Acute and chronic stress differentially regulate Cyclin-Dependent Kinase 5 in mouse brain: Implications to glucocorticoid actions and major depression

Translational Psychiatry

Volumn 5, Issue 6, 2015, Pages

  Papadopoulou, A ^a,e   Siamatras, T ^a,e   Delgado Morales, R ^b,e   Amin, N D ^c   Shukla, V ^c   Zheng, Y L ^c   Pant, H C ^c   Almeida, O F X ^b   Kino, T ^a,d  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^d SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

^e BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; ARGIPRESSIN; BIOLOGICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; CYCLIN DEPENDENT KINASE 5; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; INHIBITOR OF DIFFERENTIATION 3; MESSENGER RNA; NISCHARIN; NUCLEAR SPECKLE SPLICING REGULATORY PROTEIN 1; PEPTIDES AND PROTEINS; PROTEIN C FOS; PROTEIN PHOSPHATASE 1 REGULATORY SUBUNIT 10; SEROTONIN 1A RECEPTOR; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG; CDK5 PROTEIN, HUMAN; CDK5 PROTEIN, MOUSE;

ACUTE STRESS; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BRAIN; BRAIN REGION; BRODMANN AREA 25; BRODMANN AREA 44; BRODMANN AREA 45; BRODMANN AREA 47; CHRONIC UNPREDICTABLE STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMOBILIZATION STRESS; INFERIOR FRONTAL GYRUS; MAJOR DEPRESSION; MALE; MENTAL PATIENT; MOLECULAR PATHOLOGY; MOUSE; NEUROPATHOLOGY; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; CASE CONTROL STUDY; EXERCISE; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; METABOLISM; MIDDLE AGED; PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AGED; ANIMALS; CASE-CONTROL STUDIES; CYCLIN-DEPENDENT KINASE 5; DEPRESSIVE DISORDER, MAJOR; FEMALE; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HIPPOCAMPUS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MICE; MIDDLE AGED; PHOSPHORYLATION; PITUITARY-ADRENAL SYSTEM; PREFRONTAL CORTEX; RECEPTORS, GLUCOCORTICOID; RESTRAINT, PHYSICAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STRESS, PSYCHOLOGICAL;

EID: 84987842214     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.72     Document Type: Article

References (70)

