Local modulation of steroid action: Rapid control of enzymatic activity

Frontiers in Neuroscience

Volumn 9, Issue FEB, 2015, Pages

  Charlier, Thierry D ^a,b   Cornil, Charlotte A ^c   Patte Mensah, Christine ^d   Meyer, Laurence ^d   Mensah Nyagan, A Guy ^d   Balthazart, Jacques ^c  

^a OHIO UNIVERSITY   (United States)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

17 estradiol; Aromatase; Catechol estrogens; Hypothalamus; Neurosteroidogenesis; Phosphorylation

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; AROMATASE; CATECHOL ESTROGEN; DOPAMINE; ESTRADIOL; ESTROGEN; GLUTAMIC ACID; OXYGENASE; STEROID; TESTOSTERONE;

ARTICLE; CATABOLISM; COTURNIX JAPONICA; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HOMOGENATE; HUMAN; HYPOTHALAMUS; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; STEROID HYDROXYLATION;

EID: 84924350652     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00083     Document Type: Article

References (91)

1. Abraham, I. M., M. G. Todman, K. S. Korach, and A. E. Herbison. 2004. "Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain." Endocrinology 145 (7):3055-3061.
2. Abraham, I.M., S-K. Han, M.G. Todman, K.S. Korach, and A.E. Herbison. 2003. "Estrogen receptor Beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo." Journal of Neuroscience 23 (13):5771-5777.
3. Absil, P., M. Baillien, G. F. Ball, G. C. Panzica, and J. Balthazart. 2001. "The control of preoptic aromatase activity by afferent inputs in Japanese quail." Brain Res Brain Res Rev 37 (1-3):38-58.
4. Albert, K.A., E. Helmer-Matyjek, A.A. Nairn, T.H. Müller, J.W. Haycock, L.A. Greene, M. Goldstein, and P. Greengard. 1984. "Calcium/phospholipid-dependent protein kinase (protein kinase C) phosphorylates and activates tyrosine hydroxylase." Proc. Natl. Acad. Sci. USA 81:7713-7717.
5. Almadhidi, J., S. Moslemi, M. A. Drosdowsky, and G. E. Seralini. 1996. "Equine cytochrome P450 aromatase exhibits an estrogen 2-hydroxylase activity in vitro." J Steroid Biochem Mol Biol 59 (1):55-61.
6. Bagatell, C. J., K. D. Dahl, and W. J. Bremner. 1994. "The direct pituitary effect of testosterone to inhibit gonadotropin secretion in men is partially mediated by aromatization to estradiol." J Androl 15 (1):15-21.
7. Baillien, M., and J. Balthazart. 1997. "A direct dopaminergic control of aromatase activity in the quail preoptic area." J Steroid Biochem Mol Biol 63 (1-3):99-113.
8. Balthazart, J, M Baillien, and GF Ball. 2001a. "Phosphorylation processes mediate rapid changes of brain aromatase activity." J. Steroid Bioch. Molec. Biol. 79:261-277.
9. Balthazart, J., M. Baillien, and G. F. Ball. 2002. "Interactions between aromatase (estrogen synthase) and dopamine in the control of male sexual behavior in quail." Comp Biochem Physiol B Biochem Mol Biol 132 (1):37-55.
10. Balthazart, J., M. Baillien, and G. F. Ball. 2005. "Interactions between kinases and phosphatases in the rapid control of brain aromatase." J Neuroendocrinol 17 (9):553-559.
11. Balthazart, J., M. Baillien, and G. F. Ball. 2006. "Rapid control of brain aromatase activity by glutamatergic inputs." Endocrinology 147:359-366.
12. Balthazart, J., M. Baillien, and G.F. Ball. 2001b. "Rapid and reversible inhibition of brain aromatase activity." J. Neuroendocrinol. 13:61-71.
13. Balthazart, J., M. Baillien, T. D. Charlier, and G. F. Ball. 2003. "Calcium-dependent phosphorylation processes control brain aromatase in quail." Eur J Neurosci 17 (8):1591-606.
14. Balthazart, J., and G. F. Ball. 2006. "Is brain estradiol a hormone or a neurotransmitter." TINS 29:241-249.
