Lose dose genistein inhibits glucocorticoid receptor and ischemic brain injury in female rats

Neurochemistry International

Volumn 65, Issue 1, 2014, Pages 14-22

  Shi, Rengfei ^a   Wang, Shunli ^a   Qi, Xiang ^a   Chen, Si ^a   Chen, Peijie ^a   Zhang, Quanguang ^a  

^a SHANGHAI UNIVERSITY OF SPORT   (China)

Author keywords

Brain injury; Genistein replacement; Glucocorticoid receptor; Hippocampus; Microglia; Osmotic pump; Transient forebrain ischemia

Indexed keywords

CORTICOSTERONE; GENISTEIN; GLUCOCORTICOID RECEPTOR; PLACEBO; PROTEASOME; PROTEIN MDM2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN NERVE CELL; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DRUG MECHANISM; FEMALE; FOREBRAIN; HIPPOCAMPAL CA1 REGION; HORMONE RECEPTOR TRANSLOCATION; LONG TERM CARE; LOW DRUG DOSE; MICROGLIA; NEUROPROTECTION; NONHUMAN; OSMOTIC MINIPUMP; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR BLOCKING; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TREATMENT DURATION; UBIQUITINATION;

BRAIN INJURY; GENISTEIN REPLACEMENT; GLUCOCORTICOID RECEPTOR; HIPPOCAMPUS; MICROGLIA; OSMOTIC PUMP; TRANSIENT FOREBRAIN ISCHEMIA;

ANIMALS; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; FEMALE; GENISTEIN; GLUCOCORTICOIDS; MICROGLIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION;

EID: 84891550426     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2013.12.002     Document Type: Article

References (76)

