Susceptibility to the long-term anxiogenic effects of an acute stressor is mediated by the activation of the glucocorticoid receptors

Neuropharmacology

Volumn 61, Issue 8, 2011, Pages 1297-1305

  Jakovcevski, Mira ^a,b   Schachner, Melitta ^a,c   Morellini, Fabio ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Addiction; c fos; Hippocampus; HPA axis; Paraventricular nucleus; Tyrosine hydroxylase

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; COCAINE; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; DIAZEPAM; GLUCOCORTICOID RECEPTOR; MIFEPRISTONE; PROTEIN C FOS; TYROSINE 3 MONOOXYGENASE;

ACUTE STRESS; ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; GENE EXPRESSION; HIPPOCAMPUS; HYPOPHYSIS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LATENT PERIOD; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REWARD; TRANQUILIZING ACTIVITY;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANALYSIS OF VARIANCE; ANIMALS; ANTI-ANXIETY AGENTS; COCAINE; CONDITIONING, OPERANT; CORTICOTROPIN-RELEASING HORMONE; DIAZEPAM; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HORMONE ANTAGONISTS; HYPOTHALAMUS; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MIFEPRISTONE; PROTO-ONCOGENE PROTEINS C-FOS; RADIOIMMUNOASSAY; RATS; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; SEROTONIN RECEPTOR AGONISTS; STRESS, PSYCHOLOGICAL; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 80053598884     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.07.034     Document Type: Article

References (62)

