Estradiol regulation of progesterone synthesis in the brain

Molecular and Cellular Endocrinology

Volumn 290, Issue 1-2, 2008, Pages 44-50

  Micevych, Paul ^a,b   Sinchak, Kevin ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Estrogen positive feedback; Estrogen receptor; mGluR; Neurosteroids; Neurotransmission; Progesterone; Progesterone receptor

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; 4 CARBOXY 2 METHYLPHENYLGLYCINE; AMINOGLUTETHIMIDE; CALCIUM CHANNEL; CALCIUM ION; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); DIMETHYL SULFOXIDE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUTAMATE RECEPTOR 1; GONADOTROPIN; INOSITOL TRISPHOSPHATE; LUTEINIZING HORMONE; NEUROSTEROID; PHOSPHOLIPASE C; PROGESTERONE; PROGESTERONE RECEPTOR; THAPSIGARGIN;

ADRENAL GLAND; ASTROCYTE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CYTOPLASM; DRUG MECHANISM; ESTRUS CYCLE; GENETIC TRANSCRIPTION; HORMONAL REGULATION; HORMONE BLOOD LEVEL; HYPOTHALAMUS; MENOPAUSE; NONHUMAN; OVARY FUNCTION; OVULATION; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; ESTRADIOL; FEEDBACK, BIOCHEMICAL; HUMANS; MENOPAUSE; PROGESTERONE;

EID: 47849128961     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.04.016     Document Type: Review

References (82)

1. Alila H.W., Davis J.S., Dowd J.P., Corradino R.A., and Hansel W. Differential effects of calcium on progesterone production in small and large bovine luteal cells. J. Steroid Biochem. 36 (1990) 687-693
2. Arakane F., King S.R., Du Y., Kallen C.B., Walsh L.P., Watari H., Stocco D.M., and Strauss III J.F. Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J. Biol. Chem. 272 (1997) 32656-32662
3. Bjorkhem I., and Meaney S. Brain cholesterol: long secret life behind a barrier. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 806-815
4. Boulware M.I., Weick J.P., Becklund B.R., Kuo S.P., Groth R.D., and Mermelstein P.G. Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J. Neurosci. 25 (2005) 5066-5078
5. Brom G.M., and Schwartz N.B. Acute changes in the estrous cycle following ovariectomy in the golden hamster. Neuroendocrinology 3 (1968) 366-377
6. Buckingham J.C., Deohler K.D., and Wilson C.A. Activity of the pituitary-adrenocortical system and thyroid gland during the oestrous cycle of the rat. J. Endocrinol. 78 (1978) 359-366
7. Chaban, V., Li, J., McDonald, J., Rapkin, A., Micevych, P., 2007. Estradiol attenuates ATP-induced increase of intracellular calcium through group II metabotropic glutamate receptors in rat DRG neurons. Society for Neuronscience. Neuroscience Meeting Planner. Program No. 519.7.
