Glucocorticoid receptor activation impairs hippocampal plasticity by suppressing BDNF expression in obese mice

Psychoneuroendocrinology

Volumn 42, Issue , 2014, Pages 165-177

  Wosiski Kuhn, Marlena ^a   Erion, Joanna R ^a   Gomez Sanchez, Elise P ^b   Gomez Sanchez, Celso E ^b   Stranahan, Alexis M ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Corticosterone; Dendritic spine; Dentate gyrus; Hippocampus; Long term potentiation; Synapse; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CORTICOSTERONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; LEPTIN RECEPTOR; METYRAPONE; NEUROTROPHIN RECEPTOR P75; TRANSCRIPTION FACTOR AP 1;

ADRENAL CORTEX HYPERFUNCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ATROPHY; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; DIABETES MELLITUS; HIPPOCAMPUS; HORMONE INHIBITION; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MENTAL STRESS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RECEPTOR BINDING; SPATIAL MEMORY; STEROIDOGENESIS; SYNAPTIC INHIBITION;

CORTICOSTERONE; DENDRITIC SPINE; DENTATE GYRUS; HIPPOCAMPUS; LONG-TERM POTENTIATION; SYNAPSE; SYNAPTIC PLASTICITY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; ENZYME INHIBITORS; HIPPOCAMPUS; METYRAPONE; MICE; MICE, OBESE; NEURONAL PLASTICITY; RECEPTORS, GLUCOCORTICOID; STEROID 11-BETA-HYDROXYLASE;

EID: 84895881381     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.01.020     Document Type: Article

References (32)

1. Bouret S.G., Draper S.J., Simerly R.B. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 2004, 304:108-110.
2. Bourne J.N., Harris K.M. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 2011, 21:354-373.
3. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 2008, 31:47-67.
4. Bruehl H., Rueger M., Dziobek I., Sweat V., Tirsi A., Javier E., Arentoft A., Wolf O.T., Convit A. Hypothalamic-pituitary-adrenal axis dysregulation and memory impairments in type 2 diabetes. J. Clin. Endocrinol. Metab. 2007, 92:2439-2445.
5. Campbell J.E., Király M.A., Atkinson D.J., D'souza A.M., Vranic M., Riddell M.C. Regular exercise prevents the development of hyperglucocorticoidemia via adaptations in the brain and adrenal glands in male Zucker diabetic fatty rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R168-R176.
6. Conrad C.D., Galea L.A., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 1996, 110:1321-1334.
7. Fiala J.C., Harris K.M. Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J. Microsc. 2001, 202:468-472.
8. Golden S.H., Lazo M., Carnethon M., Bertoni A.G., Schreiner P.J., Diez Roux A.V., Lee H.B., Lyketsos C. Examining a bidirectional association between depressive symptoms and diabetes. JAMA 2008, 299:2751-2759.
9. Grønli J., Bramham C., Murison R., Kanhema T., Fiske E., Bjorvatn B., Ursin R., Portas C.M. Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper. Pharmacol. Biochem. Behav. 2006, 85:842-849.
10. Holtmaat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G.W., Svoboda K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
11. Jeanneteau F., Garabedian M.J., Chao M.V. Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect. PNAS 2008, 105:4862-4867.
12. Jöhren O., Dendorfer A., Dominiak P., Raasch W. Gene expression of mineralocorticoid and glucocorticoid receptors in the limbic system is related to type-2 like diabetes in leptin-resistant rats. Brain Res. 2007, 1184:160-167.
13. Karst H., Berger S., Turiault M., Tronche F., Schütz G., Joëls M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. PNAS 2005, 102:19204-19207.
14. Kim J.J., Yoon K.S. Stress: metaplastic effects in the hippocampus. Trends Neurosci. 1998, 21:505-509.
15. Li X.L., Aou S., Oomura Y., Hori N., Fukunaga K., Hori T. Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents. Neuroscience 2002, 113:607-615.
16. Messaoudi E., Bârdsen K., Srebro B., Bramham C.R. Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J. Neurophysiol. 1998, 79:496-499.
17. Numakawa T., Kumamaru E., Adachi N., Yagasaki Y., Izumi A., Kunugi H. Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-gamma signaling for glutamate release via a glutamate transporter. PNAS 2009, 106:647-652.
18. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego, CA. second ed.
19. Pruunsild P., Sepp M., Orav E., Koppel I., Timmusk T. Identification of cis-elements and transcription factors regulating neuronal activity-dependent transcription of human BDNF gene. J. Neurosci. 2011, 31:3295-3308.
20. Rapp P.R., Stack E.C., Gallagher M. Morphometric studies of the aged hippocampus: I. Volumetric analysis in behaviorally characterized rats. J. Comp. Neurol. 1999, 403:459-470.
21. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. PNAS 2006, 103:6741-6746.
22. Sampath-Kumar R., Yu M., Khalil M.W., Yang K. Metyrapone is a competitive inhibitor of 11beta-hydroxysteroid dehydrogenase type 1 reductase. J. Steroid Biochem. Mol. Biol. 1997, 62:195-199.
23. Sandeep T.C., Yau J.L., MacLullich A.M., Noble J., Deary I.J., Walker B.R., Seckl J.R. 11Beta-hydroxysteroid dehydrogenase inhibition improves cognitive function in healthy elderly men and type 2 diabetics. PNAS 2004, 101:6734-6739.
24. Stranahan A.M., Arumugam T.V., Lee K., Cutler R.G., Egan J.P., Mattson M.P. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat. Neurosci. 2008, 11:309-317.
25. Stranahan A.M., Arumugam T.V., Lee K., Mattson M.P. Mineralocorticoid receptor activation restores medial perforant path LTP in diabetic rats. Synapse 2010, 64:528-532.
26. Stranahan A.M., Arumugam T.V., Mattson M.P. Lowering corticosterone levels reinstates hippocampal BDNF and TrkB expression without influencing deficits in hypothalamic BDNF expression in leptin receptor deficient mice. Neuroendocrinology 2011, 93:58-64.
27. Stranahan A.M., Jiam N.T., Spiegel A.M., Gallagher M. Aging reduces total neuron number in the dorsal component of the rodent prefrontal cortex. J. Comp. Neurol. 2012, 520:1318-1326.
28. Stranahan A.M., Lee K., Martin B., Maudsley S., Golden E., Cutler R.G., Mattson M.P. Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 2009, 19:951-961.
29. Wosiski-Kuhn M., Stranahan A.M. Transient increases in dendritic spine density contribute to dentate gyrus long-term potentiation. Synapse 2012, 66:661-664.
30. Xu W., Caracciolo B., Wang H.X., Winblad B., Bäckman L., Qiu C., Fratiglioni L. Accelerated progression from mild cognitive impairment to dementia in people with diabetes. Diabetes 2010, 59:2928-2935.
31. Yau J.L., Seckl J.R. Local amplification of glucocorticoids in the aging brain and impaired spatial memory. Front. Aging Neurosci. 2012, 4:24.
32. Zagrebelsky M., Holz A., Dechant G., Barde Y.A., Bonhoeffer T., Korte M. The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons. J. Neurosci. 2005, 25:9989-9999.