Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed

Psychoneuroendocrinology

Volumn 35, Issue 4, 2010, Pages 544-556

  Alt, Simone R ^a,b   Turner, Jonathan D ^a,b   Klok, Melanie D ^c   Meijer, Onno C ^c   Lakke, Egbert A J F ^d   DeRijk, Roel H ^c,d   Muller, Claude P ^a,b  

^a LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^b UNIVERSITY OF TRIER   (Germany)

^c LEIDEN UNIVERSITY   (Netherlands)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Alternative transcripts; Epigenetics; Glucocorticoid receptor; Major depressive disorder; MRNA expression; Pyrosequencing

Indexed keywords

BENZODIAZEPINE DERIVATIVE; EARLY GROWTH RESPONSE FACTOR 1; GENOMIC DNA; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOID RECEPTOR ALPHA; GLUCOCORTICOID RECEPTOR BETA; HALOPERIDOL; SEROTONIN UPTAKE INHIBITOR; TRICYCLIC ANTIDEPRESSANT AGENT;

ADULT; AGED; AMYGDALOID NUCLEUS; ARTICLE; AUTOPSY; BEHAVIOR GENETICS; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; EXON; FEMALE; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIMBIC SYSTEM; MAJOR DEPRESSION; MALE; PRIORITY JOURNAL; PROMOTER REGION;

EID: 77950689477     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2009.09.001     Document Type: Article

References (70)

