Perimenopausal regulation of steroidogenesis in the nonhuman primate

Neurobiology of Aging

Volumn 33, Issue 7, 2012, Pages 1487.e1-1487.e13

  Sorwell, Krystina G ^a,b   Kohama, Steven G ^a   Urbanski, Henryk F ^a,b,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Aging; Dehydroepiandrosterone; Hormone replacement; Menopause; Neurosteroidogenesis

Indexed keywords

ESTRADIOL; HYDROCORTISONE; PRASTERONE; PROGESTERONE;

3BHSD1 GENE; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROMATASE GENE; ARTICLE; CLIMACTERIUM; COGNITIVE DEFECT; CONTROLLED STUDY; CYP17A1 GENE; ESTROGEN SYNTHESIS; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HORMONAL REGULATION; HORMONE SUBSTITUTION; MALE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; STEROID BLOOD LEVEL; STEROIDOGENESIS; STS GENE; SULT2B1 GENE;

EID: 84861200815     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.05.004     Document Type: Article

References (70)

1. Baulieu E.E. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 1998, 23:963-987.
2. Brann D.W., Dhandapani K., Wakade C., Mahesh V.B., Khan M.M. Neurotrophic and neuroprotective actions of estrogen: Basic mechanisms and clinical implications. Steroids 2007, 72:381-405.
3. Ceresini G., Morganti S., Rebecchi I., Freddi M., Ceda G.P., Banchini A., Solerte S.B., Ferrari E., Ablondi F., Valenti G. Evaluation of the circadian profiles of serum dehydroepiandrosterone (DHEA), cortisol, and cortisol/DHEA molar ratio after a single oral administration of DHEA in elderly subjects. Metabolism 2000, 49:548-551.
4. Chehab O., Ouertani M., Chaieb K., Haouala F., Mahdouani K. Hormonal status of cortisol and dehydroepiandrosterone sulfate in an elderly Tunisian population. C. R. Biol 2007, 330:755-763.
5. Crawford S., Santoro N., Laughlin G.A., Sowers M.F., McConnell D., Sutton-Tyrrell K., Weiss G., Vuga M., Randolph J., Lasley B. Circulating dehydroepiandrosterone sulfate concentrations during the menopausal transition. J. Clin. Endocrinol. Metab 2009, 94:2945-2951.
6. Davis S.R., Shah S.M., McKenzie D.P., Kulkarni J., Davison S.L., Bell R.J. Dehydroepiandrosterone sulfate levels are associated with more favorable cognitive function in women. J. Clin. Endocinol Metab 2008, 93:801-808.
7. Downs J.L., Mattison J.A., Ingram D.K., Urbanski H.F. Effect of age and caloric restriction on circadian adrenal steroid rhythms in rhesus macaques. Neurobiol. Aging 2008, 29:1412-1422.
8. Downs J.L., Urbanski H.F. Neuroendocrine changes in the aging reproductive axis of female rhesus macaques (Macaca mulatta). Biol. Reprod 2006, 75:539-546.
9. Farr S.A., Banks W.A., Uezu K., Gaskin F.S., Morley J.E. DHEAS improves learning and memory in aged SAMP8 mice but not in diabetic mice. Life Sci 2004, 75:2775-2785.
10. Ferrari E., Magri F. Role of neuroendocrine pathways in cognitive decline during aging. Ageing Res. Rev 2008, 7:225-233.
11. Fillit H., Weinreb H., Cholst I., Luine V., McEwen B., Amador R., Zabriskie J. Observations in a preliminary open trial of estradiol therapy for senile dementia-Alzheimer's type. Psychoneuroendocrinology 1986, 11:337-345.
12. Flood J.F., Farr S.A., Johnson D.A., Li P.K., Morley J.E. Peripheral steroid sulfatase inhibition potentiates improvement of memory retention for hippocampally administered dehydroepiandrosterone sulfate but not pregnenolone sulfate. Psychoneuroendocrinology 1999, 24:799-811.
13. Flood J.F., Roberts E. Dehydroepiandrosterone sulfate improves memory in aging mice. Brain Res 1988, 448:178-181.
14. Flood J.F., Smith G.E., Roberts E. Dehydroepiandrosterone and its sulfate enhance memory retention in mice. Brain Res 1988, 447:269-278.
15. George O., Vallée M., Le Moal M., Mayo W. Neurosteroids and cholinergic systems: implications for sleep and cognitive processes and potential role of age-related changes. Psychopharmacol. Berl 2006, 186:402-413.