8. Chaban V.V., Lakhter A.J., and Micevych P. A membrane estrogen receptor mediates intracellular calcium release in astrocytes. Endocrinology 145 (2004) 3788-3795
9. Chaban V.V., Mayer E.A., Ennes H.S., and Micevych P.E. Estradiol inhibits atp-induced intracellular calcium concentration increase in dorsal root ganglia neurons. Neuroscience 118 (2003) 941-948
10. Chappell P.E., and Levine J.E. Stimulation of gonadotropin-releasing hormone surges by estrogen. I. Role of hypothalamic progesterone receptors. Endocrinology 141 (2000) 1477-1485
11. Cooper R.L., Conn P.M., and Walker R.F. Characterization of the LH surge in middle-aged female rats. Biol. Reprod. 23 (1980) 611-615
12. Corpechot C., Robel P., Axelson M., Sjovall J., and Baulieu E.E. Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 4704-4707
13. Corpechot C., Young J., Calvel M., Wehrey C., Veltz J.N., Touyer G., Mouren M., Prasad V.V., Banner C., and Sjovall J. Neurosteroids: 3 alpha-hydroxy-5 alpha-pregnan-20-one and its precursors in the brain, plasma, and steroidogenic glands of male and female rats. Endocrinology 133 (1993) 1003-1009
14. DePaolo L.V. Attenuation of preovulatory gonadotrophin surges by epostane: a new inhibitor of 3 beta-hydroxysteroid dehydrogenase. J. Endocrinol. 118 (1988) 59-68
15. DePaolo L.V., and Barraclough C.A. Dose dependent effects of progesterone on the facilitation and inhibition of spontaneous gonadotropin surges in estrogen treated ovariectomized rats. Biol. Reprod. 21 (1979) 1015-1023
16. Dewing P., Boulware M.I., Sinchak K., Christensen A., Mermelstein P.G., and Micevych P. Membrane estrogen receptor-alpha interactions with metabotropic glutamate receptor 1a modulate female sexual receptivity in rats. J. Neurosci. 27 (2007) 9294-9300
17. Ferin M., Tempone A., Zimmering P.E., and Van de Wiele R.L. Effect of antibodies to 17beta-estradiol and progesterone on the estrous cycle of the rat. Endocrinology 85 (1969) 1070-1078
18. Filardo E.J., Quinn J.A., Bland K.I., and Frackelton Jr. A.R. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14 (2000) 1649-1660
19. Filardo E.J., Quinn J.A., Frackelton Jr. A.R., and Bland K.I. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16 (2002) 70-84
20. Freeman D.A. Cyclic AMP mediated modification of cholesterol traffic in Leydig tumor cells. J. Biol. Chem. 262 (1987) 13061-13068
21. Granot Z., Silverman E., Friedlander R., Melamed-Book N., Eimerl S., Timberg R., Hales K.H., Hales D.B., Stocco D.M., and Orly J. The life cycle of the steroidogenic acute regulatory (StAR) protein: from transcription through proteolysis. Endocr. Res. 28 (2002) 375-386
22. Guennoun R., Fiddes R.J., Gouezou M., Lombes M., and Baulieu E.E. A key enzyme in the biosynthesis of neurosteroids, 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4-isomerase (3 beta-HSD), is expressed in rat brain. Brain Res. Mol. Brain Res. 30 (1995) 287-300
23. Hammes S.R., and Levin E.R. Extranuclear steroid receptors: nature and actions. Endocr. Rev. 28 (2007) 726-741
24. Hibbert M.L., Stouffer R.L., Wolf D.P., and Zelinski-Wooten M.B. Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 1897-1901
25. 2+ without generation of inositol phosphates in NG115-401L neuronal cells. Biochem. J. 253 (1988) 81-86
26. Jo Y., King S.R., Khan S.A., and Stocco D.M. Involvement of protein kinase C and cyclic adenosine 3′,5′-monophosphate-dependent kinase in steroidogenic acute regulatory protein expression and steroid biosynthesis in Leydig cells. Biol. Reprod. 73 (2005) 244-255
