Epigenetics and the glucocorticoid receptor: A review of the implications in depression

Psychiatry Research

Volumn 242, Issue , 2016, Pages 349-356

  Farrell, Chloe ^a   O'Keane, Veronica ^a,b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ADELAIDE AND MEATH HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR;

CORTICOSTEROID RELEASE; DEPRESSION; DNA MODIFICATION; EPIGENETICS; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INCIDENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR GENE; REVIEW; STRESS; ANIMAL; GENE EXPRESSION; GENETIC EPIGENESIS; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MAJOR DEPRESSION; METABOLISM;

ANIMALS; DEPRESSION; DEPRESSIVE DISORDER; DEPRESSIVE DISORDER, MAJOR; EPIGENESIS, GENETIC; GENE EXPRESSION; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PITUITARY-ADRENAL SYSTEM; RECEPTORS, GLUCOCORTICOID;

EID: 84976320768     PISSN: 01651781     EISSN: 18727123     Source Type: Journal    
DOI: 10.1016/j.psychres.2016.06.022     Document Type: Review

References (60)

1. Alt, S.R., Turner, J.D., Klok, M.D., Meijer, O.C., Lakke, E.A.J.F., DeRijk, R.H., Muller, C.P., Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology 35 (2010), 544–556, 10.1016/j.psyneuen.2009.09.001.
2. American Psychiatric Association, 2013. Diagnostic and Statistical Manual of Mental Health Disorders, 5th ed. Arlington.
3. Anacker, C., Zunszain, P.A., Carvalho, L.A., Pariante, C.M., The glucocorticoid receptor: pivot of depression and of antidepressant treatment?. Psychoneuroendocrinology 36 (2011), 415–425, 10.1016/j.psyneuen.2010.03.007.
4. 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 34:Suppl 1 (2009), S186–S195, 10.1016/j.psyneuen.2009.05.021.
5. Bird, A., Perceptions of epigenetics. Nature 447 (2007), 396–398, 10.1038/nature05913.
6. Bremner, J.D., Childhood physical abuse and combat-related posttraumatic stress disorder in Vietnam veterans. Am. J. Psychiatry 150 (1993), 235–239, 10.1176/ajp.150.2.235.
7. Brummett, B.H., Krystal, A.D., Siegler, I.C., Kuhn, C., Surwit, R.S., Züchner, S., Ashley-Koch, A., Barefoot, J.C., Williams, R.B., Associations of a regulatory polymorphism of monoamine oxidase-A gene promoter (MAOA-uVNTR) with symptoms of depression and sleep quality. Psychosom. Med. 69 (2007), 396–401, 10.1097/PSY.0b013e31806d040b.
8. Calfa, G., Kademian, S., Ceschin, D., Vega, G., Rabinovich, A., Volosin, M., Characterization and functional significance of glucocorticoid receptors in patients with major depression: modulation by antidepressant treatment. Psychoneuroendocrinology 28 (2003), 687–701.
9. Caspi, A., et al. Influence of Life Stress on Depression: Moderation by a Polymorphism in the 5-HTT Gene. Science, 301, 2003, 386, 10.1126/science.1083968.
10. Cervilla, J.A., Rivera, M., Molina, E., Torres-Gonzalez, F., Bellon, J.A., Moreno, B., de Dios Luna, J., Lorente, J.A., de Diego-Otero, Y., King, M., Nazareth, I., Gutierrez, B., The 5-HTTLPR s/s genotype at the serotonin transporter gene (SLC6A4) increases the risk for depression in a large cohort of primary care attendees: the PREDICT-gene study. (PREDICT Study Core Group) Am. J. Med. Genet. B Neuropsychiatr. Genet. 141B (2006), 912–917.
11. Crick, F., Central dogma of molecular biology. Nature 227 (1970), 561–563, 10.1038/227561a0.