16. Grimley-Evans J., Malouf R., Huppert F., van Niekerk J.K. Dehydroepiandrosterone (DHEA) supplementation for cognitive function in healthy elderly people. Cochrane Database Syst. Rev 2006, 18. CD006221.
17. Guazzo E.P., Kirkpatrick P.J., Goodyer I.M., Shiers H.M., Herbert J. Cortisol, dehydroepiandrosterone (DHEA), and DHEA sulfate in the cerebrospinal fluid of man: relation to blood levels and the effects of age. J. Clin. Endocrinol. Metab 1996, 81:3951-3960.
18. Haley G.E., Landauer N., Renner L., Weiss A., Hooper K., Urbanski H.F., Kohama S.G., Neuringer M., Raber J. Circadian activity associated with spatial learning and memory in aging rhesus monkeys. Exp. Neurol 2009, 217:55-62.
19. Hao J., Rapp P.R., Janssen W.G., Lou W., Lasley B.L., Hof P.R., Morrison J.H. Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11465-11470.
20. Hajszan T., Maclusky N.J., Leranth C. Dehydroepiandrosterone increases hippocampal spine synapse density in ovariectomized female rats. Endocrinology 2004, 145:1042-1045.
21. Herndon J.G., Lacreuse A., Ladinsky E., Killiany R.J., Rosene D.L., Moss M.B. Age-related decline in DHEAS is not related to cognitive impairment in aged monkeys. Neuroreport 1999, 10:3507-3511.
22. Hirshman E., Merritt P., Wang C.C., Wierman M., Budescu D.V., Kohrt W., Templin J.L., Bhasin S. Evidence that androgenic and estrogenic metabolites contribute to the effects of dehydroepiandrosterone on cognition in postmenopausal women. Horm. Behav 2004, 45:144-155.
23. Juhász-Vedre G., Rózsa E., Rákos G., Dobszay M.B., Kis Z., Wölfling J., Toldi J., Párducz A., Farkas T. Dehydroepiandrosterone sulfate is neuroprotective when administered either before or after injury in a focal cortical cold lesion model. Endocrinology 2006, 147:683-686.
24. Kalmijn S., Launer L.J., Stolk R.P., de Jong F.H., Pols H.A., Hofman A., Breteler M.M., Lamberts S.W. A prospective study on cortisol, dehydroepiandrosterone sulfate, and cognitive function in the elderly. J. Clin. Endocrinol. Metab 1998, 83:3487-3492.
25. Kohama S.G., Bethea C.L. Steroid regulation of tyrosine hydroxylase messenger ribonucleic acid in dopaminergic subpopulations of monkey hypothalamus. Endocrinology 1995, 136:1790-1800.
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. Kumar P., Kamat A., Mendelson C.R. Estrogen receptor alpha (ERalpha) mediates stimulatory effects of estrogen on aromatase (CYP19) gene expression in human placenta. Mol. Endocrinol 2009, 23:784-793.
28. Labrie F. Intracrinology. Mol. Cell. Endocrinol 1991, 78:C113-C118.
29. Labrie F., Luu-The V., Lin S.X., Simard J., Labrie C., El-Alfy M., Pelletier G., Bélanger A. Intracrinology: role of the family of 17 beta-hydroxysteroid dehydrogenases in human physiology and disease. J. Mol. Endocrinol 2000, 25:1-16.
30. Labrie F., Luu-The V., Labrie C., Bélanger A., Simard J., Lin S.X., Pelletier G. Endocrine and intracrine sources of androgens in women: inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone. Endocr. Rev 2003, 24:152-182.
31. Labrie F., Bélanger A., Cusan L., Gomez J.L., Candas B. Marked decline in serum concentrations of adrenal C19 sex steroid precursors and conjugated androgen metabolites during aging. J. Clin. Endocrinol. Metab 1997, 82:2396-2402.
32. Lasley B.L., Santoro N., Randolf J.F., Gold E.B., Crawford S., Weiss G., McConnell D.S., Sowers M.F. The relationship of circulating dehydroepiandrosterone, testosterone, and estradiol to stages of the menopausal transition and ethnicity. J. Clin. Endocrinol. Metab 2002, 87:3760-3767.
33. Lemos D.R., Downs J.L., Urbanski H.F. Twenty-four-hour rhythmic gene expression in the rhesus macaque adrenal gland. Mol. Endocrinol 2006, 20:1164-1176.