27. Jung-Testas I., Hu Z.Y., Baulieu E.E., and Robel P. Neurosteroids: biosynthesis of pregnenolone and progesterone in primary cultures of rat glial cells. Endocrinology 125 (1989) 2083-2091
28. Jung-Testas I., Renoir J.M., Gasc J.M., and Baulieu E.E. Estrogen-inducible progesterone receptor in primary cultures of rat glial cells. Exp. Cell Res. 193 (1991) 12-19
29. Kallen C.B., Arakane F., Christenson L.K., Watari H., Devoto L., and Strauss III J.F. Unveiling the mechanism of action and regulation of the steroidogenic acute regulatory protein. Mol. Cell. Endocrinol. 145 (1998) 39-45
30. Karri S., Dertien J.S., Stocco D.M., and Syapin P.J. Steroidogenic acute regulatory protein expression and pregnenolone synthesis in rat astrocyte cultures. J. Neuroendocrinol. 19 (2007) 860-869
31. Kawato S., Yamada M., and Kimoto T. Brain neurosteroids are 4th generation neuromessengers in the brain: cell biophysical analysis of steroid signal transduction. Adv. Biophys. 37 (2003) 1-48
32. King S.R., Manna P.R., Ishii T., Syapin P.J., Ginsberg S.D., Wilson K., Walsh L.P., Parker K.L., Stocco D.M., Smith R.G., and Lamb D.J. An essential component in steroid synthesis, the steroidogenic acute regulatory protein, is expressed in discrete regions of the brain. J. Neurosci. 22 (2002) 10613-10620
33. Kohchi C., Ukena K., and Tsutsui K. Age- and region-specific expressions of the messenger RNAs encoding for steroidogenic enzymes p450scc, P450c17 and 3beta-HSD in the postnatal rat brain. Brain Res. 801 (1998) 233-238
34. Kuo J., Hariri O., Bondar G., Ogi J., Shung M.S., and Micevych P. Membrane estradiol receptors interact with metabotropic glutamate receptors in hypothalamic astrocytes. Reprod. Sci. 15 (2008) 36
35. Labhsetwar A.P. Role of estrogens in ovulation: a study using the estrogen-antagonist, I.C.I. 46,474. Endocrinology 87 (1970) 542-551
36. Lamacz M., Tonon M.C., Smih-Rouet F., Patte C., Gasque P., Fontaine M., and Vaudry H. The endogenous benzodiazepine receptor ligand ODN increases cytosolic calcium in cultured rat astrocytes. Brain Res. Mol. Brain Res. 37 (1996) 290-296
37. Lu K.H., Hopper B.R., Vargo T.M., and Yen S.S. Chronological changes in sex steroid, gonadotropin and prolactin secretions in aging female rats displaying different reproductive states. Biol. Reprod. 21 (1979) 193-203
38. MacLusky N.J., and McEwen B.S. Oestrogen modulates progestin receptor concentrations in some rat brain regions but not in others. Nature 274 (1978) 276-278
39. Maguire J., and Mody I. Neurosteroid synthesis-mediated regulation of GABA(A) receptors: relevance to the ovarian cycle and stress. J. Neurosci. 27 (2007) 2155-2162
40. Mahesh V.B., and Brann D.W. Interaction between ovarian and adrenal steroids in the regulation of gonadotropin secretion. J. Steroid Biochem. Mol. Biol. 41 (1992) 495-513
41. Mahesh V.B., and Brann D.W. Neuroendocrine mechanisms underlying the control of gonadotropin secretion by steroids. Steroids 63 (1998) 252-256
42. Mann D.R., Korowitz C.D., and Barraclough C.A. Adrenal gland involvement in synchronizing the preovulatory release of LH in rats. Proc. Soc. Exp. Biol. Med. 150 (1975) 115-120
43. Matt D.W., Lee J., Sarver P.L., Judd H.L., and Lu J.K. Chronological changes in fertility, fecundity and steroid hormone secretion during consecutive pregnancies in aging rats. Biol. Reprod. 34 (1986) 478-487
44. Mensah-Nyagan A.G., Do-Rego J.L., Beaujean D., Luu-The V., Pelletier G., and Vaudry H. Neurosteroids: expression of steroidogenic enzymes and regulation of steroid biosynthesis in the central nervous system. Pharmacol. Rev. 51 (1999) 63-81