1. Bamberger C.M., Bamberger A.M., de Castro M., Chrousos G.P. Glucocorticoid receptor beta, a potential endogenous inhibitor of glucocorticoid action in humans. J. Clin. Invest. 1995, 95:2435-2441.
2. Battle C.L., Shea M.T., Johnson D.M., Yen S., Zlotnick C., Zanarini M.C., Sanislow C.A., Skodol A.E., Gunderson J.G., Grilo C.M., McGlashan T.H., Morey L.C. Childhood maltreatment associated with adult personality disorders: findings from the Collaborative Longitudinal Personality Disorders Study. J. Pers. Disord. 2004, 18:193-211.
3. Bifulco A., Brown G.W., Adler Z. Early sexual abuse and clinical depression in adult life. Br. J. Psychiatry 1991, 159:115-122.
4. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002, 16:6-21.
5. Bird A. Perceptions of epigenetics. Nature 2007, 447:396-398.
6. Bjartmar L., Johansson I.M., Marcusson J., Ross S.B., Seckl J.R., Olsson T. 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 (Berl.) 2000, 151:7-12.
7. Boyle M.P., Brewer J.A., Funatsu M., Wozniak D.F., Tsien J.Z., Izumi Y., Muglia L.J. Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:473-478.
8. Breslin M.B., Geng C.D., Vedeckis W.V. Multiple promoters exist in the human GR gene, one of which is activated by glucocorticoids. Mol. Endocrinol. 2001, 15:1381-1395.
9. Breslin M.B., Vedeckis W.V. The human glucocorticoid receptor promoter upstream sequences contain binding sites for the ubiquitous transcription factor, Yin Yang 1. J. Steroid Biochem. Mol. Biol. 1998, 67:369-381.
10. Brown G.R., Anderson B. Psychiatric morbidity in adult inpatients with childhood histories of sexual and physical abuse. Am. J. Psychiatry 1991, 148:55-61.
11. Chourbaji S., Vogt M.A., Gass P. Mice that under- or overexpress glucocorticoid receptors as models for depression or posttraumatic stress disorder. Prog. Brain Res. 2008, 167:65-77.
12. Danese A., Moffitt T.E., Pariante C.M., Ambler A., Poulton R., Caspi A. Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Arch. Gen. Psychiatry 2008, 65:409-415.
13. de Kloet E.R., Joels M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
14. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19:269-301.
15. Dejeux E., El abdalaoui H., Gut I.G., Tost J. Identification and quantification of differentially methylated loci by the pyrosequencing technology. Methods Mol. Biol. 2009, 507:189-205.
16. DeRijk R.H., Schaaf M., Stam F.J., de Jong I.E., Swaab D.F., Ravid R., Vreugdenhil E., Cidlowski J.A., de Kloet E.R., Lucassen P.J. 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. 2003, 116:17-26.
17. Encio I.J., Detera-Wadleigh S.D. The genomic structure of the human glucocorticoid receptor. J. Biol. Chem. 1991, 266:7182-7188.
18. Geng C.D., Schwartz J.R., Vedeckis W.V. A conserved molecular mechanism is responsible for the auto-up-regulation of glucocorticoid receptor gene promoters. Mol. Endocrinol. 2008, 22:2624-2642.
19. Geng C.D., Vedeckis W.V. c-Myb and members of the c-Ets family of transcription factors act as molecular switches to mediate opposite steroid regulation of the human glucocorticoid receptor 1A promoter. J. Biol. Chem. 2005, 280:43264-43271.
20. Hagendorf A., Koper J.W., de Jong F.H., Brinkmann A.O., Lamberts S.W., Feelders R.A. Expression of the human glucocorticoid receptor splice variants alpha, beta, and P in peripheral blood mononuclear leukocytes in healthy controls and in patients with hyper- and hypocortisolism. J. Clin. Endocrinol. Metab. 2005, 90:6237-6243.
21. Heim C., Mletzko T., Purselle D., Musselman D.L., Nemeroff C.B. The dexamethasone/corticotropin-releasing factor test in men with major depression: role of childhood trauma. Biol. Psychiatry 2008, 63:398-405.
22. Heim C., Nemeroff C.B. Neurobiology of early life stress: clinical studies. Semin. Clin. Neuropsychiatry 2002, 7:147-159.
23. Heydendael W., Jacobson L. Differential effects of imipramine and phenelzine on corticosteroid receptor gene expression in mouse brain: potential relevance to antidepressant response. Brain Res. 2008, 1238:93-107.
24. Holliday R., Pugh J.E. DNA modification mechanisms and gene activity during development. Science 1975, 187:226-232.
25. Holsboer F. Implications of altered limbic-hypothalamic-pituitary-adrenocortical (LHPA)-function for neurobiology of depression. Acta Psychiatr. Scand. Suppl. 1988, 341:72-111.
