Cognitive dysfunction in mice lacking proper glucocorticoid receptor dimerization


Autoři: Kelly Van Looveren aff001;  Michiel Van Boxelaere aff003;  Zsuzsanna Callaerts-Vegh aff003;  Claude Libert aff001
Působiště autorů: Center for Inflammation Research, VIB, Ghent, Belgium aff001;  Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium aff002;  Laboratory of Biological Psychology, KULeuven, Leuven Belgium aff003;  Leuven Research Institute for Neuroscience & Disease (LIND), Leuven, Belgium aff004;  mINT Mouse Behavioural Core Facility, KULeuven, Leuven, Belgium aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226753

Souhrn

Stress is a major risk factor for depression and anxiety. One of the effects of stress is the (over-) activation of the hypothalamic-pituitary-adrenal (HPA) axis and the release of stress hormones such as glucocorticoids (GCs). Chronically increased stress hormone levels have been shown to have detrimental effects on neuronal networks by inhibiting neurotrophic processes particularly in the hippocampus proper. Centrally, GCs modulate metabolic as well as behavioural processes by activating two classes of corticoid receptors, high-affinity mineralocorticoid receptors (MR) and low-affinity glucocorticoid receptors (GR). Upon activation, GR can modulate gene transcription either as a monomeric protein, or as a dimer interacting directly with DNA. GR can also modulate cellular processes via non-genomic mechanisms, for example via a GPCR-protein interaction. We evaluated the behavioral phenotype in mice with a targeted mutation in the GR in a FVB/NJ background. In GRdim/dim mice, GR proteins form poor homodimers, while the GR monomer remains intact. We evaluated the effect of poor GR dimerization on hippocampus-dependent cognition as well as on exploration and emotional behavior under baseline and chronically increased stress hormone levels. We found that GRdim/dim mice did not behave differently from GRwt/wt littermates under baseline conditions. However, after chronic elevation of stress hormone levels, GRdim/dim mice displayed a significant impairment in hippocampus-dependent memory compared to GRwt/wt mice, which correlated with differential expression of hippocampal Bdnf/TrkB and Fkbp5.

Klíčová slova:

Animal behavior – Behavior – Cognitive impairment – Depression – Hippocampus – Memory – Mice – Psychological stress


Zdroje

1. Smith SM, Vale WW. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci. 2006;8(4):383–95. 17290797; PubMed Central PMCID: PMC3181830.

2. Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci. 2009;10(6):423–33. doi: 10.1038/nrn2651 19469026.

3. Joels M, Karst H, Sarabdjitsingh RA. The stressed brain of humans and rodents. Acta Physiol (Oxf). 2018;223(2):e13066. doi: 10.1111/apha.13066 29575542; PubMed Central PMCID: PMC5969253.

4. Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, et al. Regulation of the Hypothalamic-Pituitary-Adrenocortical Stress Response. Compr Physiol. 2016;6(2):603–21. doi: 10.1002/cphy.c150015 27065163; PubMed Central PMCID: PMC4867107.

5. Saaltink DJ, Vreugdenhil E. Stress, glucocorticoid receptors, and adult neurogenesis: a balance between excitation and inhibition? Cell Mol Life Sci. 2014;71(13):2499–515. doi: 10.1007/s00018-014-1568-5 24522255; PubMed Central PMCID: PMC4055840.

6. Duman RS, Aghajanian GK. Synaptic dysfunction in depression: potential therapeutic targets. Science. 2012;338(6103):68–72. doi: 10.1126/science.1222939 23042884; PubMed Central PMCID: PMC4424898.

7. Beato M, Klug J. Steroid hormone receptors: an update. Hum Reprod Update. 2000;6(3):225–36. doi: 10.1093/humupd/6.3.225 10874567.

8. Boumpas DT, Chrousos GP, Wilder RL, Cupps TR, Balow JE. Glucocorticoid therapy for immune-mediated diseases: basic and clinical correlates. Ann Intern Med. 1993;119(12):1198–208. doi: 10.7326/0003-4819-119-12-199312150-00007 8239251.

9. Cole TJ, Blendy JA, Monaghan AP, Schmid W, Aguzzi A, Schutz G. Molecular genetic analysis of glucocorticoid signaling during mouse development. Steroids. 1995;60(1):93–6. doi: 10.1016/0039-128x(94)00009-2 7792824.

