Aromatase promoter I.f is regulated by progesterone receptor in mouse hypothalamic neuronal cell lines

Journal of Molecular Endocrinology

Volumn 47, Issue 1, 2011, Pages 69-80

  Bertan Yilmaz, M ^a,b   Wolfe, Andrew ^c   Zhao, Hong ^a   Brooks, David C ^a   Bulun, Serdar E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CUKUROVA UNIVERSITY   (Turkey)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; ESTROGEN RECEPTOR ALPHA; GESTAGEN; LETROZOLE; MESSENGER RNA; MIFEPRISTONE; PROGESTERONE RECEPTOR; PROMEGESTONE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL LINE; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; HYPOTHALAMUS; IMMUNOBLOTTING; INHIBITION KINETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; AROMATASE; BASE SEQUENCE; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; ENZYME ASSAYS; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEEDBACK, PHYSIOLOGICAL; GENES, REPORTER; HYPOTHALAMUS; LUCIFERASES, RENILLA; MICE; MIFEPRISTONE; MOLECULAR SEQUENCE DATA; NEURONS; PROGESTINS; PROMEGESTONE; PROMOTER REGIONS, GENETIC; RECEPTORS, PROGESTERONE; TRANSCRIPTION, GENETIC;

EID: 79960976988     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-10-0149     Document Type: Article

References (65)

1. Abdelgadir SE, Resko JA, Ojeda SR, Lephart ED, McPhaul MJ & Roselli CE 1994 Androgens regulate aromatase cytochrome P450 messenger ribonucleic acid in rat brain. Endocrinology 135 395-401. (doi:10.1210/en.135.1.395)
2. Bakker J, Honda S, Harada N & Balthazart J 2002 The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. Journal of Neuroscience 22 9104-9112.
3. Bakker J, Honda S, Harada N & Balthazart J 2003 The aromatase knockout (ArKO) mouse provides new evidence that estrogens are required for the development of the female brain. Annals of the New York Academy of Sciences 1007 251-262. (doi:10.1196/annals.1286. 024)
4. Bakker J, Baillien M, Honda S, Harada N & Balthazart J 2004a Relationships between aromatase activity in the brain and gonads and behavioural deficits in homozygous and heterozygous aromatase knockout mice. Journal of Neuroendocrinology 16 483-490. (doi:10.1111/j.1365-2826.2004.01191.x)
5. Bakker J, Honda S, Harada N & Balthazart J 2004b Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice. Hormones and Behavior 46 1-10. (doi:10.1016/ j.yhbeh.2004.02.003)
6. Balthazart J, Baillien M & Ball GF 2001 Phosphorylation processes mediate rapid changes of brain aromatase activity. Journal of Steroid Biochemistry and Molecular Biology 79 261-277. (doi:10.1016/S0960-0760(01)00143-1)
7. Balthazart J, Baillien M, Charlier TD, Cornil CA & Ball GF 2003 Multiple mechanisms control brain aromatase activity at the genomic and non-genomic level. Journal of Steroid Biochemistry and Molecular Biology 86 367-379. (doi:10.1016/S0960-0760(03)00346-7)
8. Brock O, Douhard Q, Baum MJ & Bakker J 2010 Reduced prepubertal expression of progesterone receptor in the hypothalamus of female aromatase knockout mice. Endocrinology 151 1814-1821. (doi:10.1210/en.2009-1379)
9. Bulun SE, Lin Z, Imir G, Amin S, Demura M, Yilmaz B, Martin R, Utsunomiya H, Thung S, Gurates B et al. 2005 Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacological Reviews 57 359-383. (doi:10.1124/pr.57.3.6)
10. Chow JD, Simpson ER & Boon WC 2009 Alternative 50-untranslated first exons of the mouse Cyp19A1 (aromatase) gene. Journal of Steroid Biochemistry and Molecular Biology 115 115-125. (doi:10.1016/ j.jsbmb.2009.03.010)
11. Conneely OM, Mulac-Jericevic B, Lydon JP & De Mayo FJ 2001 Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice. Molecular and Cellular Endocrinology 179 97-103. (doi:10.1016/S0303-7207(01)00465-8)
