Estrogen receptor ligands counteract cognitive deficits caused by androgen deprivation in male rats

Hormones and Behavior

Volumn 59, Issue 4, 2011, Pages 581-584

  Lagunas, Natalia ^a   Calmarza Font, Isabel ^a   Grassi, Daniela ^a   Garcia Segura, Luis M ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

Cross maze test; Diarylpropionitrile; Estradiol; Propyl pyrazole triol; Raloxifene; Tamoxifen

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; ANDROGEN; DIARYLPROPIONITRILE; ESTRADIOL BENZOATE; RALOXIFENE; TAMOXIFEN;

ANDROGEN DEFICIENCY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CLINICAL PRACTICE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG PROTEIN BINDING; LEARNING; MALE; MAZE TEST; MEMORY; NONHUMAN; ORCHIECTOMY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RAT; SHAM PROCEDURE; TREATMENT RESPONSE;

ANIMALS; BRAIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MALE; MAZE LEARNING; NITRILES; ORCHIECTOMY; PROPIONATES; PYRAZOLES; RALOXIFENE; RATS; RATS, WISTAR; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TAMOXIFEN;

EID: 79954767107     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.02.014     Document Type: Article

References (43)

1. Aubele T., Kaufman R., Montalmant F., Kritzer M.F. Effects of gonadectomy and hormone replacement on a spontaneous novel object recognition task in adult male rats. Horm. Behav. 2008, 54:244-252.
2. Barreto G., Santos-Galindo M., Diz-Chaves Y., Pernía O., Carrero P., Azcoitia I., Garcia-Segura L.M. Selective estrogen receptor modulators decrease reactive astrogliosis in the injured brain: effects of aging and prolonged depletion of ovarian hormones. Endocrinology 2009, 150:5010-5015.
3. Beer T.M., Bland L.B., Bussiere J.R., Neiss M.B., Wersinger E.M., Garzotto M., Ryan C.W., Janowsky J.S. Testosterone loss and estradiol administration modify memory in men. J. Urol. 2006, 175:130-135.
4. Benice T.S., Raber J. Dihydrotestosterone modulates spatial working-memory performance in male mice. J. Neurochem. 2009, 110:902-911.
5. Bernstein L., Deapen D., Cerhan J.R., Schwartz S.M., Liff J., McGann-Maloney E., Perlman J.A., Ford L. Tamoxifen therapy for breast cancer and endometrial cancer risk. J. Natl Cancer Inst. 1999, 91:1654-1662.
6. Bowman R.E., Ferguson D., Luine V.N. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience 2002, 113:401-410.
7. Cerciat M., Unkila M., Garcia-Segura L.M., Arevalo M.A. Selective estrogen receptor modulators decrease the production of interleukin-6 and interferon-gamma-inducible protein-10 by astrocytes exposed to inflammatory challenge in vitro. Glia 2010, 58:93-102.
8. Cherrier M.M., Matsumoto A.M., Amory J.K., Ahmed S., Bremner W., Peskind E.R., Raskind M.A., Johnson M., Craft S. The role of aromatization in testosterone supplementation effects on cognition in older men. Neurology 2005, 64:290-296.
9. Ciriza I., Carrero P., Azcoitia I., Lundeen S.G., Garcia-Segura L.M. Selective estrogen receptor modulators protect hippocampal neurons from kainic acid excitotoxicity: differences with the effect of estradiol. J. Neurobiol. 2004, 61:209-221.
10. Conrad C.D., Jackson J.L., Wieczorek L., Baran S.E., Harman J.S., Wright R.L., Korol D.L. Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmacol. Biochem. Behav. 2004, 78:569-579.
11. Dhandapani K.M., Brann D.W. Protective effects of estrogen and selective estrogen receptor modulators in the brain. Biol. Reprod. 2002, 67:1379-1385.
12. Edinger K.L., Frye C.A. Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus. Behav. Neurosci. 2004, 118:1352-1364.
13. Edinger K.L., Frye C.A. Androgens' effects to enhance learning may be mediated in part through actions at estrogen receptor-beta in the hippocampus. Neurobiol. Learn. Mem. 2007, 87:78-85.
14. Fernández-Balsells M.M., Murad M.H., Lane M., Lampropulos J.F., Albuquerque F., Mullan R.J., Agrwal N., Elamin M.B., Gallegos-Orozco J.F., Wang A.T., Erwin P.J., Bhasin S., Montori V.M. Clinical review 1: adverse effects of testosterone therapy in adult men: a systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 2010, 95:2560-2575.
15. Forwood S.E., Winters B.D., Bussey T.J. Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 2005, 15:347-355.
16. Frye C.A. Estradiol tends to improve inhibitory avoidance performance in adrenalectomized male rats and reduces pyknotic cells in the dentate gyrus of adrenalectomized male and female rats. Brain Res. 2001, 889:358-363.
17. Frye C.A., Seliga A.M. Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn. Affect. Behav. Neurosci. 2001, 1:371-381.
