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Repeated Immobilization Stress Increases Nur77 Expression in the Bed Nucleus of the Stria Terminalis

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Abstract

The transcription factor Nur77 has been identified as a neuronal activation marker of stressful stimuli in the central nervous system. Nur77 plays a key role at all levels of the hypothalamus–pituitary–adrenal axis during the stress response. However, the participation of Nur77 in extra-hypothalamic responses to stress is unknown. In this study, we studied the impact of acute and repeated immobilization stress on Nur77 expression in the bed nucleus of stria terminalis (BNST), a region involved in autonomic, neuroendocrine, and behavioral responses to stress. After a single session of immobilization stress we observed a significant increase of Nur77-like immunoreactivity in the BNST. This effect is not lost with repeated exposure to stress, since Nur77-like immunoreactivity and Nur77 mRNA in BNST were increased after the fifteenth stress session. The administration of desipramine, a specific inhibitor of noradrenaline reuptake, prevented the increase in Nur77-like immunoreactivity and mRNA induced by stress in rats subjected to repeated exposure to immobilization stress. Our results show that acute and repeated stress modulates Nur77 expression in BNST and suggest that Nur77 participates in extra-hypothalamic responses to stress.

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References

  • Andrés ME, Forray MI, Barría CG, Gysling K (1993) Studies of cholecystokinin in the rat bed nucleus of stria terminalis. Biochem Pharmacol 45:2283–2288

    Article  PubMed  Google Scholar 

  • Bassett MH, White PC, Rainey WE (2004) A role for the NGFI-B family in adrenal zonation and adrenocortical disease. Endocr Res 30:567–574

    Article  PubMed  CAS  Google Scholar 

  • Beaudry G, Langlois MC, Weppe I, Rouillard C, Levesque D (2000) Contrasting patterns and cellular specificity of transcriptional regulation of the nuclear receptor nerve growth factor-inducible B by haloperidol and clozapine in the rat forebrain. J Neurochem 75:1694–1702

    Article  PubMed  CAS  Google Scholar 

  • Brownstein MJ, Palkovits M (1984) Catecholamines, serotonin, acetylcholine, and g-aminobutyric acid in the rat brain: biochemical studies. In: Bjorklund A, Hokfelt T (eds) Handbook of chemical neuroanatomy, Part I, vol 2. Elsevier, Amsterdam, pp 23–54

    Google Scholar 

  • Cecchi M, Khoshbouei H, Javors M, Morilak DA (2002a) Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 112:13–21

    Article  PubMed  CAS  Google Scholar 

  • Cecchi M, Khoshbouei H, Morilak DA (2002b) Modulatory effects of norepinephrine, acting on alpha 1 receptors in the central nucleus of the amygdala, on behavioral and neuroendocrine responses to acute immobilization stress. Neuropharmacology 43:1139–1147

    Article  PubMed  CAS  Google Scholar 

  • Chan RK, Brown ER, Ericsson A, Kovács KJ, Sawchenko PE (1993) A comparison of two immediate-early genes, c-fos and NGFI-B, as markers for functional activation in stress-related neuroendocrine circuitry. J Neurosci 13:5126–5138

    PubMed  CAS  Google Scholar 

  • Choi DC, Furay AR, Evanson NK, Ostrander MM, Ulrich-Lai YM, Herman JP (2007) Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic–pituitary–adrenal axis activity: implications for the integration of limbic inputs. J Neurosci 27:2025–2034

    Article  PubMed  CAS  Google Scholar 

  • Crawford PA, Sadovsky Y, Woodson K, Lee SL, Milbrandt J (1995) Adrenocortical function and regulation of the steroid 21-hydroxylase gene in NGFI-B-deficient mice. Mol Cell Biol 15:4331–4336

    PubMed  CAS  Google Scholar 

  • Crestani CC, Alves FH, Resstel LB, Correa FM (2007) Cardiovascular effects of noradrenaline microinjection in the bed nucleus of the stria terminalis of the rat brain. J Neurosci Res 85:1592–1599

    Article  PubMed  CAS  Google Scholar 

  • Crestani CC, Alves FH, Correa FM, Guimarães FS, Joca SR (2010) Acute reversible inactivation of the bed nucleus of stria terminalis induces antidepressant-like effect in the rat forced swimming test. Behav Brain Funct 6:30

    Article  PubMed  Google Scholar 

  • Cummings S, Elde R, Ells J, Lindall A (1983) Corticotropin-releasing factor immunoreactivity is widely distributed within the central nervous system of the rat: an immunohistochemical study. J Neurosci 3:1355–1368

