Distribution of the glucocorticoid receptor in the human amygdala; changes in mood disorder patients

Brain Structure and Function

Volumn 219, Issue 5, 2014, Pages 1615-1626

  Wang, Q ^a   Verweij, E W E ^a   Krugers, H J ^a   Joels, M ^b   Swaab, D F ^c   Lucassen, P J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Amygdala; Astrocyte; Bipolar disorder; HPA axis; Major depression; Stress

Indexed keywords

GLUCOCORTICOID RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN;

ADULT; AGED; AMYGDALOID NUCLEUS; ARTICLE; ASTROCYTE; BASOLATERAL AMYGDALA; BIPOLAR DISORDER; CHRONIC STRESS; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; MAJOR DEPRESSION; MALE; MIDDLE AGED; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VERY ELDERLY; ANALYSIS OF VARIANCE; CASE CONTROL STUDY; CELL COUNT; GLIA; METABOLISM; MOOD DISORDER; NERVE CELL; NONPARAMETRIC TEST; PATHOLOGY; SEXUAL DEVELOPMENT;

AGED; AGED, 80 AND OVER; AMYGDALA; ANALYSIS OF VARIANCE; CASE-CONTROL STUDIES; CELL COUNT; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; MALE; MIDDLE AGED; MOOD DISORDERS; NEUROGLIA; NEURONS; RECEPTORS, GLUCOCORTICOID; SEX CHARACTERISTICS; STATISTICS, NONPARAMETRIC;

EID: 84906852657     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0589-4     Document Type: Article

References (94)

1. Alt SR, Turner JD, Klok MD, Meijer OC, Lakke EA, Derijk RH, Muller CP (2010) Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology 35(4): 544-556. doi:10.1016/j.psyneuen.2009.09.001
2. Altshuler LL, Abulseoud OA, Foland-Ross L, Bartzokis G, Chang S, Mintz J, Hellemann G, Vinters HV (2010) Amygdala astrocyte reduction in subjects with major depressive disorder but not bipolar disorder. Bipolar Disord 12(5):541-549. doi:10.1111/j.1399-5618.2010.00838.x
3. Bao AM, Ruhe HG, Gao SF, Swaab DF (2012) Neurotransmitters and neuropeptides in depression. Handb Clin Neurol 106:107-136. doi:10.1016/B978-0- 444-52002-9
4. Bjartmar L, Johansson IM, Marcusson J, Ross SB, Seckl JR, Olsson T (2000) Selective effects on NGFI-A, MR, GR and NGFI-B hippocampal mRNA expression after chronic treatment with different subclasses of antidepressants in the rat. Psychopharmacology 151(1):7-12 (Pubitemid 30642527)
5. Bohn MC, Howard E, Vielkind U, Krozowski Z (1991) Glial cells express both mineralocorticoid and glucocorticoid receptors. J Steroid Biochem Mol Biol 40(1-3):105-111. doi:10.1016/0960-0760(91)90173-3
6. Brady LS, Whitfield HJ Jr, Fox RJ, Gold PW, Herkenham M (1991) Long-term antidepressant administration alters corticotropin-releasing hormone, tyrosine hydroxylase, and mineralocorticoid receptor gene expression in rat brain. Therapeutic implications. J Clin Invest 87(3):831-837. doi:10.1172/JCI115086
7. Brady LS, Gold PW, Herkenham M, Lynn AB, Whitfield HJ Jr (1992) The antidepressants fluoxetine, idazoxan and phenelzine alter corticotropin- releasing hormone and tyrosine hydroxylase mRNA levels in rat brain: therapeutic implications. Brain Res 572(1-2):117-125. doi:10.1016/0006-8993(92)90459-M
8. Burke HM, Davis MC, Otte C, MohrDC(2005) Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30(9):846-856. doi:10.1016/j.psyneuen.2005.02.010 (Pubitemid 40977907)
