The interplay between rapid and slow corticosteroid actions in brain

European Journal of Pharmacology

Volumn 719, Issue 1-3, 2013, Pages 44-52

  Joëls, Marian ^a   Pasricha, Natasha ^a   Karst, Henk ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Adrenalectomy; Amygdala; Chronic stress; Corticosterone; Genomic; Hippocampus; Non genomic

Indexed keywords

CORTICOSTEROID; GLUCOCORTICOID RECEPTOR; GLUTAMIC ACID; MINERALOCORTICOID RECEPTOR;

ADAPTATION; BEHAVIOR; BRAIN NERVE CELL; COGNITION; GENOMICS; HIPPOCAMPUS; HORMONE RELEASE; HUMAN; NEUROTRANSMITTER RELEASE; NONHUMAN; PERFORMANCE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; STRESS;

ADRENALECTOMY; AMYGDALA; CHRONIC STRESS; CORTICOSTERONE; GENOMIC; HIPPOCAMPUS; NON-GENOMIC;

ADRENAL CORTEX HORMONES; ANIMALS; BRAIN; COGNITION; HUMANS; NEURONS; TIME FACTORS;

EID: 84888302518     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.07.015     Document Type: Review

References (65)

1. A.M. Bao, G. Meynen, and D.F. Swaab The stress system in depression and neurodegeneration: focus on the human hypo (Pubitemid 351381758)
2. M.F. Bear, and W.C. Abraham Long-term depression in hippocampus Annu. Rev. Neurosci. 19 1996 437 462 (Pubitemid 26080835)
3. S.C. Biddie, and G.L. Hager Glucocorticoid receptor dynamics and gene regulation Stress 12 2009 193 205
4. R.M. Evans, and J.L. Arriza A molecular framework for the actions of glucocorticoid hormones in the nervous system Neuron 2 1989 1105 1112
5. N.A. Datson, M.C. Morsink, O.C. Meijer, and E.R. de Kloet Central corticosteroid actions: search for gene targets Eur. J. Pharmacol. 583 2008 272 289
6. E.R. De Kloet, M. Joels, and F. Holsboer Stress and the brain: from adaptation to disease Nat. Rev. Neurosci. 6 2005 463 475 (Pubitemid 40769171)
7. S. Di, R. Malcher-Lopes, V.L. Marcheselli, N.G. Bazan, and J.G. Tasker Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and gamma-aminobutyric acid inputs to hypothalamic magnocellular neurons Endocrinology 146 2005 4292 4301 (Pubitemid 41324025)
8. S. Duvarci, and D. Pare Glucocorticoids enhance the excitability of principal basolateral amygdala neurons J. Neurosci. 27 2007 4482 4491 (Pubitemid 46640721)
9. J.M. ffrench-Mullen Cortisol inhibition of calcium currents in guinea pig hippocampal CA1 neurons via G-protein-coupled activation of protein kinase C J. Neurosci. 15 1995 903 911
10. D. Filipini, K. Gijsbers, M.K. Birmingham, and B. Dubrovsky Effects of adrenal steroids and their reduced metabolites on hippocampal long-term potentiation J. Steroid Biochem. Mol. Biol. 40 1991 87 92
11. E. Gould, and H.A. Cameron Regulation of neuronal birth, migration and death in the rat dentate gyrus Dev. Neurosci. 18 1996 22 35 (Pubitemid 26257906)
12. E. Gould, C.S. Woolley, and B.S. McEwen Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus Neuroscience 37 1990 367 375 (Pubitemid 20268190)
13. L. Groc, D. Choquet, and F. Chaouloff The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation Nat. Neurosci. 11 2008 868 870
14. F.L. Groeneweg, H. Karst, E.R. de Kloet, and M. Joëls Rapid non-genomic effects of corticosteroids and their role in the central stress response J. Endocrinol. 209 2011 153 167
15. M. Gutièrrez-Mecinas, A.F. Trollope, A. Collins, H. Morfett, S.A. Hesketh, F. Kersanté, and J.M. Reul Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling Proc. Nat. Acad. Sci. USA 108 2011 13806 13811
16. A. Holmes, and C.L. Wellman Stress-induced prefrontal reorganization and executive dysfunction in rodents Neurosci. Biobehav. Rev. 33 2009 773 783
17. F. Holsboer The corticosteroid receptor hypothesis of depression Neuropsychopharmacology 23 2000 477 501
18. M. Joels, and T.Z. Baram The neuro-symphony of stress Nat. Rev. Neurosci. 10 2009 459 466
19. M. Joels, and E.R. de Kloet Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus Science 245 1989 1502 1505 (Pubitemid 19243242)
20. M. Joëls, and H. Karst Corticosteroid effects on calcium signaling in limbic neurons Cell Calcium 51 2012 277 283