18. Frye C.A., Edinger K., Sumida K. Androgen administration to aged male mice increases anti-anxiety behavior and enhances cognitive performance. Neuropsychopharmacology 2008, 33:1049-1061.
19. Frye C.A., Koonce C.J., Edinger K.L., Osborne D.M., Walf A.A. Androgens with activity at estrogen receptor beta have anxiolytic and cognitive-enhancing effects in male rats and mice. Horm. Behav. 2008, 54:726-734.
20. Frye C.A., Edinger K.L., Lephart E.D., Walf A.A. 3alpha-androstanediol, but not testosterone, attenuates age-related decrements in cognitive, anxiety, and depressive behavior of male rats. Front. Aging Neurosci. 2010, 2:15.
21. Garcia-Segura L.M. Aromatase in the brain: not just for reproduction anymore. J. Neuroendocrinol. 2008, 20:705-712.
22. Goekoop R., Barkhof F., Duschek E.J., Netelenbos C., Knol D.L., Scheltens P., Rombouts S.A. Raloxifene treatment enhances brain activation during recognition of familiar items: a pharmacological fMRI study in healthy elderly males. Neuropsychopharmacology 2006, 31:1508-1518.
23. Hatanaka Y., Mukai H., Mitsuhashi K., Hojo Y., Murakami G., Komatsuzaki Y., Sato R., Kawato S. Androgen rapidly increases dendritic thorns of CA3 neurons in male rat hippocampus. Biochem. Biophys. Res. Commun. 2009, 381:728-732.
24. Hawkins R.A., Freedman B., Marshall A., Killen E. Oestradiol-17 beta and prolactin levels in rat peripheral plasma. Br. J. Cancer 1975, 32:179-185.
25. Holmes M.M., Wide J.K., Galea L.A. Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behav. Neurosci. 2002, 116:928-934.
26. Kretz O., Fester L., Wehrenberg U., Zhou L., Brauckmann S., Zhao S., Prange-Kiel J., Naumann T., Jarry H., Frotscher M., Rune G.M. Hippocampal synapses depend on hippocampal estrogen synthesis. J. Neurosci. 2004, 24:5913-5921.
27. Kritzer M.F., McLaughlin P.J., Smirlis T., Robinson J.K. Gonadectomy impairs T-maze acquisition in adult male rats. Horm. Behav. 2001, 39:167-174.
28. Liu F., Day M., Muñiz L.C., Bitran D., Arias R., Revilla-Sanchez R., Grauer S., Zhang G., Kelley C., Pulito V., Sung A., Mervis R.F., Navarra R., Hirst W.D., Reinhart P.H., Marquis K.L., Moss S.J., Pangalos M.N., Brandon N.J. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat. Neurosci. 2008, 11:334-343.
29. MacLusky N.J., Hajszan T., Prange-Kiel J., Leranth C. Androgen modulation of hippocampal synaptic plasticity. Neuroscience 2006, 138:957-965.
30. Palacios S., Farias M.L., Luebbert H., Gomez G., Yabur J.A., Quail D.C., Turbi C., Kayath M.J., Almeida M.J., Mönnig E., Nickelsen T. Raloxifene is not associated with biologically relevant changes in hot flushes in postmenopausal women for whom therapy is appropriate. Am. J. Obstet. Gynecol. 2004, 191:121-131.
31. Pike A.C. Lessons learnt from structural studies of the oestrogen receptor. Best Pract. Res. Clin. Endocrinol. Metab. 2006, 20:1-14.
32. Prange-Kiel J., Rune G.M., Leranth C. Median raphe mediates estrogenic effects to the hippocampus in female rats. Eur. J. Neurosci. 2004, 19:309-317.
33. Rhodes M.E., Frye C.A. ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol. Learn. Mem. 2006, 85:183-191.
34. Roselli C.F. Brain aromatase: roles in reproduction and neuroprotection. J. Steroid Biochem. Mol. Biol. 2007, 106:143-150.
35. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol. 1990, 294:76-95.
36. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 1997, 388:507-525.
37. Spritzer M.D., Gill M., Weinberg A., Galea L.A. Castration differentially affects spatial working and reference memory in male rats. Arch. Sex. Behav. 2008, 37:19-29.
38. Stovall D.W., Utian W.H., Gass M.L., Qu Y., Muram D., Wong M., Plouffe L. The effects of combined raloxifene and oral estrogen on vasomotor symptoms and endometrial safety. Menopause 2007, 14:510-517.
39. Tapia-Gonzalez S., Carrero P., Pernia O., Garcia-Segura L.M., Diz-Chaves Y. Selective oestrogen receptor (ER) modulators reduce microglia reactivity in vivo after peripheral inflammation: potential role of microglial ERs. J. Endocrinol. 2008, 198:219-230.
40. Woolley C.S. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 2007, 47:657-680.
41. Yague J.G., Azcoitia I., DeFelipe J., Garcia-Segura L.M., Muñoz A. Aromatase expression in the normal and epileptic human hippocampus. Brain Res. 2010, 1315:41-52.
42. Zadran S., Qin Q., Bi X., Zadran H., Kim Y., Foy M.R., Thompson R., Baudry M. 17-Beta-estradiol increases neuronal excitability through MAP kinase-induced calpain activation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:21936-21941.
43. Zhao L., O'Neill K., Brinton R.D. Selective estrogen receptor modulators (SERMs) for the brain: current status and remaining challenges for developing NeuroSERMs. Brain Res. Brain Res. Rev. 2005, 49:472-493.