9. Cintra A, Bhatnagar M, Chadi G, Tinner B, Lindberg J, Gustafsson JA, Agnati LF, Fuxe K (1994) Glial and neuronal glucocorticoid receptor immunoreactive cell populations in developing, adult, and aging brain. Ann N Y Acad Sci 746:42-61
10. Cornelisse S, van Stegeren AH, Joels M (2010) Implications of psychosocial stress on memory formation in a typical male versus female student sample. Psychoneuroendocrinology. doi:10.1016/j.psyneuen.2010.09.002
11. Czeh B, Lucassen PJ (2007) What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci 257(5):250-260. doi:10.1007/s00406-007-0728-0 (Pubitemid 47301403)
12. Czeh B, Simon M, Schmelting B, Hiemke C, Fuchs E (2006) Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology 31(8):1616-1626. doi:10.1038/sj.npp.1300982 (Pubitemid 44106693)
13. DeRijk RH, Schaaf M, Stam FJ, de Jong IE, Swaab DF, Ravid R, Vreugdenhil E, Cidlowski JA, de Kloet ER, Lucassen PJ (2003) Very low levels of the glucocorticoid receptor beta isoform in the human hippocampus as shown by Taqman RT-PCR and immunocytochemistry. Brain Res Mol Brain Res 116(1-2): 17-26 pii:S0169328X03002092
14. DeRijk RH, de Kloet ER, Zitman FG, van Leeuwen N (2011) Mineralocorticoid receptor gene variants as determinants of HPA axis regulation and behavior. Endocr Dev 20:137-148. doi:10.1159/000321235000321235
15. Drevets WC (2003) Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad Sci 985:420-444
16. Eagle AL, Knox D, Roberts MM, Mulo K, Liberzon I, Galloway MP, Perrine SA (2012) Single prolonged stress enhances hippocampal glucocorticoid receptor and phosphorylated protein kinaseB levels. Neurosci Res 75(2):130-137. doi:10.1016/j.neures.2012.11.001
17. Erdmann G, Berger S, Schutz G (2008) Genetic dissection of glucocorticoid receptor function in the mouse brain. J Neuroendocrinol 20(6):655-659. doi:10.1111/j.1365-2826.2008.01717.x (Pubitemid 351858713)
18. Flandreau EI, Bourke CH, Ressler KJ, Vale WW, Nemeroff CB, Owens MJ (2012) Escitalopram alters gene expression and HPA axis reactivity in rats following chronic overexpression of corticotropin-releasing factor from the central amygdala. Psychoneuroendocrinology. doi:10.1016/j.psyneuen.2012.11.020
19. Furay AR, Bruestle AE, Herman JP (2008) The role of the forebrain glucocorticoid receptor in acute and chronic stress. Endocrinology 149(11):5482-5490. doi:10.1210/en.2008-0642
20. Gobert A, Brocco M, Dekeyne A, Di Cara B, Bouchez G, Lejeune F, Gannon RL, Millan MJ (2009) Neurokinin1 antagonists potentiate antidepressant properties of serotonin reuptake inhibitors, yet blunt their anxiogenic actions: a neurochemical, electrophysiological, and behavioral characterization. Neuropsychopharmacology 34(4):1039-1056. doi:10.1038/npp.2008.176npp2008176
21. Gosselin RD, Gibney S, O'Malley D, Dinan TG, Cryan JF (2009) Region specific decrease in glial fibrillary acidic protein immunoreactivity in the brain of a rat model of depression. Neuroscience 159(2):915-925. doi:10.1016/j.neuroscience.2008.10.018
22. Hamidi M, Drevets WC, Price JL (2004) Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol Psychiatry 55(6):563-569. doi:10.1016/j.biopsych.2003.11.006 (Pubitemid 38315029)
23. Henckens MJ, Hermans EJ, Pu Z, Joels M, Fernandez G (2009) Stressed memories: how acute stress affects memory formation in humans. J Neurosci 29(32):10111-10119. doi:10.1523/JNEUROSCI.1184-09.2009