15. Balthazart, J., A. Foidart, M. Baillien, N. Harada, and G. F. Ball. 1998. "Anatomical relationships between aromatase and tyrosine hydroxylase in the quail brain: double-label immunocytochemical studies." J Comp Neurol 391 (2):214-226.
16. Balthazart, J., R. Stoop, A. Foidart, J. C. Granneman, and J. G. Lambert. 1994. "Distribution and regulation of estrogen-2-hydroxylase in the quail brain." Brain Res Bull 35:339-45.
17. Barone, I., Giordano C., Malivindi R., Lanzino M., Rizza P., Casaburi I., Bonofiglio D., Catalano S., Andò S. (2012) "Estrogens and PTP1B function in a novel pathway to regulate aromatase enzymatic activity in breast cancer cells". Endocrinology 153 :5157-66
18. Beyer, C., G. Morali, F. Naftolin, K. Larsson, and G. Perez-Palacios. 1976. "Effect of some antiestrogens and aromatase inhibitors on androgen induced sexual behavior in castrated male rats." Hormones and Behavior 7:353-363.
19. Black, M. P., J. Balthazart, M. Baillien, and M. S. Grober. 2005. "Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex-changing fish, Lythrypnus dalli." Proc Biol Sci 272 (1579):2435-40.
20. Black, M. P., J. Balthazart, M. Baillien, and M. S. Grober. 2011. "Rapid increase in aggressive behavior precedes the decrease in brain aromatase activity during socially mediated sex change in Lythrypnus dalli." Gen Comp Endocrinol 170 (1):119-24.
21. Boulware, M. I., J. P. Weick, B. R. Becklund, S. P. Kuo, R. D. Groth, and P. G. Mermelstein. 2005. "Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein." J Neurosci 25 (20):5066-5078.
22. Catalano, S., I. Barone, C. Giordano, P. Rizza, H. Qi, G. Gu, R. Malivindi, D. Bonofiglio, and S. Ando. 2009. "Rapid estradiol/ERalpha signaling enhances aromatase enzymatic activity in breast cancer cells." Mol Endocrinol 23 (10):1634-1645.
23. Catalano, S., Barone, I., Andò, S. (2014) "Rapid estrogen effects on aromatase phosphorylation in breast cancer cells" Methods Mol Biol. 1204:155-63.
24. Charlier, T. D., N. Harada, J. Balthazart, and C. A. Cornil. 2011. "Human and Quail Aromatase Activity Is Rapidly and Reversibly Inhibited by Phosphorylating Conditions." Endocrinology 152(11):4199-210
25. Chen, B. S., and K. W. Roche. 2007. "Regulation of NMDA receptors by phosphorylation." Neuropharmacology 53 (3):362-368.
26. Cornil, C. A., G. F. Ball, and J. Balthazart. 2006. "Functional significance of the rapid regulation of brain estrogen action: Where do the estrogens come from?" Brain Res 1126:2-26.
27. Cornil, C. A., G. F. Ball, and J. Balthazart. 2012. "Rapid control of male typical behaviors by brain-derived estrogens." Front Neuroendocrinol 33 (4):425-46.
28. Cornil, C. A., C. Dalla, Z. Papadopoulou-Daifoti, M. Baillien, C. Dejace, G. F. Ball, and J. Balthazart. 2005. "Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior." Endocrinology 1416:2809-2820.
29. Cornil, C. A., C. H. Leung, E. R. Pletcher, K. C. Naranjo, S. J. Blauman, and C. J. Saldanha. 2012. "Acute and specific modulation of presynaptic aromatization in the vertebrate brain." Endocrinology 153 (6):2562-2567.
30. Cornil, C. A., V. Seutin, P. Motte, and J. Balthazart. 2004. "Electrophysiological and neurochemical characterization of neurons of the medial preoptic area in Japanese quail (Coturnix japonica)." Brain Res 1029 (2):224-240.
31. Cornil, C. A., M. Taziaux, M. Baillien, G. F. Ball, and J. Balthazart. 2005. "Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail." Horm Behav 49:45-67.
32. Cornil, CA, A Foidart, A Minet, and J Balthazart. 2000. "Immunocytochemical localization of ionotropic glutamate receptors subunits in the adult quail forebrain." J Comp Neurol 428:577-608.