12. Connolly PB & Resko JA 1989 Progestins affect reproductive behavior and androgen receptor dynamics in male guinea pig brain. Brain Research 503 312-316. (doi:10.1016/0006-8993(89)91681-8)
13. DeBold JF, Morris JL & Clemens LG 1978 The inhibitory actions of progesterone: effects on male and female sexual behavior of the hamster. Hormones and Behavior 11 28-41. (doi:10.1016/0018-506X(78)90056-9)
14. Erpino MJ 1975 Androgen-induced aggression in neonatally androgenized female mice: inhibition by progesterone. Hormones and Behavior 6 149-157. (doi:10.1016/0018-506X(75)90030-6)
15. Evans RW & Leavitt WW 1980 Progesterone inhibition of uterine nuclear estrogen receptor: dependence on RNA and protein synthesis. PNAS 77 5856-5860. (doi:10.1073/pnas.77.10.5856)
16. Fisher CR, Graves KH, Parlow AF & Simpson ER 1998 Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. PNAS 95 6965-6970. (doi:10.1073/ pnas.95.12.6965)
17. Fortune JE & Vincent SE 1983 Progesterone inhibits the induction of aromatase activity in rat granulosa cells in vitro. Biology of Reproduction 28 1078-1089. (doi:10.1095/biolreprod28.5.1078)
18. Golovine K, Schwerin M & Vanselow J 2003 Three different promoters control expression of the aromatase cytochrome p450 gene (cyp19) in mouse gonads and brain. Biology of Reproduction 68 978-984. (doi:10.1095/biolreprod.102.008037)
19. Hansen S & Sodersten P 1978 Effects of subcutaneous implants of progesterone on the induction and duration of sexual receptivity in ovariectomized rats. Journal of Endocrinology 77 373-379. (doi:10. 1677/joe.0.0770373)
20. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, Mukai H, Morrison JH, Janssen WG, Kominami S et al. 2004 Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. PNAS 101 865-870. (doi:10.1073/pnas. 2630225100)
21. Honda S, Harada N & Takagi Y 1996 The alternative exons 1 of the mouse aromatase cytochrome P-450 gene. Biochemica et Biophysica Acta 1305 145-150. (doi:10.1016/0167-4781(95)00200-6)
22. Honda S, Harada N, Abe-Dohmae S & Takagi Y 1999 Identification of cis-acting elements in the proximal promoter region for brainspecific exon 1 of the mouse aromatase gene. Brain Research. Molecular Brain Research 66 122-132. (doi:10.1016/S0169-328X(99)00017-0)
23. Iivonen S, Heikkinen T, Puolivali J, Helisalmi S, Hiltunen M, Soininen H & Tanila H 2006 Effects of estradiol on spatial learning, hippocampal cytochrome P450 19, and estrogen alpha and beta mRNA levels in ovariectomized female mice. Neuroscience 137 1143-1152. (doi:10.1016/j.neuroscience.2005. 10.023)
24. Ing NH & Tornesi MB 1997 Estradiol up-regulates estrogen receptor and progesterone receptor gene expression in specific ovine uterine cells. Biology of Reproduction 56 1205-1215. (doi:10.1095/ biolreprod56.5.1205)
25. Jakab RL, Horvath TL, Leranth C, Harada N & Naftolin F 1993 Aromatase immunoreactivity in the rat brain: gonadectomysensitive hypothalamic neurons and an unresponsive limbic ring of the lateral septum-bed nucleus-amygdala complex. Journal of Steroid Biochemistry and Molecular Biology 44 481-498. (doi:10.1016/0960-0760(93)90253-S)
26. Jones ME, Boon WC, Proietto J & Simpson ER 2006 Of mice and men: the evolving phenotype of aromatase deficiency. Trends in Endocrinology and Metabolism 17 55-64. (doi:10.1016/j.tem.2006. 01.004)
27. Keefe DL 2002 Sex hormones and neural mechanisms. Archives of Sexual Behavior 31 401-403. (doi:10.1023/A:1019883923346)
28. Lavaque E, Mayen A, Azcoitia I, Tena-Sempere M & Garcia-Segura LM 2006 Sex differences, developmental changes, response to injury and cAMP regulation of the mRNA levels of steroidogenic acute regulatory protein, cytochrome p450scc, and aromatase in the olivocerebellar system. Journal of Neurobiology 66 308-318.
