Abstract
Adverse factors of early development can produce long-lasting alterations of the brain neurochemical systems, the physiological functions and behavior. Tyrosine hydroxylase (TH), the key enzyme of catecholamine biosynthesis, determines the activity of the neurochemical system and is induced by stress hormones, glucocorticoids, in vitro and in vivo. Analysis of our own data and the data in the literature concerning the effect of stress hormones, glucocorticoids, in the critical periods of perinatal development on the TH gene expression, the level of the protein and the enzyme activity, as well as consideration of the possible mechanisms of these effects, was the purpose of the review. Administration of dexamethasone or hydrocortisone increases the level of TH mRNA in the brainstem of 20-day-old fetuses and 3-day-old rats in 6 hours; it is accompanied by an increase in the enzyme activity and immunohistochemical detection of the TH protein in the brainstem. A change in the TH gene expression in the critical period of early development leads to an increase in the level of TH mRNA in the brainstem of 25- and 70-day-old rats and the enzyme activity in the brainstem and cerebral cortex of adult animals. The period of TH sensitivity to the glucocorticoid level is agedependent. Administration of hormones on the 8th day of the life is not accompanied by changes in the TH mRNA level and the enzyme activity. The promoter of the TH gene does not have a classical functionally active hormone-dependent element. The mechanism of hormonal induction of the TH expression may be based on the noncanonical pathway of the glucocorticoids as a result of the known protein–protein interaction of the glucocorticoid receptor with other transcription factors, such as proteins of the AP-1 complex. This mechanism in the regulation of the TH expression by dexamethasone was found in the pheochromocytoma cell line. The existence of such mechanism in vivo needs to be explored in futher studies.
Similar content being viewed by others
References
Altmann, C.R. and Brivanlou, A.H., Neural patterning in the vertebrate embryo, Int. Rev. Cytol., 2001, vol. 203, pp. 447–482.
Bademci, G., Vance, J.M., and Wang, L., Tyrosine hydroxylase gene: Another piece of the genetic puzzle of Parkinson’s disease, CNS Neurol. Disord. Drug Targets, 2012, vol. 11, no. 4, pp. 469–481.
Barker, D.J., Fetal origins of coronary heart disease, BMJ, 1995, vol. 311, no. 6998, pp. 171–174.
Barth, K.A., Kishimoto, Y., Rohr, K.B., Seydler, C., Schulte-Merker, S., and Wilson, S.W., Bmp activity establishes a gradient of positional information throughout the entire neural plate, Development, 1999, vol. 126, no. 22, pp. 4977–4987.
Beck, I.M., Vanden Berghe W., Vermeulen, L., Yamamoto, K.R., Haegeman, G., and De Bosscher, K., Crosstalk in inflammation: The interplay of glucocorticoid receptor-based mechanisms and kinases and phosphatases, Endocr. Rev., 2009, vol. 30, no. 7, pp. 830–882.
Bingham, B.C., Sheela Rani C.S., Frazer, A., Strong, R., and Morilak, D.A., Exogenous prenatal corticosterone exposure mimics the effects of prenatal stress on adult brain stress response systems and fear extinction behavior, Psychoneuroendocrinology, 2013, vol. 38, no. 11, pp. 2746–2757. doi 10.1016/j.psyneuen.2013.07.003
Bonnin, A., de Miguel, R., Rodriguez-Manzaneque, J.C., Fernandez-Ruiz, J.J., Santos, A., and Ramos, J.A., Changes in tyrosine hydroxylase gene expression in mesencephalic catecholaminergic neurons of immature and adult male rats perinatally exposed to cannabinoids, Brain Res. Develop. Brain Res., 1994, vol. 81, no. 1, pp. 147–150.