24. Herman JP, Spencer R (1998) Regulation of hippocampal glucocorticoid receptor gene transcription and protein expression in vivo. J Neurosci 18(18):7462-7473 (Pubitemid 28425829)
25. Herman JP, Schafer MK, Young EA, Thompson R, Douglass J, Akil H, Watson SJ (1989) Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. J Neurosci 9(9):3072-3082 (Pubitemid 19260824)
26. Heydendael W, Jacobson L (2008) Differential effects of imipramine and phenelzine on corticosteroid receptor gene expression in mouse brain: potential relevance to antidepressant response. Brain Res 1238:93-107. doi:10.1016/j.brainres.2008.08.018
27. Heydendael W, Jacobson L (2010) Widespread hypothalamic-pituitary- adrenocortical axis-relevant and mood-relevant effects of chronic fluoxetine treatment on glucocorticoid receptor gene expression in mice. Eur J Neurosci 31(5):892-902. doi:10.1111/j.1460-9568.2010.07131.x
28. Holsboer F, Muller OA, Doerr HG, Sippell WG, Stalla GK, Gerken A, Steiger A, Boll E, Benkert O (1984) ACTH and multisteroid responses to corticotropin-releasing factor in depressive illness: relationship to multisteroid responses after ACTH stimulation and dexamethasone suppression. Psychoneuroendocrinology 9(2):147-160 (Pubitemid 14089185)
29. Ishunina TA, Fischer DF, Swaab DF (2007) Estrogen receptor alpha and its splice variants in the hippocampus in aging and Alzheimer's disease. Neurobiol Aging 28(11):1670-1681. doi:10.1016/j.neurobiolaging.2006.07.024 (Pubitemid 47384954)
30. Joels M, Baram TZ (2009) The neuro-symphony of stress. Nat Rev Neurosci 10(6):459-466. doi:10.1038/nrn2632
31. Khalili-Mahani N, Dedovic K, Engert V, Pruessner M, Pruessner JC (2010) Hippocampal activation during a cognitive task is associated with subsequent neuroendocrine and cognitive responses to psychological stress. Hippocampus 20(2):323-334. doi:10.1002/hipo.20623
32. Klok MD, Alt SR, Irurzun Lafitte AJ, Turner JD, Lakke EA, Huitinga I, Muller CP, Zitman FG, Ronald de Kloet E, Derijk RH (2011) Decreased expression of mineralocorticoid receptor mRNA and its splice variants in postmortem brain regions of patients with major depressive disorder. J Psychiatr Res 45(7):871-878. doi:10.1016/j.jpsychires.2010.12.002
33. Kretz O, Reichardt HM, Schutz G, Bock R (1999) Corticotropinreleasing hormone expression is the major target for glucocorticoid feedback-control at the hypothalamic level. Brain Res 818(2):488-491 pii:S0006-8993(98)01277-3
34. Kumsta R, Entringer S, Koper JW, van Rossum EF, Hellhammer DH, Wust S (2010) Working memory performance is associated with common glucocorticoid receptor gene polymorphisms. Neuropsychobiology 61(1):49-56. doi:10.1159/000262180
35. Landgraf R (2006) The involvement of the vasopressin system in stress-related disorders. CNS Neurol Disord Drug Targets 5(2):167-179
36. Leventopoulos M, Ruedi-Bettschen D, Knuesel I, Feldon J, Pryce CR, Opacka-Juffry J (2007) Long-term effects of early life deprivation on brain glia in Fischer rats. Brain Res 1142:119-126. doi:10.1016/j.brainres.2007.01.039 (Pubitemid 46413198)
