Forebrain CRHR1 deficiency attenuates chronic stress-induced cognitive deficits and dendritic remodeling

Neurobiology of Disease

Volumn 42, Issue 3, 2011, Pages 300-310

  Wang, Xiao Dong ^a   Chen, Yuncai ^b   Wolf, Miriam ^a   Wagner, Klaus V ^a   Liebl, Claudia ^a   Scharf, Sebastian H ^a   Harbich, Daniela ^a   Mayer, Bianca ^b   Wurst, Wolfgang ^c,d   Holsboer, Florian ^a   Deussing, Jan M ^a   Baram, Tallie Z ^b   Müller, Marianne B ^a   Schmidt, Mathias V ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Chronic stress; Cognition; CRHR1; Dendrite; Hippocampus; Nectin 3

Indexed keywords

CELL ADHESION MOLECULE; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; GLUCOCORTICOID RECEPTOR; NECTIN 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CHRONIC STRESS; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITE; FOREBRAIN; HIPPOCAMPAL CA3 REGION; MALE; MEMORY DISORDER; MENTAL DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; SOCIAL STRESS; SPATIAL MEMORY; SYNAPTOGENESIS; WEIGHT GAIN; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; BODY WEIGHT; CELL ADHESION MOLECULES; DENDRITES; DOMINANCE-SUBORDINATION; IN SITU HYBRIDIZATION; MALE; MAZE LEARNING; MEMORY; MICE; MICE, TRANSGENIC; NEURONS; PROSENCEPHALON; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; STRESS, PSYCHOLOGICAL;

EID: 79954630809     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.01.020     Document Type: Article

References (75)

