Corticosterone targets distinct steps of synaptic transmission via concentration specific activation of mineralocorticoid and glucocorticoid receptors

Journal of Neurochemistry

Volumn 128, Issue 4, 2014, Pages 476-490

  Chatterjee, Sreejata ^a   Sikdar, Sujit K ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

corticosterone; glucocorticoid receptor; imaging; mEPSC; mineralocorticoid receptor; stress

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; IMAGING; MEPSC; MINERALOCORTICOID RECEPTOR; STRESS;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CORTICOSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT ANTIBODY TECHNIQUE; GLUTAMIC ACID; HIPPOCAMPUS; NERVE NET; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; POLYMERASE CHAIN REACTION; PRIMARY CELL CULTURE; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; RNA; SYNAPTIC TRANSMISSION;

EID: 84893853454     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12478     Document Type: Article

References (72)

1. Baxter A. W., and, Wyllie D. J., (2006) Phosphatidylinositol 3 kinase activation and AMPA receptor subunit trafficking underlie the potentiation of miniature EPSC amplitudes triggered by the activation of L-type calcium channels. J. Neurosci. 26, 5456-5469. (Pubitemid 44318398)
2. Beck S. G., Choi K. C., List T. J., Okuhara D. Y., and, Birnsteil S., (1996) Corticosterone alters 5-HT1A receptor-mediated hyperpolarization in area CA1 hippocampal pyramidal neurons. Neuropsychopharmacology 14, 27-33.
3. Brinks V., van der Mark M. H., de Kloet E. R., and, Oitzl M. S., (2007) Differential MR/GR activation in mice results in emotional states beneficial or impairing for cognition. Neural Plast 2007, 90163.
4. Calabrese E. J., and, Baldwin L. A., (2003) The hormetic dose-response model is more common than the threshold model in toxicology. Toxicol. Sci. 71, 246-250. (Pubitemid 36285016)
5. Castellino F., Heuser J., Marchetti S., Bruno B., and, Luini A., (1992) Glucocorticoid stabilization of actin filaments: a possible mechanism for inhibition of corticotropin release. Proc. Natl Acad. Sci. USA 89, 3775-3779.
6. Cereseto M., Reines A., Ferrero A., Sifonios L., Rubio M., and, Wikinski S., (2006) Chronic treatment with high doses of corticosterone decreases cytoskeletal proteins in the rat hippocampus. Eur. J. Neurosci. 24, 3354-3364. (Pubitemid 44952601)
7. Chameau P., Qin Y., Spijker S., Smit A. B., and, Joels M., (2007) Glucocorticoids specifically enhance L-type calcium current amplitude and affect calcium channel subunit expression in the mouse hippocampus. J. Neurophysiol. 97, 5-14. (Pubitemid 46143335)
8. Chantong B., Kratschmar D. V., Nashev L. G., Balazs Z., and, Odermatt A., (2012) Mineralocorticoid and glucocorticoid receptors differentially regulate NF-kappaB activity and pro-inflammatory cytokine production in murine BV-2 microglial cells. J. Neuroinflammation 9, 260.
9. Chung C., Barylko B., Leitz J., Liu X., and, Kavalali E. T., (2010) Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J. Neurosci. 30, 1363-1376.
10. Dallman M. F., Akana S. F., Scribner K. A., Bradbury M. J., Walker C. D., Strack A. M., and, Cascio C. S., (1992) Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J. Neuroendocrinol. 4, 517-526.
11. De Kloet E. R., Veldhuis H. D., Wagenaars J. L., and, Bergink E. W., (1984) Relative binding affinity of steroids for the corticosterone receptor system in rat hippocampus. J. Steroid. Biochem. 21, 173-178. (Pubitemid 14075014)
12. De Kloet E. R., Vreugdenhil E., Oitzl M. S., and, Joels M., (1998) Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19, 269-301. (Pubitemid 29117816)
13. Diamond M. I., Miner J. N., Yoshinaga S. K., and, Yamamoto K. R., (1990) Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249, 1266-1272.
14. Fredj N. B., and, Burrone J., (2009) A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat. Neurosci. 12, 751-758.