1. V.Z. Ajdzanovi, B.T. Sosi-Jurjevi, B.R. Filipovi, S.L. Trifunovi, D.D. Brkic, M.I. Sekuli, and V. Milosevi Genistein affects the morphology of pituitary ACTH cells and decreases circulating levels of ACTH and corticosterone in middle-aged male rats Biol. Res. 42 2009 13 23
2. O.F. Almeida, G.L. Conde, C. Crochemore, B.A. Demeneix, D. Fischer, A.H. Hassan, M. Meyer, F. Holsboer, and T.M. Michaelidis Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate FASEB J. 14 2000 779 790 (Pubitemid 30198576)
3. D. Altavilla, A. Crisafulli, H. Marini, M. Esposito, R. D'Anna, F. Corrado, A. Bitto, and F. Squadrito Cardiovascular effects of the phytoestrogen genistein Curr. Med. Chem. Cardiovasc. Hematol. Agents 2 2004 179 186 (Pubitemid 38854979)
4. J.J. Anderson, W.W. Ambrose, and S.C. Garner Biphasic effects of genistein on bone tissue in the ovariectomized, lactating rat model Proc. Soc. Exp. Biol. Med. 217 1998 345 350
5. F.J. Antonawich, G. Miller, D.C. Rigsby, and J.N. Davis Regulation of ischemic cell death by glucocorticoids and adrenocorticotropic hormone Neuroscience 88 1999 319 325 (Pubitemid 28440412)
6. V. Arndt, C. Rogon, and J. Hohfeld To be, or not to be - molecular chaperones in protein degradation Cell. Mol. Life Sci. 64 2007 2525 2541 (Pubitemid 350035611)
7. M. Aronsson, K. Fuxe, Y. Dong, L.F. Agnati, S. Okret, and J.A. Gustafsson Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization Proc. Natl. Acad. Sci. USA 85 1988 9331 9335 (Pubitemid 19001890)
8. I. Baitharu, S.N. Deep, V. Jain, D. Prasad, and G. Ilavazhagan Inhibition of glucocorticoid receptors ameliorates hypobaric hypoxia induced memory impairment in rat Behav. Brain Res. 240 2013 76 86
9. S. Barnes Evolution of the health benefits of soy isoflavones Proc. Soc. Exp. Biol. Med. 217 1998 386 392
10. K.B. Bouker, and L. Hilakivi-Clarke Genistein: does it prevent or promote breast cancer? Environ. Health Perspect. 108 2000 701 708
11. D.W. Brann, K. Dhandapani, C. Wakade, V.B. Mahesh, and M.M. Khan Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications Steroids 72 2007 381 405 (Pubitemid 46602478)
12. D. Brann, L. Raz, R. Wang, R. Vadlamudi, and Q. Zhang Oestrogen signalling and neuroprotection in cerebral ischaemia J. Neuroendocrinol. 24 2012 34 47
13. S.C. Brooks, and D.F. Skafar From ligand structure to biological activity: modified estratrienes and their estrogenic and antiestrogenic effects in MCF-7 cells Steroids 69 2004 401 418 (Pubitemid 38829336)
14. J.C. Buckingham Glucocorticoids: exemplars of multi-tasking Br. J. Pharmacol. 147 Suppl 1 2006 S258 S268
15. M. Castello-Ruiz, G. Torregrosa, M.C. Burguete, J.B. Salom, J.V. Gil, F.J. Miranda, T. Jover-Mengual, V.G. Marrachelli, and E. Alborch Soy-derived phytoestrogens as preventive and acute neuroprotectors in experimental ischemic stroke: influence of rat strain Phytomedicine 18 2011 513 515
16. M.S. Charles, R.P. Ostrowski, A. Manaenko, K. Duris, J.H. Zhang, and J. Tang Role of the pituitary-adrenal axis in granulocyte-colony stimulating factor-induced neuroprotection against hypoxia-ischemia in neonatal rats Neurobiol. Dis. 47 2012 29 37
17. M.Y. Cheng, G. Sun, M. Jin, H. Zhao, G.K. Steinberg, and R.M. Sapolsky Blocking glucocorticoid and enhancing estrogenic genomic signaling protects against cerebral ischemia J. Cereb. Blood Flow Metab. 29 2009 130 136
18. D.W. Choi Ischemia-induced neuronal apoptosis Curr. Opin. Neurobiol. 6 1996 667 672 (Pubitemid 26387723)
19. K. Chu, B. Yin, J. Wang, G. Peng, H. Liang, Z. Xu, Y. Du, M. Fang, Q. Xia, and B. Luo Inhibition of P2X7 receptor ameliorates transient global cerebral ischemia/reperfusion injury via modulating inflammatory responses in the rat hippocampus J. Neuroinflammation 9 2012 69
20. P. Connell, C.A. Ballinger, J. Jiang, Y. Wu, L.J. Thompson, J. Hohfeld, and C. Patterson The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins Nat. Cell Biol. 3 2001 93 96 (Pubitemid 32114838)
