Shifts in hormonal stress reactivity during adolescence are not associated with changes in glucocorticoid receptor levels in the brain and pituitary of male rats

Developmental Neuroscience

Volumn 36, Issue 3-4, 2014, Pages 261-268

  Dziedzic, Noelle ^a   Ho, Amy ^a   Adabi, Bita ^a   Foilb, Allison R ^a   Romeo, Russell D ^a  

^a Program on US Russia Relations at Columbia s Harriman Institute   (United States)

Author keywords

Hypothalamic pituitary adrenal axis; Negative feedback; Puberty

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; GLUCOCORTICOID RECEPTOR; HORMONE; TESTOSTERONE;

ADOLESCENCE; ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; CORRELATION ANALYSIS; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; HIPPOCAMPUS; HORMONE METABOLISM; HORMONE RESPONSE; HYPOPHYSIS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; MALE; NEGATIVE FEEDBACK; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPRAGUE DAWLEY RAT; STRESS; WESTERN BLOTTING; DENTATE GYRUS; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; PARAVENTRICULAR THALAMIC NUCLEUS; PREPUBERTY; TESTOSTERONE BLOOD LEVEL; AGING; ANIMAL; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; METABOLISM; PSYCHOLOGY;

ADRENOCORTICOTROPIC HORMONE; AGING; ANIMALS; BRAIN; CORTICOSTERONE; HIPPOCAMPUS; HORMONES; MALE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY GLAND; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; STRESS, PSYCHOLOGICAL;

EID: 84906936199     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000362873     Document Type: Article

References (55)

