The role of phosphorylated glucocorticoid receptor in mitochondrial functions and apoptotic signalling in brain tissue of stressed Wistar rats

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 11, 2009, Pages 2181-2188

  Adzic, Miroslav ^a   Djordjevic, Ana ^a   Demonacos, Constantinos ^b   Krstic Demonacos, Marija ^b   Radojcic, Marija B ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Glucocorticoid receptor; Hippocampus; Mitochondria; Phosphorylation; Prefrontal cortex

Indexed keywords

CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE SUBUNIT 1; CYTOCHROME C OXIDASE SUBUNIT 3; GLUCOCORTICOID RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; SERINE; UNCLASSIFIED DRUG;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN TISSUE; CHRONIC STRESS; CONTROLLED STUDY; HIPPOCAMPUS; HISTOPATHOLOGY; IMMOBILIZATION STRESS; MALE; MITOCHONDRIAL RESPIRATION; NEUROENDOCRINE SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SOCIAL ISOLATION; STRESS; WISTAR RAT;

ANIMALS; APOPTOSIS; BRAIN; CORTICOSTERONE; CYCLOOXYGENASE 1; DNA FRAGMENTATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HIPPOCAMPUS; INTRACELLULAR SPACE; MALE; MEMBRANE PROTEINS; MITOCHONDRIA; PHOSPHORYLATION; PHOSPHOSERINE; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

RATTUS; RATTUS NORVEGICUS;

EID: 70349381646     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.04.001     Document Type: Article

References (43)