    PubMed  CAS  Google Scholar 

  • D’Aquila PS, Peana AT, Carboni V, Serra G (2000) Exploratory behaviour and grooming after repeated restraint and chronic mild stress: effect of desipramine. Eur J Pharmacol 399:43–47

    Article  PubMed  Google Scholar 

  • Drouin J, Maira M, Philips A (1998) Novel mechanism of action for Nur77 and antagonism by glucocorticoids: a convergent mechanism for CRH activation and glucocorticoid repression of POMC gene transcription. J Steroid Biochem Mol Biol 65:59–63

    Article  PubMed  CAS  Google Scholar 

  • Eells JB, Lipska BK, Yeung SK, Misler JA, Nikodem VM (2002) Nurr1-null heterozygous mice have reduced mesolimbic and mesocortical dopamine levels and increased stress-induced locomotor activity. Behav Brain Res 136:267–275

    Article  PubMed  CAS  Google Scholar 

  • Fahrner TJ, Carroll SL, Milbrandt J (1990) The NGFI-B protein, an inducible member of the thyroid/steroid receptor family, is rapidly modified posttranslationally. Mol Cell Biol 10:6454–6459

    PubMed  CAS  Google Scholar 

  • Forray MI, Gysling K (2004) Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic–pituitary–adrenal axis. Brain Res Brain Res Rev 47:145–160

    Article  PubMed  CAS  Google Scholar 

  • Fu Y, Luo L, Luo N, Zhu X, Garvey WT (2007) NR4A orphan nuclear receptors modulate insulin action and the glucose transport system: potential role in insulin resistance. J Biol Chem 282:31525–31533

    Article  PubMed  CAS  Google Scholar 

  • Fuentealba JA, Forray MI, Gysling K (2000) Chronic morphine treatment and withdrawal increase extracellular levels of norepinephrine in the rat bed nucleus of the stria terminalis. J Neurochem 75:741–748

    Article  PubMed  CAS  Google Scholar 

  • Gavrilovic L, Spasojevic N, Zivkovic M, Dronjak S (2009) Effect of immobilization stress on gene expression of catecholamine biosynthetic enzymes in heart auricles of socially isolated rats. Braz J Med Biol Res 42:1185–1190

    Article  PubMed  CAS  Google Scholar 

  • Gobshtis N, Ben-Shabat S, Fride E (2007) Antidepressant-induced undesirable weight gain: prevention with rimonabant without interference with behavioral effectiveness. Eur J Pharmacol 554:155–163

    Article  PubMed  CAS  Google Scholar 

  • Harris RB, Mitchell TD, Simpson J, Redmann SM Jr, Youngblood BD, Ryan DH (2002a) Weight loss in rats exposed to repeated acute restraint stress is independent of energy or leptin status. Am J Physiol Regul Integr Comp Physiol 282:R77–R88

    PubMed  CAS  Google Scholar 

  • Harris RB, Zhou J, Mitchell T, Hebert S, Ryan DH (2002b) Rats fed only during the light period are resistant to stress-induced weight loss. Physiol Behav 76:543–550

    Article  PubMed  CAS  Google Scholar 

  • Hazel TG, Nathans D, Lau LF (1988) A gene inducible by serum growth factors encodes a member of the steroid and thyroid hormone receptor superfamily. Proc Natl Acad Sci USA 85:8444–8448

    Article  PubMed  CAS  Google Scholar 

  • Honkaniemi J, Sharp FR (1996) Global ischemia induces immediate-early genes encoding zinc finger transcription factors. J Cereb Blood Flow Metab 16:557–565

    Article  PubMed  CAS  Google Scholar 

  • Honkaniemi J, Kononen J, Kainu T, Pyykonen I, Peltohuikko M (1994) Induction of multiple immediate-early genes in rat hypothalamic paraventricular nucleus after stress. Mol Brain Res 25:234–241

    Article  PubMed  CAS  Google Scholar 

  • Imaki T, Shibasaki T, Chikada N, Harada S, Naruse M, Demura H (1996) Different expression of immediate-early genes in the rat paraventricular nucleus induced by stress: relation to corticotropin-releasing factor gene transcription. Endocr J 43:629–638

    Article  PubMed  CAS  Google Scholar 

  • Invernizzi RW, Garattini S (2004) Role of presynaptic alpha2-adrenoceptors in antidepressant action: recent findings from microdialysis studies. Prog Neuropsychopharmacol Biol Psychiatry 28:819–827

    Article  PubMed  CAS  Google Scholar 

  • Itoi K, Sugimoto N (2010) The brainstem noradrenergic systems in stress, anxiety and depression. J Neuroendocrinol 22:355–361