10. Marques AH, Silverman MN, Sternberg EM. Glucocorticoid dysregulations and their clinical correlates. From receptors to therapeutics. Ann N Y Acad Sci. 2009;1179:1–18. doi: 10.1111/j.1749-6632.2009.04987.x 19906229; PubMed Central PMCID: PMC2933142.

11. Kanatsou S, Joels M, Krugers H. Brain Mineralocorticoid Receptors and Resilience to Stress. Vitam Horm. 2019;109:341–59. doi: 10.1016/bs.vh.2018.11.001 30678862.

12. de Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005;6(6):463–75. doi: 10.1038/nrn1683 15891777.

13. Joels M, Krugers HJ, Lucassen PJ, Karst H. Corticosteroid effects on cellular physiology of limbic cells. Brain Res. 2009;1293:91–100. doi: 10.1016/j.brainres.2009.03.036 WOS:000270865600010. 19332034

14. Groeneweg FL, Karst H, de Kloet ER, Joels M. Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol Cell Endocrinol. 2012;350(2):299–309. doi: 10.1016/j.mce.2011.06.020 21736918.

15. Chauveau F, Tronche C, Pierard C, Liscia P, Drouet I, Coutan M, et al. Rapid stress-induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern. Hippocampus. 2010;20(1):196–207. doi: 10.1002/hipo.20605 19360856.

16. Dorey R, Pierard C, Shinkaruk S, Tronche C, Chauveau F, Baudonnat M, et al. Membrane mineralocorticoid but not glucocorticoid receptors of the dorsal hippocampus mediate the rapid effects of corticosterone on memory retrieval. Neuropsychopharmacology. 2011;36(13):2639–49. doi: 10.1038/npp.2011.152 21814189; PubMed Central PMCID: PMC3230488.

17. Keller J, Gomez R, Williams G, Lembke A, Lazzeroni L, Murphy GM Jr., et al. HPA axis in major depression: cortisol, clinical symptomatology and genetic variation predict cognition. Mol Psychiatry. 2017;22(4):527–36. doi: 10.1038/mp.2016.120 27528460; PubMed Central PMCID: PMC5313380.

18. Claes S. Glucocorticoid receptor polymorphisms in major depression. Ann N Y Acad Sci. 2009;1179:216–28. doi: 10.1111/j.1749-6632.2009.05012.x 19906242.

19. Spijker AT, van Rossum EF. Glucocorticoid receptor polymorphisms in major depression. Focus on glucocorticoid sensitivity and neurocognitive functioning. Ann N Y Acad Sci. 2009;1179:199–215. doi: 10.1111/j.1749-6632.2009.04985.x 19906241.

20. Zimmermann CA, Arloth J, Santarelli S, Loschner A, Weber P, Schmidt MV, et al. Stress dynamically regulates co-expression networks of glucocorticoid receptor-dependent MDD and SCZ risk genes. Transl Psychiatry. 2019;9(1):41. doi: 10.1038/s41398-019-0373-1 30696808; PubMed Central PMCID: PMC6351530.

21. Murrough JW, Iacoviello B, Neumeister A, Charney DS, Iosifescu DV. Cognitive dysfunction in depression: neurocircuitry and new therapeutic strategies. Neurobiol Learn Mem. 2011;96(4):553–63. doi: 10.1016/j.nlm.2011.06.006 21704176.

22. Sumiyoshi T, Watanabe K, Noto S, Sakamoto S, Moriguchi Y, Tan KHX, et al. Relationship of cognitive impairment with depressive symptoms and psychosocial function in patients with major depressive disorder: Cross-sectional analysis of baseline data from PERFORM-J. J Affect Disord. 2019;258:172–8. doi: 10.1016/j.jad.2019.07.064 31426015.

23. Keller AS, Ball TM, Williams LM. Deep phenotyping of attention impairments and the 'Inattention Biotype' in Major Depressive Disorder. Psychol Med. 2019:1–10. doi: 10.1017/S0033291719002290 31477195.

24. Gasbarri A, Sulli A, Packard MG. The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry. 1997;21(1):1–22. doi: 10.1016/s0278-5846(96)00157-1 9075256.

