Lifetime achievement from a brain-adrenal perspective: On the CRF-urocortin-glucocorticoid balance

Journal of Chemical Neuroanatomy

Volumn 54, Issue , 2013, Pages 42-49

  De Kloet, E R ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Behavior; Brain; CRF; Depression; Genomics; Glucocorticoids; Mineralocorticoids; Stress; Urocortins

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; DNA; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MINERALOCORTICOID; MINERALOCORTICOID RECEPTOR; STRESS HORMONE; UROCORTIN;

ADAPTATION; ADRENAL GLAND; BEHAVIOR; BINDING SITE; BRAIN; CHRONIC STRESS; COGNITION; EMOTION; FEEDBACK SYSTEM; GENETIC VARIABILITY; HORMONE SYNTHESIS; HUMAN; LIFESPAN; NEUROENDOCRINOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RECEPTOR BINDING; REGULATORY MECHANISM; REVIEW; STRESS;

BEHAVIOR; BRAIN; CRF; DEPRESSION; GENOMICS; GLUCOCORTICOIDS; MINERALOCORTICOIDS; STRESS; UROCORTINS;

ADRENAL GLANDS; ANIMALS; BRAIN; CORTICOTROPIN-RELEASING HORMONE; FEEDBACK, PHYSIOLOGICAL; GLUCOCORTICOIDS; HUMANS; NEUROSECRETORY SYSTEMS; STRESS, PHYSIOLOGICAL; UROCORTINS;

EID: 84888431164     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2013.10.003     Document Type: Review

References (86)

