Chronic administration of androgens with actions at estrogen receptor beta have anti-anxiety and cognitive-enhancing effects in male rats

Age

Volumn 31, Issue 2, 2009, Pages 119-126

  Osborne, Danielle M ^a   Edinger, Kassandra ^a   Frye, Cheryl A ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

3alpha diol; 3beta diol; Aging; Androsterone; Anxiety; Cognition; Testosterone

Indexed keywords

ANDROGEN; ANDROSTANEDIONE; ANDROSTERONE; CHOLESTEROL; ESTROGEN RECEPTOR BETA; OIL;

AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; COGNITION; CONTROLLED STUDY; DRUG IMPLANT; GONADECTOMY; HORMONE RECEPTOR INTERACTION; LIGHT DARK CYCLE; MALE; MAZE TEST; NONHUMAN; RADIOIMMUNOASSAY; RAT;

EID: 67349197283     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-009-9088-1     Document Type: Article

References (54)

1. GM Alexander RS Swerdloff C Wang T Davidson V McDonald B Steiner M Hines 1998 Androgen-behavior correlations in hypogonadal men and eugonadal menII. Cognitive abilities Horm Behav 33 85 94 (Pubitemid 28285747)
2. A receptors in the rat Horm Behav 27 568 583 (Pubitemid 24003825)
3. TJ Brown GH Adler M Sharma RB Hochberg NJ MacLusky 1994 Androgen treatment decreases estrogen receptor binding in the ventromedial nucleus of the rat brain: a quantitative in vitro autoradiographic analysis Mol Cell Neurosci 5 549 555
4. I Ceccareli A Scaramuzzino AM Aloisi 2001 Effects of gonadal hormones and persist pain on non-spatial working memory in male and female rats Behav Brain Res 123 65 75
5. Cherrier MM, Aubin S, Higano CS (2009) Cognitive and mood changes in men undergoing intermittent combined androgen blockade for non-metastatic prostate cancer. Psychooncology (in press). doi: 10.1002/pon.1401
6. A/Bz receptor subtypes as targets for selective drugs Curr Med Chem 14 2680 2701
7. M Delhez M Hansenne JJ Legros 2003 Andropause and psychopathology: minor symptoms rather than pathological ones Psychoneuroendocrinology 28 863 874 (Pubitemid 36939164)
8. F Earls 1987 Sex differences in psychiatric disorders: origins and developmental influences Psych Dev 5 1 23 (Pubitemid 17067596)
9. KL Edinger CA Frye 2004 Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus Behav Neurol 118 1352 1364 (Pubitemid 39578482)
10. KL Edinger CA Frye 2005 Testosterone's anti-anxiety and analgesic effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus Psychoneuroendocrinology 30 418 430 (Pubitemid 40249808)
11. KL Edinger CA Frye 2006 Intrahippocampal administration of an androgen receptor antagonist, flutamide, can increase anxiety-like behavior in intact and DHT-replaced male rats Horm Behav 50 216 222 (Pubitemid 44041342)
12. KL Edinger CA Frye 2007 Androgens effects to enhance learning and memory may be mediated in part by actions at estrogen receptor-beta in the hippocampus Neurobiol Learn Mem 87 78 85 (Pubitemid 44679827)
13. KL Edinger CA Frye 2007 Sexual experience of male rats influences anxiety-like behavior and androgen levels Physiol Behav 92 3 443 453 (Pubitemid 47562042)
14. KL Edinger B Lee CA Frye 2004 Mnemonic effects of testosterone and its 5α-reduced metabolites in the Conditioned Fear and inhibitory avoidance tasks Pharmacol Biochem Behav 78 559 568 (Pubitemid 38901023)
15. A Fernández-Guasti L Martínez-Mota 2003 Orchidectomy sensitizes male rats to the action of diazepam on burying behavior latency: role of testosterone Pharmacol Biochem Behav 75 473 479 (Pubitemid 36859834)