1. Arzt E., Holsboer F. CRF signaling: molecular specificity for drug targeting in the CNS. Trends Pharmacol. Sci. 2006, 27:531-538.
2. Bartolomucci A., et al. Metabolic consequences and vulnerability to diet-induced obesity in male mice under chronic social stress. PLoS ONE 2009, 4:e4331.
3. Bell S.M., et al. Effects of third intracerebroventricular injections of corticotropin-releasing factor (CRF) on ethanol drinking and food intake. Psychopharmacol. Berl. 1998, 139:128-135.
4. Berger S., et al. Loss of the limbic mineralocorticoid receptor impairs behavioral plasticity. Proc. Natl Acad. Sci. USA 2006, 103:195-200.
5. Bisaz R, et al. Causal evidence for the involvement of the neural cell adhesion molecule, NCAM, in chronic stress-induced cognitive impairments. Hippocampus 2011, 21:56-71.
6. Blank T., et al. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J. Neurosci. 2002, 22:3788-3794.
7. Broadbent N.J., et al. Object recognition memory and the rodent hippocampus. Learn. Mem. 2010, 17:5-11.
8. Burgin A.B., et al. Design of phosphodiesterase 4D (PDE4D) allosteric modulators for enhancing cognition with improved safety. Nat. Biotechnol. 2010, 28:63-70.
9. Challis B.G., et al. Genetic variation in the corticotrophin-releasing factor receptors: identification of single-nucleotide polymorphisms and association studies with obesity in UK Caucasians. Int. J. Obes. Relat. Metab. Disord. 2004, 28:442-446.
10. Chen Y., et al. Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J. Neurosci. 2001, 21:7171-7181.
11. Chen Y., et al. Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc. Natl Acad. Sci. USA 2004, 101:15782-15787.
12. Chen Y., et al. Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress. Neuroscience 2004, 126:533-540.
13. Chen Y., et al. Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent. Mol. Psychiatry 2006, 11:992-1002.
14. Chen Y., et al. Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J. Neurosci. 2008, 28:2903-2911.
15. Chen Y., et al. Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling. Proc. Natl Acad. Sci. USA 2010, 107:13123-13128.
16. Coburn-Litvak P.S., et al. Chronic administration of corticosterone impairs spatial reference memory before spatial working memory in rats. Neurobiol. Learn. Mem. 2003, 80:11-23.
17. Conrad C.D. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus?. Behav. Cogn. Neurosci. Rev. 2006, 5:41-60.
18. Conrad C.D. Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis. Rev. Neurosci. 2008, 19:395-411.
19. Conrad C.D., et al. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 1996, 110:1321-1334.
20. Conrad C.D., et al. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 1999, 113:902-913.
21. Conrad C.D., et al. Chronic glucocorticoids increase hippocampal vulnerability to neurotoxicity under conditions that produce CA3 dendritic retraction but fail to impair spatial recognition memory. J. Neurosci. 2007, 27:8278-8285.
22. Contarino A., et al. Reduced anxiety-like and cognitive performance in mice lacking the corticotropin-releasing factor receptor 1. Brain Res. 1999, 835:1-9.
23. Dalva M.B., et al. Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci. 2007, 8:206-220.
24. de Kloet E.R., et al. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci. 1999, 22:422-426.
25. de Kloet E.R., et al. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
26. Dere E., et al. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci. Biobehav. Rev. 2007, 31:673-704.
27. Gibb R., Kolb B. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J. Neurosci. Methods. 1998, 79:1-4.
28. Grill H.J., et al. Long-term effects on feeding and body weight after stimulation of forebrain or hindbrain CRH receptors with urocortin. Brain Res. 2000, 867:19-28.
29. Haile C.N., et al. Chronic unpredictable stress, but not chronic predictable stress, enhances the sensitivity to the behavioral effects of cocaine in rats. Psychopharmacol. Berl. 2001, 154:213-220.
30. Hains A.B., et al. Inhibition of protein kinase C signaling protects prefrontal cortex dendritic spines and cognition from the effects of chronic stress. Proc. Natl Acad. Sci. USA 2009, 106:17957-17962.
31. Heinrichs S.C., Koob G.F. Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J. Pharmacol. Exp. Ther. 2004, 311:427-440.
32. Heinrichs S.C., et al. Learning impairment in transgenic mice with central overexpression of corticotropin-releasing factor. Neuroscience 1996, 74:303-311.
33. Herman J.P., et al. Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Mol. Endocrinol. 1989, 3:1886-1894.
34. Hogan J.B., et al. Effects of CRF1 receptor antagonists and benzodiazepines in the Morris water maze and delayed non-matching to position tests. Psychopharmacol. Berl. 2005, 178:410-419.
35. Honda T., et al. Involvement of nectins in the formation of puncta adherentia junctions and the mossy fiber trajectory in the mouse hippocampus. Mol. Cell. Neurosci. 2006, 31:315-325.
36. Joëls M., Baram T.Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 2009, 10:459-466.
37. Joëls M., et al. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004, 7:221-231.
38. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 2002, 3:453-462.
39. Kitraki E., et al. Long-lasting effects of stress on glucocorticoid receptor gene expression in the rat brain. Neuroendocrinology 1999, 69:331-338.
40. Kole M.H., et al. Bidirectional shift in the cornu ammonis 3 pyramidal dendritic organization following brief stress. Neuroscience 2004, 125:337-347.
41. Krishnan V., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404.
42. Lai M., et al. Forebrain mineralocorticoid receptor overexpression enhances memory, reduces anxiety and attenuates neuronal loss in cerebral ischaemia. Eur. J. Neurosci. 2007, 25:1832-1842.
43. Lee E.H., et al. Hippocampal CRF, NE, and NMDA system interactions in memory processing in the rat. Synapse 1993, 14:144-153.
44. Lupien S.J., et al. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 2009, 10:434-445.
45. Magariños A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 1995, 69:83-88.
46. Majima T., et al. Involvement of afadin in the formation and remodeling of synapses in the hippocampus. Biochem. Biophys. Res. Commun. 2009, 385:539-544.
47. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 1999, 22:105-122.
48. McLaughlin K.J., et al. Chronic stress enhances spatial memory in ovariectomized female rats despite CA3 dendritic retraction: possible involvement of CA1 neurons. Neuroscience 2005, 135:1045-1054.
49. McLaughlin K.J., et al. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res. 2007, 1161:56-64.
50. Mizoguchi A., et al. Nectin: an adhesion molecule involved in formation of synapses. J. Cell Biol. 2002, 156:555-565.
51. Moles A., et al. Psychosocial stress affects energy balance in mice: modulation by social status. Psychoneuroendocrinology 2006, 31:623-633.
52. Müller M.B., et al. Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nat. Neurosci. 2003, 6:1100-1107.
53. Nishi M., et al. Direct visualization of glucocorticoid receptor positive cells in the hippocampal regions using green fluorescent protein transgenic mice. Neuroscience 2007, 146:1555-1560.
54. Pavlides C., et al. Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 2002, 12:245-257.
55. Paxinos G., Watson C. The Mouse Brain in Stereotaxic Coordinates Second Edition 2001, Academic Press, San Diego.
56. Radulovic J., et al. Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J. Neurosci. 1999, 19:5016-5025.
57. Refojo D., et al. Corticotropin-releasing hormone activates ERK1/2 MAPK in specific brain areas. Proc. Natl Acad. Sci. USA 2005, 102:6183-6188.
58. Rice C.J., et al. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 2008, 149:4892-4900.
59. Roozendaal B., et al. Memory retrieval impairment induced by hippocampal CA3 lesions is blocked by adrenocortical suppression. Nat. Neurosci. 2001, 4:1169-1171.
60. Row B.W., Dohanich G.P. Post-training administration of corticotropin-releasing hormone (CRH) enhances retention of a spatial memory through a noradrenergic mechanism in male rats. Neurobiol. Learn. Mem. 2008, 89:370-378.
61. Sandi C. Stress, cognitive impairment and cell adhesion molecules. Nat. Rev. Neurosci. 2004, 5:917-930.
62. Schmidt M.V., et al. Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 2007, 32:417-429.
63. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 1953, 87:387-406.
64. Squire L.R., et al. Recognition memory and the medial temporal lobe: a new perspective. Nat. Rev. Neurosci. 2007, 8:872-883.
65. Sterlemann V., et al. Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 2010, 20:540-549.
66. Tsankova N.M., et al. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 2006, 9:519-525.
67. Usuku T., et al. Visualization of glucocorticoid receptor in the brain of green fluorescent protein-glucocorticoid receptor knockin mice. Neuroscience 2005, 135:1119-1128.
68. Van Pett K., et al. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 2000, 428:191-212.
69. van Steensel B., et al. Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. J. Cell Sci. 1996, 109(Pt 4):787-792.
70. Watanabe Y., et al. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 1992, 588:341-345.
71. Wei Q., et al. Overexpressing the glucocorticoid receptor in forebrain causes an aging-like neuroendocrine phenotype and mild cognitive dysfunction. J. Neurosci. 2007, 27:8836-8844.
72. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52:90-110.
73. Woolley C.S., et al. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 1990, 531:225-231.
74. Wright R.L., Conrad C.D. Chronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 2005, 8:151-154.
75. Wright R.L., et al. Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur. J. Neurosci. 2006, 24:595-605.