    Article  PubMed  CAS  Google Scholar 

  • Katunar MR, Saez T, Brusco A, Antonelli MC (2009) Immunocytochemical expression of dopamine-related transcription factors Pitx3 and Nurr1 in prenatally stressed adult rats. J Neurosci Res 87:1014–1022

    Article  PubMed  CAS  Google Scholar 

  • Katunar MR, Saez T, Brusco A, Antonelli MC (2010) Ontogenetic expression of dopamine-related transcription factors and tyrosine hydroxylase in prenatally stressed rats. Neurotox Res 18:69–81

    Article  PubMed  Google Scholar 

  • Korosi A, Schotanus S, Olivier B, Roubos EW, Kozicz T (2005) Chronic ether stress-induced response of urocortin 1 neurons in the Edinger-Westphal nucleus in the mouse. Brain Res 1046:172–179

    Article  PubMed  CAS  Google Scholar 

  • Kovács KJ, Sawchenko PE (1996) Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons. J Neurosci 16:262–273

    PubMed  Google Scholar 

  • Kuwaki T (2010) Orexin links emotional stress to autonomic functions. Auton Neurosci. PubMed PMID: 20813590

  • Lam BY, Zhang W, Ng DC, Maruthappu M, Llewelyn Roderick H, Chawla S (2009) CREB-dependent Nur77 induction following depolarization in PC12 cells and neurons is modulated by MEF2 transcription factors. J Neurochem 112:1065–1073

    Article  PubMed  Google Scholar 

  • Langnaese K, John R, Schweizer H, Ebmeyer U, Keilhoff G (2008) Selection of reference genes for quantitative real-time PCR in a rat asphyxial cardiac arrest model. BMC Mol Biol 9:53

    Article  PubMed  Google Scholar 

  • Lévesque D, Rouillard C (2007) Nur77 and retinoid X receptors: crucial factors in dopamine-related neuroadaptation. Trends Neurosci 30:22–30

    Article  PubMed  Google Scholar 

  • Liu B, Kwok RP, Fernstrom JD (1991) Colchicine-induced increases in immunoreactive neuropeptide levels in hypothalamus: use as an index of biosynthesis. Life Sci 49:345–352

    Article  PubMed  CAS  Google Scholar 

  • Liu ZG, Smith SW, McLaughlin KA, Schwartz LM, Osborne BA (1994) Apoptotic signals delivered through the T-cell receptor of a T-cell hybrid require the immediate-early gene nur77. Nature 367:281–284

    Article  PubMed  CAS  Google Scholar 

  • López-Rubalcava C, Lucki I (2000) Strain differences in the behavioral effects of antidepressant drugs in the rat forced swimming test. Neuropsychopharmacology 22:191–199

    Article  PubMed  Google Scholar 

  • Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445

    Article  PubMed  CAS  Google Scholar 

  • Maheux J, Ethier I, Rouillard C, Lévesque D (2005) Induction patterns of transcription factors of the nur family (nurr1, nur77, and nor-1) by typical and atypical antipsychotics in the mouse brain: implication for their mechanism of action. J Pharmacol Exp Ther 313:460–473

    Article  PubMed  CAS  Google Scholar 

  • Makino S, Gold PW, Schulkin J (1994) Effects of corticosterone on CRF mRNA and content in the bed nucleus of the stria terminalis; comparison with the effects in the central nucleus of the amygdala and the paraventricular nucleus of the hypothalamus. Brain Res 657:141–149

    Article  PubMed  CAS  Google Scholar 

  • Mansi JA, Rivest S, Drolet G (1998) Effect of immobilization stress on transcriptional activity of inducible immediate-early genes, corticotropin-releasing factor, its type 1 receptor, and enkephalin in the hypothalamus of borderline hypertensive rats. J Neurochem 70:1556–1566

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Gonzalez J, Badimon L (2005) The NR4A subfamily of nuclear receptors: new early genes regulated by growth factors in vascular cells. Cardiovasc Res 65:609–618

    Article  PubMed  CAS  Google Scholar 

  • Mateo Y, Pineda J, Meana JJ (1998) Somatodendritic alpha2-adrenoceptors in the locus coeruleus are involved in the in vivo modulation of cortical noradrenaline release by the antidepressant desipramine. J Neurochem 71:790–798

    Article  PubMed  CAS  Google Scholar 

  • Maxwell MA, Muscat GE (2006) The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl Recept Signal 4:e002

    Article  PubMed  Google Scholar 

  • Milbrandt J (1988) Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1:183–188

    Article  PubMed  CAS  Google Scholar 

  • Morilak DA, Barrera G, Echevarria DJ, Garcia AS, Hernandez A, Ma S, Petre CO (2005) Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 29:1214–1224

