Transcriptional regulation of tyrosine hydroxylase by estrogen: Opposite effects with estrogen receptors α and β and interactions with cyclic AMP

Journal of Neurochemistry

Volumn 93, Issue 6, 2005, Pages 1502-1514

  Maharjan, Shreekrishna ^a   Serova, Lidia ^a   Sabban, Esther L ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Cyclic AMP; Estradiol; Estradiol receptor ; Estradiol receptor ; Promoter; Transcription; Tyrosine hydroxylase

Indexed keywords

CALCIUM ION; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; LUCIFERASE; NUCLEAR RECEPTOR RELATED FACTOR 1; TRANSCRIPTION FACTOR AP 1; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ARTICLE; CATECHOLAMINERGIC SYSTEM; CELL STRAIN; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; ENZYME ACTIVITY; ESTROGEN RESPONSIVE ELEMENT; EXPRESSION VECTOR; GEL MOBILITY SHIFT ASSAY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; REPORTER GENE; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

AMINO ACID MOTIFS; ANIMALS; BRAIN; CATECHOLAMINES; CYCLIC AMP; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REGULATOR; GENES, REPORTER; GENETIC VECTORS; NEURONS; PC12 CELLS; PROMOTER REGIONS (GENETICS); RATS; RECEPTORS, ESTROGEN; RESPONSE ELEMENTS; TRANSFECTION; TYROSINE 3-MONOOXYGENASE;

EID: 20744442720     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03142.x     Document Type: Article

References (87)