29. Le Goascogne C, Eychenne B, Tonon MC, Lachapelle F, Baumann N & Robel P 2000 Neurosteroid progesterone is up-regulated in the brain of jimpy and shiverer mice. Glia 29 14-24. (doi:10.1002/ (SICI)1098-1136(20000101)29:1!14::AID-GLIA2O3.0.CO;2-N)
30. Lephart ED 1996 A review of brain aromatase cytochrome P450. Brain Research. Brain Research Reviews 22 1-26. (doi:10.1016/0165-0173(96)00002-1)
31. Lephart ED 1997 Molecular aspects of brain aromatase cytochrome P450. Journal of Steroid Biochemistry and Molecular Biology 61 375-380. (doi:10.1016/S0960-0760(97)80035-0)
32. Lephart ED, Butler PC, Mills RH, Jacobson NA, Ladle DR & Bloch GJ 1998 Effects of testosterone and progesterone on brain 5alphareductase and aromatase in Long-Evans males and comparison of aromatase in Long-Evans vs. Sprague-Dawley rats. Brain Research 789 327-330. (doi:10.1016/S0006-8993(97)01553-9)
33. Levine JE, Chappell PE, Schneider JS, Sleiter NC & Szabo M 2001 Progesterone receptors as neuroendocrine integrators. Frontiers in Neuroendocrinology 22 69-106. (doi:10.1006/frne.2001.0210)
34. Mani SK, Blaustein JD, Allen JM, Law SW, O'Malley BW & Clark JH 1994 Inhibition of rat sexual behavior by antisense oligonucleotides to the progesterone receptor. Endocrinology 135 1409-1414. (doi:10. 1210/en.135.4.1409)
35. Matsumoto T, Honda S & Harada N 2003a Alteration in sex-specific behaviors in male mice lacking the aromatase gene. Neuroendocrinology 77 416-424. (doi:10.1159/000071313)
36. Matsumoto T, Honda S & Harada N 2003b Neurological effects of aromatase deficiency in the mouse. Journal of Steroid Biochemistry and Molecular Biology 86 357-365. (doi:10.1016/S0960-0760(03) 00345-5)
37. Michael RP, Saayman GS & Zumpe D 1968 The suppression of mounting behaviour and ejaculation in male rhesus monkeys (Macaca mulatta) by administration of progesterone to their female partners. Journal of Endocrinology 41 421-431. (doi:10.1677/joe.0. 0410421)
38. Nausch N, Manteuffel G & Vanselow J 2007 Promoter sequence of the murine Cyp19 gene target beta-galactosidase expression to specific brain areas of transgenic mice. Journal of Steroid Biochemistry and Molecular Biology 103 119-128. (doi:10.1016/j.jsbmb.2006. 08.007)
39. Negri-Cesi P, Colciago A, Motta M, Martini L & Celotti F 2001 Aromatase expression and activity in male and female cultured rat hypothalamic neurons: effect of androgens. Molecular and Cellular Endocrinology 178 1-10. (doi:10.1016/S0303-7207(01)00442-7)
40. Perkins A & Roselli CE 2007 The ram as a model for behavioral neuroendocrinology. Hormones and Behavior 52 70-77. (doi:10.1016/j.yhbeh.2007.03.016)
41. Peterson RS, Yarram L, Schlinger BA & Saldanha CJ 2005 Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proceedings. Biological Sciences/The Royal Society 272 2089-2096. (doi:10.1098/rspb.2005.3181)
42. Pluchino N, Luisi M, Lenzi E, Centofanti M, Begliuomini S, Freschi L, Ninni F & Genazzani AR 2006 Progesterone and progestins: effects on brain, allopregnanolone and beta-endorphin. Journal of Steroid Biochemistry and Molecular Biology 102 205-213. (doi:10.1016/j. jsbmb.2006.09.023)
43. Pollio G, Xue P, Zanisi M, Nicolin A & Maggi A 1993 Antisense oligonucleotide blocks progesterone-induced lordosis behavior in ovariectomized rats. Brain Research. Molecular Brain Research 19 135-139. (doi:10.1016/0169-328X(93)90158-L)
44. Prange-Kiel J, Rune GM, Zwirner M, Wallwiener D & Kiesel L 2001 Regulation of estrogen receptor alpha and progesterone receptor (isoform A and B) expression in cultured human endometrial cells. Experimental and Clinical Endocrinology and Diabetes 109 231-237. (doi:10.1055/s-2001-15111)
45. Prange-Kiel J, Wehrenberg U, Jarry H & Rune GM 2003 Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus 13 226-234. (doi:10.1002/hipo.10075)
46. Rhoda J, Valens M, Edwards DA & Roffi J 1987 Effect of progesterone on the testosterone and estradiol levels in the hypothalamus of neonatal rats. Biology of the Neonate 51 255-259. (doi:10.1159/000242661)
