Role of glia in stress-induced enhancement and impairment of memory

Frontiers in Integrative Neuroscience

Volumn 9, Issue JAN2016, 2016, Pages

  Pearson Leary, Jiah ^a   Osborne, Danielle Maria ^b   McNay, Ewan C ^c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b LEGACY RESEARCH   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Glia; Glucocorticoids; Hippocampus; Memory; Norepinephrine; Stress

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; INTERLEUKIN 1BETA; NORADRENALIN; STRESS HORMONE;

ASTROCYTE; CELL FUNCTION; COGNITION; GLIA; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; METABOLIC REGULATION; MICROGLIA; NONHUMAN; NORADRENERGIC SYSTEM; OLIGODENDROGLIA; PROTEIN FUNCTION; REVIEW; STRESS;

EID: 84957971698     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2015.00063     Document Type: Review

References (208)

1. Aboulkassim, T., Tong, X. K., Tse, Y. C., Wong, T. P., Woo, S. B., Neet, K. E., et al. (2011). Ligand-dependent TrkA activity in brain differentially affects spatial learning and long-term memory. Mol. Pharmacol. 80, 498-508. doi: 10.1124/mol.111.071332
2. Anacker, C. (2014). Adult hippocampal neurogenesis in depression: behavioral implications and regulation by the stress system. Curr. Top. Behav. Neurosci. 18, 25-43. doi: 10.1007/7854_2014_275
3. Anacker, C., Cattaneo, A., Musaelyan, K., Zunszain, P. A., Horowitz, M., Molteni, R., et al. (2013). Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 110, 8708-8713. doi: 10.1073/pnas.1300886110
4. Arisi, G. M. (2014). Nervous and immune systems signals and connections: cytokines in hippocampus physiology and pathology. Epilepsy Behav. 38,43-47. doi: 10.1016/j.yebeh.2014.01.017
5. Ballestas, M. E., and Benveniste, E. N. (1997). Elevation of cyclic AMP levels in astrocytes antagonizes cytokine-induced adhesion molecule expression. J. Neurochem. 69, 1438-1448. doi: 10.1046/j.1471-4159.1997.69041438.x
6. Barbaccia, M. L., Serra, M., Purdy, R. H., and Biggio, G. (2001). Stress and neuroactive steroids. Int. Rev. Neurobiol. 46, 243-272. doi: 10.1016/S0074-7742(01)46065-X
7. Ben Menachem-Zidon, O., Avital, A., Ben-Menahem, Y., Goshen, I., Kreisel, T., Shmueli, E. M., et al. (2011). Astrocytes support hippocampal-dependent memory and long-term potentiation via interleukin-1 signaling. Brain Behav. Immun. 25, 1008-1016. doi: 10.1016/j.bbi.2010.11.007
8. Bibi, F., Yasir, M., Sohrab, S. S., Azhar, E. I., Al-Qahtani, M. H., Abuzenadah, A. M., et al. (2014). Link between chronic bacterial inflammation and Alzheimer disease. CNS Neurol. Disord. Drug Targets 13, 1140-1147. doi: 10.2174/1871527313666140917115741
9. Binder, E. B. (2009). The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology 34(Suppl. 1), S186-195. doi: 10.1016/j.psyneuen.2009.05.021
10. Bitzer-Quintero, O. K., and González-Burgos, I. (2012). Immune system in the brain: a modulatory role on dendritic spine morphophysiology? Neural Plast. 2012:348642. doi: 10.1155/2012/348642
11. Boitard, C., Cavaroc, A., Sauvant, J., Aubert, A., Castanon, N., Layé, S., et al. (2014). Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain Behav. Immun. 40, 9-17. doi: 10.1016/j.bbi.2014.03.005
12. Borrell, J., de Kloet, E. R., and Bohus, B. (1984). Corticosterone decreases the efficacy of adrenaline to affect passive avoidance retention of adrenalectomized rats. Life Sci. 34, 99-104. doi: 10.1016/0024-3205(84)90336-9
13. Bruehl, H., Wolf, O. T., Sweat, V., Tirsi, A., Richardson, S., and Convit, A.. Modifiers of cognitive function and brain structure in middle-aged and elderly individuals with type 2 diabetes mellitus. Brain Res. 1280, 186-194. doi: 10.1016/j.brainres.2009.05.032
14. Buckman, L. B., Hasty, A. H., Flaherty, D. K., Buckman, C. T., Thompson, M. M., Matlock, B. K., et al. (2014). Obesity induced by a high-fat diet is associated with increased immune cell entryinto the central nervous system. Brain Behav. Immun. 35, 33-42. doi: 10.1016/j.bbi.2013.06.007
15. Cahill, L., and Alkire, M. T. (2003). Epinephrine enhancement ofhuman memory consolidation: interaction with arousal at encoding. Neurobiol. Learn. Mem. 79, 194-198. doi: 10.1016/S1074-7427(02)00036-9
16. Cahill, L., Gorski, L., and Le, K. (2003). Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learn. Mem. 10,270-274. doi: 10.1101/lm.62403
17. Capsoni, S., and Cattaneo, A. (2006). On the molecular basis linking Nerve Growth Factor (NGF) to Alzheimer's disease. Cell. Mol. Neurobiol. 26, 619-633. doi: 10.1007/s10571-006-9112-2
18. Carrillo-de Sauvage, M. Á., Maatouk, L., Arnoux, I., Pasco, M., Sanz Diez, A., Delahaye, M., et al. (2013). Potent and multiple regulatory actions of microglial glucocorticoid receptors during CNS inflammation. Cell Death Differ. 20, 1546-1557. doi: 10.1038/cdd.2013.108
19. Carter, B. S., Hamilton, D. E., and Thompson, R. C. (2013). Acute and chronic glucocorticoid treatments regulate astrocyte-enriched mRNAs in multiple brain regions in vivo. Front. Neurosci. 7:139. doi: 10.3389/fnins.2013.00139
20. Carter, B. S., Meng, F., and Thompson, R. C. (2012). Glucocorticoid treatment of astrocytes results in temporally dynamic transcriptome regulation and astrocyte-enriched mRNA changes in vitro. Physiol. Genomics 44, 1188-1200. doi: 10.1152/physiolgenomics.00097.2012
21. Chameau, P., Qin, Y., Spijker, S., Smit, A. B., and Joels, M. (2007). Glucocorticoids specifically enhance L-type calcium current amplitude and affect calcium channel subunit expression in the mouse hippocampus. J. Neurophysiol. 97, 5-14. doi: 10.1152/jn.00821.2006
22. Chang, C. N., Yang, J. T., Lee, T. H., Cheng, W. C., Hsu, Y. H., and Wu, J. H. (2005). Dexamethasone enhances upregulation of nerve growth factor mRNA expression in ischemic rat brain. J. Clin. Neurosci. 12, 680-684. doi: 10.1016/j.jocn.2005.05.004
23. Chao, M. V. (2003). Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4,299-309. doi: 10.1038/nrn1078