25. Lisman JE, Grace AA. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron. 2005;46(5):703–13. doi: 10.1016/j.neuron.2005.05.002 15924857.

26. Shohamy D, Adcock RA. Dopamine and adaptive memory. Trends Cogn Sci. 2010;14(10):464–72. doi: 10.1016/j.tics.2010.08.002 20829095.

27. Boku S, Nakagawa S, Toda H, Hishimoto A. Neural basis of major depressive disorder: Beyond monoamine hypothesis. Psychiatry Clin Neurosci. 2018;72(1):3–12. doi: 10.1111/pcn.12604 28926161.

28. MacQueen GM, Campbell S, McEwen BS, Macdonald K, Amano S, Joffe RT, et al. Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci U S A. 2003;100(3):1387–92. doi: 10.1073/pnas.0337481100 12552118; PubMed Central PMCID: PMC298782.

29. Warner-Schmidt JL, Duman RS. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus. 2006;16(3):239–49. doi: 10.1002/hipo.20156 16425236.

30. Park SC. Neurogenesis and antidepressant action. Cell Tissue Res. 2019;377(1):95–106. doi: 10.1007/s00441-019-03043-5 31165247.

31. Culpepper L. Neuroanatomy and physiology of cognition. J Clin Psychiatry. 2015;76(7):e900. doi: 10.4088/JCP.13086tx3c 26231020.

32. Dillon DG, Pizzagalli DA. Mechanisms of Memory Disruption in Depression. Trends Neurosci. 2018;41(3):137–49. doi: 10.1016/j.tins.2017.12.006 29331265; PubMed Central PMCID: PMC5835184.

33. Hermans D, Van den Broeck K, Belis G, Raes F, Pieters G, Eelen P. Trauma and autobiographical memory specificity in depressed inpatients. Behav Res Ther. 2004;42(7):775–89. doi: 10.1016/S0005-7967(03)00197-9 15149898.

34. Hermans D, Vandromme H, Debeer E, Raes F, Demyttenaere K, Brunfaut E, et al. Overgeneral autobiographical memory predicts diagnostic status in depression. Behav Res Ther. 2008;46(5):668–77. doi: 10.1016/j.brat.2008.01.018 18342835.

35. Raes F, Hermans D, Williams JM, Beyers W, Brunfaut E, Eelen P. Reduced autobiographical memory specificity and rumination in predicting the course of depression. J Abnorm Psychol. 2006;115(4):699–704. doi: 10.1037/0021-843X.115.4.699 17100527.

36. Williams JM, Barnhofer T, Crane C, Herman D, Raes F, Watkins E, et al. Autobiographical memory specificity and emotional disorder. Psychol Bull. 2007;133(1):122–48. doi: 10.1037/0033-2909.133.1.122 17201573; PubMed Central PMCID: PMC2834574.

37. Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai HC, Finkelstein J, et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature. 2013;493(7433):537–41. doi: 10.1038/nature11740 23235822; PubMed Central PMCID: PMC4160519.

38. Dubrovina NI. Effects of activation of D1 dopamine receptors on extinction of a conditioned passive avoidance reflex and amnesia in aggressive and submissive mice. Neurosci Behav Physiol. 2006;36(6):679–84. doi: 10.1007/s11055-006-0073-1 16783522.

39. El-Ghundi M, O'Dowd BF, George SR. Insights into the role of dopamine receptor systems in learning and memory. Rev Neurosci. 2007;18(1):37–66. doi: 10.1515/revneuro.2007.18.1.37 17405450.

40. Fremeau RT Jr., Duncan GE, Fornaretto MG, Dearry A, Gingrich JA, Breese GR, et al. Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci U S A. 1991;88(9):3772–6. doi: 10.1073/pnas.88.9.3772 2023928; PubMed Central PMCID: PMC51535.

41. Granado N, Ortiz O, Suarez LM, Martin ED, Cena V, Solis JM, et al. D1 but not D5 dopamine receptors are critical for LTP, spatial learning, and LTP-Induced arc and zif268 expression in the hippocampus. Cereb Cortex. 2008;18(1):1–12. doi: 10.1093/cercor/bhm026 17395606.

42. Khan ZU, Gutierrez A, Martin R, Penafiel A, Rivera A, de la Calle A. Dopamine D5 receptors of rat and human brain. Neuroscience. 2000;100(4):689–99. doi: 10.1016/s0306-4522(00)00274-8 11036203.