45. Micevych P., and Sinchak K. Synthesis and function of hypothalamic neuroprogesterone in reproduction. Endocrinology 149 6 (2008) 2739-2742
46. Micevych P., Sinchak K., Mills R.H., Tao L., LaPolt P., and Lu J.K. The luteinizing hormone surge is preceded by an estrogen-induced increase of hypothalamic progesterone in ovariectomized and adrenalectomized rats. Neuroendocrinology 78 (2003) 29-35
47. Micevych P., Soma K.K., and Sinchak K. Neuroprogesterone: key to estrogen positive feedback?. Brain Res. Rev. 57 (2008) 470-480
48. Micevych P.E., Chaban V., Ogi J., Lakhter A., Lu J.K.H., and Sinchak K. Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures. Endocrinology 148 (2007) 782-789
49. Mills R.H., Romeo H.E., Lu J.K., and Micevych P.E. Site-specific decrease of progesterone receptor mRNA expression in the hypothalamus of middle-aged persistently estrus rats. Brain Res. 955 (2002) 200-206
50. Momoi K., Waterman M.R., Simpson E.R., and Zanger U.M. 3′,5′-cyclic adenosine monophosphate-dependent transcription of the CYP11A (cholesterol side chain cleavage cytochrome P450) gene involves a DNA response element containing a putative binding site for transcription factor Sp1. Mol. Endocrinol. 6 (1992) 1682-1690
51. Nass T.E., Lapolt P.S., Judd H.L., and Lu J.K. Alterations in ovarian steroid and gonadotrophin secretion preceding the cessation of regular oestrous cycles in ageing female rats. J. Endocrinol. 100 (1984) 43-50
52. Niswender G.D. Molecular control of luteal secretion of progesterone. Reproduction 123 (2002) 333-339
53. Papadopoulos V. Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: biological role in steroidogenic cell function. Endocr. Rev. 14 (1993) 222-240
54. Papadopoulos V., Amri H., Boujrad N., Cascio C., Culty M., Garnier M., Hardwick M., Li H., Vidic B., Brown A.S., Reversa J.L., Bernassau J.M., and Drieu K. Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 62 (1997) 21-28
55. Papadopoulos V., Amri H., Li H., Boujrad N., Vidic B., and Garnier M. Targeted disruption of the peripheral-type benzodiazepine receptor gene inhibits steroidogenesis in the R2C Leydig tumor cell line. J. Biol. Chem. 272 (1997) 32129-32135
56. Payne A.H., and Hales D.B. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr. Rev. 25 (2004) 947-970
57. Putnam C.D., Brann D.W., and Mahesh V.B. Acute activation of the adrenocorticotropin-adrenal axis: effect on gonadotropin and prolactin secretion in the female rat. Endocrinology 128 (1991) 2558-2566
58. Qiu J., Bosch M.A., Tobias S.C., Grandy D.K., Scanlan T.S., Ronnekleiv O.K., and Kelly M.J. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci. 23 (2003) 9529-9540
59. Rao M.C., Palfrey H.C., Nash N.T., Greisman A., Jayatilak P.G., and Gibori G. Effects of estradiol on calcium-specific protein phosphorylation in the rat corpus luteum. Endocrinology 120 (1987) 1010-1018
60. Razandi M., Pedram A., Greene G., and Levin E. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol. Endocrinol. 13 (1999) 307-319
61. Remohi J., Balmaceda J.P., Rojas F.J., and Asch R.H. The role of pre-ovulatory progesterone in the midcycle gonadotrophin surge, ovulation and subsequent luteal phase: studies with RU486 in rhesus monkeys. Hum. Reprod. 3 (1988) 431-435
62. Robel P., and Baulieu E.E. Neurosteroids and neuroactive steroids. In: Micevych P.E., and Hammer R.P. (Eds). Neurobiological Effects of Sex Steroid Hormones (1995), Cambridge University Press, Cambridge 281-296