24. Chetty, S., Friedman, A. R., Taravosh-Lahn, K., Kirby, E. D., Mirescu, C., Guo, F, et al. (2014). Stress and glucocorticoids promote oligodendrogenesis in the adult hippocampus. Mol. Psychiatry 19, 1275-1283. doi: 10.1038/mp.2013.190
25. Cullinan, W. E. (2000). GABA(A) receptor subunit expression within hypophysiotropic CRH neurons: a dual hybridization histochemical study. J. Comp. Neurol. 419, 344-351. doi: 10.1002/(SICI)1096-9861(20000410)419:3 <344::AID-CNE6>3.0.C0;2-Z
26. Daulatzai, M. A. (2014). Chronic functional bowel syndrome enhances gut-brain axis dysfunction, neuroinflammation, cognitive impairment, and vulnerability to dementia. Neurochem. Res. 39, 624-644. doi: 10.1007/s11064-014-1266-6
27. de Guia, R. M., Rose, A. J., and Herzig, S. (2014). Glucocorticoid hormones and energy homeostasis. Horm. Mol. Biol. Clin. Investig. 19, 117-128. doi: 10.1515/hmbci-2014-0021
28. de Hoz, L., and Simons, M. (2015). The emerging functions of oligodendrocytes in regulating neuronal network behaviour. Bioessays 37, 60-69. doi: 10.1002/bies.201400127
29. de Kloet, E. R., Joels, M., and Holsboer, F. (2005). Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475. doi: 10.1038/nrn1683
30. Decavel, C., and Van den Pol, A. N. (1990). GABA: a dominant neurotransmitter in the hypothalamus. J. Comp. Neurol. 302, 1019-1037. doi: 10.1002/cne.903020423
31. Deecher, D. C., Wilcox, B. D., Dave, V., Rossman, P. A., and Kimelberg, H. K. (1993). Detection of 5-hydroxytryptamine2 receptors by radioligand binding, northern blot analysis, and Ca2+ responses in rat primary astrocyte cultures. J. Neurosci. Res. 35, 246-256. doi: 10.1002/jnr.490350304
32. Dey, A., Hao, S., Erion, J. R., Wosiski-Kuhn, M., and Stranahan, A. M. (2014). Glucocorticoid sensitization of microglia in a genetic mouse model of obesity and diabetes. J. Neuroimmunol. 269, 20-27. doi: 10.1016/j.jneuroim.2014.01.013
33. Dinan, T. G., and Cryan, J. F. (2012). Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 37, 1369-1378. doi: 10.1016/j.psyneuen.2012.03.007
34. Drew, P. D., and Chavis, J. A. (2000). Inhibition of microglial cell activation by cortisol. Brain Res. Bull. 52, 391-396. doi: 10.1016/S0361-9230(00)00275-6
35. Dumas, T. C., Gillette, T., Ferguson, D., Hamilton, K., and Sapolsky, R. M. (2010). Anti-glucocorticoid gene therapy reverses the impairing effects of elevated corticosterone on spatial memory, hippocampal neuronal excitability, and synaptic plasticity. J. Neurosci. 30, 1712-1720. doi: 10.1523/JNEUR0SCI.4402-09.2010
36. Erion, J. R., Wosiski-Kuhn, M., Dey, A., Hao, S., Davis, C. L., Pollock, N. K., et al. (2014). Obesity elicits interleukin 1-mediated deficits in hippocampal synaptic plasticity. J. Neurosci. 34, 2618-2631. doi: 10.1523/JNEUROSCI.4200-13.2014
37. Espinosa-Oliva, A. M., de Pablos, R. M., Villarán, R. F., Arguelles, S., Venero, J. L., Machado, A., et al. (2011). Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol. Aging 32, 85-102. doi: 10.1016/j.neurobiolaging.2009.01.012
38. Feinstein, D. L., Heneka, M. T., Gavrilyuk, V., Dello Russo, C., Weinberg, G., and Galea, E. (2002). Noradrenergic regulation of inflammatory gene expression in brain. Neurochem. Int. 41, 357-365. doi: 10.1016/S0197-0186(02)00049-9
39. Ferry, B., and McGaugh, J. L. (1999). Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task. Neurobiol. Learn. Mem. 72, 8-12. doi: 10.1006/nlme.1998.3904
40. Fields, R. D., Araque, A., Johansen-Berg, H., Lim, S. S., Lynch, G., Nave, K. A., et al. (2014). Glial biology in learning and cognition. Neuroscientist 20, 426-431. doi: 10.1177/1073858413504465
41. Frank, M. G., Thompson, B. M., Watkins, L. R., and Maier, S. F. (2012). Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain Behav. Immun. 26, 337-345. doi: 10.1016/j.bbi.2011.10.005
42. Frohman, E. M., Vayuvegula, B., Gupta, S., and van den Noort, S. (1988). Norepinephrine inhibits gamma-interferon-induced major histocompatibility class II (Ia) antigen expression on cultured astrocytes via beta-2-adrenergic signal transduction mechanisms. Proc. Natl. Acad. Sci. U.S.A. 85, 1292-1296. doi: 10.1073/pnas.85.4.1292
43. Fuchs, E., and Flügge, G. (2003). Chronic social stress: effects on limbic brain structures. Physiol. Behav. 79,417-427. doi: 10.1016/S0031-9384(03)00161-6
44. Funder, J. W. (1994). Corticosteroid hormones and signal specificity. Ann. N.Y. Acad. Sci. 746, 1-6. discussion: 6-7, 64-67. doi: 10.1111/j.1749-6632.1994.tb39202.x
45. Gibbs, M. E., and Bowser, D. N. (2010). Astrocytic adrenoceptors and learning: alpha1-adrenoceptors. Neurochem. Int. 57, 404-410. doi: 10.1016/j.neuint.2010.03.020
46. Gibbs, M. E., Hutchinson, D. S., and Summers, R. J. (2008). Role of beta-adrenoceptors in memory consolidation: beta3-adrenoceptors act on glucose uptake and beta2-adrenoceptors on glycogenolysis. Neuropsychopharmacology 33, 2384-2397. doi: 10.1038/sj.npp.1301629
47. Gibbs, M. E., Hutchinson, D. S., and Summers, R. J. (2010). Noradrenaline release in the locus coeruleus modulates memory formation and consolidation; roles for alpha-and beta-adrenergic receptors. Neuroscience 170, 1209-1222. doi: 10.1016/j.neuroscience.2010.07.052
48. Goshen, I., Kreisel, T., Ounallah-Saad, H., Renbaum, P., Zalzstein, Y., Ben-Hur, T., et al. (2007). A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 32, 1106-1115. doi: 10.1016/j.psyneuen.2007.09.004
49. Goujon, E., Parnet, P., Layé, S., Combe, C., and Dantzer, R. (1996). Adrenalectomy enhances pro-inflammatory cytokines gene expression, in the spleen, pituitary and brain ofmice in response to lipopolysaccharide. Brain Res. Mol. Brain Res. 36, 53-62. doi: 10.1016/0169-328X(95)00242-K
50. Griffith, R., and Sutin, J. (1996). Reactive astrocyte formation in vivo is regulated by noradrenergic axons. J. Comp. Neurol. 371, 362-375
51. Griñan-Ferré, C., Pérez-Cáceres, D., Gutiérrez-Zetina, S. M., Camins, A., Palomera-Avalos, V., Ortuño-Sahagún, D., et al. (2015). Environmental enrichment improves behavior, cognition, and brain functional markers in young senescence-accelerated prone mice (SAMP8). Mol. Neurobiol. doi: 10.1007/s12035-015-9210-6. [Epub ahead of print].
