Repeated immobilization stress increases Nur77 expression in the bed nucleus of the stria terminalis

Neurotoxicity Research

Volumn 20, Issue 3, 2011, Pages 289-300

  Campos Melo, Danae ^a   Quiroz, Gabriel ^a   Noches, Verónica ^a   Gysling, Katia ^a   Forray, María Inés ^a   Andrés, María Estela ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

BNST; Corticotropin releasing factor; Desipramine; Noradrenaline; Nur77; Stress

Indexed keywords

DESIPRAMINE; MESSENGER RNA; NUCLEAR RECEPTOR NUR77;

ACUTE STRESS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BED NUCLEUS STRIA TERMINALIS; BRAIN REGION; CONTROLLED STUDY; DRUG MECHANISM; DRUG SPECIFICITY; GENE EXPRESSION REGULATION; GENE LOCATION; IMMOBILIZATION STRESS; MALE; MENTAL STRESS; NONHUMAN; PRIORITY JOURNAL; RAT; REPEAT PROCEDURE; STRIA TERMINALIS; TISSUE DISTRIBUTION;

ANALYSIS OF VARIANCE; ANIMALS; COLCHICINE; CORTICOTROPIN-RELEASING HORMONE; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; IMMOBILIZATION; MALE; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SEPTAL NUCLEI; STRESS, PSYCHOLOGICAL; TIME FACTORS; TUBULIN MODULATORS;

RATTUS;

EID: 84855648252     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-011-9243-1     Document Type: Article

References (85)

1. 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 (Pubitemid 23171090)
2. 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 (Pubitemid 40070132)
3. 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
4. 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
5. 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 (Pubitemid 34603494)
6. 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 (Pubitemid 36009367)
7. 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 (Pubitemid 24000999)
8. 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
9. 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
10. 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 (Pubitemid 46724402)
11. 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
12. 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 (Pubitemid 13016165)
13. 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 (Pubitemid 30392383)
14. 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 (Pubitemid 28335591)
15. 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 (Pubitemid 35246412)
16. 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 (Pubitemid 120004589)
17. 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 (Pubitemid 39574317)
18. 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 (Pubitemid 350044839)
19. 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 (Pubitemid 30485456)
20. 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
21. 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 (Pubitemid 44879411)
22. 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 (Pubitemid 34663914)
23. 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 (Pubitemid 34786680)
24. 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 (Pubitemid 19024988)
25. Honkaniemi J, Sharp FR (1996) Global ischemia induces immediateearly genes encoding zinc finger transcription factors. J Cereb Blood Flow Metab 16:557-565 (Pubitemid 26227064)
26. 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 (Pubitemid 24266073)
27. 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 (Pubitemid 126447897)
28. 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 (Pubitemid 39195273)
29. Itoi K, Sugimoto N (2010) The brainstem noradrenergic systems in stress, anxiety and depression. J Neuroendocrinol 22:355-361
30. 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
31. 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
32. 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 (Pubitemid 40775887)
33. 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 (Pubitemid 26010715)
34. Kuwaki T (2010) Orexin links emotional stress to autonomic functions. Auton Neurosci. PubMed PMID: 20813590
35. 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
36. 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
37. Lévesque D, Rouillard C (2007) Nur77 and retinoid X receptors: Crucial factors in dopamine-related neuroadaptation. Trends Neurosci 30:22-30 (Pubitemid 46001681)
38. 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
39. 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 (Pubitemid 24051145)
40. 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 (Pubitemid 30016020)
41. 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
42. 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 (Pubitemid 40411373)
43. 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 (Pubitemid 24281258)
44. 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 (Pubitemid 28136969)
45. 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 (Pubitemid 40138981)
46. 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 (Pubitemid 28480428)
47. Maxwell MA, Muscat GE (2006) The NR4A subgroup: Immediate early response genes with pleiotropic physiological roles. Nucl Recept Signal 4:e002
48. Milbrandt J (1988) Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1:183-188
49. 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 (Pubitemid 41674636)
50. 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 (Pubitemid 27021252)
51. 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 (Pubitemid 29074587)
52. 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 (Pubitemid 24064433)
53. 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 (Pubitemid 17096848)
54. 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 (Pubitemid 26290680)
55. 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
56. Parkes D, Rivest S, Lee S, Rivier C, Vale W (1993) Corticotropinreleasing factor activates c-fos, NGFI-B, and corticotropinreleasing factor gene expression within the paraventricular nucleus of the rat hypothalamus. Mol Endocrinol 7:1357-1367 (Pubitemid 23319119)
57. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic Press, San Diego San Diego
58. 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 (Pubitemid 351406269)
59. 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 (Pubitemid 44353386)
60. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
61. 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
62. 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 (Pubitemid 27411102)
63. 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
64. 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 (Pubitemid 47172691)
65. 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
66. 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 (Pubitemid 44654450)
67. 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 (Pubitemid 126718435)
68. Shalizi A, Gaudillière B, Yuan Z, Stegmüller J, Shirogane T, Ge Q, Tan Y, Schulman B, Harper JW, Bonni A (2006) A calciumregulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311:1012-1017 (Pubitemid 43271730)
69. 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 (Pubitemid 44397188)
70. 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 (Pubitemid 41476271)
71. 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 (Pubitemid 30479810)
72. 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
73. 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
74. 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 (Pubitemid 24259666)
75. 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
76. 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 (Pubitemid 46213917)
77. 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
78. 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 (Pubitemid 27334620)
79. von Hertzen LS, Giese KP (2005) Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25:1935-1942 (Pubitemid 40289398)
80. 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 (Pubitemid 36183715)
81. 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 (Pubitemid 36205081)
82. Walker DL, Miles LA, Davis M (2009) Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxietylike versus phasic fear-like responses. Prog Neuropsychopharmacol Biol Psychiatry 33:1291-1308
83. 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 (Pubitemid 30201590)
84. 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 (Pubitemid 24051144)
85. 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 (Pubitemid 46216756)