63. Sanchez-Criado J.E., Hernandez G., Bellido C., Gonzalez D., Tebar M., Diaz-Cruz M.A., and Alonso R. Periovulatory LHRH, LH and FSH secretion in cyclic rats treated with RU486: effects of exogenous LHRH and LHRH antagonist on LH and FSH secretion at early oestrus. J. Endocrinol. 141 (1994) 7-14
64. Sanne J.L., and Krueger K.E. Expression of cytochrome P450 side-chain cleavage enzyme and 3 beta-hydroxysteroid dehydrogenase in the rat central nervous system: a study by polymerase chain reaction and in situ hybridization. J. Neurochem. 65 (1995) 528-536
65. Shaikh A.A., and Shaikh S.A. Adrenal and ovarian steroid secretion. Endocrinology 96 (1975) 37-44
66. Shalem Z., Izhar M., Shore L.S., Shemesh M., Hansel W., and Strauss III J.F. Control of bovine placental progestin synthesis: calcium dependent steroidogenesis is modulated at the site of the cholesterol side chain cleavage enzyme. J. Steroid Biochem. 31 (1988) 835-838
67. Shemesh M., Hansel W., and Strauss III J.F. Calcium-dependent, cyclic nucleotide-independent steroidogenesis in the bovine placenta. Proc. Natl. Acad. Sci. U.S.A. 81 (1984) 6403-6407
68. Sinchak K., Mills R.H., Tao L., LaPolt P., Lu J.K., and Micevych P. Estrogen induces de novo progesterone synthesis in astrocytes. Dev. Neurosci. 25 (2003) 343-348
69. Snipes G.J., and Suter U. Cholesterol and myelin. Subcell. Biochem. 28 (1997) 173-204
70. Snyder B.W., Beecham G.D., and Schane H.P. Inhibition of ovulation in rats with epostane, an inhibitor of 3beta-hydroxysteroid dehydrogenase. Proc. Soc. Exp. Biol. Med. 176 (1984) 238-242
71. Soma K.K., Sinchak K., Lakhter A., Schlinger B.A., and Micevych P.E. Neurosteroids and female reproduction: estrogen increases 3beta-HSD mRNA and activity in rat hypothalamus. Endocrinology 146 (2005) 4386-4390
72. Stocco D.M. StAR protein and the regulation of steroid hormone biosynthesis. Ann. Rev. Physiol. 63 (2001) 193-213
73. Stocco D.M., and Clark B.J. Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem. Pharmacol. 51 (1996) 197-205
74. Stocco D.M., Wang X., Jo Y., and Manna P.R. Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol. Endocrinol. 19 (2005) 2647-2659
75. Toran-Allerand C.D., Guan X., MacLusky N.J., Horvath T.L., Diano S., Singh M., Connolly Jr. E.S., Nethrapalli I.S., and Tinnikov A.A. ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J. Neurosci. 22 (2002) 8391-8401
76. Toran-Allerand C.D., Singh M., and Setalo Jr. G. Novel mechanisms of estrogen action in the brain: new players in an old story. Front. Neuroendocrinol. 20 (1999) 97-121
77. Waterman M.R. Biochemical diversity of cAMP-dependent transcription of steroid hydroxylase genes in the adrenal cortex. J. Biol. Chem. 269 (1994) 27783-27786
78. Wintermantel T.M., Campbell R.E., Porteous R., Bock D., Grone H.J., Todman M.G., Korach K.S., Greiner E., Perez C.A., Schutz G., and Herbison A.E. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 52 (2006) 271-280
79. Wise P.M. Alterations in proestrous LH, FSH, and prolactin surges in middle-aged rats. Proc. Soc. Exp. Biol. Med. 169 (1982) 348-354
80. Young J.K. Immunoreactivity for diazepam binding inhibitor in Gomori-positive astrocytes. Regul. Pept. 50 (1994) 159-165
81. Zur Nieden R., and Deitmer J.W. The role of metabotropic glutamate receptors for the generation of calcium oscillations in rat hippocampal astrocytes in situ. Cereb. Cortex 16 (2006) 676-687
82. Zwain I.H., and Yen S.S. Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140 (1999) 3843-3852