52. Gubba, E. M., Fawcett, J. W., and Herbert, J. (2004). The effects of corticosterone and dehydroepiandrosterone on neurotrophic factor mRNA expression in primary hippocampal and astrocyte cultures. Brain Res. Mol. Brain Res. 127, 48-59. doi: 10.1016/j.molbrainres.2004.05.004
53. Guidotti, G., Calabrese, F., Anacker, C., Racagni, G., Pariante, C. M., and Riva, M. A. (2013). Glucocorticoid receptor and FKBP5 expression is altered following exposure to chronic stress: modulation by antidepressant treatment. Neuropsychopharmacology 38, 616-627. doi: 10.1038/npp.2012.225
54. Gyoneva, S., and Traynelis, S. F. (2013). Norepinephrine modulates the motility of resting and activated microglia via different adrenergic receptors. J. Biol. Chem. 288, 15291-15302. doi: 10.1074/jbc.M113.458901
55. Hartmann, J., Wagner, K. V., Liebl, C., Scharf, S. H., Wang, X. D., Wolf, M., et al. (2012). The involvement of FK506-binding protein 51 (FKBP5) in the behavioral and neuroendocrine effects of chronic social defeat stress. Neuropharmacology 62, 332-339. doi: 10.1016/j.neuropharm.2011.07.041
56. Hashikawa, N., Ogawa, T., Sakamoto, Y., Ogawa, M., Matsuo, Y., Zamami, Y., et al. (2015). Time course ofbehavioral alteration and mRNA levels of neurotrophic factor following stress exposure in mouse. Cell. Mol. Neurobiol. 35, 807-817. doi: 10.1007/s10571-015-0174-x
57. Hassanpoor, H., Fallah, A., and Raza, M. (2014). Mechanisms of hippocampal astrocytes mediation of spatial memory and theta rhythm by gliotransmitters and growth factors. Cell Biol. Int. 38, 1355-1366. doi: 10.1002/cbin.10326
58. Hatfield, T., and McGaugh, J. L. (1999). Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol. Learn. Mem. 71, 232-239. doi: 10.1006/nlme.1998.3875
59. Heisler, J. M., and O’Connor, J. C. (2015). Indoleamine 2,3-dioxygenase-dependent neurotoxic kynurenine metabolism mediates inflammation-induced deficit in recognition memory. Brain Behav. Immun. 50, 115-124. doi: 10.1016/j.bbi.2015.06.022
60. Heneka, M. T., Carson, M. J., El Khoury, J., Landreth, G. E., Brosseron, F., Feinstein, D. L., et al. (2015). Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 14, 388-405. doi: 10.1016/S1474-4422(15)70016-5
61. Heneka, M. T., Nadrigny, F., Regen, T., Martinez-Hernandez, A., Dumitrescu-Ozimek, L., Terwel, D., et al. (2010). Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine. Proc. Natl. Acad. Sci. U.S.A. 107, 6058-6063. doi: 10.1073/pnas.0909586107
62. Herman, J. P., Patel, P. D., Akil, H., and Watson, S. J. (1989). Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Mol. Endocrinol. 3, 1886-1894. doi: 10.1210/mend-3-11-1886
63. Hertz, L., Lovatt, D., Goldman, S. A., and Nedergaard, M. (2010). Adrenoceptors in brain: cellular gene expression and effects on astrocytic metabolism and [Ca(2+)]i. Neurochem. Int. 57, 411-420. doi: 10.1016/j.neuint.2010.03.019
64. Hertz, L., Peng, L., and Dienel, G. A. (2007). Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J. Cereb. Blood Flow Metab. 27, 219-249. doi: 10.1038/sj.jcbfm.9600343
65. Hertz, L., Schousboe, I., and Schousboe, A. (1984). Receptor expression in primary cultures ofneurons or astrocytes. Prog. Neuropsychopharmacol. Biol. Psychiatry 8, 521-527. doi: 10.1016/0278-5846(84)90010-1
66. Hetier, E., Ayala, J., Bousseau, A., and Prochiantz, A. (1991). Modulation of interleukin-1 and tumor necrosis factor expression by beta-adrenergic agonists in mouse ameboid microglial cells. Exp. Brain Res. 86, 407-413. doi: 10.1007/BF00228965
67. Hsu, T. M., Konanur, V. R., Taing, L., Usui, R., Kayser, B. D., Goran, M. I., et al. (2015). Effects of sucrose and high fructose corn syrup consumption on spatial memory function and hippocampal neuroinflammation in adolescent rats. Hippocampus 25, 227-239. doi: 10.1002/hipo.22368
68. Huang, R., and Hertz, L. (1995). Noradrenaline-induced stimulation of glutamine metabolism in primary cultures of astrocytes. J. Neurosci. Res. 41, 677-683. doi: 10.1002/jnr.490410514
69. Huang, Z. B., and Sheng, G. Q. (2010). Interleukin-1beta with learning and memory. Neurosci. Bull. 26, 455-468. doi: 10.1007/s12264-010-6023-5
70. Hutchinson, D. S., Summers, R. J., and Gibbs, M. E. (2007). Beta2-and beta3-adrenoceptors activate glucose uptake in chick astrocytes by distinct mechanisms: a mechanism for memory enhancement? J. Neurochem. 103, 997-1008. doi: 10.1111/j.1471-4159.2007.04789.x
71. Hutchinson, D. S., Summers, R. J., and Gibbs, M. E. (2008). Energy metabolism and memory processing: role of glucose transport and glycogen in responses to adrenoceptor activation in the chicken. Brain Res. Bull. 76, 224-234. doi: 10.1016/j.brainresbull.2008.02.019
72. Hwang, I. K., Choi, J. H., Nam, S. M., Park, O. K., Yoo, D. Y., Kim, W., et al. (2014). Activation of microglia and induction of pro-inflammatory cytokines in the hippocampus of type 2 diabetic rats. Neurol. Res. 36, 824-832. doi: 10.1179/1743132814Y.0000000330
73. Iadecola, C., and Nedergaard, M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369-1376. doi: 10.1038/nn2003
74. Ilschner, S., Nolte, C., and Kettenmann, H. (1996). Complement factor C5a and epidermal growth factor trigger the activation of outward potassium currents in cultured murine microglia. Neuroscience 73, 1109-1120. doi: 10.1016/0306-4522(96)00107-8
75. Jauregui-Huerta, F., Ruvalcaba-Delgadillo, Y., Gonzalez-Castañeda, R., Garcia-Estrada, J., Gonzalez-Perez, O., and Luquin, S. (2010). Responses of glial cells to stress and glucocorticoids. Curr. Immunol. Rev. 6, 195-204. doi: 10.2174/157339510791823790
76. Jo, W. K., Zhang, Y., Emrich, H. M., and Dietrich, D. E. (2015). Glia in the cytokine-mediated onset of depression: fine tuning the immune response. Front. Cell. Neurosci. 9:268. doi: 10.3389/fncel.2015.00268
77. Joëls, M. (2006). Corticosteroid effects in the brain: U-shape it. Trends Pharmacol. Sci. 27, 244-250. doi: 10.1016/j.tips.2006.03.007
