Combined β-adrenergic and corticosteroid receptor activation regulates AMPA receptor function in hippocampal neurons

Journal of Psychopharmacology

Volumn 26, Issue 4, 2012, Pages 516-524

  Zhou, Ming ^a   Hoogenraad, Casper C ^b,c   Joëls, Marian ^a,d   Krugers, Harm J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

AMPA receptor; corticosterone; learning; mEPSCs; noradrenaline

Indexed keywords

AMPA RECEPTOR; AMPA RECEPTOR GLUA1 SUBUNIT; AMPA RECEPTOR GLUA2 SUBUNIT; BETA ADRENERGIC RECEPTOR; CORTICOSTEROID RECEPTOR; CORTICOSTERONE; ISOPRENALINE; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL SURFACE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; CORTICOSTERONE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; ISOPROTERENOL; MALE; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA; RECEPTORS, AMPA; RECEPTORS, STEROID;

EID: 84860137267     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881111424930     Document Type: Article

References (50)

1. Barria A, Derkach V, Soderling T. Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor. J Biol Chem. 1997a ; 272: 32727-32730
2. Barria A, Muller D, Derkach V, et al. Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science. 1997b ; 276: 2042-2045
3. Bartos JA, Ulrich JD, Li H, et al. Postsynaptic clustering and activation of Pyk2 by PSD-95. J Neurosci. 2010 ; 30: 449-463
4. Carroll RC, Nicoll RA, Malenka RC. Effects of PKA and PKC on miniature excitatory postsynaptic currents in CA1 pyramidal cells. J Neurophysiol. 1998 ; 80: 2797-2800
5. Caudal D, Godsil BP, Mailliet F, et al. Acute stress induces contrasting changes in AMPA receptor subunit phosphorylation within the prefrontal cortex, amygdala and hippocampus. PLoS One. 2010 ; 5: e15282
6. Chavez-Noriega LE, Stevens CF. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J Neurosci. 1994 ; 14: 310-317
7. Chen HX, Roper SN. PKA and PKC enhance excitatory synaptic transmission in human dentate gyrus. J Neurophysiol. 2003 ; 89: 2482-2488
8. de Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005 ; 6: 463-475
9. Diamond DM, Bennett MC, Fleshner M, et al. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus. 1992 ; 2: 421-430
10. Droste SK, de Groote L, Atkinson HC, et al. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology. 2008 ; 149: 3244-3253
11. Esteban JA, Shi SH, Wilson C, et al. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci. 2003 ; 6: 136-143
12. Groc L, Choquet D, Chaouloff F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci. 2008 ; 11: 868-870
13. Hoogenraad CC, Milstein AD, Ethell IM, et al. GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci. 2005 ; 8: 906-915
14. Hu H, Real E, Takamiya K, et al. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell. 2007 ; 131: 160-173
15. Joels M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol Sci. 2006 ; 27: 244-250
16. Joels M, Baram TZ. The neuro-symphony of stress. Nat Rev Neurosci. 2009 ; 10: 459-466
17. Joels M, de Kloet ER. Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems. Prog Neurobiol. 1994 ; 43: 1-36
18. Joels M, Velzing E, Nair S, et al. Acute stress increases calcium current amplitude in rat hippocampus: temporal changes in physiology and gene expression. Eur J Neurosci. 2003 ; 18: 1315-1324
19. Joiner ML, Lise MF, Yuen EY, et al. Assembly of a beta2-adrenergic receptor-GluR1 signalling complex for localized cAMP signalling. EMBO J. 2010 ; 29: 482-495
20. Kademian SM, Bignante AE, Lardone P, et al. Biphasic effects of adrenal steroids on learned helplessness behavior induced by inescapable shock. Neuropsychopharmacology. 2005 ; 30: 58-66
21. Karst H, Berger S, Turiault M, et al. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci U S A. 2005 ; 102: 19204-19207
22. Karst H, Joels M. Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J Neurophysiol. 2005 ; 94: 3479-3486
23. Kessels HW, Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron. 2009 ; 61: 340-350
