Dihydrotestosterone increases hippocampal N-methyl-D-aspartate binding but does not affect choline acetyltransferase cell number in the forebrain or choline transporter levels in the CA1 region of adult male rats

Endocrinology

Volumn 146, Issue 4, 2005, Pages 2091-2097

  Romeo, Russell D ^a   Staub, Daniel ^b   Jasnow, Aaron M ^a   Karatsoreos, Ilia N ^c   Thornton, Janice E ^b   McEwen, Bruce S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b OBERLIN COLLEGE   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; ANDROSTANOLONE; CHOLINE ACETYLTRANSFERASE; CHOLINE TRANSPORTER; GLUTAMATE RECEPTOR; HEMICHOLINIUM 3; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; CELL COUNT; CONTROLLED STUDY; DENDRITIC SPINE; DIAGONAL BAND OF BROCA; FOREBRAIN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; WESTERN BLOTTING;

ANIMALS; CELL COUNT; CHOLINE O-ACETYLTRANSFERASE; DIHYDROTESTOSTERONE; FEMALE; HIPPOCAMPUS; MALE; MEMBRANE TRANSPORT PROTEINS; N-METHYLASPARTATE; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER;

EID: 15444368509     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2004-0886     Document Type: Article

References (65)

1. Lee SJ, Romeo RD, Svenningsson P, Campomanes CR, Allen PB, Greengard P, McEwen BS 2004 Estradiol affects spinophilin protein differently in gonadectomized males and females. Neuroscience 127:983-988
2. Brake WG, Alves SE, Dunlop JC, Lee SJ, Bulloch K, Allen PB, Greengard P, McEwen BS 2001 Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 142:1284-1289
3. Woolley CS, Gould E, Frankfurt M, McEwen BS 1990 Naturally occurring fluctuations in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039
4. Woolley CS, McEwen BS 1992 Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554
5. Gould E, Woolley CS, Frankfurt M, McEwen BS 1990 Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10:1286-1291
6. Choi JM, Romeo RD, Brake WG, Bethea CL, Rosenwaks Z, McEwen BS 2003 Estradiol increases pre- and post-synaptic proteins in the CA1 region of the hippocampus in female rhesus macaques (Macaca mulatta). Endocrinology 144:4734-4738
7. Li C, Brake WG, Romeo RD, Dunlop JC, Gordon M, Buzescu R, Margarinos AM, Allen P, Greengard P, Luine V, McEwen BS 2004 Estrogen treatment alters hippocampal dendritic spine shape, enhances synaptic protein immunoreactivity and performance in a spatial working memory task in female C57BL/6J mice. Proc Natl Acad Sci USA 101:2185-2190
8. Leranth C, Shanabiough M, Redmond DE 2002 Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J Comp Neurol 447:34-42
9. Gibbs RB, Gabor R, Cox T, Johnson DA 2004 Effects of raloxifene and estradiol on hippocampal acetylcholine release and spatial learning in the rat. Psychoneuroendocrinology 29:741-748
10. Gibbs RB1999 Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition. Horm Behav 36:222-233
11. Bimonte HA, Denenberg VH 1999 Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 24:161-173
12. Daniel JM, Fader AJ, Spencer AL, Dohanich GP 1998 Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225
13. Heikkinen T, Puolivali J, Liu L, Rissanen A, Heikki T 2002 Effects of ovariectomy and estrogen treatment on learning and hippocampal neurotransmitters in mice. Horm Behav 41:22-32
14. Luine VN 1997 Steroid hormone modulation of hippocampal dependent spatial memory. Stress 2:21-36
15. Luine VN, Jacome LF, MacLusky NJ 2003 Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144:2836-2844
16. Luine VN, Richards ST, Wu VY, Beck KD 1998 Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 34:149-162
17. Sandstrom NJ, Williams CL 2004 Spatial memory retention is enhanced by acute and continuous estradiol replacement. Horm Behav 45:128-135
18. Sandstrom NJ, Williams CL 2001 Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115:384-393
19. Cordoba-Montoya DA, Carrer HF 1997 Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 778:430-438
20. Warren SG, Humphreys AG, Juraska JM, Greenough WT 1995 LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrous rats. Brain Res 703:26-30
21. Good M, Day M, Muir JL 1999 Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region. Eur J Neurosci 11:4476-4480
22. Leranth C, Petnehazy O, MacLusky NJ 2003 Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J Neurosci 23:1588-1592
23. Lewis C, McEwen BS, Frankfurt M 1995 Estrogen-induction of dendritic spines in ventromedial hypothalamus and hippocampus: effects of neonatal aromatase blockade and adult GDX. Dev Brain Res 87:91-95
24. Leranth C, Hajszan T, MacLusky NJ 2004 Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats. J Neurosci 24:495-499
25. Meyer G, Ferres-Torres R, Mas M 1978 The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study. Brain Res 155:108-112
26. McEwen BS, Tanapat P, Weiland NG 1999 Inhibition of dendritic spine induction on hippocampal CA1 pyramidal neurons by a nonsteroidal estrogen antagonist in female rats. Endocrinology 140:1044-1047
27. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan L, Alves SE 2001 Ultrastructural evidence that hippocampal α estrogen receptors are located at extranuclear sites. J Comp Neurol 429:355-371
28. McEwen BS, Akama K, Alves SE, Brake WG, Bulloch K, Lee S, Li CJ, Yeun G, Milner TA 2001 Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc Natl Acad Sci USA 98:7093-7100
29. Romeo RD, McEwen BS 2004 Sex differences in steroid-induced synaptic plasticity. In: Miller VM, Hay M, eds. Advances in molecular and cellular biology: principles of sex-based differences in physiology. London: Elsevier Science; 247-258