78. Joels, M., and de Kloet, E. R. (1989). Effects ofglucocorticoids and norepinephrine on the excitability in the hippocampus. Science 245, 1502-1505. doi: 10.1126/science.2781292
79. Joëls, M., Karst, H., Alfarez, D., Heine, V. M., Qin, Y., van Riel, E., et al. (2004). Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7, 221-231. doi: 10.1080/10253890500070005
80. Jones, M. E., Lebonville, C. L., Barrus, D., and Lysle, D. T. (2015). The role of brain interleukin-1 in stress-enhanced fear learning. Neuropsychopharmacology 40, 1289-1296. doi: 10.1038/npp.2014.317
81. Kabitzke, P. A., Silva, L., and Wiedenmayer, C. (2011). Norepinephrine mediates contextual fear learning and hippocampal pCREB in juvenile rats exposed to predator odor. Neurobiol. Learn. Mem. 96, 166-172. doi: 10.1016/j.nlm.2011.04.003
82. Kälin, S., Heppner, F. L., Bechmann, I., Prinz, M., Tschop, M. H., and Yi, C. X. (2015). Hypothalamic innate immune reaction in obesity. Nat. Rev. Endocrinol. 11, 339-351. doi: 10.1038/nrendo.2015.48
83. Kang, K., Lee, S. W., Han, J. E., Choi, J. W., and Song, M. R. (2014a). The complex morphology of reactive astrocytes controlled by fibroblast growth factor signaling. Glia 62, 1328-1344. doi: 10.1002/glia.22684
84. Kang, W., Balordi, F., Su, N., Chen, L., Fishell, G., and Hébert, J. M. (2014b). Astrocyte activation is suppressed in both normal and injured brain by FGF signaling. Proc. Natl. Acad. Sci. USA. 111, E2987-E2995. doi: 10.1073/pnas.1320401111
85. Karatsoreos, I. N., Bhagat, S. M., Bowles, N. P., Weil, Z. M., Pfaff, D. W., and McEwen, B. S. (2010). Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 151,2117-2127. doi: 10.1210/en.2009-1436
86. Kawai, T., and Akira, S. (2010). The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384. doi: 10.1038/ni.1863
87. Kettenmann, H. (2007). Neuroscience: the brain's garbage men. Nature 446, 987-989. doi: 10.1038/nature05713
88. Kirby, E. D., Muroy, S. E., Sun, W. G., Covarrubias, D., Leong, M. J., Barchas, L. A., et al. (2013). Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2. Elife 2:e00362. doi: 10.7554/eLife.00362
89. Kirschbaum, C., Wolf, O. T., May, M., Wippich, W., and Hellhammer, D. H. (1996). Stress-and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci. 58, 1475-1483. doi: 10.1016/0024-3205(96)00118-X
90. Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J. C., Pariante, C. M., et al. (2013). Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat. Neurosci. 16, 33-41. doi: 10.1038/nn.3275
91. Koyama, Y. (2015). Functional alterations of astrocytes in mental disorders: pharmacological significance as a drug target. Front. Cell. Neurosci. 9:261. doi: 10.3389/fncel.2015.00261
92. Kreisel, T., Frank, M. G., Licht, T., Reshef, R., Ben-Menachem-Zidon, O., Baratta, M. V., et al. (2014). Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis. Mol. Psychiatry 19, 699-709. doi: 10.1038/mp.2013.155
93. Kröll, S., El-Gindi, J., Thanabalasundaram, G., Panpumthong, P., Schrot, S., Hartmann, C., et al. (2009). Control of the blood-brain barrier by glucocorticoids and the cells of the neurovascular unit. Ann. N.Y. Acad. Sci. 1165,228-239. doi: 10.1111/j.1749-6632.2009.04040.x
94. LaLumiere, R. T., Buen, T. V., and McGaugh, J. L. (2003). Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. J. Neurosci. 23, 6754-6758
95. Lalumiere, R. T., and McGaugh, J. L. (2005). Memory enhancement induced by post-training intrabasolateral amygdala infusions of beta-adrenergic or muscarinic agonists requires activation of dopamine receptors: involvement of right, but not left, basolateral amygdala. Learn. Mem. 12, 527-532. doi: 10.1101/lm.97405
96. Lambert, K. G., Gerecke, K. M., Quadros, P. S., Doudera, E., Jasnow, A. M., and Kinsley, C. H. (2000). Activity-stress increases density of GFAP-immunoreactive astrocytes in the rat hippocampus. Stress 3, 275-284. doi: 10.3109/10253890009001133
97. Lang, F., Strutz-Seebohm, N., Seebohm, G., and Lang, U. E. (2010). Significance of SGK1 in the regulation ofneuronal function. J. Physiol. (Lond.) 588, 3349-3354. doi: 10.1113/jphysiol.2010.190926
98. Laping, N. J., Nichols, N. R., Day, J. R., Johnson, S. A., and Finch, C. E. (1994). Transcriptional control of glial fibrillary acidic protein and glutamine synthetase in vivo shows opposite responses to corticosterone in the hippocampus. Endocrinology 135, 1928-1933
99. Lee, C. T., Ma, Y. L., and Lee, E. H. (2007). Serum-and glucocorticoid-inducible kinase1 enhances contextual fear memory formation through down-regulation of the expression of Hes5. J. Neurochem. 100, 1531-1542. doi: 10.1111/j.1471-4159.2006.04284.x
100. Lee, M., McGeer, E., and McGeer, P. L. (2015). Activated human microglia stimulate neuroblastoma cells to upregulate production ofbeta amyloid protein and tau: implications for Alzheimer's disease pathogenesis. Neurobiol. Aging 36, 52. doi: 10.1016/j.neurobiolaging.2014.07.024
101. Legido, A., and Katsetos, C. D. (2014). Experimental studies in epilepsy: immunologic and inflammatory mechanisms. Semin. Pediatr. Neurol. 21, 197-206. doi: 10.1016/j.spen.2014.10.001
102. Lehmann, M. L., Brachman, R. A., Martinowich, K., Schloesser, R. J., and Herkenham, M. (2013). Glucocorticoids orchestrate divergent effects on mood through adult neurogenesis. J. Neurosci. 33, 2961-2972. doi: 10.1523/JNEUROSCI.3878-12.2013
103. Levy-Gigi, E., Szabó, C., Kelemen, O., and Kéri, S. (2013). Association among clinical response, hippocampal volume, and FKBP5 gene expression in individuals with posttraumatic stress disorder receiving cognitive behavioral therapy. Biol. Psychiatry 74, 793-800. doi: 10.1016/j.biopsych.2013.05.017
104. Li, S., Wang, C., Wang, W., Dong, H., Hou, P., and Tang, Y. (2008). Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci. 82, 934-942. doi: 10.1016/j.lfs.2008.02.010
