Estradiol rapidly rescues synaptic transmission from corticosterone-induced suppression via synaptic/extranuclear steroid receptors in the hippocampus

Cerebral Cortex

Volumn 22, Issue 4, 2012, Pages 926-936

  Ooishi, Yuuki ^a   Mukai, Hideo ^a   Hojo, Yasushi ^a   Murakami, Gen ^a   Hasegawa, Yoshitaka ^a   Shindo, Tomu ^a   Morrison, John H ^b   Kimoto, Tetsuya ^a   Kawato, Suguru ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

corticosterone; estradiol; hippocampus; LTP; NDMA receptors

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CALCINEURIN INHIBITOR; CORTICOSTERONE; CYCLOSPORIN A; DEXAMETHASONE; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUCOCORTICOID RECEPTOR ANTAGONIST; HORMONE RECEPTOR STIMULATING AGENT; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; STEROID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

EID: 84859016141     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr164     Document Type: Article

References (45)

1. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, McEwen BS, Morrison JH. 2002. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci. 22:3608-3614.
2. Alfarez DN, Wiegert O, Joels M, Krugers HJ. 2002. Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience. 115:1119-1126.
3. Behl C, Widmann M, Trapp T, Holsboer F. 1995. 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun. 216:473-482.
4. Beiko J, Lander R, Hampson E, Boon F, Cain DP. 2004. Contribution of sex differences in the acute stress response to sex differences in water maze performance in the rat. Behav Brain Res. 151:239-253.
5. Bi R, Broutman G, Foy MR, Thompson RF, Baudry M. 2000. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc Natl Acad Sci USA. 97:3602-3607.
6. Breuner CW, Orchinik M. 2002. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J Endocrinol. 175:99-112.
7. Chen Y, Dube CM, Rice CJ, Baram TZ. 2008. Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J Neurosci. 28:2903-2911.
8. Dominguez R, Liu R, Baudry M. 2007. 17-Beta-estradiol-mediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-D-aspartate receptor phosphorylation in cortical synaptoneurosomes. J Neurochem. 101:232-240.
9. Fester L, Ribeiro-Gouveia V, Prange-Kiel J, von Schassen C, Bottner M, Jarry H, Rune GM. 2006. Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J Neurochem. 97:1136-1144.
10. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF, Berger TW. 1999. 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol. 81:925-929.
11. Gerges NZ, Aleisa AM, Schwarz LA, Alkadhi KA. 2004. Reduced basal CaMKII levels in hippocampal CA1 region: possible cause of stressinduced impairment of LTP in chronically stressed rats. Hippocampus. 14:402-410.
12. Gu Q, Moss RL. 1996. 17 beta-Estradiol potentiates kainate-induced currents via activation of the cAMP cascade. J Neurosci. 16:3620-3629.
13. Haynes LE, Lendon CL, Barber DJ, Mitchell IJ. 2003. 17 Beta-oestradiol attenuates dexamethasone-induced lethal and sublethal neuronal damage in the striatum and hippocampus. Neuroscience. 120:799-806.
14. Hirata R, Togashi H, Matsumoto M, Yamaguchi T, Izumi T, Yoshioka M. 2008. Characterization of stress-induced suppression of long-term potentiation in the hippocampal CA1 field of freely moving rats. Brain Res. 1226:27-32.
15. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, Mukai H, Morrison JH, Janssen WG, Kominami S, et al. 2004. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc Natl Acad Sci USA. 101:865-870.
16. Hojo Y, Higo S, Ishii H, Ooishi Y, Mukai H, Murakami G, Kominami T, Kimoto T, Honma S, Poirier D, et al. 2009. Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology. 150:5106-5112.
17. Isaacson JS, Walmsley B. 1995. Counting quanta: direct measurements of transmitter release at a central synapse. Neuron. 15:875-884.
18. Ito K, Skinkle KL, Hicks TP. 1999. Age-dependent, steroid-specific effects of oestrogen on long-term potentiation in rat hippocampal slices. J Physiol. 515(Pt 1):209-220.
19. Katz B, Miledi R. 1968. The role of calcium in neuromuscular facilitation. J Physiol. 195:481-492.