26. Jacobson L., Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 1991, 12:118-134.
27. Jumper S.A. A meta-analysis of the relationship of child sexual abuse to adult psychological adjustment. Child Abuse Negl. 1995, 19:715-728.
28. Juruena M.F., Cleare A.J., Papadopoulos A.S., Poon L., Lightman S., Pariante C.M. Different responses to dexamethasone and prednisolone in the same depressed patients. Psychopharmacology (Berl.) 2006, 189:225-235.
29. Kendler K.S., Bulik C.M., Silberg J., Hettema J.M., Myers J., Prescott C.A. Childhood sexual abuse and adult psychiatric and substance use disorders in women: an epidemiological and cotwin control analysis. Arch. Gen. Psychiatry 2000, 57:953-959.
30. Kessler R.C., Crum R.M., Warner L.A., Nelson C.B., Schulenberg J., Anthony J.C. Lifetime co-occurrence of DSM-III-R alcohol abuse and dependence with other psychiatric disorders in the National Comorbidity Survey. Arch. Gen. Psychiatry 1997, 54:313-321.
31. Knable M.B., Barci B.M., Webster M.J., Meador-Woodruff J., Torrey E.F. Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol. Psychiatry 2004, 9:609-620. 544.
32. Koga Y., Matsuzaki A., Suminoe A., Hattori H., Kanemitsu S., Hara T. Differential mRNA expression of glucocorticoid receptor alpha and beta is associated with glucocorticoid sensitivity of acute lymphoblastic leukemia in children. Pediatr. Blood Cancer 2005, 45:121-127.
33. Lewis-Tuffin L.J., Cidlowski J.A. The physiology of human glucocorticoid receptor beta (hGRbeta) and glucocorticoid resistance. Ann. N. Y. Acad. Sci. 2006, 1069:1-9.
34. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
35. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
36. Longui C.A., Vottero A., Adamson P.C., Cole D.E., Kino T., Monte O., Chrousos G.P. Low glucocorticoid receptor alpha/beta ratio in T-cell lymphoblastic leukemia. Horm. Metab. Res. 2000, 32:401-406.
37. Lu W., Mueser K.T., Rosenberg S.D., Jankowski M.K. Correlates of adverse childhood experiences among adults with severe mood disorders. Psychiatr. Serv. 2008, 59:1018-1026.
38. McCauley J., Kern D.E., Kolodner K., Dill L., Schroeder A.F., DeChant H.K., Ryden J., Derogatis L.R., Bass E.B. Clinical characteristics of women with a history of childhood abuse: unhealed wounds. JAMA 1997, 277:1362-1368.
39. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009, 12:342-348.
40. Moser D., Molitor A., Kumsta R., Tatschner T., Riederer P., Meyer J. The glucocorticoid receptor gene exon 1-F promoter is not methylated at the NGFI-A binding site in human hippocampus. World J. Biol. Psychiatry 2007, 8:262-268.
41. Mullen P.E., Martin J.L., Anderson J.C., Romans S.E., Herbison G.P. Childhood sexual abuse and mental health in adult life. Br. J. Psychiatry 1993, 163:721-732.
42. Nemeroff C.B., Heim C.M., Thase M.E., Klein D.N., Rush A.J., Schatzberg A.F., Ninan P.T., McCullough J.P., Weiss P.M., Dunner D.L., Rothbaum B.O., Kornstein S., Keitner G., Keller M.B. Differential responses to psychotherapy versus pharmacotherapy in patients with chronic forms of major depression and childhood trauma. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14293-14296.
43. Nobukuni Y., Smith C.L., Hager G.L., Detera-Wadleigh S.D. Characterization of the human glucocorticoid receptor promoter. Biochemistry 1995, 34:8207-8214.
44. Nunez B.S., Vedeckis W.V. Characterization of promoter 1B in the human glucocorticoid receptor gene. Mol. Cell. Endocrinol. 2002, 189:191-199.
45. Oakley R.H., Sar M., Cidlowski J.A. The human glucocorticoid receptor beta isoform. Expression, biochemical properties, and putative function. J. Biol. Chem. 1996, 271:9550-9559.
46. Oberlander T.F., Weinberg J., Papsdorf M., Grunau R., Misri S., Devlin A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008, 3:97-106.
47. Pariante C.M., Lightman S.L. The HPA axis in major depression: classical theories and new developments. Trends Neurosci. 2008, 31:464-468.
48. Pedersen K.B., Vedeckis W.V. Quantification and glucocorticoid regulation of glucocorticoid receptor transcripts in two human leukemic cell lines. Biochemistry 2003, 42:10978-10990.
49. Pickering B.M., Willis A.E. The implications of structured 5′ untranslated regions on translation and disease. Semin. Cell Dev. Biol. 2005, 16:39-47.
