Gestational or acute restraint in adulthood reduces levels of 5α-reduced testosterone metabolites in the hippocampus and produces behavioral inhibition of adult male rats

Frontiers in Cellular Neuroscience

Volumn , Issue SEPTEMBER, 2012, Pages 1-28

  Walf, Alicia A ^a   Frye, Cheryl A ^a,b  

^a Life Science University   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Androgens; Anxiety; Behavioral inhibition; Inhibitory avoidance; Neurosteroid; Prenatal stress; Programming; Social interaction

Indexed keywords

3ALPHA HYDROXYSTEROID DEHYDROGENASE; ANDROGEN; ANDROSTANOLONE; CORTISONE; ESTRADIOL; STEROID 5ALPHA REDUCTASE; TESTOSTERONE;

ACUTE STRESS; ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN LEVEL; CONTROLLED STUDY; DOWN REGULATION; GESTATION PERIOD; GESTATIONAL AGE; GESTATIONAL STRESS; HIPPOCAMPUS; HORMONE BLOOD LEVEL; IMMOBILIZATION STRESS; LATENT PERIOD; MALE; MAZE TEST; NONHUMAN; OPEN FIELD BEHAVIOR; RADIOIMMUNOASSAY; RAT; SOCIAL INTERACTION; STRESS; TAIL FLICK TEST; UPREGULATION;

EID: 84867068688     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00040     Document Type: Article

References (71)