105. Liang, K. C., Juler, R. G., and McGaugh, J. L. (1986). Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res. 368, 125-133. doi: 10.1016/0006-8993(86)91049-8
106. Liang, K. C., and McGaugh, J. L. (1983). Lesions of the stria terminalis attenuate the enhancing effect of post-training epinephrine on retention of an inhibitory avoidance response. Behav. Brain Res. 9, 49-58. doi: 10.1016/0166-4328(83)90013-X
107. Liang, K. C., McGaugh, J. L., and Yao, H. Y. (1990). Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res. 508, 225-233. doi: 10.1016/0006-8993(90)90400-6
108. Liberzon, I., López, J. F., Flagel, S. B., Vázquez, D. M., and Young, E. A. (1999). Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: relevance to post-traumatic stress disorder. J. Neuroendocrinol. 11, 11-17. doi: 10.1046/j.1365-2826.1999.00288.x
109. Longden, T. A., Dabertrand, F., Hill-Eubanks, D. C., Hammack, S. E., and Nelson, M. T. (2014). Stress-induced glucocorticoid signaling remodels neurovascular coupling through impairment of cerebrovascular inwardly rectifying K+ channel function. Proc. Natl. Acad. Sci. U.S.A. 111, 7462-7467. doi: 10.1073/pnas.1401811111
110. Lupien, S. J., Wilkinson, C. W., Brière, S., Ménard, C., Ng Ying Kin, N. M., and Nair, N. P. (2002a). The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology 27, 401-416. doi: 10.1016/S0306-4530(01)00061-0
111. Lupien, S. J., Wilkinson, C. W., Brière, S., Ng Ying Kin, N. M., Meaney, M. J., and Nair, N. P. (2002b). Acute modulation of aged human memory by pharmacological manipulation of glucocorticoids. J. Clin. Endocrinol. Metab. 87, 3798-3807. doi: 10.1210/jcem.87.8.8760
112. Mann, S. A., Versmold, B., Marx, R., Stahlhofen, S., Dietzel, I. D., Heumann, R., et al. (2008). Corticosteroids reverse cytokine-induced block of survival and differentiation of oligodendrocyte progenitor cells from rats. J. Neuroinflammation 5:39. doi: 10.1186/1742-2094-5-39
113. Martocchia, A., Stefanelli, M., Falaschi, G. M., Toussan, L., Ferri, C., and Falaschi, P. (2015). Recent advances in the role of cortisol and metabolic syndrome in age-related degenerative diseases. Aging Clin. Exp. Res. doi: 10.1007/s40520-015-0353-0. [Epub ahead of print].
114. McEwen, B. S., and Sapolsky, R. M. (1995). Stress and cognitive function. Curr. Opin. Neurobiol. 5, 205-216. doi: 10.1016/0959-4388(95)80028-X
115. McNay, E. C., and Gold, P. E. (2002). Food for thought: fluctuations in brain extracellular glucose provide insight into the mechanisms of memory modulation. Behav. Cogn. Neurosci. Rev. 1, 264-280. doi: 10.1177/1534582302238337
116. Melcangi, R. C., Cavarretta, I., Magnaghi, V., Ciusani, E., and Salmaggi, A. (2000). Corticosteroids protect oligodendrocytes from cytokine-induced cell death. Neuroreport 11, 3969-3972. doi: 10.1097/00001756-200012180­00013
117. Miura, H., Ozaki, N., Sawada, M., Isobe, K., Ohta, T., and Nagatsu, T. (2008). A link between stress and depression: shifts in the balance between the kynurenine and serotonin pathways of tryptophan metabolism and the etiology and pathophysiology of depression. Stress 11, 198-209. doi: 10.1080/10253890701754068
118. Miyata, S., Hattori, T., Shimizu, S., Ito, A., and Tohyama, M. (2015). Disturbance of oligodendrocyte function plays a key role in the pathogenesis of schizophrenia and major depressive disorder. Biomed Res. Int. 2015:492367. doi: 10.1155/2015/492367
119. Miyata, S., Koyama, Y., Takemoto, K., Yoshikawa, K., Ishikawa, T., Taniguchi, M., et al. (2011). Plasma corticosterone activates SGK1 and induces morphological changes in oligodendrocytes in corpus callosum. PLoS ONE 6:e19859. doi: 10.1371/journal.pone.0019859
120. Mocchetti, I., Spiga, G., Hayes, V. Y., Isackson, P. J., and Colangelo, A. (1996). Glucocorticoids differentially increase nerve growth factor and basic fibroblast growth factor expression in the rat brain. J. Neurosci. 16, 2141-2148
121. Molteni, R., Fumagalli, F., Magnaghi, V., Roceri, M., Gennarelli, M., Racagni, G, et al. (2001). Modulation of fibroblast growth factor-2 by stress and corticosteroids: from developmental events to adult brain plasticity. Brain Res. Brain Res. Rev. 37, 249-258. doi: 10.1016/S0165-0173(01)00128-X
122. Moraga-Amaro, R., Jerez-Baraona, J. M., Simon, F., and Stehberg, J. (2014). Role of astrocytes in memory and psychiatric disorders. J. Physiol. Paris 108, 240-251. doi: 10.1016/j.jphysparis.2014.08.005
123. Mori, K., Ozaki, E., Zhang, B., Yang, L., Yokoyama, A., Takeda, I., et al. (2002). Effects of norepinephrine on rat cultured microglial cells that express alpha1, alpha2, beta1 and beta2 adrenergic receptors. Neuropharmacology 43, 1026-1034. doi: 10.1016/S0028-3908(02)00211-3
124. Morris, G. P., Clark, I. A., Zinn, R., and Vissel, B. (2013). Microglia: a new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research. Neurobiol. Learn. Mem. 105, 40-53. doi: 10.1016/j.nlm.2013.07.002
125. Mufson, E. J., Ginsberg, S. D., Ikonomovic, M. D., and DeKosky, S. T. (2003). Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction. J. Chem. Neuroanat. 26, 233-242. doi: 10.1016/S0891-0618(03)00068-1
126. Munhoz, C. D., Lepsch, L. B., Kawamoto, E. M., Malta, M. B., de Lima L. S., Avellar, M. C., et al. (2006). Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J. Neurosci. 26, 3813-3820. doi: 10.1523/JNEUROSCI.4398-05.2006
127. Nelson, P. A., Sage, J. R., Wood, S. C., Davenport, C. M., Anagnostaras, S. G., and Boulanger, L. M. (2013). MHC class I immune proteins are critical hippocampus-dependent memory and gate NMDAR-dependent hippocampal long-term depression. Learn. Mem. 20, 505-517. doi: 10.1101/lm.031351.113
128. Nichols, N. R., Masters, J. N., and Finch, C. E. (1990). Changes in gene expression in hippocampus in response to glucocorticoids and stress. Brain Res. Bull. 24, 659-662. doi: 10.1016/0361-9230(90)90004-J