37. Lovallo WR, Robinson JL, Glahn DC, Fox PT (2010) Acute effects of hydrocortisone on the human brain: an fMRI study. Psychoneuroendocrinology 35(1):15-20. doi:10.1016/j.psyneuen.2009.09.010
38. Lucassen PJ, Muller MB, Holsboer F, Bauer J, Holtrop A, Wouda J, Hoogendijk WJ, De Kloet ER, Swaab DF (2001) Hippocampal apoptosis in major depression is a minor event and absent from subareas at risk for glucocorticoid overexposure. Am J Pathol 158(2):453-468. doi:10.1016/S0002-9440(10)63988-0 (Pubitemid 32158608)
39. Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE (2007) The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain Cogn 65(3):209-237. doi:10.1016/j.bandc.2007.02.007 (Pubitemid 350051538)
40. Lupien SJ, Parent S, Evans AC, Tremblay RE, Zelazo PD, Corbo V, Pruessner JC, Seguin JR (2011) Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. Proc Natl Acad Sci USA 108(34):14324-14329. doi:10.1073/pnas. 11053711081105371108
41. Mai JK, Paxinos G, Assheuer JK (2004) Atlas of the Human Brain. Elsevier Academic Press, San Diego
42. Matsubara T, Funato H, Kobayashi A, Nobumoto M, Watanabe Y (2006) Reduced glucocorticoid receptor alpha expression in mood disorder patients and first-degree relatives. Biol Psychiatry 59(8):689-695. doi:10.1016/j.biopsych. 2005.09.026
43. McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12(2):205-210 pii:S0959438802003069
44. Meyer U, Kruhoffer M, Flugge G, Fuchs E (1998) Cloning of glucocorticoid receptor and mineralocorticoid receptor cDNA and gene expression in the central nervous system of the tree shrew (Tupaia belangeri) . Brain Res Mol Brain Res 55(2):243-253 pii:S0169328X98000047
45. Meyer U, van Kampen M, Isovich E, Flugge G, Fuchs E (2001) Chronic psychosocial stress regulates the expression of both GR and MR mRNA in the hippocampal formation of tree shrews. Hippocampus 11(3):329-336. doi:10.1002/hipo.1047 (Pubitemid 32655291)
46. Meynen G, Unmehopa UA, van Heerikhuize JJ, Hofman MA, Swaab DF, Hoogendijk WJ (2006) Increased arginine vasopressin mRNA expression in the human hypothalamus in depression: a preliminary report. Biol Psychiatry 60(8):892-895. doi:10.1016/j.biopsych.2005.12.010 (Pubitemid 44527884)
47. Mifsud KR, Gutierrez-Mecinas M, Trollope AF, Collins A, Saunderson EA, Reul JM (2011) Epigenetic mechanisms in stress and adaptation. Brain Behav Immun 25(7):1305-1315. doi:10.1016/j.bbi.2011.06.005
48. Miguel-Hidalgo JJ, Overholser JC, Jurjus GJ, Meltzer HY, Dieter L, Konick L, Stockmeier CA, Rajkowska G (2011) Vascular and extravascular immunoreactivity for intercellular adhesion molecule 1 in the orbitofrontal cortex of subjects with major depression: age-dependent changes. J Affect Disord 132(3): 422-431. doi:10.1016/j.jad.2011.03.052
49. Morey RA, Gold AL, LaBar KS, Beall SK, Brown VM, Haswell CC, Nasser JD, Wagner HR, McCarthy G (2012) Amygdala volume changes in posttraumatic stress disorder in a large case-controlled veterans group. Arch Gen Psychiatry 69(11): 1169-1178. doi:10.1001/archgenpsychiatry.2012
50. Morimoto M, Morita N, Ozawa H, Yokoyama K, Kawata M (1996) Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res 26(3):235-269 pii:S0168-0102(96)01105-4
51. Nadel L, Hupbach A, Gomez R, Newman-Smith K (2012) Memory formation, consolidation and transformation. Neurosci Biobehav Rev 36(7):1640-1645. doi:10.1016/j.neubiorev.2012.03.001