1. Aikey, J.L., Nyby, J.G., Anmuth, D.M., James, P.J. (2002). Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm. Behav 42, 448-60.
2. Alonso, S.J., Navarro, E., Santana, C., Rodriguez, M. (1997). Motor lateralization, behavioral despair and dopaminergic brain asymmetry after prenatal stress. Pharmacol. Biochem. Behav 58, 443-8.
3. Andersen, S.L., Teicher, M.H. (2004). Delayed effects of early stress on hippocampal development. Neuropsychopharmacology 29, 1988-93.
4. Barker, D.J., Hales, C.N., Fall, C.H., Osmond, C., Phipps, K., Clark, P.M. (1993). Type 2 (noninsulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62-7.
5. Bortolato, M., Devoto, P., Roncada, P., Frau, R., Flore, G., Saba, P., Pistritto, G., Soggiu, A., Pisanu, S., Zappala, A., Ristaldi, M.S., Tattoli, M., Cuomo, V., Marrosu, F., Barbaccia, M.L. (2011). Isolation rearing-induced reduction of brain 5α-reductase expression: relevance to dopaminergic impairments. Neuropharmacology 60, 1301-8.
6. Bowman, R.E. (2005). Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan. J. Neuroendocrinol 17, 526-35.
7. Bowman, R.E., MacLusky, N.J., Sarmiento, Y., Frankfurt, M., Gordon, M., Luine, V.N. (2004). Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145, 3778-87.
8. Bremner, J.D., Randall, P., Vermetten, E., Staib, L., Bronen, R.A., Mazure, C., Capelli, S., McCarthy, G., Innis, R.B., Charney, D.S. (1997). Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse--a preliminary report. Biol. Psychiatry 41, 23-32.
9. Brunton, P.J., Russell, J.A. (2010). Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects. J. Neuroendocrinol 22, 258-71.
10. Buddenberg, T.E., Komorowski, M., Ruocco, L.A., Silva, M.A., Topic, B. (2009). Attenuating effects of testosterone on depressive-like behavior in the forced swim test in healthy male rats. Brain Res Bull 79, 182-6.
11. Cirulli, F., Francia, N., Branchi, I., Antonucci, M.T., Aloe, L., Suomi, S.J., Alleva, E. (2009). Changes in plasma levels of BDNF and NGF reveal a gender-selective vulnerability to early adversity in rhesus macaques. Psychoneuroendocrinology 34, 172-80.
12. DeBold, J.F., Miczek, K.A. (1981). Sexual dimorphism in the hormonal control of aggressive behavior of rats. Pharmacol. Biochem. Behav 14, 89-93.
13. Edinger, K.L., Frye, C.A. (2004). Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5α-reduced metabolites in the hippocampus. Behav. Neurosci 118, 1352-6.
14. Edinger, K.L., Frye, C.A. (2007a). Sexual experience of male rats influences anxiety-like behavior and androgen levels. Physiol. Behav 92, 443-53.
15. Edinger, K.L., Frye, C.A. (2007b). Androgens' effects to enhance learning may be mediated in part through actions at estrogen receptor-β in the hippocampus. Neurobiol. Learn. Mem 87, 78-85.
16. Entringer, S., Wüst, S., Kumsta, R., Layes, I.M., Nelson, E.L., Hellhammer, D.H., Wadhwa, P.D. (2008). Prenatal psychosocial stress exposure is associated with insulin resistance in young adults. Am. J. Obstet. Gynecol 199, 498e1-7.
17. Erskine, M.S., Kornberg, E. (1992). Stress and ACTH increase circulating concentrations of 3 alpha-androstanediol in female rats. Life Sci 51, 2065-71.
18. Fernández-Guasti, A., Martínez-Mota, L (2005). Anxiolytic-like actions of testosterone in the burying behavior test: role of androgen and GABA-benzodiazepine receptors. Psychoneuroendocrinol 30, 762-70.
19. Frye, C.A. (2009). Neurosteroids-from basic research to clinical perspectives. In: Rubin RT and Pfaff DW (Eds) Hormones/Behavior Relations of Clinical Importance, Academic Press, San Diego, pp 395-416
20. Frye, C.A., Edinger, K.L. (2004). Testosterone's metabolism in the hippocampus may mediate its anti-anxiety effects in male rats. Pharmacol. Biochem. Behav 78, 473-81.
21. Frye, C.A., Edinger, K.L., Lephart, E.D., Walf, A. A (2010). 3α-androstanediol, but not testosterone, attenuates age-related decrements in cognitive, anxiety, and depressive behavior of male rats. Front Aging Neurosci 2, 1-21.
22. Frye, C.A., Paris, J.J., Rhodes, M.E. (2007). Engaging in paced mating, but neither exploratory, anti-anxiety, nor social behavior, increases 5α-reduced progestin concentrations in midbrain, hippocampus, striatum, and cortex. Reproduction 133, 663-74.
23. Frye, C.A., Seliga, A.M. (2001). Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn. Affect Behav. Neurosci 1, 371-81.
