Previous history of chronic stress changes the transcriptional response to glucocorticoid challenge in the dentate gyrus region of the male rat hippocampus

Endocrinology

Volumn 154, Issue 9, 2013, Pages 3261-3272

  Datson, Nicole A ^a,b   Van Den Oever, Jessica M E ^a   Korobko, Oksana B ^a   Magarinos, Ana Maria ^c   De Kloet, E Ronald ^a,b   McEwen, Bruce S ^c  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ARTICLE; CHROMATIN STRUCTURE; CHRONIC STRESS; CONTROLLED STUDY; DENTATE GYRUS; EPIGENETICS; GENE EXPRESSION; GENE IDENTIFICATION; HIPPOCAMPUS; MALE; MICROARRAY ANALYSIS; MOLECULAR MECHANICS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSCRIPTION INITIATION;

ALLOSTASIS; ANIMALS; CHRONIC DISEASE; DENTATE GYRUS; DEPRESSION; DISEASE SUSCEPTIBILITY; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; MALE; NERVE TISSUE PROTEINS; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PSYCHOTIC DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84883184667     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2233     Document Type: Article

References (83)

1. McEwen BS, Eiland L, Hunter RG, Miller MM. Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology. 2012;62:3-12.
2. de Kloet ER, Joëls M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005;6:463-475.
3. Reul JM, de Kloet ER.Tworeceptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology. 1985;117:2505-2511.
4. Datson NA, van der Perk J, de Kloet ER, Vreugdenhil E. Identification of corticosteroid-responsive genes in rat hippocampus using serial analysis of gene expression. Eur J Neurosci. 2001;14:675-689.
5. Maras PM, Baram TZ. Sculpting the hippocampus from within: stress, spines, and CRH. Trends Neurosci. 2012;35:315-324.
6. Lucassen PJ, Heine VM, Muller MB, et al. Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets. 2006; 5:531-546.
7. Alfarez DN, Joëls M, Krugers HJ. Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci. 2003;17:1928-1934.
8. Bodnoff SR, Humphreys AG, Lehman JC, DiamondDM,RoseGM, Meaney MJ. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J Neurosci. 1995;15:61-69.
9. Krugers HJ, Goltstein PM, van der Linden S, Joëls M. Blockade of glucocorticoid receptors rapidly restores hippocampalCA1synaptic plasticity after exposure to chronic stress. Eur J Neurosci. 2006;23: 3051-3055.
10. Cameron HA, Tanapat P, Gould E. Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience. 1998;82:349-354.
11. Czéh B, Michaelis T, Watanabe T, et al. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA. 2001;98:12796-12801.
12. Gould E, Daniels DC, Cameron HA, McEwen BS. Expression of adrenal steroid receptors by newly born cells and pyknotic cells in the dentate gyrus of the postnatal rat. Mol Cell Neurosci. 1992;3: 44-48.
13. Lucassen PJ, Meerlo P, Naylor AS, et al. Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: implications for depression and antidepressant action. Eur Neuropsychopharmacol. 2010;20:1-17.
14. Fitzsimons CP, van Hooijdonk LW, Schouten M, et al. Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior [published online August 28, 2012]. Mol Psychiatry. doi: 10.1038/mp.2012.123.
15. Aimone JB, Wiles J, Gage FH. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci. 2006;9: 723-727.
16. Dupret D, Revest JM, Koehl M, et al. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One. 2008;3: e1959.
17. Silva AJ, Zhou Y, Rogerson T, Shobe J, Balaji J. Molecular and cellular approaches to memory allocation in neural circuits. Science. 2009;326:391-395.
18. Boldrini M, UnderwoodMD,Hen R, et al. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology. 2009;34:2376-2389.
19. Czéh B, Lucassen PJ. What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci. 2007;257:250-260.
20. Bilang-Bleuel A, Ulbricht S, Chandramohan Y, De Carli S, Droste SK, Reul JM. Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: involvement in a glucocorticoid receptor-dependent behavioural response. Eur J Neurosci. 2005;22:1691-1700.
21. ChandramohanY, Droste SK, Reul JM. Novelty stress induces phospho-acetylation of histone H3 in rat dentate gyrus granule neurons through coincident signalling via the N-methyl-D-aspartate receptor and the glucocorticoid receptor: relevance for c-fos induction. J Neurochem. 2007;101:815-828.
22. Hunter RG, McCarthy KJ, Milne TA, Pfaff DW, McEwen BS. Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci USA. 2009;106:20912-20917.
23. Hunter RG, Murakami G, Dewell S, et al. Acute stress and hippocampal histone H3 lysine 9 trimethylation, a retrotransposon silencing response. Proc Natl Acad SciUSA. 2012;109:17657-17662.
24. Datson NA, Morsink MC, Meijer OC, de Kloet ER. Central corticosteroid actions: search for gene targets. Eur J Pharmacol. 2008; 583:272-289.