1. Bale T.L., Chen A. Minireview: CRF and Wylie Vale: a story of 41 amino acids and a Texan with grit. Endocrinology 2012, 153:56-61.
2. Barik J., Marti F., Morel C., Fernandez S.P., Lanteri C., Godeheu G., Tassin J.P., Mombereau C., Faure P., Tronche F. Chronic stress triggers social aversion via glucocorticoid receptor in dopaminoceptive neurons. Science 2013, 339:332-335.
3. Binder E.B. The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology 2009, 34:S186-S195.
4. Bittencourt J.C. The tale of a person and a peptide: Wylie W, Vale Jr. and the role of corticotropin-releasing factor in the stress response. Journal Chemical Neuroanatomy 2013 May 16, (epub ahead of publication).
5. Chen A., Vaughan J., Vale W.W. Glucocorticoids regulate the expression of the mouse urocortin II gene: a putative connection between the corticotropin-releasing factor receptor pathways. Molecular Endocrinology 2003, 17:1622-1639.
6. Cole M.A., Kalman B.A., Pace T.W., Topczewski F., Lowrey M.J., Spencer R.L. Selective blockade of the mineralocorticoid receptor impairs hypothalamic-pituitary-adrenal axis expression of habituation. Journal of Neuroendocrinology 2000, 12:1034-1042.
7. Daskalakis N.P., Bagot R.C., Parker K.J., Vinkers C.H., de Kloet E.R. The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology 2013, 38:1858-1873.
8. Datson N.A., Speksnijder N., Mayer J.L., Steenbergen P.J., Korobko O., Goeman J., de Kloet E.R., Joëls M., Lucassen P.J. The transcriptional response to chronic stress and glucocorticoid receptor blockade in the hippocampal dentate gyrus. Hippocampus 2012, 22:359-371.
9. Datson N.A., van den Oever J.M., Korobko O.B., Magarinos A.M., de Kloet E.R., McEwen B.S. Prior history of chronic stress changes the transcriptional response to glucocorticoid challenge in the dentate gyrus region of the male rat hippocampus. Endocrinology 2013, 154:3261-3272.
10. de Kloet A.D., Pati D., Wang L., Hiller H., Sumners C., Frazier C.J., Seeley R.J., Herman J.P., Woods S.C., Krause E.G. Angiotensin type 1a receptors in the paraventricular nucleus of the hypothalamus protect against diet-induced obesity. Journal of Neuroscience 2013, 33:4825-4833.
11. de Kloet E.R., Reul J.M. Feedback action and tonic influence of corticosteroids on brain function: a concept arising from the heterogeneity of brain receptor systems. Psychoneuroendocrinology 1987, 12:83-105.
12. de Kloet E.R., Joëls M. Stress research: past, presence and future. Neuroscience in the 21st Century. Part 9: Regulation of Natural Behaviours 2013, 1979-2007. Springer, Berlin. D.W. Pfaff (Ed.).
13. de Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nature Reviews Neuroscience 2005, 6:463-475.
14. de Kloet E.R., Van der Vies J., de Wied D. The site of the suppressive action of dexamethasone on pituitary-adrenal activity. Endocrinology 1974, 94:61-73.
15. de Kloet E.R., Wallach G., McEwen B.S. Differences in corticosterone and dexamethasone binding to rat brain and pituitary. Endocrinology 1975, 96:598-609.
16. DeRijk R.H., de Kloet E.R., Zitman F.G., van Leeuwen N. Mineralocorticoid receptor gene variants as determinants of HPA axis regulation and behavior. Endocrine Development 2011, 20:137-148.
17. DeRijk R.H., Wüst S., Meijer O.C., Zennaro M.C., Federenko I.S., Hellhammer D.H., Giacchetti G., Vreugdenhil E., Zitman F.G., de Kloet E.R. A common polymorphism in the mineralocorticoid receptor modulates stress responsiveness. Journal of Clinical Endocrinology and Metabolism 2006, 91:5083-5089.
18. de Souza E.B., Perrin M.H., Insel T.R., Rivier J., Vale W.W., Kuhar M.J. Corticotropin-releasing factor receptors in rat forebrain: autoradiographic identification. Science 1984, 224:1449-1451.
19. de Wied D. The site of the blocking action of dexamethasone on stress-induced pituitary ACTH release. Journal of Endocrinology 1964, 29:29-37.
20. Di S., Malcher-Lopes R., Halmos K.C., Tasker J.G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. Journal of Neuroscience 2003, 23:4850-4857.
21. Dias-Ferreira E., Sousa J.C., Melo I., Morgado P., Mesquita A.R., Cerqueira J.J., Costa R.M., Sousa N. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 2009, 325:621-625.
