Glucocorticoid receptor mRNA expression in the hippocampal formation of male rats before and after pubertal development in response to acute or repeated stress

Neuroendocrinology

Volumn 87, Issue 3, 2008, Pages 160-167

  Romeo, Russell D ^a,b   Ali, Ferhina S ^a   Karatsoreos, Ilia N ^a   Bellani, Rudy ^a   Chhua, Nara ^a   Vernov, Mary ^a   McEwen, Bruce S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b Barnard College of Columbia University   (United States)

Author keywords

Adolescence; CA1; Dentate Gyrus; HPA axis; Restraint

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; CELL MATURATION; CHRONIC STRESS; CONTROLLED STUDY; DENSITOMETRY; DENTATE GYRUS; DISSOCIATION; HIPPOCAMPUS; MALE; NONHUMAN; PREPUBERTY; PRIORITY JOURNAL; PUBERTY; PYRAMIDAL NERVE CELL; QUALITATIVE ANALYSIS; RAT; STRESS; TRANSCRIPTION REGULATION;

AGE FACTORS; ANIMALS; CORTICOSTERONE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; STRESS; TIME FACTORS;

EID: 42449083252     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000109710     Document Type: Article

References (48)

1. Herman JP, Patel PD, Akil H, Watson SJ: Localization and regulation of glucocorticoid and mineralocorticoid receptor mRNAs in the hippocampal formation. Mol Endocrinol 1989;3:1886-1894.
2. Van Eekelen JAM, Jiang W, de Kloet ER, Bohn MC: Distribution of the mineralocorticoid and the glucocorticoid receptor mRNAs in the rat hippocampus. J Neurosci Res 1988;21:88-94.
3. Han F, Ozawa H, Matsuda K, Nishi M, Kawata M: Colocalization of mineralocorticoid receptor and glucocorticoid receptor in the hippocampus and hypothalamus. Neurosci Res 2005;51:371-381.
4. Reul JM, de Kloet ER: Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985;117:2505-2511.
5. Sapolsky RM, McEwen BS, Rainbow TC: Quantitative autoradiography of [3H]corticosterone receptors in rat brain. Brain Res 1983;271:331-334.
6. de Kloet ER, Vreugdenhil E, Oitzl MS, Joels M: Brain corticosteroid receptor balance in health and disease. Endocr Rev 1998;19:269-301.
7. Sapolsky RM, Krey L, McEwen BS: Glucocorticoid sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci USA 1984;81:6174-6177.
8. Jacobson L, Sapolsky RM: The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 1991;12:118-134.
9. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostander MM, Choi DC, Cullinan WE: Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamic-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 2003;24:151-180.
10. Herman JP, Mueller NK: Role of the ventral subiculum in stress integration. Behav Brain Res 2006;174:215-224.
11. McEwen BS: Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabol Clin Exp 2005;54:20-23.
12. Paskitti ME, McCreary BJ, Herman JP: Stress regulation of adrenocorticosteroid receptor gene transcription and mRNA expression in rat hippocampus: time-course analysis. Mol Brain Res 2000;80:142-152.
13. Nishimura K, Makino S, Tanaka Y, Kaneda T, Hashimoto K: Altered expression of p53 mRNA in the brain and pituitary during repeated immobilization stress: negative correlation with glucocorticoid receptor mRNA levels. J Neuroendocrinol 2004;16:84-91.
14. Tritos N, Kitraki E, Philippidis H, Stylianopoulou F: Neurotransmitter modulation of glucocorticoid receptor mRNA levels in the rat hippocampus. Neuroendocrinology 1999;69:324-330.
15. Liberzon I, Lopez JF, Flagel SB, Vazquez DM, Young EA: Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: relevance to post-traumatic stress disorder. Stress 1999;11:11-17.
16. Makino S, Smith MA, Gold PW: Increased expression of corticotropin- releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology 1995;136:3299-3309.
17. Meyer G, Ferres-Torres R, Mas M: The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study. Brain Res 1978;155:108-112.
18. Giedd JN, Vaituzis AC, Hamburger SD, Lange N, Rajapakse JC, Kaysen D, Vauss YC, Rapoport JL: Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. J Comp Neurol 1996;366:223-230.
19. Isgor C, Kabbaj M, Akil H, Watson SJ: Delayed effects of chronic variable stress during peripubertal-juvenile period of hippocampal morphology and on cognitive and stress axis function in rats. Hippocampus 2004;14:636-648.
20. Romeo RD, McEwen BS: Stress and the adolescent brain. Ann NY Acad Sci 2006;1094:202-214.
21. Gomez F, Manalo S, Dallman MF: Androgen-sensitive changes in regulation of restraint-induced adrenocorticotropin secretion between early and late puberty in male rats. Endocrinology 2004;145:59-70.