52. Patel PD, Lopez JF, Lyons DM, Burke S, Wallace M, Schatzberg AF (2000) Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain. J Psychiatr Res 34(6): 383-392 pii:S0022395600000352
53. Patel PD, Katz M, Karssen AM, Lyons DM (2008) Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex. Psychoneuroendocrinology 33(3):360-367. doi:10.1016/j.psyneuen.2007.12.003
54. Peiffer A, Veilleux S, Barden N (1991) Antidepressant and other centrally acting drugs regulate glucocorticoid receptor messenger RNA levels in rat brain. Psychoneuroendocrinology 16(6):505-515
55. Pepin MC, Beaulieu S, Barden N (1989) Antidepressants regulate glucocorticoid receptor messenger RNA concentrations in primary neuronal cultures. Brain Res Mol Brain Res 6(1):77-83 (Pubitemid 19163720)
56. Perez-Ortiz JM, Garcia-Gutierrez MS, Navarrete F, Giner S, Manzanares J (2012) Gene and protein alterations of FKBP5 and glucocorticoid receptor in the amygdala of suicide victims. Psychoneuroendocrinology. doi:10.1016/j.psyneuen. 2012.11.008
57. Perlman WR, Webster MJ, Kleinman JE, Weickert CS (2004) Reduced glucocorticoid and estrogen receptor alpha messenger ribonucleic acid levels in the amygdala of patients with major mental illness. Biol Psychiatry 56(11):844-852. doi:10.1016/j.biopsych.2004.09.006 (Pubitemid 39575458)
58. Perlman WR, Webster MJ, Herman MM, Kleinman JE, Weickert CS (2007) Age-related differences in glucocorticoid receptor mRNA levels in the human brain. Neurobiol Aging 28(3):447-458. doi:10.1016/j.neurobiolaging.2006.01.010 (Pubitemid 46188493)
59. Pfleiderer B, Zinkirciran S, Arolt V, Heindel W, Deckert J, Domschke K (2007) fMRI amygdala activation during a spontaneous panic attack in a patient with panic disorder. World J Biol Psychiatry 8(4):269-272. doi:10.1080/ 15622970701216673 (Pubitemid 350018480)
60. Plotsky PM, Owens MJ, Nemeroff CB (1998) Psychoneuroendocrinology of depression. Hypothalamic-pituitary-adrenal axis. Psychiatr Clin North Am 21(2):293-307
61. Pryce CR, Feldon J, Fuchs E, Knuesel I, Oertle T, Sengstag C, Spengler M, Weber E, Weston A, Jongen-Relo A (2005) Postnatal ontogeny of hippocampal expression of the mineral-ocorticoid and glucocorticoid receptors in the common marmoset monkey. Eur J Neurosci 21(6):1521-1535. doi:10.1111/j.1460-9568.2005. 04003.x (Pubitemid 40646598)
62. Qi XR, Kamphuis W, Wang S, Wang Q, Lucassen PJ, Zhou JN, Swaab DF (2012) Aberrant stress hormone receptor balance in the human prefrontal cortex and hypothalamic paraventricular nucleus of depressed patients. Psychoneuroendocrinology. doi:10.1016/j.psyneuen.2012.09.014
63. Raadsheer FC, Hoogendijk WJ, Stam FC, Tilders FJ, Swaab DF (1994) Increased numbers of corticotropin-releasing hormone expressing neurons in the hypothalamic paraventricular nucleus of depressed patients. Neuroendocrinology 60(4):436-444 (Pubitemid 24284827)
64. Raadsheer FC, vanHeerikhuize JJ, Lucassen PJ, Hoogendijk WJ, Tilders FJ, Swaab DF (1995) Corticotropin-releasing hormone mRNA levels in the paraventricular nucleus of patients with Alzheimer's disease and depression. Am J Psychiatry 152(9):1372-1376
65. Rajkowska G, Miguel-Hidalgo JJ (2007) Gliogenesis and glial pathology in depression. CNS Neurol Disord Drug Targets 6(3):219-233 (Pubitemid 46916253)
