Stressor exposure of male and female juvenile mice influences later responses to stressors: Modulation of GABA A receptor subunit mRNA expression

Neuroscience

Volumn 215, Issue , 2012, Pages 114-126

  Jacobson Pick, S ^a   Audet, M C ^a   McQuaid, R J ^a   Kalvapalle, R ^a   Anisman, H ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

Female; GABA; Juvenile; Male; Receptor; Stress

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA3; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA5; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; CORTICOSTERONE; MESSENGER RNA;

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2 GENE; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA3 GENE; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA5 GENE; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2 GENE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; AROUSAL; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EXPOSURE; FEMALE; GENE EXPRESSION; GENE FUNCTION; IMPULSIVENESS; JUVENILE ANIMAL; MALE; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RECEPTOR GENE; RECEPTOR UPREGULATION; SEX DIFFERENCE; SOCIAL BEHAVIOR; STRESS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN; CORTICOSTERONE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MAZE LEARNING; MICE; PROTEIN SUBUNITS; REACTION TIME; RECEPTORS, GABA-A; RNA, MESSENGER; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 84861792289     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.04.038     Document Type: Article

References (79)

1. Altemus M. Sex differences in depression and anxiety disorders: potential biological determinants. Horm Behav 2006, 50:534-538.
2. Andersen S.L. Trajectories of brain development: point of vulnerability or window of opportunity?. Neurosci Biobehav Rev 2003, 27(1-2):3-18.
3. Andersen S.L., Teicher M.H. Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse. Neurosci Biobehav Rev 2009, 33(4):516-524.
4. Anisman H., Merali Z., Hayley S. Sensitization associated with stressors and cytokine treatments. Brain Behav Immun 2003, 17(2):86-93.
5. Anisman H., Gibb J., Hayley S. Influence of continuous infusion of interleukin-1beta on depression-related processes in mice. Corticosterone, circulating cytokines, brain monoamines, and cytokine mRNA expression. Psychopharmacology 2008, 199(2):231-244.
6. Audet M.C., Anisman H. Neuroendocrine and neurochemical impact of aggressive social interactions in submissive and dominant mice. Implications for stress-related disorders. Int J Neuropsychopharmacol 2010, 13(3):361-372.
7. Audet MC, Jacobson S, Anisman H (2009) Social defeat in mice promotes desensitized corticosterone release but sensitized prefrontal cytokine expression upon subsequent aggressive challenge. In: Poster presented at the Annual Meeting of the Society for Neuroscience, Chicago, IL, USA.
8. Audet M.C., Mangano E.N., Anisman H. Behavior and pro-inflammatory cytokine variations among submissive and dominant mice engaged in aggressive encounters: moderation by corticosterone reactivity. Front Behav Neurosci 2010, 4:156. pii.
9. Avital A., Richter-Levin G. Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int J Neuropsychopharmacol 2005, 8:163-173.
10. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., Graham D., Tsankova N.M., Bolanos C.A., Rios M., Monteggia L.M., Self D.W., Nestler E.J. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311(5762):864-868.
11. Biggo G., Costa E. GABA and benzodiazepine receptor subtypes 1990, Raven Press, New York.
12. Boda E., Pini A., Hoxha E., Parolisi R., Tempia F. Selection of reference genes for quantitative real-time RT-PCR studies in mouse brain. J Mol Neurosci 2009, 37:238-253.
13. Brown K.J., Grunberg N.E. Effects of housing on male and female rats: crowding stresses male but calm females. Physiol Behav 1995, 58(6):1085-1089.
14. Buynitsky D.I., Mostofsky T. Restraint stress in biobehavioral research: recent developments. Neurosci Biobehav Rev 2009, 33(7):1089-1098.
