Glucocorticoid receptors are localized to dendritic spines and influence local actin signaling

Molecular Neurobiology

Volumn 46, Issue 2, 2012, Pages 304-315

  Jafari, Matiar ^a   Seese, Ronald R ^a   Babayan, Alex H ^a   Gall, Christine M ^a   Lauterborn, Julie C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cofilin; Dexamethasone; Extracellular signal regulated kinase; Fragile X mental retardation Protein; Glucocorticoid receptor; Rho GTPase

Indexed keywords

ACTIN; COFILIN; DEXAMETHASONE; FRAGILE X MENTAL RETARDATION PROTEIN; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOID RECEPTOR ALPHA; MESSENGER RNA; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POSTSYNAPTIC DENSITY PROTEIN 95;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; HIPPOCAMPAL CA1 REGION; IMMUNOREACTIVITY; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

EID: 84868114752     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8288-3     Document Type: Article

References (76)

1. Romeo RD, Waters EM, McEwen BS (2004) Steroid-induced hippocampal synaptic plasticity: sex differences and similarities. Neuron Glia Biol 1:219-229
2. Tata DA, Anderson BJ (2010) The effects of chronic glucocorticoid exposure on dendritic length, synapse numbers and glial volume in animal models: implications for hippocampal volume reductions in depression. Physiol Behav 99:186-193
3. Chaouloff F, Groc L (2011) Temporal modulation of hippocampal excitatory transmission by corticosteroids and stress. Front Neuroendocrinol 32:25-42
4. Haller J, Mikics E, Makara GB (2008) The effects of non-genomic glucocorticoid mechanisms on bodily functions and the central neural system. A critical evaluation of findings. Front Neuroendocrinol 29:273-291 (Pubitemid 351467120)
5. Evanson NK, Herman J, P., Sakai RR, Krause EG (2010) Nongenomic actions of adrenal steroids in the central nervous system. J Neuroendocrinol. 846-861
6. Ffrench-Mullen JM (1995) Cortisol inhibition of calcium currents in guinea pig hippocampal CA1 neurons via G-protein-coupled activation of protein kinase C. J Neurosci 15:903-911
7. Karst H, Berger S, Turiault M, Tronche F, Schütz G, Joëls 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)
8. Qi AQ, Qiu J, Xiao L, Chen YZ (2005) Rapid activation of JNK and p38 by glucocorticoids in primary cultured hippocampal cells. J Neurosci Res 80:510-517 (Pubitemid 40780811)
9. Tasker JG, Di S, Malcher-Lopes R (2006) Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 147:5549-5556 (Pubitemid 44833470)
10. Johnson LR, Farb C, Morrison JH, McEwen BS, LeDoux JE (2005) Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 136:289-299 (Pubitemid 41487104)
11. Komatsuzaki Y, Murakami G, Tsurugizawa T, Mukai H, Tanabe N, Mitsuhashi K, Kawata M, Kimoto T, Ooishi Y, Kawato S (2005) Rapid spinogenesis of pyramidal neurons induced by activation of glucocorticoid receptors in adult male rat hippocampus. Biochem Biophys Res Commun 335:1002-1007 (Pubitemid 41215519)
12. Miyashiro KY, Beckel-Mitchener A, Purk TP, Becker KG, Barret T, Liu L, Carbonetto S, Weiler IJ, Greenough WT, Eberwine J (2003) RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron 37:417-431 (Pubitemid 36183364)
13. Krugers HJ, Hoogenraad CC, Groc L (2010) Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nat Rev Neurosci 11:675-681
14. Pavlides C, Watanabe Y, Magariños AM, McEwen BS (1995) Opposing roles of type I and type II adrenal steroid receptors in hippocampal long-term potentiation. Neuroscience 68:387-394
15. Alfarez DN, Wiegert O, Joëls M, Krugers HJ (2002) Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience 115:1119-1126 (Pubitemid 35351702)
16. Maggio N, Segal M (2007) Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. J Neurosci 27:5757-5765 (Pubitemid 350021083)
17. Wiegert O, Pu Z, Shor S, Joëls M, Krugers HJ (2005) Glucocorticoid receptor activation selectively hampers N-methyl-D-aspartate receptor dependent hippocampal synaptic plasticity in vitro. Neuroscience 135:403-411 (Pubitemid 41317379)
18. Lynch G, Rex CS, Chen LY, Gall CM (2008) The substrates of memory: defects, treatments, and enhancement. Eur J Pharmacol 585:2-13
19. Rex CS, Chen LY, Sharma A, Liu J, Babayan AH, Gall CM, Lynch G (2009) Different Rho GTPase-dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation. J Cell Biol 186:85-97
20. Krucker T, Siggins GR, Halpain S (2000) Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci USA 97:6856-6861 (Pubitemid 30412804)
21. Ransom RF, Lam NG, HallettMA, Atkinson SJ, SmoyerWE (2005) Glucocorticoids protect and enhance recovery of cultured murine podocytes via actin filament stabilization. Kidney Int 68:2473-2483 (Pubitemid 43250994)