25. Datson NA, Speksnijder N, Mayer JL, et al. The transcriptional response to chronic stress and glucocorticoid receptor blockade in the hippocampal dentate gyrus. Hippocampus. 2012;22:359-371.
26. Polman JA, Hunter RG, Speksnijder N, et al. Glucocorticoids modulate the mTOR pathway in the hippocampus: differential effects depending on stress history. Endocrinology. 2012;153:4317-4327.
27. Datson NA, Meijer L, Steenbergen PJ, et al. Expression profiling in laser-microdissected hippocampal subregions in rat brain reveals large subregion-specific differences in expression. Eur J Neurosci. 2004;20:2541-2554.
28. Smyth G. Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor. New York, New York: Springer. 2005;397-420.
29. Duncan D, Prodduturi N, Zhang B. WebGestalt2: an updated and expanded version of the Web-based Gene Set Analysis Toolkit.BMC Bioinformatics. 2010;11:1-1.
30. Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 2005;33:W741-W748.
31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(Δ ΔC(T)) method. Methods. 2001;25:402-408.
32. Bagamasbad P, Ziera T, Borden SA, et al. Molecular basis for glucocorticoid induction of the kruppel-like factor 9 gene in hippocampal neurons. Endocrinology. 2012;153:5334-5345.
33. Grunewald M, Johnson S, Lu D, et al. Mechanistic role for a novel glucocorticoid-KLF11 (TIEG2) protein pathway in stress-induced monoamine oxidase A expression. J Biol Chem. 2012;287:24195-24206.
34. Smith MA, Makino S, Kvetnansky R, Post RM. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci. 1995; 15:1768-1777.
35. Zahnow CA, Panula P, Yamatodani A, Millhorn DE. Glucocorticoid hormones downregulate histidine decarboxylase mRNA and enzyme activity in rat lung. Am J Physiol. 1998;275:L407-L413.
36. Frank MG, Der-Avakian A, Bland ST, Watkins LR, Maier SF. Stress-induced glucocorticoids suppress the antisense molecular regulation of FGF-2 expression. Psychoneuroendocrinology. 2007;32: 376-384.
37. Kelly EJ, Sandgren EP, Brinster RL, Palmiter RD. A pair of adjacent glucocorticoid response elements regulate expression of two mouse metallothionein genes. Proc Natl Acad Sci USA. 1997;94:10045-10050.
38. He W, Meng T, Wu M, Shi B, Lu SJ, Li CH. Perturbation of Fgf10 signal pathway in mouse embryonic palate by dexamethasone and vitamin B12 in vivo. J Pediatr Surg. 2010;45:2030-2035.
39. Shimojo M, Hiroi N, Yakushiji F, Ueshiba H, Yamaguchi N, Miyachi Y. Differences in down-regulation of glucocorticoid receptor mRNA by cortisol, prednisolone and dexamethasone in HeLa cells. Endocr J. 1995;42:629-636.
40. Chuquet J, Quilichini P, Nimchinsky EA, Buzsáki G. Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. J Neurosci. 2010;30: 15298-15303.
41. Jakoby P, Schmidt E, Ruminot I, Gutiérrez R, Barros LF, Deitmer JW. Higher transport and metabolism of glucose in astrocytes compared with neurons: a multiphoton study of hippocampal and cerebellar tissue slices [published online January 25, 2013]. Cereb Cortex. doi:10.1093/cercor/bhs309
42. van Gemert NG, Joëls M. Effect of chronic stress and mifepristone treatment on voltage-dependent Ca2+ currents in rat hippocampal dentate gyrus. J Neuroendocrinol. 2006;18:732-741.
43. Lipstein N, Schaks S, Dimova K, et al. Nonconserved Ca(2+)/calmodulin binding sites in Munc13s differentially control synaptic short-term plasticity. Mol Cell Biol. 2012;32:4628-4641.
44. Upadhya MA, Nakhate KT, Kokare DM, Singru PS, Subhedar NK. Cocaine- and amphetamine-regulated transcript peptide increases spatial learning and memory in rats. Life Sci. 2011;88:322-334.
45. Schmitt U, Hiemke C, Fahrenholz F, Schroeder A. Over-expression of two different forms of the &alpha-secretase ADAM10 affects learning and memory in mice. Behav Brain Res. 2006;175:278-284.
46. Heine VM, Maslam S, Zareno J, Joëls M, Lucassen PJ. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci. 2004;19: 131-144.
47. Selye H. Stress in Health and Disease. Boston, Massachusetts: Butterworths; 1976.
48. Karst H, Joëls M. Effect of chronic stress on synaptic currents in rat hippocampal dentate gyrus neurons. J Neurophysiol. 2003;89:625-633.
49. Heim C, Binder EB. Current research trends in early life stress and depression: review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Exp Neurol. 2012;233: 102-111.
50. Mueller BR, Bale TL. Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci. 2008;28:9055-9065.
51. Murgatroyd C, Patchev AV, Wu Y, et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci. 2009;12:1559-1566.
52. Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7:847-854.
53. Gutièrrez-Mecinas M, Trollope AF, Collins A, et al. Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proc Natl Acad Sci USA. 2011;108:13806-13811.