43. Tran AH, Tamura R, Uwano T, Kobayashi T, Katsuki M, Ono T. Dopamine D1 receptors involved in locomotor activity and accumbens neural responses to prediction of reward associated with place. Proc Natl Acad Sci U S A. 2005;102(6):2117–22. doi: 10.1073/pnas.0409726102 15684065; PubMed Central PMCID: PMC548585.

44. Wang Y, Wu J, Zhu B, Li C, Cai JX. Dopamine D1 receptors are responsible for stress-induced emotional memory deficit in mice. Stress. 2012;15(2):237–42. doi: 10.3109/10253890.2011.607525 21875304.

45. Weiner DM, Levey AI, Sunahara RK, Niznik HB, O'Dowd BF, Seeman P, et al. D1 and D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci U S A. 1991;88(5):1859–63. doi: 10.1073/pnas.88.5.1859 1825729; PubMed Central PMCID: PMC51125.

46. Reichardt HM, Kaestner KH, Tuckermann J, Kretz O, Wessely O, Bock R, et al. DNA binding of the glucocorticoid receptor is not essential for survival. Cell. 1998;93(4):531–41. doi: 10.1016/s0092-8674(00)81183-6 9604929.

47. Watson LC, Kuchenbecker KM, Schiller BJ, Gross JD, Pufall MA, Yamamoto KR. The glucocorticoid receptor dimer interface allosterically transmits sequence-specific DNA signals. Nat Struct Mol Biol. 2013;20(7):876–83. doi: 10.1038/nsmb.2595 23728292; PubMed Central PMCID: PMC3702670.

48. Mohajeri MH, Madani R, Saini K, Lipp HP, Nitsch RM, Wolfer DP. The impact of genetic background on neurodegeneration and behavior in seizured mice. Genes Brain Behav. 2004;3(4):228–39. doi: 10.1111/j.1601-1848.2004.00073.x 15248868.

49. Li K, Nakajima M, Ibanez-Tallon I, Heintz N. A Cortical Circuit for Sexually Dimorphic Oxytocin-Dependent Anxiety Behaviors. Cell. 2016;167(1):60–72 e11. doi: 10.1016/j.cell.2016.08.067 27641503; PubMed Central PMCID: PMC5220951.

50. Marrocco J, Petty GH, Rios MB, Gray JD, Kogan JF, Waters EM, et al. A sexually dimorphic pre-stressed translational signature in CA3 pyramidal neurons of BDNF Val66Met mice. Nat Commun. 2017;8(1):808. doi: 10.1038/s41467-017-01014-4 28993643; PubMed Central PMCID: PMC5634406.

51. Darcet F, Mendez-David I, Tritschler L, Gardier AM, Guilloux JP, David DJ. Learning and memory impairments in a neuroendocrine mouse model of anxiety/depression. Front Behav Neurosci. 2014;8:136. doi: 10.3389/fnbeh.2014.00136 24822041; PubMed Central PMCID: PMC4013464.

52. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I, et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron. 2009;62(4):479–93. doi: 10.1016/j.neuron.2009.04.017 19477151; PubMed Central PMCID: PMC2759281.

53. Malisch JL, Saltzman W, Gomes FR, Rezende EL, Jeske DR, Garland T Jr. Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running. Physiol Biochem Zool. 2007;80(1):146–56. doi: 10.1086/508828 17160887.

54. Zalewska K, Ong LK, Johnson SJ, Nilsson M, Walker FR. Oral administration of corticosterone at stress-like levels drives microglial but not vascular disturbances post-stroke. Neuroscience. 2017;352:30–8. doi: 10.1016/j.neuroscience.2017.03.005 28288898.

55. Zalewska K, Pietrogrande G, Ong LK, Abdolhoseini M, Kluge M, Johnson SJ, et al. Sustained administration of corticosterone at stress-like levels after stroke suppressed glial reactivity at sites of thalamic secondary neurodegeneration. Brain Behav Immun. 2018;69:210–22. doi: 10.1016/j.bbi.2017.11.014 29162554.