1. B. Aisa, F.J. Gil-Bea, B. Marcos, R. Tordera, B. Lasheras, J. Del Río, and M.J. Ramírez Neonatal stress affects vulnerability of cholinergic neurons and cognition in the rat: involvement of the HPA axis Psychoneuroendocrinology 34 2009 1495 1505
2. L. Andréen, S. Nyberg, S. Turkmen, G. van Wingen, G. Fernández, and T. Bäckström Sex steroid induced negative mood may be explained by the paradoxical effect mediated by GABAA modulators Psychoneuroendocrinology 34 2009 1121 1132
3. N. Barden, J.M. Reul, and F. Holsboer Do antidepressants stabilize mood through actions on the hypothalamic-pituitary-adrenocortical system? Trends Neurosci. 18 1995 6 11
4. E.H. Beckley, A.C. Scibelli, and D.A. Finn Progesterone receptor antagonist CDB-4124 increases depression-like behavior in mice without affecting locomotor ability Psychoneuroendocrinology 36 2011 824 833
5. C. Belzung, and F. Berton Further pharmacological validation of the BALB/c neophobia in the free exploratory paradigm as an animal model of trait anxiety Behav. Pharmacol. 8 1997 541 548 (Pubitemid 27504704)
6. R.J. Berry, and P.N. Scriven The house mouse: a model and motor for evolutionary understanding Biol. J. Linn. Soc. 84 2005 335 347 (Pubitemid 40441042)
7. D. Bitran, M. Shiekh, J.A. Dowd, M.M. Dugan, and P. Renda Corticosterone is permissive to the anxiolytic effect that results from the blockade of hippocampal mineralocorticoid receptors Pharmacol. Biochem. Behav. 60 1998 879 887 (Pubitemid 28349949)
8. J. Bormann Electrophysiological characterization of diazepam binding inhibitor (DBI) on GABAA receptors Neuropharmacology 30 1991 1387 1389
9. M.P. Boyle, J.A. Brewer, M. Funatsu, D.F. Wozniak, J.Z. Tsien, Y. Izumi, and L.J. Muglia Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior Proc. Natl. Acad. Sci. U S A 102 2005 473 478 (Pubitemid 40116791)
10. M.P. Boyle, B.J. Kolber, S.K. Vogt, D.F. Wozniak, and L.J. Muglia Forebrain glucocorticoid receptors modulate anxiety-associated locomotor activation and adrenal responsiveness J. Neurosci. 26 2006 1971 1978
11. F.H. Bronson The adaptability of the house mouse Sci. Am. 250 1984 116 125
12. G. Calfa, D. Bussolino, and V.A. Molina Involvement of lateral septum and the ventral hippocampus in the emotional sequelae induced by social defeat:role of the glucocorticoid receptors Behav. Brain Res. 181 2007 23 34 (Pubitemid 46766688)
13. N. Calvo, and M. Volosin Glucocorticoid and mineralocorticoid receptors are involved in the facilitation of anxiety-like response induced by restraint Neuroendocrinology 73 2001 261 271 (Pubitemid 32424520)
14. C. DeBattista, and J. Belanoff The use of mifepristone in the treatment of neuropsychiatric disorders Trends Endocrinol. Metab. 17 2006 117 121
15. J.P. Druhan, and W.B. Wilent Effects of the competitive N-methyl-D-aspartate receptor antagonist, CPP, on the development and expression of conditioned hyperactivity and sensitization induced by cocaine Behav. Brain Res. 102 1999 195 210 (Pubitemid 29314580)
16. J.C. Earnheart, C. Schweizer, F. Crestani, T. Iwasato, S. Itohara, H. Mohler, and B. Lüscher GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxiety and depression states J. Neurosci. 27 2007 3845 3854 (Pubitemid 46557682)
17. B.J. Ellis, J.J. Jackson, and W.T. Boyce The stress response systems: universality and adaptive individual differences Dev. Rev. 26 2006 175 212 (Pubitemid 43758240)
18. B.H. Flores, H. Kenna, J. Keller, H.B. Solvason, and A.F. Schatzberg Clinical and biological effects of mifepristone treatment for psychotic depression Neuropsychopharmacology 31 2006 628 636 (Pubitemid 43276978)
19. E. Frank, P. Salchner, J.M. Aldag, N. Salomé, N. Singewald, R. Landgraf, and A. Wigger Genetic predisposition to anxiety-related behavior determines coping style, neuroendocrine responses, and neuronal activation during social defeat Behav. Neurosci. 120 2006 60 71.1 628-636
20. K.B.J. Franklin, and G. Paxinos The Mouse Brain in Stereotaxic Coordinates 1997 Academic Press San Diego
21. F.M. Gerner, T. Trapp, and C.A. Hauser A classic cAMP responsive element in the promoter region of the alpha 1-GABAA receptor subunit has non-classic properties Funct. Neurol. 12 1997 55 61 (Pubitemid 27244752)
22. T.C. Goes, F.D. Antunes, and F. Teixeira-Silva Trait and state anxiety in animal models: is there correlation? Neurosci. Lett. 450 2009 266 269