16. A Fernández-Guasti L Martínez-Mota 2005 Anxiolytic-like actions of testosterone in the burying behavior test: role of androgen and GABA-benzodiazepine receptors Psychoneuroendocrinology 30 762 770 (Pubitemid 40775743)
17. CA Frye TA Reed 1998 Androgenic neurosteroids: anti-seizure effects in an animal model of epilepsy Psychoneuroendocrinology 23 4 385 399 (Pubitemid 28355753)
18. CA Frye AM Seliga 2001 Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats Cogn Affect Behav Neurosci 1 371 381 (Pubitemid 38391258)
19. CA Frye SM Petralia ME Rhodes 2000 Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha,5alpha-THP Pharmacol Biochem Behav 67 587 597
20. Frye CA, Edinger K, Sumida K (2008) Androgen administration to aged male mice increases anti-anxiety behavior and enhances cognitive performance. Neuropsychopharm 33:1049-1061
21. KW Gee 1988 Steroid Modulation of the GABA/benzodiazepine receptor-linked chloride ionophore Mol Neurobiol 2 291 317
22. C Gouchie D Kimura 1991 The relationship between testosterone levels and cognitive ability patterns Psychoneuroendocrinlogy 16 323 334
23. PB Grino JE Griffen JD Wilson 1990 Testosterone at high concentrations interacts with the human androgen receptor similarly to dihydrotestosterone Endocrinology 126 1165 1172 (Pubitemid 20079537)
24. V Guerini D Sau E Scacciancoce P Rusmini P Ciana A Maggi P Martini BS Katzenellenbogen L Martini M Motta A Poletti 2005 The androgen derivative 5α-Androstane-3α,17β-diol inhibits prostate cancer cell migration through activation of estrogen receptor beta subtype Cancer Res 65 5445 5453 (Pubitemid 40827358)
25. Handa RJ, Pak TR, Kudwa AE, Lund TD, Hinds L (2007) An alternate pathway for androgen regulation of brain function: Activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5alpha-androstane-3beta,17beta-diol. Horm Behav 53:741-752
26. JP Heaton 2003 Hormone treatments and preventive strategies in the aging male: whom and when to treat? Rev Urol 1 S16 S21
27. CF Heyns MP Simonin P Grosgurin R Schall HV Porchet 2003 Comparative efficancy of triptorelinpamoate and leuprolide acetate in men with advanced prostate cancer Br J Urol Int 92 226 231 (Pubitemid 36966582)
28. S Howell S Shalet 2001 Testosterone deficiency and replacement Horm Res 56 86 92 (Pubitemid 34062901)
29. JS Janowsky 2006 The role of androgens in cognition and brain aging in men Neurosci 138 1015 1020 (Pubitemid 43306842)
30. JS Janowsky SK Oviatt ES Orwoll 1994 Testosterone influences spatial cognition in older men Behav Neurosci 108 325 332 (Pubitemid 24142694)
31. JC Kaminetsky 2005 Benefits of a new testosterone gel formulation for hypogonadal men Clin Cornerstone 7 8 12
32. M Kaufman L Pinsky 1983 The dissociation of testosterone- and 5α-dihydrotestosterone-receptor complexes formed within cultured human genital skin fibroblasts J Steroid Biochem 18 121 125 (Pubitemid 13155146)
33. JY Li JC Zhu JT Dou WJ Bai SM Deng M Li W Huang H Jin 2002 Effects of androgen supplementation therapy on partial androgen deficiency in the aging male: a preliminary study Aging Male 5 47 51 (Pubitemid 34587557)
34. LS Marks NA Mazer E Mostaghel DL Hess FJ Dorey JI Epstein RW Veltri DV Makarov AW Partin DG Bostwick ML Macairan PS Nelson 2006 Effect of testosterone replacement therapy on prostate tissue in men with late-onset hypogonadism: a randomized controlled trial JAMA 296 2351 2361 (Pubitemid 44749363)