21. M. Joëls, Z. Pu, O. Wiegert, M.S. Oitzl, and H.J. Krugers Learning under stress: how does it work? Trends Cogn. Sci. 10 2006 152 158
22. M. Joëls, R.A. Sarabdjitsingh, and H. Karst Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes Pharmacol. Rev. 64 2012 901 938
23. M. Joëls, C. Stienstra, and Y. Karten Effect of adrenalectomy on membrane properties and synaptic potentials in rat dentate granule cells J. Neurophysiol. 85 2001 699 707 (Pubitemid 32147771)
24. H. Karst, and M. Joels Calcium currents in rat dentate granule cells are altered after adrenalectomy Eur. J. Neurosci. 14 2001 503 512 (Pubitemid 34203458)
25. H. Karst, and M. Joels Effect of chronic stress on synaptic currents in rat hippocampal dentate gyrus neurons J. Neurophysiol. 89 2003 625 633 (Pubitemid 36134049)
26. H. Karst, and M. Joels Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells J. Neurophysiol. 94 2005 3479 3486 (Pubitemid 41504783)
27. H. Karst, S. Berger, G. Erdmann, G. Schutz, and M. Joels Metaplasticity of amygdalar responses to the stress hormone corticosterone Proc. Nat. Acad. Sci. USA 107 2010 14449 14454
28. H. Karst, S. Berger, M. Turiault, F. Tronche, G. Schutz, and M. Joels Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone Proc. Nat. Acad. Sci. USA 102 2005 19204 19207 (Pubitemid 43049590)
29. H. Karst, S. Nair, E. Velzing, L. Rumpff-van Essen, E. Slagter, P. Shinnick-Gallagher, and M. Joels Glucocorticoids alter calcium conductances and calcium channel subunit expression in basolateral amygdala neurons Eur. J. Neurosci. 16 2002 1083 1089 (Pubitemid 35463557)
30. A. Kavushansky, R.M. Vouimba, H. Cohen, and G. Richter-Levin Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress Hippocampus 16 2006 35 42
31. D.S. Kerr, L.W. Campbell, S.Y. Hao, and P.W. Landfield Corticosteroid modulation of hippocampal potentials: increased effect with aging Science 245 1989 1505 1509 (Pubitemid 19243243)
32. J.J. Kim, and D.M. Diamond The stressed hippocampus, synaptic plasticity and lost memories Nat. Rev. Neurosci. 3 2002 453 462 (Pubitemid 135711801)
33. J.J. Kim, H.J. Lee, A.C. Welday, E. Song, J. Cho, P.E. Sharp, M.W. Jung, and H.T. Blair Stress-induced alterations in hippocampal plasticity, place cells, and spatial memory Proc. Nat. Acad. Sci. USA 104 2007 18297 18302 (Pubitemid 350210861)
34. S.J. Kim, and D.J. Linden Ubiquitous plasticity and memory storage Neuron 56 2007 582 592 (Pubitemid 350102036)
35. 2+ currents and the excitability of pyramidal neurons in the hippocampal CA3 subfield in rats depend on corticosterone and time of day Neurosci. Lett. 307 2001 53 56 (Pubitemid 32539307)
36. M.H. Kole, L. Swan, and E. Fuchs The antidepressant tianeptine persistently modulates glutamate receptor currents of the hippocampal CA3 commissural associational synapse in chronically stressed rats Eur. J. Neurosci. 16 2002 807 816 (Pubitemid 35463572)
37. P.W. Landfield, and J.C. Eldridge Evolving aspects of the glucocorticoid hypothesis of brain aging: hormonal modulation of neuronal calcium homeostasis Neurobiol. Aging 15 1994 579 588 (Pubitemid 24241838)
38. L. Liebmann, H. Karst, K. Sidiropoulou, N. van Gemert, O.C. Meijer, P. Poirazi, and M. Joels Differential effects of corticosterone on the slow afterhyperpolarization in the basolateral amygdala and CA1 region: possible role of calcium channel subunits J. Neurophysiol. 99 2008 958 968 (Pubitemid 351253248)
39. S.L. Lightman, and B.L. Conway-Campbell The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration Nat. Rev. Neurosci. 11 2010 710 718
40. C. Liston, M.M. Miller, D.S. Goldwater, J.J. Radley, A.B. Rocher, P.R. Hof, J.H. Morrison, and B.S. McEwen Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting J. Neurosci. 26 2006 7870 7874 (Pubitemid 44315156)
41. S.J. Lupien, B.S. McEwen, M.R. Gunnar, and C. Heim Effects of stress throughout the lifespan on the brain, behaviour and cognition Nat. Rev. Neurosci. 10 2009 434 445
42. N. Maggio, and M. Segal Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus J. Neurosci. 27 2007 5757 5765 (Pubitemid 350021083)