22. Edwards C.R., Stewart P.M., Burt D., Brett L., McIntyre M.A., Sutanto W., de Kloet E.R., Monder C. Localisation of 11 beta-hydroxysteroid dehydrogenase--tissue specific protector of the mineralocorticoid receptor. Lancet 1988, 29:986-989.
23. Elliott E., Ezra-Nevo G., Regev L., Neufeld-Cohen A., Chen A. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nature Neuroscience 2010, 13:1351-1353.
24. Evans S.J., Datson N.A., Kabbaj M., Thompson R.C., Vreugdenhil E., De Kloet E.R., Watson S.J., Akil H. Evaluation of Affymetrix Gene Chip sensitivity in rat hippocampal tissue using SAGE analysis. Serial analysis of gene expression. European Journal of Neuroscience 2002, 16:409-413.
25. Fitzsimons C.P., van Hooijdonk L.W., Schouten M., Zalachoras I., Brinks V., Zheng T., Schouten T.G., Saaltink D.J., Dijkmans T., Steindler D.A., Verhaagen J., Verbeek F.J., Lucassen P.J., de Kloet E.R., Meijer O.C., Karst H., Joëls M., Oitzl M.S., Vreugdenhil E. Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Molecular Psychiatry 2013, 18:993-1005.
26. Fleischer N., Vale W. Inhibition of vasopressin-induced ACTH release from the pituitary by glucocorticoids in vitro. Endocrinology 1968, 83:1232-1236.
27. Funder J.W., Pearce P.T., Smith R., Smith A.I. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science 1988, 242:583-585.
28. Geerling J.C., Loewy A.D. Aldosterone in the brain. American Journal of Physiology Renal Physiology 2009, 297:F559-F576.
29. Gesing A., Bilang-Bleuel A., Droste S.K., Linthorst A.C., Holsboer F., Reul J.M. Psychological stress increases hippocampal mineralocorticoid receptor levels: involvement of corticotropin-releasing hormone. Journal of Neuroscience 2001, 21:4822-4829.
30. Harris A.P., Holmes M.C., de Kloet E.R., Chapman K.E., Seckl J.R. Mineralocorticoid and glucocorticoid receptor balance in control of HPA axis and behaviour. Psychoneuroendocrinology 2013, 38:648-658.
31. Herman J.P. Neural control of chronic stress adaptation. Frontiers in Behavioral Neuroscience 2013, 7:61.
32. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Frontiers in Neuroendocrinology 2003, 24:151-180.
33. Holmes M.C., Seckl J.R. The role of 11α-hydroxysteroid dehydrogenases in the brain. Molecular Cellular Endocrinolology 2006, 248:9-14.
34. Hsu S.Y., Hsueh A.J. Human stresscopin and stresscopin-related peptide are selective ligands for the type 2 corticotropin-releasing hormone receptor. Nature Medicine 2001, 7:605-611.
35. Joëls M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol Sciences 2006, 27:244-250.
36. Joëls M., Baram T.Z. The neuro-symphony of stress. Nature Reviews Neuroscience 2009, 10:459-466.
37. Joëls M., de Kloet E.R. Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. Science 1989, 245:1502-1505.
38. Johnson L.R., Farb C., Morrison J.H., McEwen B.S., LeDoux J.E. Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 2005, 136:289-299.
39. Karssen A.M., Meijer O.C., Berry A., Sanjuan Piñol R., de Kloet E.R. Low doses of dexamethasone can produce a hypocorticosteroid state in the brain. Endocrinology 2005, 146:5587-5595.
40. Karst H., Berger S., Erdmann G., Schütz G., Joëls M. Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proceedings National Academy of Sciences of the United States of America 2010, 107:14449-14454.
41. Karst H., Berger S., Turiault M., Tronche F., Schütz G., Joëls M. Mineralocorticoid receptors are indispensable for non-genomic modulation of hippocampal glutamate transmission by corticosterone. Proceedings National Academy of Sciences of the United States of America 2005, 102:19204-19207.
42. Klok M.D., Alt S.R., Lafitte I.A.J., Turner J.D., Lakke E.A., Huitinga I., Muller C.P., Zitman F.G., de Kloet E.R., Derijk R.H. Decreased expression of mineralocorticoid receptor mRNA and its splice variants in postmortem brain regions of patients with major depressive disorder. Journal of Psychiatry Research 2011, 45:871-878.
43. Klok M.D., Giltay E.J., Van der Does A.J., Geleijnse J.M., Antypa N., Penninx B.W., de Geus E.J., Willemsen G., Boomsma D.I., van Leeuwen N., Zitman F.G., de Kloet E.R., DeRijk R.H. A common and functional mineralocorticoid receptor haplotype enhances optimism and protects against depression in females. Translational Psychiatry 2011, 13:e62.