54. Daganzo SM, Erzberger JP, Lam WM, et al. Structure and function of the conserved core of histone deposition protein Asf1. Curr Biol. 2003;13:2148-2158.
55. Gregory GD, Vakoc CR, Rozovskaia T, et al. Mammalian ASH1L is a histone methyltransferase that occupies the transcribed region of active genes. Mol Cell Biol. 2007;27:8466-8479.
56. Tanaka Y, Katagiri Z, Kawahashi K, Kioussis D, Kitajima S. Trithorax-group protein ASH1 methylates histone H3 lysine 36. Gene. 2007;397:161-168.
57. Fessing MY, Mardaryev AN, Gdula MR, et al. p63 regulates Satb1 to control tissue-specific chromatin remodeling during development of the epidermis. J Cell Biol. 2011;194:825-839.
58. Keyes WM, Pecoraro M, Aranda V, et al. ΔNp63α is an oncogene that targets chromatin remodeler Lsh to drive skin stem cell proliferation and tumorigenesis. Cell Stem Cell. 2011;8:164-176.
59. Jin M, Wang XM, Tu Y, et al. The negative cell cycle regulator, Tob (transducer of ErbB-2), is a multifunctional protein involved in hippocampus-dependent learning and memory. Neuroscience. 2005; 131:647-659.
60. Kerman IA, Bernard R, Bunney WE, et al. Evidence for transcriptional factor dysregulation in the dorsal raphe nucleus of patients with major depressive disorder. Front Neurosci. 2012;6:135.
61. Bezchlibnyk YB, Wang JF, McQueen GM, Young LT. Gene expression differences in bipolar disorder revealed by cDNA array analysis of post-mortem frontal cortex. J Neurochem. 2001;79: 826-834.
62. Etain B, Milhiet V, Bellivier F, Leboyer M. Genetics of circadian rhythms and mood spectrum disorders. Eur Neuropsychopharmacol. 2011;21:S676-S682.
63. Kripke DF, Nievergelt CM, Joo E, Shekhtman T, Kelsoe Jr. Circadian polymorphisms associated with affective disorders. J Circadian Rhythms 2009;7.
64. Gibbs JE, Blaikley J, Beesley S, et al. The nuclear receptor REVERB α mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci USA. 2012;109:582-587.
65. Seo S, Lomberk G, Mathison A, et al. Krüppel-like factor 11 differentially couples to histone acetyltransferase and histone methyltransferase chromatin remodeling pathways to transcriptionally regulate dopamineD2receptor in neuronal cells. J Biol Chem. 2012; 287:12723-12735.
66. Meyer JH, Ginovart N, Boovariwala A, et al. Elevated monoamine oxidase a levels in the brain: an explanation for the monoamine imbalance of major depression. Arch Gen Psychiatry. 2006;63: 1209.
67. McKernan DP, Dinan TG, Cryan JF. "Killing the Blues": a role for cellular suicide (apoptosis) in depression and the antidepressant response? Prog Neurobiol. 2009;88:246-263.
68. Gould E, Tanapat P. Stress and hippocampal neurogenesis. Biol Psychiatry. 1999;46:1472-1479.
69. Mirescu C, Gould E. Stress and adult neurogenesis. Hippocampus. 2006;16:233-238.
70. Oomen CA, Mayer JL, de Kloet ER, Joëls M, Lucassen PJ. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci. 2007;26:3395-3401.
71. Gray JD, Milner TA, McEwen BS. Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience. 2013;239:214-227.
72. Feldker DE, Morsink MC, Veenema AH, et al. The effect of chronic exposure to highly aggressive mice on hippocampal gene expression of non-aggressive subordinates. Brain Res. 2006;1089:10-20.
73. Albensi BC, Mattson MP. Evidence for the involvement of TNF and NF-κB in hippocampal synaptic plasticity. Synapse. 2000;35:151-159.
74. YouZ, Luo C, ZhangW,et al. Pro- and anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: involvement in depression. Behav Brain Res. 2011;225:135-141.
75. Koo JW, Duman RS. IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci USA. 2008;105:751-756.
76. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 2003;302:1760-1765.
77. Goshen I, Kreisel T, Ben-Menachem-Zidon O, et al. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry. 2008;13:717-728.
78. Khairova RA, Machado-Vieira R, Du J, Manji HK. A potential role for pro-inflammatory cytokines in regulating synaptic plasticity in major depressive disorder. Int J Neuropsychopharmacol. 2009;12: 561-578.
79. Bekinschtein P, Katche C, Slipczuk LN, et al.mTORsignaling in the hippocampus is necessary for memory formation. Neurobiol Learn Mem. 2007;87:303-307.
80. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, Schuman EM. A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci USA. 2002;99:467-472.
81. Li N, Lee B, Liu RJ, et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science. 2010;329:959-964.
82. Chandran A, Iyo AH, Jernigan CS, Legutko B, Austin MC, Karolewicz B. Reduced phosphorylation of the mTOR signaling pathway components in the amygdala of rats exposed to chronic stress. Prog Neuropsychopharmacol Biol Psychiatry. 2012;40C:240-245.
83. Jernigan CS, Goswami DB, Austin MC, et al. The mTOR signaling pathway in the prefrontal cortex is compromised in major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35: 1774-1779.