129. Nisticò, R., Mori, F., Feligioni, M., Nicoletti, F., and Centonze, D. (2014). Synaptic plasticity in multiple sclerosis and in experimental autoimmune encephalomyelitis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369:20130162. doi: 10.1098/rstb.2013.0162
130. Notarianni, E. (2013). Hypercortisolemia and glucocorticoid receptor-signaling insufficiency in Alzheimer's disease initiation and development. Curr. Alzheimer Res. 10, 714-731. doi: 10.2174/15672050113109990137
131. O'Donnell, J., Zeppenfeld, D., McConnell, E., Pena, S., and Nedergaard, M. (2012). Norepinephrine: a neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem. Res. 37, 2496-2512. doi: 10.1007/s11064-012-0818-x
132. Oitzl, M. S., and de Kloet, E. R. (1992). Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106, 62-71. doi: 10.1037/0735-7044.106.1.62
133. Oitzl, M. S., Reichardt, H. M., Joels, M., and de Kloet, E. R. (2001). Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc. Natl. Acad. Sci. U.S.A. 98, 12790-12795. doi: 10.1073/pnas.231313998
134. Osborne, D. M., Pearson-Leary, J., and McNay, E. C. (2015). The neuroenergetics of stress hormones in the hippocampus and implications for memory. Front. Neurosci. 9:164. doi: 10.3389/fnins.2015.00164
135. Paredes, S., and Ribeiro, L. (2014). Cortisol: the villain in metabolic syndrome? Rev. Assoc. Med. Bras. 60, 84-92. doi: 10.1590/1806-9282.60.01.017
136. Parpura, V., Baker, B. J., Jeras, M., and Zorec, R. (2010). Regulated exocytosis in astrocytic signal integration. Neurochem. Int. 57, 451-459. doi: 10.1016/j.neuint.2010.02.007
137. Parpura, V., Grubišic, V., and Verkhratsky, A. (2011). Ca(2+) sources for the exocytotic release of glutamate from astrocytes. Biochim. Biophys. Acta 1813, 984-991. doi: 10.1016/j.bbamcr.2010.11.006
138. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., and Bessis, A. (2012). Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. U.S.A. 109, E197-E205. doi: 10.1073/pnas.1111098109
139. Patterson, S. L. (2015). Immune dysregulation and cognitive vulnerability in the aging brain: interactions of microglia, IL-1beta, BDNF and synaptic plasticity. Neuropharmacology 96, 11-18. doi: 10.1016/j.neuropharm.2014.12.020
140. Petrov, T., Krukoff, T. L., and Jhamandas, J. H. (1993). Branching projections of catecholaminergic brainstem neurons to the paraventricular hypothalamic nucleus and the central nucleus of the amygdala in the rat. Brain Res. 609, 81-92. doi: 10.1016/0006-8993(93)90858-K
141. Polman, J. A., de Kloet, E. R., and Datson, N. A. (2013). Two populations of glucocorticoid receptor-binding sites in the male rat hippocampal genome. Endocrinology 154, 1832-1844. doi: 10.1210/en.2012-2187
142. Popoli, M., Yan, Z., McEwen, B. S., and Sanacora, G. (2012). The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat. Rev. Neurosci. 13, 22-37. doi: 10.1038/nrn3138
143. Psarra, A. M., and Sekeris, C. E. (2009). Glucocorticoid receptors and other nuclear transcription factors in mitochondria and possible functions. Biochim. Biophys. Acta 1787, 431-436. doi: 10.1016/j.bbabio.2008.11.011
144. Quirarte, G. L., Roozendaal, B., and McGaugh, J. L. (1997). Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 94, 14048-14053. doi: 10.1073/pnas.94.25.14048
145. Radley, J. J., Anderson, R. M., Hamilton, B. A., Alcock, J. A., and Romig-Martin, S. A. (2013). Chronic stress-induced alterations of dendritic spine subtypes predict functional decrements in an hypothalamo-pituitary-adrenal-inhibitory prefrontal circuit. J. Neurosci. 33, 14379-14391. doi: 10.1523/JNEUROSCI.0287-13.2013
146. Rajkowska, G., and Miguel-Hidalgo, J. J. (2007). Gliogenesis and glial pathology in depression. CNS Neurol. Disord. Drug Targets 6, 219-233. doi: 10.2174/187152707780619326
147. Ramos-Rodriguez, J. J., Jimenez-Palomares, M., Murillo-Carretero, M. I., Infante-Garcia, C., Berrocoso, E., Hernandez-Pacho, F., et al. (2015). Central vascular disease and exacerbated pathology in a mixed model of type 2 diabetes and Alzheimer's disease. Psychoneuroendocrinology 62, 69-79. doi: 10.1016/j.psyneuen.2015.07.606
148. Reagan, L. P. (2012). Diabetes as a chronic metabolic stressor: causes, consequences and clinical complications. Exp. Neurol. 233, 68-78. doi: 10.1016/j.expneurol.2011.02.004
149. Reul, J. M., and de Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117, 2505-2511. doi: 10.1210/endo-117-6-2505
150. Reul, J. M., and de Kloet, E. R. (1986). Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis. J. Steroid Biochem. 24, 269-272. doi: 10.1016/0022-4731(86)90063-4
151. Reul, J. M., Bilang-Bleuel, A., Droste, S., Linthorst, A. C., Holsboer, F., and Gesing, A. (2000a). New mode of hypothalamic-pituitary-adrenocortical axis regulation: significance for stress-related disorders. Z Rheumatol 59(Suppl. 2), II/22-25
152. Reul, J. M., Gesing, A., Droste, S., Stec, I. S., Weber, A., Bachmann, C., et al. (2000b). The brain mineralocorticoid receptor: greedy for ligand, mysterious in function. Eur. J. Pharmacol. 405, 235-249. doi: 10.1016/S0014-2999(00)00677-4
153. Richter-Levin, G. (2004). The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10, 31-39. doi: 10.1177/1073858403259955
154. Rodríguez, J. J., Witton, J., Olabarria, M., Noristani, H. N., and Verkhratsky, A. (2010). Increase in the density of resting microglia precedes neuritic plaque formation and microglial activation in a transgenic model of Alzheimer's disease. Cell Death Dis. 1, e1. doi: 10.1038/cddis.2009.2
155. Roozendaal, B. (2002). Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol. Learn. Mem. 78, 578-595. doi: 10.1006/nlme.2002.4080
156. Roozendaal, B. (2003). Systems mediating acute glucocorticoid effects on memory consolidation and retrieval. Prog. Neuropsychopharmacol. Biol. Psychiatry 27, 1213-1223. doi: 10.1016/j.pnpbp.2003.09.015
157. Roozendaal, B., Carmi, O., and McGaugh, J. L. (1996). Adrenocortical suppression blocks the memory-enhancing effects of amphetamine and epinephrine. Proc. Natl. Acad. Sci. U.S.A. 93, 1429-1433. doi: 10.1073/pnas.93.4.1429
