Estrogen receptor α functions in the regulation of motivation and spatial cognition in young male rats

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Meyer, Katrin ^a,b   Korz, Volker ^b,c  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c Center for Behavioral Neuroscience   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GLUCOCORTICOID RECEPTOR; MINERALOCORTICOID RECEPTOR; TESTOSTERONE; HORMONE; PYRAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; ELEVATED PLUS MAZE TEST; ENZYME SPECIFICITY; HOMEOSTASIS; MALE; MOTIVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN FIELD TEST; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; REFERENCE MEMORY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WORKING MEMORY; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION; MAZE TEST; METABOLISM; PHYSIOLOGY; SHORT TERM MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; COGNITION; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION; HORMONES; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MOTIVATION; PYRAZOLES; RATS;

EID: 84893387299     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079303     Document Type: Article

References (51)

1. Perlman WR, Tomaskovic-Crook E, Montague DM, Webster MJ, Rubinow DR et al. (2005) Alteration in estrogen receptor alpha mRNA levels in frontal cortex and hippocampus of patients with major mental illness. Biol Psychiatry 58: 812-824. (Pubitemid 41677420)
2. Hajszan T, Milner TA, Leranth C (2007) Sex steroids and the dentate gyrus. Prog Brain Res 163: 399-415.
3. Gillies GE, McArthur S (2010) Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol Rev 62: 155-198.
4. Lagunas N, Calmarza-Font I, Grassi D, Garcia-Segura LM (2011) Estrogen receptor ligands counteract cognitive deficits caused by androgen deprivation in male rats. Horm Behav 59: 581-584.
5. McEwen BS (1988) Genomic regulation of sexual behavior. J Steroid Biochem 30: 179-183.
6. Paisley JC, Huddleston GG, Carruth LL, Petrulis A, Grober MS et al. (2012) Sexual responses of the male rat medial preoptic area and medial amygdala to estrogen I: site specific suppression of estrogen receptor alpha. Horm Behav 62: 50-57.
7. Sano K, Tsuda MC, Musatov S, Sakamoto T, Ogawa S (2013) Differential effects of site-specific knockdown of estrogen receptor a in the medial amygdala, medial pre-optic area, and ventromedial nucleus of the hypothalamus on sexual and aggressive behavior of male mice. Eur J Neurosci doi: 10.1111/ejn.12131.
8. Fester L, Ribeiro-Gouveia V, Prange-Kiel J, von Schassen C, Böttner M et al. (2006) Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J Neurochem 97: 1136-1144.
9. Bowers JM, Waddell J, McCarthy MM (2010) A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol. Biol Sex Differ 1: 8.
10. González-Burgos I, Rivera-Cervantes MC, Velázquez-Zamora DA, Feria-Velasco A, Garcia-Segura LM (2012) Selective estrogen receptor modulators regulate dendritic spine plasticity in the hippocampus of male rats. Neural Plast 2012: 309494, doi: 10.1155/2012/309494.
11. Fester L, Prange-Kiel J, Jarry H, Rune GM (2011) Estrogen synthesis in the hippocampus. Cell Tissue Res 345: 285-294.
12. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH et al. (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139: 4252-4263. (Pubitemid 28513713)
13. Scordalakes EM, Rissman EF (2003) Aggression in male mice lacking functional estrogen receptor alpha. Behav Neurosci 117: 38-45. (Pubitemid 36187429)
14. Nomura M, Andersson S, Korach KS, Gustafsson JA, Pfaff DW et al. (2006) Estrogen receptor-beta gene disruption potentiates estrogen-inducible aggression but not sexual behavior in male mice. Eur J Neurosci 23: 1860-1868.
15. Tetel MJ, Pfaff DW (2010) Contributions of estrogen receptor-α and estrogen receptor-β to the regulation of behavior. Biochim Biophys Acta 1800: 1084-1089.
16. Frye CA, Duffy CK, Walf AA (2007) Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol Learn Mem 88: 208-216. (Pubitemid 47223753)
17. Liu F, Day M, Muniz LC, Bitran D, Arias R et al. (2008) Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 11: 334-343. (Pubitemid 351311804)
18. Rissman EF (2008) Roles of oestrogen receptors a and b in behavioral neuroendocrinology: Beyond Yin/Yang. J Neuroendocrinol 20: 873-879.
19. Neese SL, Korol DL, Katzenellenbogen JA, Schantz SL (2010) Impact of estrogen receptor alpha and beta agonists on delayed alternation in middle-aged rats. Horm Behav 58: 878-890.
20. Galea LA, Uban KA, Epp JR, Brummelte S, Barha CK et al. (2008) Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can J Exp Psychol 62: 247-260.
21. Barha CK, Galea LA (2010) Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim Biophys Acta 1800: 1056-1067.