15. Groc L., Choquet D., and, Chaouloff F., (2008) The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat. Neurosci. 11, 868-870.
16. Groeneweg F. L., Karst H., de Kloet E. R., and, Joels M., (2011) Rapid non-genomic effects of corticosteroids and their role in the central stress response. J. Endocrinol. 209, 153-167.
17. Groffen A. J., Martens S., Diez Arazola R., et al,. (2010) Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science 327, 1614-1618.
18. Joels M., (2006) Corticosteroid effects in the brain: U-shape it. Trends Pharmacol. Sci. 27, 244-250.
19. Joels M., (2008) Functional actions of corticosteroids in the hippocampus. Eur. J. Pharmacol. 583, 312-321.
20. Joels M., and, de Kloet E. R., (1990) Mineralocorticoid receptor-mediated changes in membrane properties of rat CA1 pyramidal neurons in vitro. Proc. Natl Acad. Sci. USA 87, 4495-4498.
21. Karst H., and, Joels M., (2005) Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J. Neurophysiol. 94, 3479-3486. (Pubitemid 41504783)
22. Karst H., Wadman W. J., and, Joels M., (1994) Corticosteroid receptor-dependent modulation of calcium currents in rat hippocampal CA1 neurons. Brain Res. 649, 234-242. (Pubitemid 24197217)
23. Karst H., Berger S., Turiault M., Tronche F., Schutz G., and, Joels M., (2005) Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl Acad. Sci. USA 102, 19204-19207. (Pubitemid 43049590)
24. Kerr D. S., Campbell L. W., Hao S. Y., and, Landfield P. W., (1989) Corticosteroid modulation of hippocampal potentials: increased effect with aging. Science 245, 1505-1509. (Pubitemid 19243243)
25. Kerr D. S., Campbell L. W., Thibault O., and, Landfield P. W., (1992) Hippocampal glucocorticoid receptor activation enhances voltage-dependent Ca2+ conductances: relevance to brain aging. Proc. Natl Acad. Sci. USA 89, 8527-8531.
26. Kivell B. M., McDonald F. J., and, Miller J. H., (2000) Serum-free culture of rat post-natal and fetal brainstem neurons. Brain Res. Dev. Brain Res. 120, 199-210. (Pubitemid 30209912)
27. de Kloet E. R., (2008) About stress hormones and resilience to psychopathology. J. Neuroendocrinol. 20, 885-892. (Pubitemid 351858742)
28. van der Laan S., and, Meijer O. C., (2008) Pharmacology of glucocorticoids: beyond receptors. Eur. J. Pharmacol. 585, 483-491.
29. Laaris N., Haj-Dahmane S., Hamon M., and, Lanfumey L., (1995) Glucocorticoid receptor-mediated inhibition by corticosterone of 5-HT1A autoreceptor functioning in the rat dorsal raphe nucleus. Neuropharmacology 34, 1201-1210.
30. Lei S., and, McBain C. J., (2003) GABA B receptor modulation of excitatory and inhibitory synaptic transmission onto rat CA3 hippocampal interneurons. J. Physiol. 546, 439-453. (Pubitemid 36175979)
31. Liberzon I., Lopez J. F., Flagel S. B., Vazquez D. M., and, Young E. A., (1999) Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: relevance to post-traumatic stress disorder. J. Neuroendocrinol. 11, 11-17. (Pubitemid 29015395)
32. Liu L., Tsuji M., Takeda H., Takada K., and, Matsumiya T., (1999) Adrenocortical suppression blocks the enhancement of memory storage produced by exposure to psychological stress in rats. Brain Res. 821, 134-140. (Pubitemid 29219689)
33. Liu Z., Otsu Y., Vasuta C., Nawa H., and, Murphy T. H., (2007) Action-potential-independent GABAergic tone mediated by nicotinic stimulation of immature striatal miniature synaptic transmission. J. Neurophysiol. 98, 581-593. (Pubitemid 47236016)
34. Lupien S. J., Wilkinson C. W., Briere S., Menard C., Kin Ng Ying, and, N. M. and Nair N. P., (2002) The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology 27, 401-416. (Pubitemid 34121981)
35. Maggio N., and, Segal M., (2009) Differential corticosteroid modulation of inhibitory synaptic currents in the dorsal and ventral hippocampus. J. Neurosci. 29, 2857-2866.