12. Delgado, P.L., Depression: the case for a monoamine deficiency. J. Clin. Psychiatry 61:Suppl 6 (2000), 7–11.
13. Frodl, T., Schüle, C., Schmitt, G., et al. Association of the brain-derived neurotrophic factor val66met polymorphism with reduced hippocampal volumes in major depression. Arch. Gen. Psychiatry 64 (2007), 410–416, 10.1001/archpsyc.64.4.410.
14. Fuchikami, M., Morinobu, S., Segawa, M., Okamoto, Y., Yamawaki, S., Ozaki, N., DNA methylation profiles of the brain-derived neurotrophic factor (BDNF) gene as a potent diagnostic biomarker in major depression. PLoS One, 2011, 6, 10.1371/journal.pone.0023881.
15. Hartmann, J., Wagner, K.V., Liebl, C., Scharf, S.H., Wang, X., Wolf, D., Hausch, M., Rein, F., Schmidt, T., Touma, U., Cheung-Flynn, C., Cox, J., Smith, M.B., Holsboer, D.F., Müller, F., Schmidt, M.V, M.B., The involvement of FK506-binding protein 51 (FKBP5) in the behavioral and neuroendocrine effects of chronic social defeat stress. Neuropharmacology 62 (2012), 332–339, 10.1016/j.neuropharm.2011.07.041.
16. Hayashi-Takanaka, Y., Yamagata, K., Wakayama, T., Stasevich, T.J., Kainuma, T., Tsurimoto, T., Tachibana, M., Shinkai, Y., Kurumizaka, H., Nozaki, N., Kimura, H., Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling. Nucleic Acids Res. 39 (2011), 6475–6488, 10.1093/nar/gkr343.
17. Helsen, C., Claessens, F., Looking at nuclear receptors from a new angle. Mol. Cell Endocrinol. 382 (2014), 97–106, 10.1016/j.mce.2013.09.009.
18. Hollenberg, S.M., Weinberger, C., Ong, E.S., Cerelli, G., Oro, A., Lebo, R., Thompson, E.B., Rosenfeld, M.G., Evans, R.M., Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 318 (1985), 635–641.
19. Holliday, R., Epigenetics: a historical overview. Epigenetics 1 (2006), 76–80.
20. Karege, F., Perret, G., Bondolfi, G., Schwald, M., Bertschy, G., Aubry, J.-M., Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res. 109 (2002), 143–148, 10.1016/S0165-1781(02)00005-7.
21. Kessler, R.C., The Effect of Stressful Life Events on Depression. Annu Rev. Psychol. 48 (1997), 191–214, 10.1146/annurev.psych.48.1.191.
22. Kessler, R.C., Magee, W.J., Childhood adversities and adult depression: basic patterns of association in a US national survey. Psychol. Med. 23 (1993), 679–690, 10.1017/S0033291700025460.
23. Kessler, R.C., McLaughlin, K.A., Green, J.G., Gruber, M.J., Sampson, N.A., Zaslavsky, A.M., Aguilar-Gaxiola, S., Alhamzawi, A.O., Alonso, J., Angermeyer, M., Benjet, C., Bromet, E., Chatterji, S., de Girolamo, G., Demyttenaere, K., Fayyad, J., Florescu, S., Gal, G., Gureje, O., Haro, J.M., Hu, C., Karam, E.G., Kawakami, N., Lee, S., Lépine, J.-P., Ormel, J., Posada-Villa, J., Sagar, R., Tsang, A., Üstün, T.B., Vassilev, S., Viana, M.C., Williams, D.R., Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br. J. Psychiatry 197 (2010), 378–385, 10.1192/bjp.bp.110.080499.
24. Klengel, T., Pape, J., Binder, E.B., Mehta, D., The role of DNA methylation in stress-related psychiatric disorders. Neuroepigenetic Disorders 80 (2014), 115–132, 10.1016/j.neuropharm.2014.01.013.
25. Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J.C., Pariante, C.M., Pace, T.W., Mercer, K.B., Mayberg, H.S., Bradley, B., Nemeroff, C.B., Holsboer, F., Heim, C.M., Ressler, K.J., Rein, T., Binder, E.B., Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat. Neurosci. 16 (2013), 33–41, 10.1038/nn.3275.