35. K Maubach 2003 GABA(A) receptor subtype selective cognition enhancers Curr Drug Target CNS Neurol Disord 2 4 233 239
36. MA Morgan DW Pfaff 2002 Estrogen's effects on activity, anxiety, and fear in two mouse strains Behav Brain Res 132 1 85 93 (Pubitemid 34195462)
37. RGM Morris 1984 Developments of a water-maze procedure for studying spatial learning in the rat J Neurosci Methods 11 47 60
38. MG Packard 1998 Posttraining estrogen and memory modulation Horm Behav 34 2 126 139 (Pubitemid 28541754)
39. Palomba S, Orio F, Falbo A, Oppedisano R, Tolino A, Zullo F (2008) Tibolone reverses the cognitive effects caused by leuprolide acetate administration, improving mood and quality of life in patients with symptomatic uterine leiomyomas. Fertil Steril 90:165-173 (Pubitemid 351885184)
40. HZ Pan HH Chen 2007 Hyperalgesia, low-anxiety, and impairment of avoidance learning in neonatal caffeine-treated rats Psychopharmacology (Berl) 191 1 119 125
41. JK Parsons HB Carter EA Platz EJ Wright P Landis EJ Metter 2005 Serum testosterone and the risk of prostate cancer: potential implications for testosterone therapy Cancer Epidemiol Biomarkers Prev 14 2257 2260 (Pubitemid 41603276)
42. JP Raynaud 2006 Prostate cancer risk in testosterone-treated men J Steroid Biochem Mol Biol 102 261 266
43. EF Rissman AL Heck JE Leonard MA Shupnik JA Gustafsson 2002 Disruption of estrogen receptor b gene impairs spatial learning in mice Proc Natl Acad Sci USA 99 3996 3901
44. RS Rittmaster 2008 5alpha-reductase inhibitors in benign prostatic hyperplasia and prostate cancer risk reduction Best Pract Res Clin Endocrinol Metab 22 2 389 402 (Pubitemid 351611959)
45. CE Roselli LE Horton JA Resko 1987 Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area Biol Reprod 37 628 633
46. NL Schramm-Sapyta YM Cha S Chaudhry WA Wilson HS Swartzwelder CM Kuhn 2007 Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats Psychopharmacology (Berl) 191 4 867 877 (Pubitemid 46399144)
47. JM Vongher CA Frye 1999 Progesterone in conjunction with estradiol has neuroprotective effects in an animal model of neurodegeneration Pharmacol Biochem Behav 64 4 777 785
48. Vorhees CV, Johnson HL, Burns LN, Williams MT (2009) Developmental treatment with the dopamine D2/3 agonist quinpirole selectively impairs spatial learning in the Morris water maze. Neurotoxicol Teratol 31:1-10
49. AA Walf CA Frye 2005 ERbeta-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats Neuropsychopharmacol 30 1598 1609 (Pubitemid 43086017)
50. AA Walf ME Rhodes CA Frye 2004 Antidepressants effects of ERbeta-selective estrogen receptor modulators in the forced swim test Pharmacol Biochem Behav 78 523 529 (Pubitemid 38901019)
51. Walf AA, Koonce CJ, Frye CA (2008) Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor beta knockout, mice. Behav Neurosci (5):974-981. doi: 10.1037/a0012749
52. Walf AA, Koonce C, Manley K, Frye CA (2009) Proestrous compared to diestrous wildtype, but not estrogen receptor beta knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze. Behav Brain Res 196:254-260
53. Wilbert DM, Griffen JE, Wilson JD (1983) Characterization of the cytosol androgen receptor of the human prostate. J Clin Endocrinol Metab. 56:113-20
54. JQ Zhang WQ Cai S DeZhou BY Su 2002 Distribution and differences of estrogen receptor beta immunoreactivity in the brain of adult male and female rats Brain Research 935 73 80