44. Kovács K.J. CRH: the link between hormonal-, metabolic- and behavioral responses to stress. Journal Chemical Neuroanatomy 2013, (June 15, epub ahead of publication).
45. Kruk M.R., Haller J., Meelis W., de Kloet E.R. Mineralocorticoid receptor blockade during a rat's first violent encounter inhibits its subsequent propensity for violence. Behavioral Neuroscience 2013, 127:505-514.
46. Lachize S., Apostolakis E.M., van der Laan S., Tijssen A.M., Xu J., de Kloet E.R., Meijer O.C. Steroid receptor coactivator-1 is necessary for regulation of corticotropin-releasing hormone by chronic stress and glucocorticoids. Proceedings National Academy of Sciences of the United States of America 2009, 106:8038-8042.
47. Levine S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 2005, 30:939-994.
48. Lightman S.L., Conway-Campbell B.L. The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nature Reviews Neuroscience 2010, 11:710-718.
49. McEwen B.S., Weiss J.M., Schwartz L.S. Selective retention of corticosterone by limbic structures in rat brain. Nature 1968, 220:911-912.
50. McEwen B.S., Wingfield J.C. What is in a name? Integrating homeostasis, allostasis and stress. Hormones and Behaviour 2010, 57:105-111.
51. Meijer O.C., de Lange E.C., Breimer D.D., de Boer A.G., Workel J.O., de Kloet E.R. Penetration of dexamethasone into brain glucocorticoid targets is enhanced in mdr1A P-glycoprotein knockout mice. Endocrinology 1998, 139:1789-1793.
52. Mehta D., Klengel T., Conneely K.N., Smith A.K., Altmann A., Pace T.W., Rex-Haffner M., Loeschner A., Gonik M., Mercer K.B., Bradley B., Müller-Myhsok B., Ressler K.J., Binder E.B. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proceedings National Academy of Sciences of the United States of America 2013, 110:8302-8307.
53. Mezey E., Palkovits M., de, Kloet E.R., Verhoef J., de Wied D. Evidence for pituitary-brain transport of a behaviorally potent ACTH analog. Life Sciences 1978, 22:831-838.
54. Murgatroyd C., Spengler D. Genetic variation in the epigenetic machinery and mental health. Current Psychiatry Reports 2012, 14:138-149.
55. Neufeld-Cohen A., Tsoory M.M., Evans A.K., Getselter D., Gil S., Lowry C.A., Vale W.W., Chen A. A triple urocortin knockout mouse model reveals an essential role for urocortins in stress recovery. Proceedings National Academy of Sciences of the United States of America 2010, 107:19020-19025.
56. Niwa M., Jaaro-Peled H., Tankou S., Seshadri S., Hikida T., Matsumoto Y., Cascella N.G., Kano S., Ozaki N., Nabeshima T., Sawa A. Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 2013, 339:335-339.
57. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behavioral Neuroscience 1992, 106:62-71.
58. Oitzl M.S., Schwabe L., Aggleton J.P. Memory formation: its changing face. Neuroscience Biobehavioral Reviews 2012, 36:1577-1578.
59. Olijslagers J.E., de Kloet E.R., Elgersma Y., van Woerden G.M., Joëls M., Karst H. Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. European Journal of Neuroscience 2008, 27:2450-2542.
60. Oomen C.A., Mayer J.L., de Kloet E.R., Joëls M., Lucassen P.J. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. European Journal of Neurosciences 2007, 26:3395-3401.
61. Polman J.A., de Kloet E.R., Datson N.A. Two populations of glucocorticoid receptor-binding sites in the male rat hippocampal genome. Endocrinology 2013, 154:1832-1844.
62. Polman J.A., Hunter R.G., Speksnijder N., van den Oever J.M., Korobko O.B., McEwen B.S., de Kloet E.R., Datson N.A. Glucocorticoids modulate the mTOR pathway in the hippocampus: differential effects depending on stress history. Endocrinology 2012, 153:4317-4327.
63. Qi X.R., Kamphuis W., Wang S., Wang Q., Lucassen P.J., Zhou J.N., Swaab D.F. Aberrant stress hormone receptor balance in the human prefrontal cortex and hypothalamic paraventricular nucleus of depressed patients. Psychoneuroendocrinology 2013, 38:863-870.
64. Raisman G. An urge to explain the incomprehensible: Geoffrey Harris and the discovery of the neural control of the pituitary gland. Annual Reviews Neuroscience 1997, 20:533-566.