1. Pego JM, Sousa JC, Almeida OF, Sousa N. Stress and the neuroendocrinology of anxiety disorders. Curr Top Behav Neurosci 2010; 2: 97-117.
2. Chrousos GP Stress and disorders of the stress system. Nat Rev Endocrinol 2009; 5: 374-381.
3. Nader N, Chrousos GP, Kino T. Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications. FASEB J 2009; 23: 1572-1583.
4. Chrousos GP The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med 1995; 332: 1351-1362.
5. Chrousos GP, Kino T. Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress 2007; 10: 213-219.
6. Kino T, De Martino MU, Charmandari E, Mirani M, Chrousos GP. Tissue glucocorticoid resistance/hypersensitivity syndromes. J Steroid Biochem Mol Biol 2003; 85: 457-467.
7. Kino T. Tissue glucocorticoid sensitivity: beyond stochastic regulation on the diverse actions of glucocorticoids. Horm Metab Res 2007; 39: 420-424.
8. Burris TP The nuclear receptor superfamily. In: Burris, TP, McCabe, ERB (eds). Nuclear Receptors and Genetic Disease. Academic Press: London, UK, 2001, pp 1-58.
9. Chrousos GP, Kino T. Intracellular glucocorticoid signaling: a formerly simple system turns stochastic. Sci STKE 2005; 2005: pe48.
10. Su SC, Tsai LH. Cyclin-dependent kinases in brain development and disease. Annu Rev Cell Dev Biol 2011; 27: 465-491.
11. Kesavapany S, Li BS, Amin N, Zheng YL, Grant P, Pant HC. Neuronal cyclin-dependent kinase 5: role in nervous system function and its specific inhibition by the Cdk5 inhibitory peptide. Biochim Biophys Acta 2004; 1697: 143-153.
12. Dhavan R, Tsai LH. A decade of CDK5. Nat Rev Mol Cell Biol 2001; 2: 749-759.
13. Cheung ZH, Ip NY. Cdk5: a multifaceted kinase in neurodegenerative diseases. Trends Cell Biol 2012; 22: 169-175.
14. Lai KO, Ip NY. Recent advances in understanding the roles of Cdk5 in synaptic plasticity. Biochim Biophys Acta 2009; 1792: 741-745.
15. Ledda F, Paratcha G, Ibanez CF. Target-derived GFRa1 as an attractive guidance signal for developing sensory and sympathetic axons via activation of Cdk5. Neuron 2002; 36: 387-401.
16. Paglini G, Peris L, Diez-Guerra J, Quiroga S, Caceres A. The Cdk5-p35 kinase associates with the Golgi apparatus and regulates membrane traffic. EMBO Rep 2001; 2: 1139-1144.
17. Smith DS, Tsai LH. Cdk5 behind the wheel: a role in trafficking and transport? Trends Cell Biol 2002; 12: 28-36.
18. Kwon YT, Gupta A, Zhou Y, Nikolic M, Tsai LH. Regulation of N-cadherin-mediated adhesion by the p35-Cdk5 kinase. Curr Biol 2000; 10: 363-372.
19. Mandelkow EM, Mandelkow E. Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb Perspect Med 2012; 2: a006247.
20. Zhong P, Liu X, Zhang Z, Hu Y, Liu SJ, Lezama-Ruiz M et al. Cyclin-dependent kinase 5 in the ventral tegmental area regulates depression-related behaviors. J Neurosci 2014; 34: 6352-6366.
21. Yu S, Holsboer F, Almeida OF. Neuronal actions of glucocorticoids: focus on depression. J Steroid Biochem Mol Biol 2008; 108: 300-309.
22. Anacker C, Zunszain PA, Cattaneo A, Carvalho LA, Garabedian MJ, Thuret S et al. Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol Psychiatry 2011; 16: 738-750.
23. Sotiropoulos I, Catania C, Riedemann T, Fry JP, Breen KC, Michaelidis TM et al. Glucocorticoids trigger Alzheimer disease-like pathobiochemistry in rat neuronal cells expressing human tau. J Neurochem 2008; 107: 385-397.
24. Kino T, Ichijo T, Amin ND, Kesavapany S, Wang Y, Kim N et al. Cyclin-dependent kinase 5 differentially regulates the transcriptional activity of the glucocorticoid receptor through phosphorylation: clinical implications for the nervous system response to glucocorticoids and stress. Mol Endocrinol 2007; 21: 1552-1568.
25. Patchev AV, Fischer D, Wolf SS, Herkenham M, Gotz F, Gehin M et al. Insidious adrenocortical insufficiency underlies neuroendocrine dysregulation in TIF-2 deficient mice. FASEB J 2007; 21: 231-238.
26. Willner P. Chronic mild stress (CMS) revisited: consistency and behaviouralneurobiological concordance in the effects of CMS. Neuropsychobiology 2005; 52: 90-110.