50. Presul E., Schmidt S., Kofler R., Helmberg A. Identification, tissue expression, and glucocorticoid responsiveness of alternative first exons of the human glucocorticoid receptor. J. Mol. Endocrinol. 2007, 38:79-90.
51. Riggs A.D. X inactivation, differentiation, and DNA methylation. Cytogenet. Cell Genet. 1975, 14:9-25.
52. Rinne T., de Kloet E.R., Wouters L., Goekoop J.G., DeRijk R.H., van den Brink W. Hyperresponsiveness of hypothalamic-pituitary-adrenal axis to combined dexamethasone/corticotropin-releasing hormone challenge in female borderline personality disorder subjects with a history of sustained childhood abuse. Biol. Psychiatry 2002, 52:1102-1112.
53. Russcher H., Dalm V.A., de Jong F.H., Brinkmann A.O., Hofland L.J., Lamberts S.W., Koper J.W. Associations between promoter usage and alternative splicing of the glucocorticoid receptor gene. J. Mol. Endocrinol. 2007, 38:91-98.
54. Schote A.B., Turner J.D., Schiltz J., Muller C.P. Nuclear receptors in human immune cells: expression and correlations. Mol. Immunol. 2007, 44:1436-1445.
55. Shahidi H., Vottero A., Stratakis C.A., Taymans S.E., Karl M., Longui C.A., Chrousos G.P., Daughaday W.H., Gregory S.A., Plate J.M. Imbalanced expression of the glucocorticoid receptor isoforms in cultured lymphocytes from a patient with systemic glucocorticoid resistance and chronic lymphocytic leukemia. Biochem. Biophys. Res. Commun. 1999, 254:559-565.
56. Shrivastava A., Calame K. An analysis of genes regulated by the multi-functional transcriptional regulator Yin Yang-1. Nucleic Acids Res. 1994, 22:5151-5155.
57. Siegel S., Castellan N.J. Nonparametric Statistics for the Behavioral Sciences 1988, McGraw-Hill Book Co., New York. 2nd ed.
58. Tichomirowa M.A., Keck M.E., Schneider H.J., Paez-Pereda M., Renner U., Holsboer F., Stalla G.K. Endocrine disturbances in depression. J. Endocrinol. Invest. 2005, 28:89-99.
59. Turner J.D., Muller C.P. Structure of the glucocorticoid receptor (NR3C1) gene 5′ untranslated region: identification, and tissue distribution of multiple new human exon 1. J. Mol. Endocrinol. 2005, 35:283-292.
60. Turner J.D., Pelascini L.P., Macedo J.A., Muller C.P. Highly individual methylation patterns of alternative glucocorticoid receptor promoters suggest individualized epigenetic regulatory mechanisms. Nucleic Acids Res. 2008, 36:7207-7218.
61. Turner J.D., Schote A.B., Macedo J.A., Pelascini L.P., Muller C.P. Tissue specific glucocorticoid receptor expression, a role for alternative first exon usage?. Biochem. Pharmacol. 2006, 72:1529-1537.
62. Wang S.S., Kamphuis W., Huitinga I., Zhou J.N., Swaab D.F. Gene expression analysis in the human hypothalamus in depression by laser microdissection and real-time PCR: the presence of multiple receptor imbalances. Mol. Psychiatry 2008, 13:786-799. 741.
63. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
64. Webster J.C., Oakley R.H., Jewell C.M., Cidlowski J.A. Proinflammatory cytokines regulate human glucocorticoid receptor gene expression and lead to the accumulation of the dominant negative beta isoform: a mechanism for the generation of glucocorticoid resistance. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6865-6870.
65. Webster M.J., Knable M.B., O'Grady J., Orthmann J., Weickert C.S. Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders. Mol. Psychiatry 2002, 7:985-994. 924.
66. Weiss E.L., Longhurst J.G., Mazure C.M. Childhood sexual abuse as a risk factor for depression in women: psychosocial and neurobiological correlates. Am. J. Psychiatry 1999, 156:816-828.
67. Widom C.S., DuMont K., Czaja S.J. A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Arch. Gen. Psychiatry 2007, 64:49-56.
68. Yau J.L., Noble J., Chapman K.E., Seckl J.R. Differential regulation of variant glucocorticoid receptor mRNAs in the rat hippocampus by the antidepressant fluoxetine. Brain Res. Mol. Brain Res. 2004, 129:189-192.
69. Young E.A., Abelson J.L., Curtis G.C., Nesse R.M. Childhood adversity and vulnerability to mood and anxiety disorders. Depress. Anxiety 1997, 5:66-72.
70. Young E.A., Lopez J.F., Murphy-Weinberg V., Watson S.J., Akil H. Mineralocorticoid receptor function in major depression. Arch. Gen. Psychiatry 2003, 60:24-28.