56. Callaerts-Vegh Z, Beckers T, Ball SM, Baeyens F, Callaerts PF, Cryan JF, et al. Concomitant deficits in working memory and fear extinction are functionally dissociated from reduced anxiety in metabotropic glutamate receptor 7-deficient mice. J Neurosci. 2006;26(24):6573–82. doi: 10.1523/JNEUROSCI.1497-06.2006 16775145.

57. Naert A, Callaerts-Vegh Z, D'Hooge R. Nocturnal hyperactivity, increased social novelty preference and delayed extinction of fear responses in post-weaning socially isolated mice. Brain Res Bull. 2011;85(6):354–62. doi: 10.1016/j.brainresbull.2011.03.027 21501666.

58. Hughes RN. The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory. Neurosci Biobehav Rev. 2004;28(5):497–505. doi: 10.1016/j.neubiorev.2004.06.006 15465137.

59. Kraeuter AK, Guest PC, Sarnyai Z. The Y-Maze for Assessment of Spatial Working and Reference Memory in Mice. Methods Mol Biol. 2019;1916:105–11. doi: 10.1007/978-1-4939-8994-2_10 30535688.

60. Hiramatsu M, Sasaki M, Nabeshima T, Kameyama T. Effects of dynorphin A (1–13) on carbon monoxide-induced delayed amnesia in mice. Pharmacol Biochem Behav. 1997;56(1):73–9. doi: 10.1016/S0091-3057(96)00159-1 8981612.

61. Sarter M, Bodewitz G, Stephens DN. Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines. Psychopharmacology (Berl). 1988;94(4):491–5. doi: 10.1007/bf00212843 2836875.

62. Ito R, Robbins TW, Pennartz CM, Everitt BJ. Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning. J Neurosci. 2008;28(27):6950–9. doi: 10.1523/JNEUROSCI.1615-08.2008 18596169; PubMed Central PMCID: PMC3844800.

63. Tzschentke TM. Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol. 2007;12(3–4):227–462. doi: 10.1111/j.1369-1600.2007.00070.x 17678505.

64. Ferbinteanu J, McDonald RJ. Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus. 2001;11(2):187–200. doi: 10.1002/hipo.1036 11345125.

65. McDonald RJ, White NM. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci. 1993;107(1):3–22. doi: 10.1037//0735-7044.107.1.3 8447956.

66. Anagnostaras SG, Gale GD, Fanselow MS. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus. 2001;11(1):8–17. doi: 10.1002/1098-1063(2001)11:1<8::AID-HIPO1015>3.0.CO;2-7 11261775.

67. Bast T, Zhang WN, Feldon J. Dorsal hippocampus and classical fear conditioning to tone and context in rats: effects of local NMDA-receptor blockade and stimulation. Hippocampus. 2003;13(6):657–75. doi: 10.1002/hipo.10115 12962312.

68. Goddyn H, Leo S, Meert T, D'Hooge R. Differences in behavioural test battery performance between mice with hippocampal and cerebellar lesions. Behav Brain Res. 2006;173(1):138–47. doi: 10.1016/j.bbr.2006.06.016 16860407.

69. Lo AC, De Maeyer JH, Vermaercke B, Callaerts-Vegh Z, Schuurkes JA, D'Hooge R. SSP-002392, a new 5-HT4 receptor agonist, dose-dependently reverses scopolamine-induced learning and memory impairments in C57Bl/6 mice. Neuropharmacology. 2014;85:178–89. doi: 10.1016/j.neuropharm.2014.05.013 24863046.

70. Winocur G, Bindra D. Effects of additional cues on passive avoidance learning and extinction in rats with hippocampal lesions. Physiol Behav. 1976;17(6):915–20. doi: 10.1016/0031-9384(76)90008-1 14677582.

71. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):RESEARCH0034. doi: 10.1186/gb-2002-3-7-research0034 12184808; PubMed Central PMCID: PMC126239.

72. Dwivedi Y, Rizavi HS, Pandey GN. Antidepressants reverse corticosterone-mediated decrease in brain-derived neurotrophic factor expression: differential regulation of specific exons by antidepressants and corticosterone. Neuroscience. 2006;139(3):1017–29. doi: 10.1016/j.neuroscience.2005.12.058 16500030; PubMed Central PMCID: PMC1513636.