15. Chisari A., Carino M., Perone M., Gaillard R.C., Spinedi E. Sex and strain variability in the rat hypothalamo-pituitary-adrenal (HPA) axis function. J Endocrinol Invest 1995, 18(1):25-33.
16. Costa E. From GABAA receptor diversity emerges a unified vision of GABAergic inhibition. Annu Rev Pharmacol Toxicol 1998, 38:321-350.
17. Crestani F., Lorez M., Baer K., Essrich C., Benke D., Laurent J.P., Belzung C., Fritschy J.M., Lüscher B., Mohler H. Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 1999, 2(9):833-839.
18. De Boer S.F., Slanger J.L., Van der Guther J. Brain benzodiazepine receptor control of stress hormones. Stress neuroendocrine and molecular approaches 1995, 719-734. Gordon and Breach, Philadelphia. R. (Kvetnansky, R. McCarty, J. Axelrod (Eds.).
19. Doremus-Fitzwater T.L., Varlinskaya E.I., Spear L.P. Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 2009, 97(3-4):484-494.
20. Douglas L.A., Varlinskaya E.I., Spear L.P. Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation. Physiol Behav 2003, 80(2-3):317-325.
21. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., Raichle M.E. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997, 386:824-827.
22. DuBois D.W., Perlegas A., Floyd D.W., Weiner J.L., McCool B.A. Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57BL/6J and DBA/2J mice. J Pharmacol Exp Ther 2006, 318(2):629-640.
23. Earls F. Sex differences in psychiatric disorders: origins and developmental influences. Psychiatr Dev 1987, 5(1):1-23.
24. Earnheart J.C., Schweizer C., Crestani F., Iwasato T., Itohara S., Mohler H., Lüscher B. GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxiety and depression states. J Neurosci 2007, 27(14):3845-3854.
25. Eser D., Baghai T.C., Schüle C., Nothdurfter C., Rupprecht R. Neuroactive steroids as endogenous modulators of anxiety. Curr Pharm Des 2008, 14(33):3525-3533. Review.
26. Franklin K.B.J., Paxinos G. A stereotaxic atlas of the mouse brain 1997, Academic Press, San Diego, CA.
27. Galanopoulou A.S. Sex- and cell-type-specific patterns of GABAA receptor and estradiol-mediated signaling in the immature rat Substantia nigra. Eur J Neurosci 2006, 23(9):2423-2430.
28. Gibb J., Hayley S., Gandhi R., Poulter M.O., Anisman H. Synergistic and additive actions of a psychosocial stressor and endotoxin challenge: circulating and brain cytokines, plasma corticosterone and behavioral changes in mice. Brain Behav Immun 2008, 22(4):573-589.
29. Gibb J., Hayley S., Poulter M.O., Anisman H. Effects of stressors and immune activating agents on peripheral and central cytokines in mouse strains that differ in stressor responsivity. Brain Behav Immun 2011, 25(3):468-482.
30. Goel N., Bale T.L. Examining the intersection of sex and stress in modelling neuropsychiatric disorders. J Neuroendocrinol 2009, 21(4):415-420.
31. Gulinello M., Gong Q.H., Li X., Smith S.S. Short-term exposure to a neuroactive steroid increases alpha4 GABA(A) receptor subunit levels in association with increased anxiety in the female rat. Brain Res 2001, 910(1-2):55-66.
32. Gutkowska J., Paquette A., Wang D., Lavoie J.M., Jankowski M. Effect of exercise training on cardiac oxytocin and natriuretic peptide systems in ovariectomized rats. Am J Physiol Regul Integr Comp Physiol 2007, 293:R267-R275.
33. Haller J., Fuchs E., Halász J., Makara G.B. Defeat is a major stressor in males while social instability is stressful mainly in females: towards the development of a social stress model in female rats. Brain Res Bull 1999, 50(1):33-39.
34. Handa R.J., Burgess L.H., Kerr J.E., O'Keefe J.A. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 1994, 28:464-476.
35. Haney M., Miczek K.A. Ultrasounds during agonistic interactions between female rats (Rattus norvegicus). J Comp Psychol 1993, 107(4):373-379.
36. Jacobson-Pick S., Richter-Levin G. Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behav Brain Res 2010, 214(2):268-276.
