A direct androgenic involvement in the expression of human corticotropin-releasing hormone

Molecular Psychiatry

Volumn 11, Issue 6, 2006, Pages 567-576

  Bao, A M ^a,b   Fischer, D F ^a,c,e   Wu, Y H ^a   Hol, E M ^a   Balesar, R ^a   Unmehopa, U A ^a   Zhou, J N ^d   Swaab, D F ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^e Galapagos Genomics   (Netherlands)

Author keywords

Androgen receptor; Androgen responsive element; Corticotropin releasing hormone; Hypothalamic pituitary adrenal axis

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CORTICOTROPIN RELEASING FACTOR; TESTOSTERONE;

ADULT; AGED; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; FEMALE; HORMONE ACTION; HORMONE BINDING; HORMONE RECEPTOR INTERACTION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN TISSUE; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; MOOD DISORDER; NERVE CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROMOTER REGION; THALAMUS MIDLINE NUCLEUS;

ADULT; AGED; AGED, 80 AND OVER; CORTICOTROPIN-RELEASING HORMONE; FEMALE; HUMANS; MALE; MIDDLE AGED; MOOD DISORDERS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RECEPTORS, ANDROGEN; RESPONSE ELEMENTS; TESTOSTERONE; TISSUE DISTRIBUTION;

EID: 33745712835     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/sj.mp.4001800     Document Type: Article

References (82)