24. Frye, C.A., Walf, A.A. (2004). Hippocampal 3α, 5α-THP may alter depressive behavior of pregnant and lactating rats. Pharmacol. Biochem. Behav 78, 531-40.
25. Frye, C.A., Wawrzycki, J. (2004). Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Horm. Behav 44, 319-26.
26. Galea, L.A. (2008). Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res. Rev 57, 332-41.
27. Gee, K.W. (1988). Steroid modulation of the GABA/benzodiazepine receptor-linked chloride ionophore. Mol. Neurobiol 2, 291-317.
28. Goel, N., Plyler, K.S., Daniels, D., Bale, T.L. (2011). Androgenic influence on serotonergic activation of the HPA stress axis. Endocrinology 152, 2001-10.
29. Guo, A.L., Petraglia, F., Criscuolo, M., Ficarra, G., Nappi, R.E., Palumbo, M.A., Trentini, G.P., Purdy, R.H., Genazzani, A.R. (1995). Evidence for a role of neurosteroids in modulation of diurnal changes and acute stress-induced corticosterone secretion in rats. Gynecol Endocrinol 9, 1-7.
30. Gustafsson, J.A., Stenberg, A. (1974). Neonatal programming of androgen responsiveness of liver of adult rats. J. Biol. Chem 249, 719-23.
31. Gustafsson, J.A., Stenberg, A. (1974). Irreversible androgenic programming at birth of microsomal and soluble rat liver enzymes active on androstene-3, 17-dione and 5α-androstane-3α, 17β-diol. J. Biol. Chem 249, 711-8.
32. Koehl, M., Darnaudery, M., Dulluc, J., Van Reeth, O., Le Moal, M., Maccari, S. (1991). Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J. Neurobiol 40, 302-15.
33. Kim, J.J., Song, E.Y., Kosten, T.A. (2006). Stress effects in the hippocampus: synaptic plasticity and memory. Stress 9, 1-11.
34. Lee, P.R., Brady, D.L., Shapiro, R.A., Dorsa, D.M., Koenig, J.L. (2007). Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin. Brain Res 1156, 152-67.
35. Lemaire, V., Koehl, M., Le Moal, M., Abrous, D.N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. PNAS 97, 11032-7.
36. Lumia, A.R., Thorner, K.M., McGinnis, M.Y. (1994). Effects of chronically high doses of the anabolic androgenic steroid, testosterone, on intermale aggression and sexual behavior in male rats. Physiol. Behav 55, 331-5.
37. Macrì, S., Laviola, G., Leussis, M.P., Andersen, S.L. (2010). Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats. Psychoneuroendocrinology 35, 392-402.
38. McCormick, C.M., Smythe, J.W., Sharma, S., Meaney, M.J. (1995). Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res. Dev. Brain Res. 84, 55-61.
39. McGinnis, M.Y. (2004). Anabolic androgenic steroids and aggression: studies using animal models. Ann N Y Acad Sci 1036, 399-415.
40. Mitev, Y.A., Darwish, M., Wolf, S.S., Holsboer, F., Almeida, O.F., Patchev, V.K. (2003). Gender differences in the regulation of 3α-hydroxysteroid dehydrogenase in rat brain and sensitivity to neurosteroid-mediated stress protection. Neuroscience 120, 541-9.
41. Mueller, B.R., Bale, T.L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28, 9055-65.
42. Mueller, B.R., Bale, T.L. (2007). Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav 91, 55-65.
43. Ordyan, N.E., Pivina, S.G. (2005). Effects of prenatal stress on the activity of an enzyme involved in neurosteroid synthesis during the "critical period" of sexual differentiation of the brain in male rats. Neurosci Behav Physiol. 35, 931-5.
44. Paris, J.J., Frye, C.A. (2011a). Gestational exposure to variable stressors produces decrements in cognitive and neural development of juvenile male and female rats. Curr. Top Med. Chem 11, 1706-13.
45. Paris, J.J., Frye, C.A. (2011b). Juvenile offspring of rats exposed to restraint stress in late gestation have impaired cognitive performance and dysregulated progestogen formation. Stress 14, 23-32.
46. Paris, J.J., Brunton, P.J., Russell, J.A., Frye, C.A. (2011a). Immune stress in late pregnant rats decreases length of gestation and fecundity, and alters later cognitive and affective behaviour of surviving pre-adolescent offspring. Stress 14, 652-64.
47. Paris, J.J., Brunton, P.J., Russell, J.A., Walf, A.A., Frye, C.A. (2011b). Inhibition of 5α-reductase activity in late pregnancy decreases gestational length and fecundity and impairs object memory and central progestogen milieu of juvenile rat offspring. J. Neuroendocrinol 23, 1079-90.