73. Jafari M, Seese RR, Babayan AH, Gall CM, Lauterborn JC. Glucocorticoid receptors are localized to dendritic spines and influence local actin signaling. Mol Neurobiol. 2012;46(2):304–15. doi: 10.1007/s12035-012-8288-3 22717988; PubMed Central PMCID: PMC3973133.

74. Schaaf MJ, de Jong J, de Kloet ER, Vreugdenhil E. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res. 1998;813(1):112–20. doi: 10.1016/s0006-8993(98)01010-5 9824681.

75. Smith MA, Makino S, Kvetnansky R, Post RM. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci. 1995;15(3 Pt 1):1768–77. doi: 10.1523/JNEUROSCI.15-03-01768.1995 7891134.

76. Belujon P, Grace AA. Dopamine System Dysregulation in Major Depressive Disorders. Int J Neuropsychopharmacol. 2017;20(12):1036–46. doi: 10.1093/ijnp/pyx056 29106542; PubMed Central PMCID: PMC5716179.

77. De Bundel D, Gangarossa G, Biever A, Bonnefont X, Valjent E. Cognitive dysfunction, elevated anxiety, and reduced cocaine response in circadian clock-deficient cryptochrome knockout mice. Front Behav Neurosci. 2013;7:152. doi: 10.3389/fnbeh.2013.00152 24187535; PubMed Central PMCID: PMC3807562.

78. Kempadoo KA, Mosharov EV, Choi SJ, Sulzer D, Kandel ER. Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory. Proc Natl Acad Sci U S A. 2016;113(51):14835–40. doi: 10.1073/pnas.1616515114 27930324; PubMed Central PMCID: PMC5187750.

79. Papp M, Gruca P, Lason-Tyburkiewicz M, Litwa E, Niemczyk M, Tota-Glowczyk K, et al. Dopaminergic mechanisms in memory consolidation and antidepressant reversal of a chronic mild stress-induced cognitive impairment`. Psychopharmacology (Berl). 2017;234(17):2571–85. doi: 10.1007/s00213-017-4651-4 28567697; PubMed Central PMCID: PMC5548836.

80. Yadid G, Friedman A. Dynamics of the dopaminergic system as a key component to the understanding of depression. Prog Brain Res. 2008;172:265–86. doi: 10.1016/S0079-6123(08)00913-8 18772037.

81. Farley SJ, McKay BM, Disterhoft JF, Weiss C. Reevaluating hippocampus-dependent learning in FVB/N mice. Behav Neurosci. 2011;125(6):871–8. doi: 10.1037/a0026033 22122148; PubMed Central PMCID: PMC3246014.

82. Oitzl MS, de Kloet ER, Joels M, Schmid W, Cole TJ. Spatial learning deficits in mice with a targeted glucocorticoid receptor gene disruption. Eur J Neurosci. 1997;9(11):2284–96. doi: 10.1111/j.1460-9568.1997.tb01646.x 9464923.

83. Oitzl MS, Reichardt HM, Joels M, de Kloet ER. Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc Natl Acad Sci U S A. 2001;98(22):12790–5. doi: 10.1073/pnas.231313998 11606764; PubMed Central PMCID: PMC60132.

84. Miller BH, Schultz LE, Gulati A, Su AI, Pletcher MT. Phenotypic characterization of a genetically diverse panel of mice for behavioral despair and anxiety. PLoS One. 2010;5(12):e14458. doi: 10.1371/journal.pone.0014458 21206921; PubMed Central PMCID: PMC3012073.

85. Ballegeer M, Van Looveren K, Timmermans S, Eggermont M, Vandevyver S, Thery F, et al. Glucocorticoid receptor dimers control intestinal STAT1 and TNF-induced inflammation in mice. J Clin Invest. 2018;128(8):3265–79. doi: 10.1172/JCI96636 29746256; PubMed Central PMCID: PMC6063488.

86. Siopi E, Denizet M, Gabellec MM, de Chaumont F, Olivo-Marin JC, Guilloux JP, et al. Anxiety- and Depression-Like States Lead to Pronounced Olfactory Deficits and Impaired Adult Neurogenesis in Mice. J Neurosci. 2016;36(2):518–31. doi: 10.1523/JNEUROSCI.2817-15.2016 26758842; PubMed Central PMCID: PMC6602024.