1. Swaab DF. The human hypothalamus. In: Aminoff MJ, Boller F, Swaab DF (eds). Basic and Clinical Aspects. Part I: Nuclei of the hypothalamus, Handbook of Clinical Neurology. Elsevier: Amsterdam, 2003 p 476.
2. Holsboer F, Barden N. Antidepressants and hypothalamic-pituitary- adrenocortical regulation. Endocr Rev 1996; 17: 187-205.
3. Swaab DF, Fliers E, Hoogendijk WJ, Veltman DJ, Zhou JN. Interaction of prefrontal cortical and hypothalamic systems in the pathogenesis of depression. Prog Brain Res 2000; 126: 369-396.
4. Bissette G. Central nervous system CRF in stress: radioimmunoassay studies. In: De Souza E, Nemeroff CB (eds). Corticotropin-Releasing Factor: Basic and Clinical Studies of a Neuropeptide. CRC-Press: Boca Raton, Fl, USA, 1990 pp 21-28.
5. Shea A, Walsh C, Macmillan H, Steiner M. Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 2005; 30: 162-178.
6. Lehtinen V, Joukamaa M. Epidemiology of depression: prevalence, risk factors and treatment situation. Acta Psychiatr Scand Suppl 1994; 377: 7-10.
7. Gold PW, Goodwin FK, Chrousos GP. Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (1). N Engl J Med 1988; 319: 348-353.
8. Gold PW, Goodwin FK, Chrousos GP. Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (2). N Engl J Med 1988; 319: 413-420.
9. Haleem DJ, Kennett G, Curzon G. Adaptation of female rats to stress: shift to male pattern by inhibition of corticosterone synthesis. Brain Res 1988; 458: 339-347.
10. De Vries GJ, Buijs RM, Van Leeuwen FW. Sex differences in vasopressin and other neurotransmitter systems in the brain. Prog Brain Res 1984; 61: 185-203.
11. Ahima RS, Harlan RE. Regulation of glucocorticoid receptor immunoreactivity in the rat hippocampus by androgenic-anabolic steroids. Brain Res 1992; 585: 311-314.
12. Pearlstein T, Rosen K, Stone AB. Mood disorders and menopause. Endocrinol Metab Clin North Am 1997; 26: 279-294.
13. Seale JV, Wood SA, Atkinson HC, Bate E, Lightman SL, Ingram CD et al. Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats. J Neuroendocrinol 2004; 16: 516-524.
14. Lund TD, Munson DJ, Haldy ME, Handa RJ. Androgen inhibits, while oestrogen enhances, restraint-induced activation of neuropeptide neurones in the paraventricular nucleus of the hypothalamus. J Neuroendocrinol 2004; 16: 272-278.
15. Kirschbaum C, Schommer N, Federenko I, Gaab J, Neumann O, Oellers M et al. Short-term estradiol treatment enhances pituitary-adrenal axis and sympathetic responses to psychosocial stress in healthy young men. J Clin Endocrinol Metab 1996; 81: 3639-3643.
16. Roy BN, Reid RL, Van Vugt DA. The effects of estrogen and progesterone on corticotropin-releasing hormone and arginine vasopressin messenger ribonucleic acid levels in the paraventricular nucleus and supraoptic nucleus of the rhesus monkey. Endocrinology 1999; 140: 2191-2198.
17. Kitay JI. Pituitary-adrenal function in the rat after gonadectomy and gonadal hormone replacement. Endocrinology 1963; 73: 253-260.
18. Ramaley JA. Effects of ovariectomy on dexamethasone suppression of the adrenal axis in adult rats. Neuroendocrinology 1976; 20: 260-269.
19. Phillips JG, Poolsanguan W. A method to study temporal changes in adrenal activity in relation to sexual status in the female laboratory rat. J Endocrinol 1978; 77: 283-291.
20. Jacobs AJ, Odom MJ, Word RA, Carr BR. Effect of oral contraceptives on adrenocorticotropin and growth hormone secretion following CRH and GHRH administration. Contraception 1989; 40: 691-699.
21. Hellman L, Yoshida K, Zumoff B, Levin J, Kream J, Fukushima DK. The effect of medroxyprogesterone acetate on the pituitary-adrenal axis. J Clin Endocrinol Metab 1976; 42: 912-917.
22. Bao AM, Hestiantoro A, Van Someren EJ, Swaab DF, Zhou JN. Colocalization of corticotropin-releasing hormone and oestrogen receptor-alpha in the paraventricular nucleus of the hypothalamus in mood disorders. Brain 2005; 128: 1301-1313.
23. Vamvakopoulos NC, Chrousos GP. Evidence of direct estrogenic regulation of human corticotropin-releasing hormone gene expression. Potential implications for the sexual dimophism of the stress response and immune/inflammatory reaction. J Clin Invest 1993; 92: 1896-1902.
24. Le Mevel JC, Abitbol S, Beraud G, Maniey J. Dynamic changes in plasma adrenocorticotrophin after neurotropic stress in male and female rats. J Endocrinol 1978; 76: 359-360.
25. Le Mevel JC, Abitbol S, Beraud G, Maniey J. Temporal changes in plasma adrenocorticotropin concentration after repeated neurotropic stress in male and female rats. Endocrinology 1979; 105: 812-817.
26. Kant GJ, Lenox RH, Bunnell BN, Mougey EH, Pennington LL, Meyerhoff JL. Comparison of stress response in male and female rats: pituitary cyclic AMP and plasma prolactin, growth hormone and corticosterone. Psychoneuroendocrinology 1983; 8: 421-428.