Bornstein, S.R., Tian, H., Haidan, A., Böttner, A., Hiroi, N., Eisenhofer, G., McCann, S.M., Chrousos, G.P., and Roffler-Tarlov, S., Deletion of tyrosine hydroxylase gene reveals functional interdependence of adrenocortical and chromaffin cell system in vivo, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, no. 26, pp. 14742–14747. doi 10.1073/pnas.97.26.14742
Boschi, N.M., Takeuchi, K., Sterling, C., and Tank, A.W., Differential expression of polycytosine-binding protein isoforms in adrenal gland, locus coeruleus and midbrain, Neuroscience, 2015, vol. 286, pp. 1–12. doi 10.1016/j.neuroscience.2014.11.038
Candy, J. and Collet, C., Two tyrosine hydroxylase genes in teleosts, Biochim. Biophys. Acta, 2005, vol. 1727, no. 1, pp. 35–44.
Carson, R.P. and Robertson, D., Genetic manipulation of noradrenergic neurons, J. Pharmacol. Exp. Ther., 2002, vol. 301, no. 2, pp. 410–417.
Champagne, D.L., de Kloet, E.R., and Joels, M., Fundamental aspects of the impact of glucocorticoids on the (immature) brain, Semin. Fetal Neonatal Med., 2009, vol. 14, no. 3, pp. 136–142. doi 10.1016/j.siny.2008.11.006
Craig, S.P., Buckle, V.J., Lamouroux, A., Mallet, J., and Craig, I., Localization of the human tyrosine hydroxylase gene to 11p15: Gene duplication and evolution of metabolic pathways, Cytogenet. Cell Genet., 1986, vol. 42, nos. 1/2, pp. 29–32.
Dent, G.W., Smith, M.A., and Levine, S., Stress-induced alterations in locus coeruleus gene expression during ontogeny, Brain Res. Develop. Brain Res., 2001, vol. 127, no. 1, pp. 23–30.
Diamond, M.I., Miner, J.N., Yoshinaga, S.K., and Yamamoto, K.R., Transcription factor interactions: Selectors of positive or negative regulation from a single DNA element, Science, 1990, vol. 249, no. 4974, pp. 1266–1272.
Dunkley, P.R., Bobrovskaya, L., Graham, M.E., von Nagy-Felsobuki, E.I., and Dickson, P.W., Tyrosine hydroxylase phosphorylation: Regulation and consequences, J. Neurochem., 2004, vol. 91, no. 5, pp. 1025–1043.
Dygalo, N.N. and Kalinina, T.S., Effects of the interaction of genotype and glucocorticoids on brain tyrosine hydroxylase activity in rat fetuses, Genetika, 1993, vol. 29, no. 9, pp. 1453–1459.
Dygalo, N.N., Kalinina, T.S., and Shishkina, G.T., Neonatal programming of rat behavior by downregulation of alpha2Aadrenoreceptor gene expression in the brain, Ann. N.Y.: Acad. Sci., 2008, vol. 1148, pp. 409–414. doi 10.1196/annals.1410.063
Fossom, L.H., Sterling, C.R., and Tank, A.W., Regulation of tyrosine hydroxylase gene transcription rate and tyrosine hydroxylase mRNA stability by cyclic amp and glucocorticoid, Mol. Pharmacol., 1992, vol. 42, no. 5, pp. 898–908.
Friggi-Grelin, F., Coulom, H., Meller, M., Gomez, D., Hirsh, J., and Birman, S., Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase, J. Neurobiol., 2003, vol. 54, no. 4, pp. 618–627. doi 10.1002/neu.10185
Fujinaga, M. and Scott, J.C., Gene expression of catecholamine synthesizing enzymes and beta adrenoceptor subtypes during rat embryogenesis, Neurosci. Lett., 1997, vol. 231, no. 2, pp. 108–112.
Fung, B.P., Yoon, S.O., and Chikaraishi, D.M., Sequences that direct rat tyrosine-hydroxylase gene-expression, J. Neurochem., 1992, vol. 58, no. 6, pp. 2044–2052.