24. Krugers HJ, Hoogenraad CC, Groc L. Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nat Rev Neurosci. 2010 ; 11: 675-681
25. Liebmann L, Karst H, Joels M. Effects of corticosterone and the beta-agonist isoproterenol on glutamate receptor-mediated synaptic currents in the rat basolateral amygdala. Eur J Neurosci. 2009 ; 30: 800-807
26. Malenka RC. Synaptic plasticity and AMPA receptor trafficking. Ann N Y Acad Sci. 2003 ; 1003: 1-11
27. Mammen AL, Kameyama K, Roche KW, et al. Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J Biol Chem. 1997 ; 272: 32528-32533
28. Man HY, Sekine-Aizawa Y, Huganir RL. Regulation of {alpha}-amino-3- hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proc Natl Acad Sci U S A. 2007 ; 104: 3579-3584
29. Martin S, Henley JM, Holman D, et al. Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS One. 2009 ; 4: e4714
30. McIntyre CK, Hatfield T, McGaugh JL. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. Eur J Neurosci. 2002a ; 16: 1223-1226
31. McIntyre CK, Pal SN, Marriott LK, et al. Competition between memory systems: acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. J Neurosci. 2002b ; 22: 1171-1176
32. Nowak L, Bregestovski P, Ascher P, et al. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 1984 ; 307: 462-465
33. Okuda S, Roozendaal B, McGaugh JL. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proc Natl Acad Sci U S A. 2004 ; 101: 853-858
34. Olijslagers JE, de Kloet ER, Elgersma Y, et al. Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci. 2008 ; 27: 2542-2550
35. Plant K, Pelkey KA, Bortolotto ZA, et al. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat Neurosci. 2006 ; 9: 602-604
36. Pu Z, Krugers HJ, Joels M. Corticosterone time-dependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learn Mem. 2007 ; 14: 359-367
37. Pu Z, Krugers HJ, Joels M. Beta-adrenergic facilitation of synaptic plasticity in the rat basolateral amygdala in vitro is gradually reversed by corticosterone. Learn Mem. 2009 ; 16: 155-160
38. Roche KW, O'Brien RJ, Mammen AL, et al. Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron. 1996 ; 16: 1179-1188
39. Roozendaal B. 1999 Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology. 2000 ; 25: 213-238
40. Roozendaal B, de Quervain DJ, Schelling G, et al. A systemically administered beta-adrenoceptor antagonist blocks corticosterone-induced impairment of contextual memory retrieval in rats. Neurobiol Learn Mem. 2004a ; 81: 150-154
41. Roozendaal B, Hahn EL, Nathan SV, et al. Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. J Neurosci. 2004b ; 24: 8161-8169
42. Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci. 2009 ; 10: 423-433
43. Rumpel S, LeDoux J, Zador A, et al. Postsynaptic receptor trafficking underlying a form of associative learning. Science. 2005 ; 308: 83-88
44. Sandi C, Loscertales M, Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur J Neurosci. 1997 ; 9: 637-642
45. Schmidt P, Holsboer F, Spengler D. Beta(2)-adrenergic receptors potentiate glucocorticoid receptor transactivation via G protein beta gamma-subunits and the phosphoinositide 3-kinase pathway. Mol Endocrinol. 2001 ; 15: 553-564
46. Stone EA, McEwen BS, Herrera AS, et al. Regulation of alpha and beta components of noradrenergic cyclic AMP response in cortical slices. Eur J Pharmacol. 1987 ; 141: 347-356
47. Valentino RJ, Van Bockstaele E. Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol. 2008 ; 583: 194-203
48. Whitlock JR, Heynen AJ, Shuler MG, et al. Learning induces long-term potentiation in the hippocampus. Science. 2006 ; 313: 1093-1097
49. Williams CL, McGaugh JL. Reversible lesions of the nucleus of the solitary tract attenuate the memory-modulating effects of posttraining epinephrine. Behav Neurosci. 1993 ; 107: 955-962
50. Zhou M, Conboy L, Sandi C, et al. Fear conditioning enhances spontaneous AMPA receptor-mediated synaptic transmission in mouse hippocampal CA1 area. Eur J Neurosci. 2009 ; 30: 1559-1564