33. Daubner, S. C., C. Lauriano, J. W. Haycock, and P. F. Fitzpatrick. 1992. "Site-directed mutagenesis of serine 40 of rat tyrosine hydroxylase. Effects of dopamine and cAMPdependent phosphorylation on enzyme activity." J Biol Chem 267 (18):12639-12646.
34. Dewing, P., M. I. Boulware, K. Sinchak, A. Christensen, P. G. Mermelstein, and P. Micevych. 2007. "Membrane estrogen receptor-alpha interactions with metabotropic glutamate receptor 1a modulate female sexual receptivity in rats." J Neurosci 27 (35):9294-9300.
35. Dickens, M. J., C. A. Cornil, and J. Balthazart. 2011. "Acute Stress Differentially Affects Aromatase Activity in Specific Brain Nuclei of Adult Male and Female Quail." Endocrinology. 152(11):4242-4251.
36. Dickens, M. J., C. A. Cornil, and J. Balthazart. 2013. "Neurochemical control of rapid stressinduced changes in brain aromatase activity." J Neuroendocrinol 25 (4):329-339.
37. Diotel, N., Le Page, Y., Mouriec, K., Tong, S.K., Pellegrini, E., Vaillant, C., Anglade, I., Brion F., Pakdel, F., Chung, B.C., Kah, O. (2010) "Aromatase in the brain of teleost fish: expression, regulation and putative functions". Front Neuroendocrinol 31(2):172-92
38. Fisher, C.R., K.H. Graves, A.F. Parlow, and E.V. Simpson. 1998. "Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of cyp19 gene." PNAS 95:6965-6970.
39. Foidart, A., N. Harada, and J. Balthazart. 1995. "Aromatase-immunoreactive cells are present in mouse brain areas that are known to express high levels of aromatase activity." Cell Tissue Res. 280:561-574.
40. Foidart, A., J. Reid, P. Absil, N. Yoshimura, N. Harada, and J. Balthazart. 1995. "Critical reexamination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme." J Chem Neuroanat 8:267-282.
41. Forlano, P. M., B. A. Schlinger, and A. H. Bass. 2006. "Brain aromatase: new lessons from nonmammalian model systems." Front Neuroendocrinol 27 (3):247-274.
42. Forlano, P.M., D.L. Deitcher, D.A. Myers, and A.H. Bass. 2001. "Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as a source." J. Neurosci. 21:8943-8955.
43. Fusani, L., J.B. Hutchison, and M. Gahr. 2001. "Testosterone regulates the activity and expression of aromatase in the canary neostriatum." J. Neurobiol. 49:1-8.
44. Hayashi, T., and N. Harada. 2014. "Post-translational dual regulation of cytochrome P450 aromatase at the catalytic and protein levels by phosphorylation/dephosphorylation." FEBS J 281 (21):4830-40.
45. Hayden-Hixson, D. M., and C. F. Ferris. 1991. "Steroid-specific regulation of agonistic responding in the anterior hypothalamus of male hamsters." Physiol Behav 50 (4):793-799.
46. Honda, S., N. Harada, S. Ito, Y. Takagi, and S. Maeda. 1998. "Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp 19 gene." Biochem. Biophys. Res. Comm. 252:445-449.
47. Hong, Y., H. Li, Y. C. Yuan, and S. Chen. 2009. "Sequence-function correlation of aromatase and its interaction with reductase." J Steroid Biochem Mol Biol. 118(4-5):203-206
48. Joels, M. 1997. "Steroid hormones and excitability in the mammalian brain." Front Neuroendocrinol 18 (1):2-48.
49. Johnson, A.L., and A. van Tienhoven. 1981. "Pharmacokinetics of estradiol-17 beta in the laying hen." J. Endocrinol 60:2720-2723.
50. Kenealy, B. P., K. L. Keen, O. K. Ronnekleiv, and E. Terasawa. 2011. "STX, a novel nonsteroidal estrogenic compound, induces rapid action in primate GnRH neuronal calcium dynamics and peptide release." Endocrinology 152 (8):3182-3191. 10.1210/en.2011-0097.
51. Konkle, A. T., and J. Balthazart. 2011. "Sex Differences in the Rapid Control of Aromatase Activity in the Quail Preoptic Area." J Neuroendocrinol 23 (5):424-434.
52. Lord, L.D., J. Bond, and R.R. Thompson. 2009. "Rapid steroid influences on visually guided sexual behavior in mal goldfish." Horm Behav 56(5):519-26.