37. Jacobson-Pick S., Elkobi A., Vander S., Rosenblum K., Richter-Levin G. Juvenile stress-induced alteration of maturation of the GABAA receptor alpha subunit in the rat. Int J Neuropsychopharmacol 2008, 11(7):891-903.
38. Jacobson-Pick S., Audet M.C., Nathoo N., Anisman H. Stressor experiences during the juvenile period increase stressor responsivity in adulthood: transmission of stressor experiences. Behav Brain Res 2011, 216(1):365-574.
39. Johnson J.D., O'Connor K.A., Watkins L.R., Maier S.F. The role of IL-1beta in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 2004, 127(3):569-577.
40. A receptor binding in rat brain measured by an improved in vitro binding assay. Exp Brain Res 1990, 81(2):297-302.
41. Kalueff A.V., Nutt D.J. Role of GABA in anxiety and depression. Depress Anxiety 2007, 24(7):495-517.
42. Keeney A., Jessop D.S., Harbuz M.S., Marsden C.A., Hogg S., Blackburn-Munro R.E. Differential effects of acute and chronic social defeat stress on hypothalamic-pituitary-adrenal axis function and hippocampal serotonin release in mice. J Neuroendocrinol 2006, 18(5):330-338.
43. Kessler R.C., McGonagle K.A., Swartz M., Blazer D.G., Nelson C.B. Sex and depression in the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence. J Affect Disord 1993, 29(2-3):85-96.
44. Klempan T.A., Sequeira A., Canetti L., Lalovic A., Ernst C., ffrench-Mullen J., Turecki G. Altered expression of genes involved in ATP biosynthesis and GABAergic neurotransmission in the ventral prefrontal cortex of suicides with and without major depression. Mol Psychiatry 2009, 14(2):175-189.
45. Krystal J.H., Sanacora G., Blumberg H., Anand A., Charney D.S., Marek G., Epperson C.N., Goddard A., Mason G.F. Glutamate and GABA systems as targets for novel antidepressant and mood-stabilizing treatments. Mol Psychiatry 2002, 1:S71-80.
46. Kultas-Ilinsky K., Leontiev V., Whiting P.J. Expression of 10 GABA(A) receptor subunit messenger RNAs in the motor-related thalamic nuclei and basal ganglia of Macaca mulatta studied with in situ hybridization histochemistry. Neuroscience 1998, 85(1):179-204.
47. LeDoux J. The amygdala. Curr Biol 2007, 17(20):R868-74. Review.
48. Löw K., Crestani F., Keist R., Benke D., Brünig I., Benson J.A., Fritschy J.M., Rülicke T., Bluethmann H., Möhler H., Rudolph U. Molecular and neuronal substrate for the selective attenuation of anxiety. Science 2000, 290(5489):131-134.
49. Macdonald R.L., Olsen R.W. GABAA receptor channels. Annu Rev Neurosci 1994, 17:569-602.
50. McCormick C.M., Kehoe P., Kovacs S. Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization. Int J Dev Neurosci 1998, 16:175-185.
51. McKernan R.M., Rosahl T.W., Reynolds D.S., et al. Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABA(A) receptor alpha1 subtype. Nat Neurosci 2000, 3:587-592.
52. Menard J., Treit D. Effects of centrally administered anxiolytic compounds in animal models of anxiety. Neurosci Biobehav Rev 1999, 23(4):591-613.
53. Merali Z., Du L., Hrdina P., Palkovits M., Faludi G., Poulter M.O., Anisman H. Dysregulation in the suicide brain: mRNA expression of corticotropin-releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region. J Neurosci 2004, 24(6):1478-1485.
54. Merali Z., Khan S., Michaud D.S., Shippy S., Anisman H. Does amygdaloid corticotropin-releasing hormone (CRH) mediate anxiety-like behaviors? Dissociation of anxiogenic effects and CRH release. Eur J Neurosci 2004, 20:229-239.
55. Mitchell E.A., Herd M.B., Gunn B.G., Lambert J.J., Belelli D. Neurosteroid modulation of GABAA receptors: molecular determinants and significance in health and disease. Neurochem Int 2008, 52(4-5):588-595.
56. Mody I., Maguire J. The reciprocal regulation of stress hormones and GABA(A) receptors. Front Cell Neurosci 2011, 6:4.
57. Mohler H., Fritschy J.M., Rudolph U. A new benzodiazepine pharmacology. J Pharmacol Exp Ther 2002, 300:2-8.