Gallo, L.A., Tran, M., Moritz, K.M., and Wlodek, M.E., Developmental programming: Variations in early growth and adult disease, Clin. Exp. Pharmacol. Physiol., 2013, vol. 40, no. 11, pp. 795–802. doi 10.1111/1440-1681.12092
Goridis, C. and Rohrer, H., Specification of catecholaminergic and serotonergic neurons, Nat. Rev. Neurosci., 2002, vol. 3, no. 7, pp. 531–541. doi 10.1038/nrn871
Groeneweg, F.L., Karst, H., de Kloet, E.R., and Joels, M., Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling, Mol. Cell. Endocrinol., 2012, vol. 350, no. 2, pp. 299–309. doi 10.1016/j.mce.2011.06.020
Guo, S., Brush, J., Teraoka, H., Goddard, A., Wilson, S.W., Mullins, M.C., and Rosenthal, A., Development of noradrenergic neurons in the zebrafish hindbrain requires BMP, FGF8, and the homeodomain protein Soulless/Phox2a, Neuron, 1999, vol. 24, no. 3, pp. 555–566.
Hagerty, T., Morgan, W.W., Elango, N., and Strong, R., Identification of a glucocorticoid-responsive element in the promoter region of the mouse tyrosine hydroxylase gene, J. Neurochem., 2001, vol. 76, no. 3, pp. 825–834.
Harris, A. and Seckl, J., Glucocorticoids, prenatal stress and the programming of disease, Horm. Behav., 2011, vol. 59, no. 3, pp. 279–289. doi 10.1016/j.yhbeh.2010.06.007
Haycock, J.W., Species differences in the expression of multiple tyrosine hydroxylase protein isoforms, J. Neurochem., 2002, vol. 81, no. 5, pp. 947–953.
Hebert, M.A., Serova, L.I., and Sabban, E.L., Single and repeated immobilization stress differentially trigger induction and phosphorylation of several transcription factors and mitogen-activated protein kinases in the rat locus coeruleus, J. Neurochem., 2005, vol. 95, no. 2, pp. 484–498.
Herlenius, E. and Lagercrantz, H., Development of neurotransmitter systems during critical periods, Exp. Neurol., 2004, vol. 190, pp. 8–21. doi 10.1016/j.expneurol.2004.03.027
Hernandez-Sanchez, C., Bartulos, O., Valenciano, A.I., Mansilla, A., and de Pablo, F., The regulated expression of chimeric tyrosine hydroxylaseinsulin transcripts during early development, Nucl. Acids, 2006, vol. 34, no. 12, pp. 3455–3464.
Hippenmeyer, S., Kramer, I., and Arber, S., Control of neuronal phenotype: What targets tell the cell bodies, Trends Neurosci., 2004, vol. 27, no. 8, pp. 482–488. doi 10.1016/j.tins.2004.05.012
Hirsch, M.R., Tiveron, M.C., Guillemot, F., Brunet, J.F., and Goridis, C., Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system, Development, 1998, vol. 125, no. 4, pp. 599–608.
Holm, P.C., Rodriguez, F.J., Kele, J., Castelo-Branco, G., Kitajewski, J., and Arenas, E., BMPs, FGF8 and Wnts regulate the differentiation of locus coeruleus noradrenergic neuronal precursors, J. Neurochem., 2006, vol. 99, no. 1, pp. 343–352. doi 10.1111/j.1471-4159.2006.04039.x
Kalinina, T.S. and Dygalo, N.N., Development of the brain noradrenergic system in rats after prenatal exposure to corticosterone, Izv. Akad. Nauk, Ser. Biol., 2013, vol. 4, pp. 447–452.
Kalinina, T.S., Shishkina, G.T., and Dygalo, N.N., Induction of tyrosine hydroxylase gene expression by glucocorticoids in the perinatal rat brain is age-dependent, Neurochem. Res, 2012, vol. 37, no. 4, pp. 811–818.
Kapoor, A., Petropoulos, S., and Matthews, S.G., Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids, Brain Res. Rev., 2008, vol. 57, no. 2, pp. 586–595. doi 10.1016/j.brainresrev.2007.06.013
Kassel, O. and Herrlich, P., Crosstalk between the glucocorticoid receptor and other transcription factors: Molecular aspects, Mol. Cell. Endocrinol., 2007, vol. 275, nos. 1–2, pp. 13–29.
Kobayashi, K., Morita, S., Sawada, H., Mizuguchi, T., Yamada, K., Nagatsu, I., Hata, T., Watanabe, Y., Fujita, K., and Nagatsu, T., Targeted disruption of the tyrosinehydroxylase locus results in severe catecholamine depletion and perinatal lethality in mice, J. Biol. Chem., 1995, vol. 270, no. 45, pp. 27235–27243.