36. Maggio N., and, Segal M., (2012) Steroid modulation of hippocampal plasticity: switching between cognitive and emotional memories. Front. Cell. Neurosci. 6, 12.
37. Martin S., Henley J. M., Holman D., Zhou M., Wiegert O., van Spronsen M., Joels M., Hoogenraad C. C., and, Krugers H. J., (2009) Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS ONE 4, e4714.
38. McCormick C. M., McNamara M., Mukhopadhyay S., and, Kelsey J. E., (1997) Acute corticosterone replacement reinstates performance on spatial and nonspatial memory tasks 3 months after adrenalectomy despite degeneration in the dentate gyrus. Behav. Neurosci. 111, 518-531. (Pubitemid 27251322)
39. McEwen B. S., (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873-904. (Pubitemid 47086281)
40. McIntyre W. R., and, Samuels H. H., (1985) Triamcinolone acetonide regulates glucocorticoid-receptor levels by decreasing the half-life of the activated nuclear-receptor form. J. Biol. Chem. 260, 418-427. (Pubitemid 15164067)
41. Meyer A. S., and, Schmidt T. J., (1995) Potential mechanisms underlying autoregulation of glucocorticoid receptor mRNA levels in the DHD/K12/PROb rat colonic adenocarcinoma cell line. J. Steroid Biochem. Mol. Biol. 55, 219-228.
42. Musazzi L., Milanese M., Farisello P., et al,. (2010) Acute stress increases depolarization-evoked glutamate release in the rat prefrontal/frontal cortex: the dampening action of antidepressants. PLoS ONE 5, e8566.
43. Nishi M., Noriko H. H., and, Kawata M., (2011) Intranuclear dynamics of corticosteroid receptors and effects of proteasomal activity in cultured hippocampal neural cells. Neurosci. Lett. 494, 65-69.
44. Noguchi T., Makino S., Matsumoto R., Nakayama S., Nishiyama M., Terada Y., and, Hashimoto K., (2010) Regulation of glucocorticoid receptor transcription and nuclear translocation during single and repeated immobilization stress. Endocrinology 151, 4344-4355.
45. O'Donnell D., Larocque S., Seckl J. R., and, Meaney M. J., (1994) Postnatal handling alters glucocorticoid, but not mineralocorticoid messenger RNA expression in the hippocampus of adult rats. Brain Res. Mol. Brain Res. 26, 242-248.
46. Paskitti M. E., McCreary B. J., and, Herman J. P., (2000) Stress regulation of adrenocorticosteroid receptor gene transcription and mRNA expression in rat hippocampus: time-course analysis. Brain Res. Mol. Brain Res. 80, 142-152.
47. Pearce D., and, Yamamoto K. R., (1993) Mineralocorticoid and glucocorticoid receptor activities distinguished by nonreceptor factors at a composite response element. Science 259, 1161-1165. (Pubitemid 23085354)
48. Pugh C. R., Tremblay D., Fleshner M., and, Rudy J. W., (1997) A selective role for corticosterone in contextual-fear conditioning. Behav. Neurosci. 111, 503-511. (Pubitemid 27251320)
49. Rao S. P., and, Sikdar S. K., (2004) Estradiol-induced changes in the activity of hippocampal neurons in network culture are suppressed by co-incubation with gabapentin. Brain Res. 1022, 126-136. (Pubitemid 39194993)
50. Reul J. M., van den Bosch F. R., and, de Kloet E. R., (1987a) Relative occupation of type-I and type-II corticosteroid receptors in rat brain following stress and dexamethasone treatment: functional implications. J. Endocrinol. 115, 459-467. (Pubitemid 18003084)
51. Reul J. M., van den Bosch F. R., and, de Kloet E. R., (1987b) Differential response of type I and type II corticosteroid receptors to changes in plasma steroid level and circadian rhythmicity. Neuroendocrinology 45, 407-412. (Pubitemid 17053164)
52. Roozendaal B., and, McGaugh J. L., (1996) The memory-modulatory effects of glucocorticoids depend on an intact stria terminalis. Brain Res. 709, 243-250. (Pubitemid 26071270)
53. Rosewicz S., McDonald A. R., Maddux B. A., Goldfine I. D., Miesfeld R. L., and, Logsdon C. D., (1988) Mechanism of glucocorticoid receptor down-regulation by glucocorticoids. J. Biol. Chem. 263, 2581-2584. (Pubitemid 18062893)