26. Kulis, Maher, DNA methylation and cancer. Adv. Genet 70 (2010), 27–56.
27. Kumar, R., Thompson, E.B., Gene regulation by the glucocorticoid receptor: structure: function relationship. J. Steroid Biochem. Mol. Biol. 94 (2005), 383–394, 10.1016/j.jsbmb.2004.12.046.
28. Lim, D., Maher, E., 2010. DNA methylation: a form of epigenetic control of gene expression, vol. 12, pp. 37–42. doi:10.1576/toag.12.1.037.27556.
29. Maes, M., Yirmyia, R., Noraberg, J., Brene, S., Hibbeln, J., Perini, G., Kubera, M., Bob, P., Lerer, B., Maj, M., The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab. Brain Dis. 24 (2009), 27–53, 10.1007/s11011-008-9118-1.
30. Matheson, S.L., Shepherd, A.M., Pinchbeck, R.M., Laurens, K.R., Carr, V.J., Childhood adversity in schizophrenia: a systematic meta-analysis. Psychol. Med. 43 (2013), 225–238, 10.1017/S0033291712000785.
31. McGowan, P.O., Sasaki, A., D'Alessio, A.C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., Meaney, M.J., Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12 (2009), 342–348, 10.1038/nn.2270.
32. Melas, P.A., Forsell, Y., Hypomethylation of MAOA's first exon region in depression: a replication study. Psychiatry Res. 226 (2015), 389–391, 10.1016/j.psychres.2015.01.003.
33. Menke, A., Klengel, T., Rubel, J., Brückl, T., Pfister, H., Lucae, S., Uhr, M., Holsboer, F., Binder, E.B., Genetic variation in FKBP5 associated with the extent of stress hormone dysregulation in major depression. Genes Brain Behav. 12 (2013), 289–296, 10.1111/gbb.12026.
34. 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 8 (2007), 262–268, 10.1080/15622970701429862.
35. Nagasawa, M., Ogino, Y., Kurata, K., Otsuka, T., Yoshida, J., Tomonaga, S., Furuse, M., Hypothesis with abnormal amino acid metabolism in depression and stress vulnerability in Wistar Kyoto rats. Amino Acids 43 (2012), 2101–2111, 10.1007/s00726-012-1294-y.
36. Necela, B.M., Cidlowski, J.A., Mechanisms of glucocorticoid receptor action in noninflammatory and inflammatory cells. Proc. Am. Thorac. Soc. 1 (2004), 239–246, 10.1513/pats.200402-005MS.
37. Nicolaides, N.C., Galata, Z., Kino, T., Chrousos, G.P., Charmandari, E., The human glucocorticoid receptor: molecular basis of biologic function. Steroids 75 (2010), 1–12, 10.1016/j.steroids.2009.09.002.
38. Nikolaus, S., Larisch, R., Beu, M., Vosberg, H., Müller-Gärtner, H.W., Diffuse cortical reduction of neuronal activity in unipolar major depression: a retrospective analysis of 337 patients and 321 controls. Nucl. Med Commun. 21 (2000), 1119–1125.
39. O'Keane, V., Frodl, T., Dinan, T.G., A review of Atypical depression in relation to the course of depression and changes in HPA axis organization. Psychoneuroendocrinology 37 (2012), 1589–1599, 10.1016/j.psyneuen.2012.03.009.
40. Oakley, R.H., Cidlowski, J.A., The biology of the glucocorticoid receptor: new signaling mechanisms in health and disease. J. Allergy Clin. Immunol. 132 (2013), 1033–1044, 10.1016/j.jaci.2013.09.007.
41. 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 3 (2008), 97–106.
42. Perroud, N., Paoloni-Giacobino, A., Prada, P., Olié, E., Salzmann, A., Nicastro, R., Guillaume, S., Mouthon, D., Stouder, C., Dieben, K., Huguelet, P., Courtet, P., Malafosse, A., Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma. Transl. Psychiatry, 1, 2011, e59, 10.1038/tp.2011.60.