1. McEwen BS: Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 2007; 87: 873-904
2. Ulrich-Lai YM, Herman JP: Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009; 10: 397-409
3. Roozendaal B: Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 2000; 25: 213-238
4. Sapolsky RM, Romero LM, Munck AU: How do glucocorticoids influence stress responses?. Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 2000; 21: 55-89
5. Dhabhar FS: Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulation 2009; 16: 300-317
6. McEwen BS, Stellar E: Stress and the individual: Mechanisms leading to disease. Arch Intern Med 1993; 153: 2093-2101
7. McEwen BS: Mood disorders and allostatic load. Biol Psychiatry 2003; 54: 200-207
8. Sapolsky RM: Glucocorticoids, stress, and their adverse neurological effects: Relevance to aging. Exp Gerontol 1999; 34: 721-732
9. Herbert J, Goodyer I, Grossman AB, Hastings MH, De Kloet ER, Lightman SL, Lupien SJ, Roozendaal B, Seckl JR: Do corticosteroids damage the brain?. J Neuroendocrinol 2006; 18: 393-411
10. McEwen BS: Protection and damage from acute and chronic stress: Allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann NY Acad Sci 2004; 1032: 1-7
11. Van Praag HM: Can stress cause depression?. Prog Neuropsychopharmacol Biol Psychiatry 2004; 28: 891-907
12. McEwen BS: Glucocorticoids, depression, and mood disorders: Structural remodeling in the brain. Metabol Clin Exp 2005; 54: 20-23
13. Romeo RD: Adolescence: A central event in shaping stress reactivity. Dev Psychobiol 2010; 52: 244-253
14. Romeo RD: Pubertal maturation and programming of hypothalamic-pituitary- Adrenal reactivity. Front Neuroendocrinol 2010; 31: 232-240
15. McCormick CM, Mathews IZ: HPA function in adolescence: Role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 2007; 86: 220-233
16. McCormick CM: An animal model of social instability stress in adolescence and risk for drugs of abuse. Physiol Behav 2010; 99: 194-203
17. Dahl RE, Gunnar MR: Heightened stress responsiveness and emotional reactivity during pubertal maturation: Implications for psychopathology. Dev Psychopathol 2009; 21: 1-6
18. 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
19. 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
20. 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
21. Romeo RD, Lee SJ, McEwen BS: Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology 2004; 80: 387-393
22. 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
23. 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
24. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP: Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 2009; 97: 484-494
25. Foilb AR, Lui P, Romeo RD: The transformation of hormonal stress responses throughout puberty and adolescence. J Endocrinol 2011; 210: 391-398
26. Lui P, Padow VA, Franco D, Hall BS, Park B, Klein ZA, Romeo RD: Divergent stress-induced neuroendocrine and behavioral responses prior to puberty. Physiol Behav 2012; 107: 104-111
27. Andersen SL: Trajectories of brain development: Point of vulnerability or window of opportunity. Neurosci Biobehav Rev 2003; 27: 3-18
28. McCormick CM, Green MR: From the stressed adolescent to the anxious and depressed adult: Investigations in rodent models. Neuroscience 2013; 249: 242-257
29. Gulley JM, Juraska JM: The effects of abused drugs on adolescent development of corticolimbic circuitry and behavior. Neuroscience 2013; 249: 3-20
30. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M: Brain corticosteroid receptor balance in health and disease. Endocr Rev 1998; 19: 269-301
31. Furay AR, Bruestle AE, Herman JP: The role of the forebrain glucocorticoid receptor in acute and chronic stress. Endocrinology 2008; 149: 5482-5490
32. Van Haarst AD, Oitzl MS, Workel JO, De Kloet ER: Chronic brain glucocorticoid receptor blockade enhances the rise in circadian and stress-induced pituitary-Adrenal activity. Endocrinology 1996; 137: 4935-4943
33. Meaney MJ, Sapolsky RM, McEwen BS: The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Dev Brain Res 1985; 18: 159-164
34. Vazquez DM: Stress and the developing limbic-hypothalamic-pituitary- Adrenal axis. Psychoneuroendocrinology 1998; 23: 663-700
35. Romeo RD, Ali FS, Karatsoreos IN, Bellani R, Chhua N, Vernov M, McEwen BS: Glucocorticoid receptor mRNA expression in the hippocampal formation of male rats before and after pubertal development in response to acute or repeated stress. Neuroendocrinology 2008; 87: 160-167
36. Perlman WR, Webster MJ, Herman MM, Kleinman JE, Weickert CS: Age-related differences in glucocorticoid receptor mRNA levels in the human brain. Neurobiol Aging 2007; 28: 447-458
37. Pryce CR: Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: Inter-species and intra-species differences. Brain Res Rev 2008; 57: 596-605
38. 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
39. Spear LP: The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000; 24: 417-463
40. Herman JP, Cullinan WE: Neurocircuitry of stress: Central control of the hypothalamo-pituitary- Adrenocortical axis. Trend Neurosci 1997; 20: 78-84
41. Dong Y, Poellinger L, Gustafsson JA, Okret S: Regulation of glucocorticoid receptor expression: Evidence for transcriptional and posttranslational mechanisms. Mol Endocrinol 1988; 2: 1256-1264
42. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates, ed 5. New York, Elsevier, 2005
43. Romeo RD, Richardson HN, Sisk CL: Puberty and the maturation of the male brain and sexual behavior: Recasting a behavioral potential. Neurosci Biobehav Rev 2002; 26: 379-389
44. Romeo RD: Puberty: A period of both organizational and activational effects of steroid hormones on neurobehavioral development. J Neuroendocrinol 2003; 15: 1185-1192
45. Romeo RD, Kaplowitz ET, Ho A, Franco D: The influence of puberty on stress reactivity and forebrain glucocorticoid receptor levels in inbred and outbred strains of male and female mice. Psychoneuroendocrinology 2013; 38: 592-596
46. 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
47. Conway-Campbell BL, McKenna MA, Wiles CC, Atkinson HC, De Kloet ER, Lightman SL: Proteasome-dependent down-regulation of activated nuclear hippocampal glucocorticoid receptors determines dynamic responses to corticosterone. Endocrinology 2007; 148: 5470-5477
48. Spencer RL, Kalman BA, Cotter CS, Deak T: Discrimination between changes in glucocorticoid receptor expression and activation in rat brain using Western blot analysis. Brain Res 2000; 868: 275-286
49. Mizoguchi K, Ikeda R, Shoji H, Tanaka Y, Maruyama W, Tabira T: Aging attenuates glucocorticoid negative feedback in rat brain. Neuroscience 2009; 159: 259-270
50. Murphy EK, Spencer RL, Sipe KJ, Herman JP: Decrements in nuclear glucocorticoid receptor (GR) protein levels and DNA binding in aged rat hippocampus. Endocrinology 2002; 143: 1362-1370
51. 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
52. Spiga F, Lightman SL: Dose-dependent effects of corticosterone on nuclear glucocorticoid receptors and their binding to DNA in the brain and pituitary of the rat. Brain Res 2009; 1293: 101-107
53. 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
54. Tritos N, Kitraki E, Philippidis H, Stylianopoulou F: Neurotransmitter modulation of glucocorticoid receptor mRNA levels in the rat hippocampus. Neuroendocrinology 1999; 69: 324-330
55. Caudal D, Jay TM, Godsil BP: Behavioral stress induces regionally distinct shift of brain mineralocorticoid and glucocorticoid receptor levels. Front Behav Neurosci 2014; 8: 19.