158. Roozendaal, B., andMcGaugh, J. L. (1996). Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn. Mem. 65, 1-8. doi: 10.1006/nlme.1996.0001
159. Roozendaal, B., Nguyen, B. T., Power, A. E., and McGaugh, J. L. (1999). Basolateral amygdala noradrenergic influence enables enhancement ofmemory consolidation induced by hippocampal glucocorticoid receptor activation. Proc. Natl. Acad. Sci. U.S.A. 96, 11642-11647. doi: 10.1073/pnas.96.20.11642
160. Ross, F. M., Allan, S. M., Rothwell, N. J., and Verkhratsky, A. (2003). A dual role for interleukin-1 in LTP in mouse hippocampal slices. J. Neuroimmunol. 144, 61-67. doi: 10.1016/j.jneuroim.2003.08.030
161. Sahlender, D. A., Savtchouk, I., and Volterra, A. (2014). What do we know about gliotransmitter release from astrocytes? Philos. Trans. R. Soc. Lond. B Biol. Sci. 369:20130592. doi: 10.1098/rstb.2013.0592
162. Salehi, B., Cordero, M. I., and Sandi, C. (2010). Learning under stress: the inverted-U-shape function revisited. Learn. Mem. 17, 522-530. doi: 10.1101/lm.1914110
163. Sandi, C., Loscertales, M., and Guaza, C. (1997). Experience-dependent facilitating effect ofcorticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 9, 637-642. doi: 10.1111/j.1460-9568.1997.tb01412.x
164. Sandi, C., and Rose, S. P. (1994a). Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. Eur. J. Neurosci. 6, 1292-1297. doi: 10.1111/j.1460-9568.1994.tb00319.x
165. Sandi, C., and Rose, S. P. (1994b). Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res. 647, 106-112. doi: 10.1016/0006-8993(94)91404-4
166. Sandi, C., and Rose, S. P. (1997). Training-dependent biphasic effects of corticosterone in memory formation for a passive avoidance task in chicks. Psychopharmacology (Berl.) 133, 152-160. doi: 10.1007/s002130050385
167. Sapolsky, R. M. (1996). Why stress is bad for your brain. Science 273,749-750. doi: 10.1126/science.273.5276.749
168. Sapolsky, R. M., Krey, L. C., and McEwen, B. S. (1985). Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci. 5, 1222-1227.
169. Sarrieau, A., Vial, M., Philibert, D., Moguilewsky, M., Dussaillant, M., McEwen, B, et al. (1984). In vitro binding of tritiated glucocorticoids directly on unfixed rat brain sections. J. Steroid Biochem. 20, 1233-1238. doi: 10.1016/0022-4731(84)90150-X
170. Schindowski, K., Belarbi, K., and Buée, L. (2008). Neurotrophic factors in Alzheimer's disease: role of axonal transport. Genes Brain Behav 7(Suppl. 1), 56. doi: 10.1111/j.1601-183X.2007.00378.x
171. Schmidt, U., Buell, D. R., Ionescu, I. A., Gassen, N. C., Holsboer, F., Cox, M. B., et al. (2015). A role for synapsin in FKBP51 modulation of stress responsiveness: convergent evidence from animal and human studies. Psychoneuroendocrinology 52, 43-58. doi: 10.1016/j.psyneuen.2014.11.005
172. Schoenfeld, T. J., and Gould, E. (2013). Differential effects of stress and glucocorticoids on adult neurogenesis. Curr. Top. Behav. Neurosci. 15,139-164. doi: 10.1007/7854_2012_233
173. Schousboe, A., Westergaard, N., Sonnewald, U., Petersen, S. B., Huang, R., Peng, L., et al. (1993). Glutamate and glutamine metabolism and compartmentation in astrocytes. Dev. Neurosci. 15, 359-366. doi: 10.1159/000111356
174. Sierra, A., Gottfried-Blackmore, A., Milner, T. A., McEwen, B. S., and Bulloch, K. (2008). Steroid hormone receptor expression and function in microglia. Glia 56, 659-674. doi: 10.1002/glia.20644
175. Simard, M., Couldwell, W. T., Zhang, W., Song, H., Liu, S., Cotrina, M. L., et al. (1999). Glucocorticoids-potent modulators ofastrocytic calcium signaling. Glia 28, 1-12.
176. Smith, L. K., He, Y., Park, J. S., Bieri, G., Snethlage, C. E., Lin, K., et al. (2014). beta2-microglobulin is a systemic pro-aging factor that impairs cognitive function and neurogenesis. Nat. Med. 21, 932-937. doi: 10.1038/nm.3898
177. Spanswick, S. C., Epp, J. R., and Sutherland, R. J. (2011). Time-course of hippocampal granule cell degeneration and changes in adult neurogenesis after adrenalectomy in rats. Neuroscience 190, 166-176. doi: 10.1016/j.neuroscience.2011.06.023
178. Stehberg, J., Moraga-Amaro, R., Salazar, C., Becerra, A., Echeverría, C., Orellana, J. A., et al. (2012). Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J. 26, 3649-3657. doi: 10.1096/fj.11-198416
179. Stranahan, A. M., Arumugam, T. V., Cutler, R. G., Lee, K., Egan, J. M., and Mattson, M. P. (2008). Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat. Neurosci. 11, 309-317. doi: 10.1038/nn2055
180. Strutz-Seebohm, N., Seebohm, G., Mack, A. F., Wagner, H. J., Just, L., Skutella, T., et al. (2005). Regulation of GluR1 abundance in murine hippocampal neurones by serum-and glucocorticoid-inducible kinase 3. J. Physiol. (Lond.) 565, 381-390. doi: 10.1113/jphysiol.2004.079582
181. Stuart, M. J., and Baune, B. T. (2014). Chemokines and chemokine receptors in mood disorders, schizophrenia, and cognitive impairment: a systematic review of biomarker studies. Neurosci. Biobehav. Rev. 42, 93-115. doi: 10.1016/j.neubiorev.2014.02.001
182. Stuchlik, A., Petrasek, T., and Vales, K. (2009). A dose-response study of the effects of pre-test administration of beta-adrenergic receptor antagonist propranolol on the learning of active place avoidance, a spatial cognition task, in rats. Behav. Brain Res. 200, 144-149. doi: 10.1016/j.bbr.2009.01.010
183. Subbarao, K. V., and Hertz, L. (1990). Effect of adrenergic agonists on glycogenolysis in primary cultures of astrocytes. Brain Res. 536, 220-226. doi: 10.1016/0006-8993(90)90028-A
184. Subbarao, K. V., and Hertz, L. (1991). Stimulation of energy metabolism by alpha-adrenergic agonists in primary cultures of astrocytes. J. Neurosci. Res. 28, 399-405. doi: 10.1002/jnr.490280312