Kreider, M.L., Tate, C.A., Cousins, M.M., Oliver, C.A., Seidler, F.J., and Slotkin, T.A., Lasting effects of developmental dexamethasone treatment on neural cell number and size, synaptic activity, and cell signaling: critical periods of vulnerability, dose-effect relationships, regional targets, and sex selectivity, Neuropsychopharmacology, 2006, vol. 31, no. 1, pp. 12–35. doi 10.1038/sj.npp.1300783
Kumer, S.C. and Vrana, K.E., Intricate regulation of tyrosine hydroxylase activity and gene expression, J. Neurochem., 1996, vol. 67, no. 2, pp. 443–462.
Kvetnansky, R., Sabban, E.L., and Palkovits, M., Catecholaminergic systems in stress: structural and molecular genetic approaches, Physiol. Rev., 2009, vol. 89, no. 2, pp. 535–606.
Langlais, D., Couture, C., Balsalobre, A., and Drouin, J., The Stat3/GR interaction code: predictive value of direct/indirect DNA recruitment for transcription outcome, Mol. Cell, 2012, vol. 47, no. 1, pp. 38–49. doi 10.1016/j.molcel.2012.04.021
Lenartowski, R. and Goc, A., Epigenetic, transcriptional and posttranscriptional regulation of the tyrosine hydroxylase gene, Int. J. Dev. Neurosci., 2011, vol. 29, no. 8, pp. 873–883.
Lewis, E.J., Tank, A.W., Weiner, N., and Chikaraishi, D.M., Regulation of tyrosine hydroxylase mRNA by glucocorticoid and cyclic AMP in a rat pheochromocytoma cell line. Isolation of a cDNA clone for tyrosine hydroxylase mRNA, J. Biol. Chem., 1983, vol. 258, no. 23, pp. 14632–14637.
Liberman, A.C., Refojo, D., Druker, J., Toscano, M., Rein, T., Holsboer, F., and Arzt, E., The activated glucocorticoid receptor inhibits the transcription factor t-bet by direct protein-protein interaction, FASEB J., 2007, vol. 21, no. 4, pp. 1177–1188. doi 10.1096/fj.06-7452com
Lopez-Sanchez, C., Bartulos, O., Martinez-Campos, E., Ganan, C., Valenciano, A.I., Garcia-Martinez, V., De Pablo, F., and Hernandez-Sanchez, C., Tyrosine hydroxylase is expressed during early heart development and is required for cardiac chamber formation, Cardiovasc. Res., 2010, vol. 88, no. 1, pp. 111–120.
Makino, S., Smith, M.A., and Gold, P.W., Regulatory role of glucocorticoids and glucocorticoid receptor mRNA levels on tyrosine hydroxylase gene expression in the locus coeruleus during repeated immobilization stress, Brain Res., 2002, vol. 943, no. 2, pp. 216–223.
Markey, K.A., Towle, A.C., and Sze, P.Y., Glucocorticoid influence on tyrosine hydroxylase activity in mouse locus coeruleus during postnatal development, Endocrinology, 1982, vol. 111, no. 5, pp. 1519–1523. doi 10.1210/endo-111-5-1519
Markham, J.A. and Koenig, J.I., Prenatal stress: Role in psychotic and depressive diseases, Psychopharmacology, 2011, vol. 214, no. 1, pp. 89–106. doi 10.1007/s00213-010-2035-0
Matthews, K., Dalley, J.W., Matthews, C., Tsai, T.H., and Robbins, T.W., Periodic maternal separation of neonatal rats produces region- and gender-specific effects on biogenic amine content in postmortem adult brain, Synapse, 2001, vol. 40, no. 1, pp. 1–10. doi 10.1002/1098-2396(200104)40:1<1::AID-SYN1020>3.0.CO;2-E
McArthur, S., McHale, E., and Gillies, G.E., The size and distribution of midbrain dopaminergic populations are permanently altered by perinatal glucocorticoid exposure in a sexregion- and time-specific manner, Neuropsychopharmacology, 2007, vol. 32, no. 7, pp. 1462–1476. doi 10.1038/sj.npp.1301277
Morin, X., Cremer, H., Hirsch, M.R., Kapur, R.P., Goridis, C., and Brunet, J.F., Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a, Neuron, 1997, vol. 18, no. 3, pp. 411–423.