47. Roselli CE, Abdelgadir SE & Resko JA 1997 Regulation of aromatase gene expression in the adult rat brain. Brain Research Bulletin 44 351-357. (doi:10.1016/S0361-9230(97)00214-1)
48. Rune GM, Lohse C, Prange-Kiel J, Fester L & Frotscher M 2006 Synaptic plasticity in the hippocampus: effects of estrogen from the gonads or hippocampus? Neurochemical Research 31 145-155. (doi:10.1007/s11064-005-9004-8)
49. Schneider JS, Burgess C, Sleiter NC, DonCarlos LL, Lydon JP, O'Malley B & Levine JE 2005 Enhanced sexual behaviors and androgen receptor immunoreactivity in the male progesterone receptor knockout mouse. Endocrinology 146 4340-4348. (doi:10.1210/en.2005-0490)
50. Sharma TP, Blache D, Roselli CE & Martin GB 2004 Distribution of aromatase activity in brain and peripheral tissues of male sheep: effect of nutrition. Reproduction, Fertility, and Development 16 709-715. (doi:10.1071/RD04018)
51. Shozu M, Sebastian S, Takayama K, Hsu WT, Schultz RA, Neely K, Bryant M & Bulun SE 2003 Estrogen excess associated with novel gain-of-function mutations affecting the aromatase gene. New England Journal of Medicine 348 1855-1865. (doi:10.1056/NEJMoa021559)
52. Simpson ER 2004a Aromatase: biologic relevance of tissue-specific expression. Seminars in Reproductive Medicine 22 11-23. (doi:10. 1055/s-2004-823023)
53. Simpson ER 2004b Models of aromatase insufficiency. Seminars in Reproductive Medicine 22 25-30. (doi:10.1055/s-2004-823024)
54. Simpson ER & Davis SR 2001 Minireview: aromatase and the regulation of estrogen biosynthesis - some new perspectives. Endocrinology 142 4589-4594. (doi:10.1210/en.142.11.4589)
55. Simpson E, Rubin G, Clyne C, Robertson K, O'Donnell L, Davis S & Jones M 1999 Local estrogen biosynthesis in males and females. Endocrine-Related Cancer 6 131-137. (doi:10.1677/erc.0.0060131)
56. Smanik EJ, Young HK, Muldoon TG & Mahesh VB 1983 Analysis of the effect of progesterone in vivo on estrogen receptor distribution in the rat anterior pituitary and hypothalamus. Endocrinology 113 15-22. (doi:10.1210/endo-113-1-15)
57. Sodersten P & Hansen S 1977 Effects of oestradiol and progesterone on the induction and duration of sexual receptivity in cyclic female rats. Journal of Endocrinology 74 477-485. (doi:10.1677/joe.0. 0740477)
58. Tagawa N, Sugimoto Y, Yamada J & Kobayashi Y 2006 Strain differences of neurosteroid levels in mouse brain. Steroids 71 776-784. (doi:10. 1016/j.steroids.2006.05.008)
59. Trainor BC, Bird IM, Alday NA, Schlinger BA & Marler CA 2003 Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior. Neuroendocrinology 78 36-44. (doi:10.1159/000071704)
60. Voigt C, Ball GF & Balthazart J 2007 Neuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain. Journal of Chemical Neuroanatomy 33 75-86. (doi:10.1016/j.jchemneu. 2006.12.004)
61. Wagner CK 2006 The many faces of progesterone: a role in adult and developing male brain. Frontiers in Neuroendocrinology 27 340-359. (doi:10.1016/j.yfrne.2006.07.003)
62. Witt DM, Young LJ & Crews D 1995 Progesterone modulation of androgen-dependent sexual behavior in male rats. Physiology and Behavior 57 307-313. (doi:10.1016/0031-9384(94)00247-3)
63. Yilmaz MB, Wolfe A, Cheng YH, Glidewell-Kenney C, Jameson JL & Bulun SE 2009 Aromatase promoter I.f is regulated by estrogen receptor alpha (ESR1) in mouse hypothalamic neuronal cell lines. Biology of Reproduction 81 956-965. (doi:10.1095/biolreprod.109. 077206)
64. Zhao C, Fujinaga R, Tanaka M, Yanai A, Nakahama K & Shinoda K 2007 Region-specific expression and sex-steroidal regulation on aromatase and its mRNA in the male rat brain: immunohistochemical and in situ hybridization analyses. Journal of Comparative Neurology 500 557-573. (doi:10.1002/cne.21193)
65. Zhao H, Innes J, Brooks DC, Reierstad S, Yilmaz MB, Lin Z & Bulun SE 2009 A novel promoter controls Cyp19a1 gene expression in mouse adipose tissue. Reproductive Biology and Endocrinology 24 7-37. (doi:10.1186/1477-7827-7-37)