23. G. Griebel, C. Belzung, R. Misslin, and E. Vogel The free-exploratory paradigm: an effective method for measuring neophobic behaviour in mice and testing potential neophobia-reducing drugs Behav. Pharmacol. 4 1993 637 644 (Pubitemid 24002278)
24. M. Jakovcevski, M. Schachner, and F. Morellini Individual variability in the stress response of C57BL/6J male mice correlates with trait anxiety Genes Brain Behav. 7 2008 235 243 (Pubitemid 351342200)
25. M. Joëls, and E.R. de Kloet Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems Prog. Neurobiol. 43 1994 1 36 (Pubitemid 24221853)
26. E.R. de Kloet, E. Vreugdenhil, M.S. Oitzl, and M. Joels Brain corticosteroid receptor balance in health and disease Endocr. Rev. 19 1998 269 301 (Pubitemid 29117816)
27. E.R. de Kloet, R.H. Derijk, and O.C. Meijer Therapy insight: is there an imbalanced response of mineralocorticoid and glucocorticoid receptors in depression? Nat. Clin. Pract. Endocrinol. Metab. 3 2007 168 179 (Pubitemid 46146969)
28. K. Kohda, K. Harada, K. Kato, A. Hoshino, J. Motohashi, T. Yamaji, S. Morinobu, N. Matsuoka, and N. Kato Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: a putative post-traumatic stress disorder model Neuroscience 148 2007 22 33 (Pubitemid 47211627)
29. S.M. Korte Corticosteroids in relation to fear, anxiety and psychopathology Neurosci. Biobehav. Rev. 25 2001 117 142 (Pubitemid 32377167)
30. S.M. Korte, S.F. de Boer, E.R. de Kloet, and B. Bohus Anxiolytic-like effects of selective mineralocorticoid and glucocorticoid antagonists on fear-enhanced behavior in the elevated plus-maze Psychoneuroendocrinology 20 1995 385 394
31. S.M. Korte, G.A. Korte-Bouws, G.F. Koobm, E.R. De Kloet, and B. Bohus Mineralocorticoid and glucocorticoid receptor antagonists in animal models of anxiety Pharmacol. Biochem. Behav. 54 1996 261 267 (Pubitemid 26146676)
32. V. Krishnan, M.H. Han, D.L. Graham, O. Berton, W. Renthal, S.J. Russo, Q. Laplant, A. Graham, M. Lutter, D.C. Lagace, S. Ghose, R. Reister, P. Tannous, T.A. Green, R.L. Neve, S. Chakravarty, A. Kumar, A.J. Eisch, D.W. Self, F.S. Lee, C.A. Tamminga, D.C. Cooper, H.K. Gershenfeld, and E.J. Nestler Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions Cell 131 2007 391 404 (Pubitemid 47576141)
33. S.A. Krömer, M.S. Kessler, D. Milfay, I.N. Birg, M. Bunck, L. Czibere, M. Panhuysen, B. Pütz, J.M. Deussing, F. Holsboer, R. Landgraf, and C.W. Turck Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety J. Neurosci. 25 2005 4375 4384 (Pubitemid 40628782)
34. R. Landgraf, and A. Wigger High vs low anxiety-related behavior rats: an animal model of extremes in trait anxiety Behav. Genet. 32 2002 301 314 (Pubitemid 35192992)
35. R. Landgraf, A. Wigger, F. Holsboer, and I.D. Neumann Hyper-reactive hypothalamo-pituitary-adrenocortical axis in rats bred for high anxiety-related behaviour J. Neuroendocrinol. 11 1999 405 407 (Pubitemid 29243762)
36. A.C. Linthorst, C. Flachskamm, N. Barden, F. Holsboer, and J.M. Reul Glucocorticoid receptor impairment alters CNS responses to psychological stressor: an in vivo microdialysis study in transgenic mice Eur. J. Neurosci. 12 2000 283 291 (Pubitemid 30068433)
37. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 428
38. J.P. McLaughlin, B.B. Land, S. Li, J.E. Pintar, and C. Chavkin Prior activation of kappa opioid receptors by U50,488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning Neuropsychopharmacology 31 2006 787 794
39. F. Morellini, and M. Schachner Enhanced novelty-induced activity, reduced anxiety, delayed resynchronization to daylight reversal and weaker muscle strength in tenascin-C-deficient mice Eur. J. Neurosci. 23 2006 1255 1268
40. P. Muigg, S. Scheiber, P. Salchner, M. Bunck, R. Landgraf, and N. Singewald Differential stress-induced neuronal activation patterns in mouse lines selectively bred for high, normal or low anxiety PLoS One 4 2009 e5346
41. L. Musazzi, M. Milanese, P. Farisello, S. Zappettini, D. Tardito, V.S. Barbiero, T. Bonifacino, A. Mallei, P. Baldelli, G. Racagni, M. Raiteri, F. Benfenati, G. Bonanno, and M. Popoli Acute stress increases depolarization- evoked glutamate release in the rat prefrontal/frontal cortex: the dampening action of antidepressants PLoS One 5 2010 e8566
42. B. Myers, and B. Greenwood-Van Meerveld Corticosteroid receptor-mediated mechanisms in the amygdala regulate anxiety and colonic sensitivity Am. J. Physiol. Gastrointest. Liver. Physiol. 292 2007 G1622 G1629