1. Anolik J. H., Klinge C. M., Hilf R. and Bambara R. A. (1995) Cooperative binding of estrogen receptor to DNA depends on spacing of binding sites, flanking sequence, and ligand. Biochemistry 34, 2511-2520.
2. Arbogast L. A. and Hyde J. F. (2000) Estradiol attenuates the forskolin-induced increase in hypothalamic tyrosine hydroxylase activity. Neuroendocrinology 71, 219-227.
3. Batistuzzo de Medeiros S. R., Krey G., Hihi A. K. and Wahli W. (1997) Functional interactions between the estrogen receptor and the transcription activator Sp1 regulate the estrogen-dependent transcriptional activity of the vitellogenin A1 io promoter. J. Biol. Chem. 272, 18250-18260.
4. Blum M., McEwen B. S. and Roberts J. L. (1987) Transcriptional analysis of tyrosine hydroxylase gene expression in the tuberoinfundibular dopaminergic neurons of the rat arcuate nucleus after estrogen treatment. J. Biol. Chem. 262, 817-821.
5. Brandenberger A. W., Tee M. K., Lee J. Y., Chao V. and Jaffe R. B. (1997) Tissue distribution of estrogen receptors alpha (ER-alpha) and beta (ER-beta) mRNA in the midgestational human fetus. J. Clin. Endocrinol. Metab. 82, 3509-3512.
6. Carley M. E., Rickard D. J., Gebhart J. B., Webb M. J., Podratz K. C. and Spelsberg T. C. (2003) Distribution of estrogen receptors alpha and beta mRNA in mouse urogenital tissues and their expression after oophorectomy and estrogen replacement. Int. Urogynecol. J. Pelvic Floor Dysfunct. 14, 141-145.
7. Cazorla P., Smidt M. P., O'Malley K. L. and Burbach J. P. (2000) A response element for the homeodomain transcription factor Ptx3 in the tyrosine hydroxylase gene promoter. J. Neurochem. 74, 1829-1837.
8. Coleman K. M., Dutertre M., El-Gharbawy A., Rowan B. G., Weigel N. L. and Smith C. L. (2003) Mechanistic differences in the activation of estrogen receptor-alpha (ER alpha)- and ER beta-dependent gene expression by cAMP signaling pathway (s). J. Biol. Chem. 278, 12834-12845.
9. Cowley S. M. and Parker M. G. (1999) A comparison of transcriptional activation by ER alpha and ER beta. J. Steroid Biochem. Mol. Biol. 69, 165-175.
10. Curran-Rauhut M. A. and Petersen S. L. (2003) Oestradiol-dependent and -independent modulation of tyrosine hydroxylase mRNA levels in subpopulations of A1 and A2 neurones with oestrogen receptor (ER) alpha and ER beta gene expression. J. Neuroendocrinol. 15, 296-303.
11. Delaunay E, Pettersson K., Tujague M. and Gustafsson J. A. (2000) Functional differences between the amino-terminal domains of estrogen receptors alpha and beta. Mol. Pharmacol. 58, 584-590.
12. Enmark E. and Gustafsson J. A. (1999) Oestrogen receptors - an overview. J. Intern. Med. 246, 133-138.
13. Federoff H. J., Grabczyk E. and Fishman M. C. (1988) Dual regulation of GAP-43 gene expression by nerve growth factor and glucocorticoids. J. Biol. Chem. 263, 19290-19295.
14. Fung B, P., Yoon S. O. and Chikaraishi D. M. (1992) Sequences that direct rat tyrosine hydroxylase gene expression. J. Neurochem. 58, 2044-2052.
15. Gizang-Ginsberg E. and Ziff E. B. (1990) Nerve growth factor regulates tyrosine hydroxylase gene transcription through a nucleoprotein complex that contains c-Fos. Genes Dev. 4, 477-491.
16. Gizang-Ginsberg E. and Ziff E. B. (1994) Fos family members successively occupy the tyrosine hydroxylase gene AP-1 site after nerve growth factor or epidermal growth factor stimulation and can repress transcription. Mol Endocrinol. 8, 249-262.
17. Glass C. K., Rose D. W. and Rosenfeld M. G. (1997) Nuclear receptor coactivators. Curr. Opin. Cell Biol. 9, 222-232.
18. Gollapudi L. and Oblinger M. M. (2001) Estrogen effects on neurite outgrowth and cytoskeletal gene expression in ERalpha-transfected PC12 cell lines. Exp. Neurol. 171, 308-316.
19. Gruber C. J., Gruber D. M., Gruber I. M., Wieser F. and Huber J. C. (2004) Anatomy of the estrogen response element. Trends Endocrinol. Metab. 15, 73-78.
20. Haegler P. and Gysling K. (2004) The activation of estrogen receptors alpha and beta exerts opposite effects on transcription of human urocortin gene. Society for Neuroscience, Abstract 841.810.
21. Hall J. M. and McDonnell D. P. (1999) The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140, 5566-5578.
22. Hall J. M., Couse J. F. and Korach K. S. (2001) The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276, 36869-36872.
23. Horwitz K. B., Jackson T. A., Bain D. L., Richer J. K., Takimoto G. S. and Tung L. (1996) Nuclear receptor coactivators and corepressors. Mol. Endocrinol. 10, 1167-1177.