34. Lemos D.R., Downs J.L., Raitiere M.N., Urbanski H.F. Photoperiodic modulation of adrenal gland function in the rhesus macaque: effect on 24-h plasma cortisol and dehydroepiandrosterone sulfate rhythms and adrenal gland gene expression. J. Endocrinol 2009, 201:275-285.
35. Liu C.H., Laughlin G.A., Fischer U.G., Yen S.S. Marked attenuation of ultradian and circadian rhythms of dehydroepiandrosterone in postmenopausal women: evidence for a reduced 17,20-desmolase enzymatic activity. J. Clin. Endocrinol. Metab 1990, 71:900-906.
36. Lu T., Pan Y., Kao S.Y., Li C., Kohane I., Chan J., Yankner B.A. Gene regulation and DNA damage in the ageing human brain. Nature 2004, 429:883-891.
37. Luu-The V., Labrie F. The intracrine sex steroid biosynthesis pathways. Prog. Brain Res 2010, 181:177-192.
38. Lupien S., Lecours A.R., Schwartz G., Sharma S., Hauger R.L., Meaney M.J., Nair N.P. Longitudinal study of basal cortisol levels in healthy elderly subjects: Evidence for subgroups. Neurobiol. Aging 1996, 17:95-105.
39. Manson J.E., Hsia J., Johnson K.C., Rossouw J.E., Assaf A.R., Lasser N.L., Trevisan M., Black H.R., Heckbert S.R., Detrano R., Strickland O.L., Wong N.D., Crouse J.R., Stein E., Cushman M. Estrogen plus progestin and the risk of coronary heart disease. N. Engl. J. Med 2003, 349:523-534. Women's Health Initiative Investigators.
40. Mao X., Barger S.W. Neuroprotection by dehydroepiandrosterone-sulfate: Role of an NFkappaB-like factor. Neuroreport 1998, 9:759-763.
41. Markowski M., Ungeheuer M., Bitran D., Locurto C. Memory-enhancing effects of DHEAS in aged mice on a win-shift water escape task. Physiol. Behav 2001, 72:521-525.
42. Mellon S.H., Griffin L.D. Neurosteroids: biochemistry and clinical significance. Trends Endocrinol. Metab 2002, 13:35-43.
43. Mizuno M., Terasawa E. Search for neural substrates mediating inhibitory effects of oestrogen on pulsatile luteinising hormone-releasing hormone release in vivo in ovariectomized female rhesus monkeys (Macaca mulatta). J. Neuroendocrinol 2005, 17:238-245.
44. Moeller G., Adamski J. Integrated view on 17beta-hydroxysteroid dehydrogenases. Mol. Cell. Endocrinol 2009, 301:7-19.
45. Noriega N.C., Kohama S.G., Urbanski H.F. Microarray analysis of relative gene expression stability for selection of internal reference genes in the rhesus macaque brain. BMC Mol. Biol 2010, 11:47-71.
46. Panjari M., Bell R.J., Jane F., Adams J., Morrow C., Davis S.R. The safety of 52 weeks of oral DHEA therapy for postmenopausal women. Maturitas 2009, 63:240-245.
47. Pawlikowski M., Kolomecka M., Wojtczak A., Karasek M. Effects of six months melatonin treatment on sleep quality and serum concentrations of estradiol, cortisol, dehydroepiandrosterone sulfate, and somatomedin C in elderly women. Neuro Endocrinol. Lett 2002, 23(suppl 1):17-19.
48. Phillips A.C., Carroll D., Gale C.R., Lord J.M., Arlt W., Batty G.D. Cortisol, DHEA sulphate, their ratio, and all-cause and cause-specific mortality in the Vietnam Experience Study. Eur. J. Endocrinol 2010, 163:285-292.
49. Pluchino N., Genazzani A.D., Bernardi F., Casarosa E., Pieri M., Palumbo M., Picciarelli G., Gabbanini M., Luisi M., Genazzani A.R. Tibolone, transdermal estradiol or oral estrogen-progestin therapies: Effects on circulating allopregnanolone, cortisol and dehydroepiandrosterone levels. Gynecol. Endocrinol 2005, 20:144-149.
50. Prange-Kiel J., Fester L., Zhou L., Jarry H., Rune G.M. Estrus cyclicity of spinogenesis: underlying mechanisms. J. Neural Transm 2009, 116:1417-1425.
51. Prange-Kiel J., Jarry H., Schoen M., Kohlmann P., Lohse C., Zhou L., Rune G.M. Gonadotropin-releasing hormone regulates spine density via its regulatory role in hippocampal estrogen synthesis. J. Cell Biol 2008, 180:417-426.
52. Prange-Kiel J., Wehrenberg U., Jarry H., Rune G.M. Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus 2003, 13:226-234.