22. Rubenstein NM, Callahan JA, Lo DH, Firestone GL (2007) Selective glucocorticoid control of Rho kinase isoforms regulate cellcell interactions. Biochem Biophys Res Commun 354:603-607 (Pubitemid 46161368)
23. Filla MS, Schwinn MK, Nosie AK, Clark RW, Peters DM (2011) Dexamethasone-associated cross-linked actin network formation in human trabecular meshwork cells involves β3 integrin signaling. Invest Ophthalmol Vis Sci 52:2952-2959
24. Bakker CE, Verheij C, Willemsen R, Vanderhelm R, Oerlemans F, Vermey M, Bygrave A, Hoogeveen AT, Oostra BA, Reyniers E, Deboulle K, Dhooge R, Cras P, Vanvelzen D, Nagels G, Martin JJ, Dedyn PP, Darby JK, Willems PJ, Consortium TD-BFX (1994) Fmr1 knockout mice: a model to study fragile x mental retardation. The Dutch-Belgium Fragile X Consortium. Cell 78:23-33 (Pubitemid 24228297)
25. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51
26. D'Agostino J, Vaeth GF, Henning SJ (1982) Diurnal rhythm of total and free concentrations of serum corticosterone in the rat. Acta Endocrinol (Copenh) 100:85-90 (Pubitemid 12150489)
27. Chen LY, Rex CS, Casale M, Gall CM, Lynch G (2007) Changes in synaptic morphology accompany actin signaling during LTP. J Neurosci 27:5363-5372 (Pubitemid 46790170)
28. Sarabdjitsingh RA, Meijer OC, de Kloet ER (2010) Specificity of glucocorticoid receptor primary antibodies for analysis of receptor localization patterns in cultured cells in hippocampus. Brain Res 1331:1-11
29. Bickel PE, Scherer PE, Schnitzer JE, Oh P, Lisanti MP, Lodish HF (1997) Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J Biol Chem 272:13793-13802 (Pubitemid 27225457)
30. Chen LY, Rex CS, Babayan AH, Kramár EA, Lynch G, Gall CM, Lauterborn JC (2010) Physiological activation of synaptic Rac> PAK (p-21 activated kinase) signaling is defective in a mouse model of fragile X syndrome. J Neurosci 30:10977-10984
31. Chen L, Rex C, Sanaiha Y, Lynch G, Gall C (2010) Learning induces neurotrophin signaling at hippocampal synapses. Proc Natl Acad Sci USA 107:7030-7035
32. Chen LY, Rex CS, Pham DT, Lynch G, Gall CM (2010) BDNF signaling during learning is regionally differentiated within hippocampus. J Neurosci 30:15097-15101
33. Rex CS, Gavin CF, RubioMD, Kramar EA, Chen LY, Jia Y, Huganir RL, Muzyczka N, Gall CM, Miller CA, Lynch G, Rumbaugh G (2010) Myosin IIb regulates actin dynamics during synaptic plasticity and memory formation. Neuron 67:603-617
34. Lauterborn JC, Pineda EA, Chen LY, Ramirez EA, Lynch G, Gall CM (2009) Ampakines cause sustained increases in brain-derived neurotrophic factor signaling at excitatory synapses without changes in AMPA receptor subunit expression. Neuroscience 159:283-295
35. Morales-Medina JC, Sanchez F, Flores G, Dumont Y, Quirion R (2009) Morphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J Chem Neuroanat 38:266-272
36. Liston C, Gan WB (2011) Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci USA 108:16074-16079
37. Diamond DM, Bennett MC, Fleshner M, Rose GM (1992) Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2:421-430
38. Joëls M, Krugers HJ (2007) LTP after stress: up or down? Neural Plast 2007:93202-93208
39. Bernard-Trifilo JA, Kramár EA, Torp R, Lin CY, Pineda EA, Lynch G, Gall CM (2005) Integrin signaling cascades are operational in adult hippocampal synapses and modulate NMDA receptor physiology. J Neurochem 93:834-849 (Pubitemid 40695743)
40. Megías M, Emri Z, Freund TF, Gulyás AI (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527-540 (Pubitemid 32171874)
41. Aoki C, Miko I, Oviedo H, Mikeladze-Dvali T, Alexandre L, Sweeney N, Bredt DS (2001) Electron microscopic immunocytochemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic, and nonsynaptic sites of adult and neonatal rat visual cortex. Synapse 40:239-257 (Pubitemid 32391251)
42. Hunt C, Schenker L, Kennedy M (1996) PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J Neurosci 16:1380-1388 (Pubitemid 26145918)
43. Sans N, Petralia R, Wang Y, Jn B, Hell J, Wenthold R (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 20:1260-1271 (Pubitemid 30220482)
44. Ronesi JA, Huber KM (2008) Metabotropic glutamate receptors and fragile x mental retardation protein: partners in translational regulation at the synapse. Sci Signal 1:pe6
45. Dictenberg JB, Swanger SA, Antar LN, Singer RH, Bassell GJ (2008) A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev Cell 14:926-939 (Pubitemid 351757204)
46. Kao DI, Aldridge GM, Weiler IJ, Greenough WT (2010) Altered mRNA transport, docking, and protein translation in neurons lacking fragile X mental retardation protein. Proc Natl Acad Sci USA 107:15601-15606