27. Su TP, Pagliaro M, Schmidt PJ, Pickar D, Wolkowitz O, Rubinow DR. Neuropsychiatric effects of anabolic steroids in male normal volunteers. JAMA 1993; 269: 2760-2764.
28. Pope Jr HG, Kouri EM, Hudson JI. Effects of supraphysiologic doses of testosterone on mood and aggression in normal men: a randomized controlled trial. Arch Gen Psychiatry 2000; 57: 133-140; discussion 155-156.
29. Pope Jr HG, Cohane GH, Kanayama G, Siegel AJ, Hudson JI. Testosterone gel supplementation for men with refractory depression: a randomized, placebo-controlled trial. Am J Psychiatry 2003; 160: 105-111.
30. Rabkin JG, Wagner GJ, Rabkin R. A double-blind, placebo-controlled trial of testosterone therapy for HIV-positive men with hypogonadal symptoms. Arch Gen Psychiatry 2000; 57: 141-147; discussion 155-156.
31. Seidman SN, Spatz E, Rizzo C, Roose SP. Testosterone replacement therapy for hypogonadal men with major depressive disorder: a randomized, placebo-controlled clinical trial. J Clin Psychiatry 2001; 62: 406-412.
32. Heuser I. Depression, endocrinologically a syndrome of premature aging? Maturitas 2002; 41(Suppl 1): S19-S23.
33. Barrett-Connor E, Von Muhlen DG, Kritz-Silverstein D. Bioavailable testosterone and depressed mood in older men: the Rancho Bernardo Study. J Clin Endocrinol Metab 1999; 84: 573-577.
34. Handa RJ, Nunley KM, Lorens SA, Louie JP, McGivern RF, Bollnow MR. Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol Behav 1994; 55: 117-124.
35. Viau V, Meaney MJ. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991; 129: 2503-2511.
36. Miesfeld RL. The structure and function of steroid receptor proteins. Crit Rev Biochem Mol Biol 1989; 24: 101-117.
37. Evans RM. The steroid and thyroid hormone receptor superfamily. Science 1988; 240: 889-895.
38. Fernandez-Guasti A, Kruijver FP, Fodor M, Swaab DF. Sex differences in the distribution of androgen receptors in the human hypothalamus. J Comp Neurol 2000; 425: 422-435.
39. van de Nes JA, Kamphorst W, Ravid R, Swaab DF. Comparison of beta-protein/A4 deposits and Alz-50-stained cytoskeletal changes in the hypothalamus and adjoining areas of Alzheimer's disease patients: amorphic plaques and cytoskeletal changes occur independently. Acta Neuropathol (Berlin) 1998; 96: 129-138.
40. Kruijver FP, Fernandez-Guasti A, Fodor M, Kraan EM, Swaab DF. Sex differences in androgen receptors of the human mamillary bodies are related to endocrine status rather than to sexual orientation or transsexuality. J Clin Endocrinol Metab 2001; 86: 818-827.
41. Raadsheer FC, Sluiter AA, Ravid R, Tilders FJ, Swaab DF. Localization of corticotropin-releasing hormone (CRH) neurons in the paraventricular nucleus of the human hypothalamus; age-dependent colocalization with vasopressin. Brain Res 1993; 615: 50-62.
42. Raadsheer FC, Hoogendijk WJ, Stam FC, Tilders FJ, Swaab DF. Increased numbers of corticotropin-releasing hormone expressing neurons in the hypothalamic paraventricular nucleus of depressed patients. Neuroendocrinology 1994; 60: 436-444.
43. Huitinga I, van der Cammen M, Salm L, Erkut Z, van Dam A, Tilders F et al. IL-1beta immunoreactive neurons in the human hypothalamus: reduced numbers in multiple sclerosis. J Neuroimmunol 2000; 107: 8-20.
44. van Oers JW, Tilders JH, Berkenbosch F. Characterization and biological activity of a rat monoclonal antibody to rat/human corticotropin-releasing factor. Endocrinology 1989; 124: 1239-1246.
45. Adams JC. Biotin amplification of biotin and horseradish peroxidase signals in histochemical stains. J Histochem Cytochem 1992; 40: 1457-1463.
46. Kruijver FP, Balesar R, Espila AM, Unmehopa UA, Swaab DF. Estrogen receptor-alpha distribution in the human hypothalamus in relation to sex and endocrine status. J Comp Neurol 2002; 454: 115-139.
47. Fischer DF, Backendorf C. Promoter analysis in the human SPRR gene family. Meth Mol Biol 2004; 289: 303-313.
48. Schreiber E, Matthias P, Muller MM, Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res 1989; 17: 6419.
49. DuBridge RB, Tang P, Hsia HC, Leong PM, Miller JH, Calos MP. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol Cell Biol 1987; 7: 379-387.
50. Graham FL, van der Eb AJ. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 1973; 52: 456-467.
51. Stephanou A, Melino G, Knight RA, Annicchiarico-Petruzzelli M, Sarlis NJ, Finazzi-Agro A et al. Interleukin-6 and corticotrophin-releasing hormone mRNA are modulated during differentiation of human neuroblastoma cells. Neuropeptides 1992; 23: 45-49.
52. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
53. Prins GS, Birch L, Greene GL. Androgen receptor localization in different cell types of the adult rat prostate. Endocrinology 1991; 129: 3187-3199.
54. Iqbal J, Swanson JJ, Prins GS, Jacobson CD. Androgen receptor-like immunoreactivity in the Brazilian opossum brain and pituitary: distribution and effects of castration and testosterone replacement in the adult male. Brain Res 1995; 703: 1-18.