22. Mukai H, Kimoto T, Hojo Y, Kawato S, Murakami G et al. (2010) Modulation of synaptic plasticity by brain estrogen in the hippocampus. Biochim Biophys Acta 1800: 1030-1044.
23. Cornil CA, Ball GF, Balthazart J (2012) Rapid control of male typical behaviors by brain-derived estrogens. Front Neuroendocrinol 33: 425-46.
24. Meyer K, Korz V (2013) Age dependent differences in the regulation of hippocampal steroid hormones and receptor genes: Relations to motivation and cognition in male rats. Horm Behav 63: 376-384.
25. Chen S, Wang J, Yu G, Liu W, Pearce D (1997) Androgen and glucocorticoid receptor heterodimer formation. A possible mechanism for mutual inhibition of transcriptional activity. J Biol Chem 272: 14087-14092. (Pubitemid 27232812)
26. Cvoro A, Yuan C, Paruthiyil S, Miller OH, Yamamoto KR et al. (2011) Cross Talk between Glucocorticoid and Estrogen Receptors Occurs at a Subset of Proinflammatory Genes. J Immunol 186: 4354-4360.
27. Savatier J, Jalaguier S, Ferguson ML, Cavaillès V, Royer CA (2010) Estrogen receptor interactions and dynamics monitored in live cells by fluorescence cross-correlation spectroscopy. Biochemistry 49: 772-781.
28. McEwen BS (1992) Steroid hormones: effect on brain development and function. Horm Res 37 Suppl 3: 1-10.
29. Wu TW, Chen S, Brinton RD (2011) Membrane estrogen receptors mediate calcium signaling and MAP kinase activation in individual hippocampal neurons. Brain Res 1379: 34-43.
30. Fernandez SM, Lewis MC, Pechenino AS, Harburger LL, Orr PT et al. (2008) Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J Neurosci 28: 8660-8667.
31. Solum DT, Handa RJ (2002) Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus. J Neurosci 22: 2650-2659. (Pubitemid 37465814)
32. Spencer-Segal JL, Tsuda MC, Mattei L, Waters EM, Romeo RD et al. (2012) Estradiol acts via estrogen receptors alpha and beta on pathways important for synaptic plasticity in the mouse hippocampal formation. Neuroscience 202: 131-146.
33. Yang LC, Zhang QG, Zhou CF, Yang F, Zhang YD et al. (2010) Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS One 5: e9851.
34. Schaaf MJM, Hoetelmans RWM, de Kloet ER, Vreugdenhil E (1997) Corticosterone regulates expression of BDNF and trkB but not NT-3 and trkC mRNA in the rat hippocampus. J Neurosci Res 48: 334-341.
35. Uzakov S, Frey JU, Korz V (2005) Reinforcement of rat hippocampal LTP by holeboard training. Learn Mem 12: 165-171. (Pubitemid 40517084)
36. Sun J, Huang YR, Harrington WR, Sheng S, Katzenellenbogen JA et al. (2002) Antagonists selective for estrogen receptor alpha. Endocrinology 143: 941-947. (Pubitemid 34168188)
37. Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenellenbogen JA et al. (2003) Activities of estrogen receptor alpha- and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol 206: 13-22. (Pubitemid 37011249)
38. T method. Methods 25: 403-508.
39. Scharfman HE, MacLusky NJ (2006) Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: Complexity of steroid hormone-growth factor interactions in the adult CNS. Front Neuroendocrinol 27: 415-435. (Pubitemid 44738017)
40. Falkenberg T, Mohammed AK, Henriksson B, Persson H, Winblad B et al. (1992) Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett 138: 153-156.
41. Ma YL, Wang HL, Wu HC, Wei CL, Lee EH (1998) Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 82: 957-967. (Pubitemid 27502041)
42. Ranhotra HS (2012) The estrogen-related receptors: orphans orchestrating myriad functions. J Recept Signal Transduct Res 32: 47-56.
43. Richter JD, Lorenz LJ (2002) Selective translation of mRNAs at synapses. Curr Opin Neurobiol 12: 300-304. (Pubitemid 34618522)
44. Bramham CR, Wells DG (2007) Dendritic mRNA: transport, translation and function. Nature Rev Neurosci 8: 776-789. (Pubitemid 47462112)
45. Korz V, Frey JU (2007) Hormonal and monoamine signaling during reinforcement of hippocampal long-term potentiation and memory retrieval. Learn Mem 14: 160-166. (Pubitemid 46495193)
46. Schulz K, Korz V (2010) Hippocampal testosterone relates to reference memory performance and synaptic plasticity in male rats. Front Behav Neurosci 4; doi: 10.3389/fnbeh.2010.00187.
47. McEwen BS, Luine VN, Plapinger L, de Kloet ER (1975) Putative estrogen and glucocorticoid receptors in the limbic brain. J Steroid Biochem 6: 971-977.
48. Takeshita H (1976) Evidence for soluble estradiol receptors in the amygdala of male and female rats. Yonago Acta Med 20: 125-141.
49. McEwen BS (2002) Estrogen actions throughout the brain. Recent Prog Horm Res 57: 357-384.
50. MacLusky NJ, Lieberburg I, McEwen BS (1979) The development of estrogen receptor systems in the rat brain: perinatal development. Brain Res 178: 129-142. (Pubitemid 10241294)
51. Han X, Aenlle KK, Bean LA, Rani A, Semple-Rowland SL et al. (2013) Role of Estrogen Receptor α and β in Preserving Hippocampal Function during Aging. J Neurosci 33: 2671-83.