66. Rajkowska G, Hughes J, Stockmeier CA, Javier Miguel-Hidalgo J, Maciag D (2012) Coverage of blood vessels by astrocytic endfeet is reduced in major depressive disorder. Biol Psychiatry 73(7):613-621. doi:10.1016/j.biopsych.2012. 09.024
67. Rauch SL, Shin LM, Segal E, Pitman RK, Carson MA, McMullin K, Whalen PJ, Makris N (2003) Selectively reduced regional cortical volumes in post-traumatic stress disorder. NeuroReport 14(7):913-916. doi:10.1097/01.wnr.0000071767.24455. 10 (Pubitemid 36829763)
68. Reul JM, Stec I, Soder M, Holsboer F (1993) Chronic treatment of rats with the antidepressant amitriptyline attenuates the activity of the hypothalamic-pituitary-adrenocortical system. Endocrinology 133(1):312-320 (Pubitemid 23206409)
69. Reul JM, Labeur MS, Grigoriadis DE, De Souza EB, Holsboer F (1994) Hypothalamic-pituitary-adrenocortical axis changes in the rat after long-term treatment with the reversible monoamine oxidase-A inhibitor moclobemide. Neuroendocrinology 60(5):509-519
70. Rossby SP, Nalepa I, Huang M, Perrin C, Burt AM, Schmidt DE, Gillespie DD, Sulser F (1995) Norepinephrine-independent regulation of GRII mRNA in vivo by a tricyclic antidepressant. Brain Res 687(1-2):79-82
71. Sanchez MM, Young LJ, Plotsky PM, Insel TR (2000) Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. J Neurosci 20(12):4657-4668. doi:20/12/4657
72. Sapolsky RM, Krey LC, McEwen BS (1984) Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci USA 81(19): 6174-6177 (Pubitemid 15220802)
73. Sartorius N (2003) Physical symptoms of depression as a public health concern. J Clin Psychiatry 64(Suppl 7):3-4
74. Schwabe L, Joels M, Roozendaal B, Wolf OT, Oitzl MS (2012) Stress effects on memory: an update and integration. Neurosci Biobehav Rev 36(7):1740-1749. doi:10.1016/j.neubiorev.2011.07.002
75. Seckl JR, Fink G (1992) Antidepressants increase glucocorticoid and mineralocorticoid receptor mRNA expression in rat hippocampus in vivo. Neuroendocrinology 55(6):621-626
76. Seckl JR, Dickson KL, Yates C, Fink G (1991) Distribution of glucocorticoid and mineralocorticoid receptor messenger RNA expression in human postmortem hippocampus. Brain Res 561(2):332-337. doi:10.1016/0006-8993(91) 91612-5
77. Sinclair D, Webster MJ, Wong J, Weickert CS (2010) Dynamic molecular and anatomical changes in the glucocorticoid receptor in human cortical development. Mol Psychiatry. doi:10.1038/mp.2010.28
78. Sinclair D, Tsai SY, Woon HG, Weickert CS (2011) Abnormal glucocorticoid receptor mRNA and protein isoform expression in the prefrontal cortex in psychiatric illness. Neuropsychopharmacology 36(13):2698-2709. doi:10.1038/npp.2011.160
79. Sinclair D, Webster MJ, Fullerton JM, Weickert CS (2012) Glucocorticoid receptor mRNA and protein isoform alterations in the orbitofrontal cortex in schizophrenia and bipolar disorder. BMC Psychiatry 12:84. doi:10.1186/1471-244X- 12-84
80. Stockmeier CA, Mahajan GJ, Konick LC, Overholser JC, Jurjus GJ, Meltzer HY, Uylings HB, Friedman L, Rajkowska G (2004) Cellular changes in the postmortem hippocampus in major depression. Biol Psychiatry 56(9):640-650. doi:10.1016/j.biopsych.2004.08.022 (Pubitemid 39446845)