    Article  PubMed  CAS  Google Scholar 

  • Murphy EP, Conneely OM (1997) Neuroendocrine regulation of the hypothalamic pituitary adrenal axis by the nurr1/nur77 subfamily of nuclear receptors. Mol Endocrinol 11:39–47

    Article  PubMed  CAS  Google Scholar 

  • Nankova BB, Fuchs SY, Serova LI, Ronai Z, Wild D, Sabban EL (1998) Selective in vivo stimulation of stress-activated protein kinase in different rat tissues by immobilization stress. Stress 2:289–298

    Article  PubMed  CAS  Google Scholar 

  • Neumann-Haefelin T, Wiessner C, Vogel P, Back T, Hossmann KA (1994) Differential expression of the immediate early genes c-fos, c-jun, junB, and NGFI-B in the rat brain following transient forebrain ischemia. J Cereb Blood Flow Metab 14:206–216

    Article  PubMed  CAS  Google Scholar 

  • Nobrega JN, Coscina DV (1987) Effects of chronic amitriptyline and desipramine on food intake and body weight in rats. Pharmacol Biochem Behav 27:105–112

    Article  PubMed  CAS  Google Scholar 

  • Ohkura N, Ito M, Tsukada T, Sasaki K, Yamaguchi K, Miki K (1996) Structure, mapping and expression of a human NOR-1 gene, the third member of the Nur77/NGFI-B family. Biochim Biophys Acta 1308:205–214

    PubMed  Google Scholar 

  • Pacak K, McCarty R, Palkovits M, Kopin IJ, Goldstein DS (1995) Effects of immobilization on in vivo release of norepinephrine in the bed nucleus of the stria terminalis in conscious rats. Brain Res 688:242–246

    Article  PubMed  CAS  Google Scholar 

  • Parkes D, Rivest S, Lee S, Rivier C, Vale W (1993) Corticotropin-releasing factor activates c-fos, NGFI-B, and corticotropin-releasing factor gene expression within the paraventricular nucleus of the rat hypothalamus. Mol Endocrinol 7:1357–1367

    Article  PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Pego JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OFX, Sousa N (2008) Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci 27:1503–1516

    Article  PubMed  CAS  Google Scholar 

  • Pei L, Waki H, Vaitheesvaran B, Wilpitz DC, Kurland IJ, Tontonoz P (2006) NR4A orphan nuclear receptors are transcriptional regulators of hepatic glucose metabolism. Nat Med 12:1048–1055

    Article  PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  PubMed  CAS  Google Scholar 

  • Phelix CF, Liposits Z, Paull WK (1992) Monoamine innervation of bed nucleus of stria terminalis: an electron microscopic investigation. Brain Res Bull 28:949–965

    Article  PubMed  CAS  Google Scholar 

  • Philips A, Maira M, Mullick A, Chamberland M, Lesage S, Hugo P, Drouin J (1997) Antagonism between Nur77 and glucocorticoid receptor for control of transcription. Mol Cell Biol 17:5952–5959

    PubMed  CAS  Google Scholar 

  • Rivest S, Rivier C (1994) Stress and interleukin-1-beta-induced activation of c-Fos, NGFI-B and CRF gene expression in the hypothalamic PVN comparison between Sprague–Dawley, Fisher-344 and Lewis rats. J Neuroendocrinol 6:101–117

    Article  PubMed  CAS  Google Scholar 

  • Rojas P, Joodmardi E, Hong Y, Perlmann T, Ogren SO (2007) Adult mice with reduced Nurr1 expression: an animal model for schizophrenia. Mol Psychiatry 12:756–766

    Article  PubMed  CAS  Google Scholar 

  • Rojas P, Joodmardi E, Perlmann T, Ogren SO (2010) Rapid increase of Nurr1 mRNA expression in limbic and cortical brain structures related to coping with depression-like behavior in mice. J Neurosci Res 88:2284–2293

    Article  PubMed  CAS  Google Scholar 

  • Santibañez M, Gysling K, Forray MI (2006) Desipramine prevents the sustained increase in corticotropin-releasing hormone-like immunoreactivity induced by repeated immobilization stress in the rat central extended amygdala. J Neurosci Res 84:1270–1281

    Article  PubMed  Google Scholar 

  • Saucedo-Cardenas O, Conneely OM (1996) Comparative distribution of NURR1 and NUR77 nuclear receptors in the mouse central nervous system. J Mol Neurosci 7:51–63

    Article  PubMed  CAS  Google Scholar 

  • Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A (2006) A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311:1012–1017