53. Rhodes M.E., Li P.K., Burke A.M., Johnson D.A. Enhanced plasma DHEAS, brain acetylcholine and memory mediated by steroid sulfatase inhibition. Brain Res 1997, 773:28-32.
54. Robel P., Bourreau E., Corpéchot C., Dang D.C., Halberg F., Clarke C., Haug M., Schlegel M.L., Synguelakis M., Vourch C., et al. Neuro-steroids: 3 beta-hydroxy-delta 5-derivatives in rat and monkey brain. J. Steroid Biochem 1987, 27:649-655.
55. Roberts E., Bologa L., Flood J.F., Smith G.E. Effects of dehydroepiandrosterone and its sulfate on brain tissue in culture and on memory in mice. Brain Res 1987, 406:357-362.
56. Rosati F., Sturli N., Cungi M.C., Morello M., Villanelli F., Bartolucci G., Finocchi C., Peri A., Serio M., Danza G. Gonadotropin-releasing hormone modulates cholesterol synthesis and steroidogenesis in SH-SY5Y cells. J. Steroid Biochem. Mol. Biol 2011, 124:77-83.
57. Rosenfeld R.S., Rosenberg B.J., Fukushima D.K., Hellman L. 24-Hour secretory pattern of dehydroisoandrosterone and dehydroisoandrosterone sulfate. J. Clin. Endocrinol. Metab 1975, 40:850-855.
58. Rune G.M., Frotscher M. Neurosteroid synthesis in the hippocampus: role in synaptic plasticity. Neuroscience 2005, 136:833-842.
59. Sanders J.L., Cappola A.R., Arnold A.M., Boudreau R.M., Chaves P.H., Robbins J., Cushman M., Newman A.B. Concurrent change in dehydroepiandrosterone sulfate and functional performance in the oldest old: results from the Cardiovascular Health Study All Stars study. J. Gerontol. A Biol. Sci. Med. Sci 2010, 65:976-981.
60. Schumacher M., Weill-Engerer S., Liere P., Robert F., Franklin R.J., Garcia-Segura L.M., Lambert J.J., Mayo W., Melcangi R.C., Parducz A., Suter U., Carelli C., Baulieu E.E., Akwa Y. Steroid hormones and neurosteroids in normal and pathological aging of the nervous system. Prog. Neurobiol 2003, 71:3-29.
61. Sorwell K.G., Urbanski H.F. Dehydroepiandrosterone and age-related cognitive decline. Age (Dordr) 2010, 32:61-67.
62. Taniguchi F., Couse J.F., Rodriguez K.F., Emmen J.M., Poirier D., Korach K.S. Estrogen receptor-alpha mediates an intraovarian negative feedback loop on thecal cell steroidogenesis via modulation of Cyp17a1 (cytochrome P450, steroid 17alpha-hydroxylase/17,20 lyase) expression. FASEB J 2007, 21:586-595.
63. Tang M.X., Jacobs D., Stern Y., Marder K., Schofield P., Gurland B., Andrews H., Maueux R. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 1996, 348:429-432.
64. Urbanski H.F. Circadian variation in the physiology and behavior of humans and nonhuman primates. Animal Models of Behavioral Analysis. Neuromethods 50 2011, 217-235. Springer, New York. J. Raber (Ed.).
65. Urbanski H.F., Garyfallou V.T., Kohama S.G., Hess D.L. Alpha-adrenergic receptor antagonism and N-methyl-d-aspartate (NMDA) induced luteinizing hormone release in female rhesus macaques. Brain Res 1997, 744:96-104.
66. Urbanski H.F., Noriega N.C., Lemos D.R., Kohama S.G. Gene expression profiling in the rhesus macaque: experimental design considerations. Methods 2009, 49:26-31.
67. Webb S.J., Geoghegan T.E., Prough R.A., Michael Miller K.K. The biological actions of dehydroepiandrosterone involves multiple receptors. Drug Metab. Rev 2006, 38:89-116.
68. Wolf O.T., Kirschbaum C. Actions of dehydroepiandrosterone and it ssulfate in the central nervous system: effects on cognition and emotion in animals and humans. Brain Res. Brain Res. Rev 1999, 30:264-288.
69. Yilmaz M.B., Wolfe A., Cheng Y.H., Glidewell-Kenney C., Jameson J.L., Bulun S.E. Aromatase promoter I.f is regulated by estrogen receptor alpha (ESR1) in mouse hypothalamic neuronal cell lines. Biol. Reprod 2009, 81:956-965.
70. Zwain I.H., Yen S.S. Dehydroepiandrosterone: Biosynthesis and metabolism in the brain. Endocrinology 1999, 140:880-887.