21. E.R. De Kloet, E. Vreugdenhil, M.S. Oitzl, and M. Joels Brain corticosteroid receptor balance in health and disease Endocr. Rev. 19 1998 269 301 (Pubitemid 29117816)
22. F.S. De Ronde, E.R. de Kloet, and C. Nyakas Corticosteroid receptor plasticity and recovery of a deficient hippocampus-associated behavior after unilateral (dorsal) hippocampectomy Brain Res. 374 1986 219 226 (Pubitemid 16077972)
23. A. Donzelli, D. Braida, A. Finardi, V. Capurro, A.E. Valsecchi, M. Colleoni, and M. Sala Neuroprotective effects of genistein in Mongolian gerbils: estrogen receptor-beta involvement J. Pharmacol. Sci. 114 2010 158 167
24. M. Fan, A. Park, and K.P. Nephew CHIP (carboxyl terminus of Hsc70-interacting protein) promotes basal and geldanamycin-induced degradation of estrogen receptor-alpha Mol. Endocrinol. 19 2005 2901 2914 (Pubitemid 41697710)
25. I. Harukuni, and A. Bhardwaj Mechanisms of brain injury after global cerebral ischemia Neurol. Clin. 24 2006 1 21 (Pubitemid 43144627)
26. R. Hayashi, H. Wada, K. Ito, and I.M. Adcock Effects of glucocorticoids on gene transcription Eur. J. Pharmacol. 500 2004 51 62 (Pubitemid 39303996)
27. C. Hibberd, J.L. Yau, and J.R. Seckl Glucocorticoids and the ageing hippocampus J. Anat. 197 Pt 4 2000 553 562 (Pubitemid 32051535)
28. L. Hilakivi-Clarke, J.E. Andrade, and W. Helferich Is soy consumption good or bad for the breast? J. Nutr. 140 2010 2326S 2334S
29. J. Hohfeld, D.M. Cyr, and C. Patterson From the cradle to the grave: molecular chaperones that may choose between folding and degradation EMBO Rep. 2 2001 885 890 (Pubitemid 33040574)
30. I.K. Hwang, K.Y. Yoo, Y.S. Nam, J.H. Choi, I.S. Lee, Y.G. Kwon, T.C. Kang, Y.S. Kim, and M.H. Won Mineralocorticoid and glucocorticoid receptor expressions in astrocytes and microglia in the gerbil hippocampal CA1 region after ischemic insult Neurosci. Res. 54 2006 319 327 (Pubitemid 43374451)
31. D. Kaufer, W.O. Ogle, Z.S. Pincus, K.L. Clark, A.C. Nicholas, K.M. Dinkel, T.C. Dumas, D. Ferguson, A.L. Lee, M.A. Winters, and R.M. Sapolsky Restructuring the neuronal stress response with anti-glucocorticoid gene delivery Nat. Neurosci. 7 2004 947 953 (Pubitemid 39129503)
32. D.J. Kim, S.H. Seok, M.W. Baek, H.Y. Lee, Y.R. Na, S.H. Park, H.K. Lee, N.K. Dutta, K. Kawakami, and J.H. Park Developmental toxicity and brain aromatase induction by high genistein concentrations in zebrafish embryos Toxicol. Mech. Methods 19 2009 251 256
33. M.S. Kindy Inhibition of tyrosine phosphorylation prevents delayed neuronal death following cerebral ischemia J. Cereb. Blood Flow Metab. 13 1993 372 377 (Pubitemid 23129389)
34. H.K. Kinyamu, and T.K. Archer Estrogen receptor-dependent proteasomal degradation of the glucocorticoid receptor is coupled to an increase in mdm2 protein expression Mol. Cell. Biol. 23 2003 5867 5881 (Pubitemid 36951348)
35. H.J. Krugers, S. Maslam, J. Korf, M. Joels, and F. Holsboer The corticosterone synthesis inhibitor metyrapone prevents hypoxia/ischemia-induced loss of synaptic function in the rat hippocampus Stroke 31 2000 1162 1172 (Pubitemid 30253541)
36. J.A. Lavigne, Y. Takahashi, G.V. Chandramouli, H. Liu, S.N. Perkins, S.D. Hursting, and T.T. Wang Concentration-dependent effects of genistein on global gene expression in MCF-7 breast cancer cells: an oligo microarray study Breast Cancer Res. Treat. 110 2008 85 98 (Pubitemid 351793861)
37. H. Lee, Y.O. Kim, H. Kim, S.Y. Kim, H.S. Noh, S.S. Kang, G.J. Cho, W.S. Choi, and K. Suk Flavonoid wogonin from medicinal herb is neuroprotective by inhibiting inflammatory activation of microglia FASEB J. 17 2003 1943 1944
38. N.J. Linford, and D.M. Dorsa 17beta-Estradiol and the phytoestrogen genistein attenuate neuronal apoptosis induced by the endoplasmic reticulum calcium-ATPase inhibitor thapsigargin Steroids 67 2002 1029 1040 (Pubitemid 35345166)