54. Rozeboom A. M., Akil H., and, Seasholtz A. F., (2007) Mineralocorticoid receptor overexpression in forebrain decreases anxiety-like behavior and alters the stress response in mice. Proc. Natl Acad. Sci. USA 104, 4688-4693. (Pubitemid 47186286)
55. Sandi C., Loscertales M., and, Guaza C., (1997) Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 9, 637-642. (Pubitemid 27190073)
56. Sapolsky R. M., Krey L. C., and, McEwen B. S., (1984) Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl Acad. Sci. USA 81, 6174-6177. (Pubitemid 15220802)
57. Sapolsky R. M., Meaney M. J., and, McEwen B. S., (1985) The development of the glucocorticoid receptor system in the rat limbic brain. III. Negative-feedback regulation. Brain Res. 350, 169-173. (Pubitemid 15108943)
58. Sara Y., Virmani T., Deak F., Liu X., and, Kavalali E. T., (2005) An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45, 563-573. (Pubitemid 40249868)
59. Schmidt T. J., Barnett C. A., and, Litwack G., (1982) Activation of the glucocorticoid-receptor complex. J. Cell. Biochem. 20, 15-27. (Pubitemid 13124664)
60. Smeets T., Giesbrecht T., Jelicic M., and, Merckelbach H., (2007) Context-dependent enhancement of declarative memory performance following acute psychosocial stress. Biol. Psychol. 76, 116-123. (Pubitemid 47268634)
61. Sporns O., and, Jenkinson S., (1997) Potassium ion- and nitric oxide-induced exocytosis from populations of hippocampal synapses during synaptic maturation in vitro. Neuroscience 80, 1057-1073. (Pubitemid 27359792)
62. van Steensel B., van Haarst A. D., de Kloet E. R., and, van Driel R., (1991) Binding of corticosteroid receptors to rat hippocampus nuclear matrix. FEBS Lett. 292, 229-231.
63. Sundberg M., Savola S., Hienola A., Korhonen L., and, Lindholm D., (2006) Glucocorticoid hormones decrease proliferation of embryonic neural stem cells through ubiquitin-mediated degradation of cyclin D1. J. Neurosci. 26, 5402-5410. (Pubitemid 44318392)
64. Uz T., Dwivedi Y., Qeli A., Peters-Golden M., Pandey G., and, Manev H., (2001) Glucocorticoid receptors are required for up-regulation of neuronal 5-lipoxygenase (5LOX) expression by dexamethasone. FASEB J. 15, 1792-1794.
65. Verkuyl J. M., and, Joels M., (2003) Effect of adrenalectomy on miniature inhibitory postsynaptic currents in the paraventricular nucleus of the hypothalamus. J. Neurophysiol. 89, 237-245. (Pubitemid 36134017)
66. Verkuyl J. M., Hemby S. E., and, Joels M., (2004) Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur. J. Neurosci. 20, 1665-1673. (Pubitemid 39274050)
67. Verkuyl J. M., Karst H., and, Joels M., (2005) GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress. Eur. J. Neurosci. 21, 113-121. (Pubitemid 40193880)
68. Virmani T., Ertunc M., Sara Y., Mozhayeva M., and, Kavalali E. T., (2005) Phorbol esters target the activity-dependent recycling pool and spare spontaneous vesicle recycling. J. Neurosci. 25, 10922-10929. (Pubitemid 41692622)
69. Xiao L., Qi A., and, Chen Y., (2005) Cultured embryonic hippocampal neurons deficient in glucocorticoid (GC) receptor: a novel model for studying nongenomic effects of GC in the neural system. Endocrinology 146, 4036-4041. (Pubitemid 41175775)
70. Yang Z., Guo C., Zhu P., Li W., Myatt L., and, Sun K., (2007) Role of glucocorticoid receptor and CCAAT/enhancer-binding protein alpha in the feed-forward induction of 11beta-hydroxysteroid dehydrogenase type 1 expression by cortisol in human amnion fibroblasts. J. Endocrinol. 195, 241-253. (Pubitemid 350143104)
71. Yang-Yen H. F., Chambard J. C., Sun Y. L., Smeal T., Schmidt T. J., Drouin J., and, Karin M., (1990) Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell 62, 1205-1215.
72. Yau J. L., Olsson T., Morris R. G., Meaney M. J., and, Seckl J. R., (1995) Glucocorticoids, hippocampal corticosteroid receptor gene expression and antidepressant treatment: relationship with spatial learning in young and aged rats. Neuroscience 66, 571-581.