30. Woolley CS, McEwen BS 1994 Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680-7687
31. Daniel JM, Dohanich GP 2001 Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 21:6949-6956
32. Weiland NG 1992 Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinology 131:662-668
33. Gibbs RB, Wu D, Hersh LB, Pfaff DW 1994 Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp Neurol 129:70-80
34. Gibbs RB 1996 Fluctuations in relative levels of choline acetyltransferase mRNA in different regions of the rat basal forebrain across the estrous cycle: effects of estrogen and progesterone. J Neurosci 16:1049-1055
35. Gibbs RB 1997 Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Res 757:10-16
36. Gibbs RB 2000 Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function. Neuroscience 101:931-938
37. Luine VN, McEwen BS 1983 Sex differences in cholinergic enzymes of diagonal band nuclei in the rat preoptic area. Neuroendocrinology 36:475-482
38. Luine VN 1985 Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp Neurol 89:484-490
39. Luine VN, Renner KJ, McEwen BS 1986 Sex-dependent differences in estrogen regulation of choline acetyltransferase are altered by neonatal treatments. Endocrinology 119:874-878
40. Gabor R, Nagle R, Johnston DA, Gibbs RB 2003 Estrogen enhances potassium-stimulated acetylcholine release in the rat hippocampus. Brain Res 962: 244-247
41. Romeo RD, Lee SJ, Wang A, McEwen BS 2004 Sex differences in estrogen-induced hippocampal NMDA receptors and forebrain cholinergic activity in adult rats. Horm Behav 46:100
42. Leranth C, Shanabrough M, Horvath TL 2000 Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience 101:349-356
43. Lam T-T, Leranth C 2003 Role of the medial septum diagonal band of Broca cholinergic neurons in oestrogen-induced spine synapse formation on hippocampal CA1 pyramidal cells of female rats. Eur J Neurosci 17:1997-2005
44. Kovacs EG, MacLusky NJ, Leranth C 2003 Effects of testosterone on hippocampal CA1 spine synaptic density in the male rate are inhibited by fimbria/ fornix transection. Neuroscience 122:807-810
45. Gaykema RP, Luiten PG, Nyakas C, Trabar J 1990 Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293:103-124
46. Jope RS 1979 High affinity choline transport and acetyl CoA production in brain and their role in the regulation of acetylcholine synthesis. Brain Res 180:313-344
47. Lowenstein PR, Coyle JT 1986 Rapid regulation of [3H]hemicholinium-3 binding sites in the rat brain. Brain Res 381:191-194
48. Ferguson SM, Bazalakova M, Savchenko V, Tapia JC, Wright J, Blakely RD 2004 Lethal impairment of cholinergic neurotransmission in hemicholinium-3- sensitive choline transporter knockout mice. Proc Natl Acad Sci USA 101: 8762-8767
49. Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman CJ, Yi H, Levey AI, Blakely RD 2003 Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci 23:9697-9709
50. Brice A, Berrard S, Raynaud B, Ansieau S, Coppola T, Weber MJ, Mallet J 1991 Complete sequence of a cDNA encoding an active rat choline acetyl-transferase: a tool to investigate the plasticity of cholinergic phenotype expression. J Neurosci Res 23:266-273
51. Karatsoreos IN, Yan L, LeSauter J, Silver R 2004 Phenotype matters: identification of light-responsive cells in the mouse suprachiasmatic nucleus. J Neurosci 24:68-75
52. Paxinos G, Watson C 1986 The rat brain in stereotaxic atlas. 2nd ed. London: Academic Press
53. Nakamura N, Fujita H, Kawata M 2002 Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats. Neuroscience 109:473-485
54. Roselli CE, Horton LE, Resko JA 1985 Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 117:2471-2477
55. Kus L, Handa RJ, Hautman JM, Beitz AJ 1995 Castration increases [125I]MK-801 binding in the hippocampus of male rats. Brain Res 683:270-274
56. Sheng M 2001 Molecular organization of the postsynaptic specialization. Proc Natl Acad Sci USA 98:7058-7061
57. Pouliot WA, Handa RJ, Beck SG 1996 Androgen modulates N-methyl-D-aspartate-mediated depolarization in CAl hippocampal pyramidal cells. Synapse 23:10-19
58. Harley CW, Malsbury CW, Squires A, Brown RAM 2000 Testosterone decreases CA1 plasticity in vivo in gonadectomized male rats. Hippocampus 10:693-697
59. Frye CA, Lacey EH 2001 Posttraining androgens' enhancement of cognitive performance is temporally distinct from androgens' increases in affective behavior. Cogn Affect Behav Neurosci 1:172-182
60. Cherrier MM, Craft S, Matsumoto AH 2003 Cognitive changes associated with supplementation of testosterone or dihydrotestosterone in mildly hypogonadal men: a preliminary report. J Androl 24:568-576
61. Frye CA, Edinger KL, Seliga AM, Wawrzycki JM 2004 5α-Reduced androgens may have actions in the hippocampus to enhance cognitive performance of male rats. Psychoneuroendocrinology 29:1019-1027
62. Bimonte-Nelson HA, Singleton RS, Nelson ME, Eckman CB, Barber J, Scott TY, Granholm AC 2003 Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp Neurol 181:301-312
63. Kerr JE, Allore RJ, Beck SG, Handa RJ 1995 Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 136:3213-3221
64. Xiao L, Jordan CL 2002 Sex differences, laterality, and hormonal regulation of androgen receptor immunoreactivity in rat hippocampus. Horm Behav 42: 327-336
65. Sar M, Lubahn DB, French FS, Wilson EM 1990 Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinology 127:3180-3186