65. Ratka A., Sutanto W., Bloemers M., De Kloet E.R. On the role of brain mineralocorticoid (type I) and glucocorticoid (type II) receptors in neuroendocrine regulation. Neuroendocrinology 1989, 50:117-123. http://www.ncbi.nlm.nih.gov/pubmed/2550833.
66. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985, 117:2505-2511.
67. Reul J.M., Holsboer F. Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Current Opinion in Pharmacology 2002, 2:23-33.
68. Reul J.M., Tonnaer J.A., De Kloet E.R. Neurotrophic ACTH analogue promotes plasticity of type I corticosteroid receptor in brain of senescent male rats. Neurobiology of Aging 1988, 9:253-260.
69. Reyes T.M., Lewis K., Perrin M.H., Kunitake K.S., Vaughan J., Arias C.A., Hogenesch J.B., Gulyas J., Rivier J., Vale W.W., Sawchenko P.E. Urocortin II: a member of the corticotropin-releasing factor (CRF) neuropeptide family that is selectively bound by type 2 CRF receptors. Proceedings National Academy of Sciences of the United States of America 2001, 98:2843-2848.
70. Sarabdjitsingh R.A., Conway-Campbell B.L., Leggett J.D., Waite E.J., Meijer O.C., de Kloet E.R., Lightman S.L. Stress responsiveness varies over the ultradian glucocorticoid cycle in a brain-region-specific manner. Endocrinology 2010, 151:5369-5379.
71. Schaaf M.J., Hoetelmans R.W., de Kloet E.R., Vreugdenhil E. Corticosterone regulates expression of BDNF and trkB but not NT-3 and trkC mRNA in the rat hippocampus. Journal of Neuroscience Research 1997, 48:334-341.
72. Schaaf M.J., Sibug R.M., Duurland R., Fluttert M.F., Oitzl M.S., de Kloet E.R., Vreugdenhilm E. Corticosterone effects on BDNF mRNA expression in the rat hippocampus during morris water maze training. Stress 1999, 3:173-183.
73. Schwabe L., Schächinger H., de Kloet E.R., Oitzl M.S. Corticosteroids operate as switch between memory systems. Journal Cognitive Neuroscience 2009, 22:1362-1372.
74. Selye H. A syndrome produced by diverse nocuous agents. Nature 1936, 138:132.
75. Smith S.M., Vale W.W. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clininical Neuroscience 2006, 8:383-395.
76. Ter Horst J.P., van der Mark M.H., Arp M., Berger S., de Kloet E.R., Oitzl M.S. Stress or no stress: mineralocorticoid receptors in the forebrain regulate behavioral adaptation. Neurobiology of Learning and Memory 2012, 98:33-40.
77. Ter Horst J.P., Kentrop J., de Kloet E.R., Oitzl M.S. Stress and estrous cycle affect strategy but not performance of female C57BL/6J mice. Behavioural Brain Research 2013, 241:92-95.
78. Vale W., Spiess J., Rivier C., Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213:1394-1397.
79. van Eekelen J.A., Jiang W., De Kloet E.R., Bohn M.C. Distribution of the mineralocorticoid and the glucocorticoid receptor mRNAs in the rat hippocampus. Journal Neuroscience Research 1988, 21:88-94.
80. 2+ currents in rat hippocampal dentate gyrus. Journal of Neuroendocrinology 2006, 18:732-741.
81. van Haarst A.D., Oitzl M.S., Workel J.O., de Kloet E.R. Chronic brain glucocorticoid receptor blockade enhances the rise in circadian and stress-induced pituitary-adrenal activity. Endocrinology 1996, 137:4935-4943.
82. van Steensel B., van Binnendijk E.P., Hornsby C.D., van der Voort H.T., Krozowski Z.S., de Kloet E.R., van Driel R. Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. Journal Cell Science 1996, 109:787-792.
83. Veldhuis H.D., De Kloet E.R. Vasopressin-related peptides increase the hippocampal corticosterone receptor capacity of diabetes insipidus (Brattleboro) rat. Endocrinology 1982, 110:153-159.
84. Verkuyl J.M., Joëls M. Effect of adrenalectomy on miniature inhibitory postsynaptic currents in the paraventricular nucleus of the hypothalamus. Journal of Neurophysiology 2003, 89:237-245.
85. Zalachoras I., Houtman R., Atucha E., Devos R., Tijssen A.M., Hu P., Lockey P.M., Datson N.A., Belanoff J.K., Lucassen P.J., Joëls M., de Kloet E.R., Roozendaal B., Hunt H., Meijer O.C. Differential targeting of brain stress circuits with a selective glucocorticoid receptor modulator. Proceedings National Academy of Sciences of the United States of America 2013, 110:7910-7915.
86. Zalachoras I., Houtman R., Meijer O.C. Understanding stress-effects in the brain via transcriptional signal transduction pathways. Neuroscience 2013, 242:97-109.