53. MacLusky, N.J., and F. Naftolin. 1981. "Sexual differentiation of the central nervous system." Science 211 (4488):1294-1303.
54. Mermelstein, P. G., J. B. Becker, and D. J. Surmeier. 1996. "Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor." J Neurosci 16 (2):595-604.
55. Metzdorf, R., M. Gahr, and L. Fusani. 1999. "Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds." J. Comp. Neurol. 407:115-129.
56. Micevych, P.E., and P.G. Mermelstein. 2008. "Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in the brain." Mol Neurobiol 38:66-77.
57. Miller, T. W., I. Shin, N. Kagawa, D. B. Evans, M. R. Waterman, and C. L. Arteaga. 2008. "Aromatase is phosphorylated in situ at serine-118." J Steroid Biochem Mol Biol 112 (1-3):95-101
58. Miller, W. L. 2005. "Minireview: regulation of steroidogenesis by electron transfer." Endocrinology 146 (6):2544-2550.
59. Moss, R. L., Q. Gu, and M. Wong. 1997. "Estrogen: nontranscriptional signaling pathway." Recent Prog Horm Res 52:33-68; discussion 68-9.
60. Onagbesan, O. M., and M. J. Peddie. 1989. "Calcium-dependent stimulation of estrogen secretion by FSH from theca cells of the domestic hen (Gallus domesticus)." Gen Comp Endocrinol 75 (2):177-86.
61. Osawa, Y., T. Higashiyama, Y. Shimizu, and C. Yarborough. 1993. "Multiple functions of aromatase and the active site structure; aromatase is the placental estrogen 2-hydroxylase." J Steroid Biochem Mol Biol 44 (4-6):469-80.
62. Remage-Healey, L., and A. H. Bass. 2004. "Rapid, hierarchical modulation of vocal patterning by steroid hormones." J Neurosci 24 (26):5892-5900.
63. Remage-Healey, L., M. J. Coleman, R. K. Oyama, and B. A. Schlinger. 2010. "Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird." Proc Natl Acad Sci U S A 107 (8):3852-3857.
64. Remage-Healey, L., S. Dong, N. T. Maidment, and B. A. Schlinger. 2011. "Presynaptic control of rapid estrogen fluctuations in the songbird auditory forebrain." J Neurosci 31 (27):10034-8.
65. Remage-Healey, L., N. T. Maidment, and B. A. Schlinger. 2008. "Forebrain steroid levels fluctuate rapidly during social interactions." Nat Neurosci 11 (11):1327-34.
66. Remage-Healey, L., R. K. Oyama, and B. A. Schlinger. 2009. "Elevated aromatase activity in forebrain synaptic terminals during song." J Neuroendocrinol 21 (3):191-199.
67. Rochira, V., L. Zirilli, A. D. Genazzani, A. Balestrieri, C. Aranda, B. Fabre, P. Antunez, C. Diazzi, C. Carani, and L. Maffei. 2006. "Hypothalamic-pituitary-gonadal axis in two men with aromatase deficiency: evidence that circulating estrogens are required at the hypothalamic level for the integrity of gonadotropin negative feedback." Eur J Endocrinol 155 (4):513-22.
68. Roepke, T. A., O. K. Ronnekleiv, and M. J. Kelly. 2005. "Physiological consequences of membrane-initiated estrogen signaling in the brain." Front Biosci 16:1560-1573.
69. Rønnekleiv, O. K., and M. J. Kelly. 2002. "Rapid membrane effects of estrogen in the central nervous system." In Hormones, brain and Behavior, edited by D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach and R. T. Rubin, 361-380. Elseviier Science.
70. Roselli, C. E., L. E. Horton, and J. A. Resko. 1985. "Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system." Endocrinology 117:2471-2477.
71. Roselli, C. E., and J. A. Resko. 1984. "Androgens regulate brain aromatase activity in adult male through a receptor mechanism." Endocrinology 114:2183-2189.
72. Roselli, C. E., and J. A. Resko. 1989. "Testosterone regulates aromatase activity in discrete brain areas of male rhesus macaques." Biol Reprod 40:929-934.