39. N.J. Linford, Y. Yang, D.G. Cook, and D.M. Dorsa Neuronal apoptosis resulting from high doses of the isoflavone genistein: role for calcium and p42/44 mitogen-activated protein kinase J. Pharmacol. Exp. Ther. 299 2001 67 75 (Pubitemid 32905119)
40. P. Lipton Ischemic cell death in brain neurons Physiol. Rev. 79 1999 1431 1568 (Pubitemid 29473320)
41. T. Lovekamp-Swan, M. Glendenning, and D.A. Schreihofer A high soy diet reduces programmed cell death and enhances bcl-xL expression in experimental stroke Neuroscience 148 2007 644 652 (Pubitemid 47432726)
42. N.Z. Lu, and J.A. Cidlowski The origin and functions of multiple human glucocorticoid receptor isoforms Ann. N. Y. Acad. Sci. 1024 2004 102 123 (Pubitemid 38879596)
43. Y. Ma, J.C. Sullivan, and D.A. Schreihofer Dietary genistein and equol (4′,7 isoflavandiol) reduce oxidative stress and protect rats against focal cerebral ischemia Am. J. Physiol. Regul. Integr. Comp. Physiol. 299 2010 R871 R877
44. B.S. McEwen Invited review: estrogens effects on the brain: multiple sites and molecular mechanisms J. Appl. Physiol. 91 2001 2785 2801 (Pubitemid 33108046)
45. N.J. McKenna, and B.W. O'Malley Combinatorial control of gene expression by nuclear receptors and coregulators Cell 108 2002 465 474 (Pubitemid 34260872)
46. S. Mesiano, S.L. Katz, J.Y. Lee, and R.B. Jaffe Phytoestrogens alter adrenocortical function: genistein and daidzein suppress glucocorticoid and stimulate androgen production by cultured adrenal cortical cells J. Clin. Endocrinol. Metab. 84 1999 2443 2448
47. T. Morioka, A.N. Kalehua, and W.J. Streit Characterization of microglial reaction after middle cerebral artery occlusion in rat brain J. Comp. Neurol. 327 1993 123 132 (Pubitemid 23006616)
48. J.K. Morse, and J.N. Davis Regulation of ischemic hippocampal damage in the gerbil: adrenalectomy alters the rate of CA1 cell disappearance Exp. Neurol. 110 1990 86 92 (Pubitemid 20376004)
49. T. Nitatori, N. Sato, S. Waguri, Y. Karasawa, H. Araki, K. Shibanai, E. Kominami, and Y. Uchiyama Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis J. Neurosci. 15 1995 1001 1011
50. C. Nyakas, E.R. De Kloet, H.D. Veldhuis, and B. Bohus Hippocampal corticosterone receptors and novelty-induced behavioral activity: effect of kainic acid lesion in the hippocampus Brain Res. 288 1983 219 228 (Pubitemid 14212710)
51. S. Ohno, Y. Nakajima, K. Inoue, H. Nakazawa, and S. Nakajin Genistein administration decreases serum corticosterone and testosterone levels in rats Life Sci. 74 2003 733 742 (Pubitemid 37494900)
52. H.B. Patisaul, and W. Jefferson The pros and cons of phytoestrogens Front. Neuroendocrinol. 31 2010 400 419
53. M.A. Perez-Pinzon, T.M. Vitro, W.D. Dietrich, and T.J. Sick The effect of rapid preconditioning on the microglial, astrocytic and neuronal consequences of global cerebral ischemia Acta Neuropathol. 97 1999 495 501 (Pubitemid 29195113)
54. W.B. Pratt, Y. Morishima, M. Murphy, and M. Harrell Chaperoning of glucocorticoid receptors Handb. Exp. Pharmacol. 2006 111 138
55. W.A. Pulsinelli, and J.B. Brierley A new model of bilateral hemispheric ischemia in the unanesthetized rat Stroke 10 1979 267 272 (Pubitemid 9141527)
56. Y. Qian, T. Guan, M. Huang, L. Cao, Y. Li, H. Cheng, H. Jin, and D. Yu Neuroprotection by the soy isoflavone, genistein, via inhibition of mitochondria-dependent apoptosis pathways and reactive oxygen induced-NF-kappaB activation in a cerebral ischemia mouse model Neurochem. Int. 60 2012 759 767
57. A.K. Rose, S.G. Shaw, M.A. Prendergast, and H.J. Little The importance of glucocorticoids in alcohol dependence and neurotoxicity Alcohol. Clin. Exp. Res. 34 2010 2011 2018
58. R.M. Sapolsky Stress, glucocorticoids, and damage to the nervous system: the current state of confusion Stress 1 1996 1 19