Nagamoto-Combs, K., Piech, K.M., Best, J.A., Sun, B., and Tank, A.W., Tyrosine hydroxylase gene promoter activity is regulated by both cyclic AMP-responsive element and AP1 sites following calcium influx. Evidence for cyclic ampresponsive element binding protein-independent regulation, J. Biol. Chem., 1997, vol. 272, no. 9, pp. 6051–6058.
Nagatsu, T., Levitt, M., and Udenfriend, S., Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis, J. Biol. Chem., 1964, vol. 2910-2917.
Naumenko, E.V. and Dygalo, N.N., Noradrenergic Brain Mechanisms and Emotional Stress in Adult Rats after Prenatal Hydrocortisone Treatment. Biogenic Amines in Development, Amsterdam: Elsevier/North Holland Biomedical Press, 1980, pp. 373–388.
Newton, R. and Holden, N.S., Separating transrepression and transactivation: A distressing divorce for the glucocorticoid receptor?, Mol. Pharmacol., 2007, vol. 72, no. 4, pp. 799–809.
Oakley, R.H. and Cidlowski, J.A., The biology of the glucocorticoid receptor: New signaling mechanisms in health and disease, J. Allergy Clin. Immunol., 2013, vol. 132, no. 5, pp. 1033–1044. doi 10.1016/j.jaci.2013.09.007
Okada, Y., Saika, S., Shirai, K., Ohnishi, Y., and Senba, E., Expression of AP-1 (c-fos/c-jun) in developing mouse corneal epithelium, Graefe’s Archive for Clinical and Experimental Ophthalmology = Albrecht von Graefes Archiv fur Klinische und Experimentelle Ophthalmologie, 2003, vol. 241, no. 4, pp. 330–333.
Pattyn, A., Goridis, C., and Brunet, J.F., Specification of the central noradrenergic phenotype by the homeobox gene Phox2b, Mol. Cell. Neurosci., 2000, vol. 15, no. 3, pp. 235–243. doi 10.1006/mcne.1999.0826
Paulding, W.R., Schnell, P.O., Bauer, A.L., Striet, J.B., Nash, J.A., Kuznetsova, A.V., and Czyzyk-Krzeska, M.F., Regulation of gene expression for neurotransmitters during adaptation to hypoxia in oxygensensitive neuroendocrine cells, Microsc. Res. Techniq., 2002, vol. 59, no. 3, pp. 178–187. doi 10.1002/jemt.10192
Pennypacker, K.R., AP-1 transcription factor complexes in CNS disorders and development, J. Florida Med. Assoc., 1995, vol. 82, no. 8, pp. 551–554.
Pfahl, M., Nuclear receptor/AP-1 interaction, Endocr. Rev., 1993, vol. 14, no. 5, pp. 651–658.
Puymirat, J., Faivre-Bauman, A., Bizzini, B., and Tixier-Vidal, A., Prenatal and postnatal ontogenesis of neurotransmitter- synthetizing enzymes and [125I]tetanus toxin binding capacity in the mouse hypothalamus, Brain Res., 1982, vol. 255, no. 2, pp. 199–206.
Qian, Y., Fritzsch, B., Shirasawa, S., Chen, C.L., Choi, Y., and Ma, Q., Formation of brainstem (nor)adrenergic centers and first-order relay visceral sensory neurons is dependent on homeodomain protein Rnx/Tlx3, Genes Dev., 2001, vol. 15, no. 19, pp. 2533–2545.
Radcliffe, P.M., Sterling, C.R., and Tank, A.W., Induction of tyrosine hydroxylase mRNA by nicotine in rat midbrain is inhibited by mifepristone, J. Neurochem., 2009, vol. 109, no. 5, pp. 1272–1284. doi 10.1111/j.1471-4159.2009.06056.x
Raivich, G. and Behrens, A., Role of the AP-1 transcription factor c-Jun in developing, adult and injured brain, Progr. Neurobiol., 2006, vol. 78, no. 6, pp. 347–363.