55. Roche PJ, Hoare SA, Parker MG. A consensus DNA-binding site for the androgen receptor. Mol Endocrinol 1992; 6: 2229-2235.
56. Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000; 16: 276-277.
57. Holterhus PM, Piefke S, Hiort O. Anabolic steroids, testosterone- precursors and virilizing androgens induce distinct activation profiles of androgen responsive promoter constructs. J Steroid Biochem Mol Biol 2002; 82: 269-275.
58. Tan JA, Marschke KB, Ho KC, Perry ST, Wilson EM, French FS. Response elements of the androgen-regulated C3 gene. J Biol Chem 1992; 267: 4456-4466.
59. Bingaman EW, Baeckman LM, Yracheta JM, Handa RJ, Gray TS. Localization of androgen receptor within peptidergic neurons of the rat forebrain. Brain Res Bull 1994; 35: 379-382.
60. Meloni EG, Jackson AV, Cohen BM, Carlezon Jr WA. Corticotropin-releasing factor from the rat brain measured by protein immunoblot. Peptides 2005; 26: 2252-2256.
61. Alonso G, Szafarczyk A, Assenmacher I. Immunoreactivity of hypothalamo-neurohypophysial neurons which secrete corticotropin-releasing hormone (CRH) and vasopressin (Vp): immunocytochemical evidence for a correlation with their functional state in colchicine-treated rats. Exp Brain Res 1986; 61: 497-505.
62. Kawata M. Roles of steroid hormones and their receptors in structural organization in the nervous system. Neurosci Res 1995; 24: 1-46.
63. Roselli CE, Horton LE, Resko JA. Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 1985; 117: 2471-2477.
64. Schumacher M, Balthazart J. Neuroanatomical distribution of testosterone-metabolizing enzymes in the Japanese quail. Brain Res 1987; 422: 137-148.
65. Steimer T, Hutchison JB. Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature 1981; 292: 345-347.
66. Vockel A, Prove E, Balthazart J. Sex- and age-related differences in the activity of testosterone-metabolizing enzymes in microdissected nuclei of the zebra finch brain. Brain Res 1990; 511: 291-302.
67. Plotsky PM, Meaney MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 1993; 18: 195-200.
68. Viau V, Sharma S, Plotsky PM, Meaney MJ. Increased plasma ACTH responses to stress in nonhandled compared with handled rats require basal levels of corticosterone and are associated with increased levels of ACTH secretagogues in the median eminence. J Neurosci 1993; 13: 1097-1105.
69. Shanks N, Windle RJ, Perks PA, Harbuz MS, Jessop DS, Ingram CD et al. Early-life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation. Proc Natl Acad Sci USA 2000; 97: 5645-5650.
70. Hary L, Dupouy JP, Gregoire I. Effects of castration and testosterone on the pituitary and adrenal responses of the newborn rat to ether inhalation. Neuroendocrinology 1986; 42: 137-142.
71. Barraclough CA, Gorski RA. Evidence that the hypothalamus is responsible for androgen-induced sterility in the female rat. Endocrinology 1961; 68: 68-79.
72. Seale JV, Wood SA, Atkinson HC, Harbuz MS, Lightman SL. Postnatal masculinisation alters the HPA axis phenotype in the adult female rat. J Physiol 2005; 563: 265-274.
73. Meyer-Bahlburg HF, Ehrhardt AA. Prenatal diethylstilbestrol exposure: behavioral consequences in humans. Monogr Neural Sci 1986; 12: 90-95.
74. Meyer-Bahlburg HFL, Ehrhardt AA. A prenatal-hormone hypothesis for depression in adults with a history of fetal DES exposure. In: Halbreich U (ed). Hormones and Depression. Raven Press: NY, USA, 1987 pp 325-338.
75. El Hani A, Dalle M, Delost P. Role of testosterone in the sexual dimorphism of adrenal activity at puberty in the guinea-pig. J Endocrinol 1980; 87: 455-461.
76. Bingaman EW, Magnuson DJ, Gray TS, Handa RJ. Androgen inhibits the increases in hypothalamic corticotropin-releasing hormone (CRH) and CRH-immunoreactivity following gonadectomy. Neuroendocrinology 1994; 59: 228-234.
77. Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol Psychiatry 2003; 54: 1389-1398.
78. Holmes A, Heilig M, Rupniak NM, Steckler T, Griebel G. Neuropeptide systems as novel therapeutic targets for depression and anxiety disorders. Trends Pharmacol Sci 2003; 24: 580-588.
79. Neumann ID, Torner L, Wigger A. Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats. Neuroscience 2000; 95: 567-575.
80. Neumann ID, Wigger A, Torner L, Holsboer F, Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J Neuroendocrinol 2000; 12: 235-243.
81. Scott LV, Dinan TG. Vasopressin and the regulation of hypothalamic-pituitary-adrenal axis function: implications for the pathophysiology of depression. Life Sci 1998; 62: 1985-1998.
82. van West D, Del-Favero J, Aulchenko Y, Oswald P, Souery D, Forsgren T et al. A major SNP haplotype of the arginine vasopressin 1B receptor protects against recurrent major depression. Mol Psychiatry 2004; 9: 287-292.