20. Kawato S. 2004. Endocrine disrupters as disrupters of brain function: a neurosteroid viewpoint. Environ Sci. 11:1-14.
21. Kawato S, Hojo Y, Kimoto T. 2002. Histological and metabolism analysis of P450 expression in the brain. Methods Enzymol. 357:241-249.
22. Komatsuzaki Y, Murakami G, Tsurugizawa T, Mukai H, Tanabe N, Mitsuhashi K, Kawata M, Kimoto T, Ooishi Y, Kawato S. 2005. Rapid spinogenesis of pyramidal neurons induced by activation of glucocorticoid receptors in adult male rat hippocampus. Biochem Biophys Res Commun. 335:1002-1007.
23. Kramar EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, Lynch G. 2009. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci. 29:12982-12993.
24. Krupp JJ, Vissel B, Thomas CG, Heinemann SF, Westbrook GL. 2002. Calcineurin acts via the C-terminus of NR2A to modulate desensitization of NMDA receptors. Neuropharmacology. 42:593-602.
25. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA. 1993. Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol. 70:1451-1459.
26. Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA. 2001. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem. 44:4230-4251.
27. Mukai H, Takata N, Ishii HT, Tanabe N, Hojo Y, Furukawa A, Kimoto T, Kawato S. 2006. Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology. Neuroscience. 138:757-764.
28. Mukai H, Tsurugizawa T, Murakami G, Kominami S, Ishii H, Ogiue-Ikeda M, Takata N, Tanabe N, Furukawa A, Hojo Y, et al. 2007. Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J Neurochem. 100:950-967.
29. Murphy DD, Segal M. 1996. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci. 16:4059-4068.
30. Ogiue-Ikeda M, Tanabe N, Mukai H, Hojo Y, Murakami G, Tsurugizawa T, Takata N, Kimoto T, Kawato S. 2008. Rapid modulation of synaptic plasticity by estrogens as well as endocrine disrupters in hippocampal neurons. Brain Res Rev. 57:363-375.
31. Pavlides C, Nivon LG, McEwen BS. 2002. Effects of chronic stress on hippocampal long-term potentiation. Hippocampus. 12:245-257.
32. Reagan LP, McEwen BS. 1997. Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J Chem Neuroanat. 13:149-167.
33. Shibuya K, Takata N, Hojo Y, Furukawa A, Yasumatsu N, Kimoto T, Enami T, Suzuki K, Tanabe N, Ishii H, et al. 2003. Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction. Biochim Biophys Acta. 1619:301-316.
34. Smith CC, McMahon LL. 2006. Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci. 26:8517-8522.
35. Snyder MA, Cooke BM, Woolley CS. 2011. Estradiol potentiation of NR2B-dependent EPSCs is not due to changes in NR2B protein expression or phosphorylation. Hippocampus. 21:398-408.
36. Stauffer SR, Coletta CJ, Tedesco R, Nishiguchi G, Carlson K, Sun J, Katzenellenbogen BS, Katzenellenbogen JA. 2000. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alphaselective agonists. J Med Chem. 43:4934-4947.
37. Tohei A, Tomabechi T, Mamada M, Akai M, Watanabe G, Taya K. 1997. Effects of repeated ether stress on the hypothalamic-pituitary-testes axis in adult rats with special reference to inhibin secretion. J Vet Med Sci. 59:329-334.
38. Toran-Allerand CD, Guan X, MacLusky NJ, Horvath TL, Diano S, Singh M, Connolly ES, Jr., Nethrapalli IS, Tinnikov AA. 2002. ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci. 22:8391-8401.
39. Vidal C, Jordan W, Zieglgansberger W. 1986. Corticosterone reduces the excitability of hippocampal pyramidal cells in vitro. Brain Res. 383:54-59.
40. Vouimba RM, Foy MR, Foy JG, Thompson RF. 2000. 17beta-estradiol suppresses expression of long-term depression in aged rats. Brain Res Bull. 53:783-787.
41. Warner M, Gustafsson JA. 2006. Nongenomic effects of estrogen: why all the uncertainty? Steroids. 71:91-95.
42. Watanabe Y, Gould E, McEwen BS. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588:341-345.
43. Woolley CS, Gould E, McEwen BS. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531:225-231.
44. Zhang L, Rubinow DR, Xaing G, Li BS, Chang YH, Maric D, Barker JL, Ma W. 2001. Estrogen protects against beta-amyloid-induced neurotoxicity in rat hippocampal neurons by activation of Akt. Neuroreport. 12:1919-1923.
45. Zucker RS. 1989. Short-term synaptic plasticity. Annu Rev Neurosci. 12:13-31.