» Articles » PMID: 20051515

The Stress Hormone Corticosterone Increases Synaptic Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid (AMPA) Receptors Via Serum- and Glucocorticoid-inducible Kinase (SGK) Regulation of the GDI-Rab4 Complex

Overview
Journal J Biol Chem
Specialty Biochemistry
Date 2010 Jan 7
PMID 20051515
Citations 39
Authors
Affiliations
Soon will be listed here.
Abstract

Corticosterone, the major stress hormone, plays an important role in regulating neuronal functions of the limbic system, although the cellular targets and molecular mechanisms of corticosteroid signaling are largely unknown. Here we show that a short treatment of corticosterone significantly increases alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR)-mediated synaptic transmission and AMPAR membrane trafficking in pyramidal neurons of prefrontal cortex, a key region involved in cognition and emotion. This enhancing effect of corticosterone is through a mechanism dependent on Rab4, the small GTPase-controlling receptor recycling between early endosome and plasma membrane. Guanosine nucleotide dissociation inhibitor (GDI), which regulates the cycle of Rab proteins between membrane and cytosol, forms an increased complex with Rab4 after corticosterone treatment. Corticosterone also triggers an increased GDI phosphorylation at Ser-213 by the serum- and glucocorticoid-inducible kinase (SGK). Moreover, AMPAR synaptic currents and surface expression and their regulation by corticosterone are altered by mutating Ser-213 on GDI. These results suggest that corticosterone, via SGK phosphorylation of GDI at Ser-213, increases the formation of GDI-Rab4 complex, facilitating the functional cycle of Rab4 and Rab4-mediated recycling of AMPARs to the synaptic membrane. It provides a potential mechanism underlying the role of corticosteroid stress hormone in up-regulating excitatory synaptic efficacy in cortical neurons.

Citing Articles

A Scoping Review of Corticosterone-Induced Changes in Ionotropic Glutamate Receptor Levels and Localization in the Rodent Brain: Implications for the Auditory System.

Edlund E, Domarecka E, Olze H, Szczepek A Brain Sci. 2025; 15(2).

PMID: 40002443 PMC: 11852854. DOI: 10.3390/brainsci15020110.


TrkB-mediated neuroprotection in female hippocampal neurons is autonomous, estrogen receptor alpha-dependent, and eliminated by testosterone: a proposed model for sex differences in neonatal hippocampal neuronal injury.

Chanana V, Zafer D, Kintner D, Chandrashekhar J, Eickhoff J, Ferrazzano P Biol Sex Differ. 2024; 15(1):30.

PMID: 38566248 PMC: 10988865. DOI: 10.1186/s13293-024-00596-1.


Multiplexed Membrane Signaling by Glucocorticoids.

Harrison L, Tasker J Curr Opin Endocr Metab Res. 2023; 26.

PMID: 38075196 PMC: 10703063. DOI: 10.1016/j.coemr.2022.100390.


The Neuroendocrine Impact of Acute Stress on Synaptic Plasticity.

Dos-Santos R, Sweeten B, Stelly C, Tasker J Endocrinology. 2023; 164(11).

PMID: 37788632 PMC: 11046011. DOI: 10.1210/endocr/bqad149.


A proton-inhibited DEG/ENaC ion channel maintains neuronal ionstasis and promotes neuronal survival under stress.

Petratou D, Gjikolaj M, Kaulich E, Schafer W, Tavernarakis N iScience. 2023; 26(7):107117.

PMID: 37416472 PMC: 10320524. DOI: 10.1016/j.isci.2023.107117.


References
1.
Groc L, Choquet D, Chaouloff F . The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci. 2008; 11(8):868-70. DOI: 10.1038/nn.2150. View

2.
Lang F, Cohen P . Regulation and physiological roles of serum- and glucocorticoid-induced protein kinase isoforms. Sci STKE. 2001; 2001(108):re17. DOI: 10.1126/stke.2001.108.re17. View

3.
Kobayashi T, Cohen P . Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem J. 1999; 339 ( Pt 2):319-28. PMC: 1220160. View

4.
van der Sluijs P, Hull M, Webster P, MALE P, Goud B, Mellman I . The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell. 1992; 70(5):729-40. DOI: 10.1016/0092-8674(92)90307-x. View

5.
Martin S, Henley J, Holman D, Zhou M, Wiegert O, van Spronsen M . Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS One. 2009; 4(3):e4714. PMC: 2659165. DOI: 10.1371/journal.pone.0004714. View