27. Bessa JM, Ferreira D, Melo I, Marques F, Cerqueira JJ, Palha JA et al. The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol Psychiatry 2009; 14: 764-773, 739.
28. Zheng YL, Kesavapany S, Gravell M, Hamilton RS, Schubert M, Amin N et al. A Cdk5 inhibitory peptide reduces tau hyperphosphorylation and apoptosis in neurons. EMBO J 2005; 24: 209-220.
29. Kino T, Tiulpakov A, Ichijo T, Chheng L, Kozasa T, Chrousos GP. G protein β interacts with the glucocorticoid receptor and suppresses its transcriptional activity in the nucleus. J Cell Biol 2005; 169: 885-896.
30. Ng SS, Chang TH, Tailor P, Ozato K, Kino T. Virus-induced differential expression of nuclear receptors and coregulators in dendritic cells: implication to interferon production. FEBS Lett 2011; 585: 1331-1337.
31. Fuchsl AM, Langgartner D, Reber SO. Mechanisms underlying the increased plasma ACTH levels in chronic psychosocially stressed male mice. PLoS One 2013; 8: e84161.
32. Ortiz JB, Mathewson CM, Hoffman AN, Hanavan PD, Terwilliger EF, Conrad CD. Hippocampal brain-derived neurotrophic factor mediates recovery from chronic stress-induced spatial reference memory deficits. Eur J Neurosci 2014; 40: 3351-3362.
33. Kino T, Jaffe H, Amin ND, Chakrabarti M, Zheng YL, Chrousos GP et al. Cyclin-dependent kinase 5 modulates the transcriptional activity of the miner-alocorticoid receptor and regulates expression of brain-derived neurotrophic factor. Mol Endocrinol 2010; 24: 941-952.
34. Sharma D, Bhave S, Gregg E, Uht R. Dexamethasone induces a putative repressor complex and chromatin modifications in the CRH promoter. Mol Endocrinol 2013; 27: 1142-1152.
35. Mifsud KR, Gutierrez-Mecinas M, Trollope AF, Collins A, Saunderson EA, Reul JM. Epigenetic mechanisms in stress and adaptation. Brain Behav Immun 2011; 25: 1305-1315.
36. Garcia-Perez D, Laorden ML, Milanes MV, Nunez C. Glucocorticoids regulation of FosB/AFosB expression induced by chronic opiate exposure in the brain stress system. PLoS One 2012; 7: e50264.
37. Boyarskikh UA, Bondar NP, Filipenko ML, Kudryavtseva NN. Downregulation of serotonergic gene expression in the Raphe nuclei of the midbrain under chronic social defeat stress in male mice. Mol Neurobiol 2013; 48: 13-21.
38. Konishi H, Ogawa T, Nakagomi S, Inoue K, Tohyama M, Kiyama H. Id1, Id2 and Id3 are induced in rat melanotrophs of the pituitary gland by dopamine suppression under continuous stress. Neuroscience 2010; 169: 1527-1534.
39. Head GA, Mayorov DN. Imidazoline receptors, novel agents and therapeutic potential. Cardiovasc Hematol Agents Med Chem 2006; 4: 17-32.
40. Olah J, Vincze O, Virok D, Simon D, Bozso Z, Tokesi N et al. Interactions of pathological hallmark proteins: tubulin polymerization promoting protein/p25, β-amyloid, and α-synuclein. J Biol Chem 2011; 286: 34088-34100.
41. Charmandari E, Chrousos GP, Lambrou GI, Pavlaki A, Koide H, Ng SS et al. Peripheral CLOCK regulates target-tissue glucocorticoid receptor transcriptional activity in a circadian fashion in man. PLoS One 2011; 6: e25612.
42. Anacker C, Cattaneo A, Musaelyan K, Zunszain PA, Horowitz M, Molteni R et al. Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proc Natl Acad Sci USA 2013; 110: 8708-8713.
43. McEwen BS, Morrison JH. The brain on stress: vulnerability and plasticity of the prefrontal cortex over the life course. Neuron 2013; 79: 16-29.
44. Preston AR, Eichenbaum H. Interplay of hippocampus and prefrontal cortex in memory. Curr Biol 2013; 23: R764-R773.
45. Orti E, Bodwell JE, Munck A. Phosphorylation of steroid hormone receptors. Endocr Rev 1992; 13: 105-128.
46. Bennett MR, Lagopoulos J. Stress and trauma: BDNF control of dendritic-spine formation and regression. Prog Neurobiol 2014; 112: 80-99.
47. Gold PW, Goodwin FK, Chrousos GP. Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (1). N Engl J Med 1988; 319: 348-353.
48. Gold PW, Goodwin FK, Chrousos GP. Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (2). N Engl J Med 1988; 319: 413-420.