    Article  PubMed  CAS  Google Scholar 

  • Shepard JD, Schulkin J, Myers DA (2006) Chronically elevated corticosterone in the amygdala increases corticotropin releasing factor mRNA in the dorsolateral bed nucleus of stria terminalis following duress. Behav Brain Res 174:193–196

    Article  PubMed  CAS  Google Scholar 

  • St-Hilaire M, Landry E, Lévesque D, Rouillard C (2005) Denervation and repeated L-DOPA induce complex regulatory changes in neurochemical phenotypes of striatal neurons: implication of a dopamine D1-dependent mechanism. Neurobiol Dis 20:450–460

    Article  PubMed  CAS  Google Scholar 

  • Stout SC, Mortas P, Owens MJ, Nemeroff CB, Moreau J (2000) Increased corticotropin-releasing factor concentrations in the bed nucleus of the stria terminalis of anhedonic rats. Eur J Pharmacol 401:39–46

    Article  PubMed  CAS  Google Scholar 

  • Suvrathan A, Tomar A, Chattarji S (2010) Effects of chronic and acute stress on rat behaviour in the forced-swim test. Stress 13:533–540

    PubMed  Google Scholar 

  • Svenningsson P, Nomikos GG, Fredholm BB (1995) Biphasic changes in locomotor behavior and in expression of mRNA for NGFI-A and NGFI-B in rat striatum following acute caffeine administration. J Neurosci 15:7612–7624

    PubMed  CAS  Google Scholar 

  • Szarek BL, Brandt DM (1993) A comparison of weight changes with fluoxetine, desipramine, and amitriptyline: a retrospective study of psychiatric inpatients. J Nerv Ment Dis 181:702–704

    Article  PubMed  CAS  Google Scholar 

  • Thal SC, Wyschkon S, Pieter D, Engelhard K, Werner C (2008) Selection of endogenous control genes for normalization of gene expression analysis after experimental brain trauma in mice. J Neurotrauma 25:785–794

    Article  PubMed  Google Scholar 

  • Trnecková L, Rotllant D, Klenerová V, Hynie S, Armario A (2007) Dynamics of immediate early gene and neuropeptide gene response to prolonged immobilization stress: evidence against a critical role of the termination of exposure to the stressor. J Neurochem 100:905–914

    Article  PubMed  Google Scholar 

  • Umemoto S, Kawai Y, Senba E (1994) Differential regulation of IEGs in the rat PVH in single and repeated stress models. Neuroreport 6:201–204

    Article  PubMed  CAS  Google Scholar 

  • Umemoto S, Kawai Y, Ueyama T, Senba E (1997) Chronic glucocorticoid administration as well as repeated stress affects the subsequent acute immobilization stress-induced expression of immediate early genes but not that of NGFI-A. Neuroscience 80:763–773

    Article  PubMed  CAS  Google Scholar 

  • von Hertzen LS, Giese KP (2005) Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25:1935–1942

    Article  Google Scholar 

  • Vyas A, Bernal S, Chattarji S (2003) Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res 965:290–294

    Article  PubMed  CAS  Google Scholar 

  • Walker DL, Toufexis DJ, Davis M (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463:199–216

    Article  PubMed  CAS  Google Scholar 

  • Walker DL, Miles LA, Davis M (2009) Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog Neuropsychopharmacol Biol Psychiatry 33:1291–1308

    Article  PubMed  CAS  Google Scholar 

  • Werme M, Ringholm A, Olson L, Brene S (2000) Differential patterns of induction of NGFI-B, Nor1 and c-fos mRNAs in striatal subregions by haloperidol and clozapine. Brain Res 863:112–119

    Article  PubMed  CAS  Google Scholar 

  • Woronicz JD, Calnan B, Ngo V, Winoto A (1994) Requirement for the orphan steroid receptor Nur77 in apoptosis of T-cell hybridomas. Nature 367:277–281

    Article  PubMed  CAS  Google Scholar 

  • Zhang SJ, Steijaert MN, Lau D, Schutz G, Delucinge-Vivier C, Descombes P, Bading H (2007) Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53:549–562

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by FONDECYT Projects 3085027 (DCM) and 1070349 (MEA) and Millennium Nucleus in Stress and Addiction MSI N° P06/008-F. We acknowledge Mr. Elias Blanco for his support in confocal microscopy.

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Correspondence to María Estela Andrés.

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Campos-Melo, D., Quiroz, G., Noches, V. et al. Repeated Immobilization Stress Increases Nur77 Expression in the Bed Nucleus of the Stria Terminalis. Neurotox Res 20, 289–300 (2011). https://doi.org/10.1007/s12640-011-9243-1

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