24. Icard-Liepkalns C., Biguet N. F., Vyas S., Robert J. J., Sassone-Corsi P. and Mallet J. (1992) AP-1 complex and c-fos transcription are involved in TPA provoked and trans-synaptic inductions of the tyrosine hydroxylase gene: insights into long-term regulatory mechanisms. J. Neurosci. Res. 32, 290-298.
25. Katzenellenbogen J. A., O'Malley B. W. and Katzenellenbogen B. S. (1996) Tripartite steroid hormone receptor pharmacology: interaction with multiple effector sites as a basis for the cell- and promoter-specific action of these hormones. Mol. Endocrinol. 10, 119-131.
26. Kilbourne E. J., Nankova B. B., Lewis E. J., McMahon A., Osaka H., Sabban D. B. and Sabban E. L. (1992) Regulated expression of the tyrosine hydroxylase gene by membrane depolarization. Identification of the responsive element and possible second messengers. J. Biol. Chem. 267, 7563-7569.
27. Kim K. S., Lee M. K., Carroll J. and Joh T. H. (1993) Both the basal and inducible transcription of the tyrosine hydroxylase gene are dependent upon a cAMP response element. J. Biol. Chem. 268, 15689-15695.
28. Kim K. S., Kim C. H., Hwang D. Y., Seo H., Chung S., Hong S. J., Lim J. K., Anderson T. and Isacson O. (2003) Orphan nuclear receptor Nurr1 directly transactivates the promoter activity of the tyrosine hydroxylase gene in a cell-specific manner. J. Neurochem. 85, 622-634.
29. Klein-Hitpass L., Schorpp M., Wagner U. and Ryffel G. U. (1986) An estrogen-responsive element derived from the 5′ flanking region of the Xenopus vitellogenin A2 gene functions in transfected human cells. Cell 46, 1053-1061.
30. Klinge C. M. (2001) Estrogen receptor interaction with estrogen response elements. Nucl. Acids Res. 29, 2905-2919.
31. Kos M., O'Brien S., Flouriot G. and Gannon F. (2000) Tissue-specific expression of multiple mRNA variants of the mouse estrogen receptor alpha gene. FEBS Lett. 477, 15-20.
32. Krezel W., Dupont S., Krust A., Chambon P, and Chapman P. F. (2001) Increased anxiety and synaptic plasticity in estrogen receptor beta-deficient mice. Proc. Natl Acad. Sci. USA 98, 12278-12282.
33. Kuiper G. G., Enmark E., Pelto-Huikko M., Nilsson S. and Gustafsson J. A. (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl Acad. Sci. USA 93, 5925-5930.
34. Kuiper G. G., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S. and Gustafsson J. A. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863-870.
35. Kuiper G. G., Lemmen J. G., Carlsson B., Corton J. C., Safe S. H., van der Saag P. T., van der Burg B. and Gustafsson J. A. (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139, 4252-4263.
36. Kushner P. J., Agard D. A., Greene G. L., Scanlan T. S., Shiau A. K., Uht R. M. and Webb P. (2000) Estrogen receptor pathways to AP-1. J. Steroid Biochem. Mol. Biol. 74, 311-317.
37. Lazaroff M., Patankar S., Yoon S. O. and Chikaraishi D. M. (1995) The cyclic AMP response element directs tyrosine hydroxylase expression in catecholaminergic central and peripheral nervous system cell lines from transgenic mice. J. Biol. Chem. 270, 21579-21589.
38. Lewis-Tuffin L. J., Quinn P. G. and Chikaraishi D. M. (2004) Tyrosine hydroxylase transcription depends primarily on cAMP response element activity, regardless of the type of inducing stimulus. Mol. Cell. Neurosci. 25, 536-547.
39. Liaw J. J., He J. R., Hartman R. D. and Barraclough C. A. (1992) Changes in tyrosine hydroxylase mRNA levels in medullary A1 and A2 neurons and locus coeruleus following castration and estrogen replacement in rats. Brain Res. Mol. Brain Res. 13, 231-238.
40. Liu M. M., Albanese C., Anderson C. M., Hilty K., Webb P., Uht R. M., Price R. H. Jr, Pestell R. G. and Kushner P. J. (2002) Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J. Biol. Chem. 277, 24353-24360.
41. Lubahn D. B., Moyer J. S., Golding T. S., Couse J. F., Korach K. S. and Smithies O. (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl Acad. Sci. USA 90, 11162-11166.
42. Lustig R. H., Hua P. Yu W., Ahmad F. J. and Baas P. W. (1994) An in vitro model for the effects of estrogen on neurons employing estrogen receptor-transfected PC12 cells. J. Neurosci. 14, 3945-3957.
43. Matsushita N., Okada H., Yasoshima Y., Takahashi K., Kiuchi K. and Kobayashi K. (2002) Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. J. Neurochem. 82, 295-304.
44. McEwen B. S. and Alves S. E. (1999) Estrogen actions in the central nervous system. Endocr. Rev. 20, 279-307.
45. McKenna N. J., Xu J., Nawaz Z., Tsai S. Y., Tsai M. J. and O'Malley B. W. (1999) Nuclear receptor coactivators: multiple enzymes, multiple complexes, multiple functions. J. Steroid Biochem. Mol. Biol. 69, 3-12.