22. Di Luigi L, Guidetti L, Baldari C, Gallotta MC, Sgro P, Perroni F, Romanelli F, Lenzi A: Cortisol, dehydroepiandrosterone sulphate and dehydroepiandrosterone sulphate/cortisol ratio responses to physical stress in males are influenced by pubertal development. J Endocrinol Invest 2006;29:796-804.
23. McCormick CM, Merrick A, Secen J, Helmreich DL: Social instability in adolescence alters the central and peripheral hypothalamic-pituitary-adrenal responses to a repeated homotypic stressor in male and female rats. J Neuroendocrinol 2006;19:116-126.
24. Gomez F, Houshyar H, Dallman MF: Marked regulatory shifts in gonadal, adrenal, and metabolic system responses to repeated restraint stress occur within a 3-week period in prepubertal male rats. Endocrinology 2002;143:2852-2862.
25. Viau V, Bingham B, Davis J, Lee P, Wong M: Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat. Endocrinology 2005;146:137-146.
26. Goldman L, Winget C, Hollingshead GW, Levine S: Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 1973;12:199-211.
27. Vazquez DM, Akil H: Pituitary-adrenal response to ether vapor in the weanling animal: characterization of the inhibitory effect of glucocorticoids on adrenocorticotropin secretion. Pediatr Res 1993;34:646-653.
28. Romeo RD, Lee SJ, Chhua N, McPherson CR, McEwen BS: Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 2004;79:125-132.
29. Romeo RD, Bellani R, Karatsoreos IN, Chhua N, Vernov M, Conrad CD, McEwen BS: Stress history and pubertal development interact to shape hypothalamic pituitary adrenal axis plasticity. Endocrinology 2006;147:1664-1674.
30. Romeo RD, Karatsoreos IN, McEwen BS: Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor. Horm Behav 2006;50:463-468.
31. Romeo RD, Lee SJ, McEwen BS: Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology 2004;80:387-393.
32. Döhler KD, Wuttke W: Changes with age in levels of serum gonadotropins, prolactin, and gonadal steroids in prepubertal male and female rats. Endocrinology 1975;97:898-907.
33. Romeo RD, Karatsoreos IN, Jasnow AM, McEwen BS: Age- and stress-induced changes in corticotropin-releasing hormone mRNA expression in the paraventricular nucleus of the hypothalamus. Neuroendocrinology 2007;85:199-206.
34. Romeo RD, Fossella JA, Bateup HS, Sisti HM, Brake WG, McEwen BS: Maternal separation suppresses TGFα mRNA expression in the prefrontal cortex of male and female neonatal C57BL/6 mice. Dev Brain Res 2004;152:73-77.
35. Paxinos G, Watson, C: The Rat Brain in Stereotaxic Atlas, 2nd ed. London, Academic Press, 1986.
36. Vazquez DM: Stress and the developing limbic-hypothalamic-pituitary- adrenal axis. Psychoneuroendocrinology 1998;23:663-700.
37. Herman JP, Watson SJ, Spencer RL: Defense of adrenocorticosteroid receptor expression in rat hippocampus: effects of stress and strain. Endocrinology 1999;140:3981-3991.
38. Herman JP, Cullinan WE: Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997;20:78-84.
39. Fonte C, Grenier J, Trousson A, Chauchereau A, Lahuna O, Baulieu EE, Schumacher M, Massaad C: Involvement of beta-catenin and unusual behavior of CBP and P300 in glucocorticosterone signaling in Schwann cells. Proc Natl Acad Sci USA 2005;102:14260-14265.
40. Grenier J, Trousson A, Chauchereau A, Cartaud J, Schumacher M, Massaad C: Differential recruitment of p160 coactivators by glucocorticoid receptor between Schwann cells and astrocytes. Mol Endocrinol 2006;20:254-267.
41. Meijer OC, van der Laan S, Lachize S, Steenbergen PJ, de Kloet ER: Steroid receptor coregulation diversity: what can it mean for the stressed brain? Neuroscience 2006;138:891-899.
42. Pace TWW, Spencer RL: Disruption of mineralocorticoid receptor function increases corticosterone responding to a mild, but not moderate, psychological stressor. Am J Physiol 2005;288:E1082-E1088.
43. Sapolsky RM: Stress and plasticity in the limbic system. Neurochem Res 2003;28:1735-1742.
44. McEwen BS, Margarinos AM: Stress effects on morphology and function of the hippocampus. Ann NY Acad Sci 1997;821:271-284.
45. McEwen BS, Milner TA: Hippocampal formation: shedding light on the influence of sex and stress on the brain. Brain Res Rev; in press.
46. Watanabe Y, Gould E, McEwen BS: Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992;588:341-345.
47. Magarinos AM, McEwen BS: Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 1995;69:83-88.
48. Pham K, Nacher J, Hof PR, McEwen BS: Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in adult rat dentate gyrus. Eur J Neurosci 2003;17:879-886.