43. N. Maggio, and M. Segal Differential corticosteroid modulation of inhibitory synaptic currents in the dorsal and ventral hippocampus J. Neurosci. 29 2009 2857 2866
44. S. Martin, J.M. Henley, D. Holman, M. Zhou, O. Wiegert, M. van Spronsen, M. Joels, C.C. Hoogenraad, and H.J. Krugers Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity PLoS One 4 2009 e4714
45. B.S. McEwen, and A.M. Magarinos Stress effects on morphology and function of the hippocampus Ann. N.Y. Acad. Sci. 821 1997 271 284 (Pubitemid 27343028)
46. M.L. Meewisse, J.B. Reitsma, G.J. de Vries, B.P. Gersons, and M. Olff Cortisol and post-traumatic stress disorder in adults: systematic review and meta-analysis Br. J. Psychiatry 191 2007 387 392 (Pubitemid 350069578)
47. J.E. Olijslagers, E.R. de Kloet, Y. Elgersma, G.M. van Woerden, M. Joels, and H. Karst Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors Eur. J. Neurosci. 27 2008 2542 2550 (Pubitemid 351781663)
48. N. Pasricha, M. Joels, and H. Karst Rapid effects of corticosterone in the mouse dentate gyrus via a nongenomic pathway J. Neuroendocrinol. 23 2011 143 147
49. J. Passecker, V. Hok, A. Della-Chiesa, E. Chah, and S.M. O'Mara Dissociation of dorsal hippocampal regional activation under the influence of stress in freely behaving rats. Front Behav. Neurosci. 5 2011 66
50. D.W. Pfaff, M.T. Silva, and J.M. Weiss Telemetered recording of hormone effects on hippocampal neurons Science 172 1971 394 395
51. J.M. Reul, and E.R. de Kloet Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation Endocrinology 117 1985 2505 2511 (Pubitemid 16194083)
52. B. Roozendaal, A. Hernandez, S.M. Cabrera, R. Hagewoud, M. Malvaez, D.P. Stefanko, J. Haettig, and M.A. Wood Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification J. Neurosci. 30 2010 5037 5046
53. B. Roozendaal, B.S. McEwen, and S. Chattarji Stress, memory and the amygdala Nat. Rev. Neurosci. 10 2009 423 433
54. R.A. Sarabdjitsingh, D. Kofink, H. Karst, E.R. de Kloet, and M. Joëls Stress-induced enhancement of mouse amygdalar synaptic plasticity depends on glucocorticoid and ß-adrenergic activity PLoS One 7 2012 e42143
55. L. Schwabe, and O.T. Wolf Stress-induced modulation of instrumental behavior: from goal-directed to habitual control of action Behav. Brain Res. 219 2011 321 328
56. L. Schwabe, M. Joëls, B. Roozendaal, O.T. Wolf, and M.S. Oitzl Stress effects on memory: an update and integration Neurosci. Biobehav. Rev. 36 2012 1740 1749
57. N.G. Van Gemert, D.M. Carvalho, H. Karst, S. van der Laan, M. Zhang, O.C. Meijer, J.W. Hell, and M. Joels Dissociation between rat hippocampal CA1 and dentate gyrus cells in their response to corticosterone: effects on calcium channel protein and current Endocrinology 150 2009 4615 4624
58. A. Vyas, R. Mitra, B.S. Shankaranarayana Rao, and S. Chattarji Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons J. Neurosci. 22 2002 6810 6818 (Pubitemid 35386438)
59. O. Wiegert, M. Joels, and H. Krugers Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus Learn. Mem. 13 2006 110 113
60. J. Wossink, H. Karst, O. Mayboroda, and M. Joëls Morphological and functional properties of rat dentate granule cells after adrenalectomy Neuroscience 108 2001 263 272 (Pubitemid 33152967)
61. C.S. Wyrwoll, M.C. Holmes, and J.R. Seckl 11β-hydroxysteroid dehydrogenases and the brain: from zero to hero, a decade of progress Front. Neuroendocrinol. 32 2011 265 286
62. R. Yehuda Advances in understanding neuroendocrine alterations in PTSD and their therapeutic implications Ann. N.Y. Acad. Sci. 1071 2006 137 166 (Pubitemid 44126726)
63. E.Y. Yuen, W. Liu, I.N. Karatsoreos, J. Feng, B.S. McEwen, and Z. Yan Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory Proc. Nat. Acad. Sci. USA 106 2009 14075 14079
64. E.Y. Yuen, W. Liu, I.N. Karatsoreos, Y. Ren, J. Feng, B.S. McEwen, and Z. Yan Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory Mol. Psychiatry 16 2011 156 170
65. E.Y. Yuen, J. Wei, W. Liu, P. Zhong, X. Li, and Z. Yan Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex Neuron 73 2012 962 977