47. Todd PK, Mack KJ, Malter JS (2003) The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95. Proc Natl Acad Sci USA 100:14374-14378 (Pubitemid 37499244)
48. Kramár EA, Lin B, Rex CS, Gall CM, Lynch G (2006) Integrindriven actin polymerization consolidates long-term potentiation. Proc Natl Acad Sci USA 103:5579-5584
49. Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453-462 (Pubitemid 135711801)
50. Bamburg JR, McGough A, Ono S (1999) Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 9:364-370 (Pubitemid 29447718)
51. Martinez-Quiles N, Ho HY, Kirschner MW, Ramesh N, Geha RS (2004) Erk/Src phosphorylation of cortactin acts as a switch onswitch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 24:5269-5280 (Pubitemid 38738162)
52. Mullins RD, Heuser JA, Pollard TD (1998) The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci USA 95:6181-6186 (Pubitemid 28248985)
53. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, Cooper JA (2001) Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11:370-374 (Pubitemid 32200742)
54. Wang YF, Hatton GI (2007) Interaction of extracellular signalregulated protein kinase 1/2 with actin cytoskeleton in supraoptic oxytocin neurons and astrocytes: role in burst firing. J Neurosci 27:13822-13834 (Pubitemid 350278257)
55. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84:87-136 (Pubitemid 38049877)
56. Alonso M, Medina JH, Pozzo-Miller L (2004) ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn Mem 11:172-178 (Pubitemid 38456599)
57. Olijslagers JE, de Kloet ER, Elgersma Y, van Woerden GM, Joëls M, Karst H (2008) Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci 27:2542-2550 (Pubitemid 351781663)
58. Hill MN, McEwen BS (2009) Endocannabinoids: The silent partner of glucocorticoids in the synapse. Proc Natl Acad Sci USA 106:4579-4580
59. Barsegyan A,Mackenzie SM, Kurose BD, McGaugh JL, Roozendaal B (2010) Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proc Natl Acad Sci USA 107:16655-16660
60. Schmidt KL, Malisch JL, Breuner CW, Soma KK (2010) Corticosterone and cortisol binding sites in plasma, immune organs and brain of developing zebra finches: intracellular and membrane-associated receptors. Brain Behav Immun 24:908-918
61. Weiler IJ, Greenough WT (1993) Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc Natl Acad Sci USA 90:7168-7171 (Pubitemid 23222410)
62. Woolley CA, Gould E, McEwen BS (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225-231 (Pubitemid 20348626)
63. Magarinos AM, McEwen BS (1995) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 69:83-88
64. Sousa N, Paula-Barbosa MM, Almeida OF (1999) Ligand and subfield specificity of corticoid-induced neuronal loss in the rat hippocampal formation. Neuroscience 89:1079-1087 (Pubitemid 29074627)
65. Yang CH, Huang CC, Hsu KS (2004) Behavioral stress modifies hippocampal synaptic plasticity through corticosterone-induced sustained extracellular signal-regulated kinase/mitogen-activated protein kinase activation. J Neurosci 24:11029-11034
66. Lee SY, Kang JS, Song GY, Myung CS (2006) Stress induces the expression of heterotrimeric G protein beta subunits and the phosphorylation of PKB/Akt and ERK1/2 in rat brain. Neurosci Res 56:180-192 (Pubitemid 44374791)
67. Munhoz CD, Sorrells SF, Caso JR, Scavone C, Sapolsky RM (2010) Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dosedependent manner. J Neurosci 30:13690-13698
68. Kramár EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, Lynch G (2009) Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci 29:12982-12993
69. Kramár E, Chen L, Lauterborn J, Simmons D, Gall C, Lynch G (2010) BDNF and BDNF upregulation restores synaptic plasticity in middle-aged ovariectomized rats in Society for Neuroscience. 2010 Neuroscience Meeting Planner, San Diego
70. Rüegg J, Holsboer F, Turck C, Rein T (2004) Cofilin 1 is revealed as an inhibitor of glucocorticoid receptor by analysis of hormoneresistant cells. Mol Cell Biol 24:9371-9382 (Pubitemid 39391675)
71. Webb BA, Zhou S, Eves R, Shen L, Jia L, Mak AS (2006) Phosphorylation of cortactin by p21-activated kinase. Arch Biochem Biophys 456:183-193 (Pubitemid 44880282)
72. Inoue Y, Tsuda S, Nakagawa K, Hojo M, Adachi T (2011) Modeling myosin-dependent rearrangement and force generation in an actomyosin network. J Theor Biol 281:65-73
73. Oitzl MS, de Kloet ER (1992) Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 106:62-71
74. Shors TJ, Weiss C, Thompson RF (1992) Stress-induced facilitation of classical conditioning. Science 257:537-539
75. Sandi C, Rose SP (1994) Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res 647:106-112 (Pubitemid 24154507)
76. Sandi C, Loscertales M, 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)