49. Hamani C, Mayberg H, Stone S, Laxton A, Haber S, Lozano AM. The subcallosal cingulate gyrus in the context of major depression. Biol Psychiatry 2011; 69: 301-308.
50. Hamon M, Blier P. Monoamine neurocircuitry in depression and strategies for new treatments. Prog Neuropsychopharmacol Biol Psychiatry 2013; 45: 54-63.
51. Pierrot-Deseilligny C. From the abducens nucleus to spatial memory: an ocular motor journey. Rev Neurol (Paris) 2005; 161: 549-565.
52. Price JL, Drevets WC. Neural circuits underlying the pathophysiology of mood disorders. Trends Cogn Sci 2012; 16: 61-71.
53. Morimoto RI Stress, aging, and neurodegenerative disease. N Engl J Med 2006; 355: 2254-2255.
54. Liu Y, Yang N, Zuo P. cDNA microarray analysis of gene expression in the cerebral cortex and hippocampus of BALB/c mice subjected to chronic mild stress. Cell Mol Neurobiol 2010; 30: 1035-1047.
55. Lee JH, Ko E, Kim YE, Min JY, Liu J, Kim Y et al. Gene expression profile analysis of genes in rat hippocampus from antidepressant treated rats using DNA microarray. BMC Neurosci 2010; 11: 152.
56. Cuadrado-Tejedor M, Ricobaraza A, Del Rio J, Frechilla D, Franco R, Perez-Mediavilla A et al. Chronic mild stress in mice promotes cognitive impairment and CDK5-dependent tau hyperphosphorylation. Behav Brain Res 2011; 220: 338-343.
57. Nihonmatsu-Kikuchi N, Hayashi Y, Yu XJ, Tatebayashi Y. Depression and Alzheimer's disease: novel postmortem brain studies reveal a possible common mechanism. J Alzheimers Dis 2013; 37: 611-621.
58. Lagace DC, Benavides DR, Kansy JW, Mapelli M, Greengard P, Bibb JA et al. Cdk5 is essential for adult hippocampal neurogenesis. Proc Natl Acad Sci USA 2008; 105: 18567-18571.
59. Fernandez-Guasti A, Fiedler JL, Herrera L, Handa RJ. Sex, stress, and mood disorders: at the intersection of adrenal and gonadal hormones. Horm Metab Res 2012; 44: 607-618.
60. Dalla C, Pitychoutis PM, Kokras N, Papadopoulou-Daifoti Z. Sex differences in response to stress and expression of depressive-like behaviours in the rat. Curr Top Behav Neurosci 2011; 8: 97-118.
61. Bangasser DA, Valentino RJ. Sex differences in stress-related psychiatric disorders: neurobiological perspectives. Front Neuroendocrinol 2014; 35: 303-319.
62. Mitic M, Simic I, Djordjevic J, Radojcic MB, Adzic M. Gender-specific effects of fluoxetine on hippocampal glucocorticoid receptor phosphorylation and behavior in chronically stressed rats. Neuropharmacology 2013; 70: 100-111.
63. Coffey ET Nuclear and cytosolic JNK signalling in neurons. Nat Rev Neurosci 2014; 15: 285-299.
64. Mehan S, Meena H, Sharma D, Sankhla R. JNK: a stress-activated protein kinase therapeutic strategies and involvement in Alzheimer's and various neurodegenerative abnormalities. J Mol Neurosci 2011; 43: 376-390.
65. Sodero AO, Trovo L, Iannilli F, Van Veldhoven P, Dotti CG, Martin MG. Regulation of tyrosine kinase B activity by the cyp46/cholesterol loss pathway in mature hippocampal neurons: relevance for neuronal survival under stress and in aging. J Neurochem 2011; 116: 747-755.
66. Kerman IA, Bernard R, Bunney WE, Jones EG, Schatzberg AF, Myers RM et al. Evidence for transcriptional factor dysregulation in the dorsal raphe nucleus of patients with major depressive disorder. Front Neurosci 2012; 6: 135.
67. DeFranco DB, Qi M, Borror KC, Garabedian MJ, Brautigan DL. Protein phosphatase types 1 and/or 2A regulate nucleocytoplasmic shuttling of glucocorticoid receptors. Mol Endocrinol 1991; 5: 1215-1228.
68. Andrus BM, Blizinsky K, Vedell PT, Dennis K, Shukla PK, Schaffer DJ et al. Gene expression patterns in the hippocampus and amygdala of endogenous depression and chronic stress models. Mol Psychiatry 2012; 17: 49-61.
69. Kang HJ, Adams DH, Simen A, Simen BB, Rajkowska G, Stockmeier CA et al. Gene expression profiling in postmortem prefrontal cortex of major depressive disorder. J Neurosci 2007; 27: 13329-13340.
70. Mehta D, Menke A, Binder EB. Gene expression studies in major depression. Curr Psychiatry Rep 2010; 12: 135-144.