Rani, C.S., Elango, N., Wang, S.S., Kobayashi, K., and Strong, R., Identification of an activator protein-1-like sequence as the glucocorticoid response element in the rat tyrosine hydroxylase gene, Mol. Pharmacol., 2009, vol. 75, no. 3, pp. 589–598.
Rani, C.S.S., Soto-Pina, A., Iacovitti, L., and Strong, R., Evolutionary conservation of an atypical glucocorticoidresponsive element in the human tyrosine hydroxylase gene, J. Neurochem., 2013, vol. 126, no. 1, pp. 19–28. doi 10.1111/jnc.12294
Reynolds, R.M., Programming effects of glucocorticoids, Clin. Obstet. Gynecol., 2013, vol. 56, no. 3, pp. 602–609.
Rios, M., Habecker, B., Sasaoka, T., Eisenhofer, G., Tian, H., Landis, S., Chikaraishi, D., and Roffler-Tarlov, S., Catecholamine synthesis is mediated by tyrosinase in the absence of tyrosine hydroxylase, J. Neurosci., 1999, vol. 19, no. 9, pp. 3519–3526.
Romano, G., Suon, S., Jin, H., Donaldson, A.E., and Iacovitti, L., Characterization of five evolutionary conserved regions of the human tyrosine hydroxylase (TH) promoter: Implications for the engineering of a human TH minimal promoter assembled in a self-inactivating lentiviral vector system, J. Cell Physiol., 2005, vol. 204, no. 2, pp. 666–677.
Sabban, E.L. and Kvetnansky, R., Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events, Trends Neurosci., 2001, vol. 24, no. 2, pp. 91–98.
Sabban, E.L., Hebert, M.A., Liu, X., Nankova, B., and Serova, L., Differential effects of stress on gene transcription factors in catecholaminergic systems, Ann. N. Y. Acad. Sci., 2004, vol. 1032, pp. 130–140.
Sapolsky, R.M., Romero, L.M., and Munck, A.U., How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions, Endocr. Rev., 2000, vol. 21, no. 1, pp. 55–89.
Shishkina, G.T., Kalinina, T.S., and Dygalo, N.N., Attenuation of alpha2A-adrenergic receptor expression in neonatal rat brain by RNA interference or antisense oligonucleotide reduced anxiety in adulthood, Neuroscience, 2004a, vol. 129, no. 3, pp. 521–528. doi 10.1016/j.neuroscience.2004.08.015
Shishkina, G.T., Kalinina, T.S., Popova, N.K., and Dygalo, N.N., Influence of neonatal short-term reduction in brainstem alpha2A-adrenergic receptors on receptor ontogenesis, acoustic startle reflex, and prepulse inhibition in rats, Behav. Neurosci., 2004b, vol. 118, no. 6, pp. 1285–1292. doi 10.1037/0735-7044.118.6.1285
Simon, H.H., Scholz, C., and O’Leary, D.D., Engrailed genes control developmental fate of serotonergic and noradrenergic neurons in mid- and hindbrain in a gene dosedependent manner, Mol. Cell. Neurosci., 2005, vol. 28, no. 1, pp. 96–105. doi 10.1016/j.mcn.2004.08.016
Slotkin, T.A., Kreider, M.L., Tate, C.A., and Seidler, F.J., Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems, Neuropsychopharmacology, 2006, vol. 31, no. 5, pp. 904–911. doi 10.1038/sj.npp.1300892
Sukhareva, E.V., Dygalo, N.N., and Kalinina, T.S., Influence of dexamethasone on the expression of early response genes c-fos and c-jun in different parts of the neonatal brain, (Moscow, 2016).
