.2013.02.005.
25. D.A. Schreihofer, L. Redmond, Soy phytoestrogens are neuroprotective against stroke-like injury in vitro, Neuroscience 158 (2009) 602-609, http://dx.doi.org/10.1016/j.neuroscience.2008.10.003.
26. G.J. Brewer, Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus, J. Neurosci. Res. 42 (1995) 674-683.
27. M. Kajta, H. Domin, G. Grynkiewicz, W. Lason, Genistein inhibits glutamate-induced apoptotic processes in primary neuronal cell cultures: an involvement of aryl hydrocarbon receptor and estrogen receptor/glycogen synthase kinase-3beta intracellular signaling pathway, Neuroscience 145 (2007) 592-604, http://dx.doi.org/10.1016/j.neuroscience.2006.11.059.
28. M. Kajta, W. Lasoń, T. Kupiec, Effects of estrone on NMDA- and staurosporine-induced changes in caspase-3-like protease activity and LDH-release: time- and tissue-dependent effects in neuronal primary cultures, Neuroscience 123 (2004) 515-526, http://dx.doi.org/10.1016/j.neuroscience.2003.09.005.
29. T. Hirsch, S.A. Susin, I. Marzo, P. Marchetti, N. Zamzami, G. Kroemer, Mitochondrial permeability transition in apoptosis and necrosis, Cell. Biol. Toxicol. 14 (1998) 141-145.
30. D.W. Nicholson, A. Ali, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labelle, Y.A. Lazebnik, N.A. Munday, S.M. Raju, M.E. Smulson, T.-T. Yamin, V.L. Yu, D.K. Miller, Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis, Nature 376 (1995) 37-43.
31. C. Mytilineou, E.K. Leonardi, P. Radcliffe, E.H. Heinonen, S.K. Han, P. Werner, G. Cohen, C.W. Olanow, Deprenyl and desmethylselegiline protect mesencephalic neurons from toxicity induced by glutathione depletion, J. Pharmacol. Exp. Ther. 284 (1998) 700-706.
32. A.K. Wojtowicz, K.A. Szychowski, M. Kajta, PPAR-γ agonist GW1929 but not antagonist GW9662 reduces TBBPA-induced neurotoxicity in primary neocortical cells, Neurotox. Res. 25 (2014) 311-322, http://dx.doi.org/10.1007/s12640-013-9434-z.
33. A. Heyer, M. Hasselblatt, N. von Ahsen, H. Häfner, A.L. Sirén, H. Ehrenreich, In vitro gender differences in neuronal survival on hypoxia and in 17beta-estradiol-mediated neuroprotection, J. Cereb. Blood Flow Metab. 25 (2005) 427-430, http://dx.doi.org/10.1038/sj.jcbfm.9600056.
34. +, Mol. Neurobiol. 47 (2013) 757-769, http://dx.doi.org/10.1007/s12035-012-8382-6.
35. X. Antoniou, A. Sclip, C. Ploia, A. Colombo, G. Moroy, T. Borsello, JNK contributes to Hif-1alpha regulation in hypoxic neurons, Molecules 15 (2009) 114-127, http://dx.doi.org/10.3390/molecules15010114.
36. D.M. Stroka, T. Burkhardt, I. Desbaillets, R.H. Wenger, D.A. Neil, C. Bauer, M. Gassmann, D. Candinas, HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia, FASEB J. 15 (2001) 2445-2453, http://dx.doi.org/10.1096/fj.01-0125com.
37. S.B. Liu, N. Zhang, Y.Y. Guo, R. Zhao, T.Y. Shi, S.F. Feng, S.Q. Wang, Q. Yang, X.Q. Li, Y.M. Wu, L. Ma, Y. Hou, L.Z. Xiong, W. Zhang, M.G. Zhao, G-protein-coupled receptor 30 mediates rapid neuroprotective effects of estrogen via depression of NR2B-containing NMDA receptors, J. Neurosci. 32 (2012) 4887-4900, http://dx.doi.org/10.1523/JNEUROSCI.5828-11.2012.
38. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, P.H. Seeburg, Developmental and regional expression in the rat brain and functional properties of four NMDA receptors, Neuron 12 (1994) 529-540.
39. M. Gillard, P. Chatelain, Changes in pH differently affect the binding properties of histamine H1 receptor antagonists, Eur. J. Pharmacol. 530 (2006) 205-214, http://dx.doi.org/10.1016/0165-0270(95)00165-4.
40. B.J. Connell, T.M. Saleh, Differential neuroprotection of selective estrogen receptor agonists against autonomic dysfunction and ischemic cell death in permanent versus reperfusion injury, Adv. Pharmacol. Sci. 2011 (2011) 976951, http://dx.doi.org/10.1155/2011/976951.
41. H.H. Lee, S.M. Belcher, Rapid signaling actions of environmental estrogens in developing granule cell neurons are mediated by estrogen receptor β, Endocrinology 151 (2010) 5689-5699, http://dx.doi.org/10.1210/en.2010-0710.
42. X.J. Tan, Y.B. Dai, W.F. Wu, H.J. Kim, R.P. Barros, T.I. Richardson, B.C. Yaden, M. Warner, D.L. McKinzie, V. Krishnan, J.A. Gustafsson, Reduction of dendritic spines and elevation of GABAergic signaling in the brains of mice treated with an estrogen receptor β ligand, Proc. Natl. Acad. Sci. U.S.A. 109 (2012) 1708-1712, http://dx.doi.org/10.1073/pnas.1121162109.
43. D.B. Dubal, H. Zhu, J. Yu, S.W. Rau, P.J. Shughrue, I. Merchenthaler, M.S. Kindy, P.M. Wise, Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury, Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1952-1957, http://dx.doi.org/10.1073/pnas.98.4.1952.
44. D.B. Dubal, S.W. Rau, P.J. Shughrue, H. Zhu, J. Yu, A.B. Cashion, S. Suzuki, L.M. Gerhold, M.B. Bottner, S.B. Dubal, I. Merchanthaler, M.S. Kindy, P.M. Wise, Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERalpha in estradiol-mediated protection against delayed cell death, Endocrinology 147 (2006) 3076-3084, http://dx.doi.org/10.1210/en.2005-1177.
45. Q.G. Zhang, L. Raz, R. Wang, D. Han, L. De Sevilla, F. Yang, R.K. Vadlamudi, D.W. Brann, Estrogen attenuates ischemic oxidative damage via an estrogen receptor alpha-mediated inhibition of NADPH oxidase activation, J. Neurosci. 29 (2009) 13823-13836, http://dx.doi.org/10.1523/JNEUROSCI.3574-09.2009.
46. J.G. Elzer, S. Muhammad, T.M. Wintermantel, A. Regnier-Vigouroux, J. Ludwig, G. Schütz, M. Schwaninger, Neuronal estrogen receptor-alpha mediates neuroprotection by 17beta-estradiol, J. Cereb. Blood Flow Metab. 30 (2010) 935-942, http://dx.doi.org/10.1038/jcbfm.2009.258.
47. K. Shimada, K.T. Kitazato, T. Kinouchi, K. Yagi, Y. Tada, J. Satomi, T. Kageji, S. Nagahiro, Activation of estrogen receptor-α and of angiotensin-converting enzyme 2 suppresses ischemic brain damage in oophorectomized rats, Hypertension 57 (2011) 1161-1166, http://dx.doi.org/10.1161/HYPERTENSIONAHA.110.167650.
48. J. Guo, D.N. Krause, J. Horne, J.H. Weiss, X. Li, S.P. Duckles, Estrogen-receptor-mediated protection of cerebral endothelial cell viability and mitochondrial function after ischemic insult in vitro, J. Cereb. Blood Flow Metab. 30 (2010) 545-554, http://dx.doi.org/10.1016/j.freeradbiomed.2012.03.005.