48. Patchev, V.K., Shoaib, M., Holsboer, F., Almeida, O.F. (1994). The neurosteroid tetrahydroprogesterone counteracts corticotropin-releasing hormone-induced anxiety and alters the release and gene expression of corticotropin-releasing hormone in the rat hypothalamus. Neuroscience 62, 265-71.
49. Patchev, V.K., Hassan, A.H., Holsboer, D.F., Almeida, O.F. (1996). The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15, 533-40.
50. Rodbard, D., Hutt, D.M. (1974). Statistical analysis of radioimmunoassays and immunoradiometric (labelled antibody) assays. A generalized weighted, iterative, least-squares method for logistic curve fitting. International Atomic Energy Agency 1, 165-192.
51. Russell, J.A., Brunton, P. (2010). Prenatal social stress and programmed hyper-sensitivity to stress in adult offspring: gender specific modulation by neuroactive steroids in the rat. International Behavioral Neuroscience Annual Meeting abstract, 40.
52. Sánchez P, Torres JM, Gavete P, Ortega E. (2008). Effects of swim stress on mRNA and protein levels of steroid 5α-reductase isozymes in prefrontal cortex of adult male rats. Neurochem Int 52, 426-31.
53. Sánchez P, Torres JM, Olmo A, O'Valle F, Ortega E (2009). Effects of environmental stress on mRNA and protein expression levels of steroid 5α-Reductase isozymes in adult rat brain. Horm Behav 56, 348-53.
54. Schmitz, C., Rhodes, M.E., Bludau, M., Kaplan, S., Ong, P., Ueffing, I., Vehoff, J., Korr, H., Frye, C.A. (2002). Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol. Psychiatry 7, 810-3.
55. Seckl, J.R. (2004). Prenatal glucocorticoids and long-term programming. Eur. J. Endocrinol 151, U49-62.
56. Setiawan, E., Jackson, M.F., MacDonald, J.F., Matthews, S.G. (2007). Effects of repeated prenatal glucocorticoid exposure on long-term potentiation in the juvenile guinea-pig hippocampus. J. Physiol 581, 1033-42.
57. Spritzer, M.D., Galea, L.A. (2007). Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev. Neurobiol 67, 1321-33.
58. Sternberg, W.F. (1999). Sex differences in the effects of prenatal stress on stress-induced analgesia. Physiol. Behav 68, 63-72.
59. Szuran, T.F., Pliska, V., Pokorny, J., Welzl, H. (2000). Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol. Behav 71, 353-62.
60. Torres, J.M., Ortega, E. (2003). Differential regulation of steroid 5α-reductase isozymes expression by androgens in the adult rat brain. FASEB J 17, 1428-33.
61. Torres, J.M., Ortega, E. (2006). Steroid 5α-reductase isozymes in the adult female rat brain: central role of dihydrotestosterone. J. Mol. Endocrinol 36, 239-45.
62. Tsuruo, Y. (2005). Topography and function of androgen-metabolizing enzymes in the central nervous system. Anat. Sci. Int 80, 1-11.
63. Walf, A.A., Frye, C.A. (2005). Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic-pituitary-adrenal axis activity. Neuropsychopharmacology 30, 1288-301.
64. Walf, A.A., Frye, C.A. (2007). Estradiol decreases anxiety behavior and enhances inhibitory avoidance and gestational stress produces opposite effects. Stress 10, 251-60.
65. Ward, I.L., Ward, O.B., Winn, R.J., Bielawski, D. (1994). Male and female sexual behavior potential of male rats prenatally exposed to the influence of alcohol, stress, or both factors. Behav. Neurosci 108, 1188-95.
66. Ward, I.L., Ward, O.B., French, J.A., Hendricks, S.E., Mehan, D., Winn, R.J. (1996). Prenatal alcohol and stress interact to attenuate ejaculatory behavior, but not serum testosterone or LH in adult male rats. Behav Neurosci 110, 1469-77.
67. Ward, I.L., Bennett, A.L., Ward, O.B., Hendricks, S.E., French, J.A. (1999). Androgen threshold to activate copulation differs in male rats prenatally exposed to alcohol, stress, or both factors. Horm. Behav 36, 129-40.
68. Weinstock, M. (2007). Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem. Res 32, 1730-40.
69. Weinstock, M., Matlina, E., Maor, G.I., Rosen, H., McEwen, B.S. (1992). Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res 595, 195-200.
70. Zagron, G., Weinstock, M. (2006). Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav. Brain Res 175, 323-8.
71. Zuena, A.R., Mairesse, J., Casolini, P., Cinque, C., Alemà, G.S., Morley-Fletcher, S., Chiodi, V., Spagnoli, L.G., Gradini, R., Catalani, A., Nicoletti, F., Maccari, S. (2008). Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE 3, 2170.