73. Roselli, CE, and JA Resko. 2001. "Cytochrome P450 aromatase (CYP19) in the non-human primate brain: distribution, regulation, and functional significance." J. Steroid Bioch. Molec. Biol. 79:247-253.
74. Saldanha, C.J., M.J. Tuerk, Y.H. Kim, A.O. Fernandes, A.P. Arnold, and B.A. Schlinger. 2000. "Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody." J. Comp. Neurol. 423:619-630.
75. Schumacher, M., and J. Balthazart. 1986. "Testosterone-induced brain aromatase is sexually dimorphic." Brain Res. 370:285-293.
76. Seredynski, A. L., J. Balthazart, V. J. Christophe, G. F. Ball, and C. A. Cornil. 2013. "Neuroestrogens rapidly regulate sexual motivation but not performance." J Neurosci 33 (1):164-74.
77. Shen, P., B.A. Schlinger, A.T. Campagnoni, and A.P. Arnold. 1995. "An atlas of aromatase mRNA expression in the zebra finch brain." J. Comp. Neurol. 360:172-184.
78. Steimer, T., and J.B. Hutchison. 1991. "Micromethods for the in vitro study of steroid metabolism in the brain using radiolabelled tracers." In Neuroendocrine research methods, Vol 2, edited by B. Greenstein, 875-919-0. Chur, Switzerland: Harwood Academic Publishers.
79. Taziaux, M., M. Keller, J. Bakker, and J. Balthazart. 2007. "Sexual behavior activity tracks rapid changes in brain estrogen concentrations." The Journal of Neuroscience 27 (24):6563-6572.
80. Thompson, E. A., Jr., and P. K. Siiteri. 1974. "Utilization of oxygen and reduced nicotinamide adenine dinucleotide phosphate by human placental microsomes during aromatization of androstenedione." J Biol Chem 249 (17):5364-5372.
81. Toda, K., T. Saibara, T. Okada, S. Onishi, and Y. Shizuta. 2001. "A loss of aggressive behaviour and its reinstatement by oestrogen in mice lacking the aromatase gene (Cyp19)." J Endocrinol 168 (2):217-20.
82. Trainor, B. C., M. S. Finy, and R. J. Nelson. 2008. "Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice." Horm Behav 53:192-199.
83. Trainor, B. C., S. Lin, M. S. Finy, M. R. Rowland, and R. J. Nelson. 2007. "Photoperiod reverses the effects of estrogens on male aggression via genomic and nongenomic pathways." Proc Natl Acad Sci U S A 104 (23):9840-5.
84. Trainor, B.C., H. H. Kyomen, and C.A. Marler. 2006. "Estrogenic encounters: how interaction between aromatase and the environment modulate agression." Front Neuroendocrinol 27:170-179.
85. Tremere, L. A., J. K. Jeong, and R. Pinaud. 2009. "Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression." J Neurosci 29 (18):5949-5963.
86. Tsang, C. P., and A. A. Grunder. 1984. "Production, clearance rates and metabolic fate of estradiol- 17 beta in the plasma of the laying hen." Steroids 43 (1):71-84.
87. Wade, C. B., and D. M. Dorsa. 2003. "Estrogen activation of cyclic adenosine 5'-monophosphate response element-mediated transcription requires the extracellularly regulated kinase/mitogen-activated protein kinase pathway." Endocrinology 144 (3):832-838.
88. Wagner, C.K., and J.I. Morrell. 1997. "Neuroanatomical distribution of aromatase mRNA in the rat brain: indications of regional regulation." J. Steroid Biochem. Mol. Biol. 61:307-314.
89. Watters, J. J., J. S. Campbell, M. J. Cunningham, E. G. Krebs, and D. M. Dorsa. 1997. "Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription." Endocrinology 138 (9):4030-4033.
90. Whirl-Carrillo, M., E. M. McDonagh, J. M. Hebert, L. Gong, K. Sangkuhl, C. F. Thorn, R. B. Altman, and T. E. Klein. 2012. "Pharmacogenomics knowledge for personalized medicine." Clin Pharmacol Ther 92 (4):414-417.
91. Wu, T. W., J. M. Wang, S. Chen, and R. D. Brinton. 2005. "17Beta-estradiol induced Ca2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection." Neuroscience 135 (1):59-72.