43. R.M. Nesse Proximate and evolutionary studies of anxiety, stress and depression: synergy at the interface Neurosci. Biobehav. Rev. 23 1999 895 903
44. T.A. O'Leary, D.J. Rohsenow, R. Martin, S.M. Colby, C.A. Eaton, and P.M. Monti The relationship between anxiety levels and outcome of cocaine abuse treatment Am. J. Drug Alcohol Abuse 26 2000 179 194 (Pubitemid 30366624)
45. V.A. Redila, and C. Chavkin Stress-induced reinstatement of cocaine seeking is mediated by kappa opioid system Psychopharmacology 200 2008 59 70
46. J. Rochford, S. Beaulieu, I. Rousse, J.R. Glowa, and N. Barden Behavioral reactivity to aversive stimuli in a transgenic mouse model of impaired glucocorticoid (type II) receptor function: effects of diazepam and FG-7142 Psychopharmacology (Berl) 132 1997 145 152 (Pubitemid 27338989)
47. P. Salchner, S.B. Sartori, C. Sinner, A. Wigger, E. Frank, R. Landgraf, and N. Singewald Airjet and FG-7142-induced fos expression differs in rats selectively bred for high and low anxiety-related behavior Neuropharmacology 50 2006 1048 1058 (Pubitemid 43794907)
48. N. Salomé, P. Salchner, O. Viltart, H. Sequeira, A. Wigger, R. Landgraf, and N. Singewald Neurobiological correlates of high (HAB) versus low anxiety-related behavior (LAB): differential Fos expression in HAB and LAB rats Biol. Psychiatry 55 2004 715 723 (Pubitemid 38376183)
49. R.M. Sapolsky, S. Zola-Morgan, and L.R. Squire Inhibition of glucocorticoid secretion by the hippocampal formation in the primate J. Neurosci. 11 1991 3695 3704
50. W.J. Schwartz, and P. Zimmerman Circadian timekeeping in BALB/c and C57BL/6 inbred mouse strains J. Neurosci. 10 1990 3685 3694
51. Y.B. Sim, S.H. Park, Y.J. Kang, S.M. Kim, J.K. Lee, J.S. Jung, and H.W. Suh The regulation of blood glucose level in physical and emotional stress models: possible involvement of adrenergic and glucocorticoid systems Arch. Pharm. Res. 33 2010 1679 1683
52. J.P. Smith, and S.W. Book Comorbidity of generalized anxiety disorder and alcohol use disorders among individuals seeking outpatient substance abuse treatment Addict. Behav. 35 2010 42 45
53. J.W. Smythe, D. Murphy, C. Timothy, and B. Costall Hippocampal mineralocorticoid, but not glucocorticoid, receptors modulate anxiety-like behavior in rats Pharmacol. Biochem. Behav. 56 1997 507 513 (Pubitemid 27145833)
54. F. Teixeira-Silva, F. Dias Antunes, P.R. Santos Silva, T.C. Goes, E.C. Dantas, M.F. Santiago, and R. Machado de Andrade The free-exploratory paradigm as a model of trait anxiety in rats: test-retest reliability Physiol. Behav. 96 2009 729 734
55. A. Troisi The concept of alternative strategies and its relevance to psychiatry and clinical psychology Neurosci. Biobehav. Rev. 29 2005 159 168 (Pubitemid 40094585)
56. F. Tronche, C. Kellendonk, O. Kretz, P. Gass, K. Anlag, P.C. Orban, R. Bock, R. Klein, and G. Schütz Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety Nat. Genet. 23 1999 99 103 (Pubitemid 29418797)
57. T.M. Tzschentke Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues Prog. Neurobiol. 56 1998 613 672 (Pubitemid 29012461)
58. M.J. Webster, M.B. Knable, J. O'Grady, J. Orthmann, and C.S. Weickert Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders Mol. Psychiatry 7 2002 985 994 (Pubitemid 35333054)
59. Q. Wei, X.Y. Lu, L. Liu, G. Schafer, K.R. Shieh, S. Burke, T.E. Robinson, S.J. Watson, A.F. Seasholtz, and H. Akil Glucocorticoid receptor overexpression in forebrain: a mouse model of increased emotional lability Proc. Natl. Acad. Sci. U S A 101 2004 11851 11856 (Pubitemid 39095383)
60. S. Wust, E.F. Van Rossum, I.S. Federenko, J.W. Koper, R. Kumsta, and D.H. Hellhammer Common polymorphisms in the glucocorticoid receptor gene are associated with adrenocorticalresponses to psychosocial stress J. Clin. Endocrinol. Metab. 89 2004 565 573 (Pubitemid 38269859)
61. D. Xu, A. Buehner, J. Xu, T. Lambert, C. Nekl, M.K. Nielsen, and Y. Zhou A polymorphic glucocorticoid receptor in a mouse population may explain inherited altered stress response and increased anxiety-type behaviors FASEB J. 20 2006 2414 2416
62. A.A. Zozulya, M.V. Gabaeva, O.Y. Sokolov, I.D. Surkina, and N.V. Kost Personality, coping style, and constitutional neuroimmunology J. Immunotoxicol. 5 2008 221 225 (Pubitemid 351882415)