87. Surget A, Saxe M, Leman S, Ibarguen-Vargas Y, Chalon S, Griebel G, et al. Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol Psychiatry. 2008;64(4):293–301. doi: 10.1016/j.biopsych.2008.02.022 18406399.

88. Judd LL, Schettler PJ, Brown ES, Wolkowitz OM, Sternberg EM, Bender BG, et al. Adverse consequences of glucocorticoid medication: psychological, cognitive, and behavioral effects. Am J Psychiatry. 2014;171(10):1045–51. doi: 10.1176/appi.ajp.2014.13091264 25272344.

89. Belanoff JK, Gross K, Yager A, Schatzberg AF. Corticosteroids and cognition. J Psychiatr Res. 2001;35(3):127–45. doi: 10.1016/s0022-3956(01)00018-8 11461709.

90. McEwen BS, Weiss JM, Schwartz LS. Selective retention of corticosterone by limbic structures in rat brain. Nature. 1968;220(5170):911–2. doi: 10.1038/220911a0 4301849.

91. McEwen BS, Weiss JM, Schwartz LS. Uptake of corticosterone by rat brain and its concentration by certain limbic structures. Brain Res. 1969;16(1):227–41. doi: 10.1016/0006-8993(69)90096-1 5348850.

92. Conrad CD. A critical review of chronic stress effects on spatial learning and memory. Prog Neuropsychopharmacol Biol Psychiatry. 2010;34(5):742–55. doi: 10.1016/j.pnpbp.2009.11.003 19903505.

93. Ibarguen-Vargas Y, Surget A, Touma C, Palme R, Belzung C. Multifaceted strain-specific effects in a mouse model of depression and of antidepressant reversal. Psychoneuroendocrinology. 2008;33(10):1357–68. doi: 10.1016/j.psyneuen.2008.07.010 18790573.

94. Mozhui K, Karlsson RM, Kash TL, Ihne J, Norcross M, Patel S, et al. Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci. 2010;30(15):5357–67. doi: 10.1523/JNEUROSCI.5017-09.2010 20392957; PubMed Central PMCID: PMC2866495.

95. Hurtubise JL, Howland JG. Effects of stress on behavioral flexibility in rodents. Neuroscience. 2017;345:176–92. doi: 10.1016/j.neuroscience.2016.04.007 27066767.

96. Park M, Kim CH, Jo S, Kim EJ, Rhim H, Lee CJ, et al. Chronic Stress Alters Spatial Representation and Bursting Patterns of Place Cells in Behaving Mice. Sci Rep. 2015;5:16235. doi: 10.1038/srep16235 26548337; PubMed Central PMCID: PMC4637823.

97. Ogawa T, Okihara H, Kokai S, Abe Y, Karin Harumi UK, Makiguchi M, et al. Nasal obstruction during adolescence induces memory/learning impairments associated with BDNF/TrkB signaling pathway hypofunction and high corticosterone levels. J Neurosci Res. 2018;96(6):1056–65. doi: 10.1002/jnr.24216 29392750.

98. Salehi A, Rabiei Z, Setorki M. Effect of gallic acid on chronic restraint stress-induced anxiety and memory loss in male BALB/c mice. Iran J Basic Med Sci. 2018;21(12):1232–7. doi: 10.22038/ijbms.2018.31230.7523 30627366; PubMed Central PMCID: PMC6312671.

99. Allen AP, Curran EA, Duggan A, Cryan JF, Chorcorain AN, Dinan TG, et al. A systematic review of the psychobiological burden of informal caregiving for patients with dementia: Focus on cognitive and biological markers of chronic stress. Neurosci Biobehav Rev. 2017;73:123–64. doi: 10.1016/j.neubiorev.2016.12.006 27986469.

100. Campeau S, Liberzon I, Morilak D, Ressler K. Stress modulation of cognitive and affective processes. Stress. 2011;14(5):503–19. doi: 10.3109/10253890.2011.596864 21790481; PubMed Central PMCID: PMC3313908.

101. Girotti M, Adler SM, Bulin SE, Fucich EA, Paredes D, Morilak DA. Prefrontal cortex executive processes affected by stress in health and disease. Prog Neuropsychopharmacol Biol Psychiatry. 2018;85:161–79. doi: 10.1016/j.pnpbp.2017.07.004 28690203; PubMed Central PMCID: PMC5756532.