46. Melia K. R., Rasmussen K., Terwilliger R. Z., Haycock J. W., Nestler E. J. and Duman R. S. (1992) Coordinate regulation of the cyclic AMP system with firing rate and expression of tyrosine hydroxylase in the rat locus coeruleus: effects of chronic stress and drug treatments. J. Neurochem. 58, 494-502.
47. Menuet A., Anglade I., Flouriot G., Pakdel F. and Kah O. (2001) Tissue-specific expression of two structurally different estrogen receptor alpha isoforms along the female reproductive axis of an oviparous species, the rainbow trout. Biol. Reprod. 65, 1548-1557.
48. Miner L. L., Pandalai S. P., Weisberg E. P., Sell S. L., Kovacs D. M. and Kaplan B. B. (1992) Cold-induced alterations in the binding of adrenomedullary nuclear proteins to the promoter region of the tyrosine hydroxylase gene. J. Neurosci. Res. 33, 10-18.
49. Nagamoto-Combs K., Piech K. M., Best J. A., Sun B. and Tank A. W. (1997) Tyrosine hydroxylase gene promoter activity is regulated by both cyclic AMP-responsive element and AP1 sites following calcium influx. Evidence for cyclic AMP-responsive element binding protein-independent regulation. J. Biol. Chem. 272, 6051-6058.
50. Nagatsu T., Levitt M. and Udenfriend S. (1964) Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis. J. Biol. Chem. 239, 2910-2917.
51. Nakashima A., Ota A. and Sabban E. L. (2003) Interactions between Egr1 and AP1 factors in-regulation of tyrosine hydroxylase transcription. Brain Res. Mol. Brain Res. 112, 61-69.
52. Nankova B., Kvetnansky R., McMahon A., Viskupic E., Hiremagalur B., Frankle G., Fukuhara K., Kopin I. J. and Sabban E. L. (1994) Induction of tyrosine hydroxylase gene expression by a nonneuronal nonpituitary-mediated mechanism in immobilization stress. Proc. Natl Acad. Sci. USA 91, 5937-5941.
53. Nankova B. B., Rivkin M., Kelz M., Nestler E. J. and Sabban E. L. (2000) Fos-related antigen 2: potential mediator of the transcriptional activation in rat adrenal medulla evoked by repeated immobilization stress. J. Neurosci. 20, 5647-5653.
54. Nestler E. J., Alreja M. and Aghajanian G. K. (1999) Molecular control of locus coeruleus neurotransmission. Biol. Psychiatry 46, 1131-1139.
55. Nilsen J., Mor G. and Naftolin F. (1998) Raloxifene induces neurite outgrowth in estrogen receptor positive PC12 cells. Menopause 5, 211-216.
56. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M. and Gustafsson J. A. (2001) Mechanisms of estrogen action. Physiol. Rev. 81, 1535-1565.
57. Ogawa S., Taylor J. A., Lubahn D. B., Korach K. S. and Pfaff D. W. (1996) Reversal of sex roles in genetic female mice by disruption of estrogen receptor gene. Neuroendocrinology 64, 467-470.
58. Ogawa S., Chan J., Chester A. E., Gustafsson J. A., Korach K. S. and Pfaff D. W. (1999) Survival of reproductive behaviors in estrogen receptor beta gene-deficient (betaERKO) male and female mice. Proc. Natl Acad. Sci. USA 96, 12887-12892.
59. Ostlund H., Keller E. and Hurd Y. L. (2003) Estrogen receptor gene expression in relation to neuropsychiatric disorders. Ann. N. Y. Acad. Sci. 1007, 54-63.
60. Paech K., Webb P., Kuiper G. G., Nilsson S., Gustafsson J., Kushner P. J. and Scanlan T. S. (1997) Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 277, 1508-1510.
61. Papanikolaou N. A. and Sabban E. L. (1999) Sp1/Egr1 motif: a new candidate in the regulation of rat tyrosine hydroxylase gene transcription by immobilization stress. J. Neurochem. 73, 433-436.
62. Pasqualini C., Leviel V., Guibert B., Faucon-Biguet N. and Kerdelhui B. (1991) Inhibitory action of acute estradiol treatment on the activity and quantity of tyrosine hydroxylase in the median eminence of ovariectomized rats. J. Neuroendocrinol. 3, 575-580.
63. Pau K. Y., Hess D. L., Kohama S., Bao J., Pau C. Y. and Spies H. G. (2000) Oestrogen upregulates noradrenaline release in the medio-basal hypothalamus and tyrosine hydroxylase gene expression in the brainstem of ovariectomized rhesus macaques. J. Neuroendocrinol. 12, 899-909.
64. Pettersson K., Delaunay F. and Gustafsson J. A. (2000) Estrogen receptor beta acts as a dominant regulator of estrogen signaling. Oncogene 19, 4970-4978.
65. Pfaff D., Frohlich J. and Morgan M. (2002) Hormonal and genetic influences on arousal - sexual and otherwise. Trends Neurosci. 25, 45-50.
66. Pfaffl M. W., Lange I. G., Daxenberger A. and Meyer H. H. (2001) Tissue-specific expression pattern of estrogen receptors (ER): quantification of ER alpha and ER beta mRNA with real-time RT-PCR. APMIS 109, 345-355.