58. Nikolaus S., Antke C., Beu M., Müller H.W. Cortical GABA, striatal dopamine and midbrain serotonin as the key players in compulsive and anxiety disorders - results from in vivo imaging studies. Rev Neurosci 2010, 21(2):119-139. Review.
59. Palanza P., Morley-Fletcher S., Laviola G. Novelty seeking in periadolescent mice. Sex differences and influence of intrauterine position. Physiol Behav 2001, 72(1-2):255-262.
60. Pirker S., Schwarzer C., Wieselthaler A., Sieghart W., Sperk G. GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 2000, 101(4):815-850.
61. Poulter M.O., Du L., Weaver I.C., Palkovits M., Faludi G., Merali Z., Szyf M., Anisman H. GABAA receptor promoter hypermethylation in suicide brain: implications for the involvement of epigenetic processes. Biol Psychiatry 2008, 64(8):645-652.
62. Poulter M.O., Du L., Zhurov V., Merali Z., Anisman H. Plasticity of the GABA(A) receptor subunit cassette in response to stressors in reactive versus resilient mice. Neuroscience 2010, 165(4):1039-1051.
63. Primus R.J., Kellogg C.K. Pubertal-related changes influence the development of environment-related social interaction in the male rat. Dev Psychobiol 1989, 22(6):633-643.
64. Prince C.R., Collins C., Anisman H. Stressor-provoked response patterns in a swim task: modification by diazepam. Pharmacol Biochem Behav 1986, 24(2):323-328.
65. Pritchett D.B., Luddens H., Seeburg P.H. Type I and type II GABAA-benzodiazepine receptors produced in transfected cells. Science 1989, 245:1389-1392.
66. Rico J.L., Ferraz D.B., Ramalho-Pinto F.J., Morato S. Neonatal exposure to LPS leads to heightened exploratory activity in adolescent rats. Behav Brain Res 2010, 215(1):102-109.
67. Rudolph U., Möhler H. Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 2004, 44:475-498.
68. Rudolph U., Crestani F., Benke D., Brünig I., Benson J.A., Fritschy J.M., Martin J.R., Bluethmann H., Möhler H. Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 1999, 401(6755):796-800.
69. Sanders S.K., Shekhar A. Regulation of anxiety by GABAA receptors in the rat amygdala. Pharmacol Biochem Behav 1995, 52(4):701-706.
70. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3(6):1101-1108.
71. Seedat S., Scott K.M., Angermeyer M.C., Berglund P., Bromet E.J., Brugha T.S., Demyttenaere K., de Girolamo G., Haro J.M., Jin R., Karam E.G., Kovess-Masfety V., Levinson D., Mora M.E.D., Ono Y., Ormel J., Pennell B.E., Posada-Villa J., Sampson N.A., Williams D., Kessler R.C. Cross-National Associations between Gender and Mental Disorders in the World Health Organization World Mental Health Surveys. Arch Gen Psychiatry 2009, 66(7):785-795.
72. Sequeira A., Mamdani F., Ernst C., Vawter M.P., Bunney W.E., Lebel V., Rehal S., Klempan T., Gratton A., Benkelfat C., Rouleau G.A., Mechawar N., Turecki G. Global brain gene expression analysis links glutamatergic and GABAergic alterations to suicide and major depression. PLoS One 2009, 4(8):e6585.
73. Sgoifo D., Stilli S., Parmigiani B., Aimi Musso.E. Maternal aggression as a model for acute social stress in the rat: a behavioral-electrocardiographic study. Aggressive Behav 1995, 21:78-89.
74. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24(4):417-463.
75. Tamashiro K.L., Nguyen M.M., Sakai R.R. Social stress: from rodents to primates. Front Neuroendocrinol 2005, 26(1):27-40.
76. Tsoory M., Cohen H., Richter-Levin G. Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol 2007, 17:245-256.
77. Varlinskaya E.I., Spear L.P. Social interactions in adolescent and adult Sprague-Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res 2008, 188(2):398-405.
78. Vialou V., Maze I., Renthal W., LaPlant Q.C., Watts E.L., Mouzon E., Ghose S., Tamminga C.A., Nestler E.J. Serum response factor promotes resilience to chronic social stress through the induction of Delta Fos B. J Neurosci 2010, 30(43):14585-14592.
79. Vom Saal F.S., Franks P., Boechler M., Palanza P., Parmigiani S. Nest defense and survival of offspring in highly aggressive wild Canadian female house mice. Physiol Behav 1995, 58(4):669-678.