102. Coburn-Litvak PS, Pothakos K, Tata DA, McCloskey DP, Anderson BJ. Chronic administration of corticosterone impairs spatial reference memory before spatial working memory in rats. Neurobiol Learn Mem. 2003;80(1):11–23. doi: 10.1016/s1074-7427(03)00019-4 12737930.

103. Graybeal C, Feyder M, Schulman E, Saksida LM, Bussey TJ, Brigman JL, et al. Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: rescue with BDNF. Nat Neurosci. 2011;14(12):1507–9. doi: 10.1038/nn.2954 22057192; PubMed Central PMCID: PMC3389817.

104. Monteiro S, Roque S, de Sa-Calcada D, Sousa N, Correia-Neves M, Cerqueira JJ. An efficient chronic unpredictable stress protocol to induce stress-related responses in C57BL/6 mice. Front Psychiatry. 2015;6:6. doi: 10.3389/fpsyt.2015.00006 25698978; PubMed Central PMCID: PMC4313595.

105. van Boxelaere M, Clements J, Callaerts P, D'Hooge R, Callaerts-Vegh Z. Unpredictable chronic mild stress differentially impairs social and contextual discrimination learning in two inbred mouse strains. PLoS One. 2017;12(11):e0188537. doi: 10.1371/journal.pone.0188537 29166674; PubMed Central PMCID: PMC5699833.

106. Sukoff Rizzo SJ, Silverman JL. Methodological Considerations for Optimizing and Validating Behavioral Assays. Curr Protoc Mouse Biol. 2016;6(4):364–79. doi: 10.1002/cpmo.17 27906464; PubMed Central PMCID: PMC6054129.

107. Willis EF, Bartlett PF, Vukovic J. Protocol for Short- and Longer-term Spatial Learning and Memory in Mice. Front Behav Neurosci. 2017;11:197. doi: 10.3389/fnbeh.2017.00197 29089878; PubMed Central PMCID: PMC5651027.

108. McIlwain KL, Merriweather MY, Yuva-Paylor LA, Paylor R. The use of behavioral test batteries: effects of training history. Physiol Behav. 2001;73(5):705–17. doi: 10.1016/s0031-9384(01)00528-5 11566205.

109. Mehla J, Lacoursiere SG, Lapointe V, McNaughton BL, Sutherland RJ, McDonald RJ, et al. Age-dependent behavioral and biochemical characterization of single APP knock-in mouse (APP(NL-G-F/NL-G-F)) model of Alzheimer's disease. Neurobiol Aging. 2019;75:25–37. doi: 10.1016/j.neurobiolaging.2018.10.026 30508733.

110. Datson NA, Morsink MC, Meijer OC, de Kloet ER. Central corticosteroid actions: Search for gene targets. Eur J Pharmacol. 2008;583(2–3):272–89. doi: 10.1016/j.ejphar.2007.11.070 18295201.

111. Binder EB. The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology. 2009;34 Suppl 1:S186–95. doi: 10.1016/j.psyneuen.2009.05.021 19560279.

112. Miranda M, Morici JF, Zanoni MB, Bekinschtein P. Brain-Derived Neurotrophic Factor: A Key Molecule for Memory in the Healthy and the Pathological Brain. Front Cell Neurosci. 2019;13:363. doi: 10.3389/fncel.2019.00363 31440144; PubMed Central PMCID: PMC6692714.

113. Hersi AI, Kitaichi K, Srivastava LK, Gaudreau P, Quirion R. Dopamine D-5 receptor modulates hippocampal acetylcholine release. Brain Res Mol Brain Res. 2000;76(2):336–40. doi: 10.1016/s0169-328x(00)00015-2 10762709.

114. Furini CR, Myskiw JC, Schmidt BE, Marcondes LA, Izquierdo I. D1 and D5 dopamine receptors participate on the consolidation of two different memories. Behav Brain Res. 2014;271:212–7. doi: 10.1016/j.bbr.2014.06.027 24959860.

115. McNamara CG, Dupret D. Two sources of dopamine for the hippocampus. Trends Neurosci. 2017;40(7):383–4. doi: 10.1016/j.tins.2017.05.005 28511793; PubMed Central PMCID: PMC5489110.


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