81. Swaab DF, Bao AM, Lucassen PJ (2005) The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 4(2):141-194. doi:10.1016/j.arr.2005.03.003 (Pubitemid 41114861)
82. Tham MW, Woon PS, Sum MY, Lee TS, Sim K (2011) White matter abnormalities in major depression: evidence from post-mortem, neuroimaging and genetic studies. J Affect Disord 132(1-2):26-36. doi:10.1016/j.jad.2010.09.013
83. Turner JD, Muller CP (2005) Structure of the glucocorticoid receptor (NR3C1) gene 5′ untranslated region: identification, and tissue distribution of multiple new human exon 1. J Mol Endocrinol 35(2):283-292. doi:10.1677/jme.1.01822 (Pubitemid 41556176)
84. van de Nes JA, Kamphorst W, Ravid R, Swaab DF (1998) 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 Neuropathologica 96(2):129-138 (Pubitemid 28356525)
85. Virgin CE Jr, Ha TP, Packan DR, Tombaugh GC, Yang SH, Horner HC, Sapolsky RM (1991) Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J Neurochem 57(4):1422-1428 (Pubitemid 21922771)
86. Wang SS, Kamphuis W, Huitinga I, Zhou JN, Swaab DF (2008) Gene expression analysis in the human hypothalamus in depression by laser microdissection and real-time PCR: the presence of multiple receptor imbalances. Mol Psychiatry 13(8):786-799, 741. doi:10.1038/mp.2008.38
87. Wang Q, Joels M, Swaab DF, Lucassen PJ (2012) Hippocampal GR expression is increased in elderly depressed females. Neuropharmacology 62(1):527-533. doi:10.1016/j.neuropharm.2011.09.014
88. Wang Q, Van Heerikhuize J, Aronica E, Kawata M, Seress L, Joels M, Swaab DF, Lucassen PJ (2013) Glucocorticoid receptor protein expression in human hippocampus; stability with age. Neurobiol Aging. doi:10.1016/j.neurobiolaging. 2012.11.019
89. Welberg LA, Seckl JR, Holmes MC (2000) Inhibition of 11beta- hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur J Neurosci 12(3):1047-1054 (Pubitemid 30168784)
90. Wickert L, Selbig J, Watzka M, Stoffel-Wagner B, Schramm J, Bidlingmaier F, Ludwig M (2000) Differential mRNA expression of the two mineralocorticoid receptor splice variants within the human brain: structure analysis of their different DNA binding domains. J Neuroendocrinol 12(9):867-873 pii:jne535
91. Xing GQ, Russell S, Webster MJ, Post RM (2004) Decreased expression of mineralocorticoid receptor mRNA in the prefrontal cortex in schizophrenia and bipolar disorder. Int J Neuropsychopharmacol 7(2):143-153. doi:10.1017/ S1461145703004000 (Pubitemid 38823281)
92. Yi SJ, Masters JN, Baram TZ (1994) Glucocorticoid receptor mRNA ontogeny in the fetal and postnatal rat forebrain. Mol Cell Neurosci 5(5):385-393. doi:10.1006/mcne.1994.1048 (Pubitemid 24314409)
93. Young EA, Altemus M, Lopez JF, Kocsis JH, Schatzberg AF, DeBattista C, Zubieta JK (2004) HPA axis activation in major depression and response to fluoxetine: a pilot study. Psychoneuroendocrinology 29(9):1198-1204. doi:10.1016/j.psyneuen. 2004.02.002
94. Zobel A, Jessen F, von Widdern O, Schuhmacher A, Hofels S, Metten M, Rietschel M, Scheef L, Block W, Becker T, Schild HH, Maier W, Schwab SG (2008) Unipolar depression and hippocampal volume: impact of DNA sequence variants of the glucocorticoid receptor gene. Am J Med Genet B Neuropsychiatr Genet 147B(6):836-843. doi:10.1002/ajmg.b.30709