Sukhareva, E.V., Kalinina, T.S., Lanshakov, D.A., Bulygina, V.V., and Dygalo, N.N., Proteins of the AP-1 complex in induction of brain tyrosinhydroxylase by glucocorticoids in early ontogenesis, Mater. Sed’m. Vseros. nauch.-prakt. konf. “Fundamental’nye aspekty kompensatorno-prisposobitel’nykh protsessov” i Molodezhn. simp. “Molekulyarno-kletochnye i mediko-ekologicheskie problemy kompensatsii i prisposobleniya” (Proc. 7th Sci.-Pract. Conf. Fundamental Aspects of Compensatory and Adaptive Processes and Youth Symp. Molecular-Cellular and Medical-Environmental Issues of Compensation and Adaptation), 2015, pp. 271–272.
Sun, B., Chen, X., Xu, L., Sterling, C., and Tank, A.W., Chronic nicotine treatment leads to induction of tyrosine hydroxylase in locus ceruleus neurons: The role of transcriptional activation, Mol. Pharmacol., 2004, vol. 66, no. 4, pp. 1011–1021.
Tank, A.W., Curella, P., and Ham, L., Induction of mRNA for tyrosine hydroxylase by cyclic AMP and glucocorticoids in a rat pheochromocytoma cell line: Evidence for the regulation of tyrosine hydroxylase synthesis by multiple mechanisms in cells exposed to elevated levels of both inducing agents, Mol. Pharmacol., 1986, vol. 30, no. 5, pp. 497–503.
Tank, A.W., Xu, L., Chen, X., Radcliffe, P., and Sterling, C.R., Post-transcriptional regulation of tyrosine hydroxylase expression in adrenal medulla and brain, Ann. N. Y. Acad. Sci., 2008, vol. 1148, pp. 238–248.
Tekin, I., Roskoski, R., Jr., Carkaci-Salli, N., and Vrana, K.E., Complex molecular regulation of tyrosine hydroxylase, J. Neur. Transm. (Vienna), 2014, vol. 121, no. 12, pp. 1451–1481. doi 10.1007/s00702-014-1238-7
Teurich, S. and Angel, P., The glucocorticoid receptor synergizes with Jun homodimers to activate AP-1-regulated promoters lacking GR binding sites, Chem. Sens., 1995, vol. 20, no. 2, pp. 251–255.
Thomas, S.A., Matsumoto, A.M., and Palmiter, R.D., Noradrenaline is essential for mouse fetal development, Nature, 1995, vol. 374, no. 6523, pp. 643–646.
Vogel-Höpker, A. and Rohrer, H., The specification of noradrenergic locus coeruleus (LC) neurones depends on bone morphogenetic proteins (BMPs), Development, 2002, vol. 129, no. 4, pp. 983–991.
Wurst, W. and Bally-Cuif, L., Neural plate patterning: Upstream and downstream of the isthmic organizer, Nat. Rev. Neurosci., 2001, vol. 2, no. 2, pp. 99–108. doi 10.1038/35053516
Yamamoto, K., Ruuskanen, J.O., Wullimann, M.F., and Vernier, P., Two tyrosine hydroxylase genes in vertebrates. New dopaminergic territories revealed in the zebrafish brain, Mol. Cell. Neurosci., 2010, vol. 43, no. 4, pp. 394–402.
Zhong, S., Quealy, J.A., Bode, A.M., Nomura, M., Kaji, A., Ma, W.Y., and Dong, Z., Organ-specific activation of activator protein-1 in transgenic mice by 12-o-tetradecanoylphorbol-13-acetate with different administration methods, Cancer Res., 2001, vol. 61, no. 10, pp. 4084–4091.
Zhou, Q.Y., Quaife, C.J., and Palmiter, R.D., Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development, Nature, 1995, vol. 374, no. 6523, pp. 640–643.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © E.V. Sukhareva, T.S. Kalinina, V.V. Bulygina, N.N. Dygalo, 2016, published in Vavilovskii Zhurnal Genetiki i Selektsii, 2016, Vol. 20, No. 2, pp. 212–219.
Rights and permissions
About this article
Cite this article
Sukhareva, E.V., Kalinina, T.S., Bulygina, V.V. et al. Tyrosine hydroxylase in the brain and its regulation by glucocorticoids. Russ J Genet Appl Res 7, 226–234 (2017). https://doi.org/10.1134/S2079059717030145
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S2079059717030145