59. R.M. Sapolsky, and W.A. Pulsinelli Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications Science 229 1985 1397 1400 (Pubitemid 16222382)
60. M. Satou, and K. Ueda Synchronized rhythmic discharges of the secondary olfactory neurons in carp Brain Res. 158 1978 313 329 (Pubitemid 9079142)
61. W. Scherer, N. Lippman, J. Kaim, and J. LoPresti Antimicrobial properties of VLC liners J. Esthet. Dent. 2 1990 31 32
62. D.A. Schreihofer, and L. Redmond Soy phytoestrogens are neuroprotective against stroke-like injury in vitro Neuroscience 158 2009 602 609
63. Z.M. Shao, Z.Z. Shen, J.A. Fontana, and S.H. Barsky Genistein's "ER-dependent and independent" actions are mediated through ER pathways in ER-positive breast carcinoma cell lines Anticancer Res. 20 2000 2409 2416 (Pubitemid 30614444)
64. J.E. Sherin, and C.B. Nemeroff Post-traumatic stress disorder: the neurobiological impact of psychological trauma Dialogues Clin. Neurosci. 13 2011 263 278
65. V.L. Smith-Swintosky, L.C. Pettigrew, R.M. Sapolsky, C. Phares, S.D. Craddock, S.M. Brooke, and M.P. Mattson Metyrapone, an inhibitor of glucocorticoid production, reduces brain injury induced by focal and global ischemia and seizures J. Cereb. Blood Flow Metab. 16 1996 585 598 (Pubitemid 26227067)
66. B.A. Stein, and R.M. Sapolsky Chemical adrenalectomy reduces hippocampal damage induced by kainic acid Brain Res. 473 1988 175 180 (Pubitemid 19008228)
67. Y. Tateishi, Y. Kawabe, T. Chiba, S. Murata, K. Ichikawa, A. Murayama, K. Tanaka, T. Baba, S. Kato, and J. Yanagisawa Ligand-dependent switching of ubiquitin-proteasome pathways for estrogen receptor EMBO J. 23 2004 4813 4823 (Pubitemid 40069711)
68. V.N. Trieu, and F.M. Uckun Genistein is neuroprotective in murine models of familial amyotrophic lateral sclerosis and stroke Biochem. Biophys. Res. Commun. 258 1999 685 688 (Pubitemid 29290330)
69. V.N. Trieu, Y. Dong, Y. Zheng, and F.M. Uckun In vivo antioxidant activity of genistein in a murine model of singlet oxygen-induced cerebral stroke Radiat. Res. 152 1999 508 516 (Pubitemid 29514153)
70. A. Vincent, and L.A. Fitzpatrick Soy isoflavones: are they useful in menopause? Mayo Clin. Proc. 75 2000 1174 1184
71. R. Wang, J. Tu, Q. Zhang, X. Zhang, Y. Zhu, W. Ma, C. Cheng, D.W. Brann, and F. Yang Genistein attenuates ischemic oxidative damage and behavioral deficits via eNOS/Nrf2/HO-1 signaling Hippocampus 23 2013 634 647
72. R.L. Wolman, N.A. Nussmeier, A. Aggarwal, M.S. Kanchuger, G.W. Roach, M.F. Newman, C.M. Mangano, K.E. Marschall, C. Ley, D.M. Boisvert, G.M. Ozanne, A. Herskowitz, S.H. Graham, and D.T. Mangano Cerebral injury after cardiac surgery: identification of a group at extraordinary risk. Multicenter Study of Perioperative Ischemia Research Group (McSPI) and the Ischemia Research Education Foundation (IREF) Investigators Stroke 30 1999 514 522
73. S. Yamashita, S. Tsukamoto, M. Kumazoe, Y.H. Kim, K. Yamada, and H. Tachibana Isoflavones suppress the expression of the fcepsilonRI high-affinity immunoglobulin E receptor independent of the estrogen receptor J. Agric. Food Chem. 60 2012 8379 8385
74. Q.G. Zhang, R. Wang, M. Khan, V. Mahesh, and D.W. Brann Role of Dickkopf-1, an antagonist of the Wnt/beta-catenin signaling pathway, in estrogen-induced neuroprotection and attenuation of tau phosphorylation J. Neurosci. 28 2008 8430 8441
75. Q.G. Zhang, L. Raz, R. Wang, D. Han, L. De Sevilla, F. Yang, R.K. Vadlamudi, and 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
76. Q.G. Zhang, D. Han, R.M. Wang, Y. Dong, F. Yang, R.K. Vadlamudi, and D.W. Brann C terminus of Hsc70-interacting protein (CHIP)-mediated degradation of hippocampal estrogen receptor-alpha and the critical period hypothesis of estrogen neuroprotection Proc. Natl. Acad. Sci. USA 108 2011 E617 E624