67. Piech-Dumas K. M. and Tank A. W. (1999) CREB mediates the cAMP-responsiveness of the tyrosine hydroxylase gene: use of an antisense RNA strategy to produce CREB-deficient PC12 cell lines. Brain Res. Mol. Brain Res. 70, 219-230.
68. Porter W., Saville B., Hoivik D. and Safe S. (1997) Functional synergy between the transcription factor Sp1 and the estrogen receptor. Mol. Endocrinol. 11, 1569-1580.
69. Quandt K., Frech K., Karas H., Wingender E. and Werner T. (1995) Matlnd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucl. Acids Res. 23, 4878-4884.
70. Rowan B. G., Garrison N., Weigel N. L. and O'Malley B. W. (2000) 8-Bromo-cyclic AMP induces phosphorylation of two sites in SRC-1 that facilitate ligand-independent activation of the chicken progesterone receptor and are critical for functional cooperation between SRC-1 and CREB binding protein. Mol. Cell Biol. 20, 8720-8730.
71. Sabbah M., Courilleau D., Mester J. and Redeuilh G. (1999) Estrogen induction of the cyclin D1 promoter: involvement of a cAMP response-like element. Proc. Natl Acad. Sci. USA 96, 11217-11222.
72. Sabban E. L. (1997) Control of tyrosine hydroxylase gene expression in chromaffin and PC12 cells. Semin. Cell Dev. Biol. 8, 101-111.
73. Safe S. (2001) Transcriptional activation of genes by 17 beta-estradiol through estrogen receptor-Sp1 interactions. Vitam. Horm. 62, 231-252.
74. Saville B., Wormke M., Wang F., Nguyen T., Enmark E., Kuiper G., Gustafsson J. A. and Safe S. (2000) Ligand-, cell-, and estrogen receptor subtype (alpha/beta)-dependent activation at GC-rich (Sp1) promoter elements. J. Biol. Chem. 275, 5379-5387.
75. Serova L. and Sabban E. L. (2002) Involvement of alpha 7 nicotinic acetylcholine receptors in gene expression of dopamine biosynthetic enzymes in rat brain. J. Pharmacol. Exp. Ther. 303, 896-903.
76. Serova L. I. and Sabban E. L. (2004) Estrogen triggered alterations in GTP cyclohydrolase I and tyrosine hydrolase gene expression in the nucleus of solitary tract, in Pterins, Folates, and Neurotransmitters in Molecular Medicine (Blau N. and Thony B., eds), pp. 78-82. SPS-Verlagsgesellschaft, Heilbronn.
77. Serova L., Rivkin M., Nakashima A. and Sabban E. L. (2002) Estradiol stimulates gene expression of norepinephrine biosynthetic enzymes in rat locus coeruleus. Neuroendocrinology 75, 193-200.
78. Serova L. I., Maharjan S., Huang A., Sun D., Kaley G. and Sabban E. L. (2004) Response of tyrosine hydroxylase and GTP cyclohydrolase I gene expression to estrogen in brain catecholaminergic regions varies with mode of administration. Brain Res. 1015, 1-8.
79. Shughrue P. J., Lane M. V. and Merchenthaler I. (1997) Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 388, 507-525.
80. Smith L. H., Coats S. R., Qin H., Petrie M. S., Covington J. W., Su M., Eren M. and Vaughan D. E. (2004) Differential and opposing regulation of PAI-I promoter activity by estrogen receptor alpha and estrogen receptor beta in endothelial cells. Circ. Res. 95, 269-275.
81. Socorro S., Power D. M., Olsson P. E. and Canario A. V. (2000) Two estrogen receptors expressed in the teleost fish, Sparus aurata: cDNA cloning, characterization and tissue distribution. J. Endocrinol. 166, 293-306.
82. Thanky N. R., Son J. H. and Herbison A. E. (2002) Sex differences in the regulation of tyrosine hydroxylase gene transcription by estrogen in the locus coeruleus of TH9-LacZ. transgenic mice. Brain Res. Mol. Brain Res. 104, 220-226.
83. Tinti C., Conti B., Cubells J. F., Kim K. S., Baker H. and Joh T. H. (1996) Inducible cAMP early repressor can modulate tyrosine hydroxylase gene expression after stimulation of cAMP synthesis. J. Biol. Chem. 271, 25375-25381.
84. Tora L., White J., Brou C., Tasset D., Webster N., Scheer E. and Chambon P. (1989) The human estrogen receptor has two independent non-acidic transcriptional activation functions. Cell 59, 477-487.
85. Tseng J. Y., Kolb P. E., Raskind M. A. and Miller M. A. (1997) Estrogen regulates galanin but not tyrosine hydroxylase gene expression in the rat locus ceruleus. Brain Res. Mol. Brain Res. 50, 100-106.
86. Webb P., Lopez G. N., Uht R. M. and Kushner P. J. (1995) Tamoxifen activation of the estrogen receptor/AP-1 pathway: potential origin for the cell-specific estrogen-like effects of antiestrogens. Mol. Endocrinol. 9, 443-456.
87. Webb P., Nguyen P., Valentine C., Lopez G. N., Kwok G. R., McInerney E., Katzenellenbogen B. S., Enmark E., Gustafsson J. A., Nilsson S. and Kushner P. J. (1999) The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirements for receptor transactivation functions. Mol. Endocrinol. 13, 1672-1685.