185. Suwanjang, W., Holmström, K. M., Chetsawang, B., and Abramov, A. Y. (2013). Glucocorticoids reduce intracellular calcium concentration and protects neurons against glutamate toxicity. Cell Calcium 53, 256-263. doi: 10.1016/j.ceca.2012.12.006
186. Suzuki, A., Stern, S. A., Bozdagi, O., Huntley, G. W., Walker, R. H., Magistretti, P. J., et al. (2011). Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144, 810-823. doi: 10.1016/j.cell.2011.02.018
187. Swanson, L. W., and Hartman, B. K. (1975). The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J. Comp. Neurol. 163, 467-505. doi: 10.1002/cne.901630406
188. Tai, D. J., Su, C. C., Ma, Y. L., and Lee, E. H. (2009). SGK1 phosphorylation of IkappaB Kinase alpha and p300 Up-regulates NF-kappaB activity and increases N-Methyl-D-aspartate receptor NR2A and NR2B expression. J. Biol. Chem. 284,4073-4089. doi: 10.1074/jbc.M805055200
189. Tanaka, K. F., Kashima, H., Suzuki, H., Ono, K., and Sawada, M. (2002). Existence of functional beta1-and beta2-adrenergic receptors on microglia. J. Neurosci. Res. 70, 232-237. doi: 10.1002/jnr.10399
190. Thomas, W. E. (1992). Brain macrophages: evaluation of microglia and their functions. Brain Res. Brain Res. Rev. 17, 61-74. doi: 10.1016/0165-0173(92)90007-9
191. Tonelli, L. H., and Postolache, T. T. (2005). Tumor necrosis factor alpha, interleukin-1 beta, interleukin-6 and major histocompatibility complex molecules in the normal brain and after peripheral immune challenge. Neurol. Res. 27, 679-684. doi: 10.1179/016164105X49463
192. Tynan, R. J., Weidenhofer, J., Hinwood, M., Cairns, M. J., Day, T. A., and Walker, F. R. (2012). A comparative examination of the anti-inflammatory effects of SSRI and SNRI antidepressants on LPS stimulated microglia. Brain Behav. Immun. 26, 469-479. doi: 10.1016/j.bbi.2011.12.011
193. Unemura, K., Kume, T., Kondo, M., Maeda, Y., Izumi, Y., and Akaike, A. (2012). Glucocorticoids decrease astrocyte numbers by reducing glucocorticoid receptor expression in vitro and in vivo. J. Pharmacol. Sci. 119, 30-39. doi: 10.1254/jphs.12047FP
194. Van Eekelen, J. A., Jiang, W., De Kloet, E. R., and Bohn, M. C. (1988). Distribution of the mineralocorticoid and the glucocorticoid receptor mRNAs in the rat hippocampus. J. Neurosci. Res. 21, 88-94. doi: 10.1002/jnr.490210113
195. Varga, D., Herédi, J., Kánvási, Z., Ruszka, M., Kis, Z., Ono, E., et al. (2015). Systemic L-Kynurenine sulfate administration disrupts object recognition memory, alters open field behavior and decreases c-Fos immunopositivity in C57Bl/6 mice. Front. Behav. Neurosci. 9:157. doi: 10.3389/fnbeh.2015.00157
196. Volterra, A., and Meldolesi, J. (2005). Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6, 626-640. doi: 10.1038/nrn1722
197. Walker, D. G., and Lue, L. F. (2015). Immune phenotypes of microglia in human neurodegenerative disease: challenges to detecting microglial polarization in human brains. Alzheimers. Res. Ther. 7, 56. doi: 10.1186/s13195-015-0139-9
198. Willi, S. M., Kennedy, A., Brant, B. P., Wallace, P., Rogers, N. L., and Garvey, W. T. (2002). Effective use of thiazolidinediones for the treatment of glucocorticoid-induced diabetes. Diabetes Res. Clin. Pract. 58, 87-96. doi: 10.1016/S0168-8227(02)00127-4
199. Williamson, L. L., and Bilbo, S. D. (2013). Chemokines and the hippocampus: a new perspective on hippocampal plasticity and vulnerability. Brain Behav. Immun. 30, 186-194. doi: 10.1016/j.bbi.2013.01.077
200. Womble, J. R., Larson, D. F., Copeland, J. G., Brown, B. R., Haddox, M. K., and Russell, D. H. (1980). Adrenal medulla denervation prevents stress-induced epinephrine plasma elevation and cardiac hypertrophy. Life Sci. 27, 2417-2420. doi: 10.1016/0024-3205(80)90513-5
201. Wong, D. L., Tai, T. C., Wong-Faull, D. C., Claycomb, R., Meloni, E. G., Myers, K. M., et al. (2012). Epinephrine: a short-and long-term regulator of stress and development of illness: a potential new role for epinephrine in stress. Cell. Mol. Neurobiol. 32, 737-748. doi: 10.1007/s10571-011-9768-0
202. Wood, S. K., Wood, C. S., Lombard, C. M., Lee, C. S., Zhang, X. Y., Finnell, J. E., et al. (2015). Inflammatory factors mediate vulnerability to a social stress-induced depressive-like phenotype in passive coping rats. Biol. Psychiatry 78, 38-48. doi: 10.1016/j.biopsych.2014.10.026
203. Xiang, Z., Haroutunian, V., Ho, L., Purohit, D., and Pasinetti, G. M. (2006). Microglia activation in the brain as inflammatory biomarker of Alzheimer's disease neuropathology and clinical dementia. Dis. Markers 22, 95-102. doi: 10.1155/2006/276239
204. Yang, F. C., and Liang, K. C. (2014). Interactions of the dorsal hippocampus, medial prefrontal cortex and nucleus accumbens in formation of fear memory: difference in inhibitory avoidance learning and contextual fear conditioning. Neurobiol. Learn. Mem. 112, 186-194. doi: 10.1016/j.nlm.2013.07.017
205. Yang, Y. C., Lin, C. H., and Lee, E. H. (2006). Serum-and glucocorticoid-inducible kinase 1 (SGK1) increases neurite formation through microtubule depolymerization bySGK1 and bySGK1 phosphorylation oftau. Mol. Cell. Biol. 26, 8357-8370. doi: 10.1128/MCB.01017-06
206. Yazir, Y., Utkan, T., Gacar, N., and Aricioglu, F. (2015). Resveratrol exerts anti­inflammatory and neuroprotective effects to prevent memory deficits in rats exposed to chronic unpredictable mild stress. Physiol. Behav. 138,297-304. doi: 10.1016/j.physbeh.2014.10.010
207. Ye, L., Wang, F., and Yang, R. H. (2011). Diabetes impairs learning performance and affects the mitochondrial function of hippocampal pyramidal neurons. Brain Res. 1411, 57-64. doi: 10.1016/j.brainres.2011.07.011
208. Yun, J., Koike, H., Ibi, D., Toth, E., Mizoguchi, H., Nitta, A., et al. (2010). Chronic restraint stress impairs neurogenesis and hippocampus-dependent fear memory in mice: possible involvement of a brain-specific transcription factor Npas4. J. Neurochem. 114, 1840-1851. doi: 10.1111/j.1471-4159.2010.06893.x