43. Portela, A., Esteller, M., Epigenetic modifications and human disease. Nat. Biotechnol. 28 (2010), 1057–1068, 10.1038/nbt.1685.
44. Pynoos, R.S., Steinberg, A.M., Piacentini, J.C., A developmental psychopathology model of childhood traumatic stress and intersection with anxiety disorders. Biol. Psychiatry 46 (1999), 1542–1554.
45. Radtke, K.M., Ruf, M., Gunter, H.M., Dohrmann, K., Schauer, M., Meyer, A., Elbert, T., Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl. Psychiatry, 1, 2011, e21, 10.1038/tp.2011.21.
46. Radtke, K.M., Schauer, M., Gunter, H.M., Ruf-Leuschner, M., Sill, J., Meyer, A., Elbert, T., Epigenetic modifications of the glucocorticoid receptor gene are associated with the vulnerability to psychopathology in childhood maltreatment. Transl. Psychiatry, 5, 2015, e571.
47. Raison, C.L., Miller, A.H., The neuroimmunology of stress and depression. Semin Clin. Neuropsychiatry 6 (2001), 277–294.
48. Smart, C., Strathdee, G., Watson, S., Murgatroyd, C., McAllister-Williams, R.H., Early life trauma, depression and the glucocorticoid receptor gene – an epigenetic perspective. Psychol. Med. 45 (2015), 3393–3410, 10.1017/S0033291715001555.
49. Smoak, K.A., Cidlowski, J.A., Mechanisms of glucocorticoid receptor signaling during inflammation. Mech. Ageing Dev. 125 (2004), 697–706, 10.1016/j.mad.2004.06.010.
50. Swirnoff, A.H., Milbrandt, J., DNA-binding specificity of NGFI-A and related zinc finger transcription factors. Mol. Cell Biol. 15 (1995), 2275–2287.
51. 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. 35 (2005), 283–292, 10.1677/jme.1.01822.
52. Urdinguio, R.G., Sanchez-Mut, J.V., Esteller, M., Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. Lancet Neurol. 8 (2009), 1056–1072, 10.1016/S1474-4422(09)70262-5.
53. Weaver, I.C., Meaney, M.J., Szyf, M., Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl. Acad. Sci. USA 103 (2006), 3480–3485, 10.1073/pnas.0507526103.
54. Weaver, I.C., Champagne, F.A., Brown, S.E., Dymov, S., Sharma, S., Meaney, M.J., Szyf, M., Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 25 (2005), 11045–11054, 10.1523/JNEUROSCI.3652-05.2005.
55. 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. 7 (2004), 847–854, 10.1038/nn1276.
56. WHO, WHO Global Burden of Disease: 2004 Update. 2008.
57. WHO, 2001. The World Health Report 2001. Mental Health: New Understanding, New Hope.
58. Yehuda, R., Daskalakis, N.P., Lehrner, A., Desarnaud, F., Bader, H.N., Makotkine, I., Flory, J.D., Bierer, L.M., Meaney, M.J., Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring. Am. J. Psychiatry 171 (2014), 872–880, 10.1176/appi.ajp.2014.13121571.
59. Yehuda, R., Flory, J.D., Bierer, L.M., Henn-Haase, C., Lehrner, A., Desarnaud, F., Makotkine, I., Daskalakis, N.P., Marmar, C.R., Meaney, M.J., Lower Methylation of Glucocorticoid Receptor Gene Promoter 1F in Peripheral Blood of Veterans with Posttraumatic Stress Disorder. Biol. Psychiatry 77 (2015), 356–364, 10.1016/j.biopsych.2014.02.006.
60. Zhou, J., Cidlowski, J.A., The human glucocorticoid receptor: one gene, multiple proteins and diverse responses. Steroids 70 (2005), 407–417, 10.1016/j.steroids.2005.02.006.