1. Alesci S., Manoli I., Michopoulos V.J., Brouwers F.M., Le H., Gold P.W., et al. Development of a human mitochondria-focused cDNA microarray (hMitChip) and validation in skeletal muscle cells: implications for pharmaco- and mitogenomics. Pharmacogenomics J 6 (2006) 333-342
2. Armario A., Lopez-Calderon A., Jolin T., and Balasch J. Response of anterior pituitary hormones to chronic stress. The specificity of adaptation. Neurosci Biobehav Rev 10 (1986) 245-250
3. Bagchi D., Carryl O., Tran M., Krohn R., Bagchi D., Garg A., et al. Stress, diet and alcohol-induced oxidative gastrointestinal mucosal injury in rats and protection by bismuth subsalicylate. J Appl Toxicol 18 (1999) 3-13
4. Cao G., Minami M., Pei W., Yan C., Chen D., O'Horo C., et al. Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J Cereb Blood Flow Metab 21 (2001) 321-333
5. Chen W., Dang T., Blind R.D., Wang Z., Cavasotto C.N., Hittelman A.B., et al. Glucocorticoid receptor phosphorylation differentially affects target gene expression. Mol Endo 22 (2008) 1754-1766
6. Davies L., Karthikeyan N., Lynch J.T., Sial E.A., Gkourtsa A., Demonacos C., et al. Cross talk of signaling pathways in the regulation of the glucocorticoid receptor function. Mol Endo 22 (2008) 1331-1344
7. De Kloet E.R., and Reul J.M.H.M. Feedback action and tonic influence of corticosteroids on brain function: a concept arising from the heterogeneity of brain receptor systems. Psychoneuroendocrinology 12 (1987) 83-105
8. Demonacos C., Djordjevic-Markovic R., Tsawdaroglou N., and Sekeris C.E. The mitochondrion as a primary site of action of glucocorticoids: the interaction of the glucocorticoid receptor with mitochondrial DNA sequences showing partial similarity to the nuclear glucocorticoid responsive elements. J Steroid Biochem Mol Biol 55 (1995) 43-55
9. Demonacos C.V., Karayanni N., Hatzoglou E., Tsiriyiotis C., Spandidos D.A., and Sekeris C.E. Mitochondrial genes as sites of primary action of steroid hormones. Steroids 61 (1996) 226-232
10. Diorio D., Viau V., and Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13 (1993) 3839-3847
11. Figiel M., and Engele J. Pituary adenilate cyclise-activating polypeptide (PACAP), a neuron-derived peptide regulating glial glutamate transport and metabolism. J Neurosci 20 (2000) 3596-3605
12. Filipkowski R.K., Hetman M., Kaminska B., and Kaczmarek L. DNA fragmentation in rat brain after intraperitoneal administration of kainite. Neuroreport 5 (1994) 1538-1540
13. Gajkowska B., Motyl T., Olszewska-Badarczuk H., and Godlewski M.M. Expression of BAX in cell nucleus after experimentally induced apoptosis revealed by immunogold and embedment-free electron microscopy. Cell Biol Int 25 (2001) 725-733
14. Gao J., Chi Z.F., Liu X.W., Shan P.Y., and Wang R. Mitochondrial dysfunction and ultrastructure damage in the hippocampus of pilocarpine-induced epileptic rat. Neurosci Lett 411 (2007) 152-157
15. Hauger R.L., Lorang M., Irwin M., and Aguilera G. CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Res 532 (1990) 34-40
16. Ismaili N., and Garabedian M.J. Modulation of glucocorticoid receptor function via phosphorylation. Ann NY Acad Sci 1024 (2004) 86-101
17. Kerr J.F., Gobe G.C., Winterford C.M., and Harmon B.V. Anatomical methods in cell death. Methods Cell Biol 46 (1995) 1-27
18. Kino T., Ichijo T., Amin N.D., 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 Endo 21 (2007) 1552-1568
19. Koufali M.M., Moutsatsou P., Sekeris C.E., and Breen K.C. The dynamic localization of the glucocorticoid receptor in rat C6 glioma cell mitochondria. Mol Cell Endo 209 (2003) 51-60
20. Krstic M.D., Rogatsky I., Yamamoto K.R., and Garabedian M.J. Mitogen-activated and cyclin-dependent protein kinases selectively and differentially modulate transcriptional enhancement by the glucocorticoid receptor. Mol Cell Biol 17 (1997) 3947-3954
21. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
22. Li Y., Chopp M., Jiang N., Yao F., and Zaloga C. Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 15 (1995) 389-397
23. Li Y., Chopp M., Jiang N., Zhang Z.G., and Zaloga C. Induction of DNA fragmentation after 10 to 120 min of focal cerebral ischemia in rats. Stroke 26 (1995) 1252-1258
24. Liang H.L., Ongwijitwat S., and Wong-Riley M.T.T. Bigenomic functional regulation of all 13 cytochrome c oxidase subunit transcripts in rat neurons in vitro and in vivo. Neuroscience 140 (2006) 177-190
25. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T))method. Methods 25 (2001) 402-408
26. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951) 265-267
27. Magarinos A.M., Somoza G., and De Nicola A.F. Glucocorticoid negative feedback and glucocorticoid receptors after hippocampectomy in rats. Horm Metab Res 19 (1987) 105-109
28. Malkesman O., Maayan R., Weizman A., and Weller A. Aggressive behavior and HPA axis hormones after social isolation in adult rats of two different genetic animal models for depression. Behav Brain Res 175 (2006) 408-414
29. Manoli I., Alesci S., Blackman M.R., Yan Su A., Owen M.R., and Chrousos G.P. Mitochondria as key components of the stress response. Trends Endocrinol Metab 18 (2007) 190-198
30. Merino J.J., Cordero M.I., and Sandi C. Regulation of hippocampal cell adhesion molecules NCAM and L1 by contextual fear conditioning is dependent upon time and stressor intensity. Eur J Neurosci 12 (2000) 3283-3290
31. Moutsatsou P., Psarra A.M.G., Tsiapara A., Paraskevakou H., Davaris P., and Sekeris C.E. Localization of the glucocorticoid receptor in rat brain mitochondria. Arch Biochem Biophys 386 (2001) 69-78
32. Pitman D.L., Ottenweller J.E., and Natelson B.H. Plasma corticosterone levels during repeated presentation of two intensities of restraint stress: chronic stress and habituation. Physiol Behav 43 (1988) 47-55
33. Psarra A.M.G., and Sekeris C.E. Nuclear receptors and other nuclear transcriptiona factors in mitochondria: regulatory molecules in a new environment. Biochem Biophys Acta 1783 (2008) 1-11
34. Rogatsky I., Waase C.L., and Garabedian M.J. Phosphorylation and inhibition of rat glucocorticoid receptor transcriptional activation by glycogen synthase kinase-3 (GSK-3): species-specific differences between human and rat glucocorticoid receptor signaling as revealed through GSK-3 phosphorylation. J Biol Chem 273 (1998) 14315-14321
35. Rutledge R.G., and Cote C. Mathematics of quantitative kinetic PCR and the application of standard curves. Nucl Acids Res 31 (2003) e93
36. Sanchez E.R., Hirst M., Scherrer L.C., Tang H.Y., Welsh M.J., Harmon J.M., et al. Hormone-free mouse glucocorticoid receptors overexpressed in Chinese hamster ovary cells are localized to the nucleus and are associated with both hsp70 and hsp90. J Biol Chem 265 (1990) 20123-20130
37. Sanchez M.M., Aguado F., Sanchez-Toscano F., and Saphier D. Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139 (1998) 579-587
38. Sionov R.V., Cohen O., Kfi S., Zilberman Y., and Yefenof E. Role of mitochondrial glucocorticoid receptor in glucocorticoid-induced apoptosis. J Exp Med 203 (2006) 189-201
39. Spencer R.L., Kalman B.A., Cotter C.S., and Deak T. Discrimination between changes in glucocorticoid receptor expression and activation in rat brain using western blot analysis. Brain Res 868 (2000) 275-286
40. Trzeciak A.R., Nyaga S.G., Jaruga P., Lohani A., Dizdaroglu M., and Evans M.K. Cellular repair of oxidatively induced DNA base lesions is defective in prostate cancer cell lines, PC-3 and DU-145. Carcinogenesis 25 (2004) 1359-1370
41. Tsiriyotis C., Spandidos D.A., and Sekeris C.E. The mitochondrion as a primary site of action of glucocorticoids: mitochondrial nucleotide sequences, showing similarity to hormone response elements, confer dexamethasone inducibility to chimaeric genes transfected in LATK-cells. Biochem Biophys Res Commun 235 (1997) 349-354
42. Weigel N.L., and Moore N.L. Steroid receptor phosphorylation: a key modulator of multiple receptor functions. Mol Endo 21 (2007) 2311-2319
43. Wren A.M., Small C.J., Abbott C.R., Jethwa P.H., Kennedy A.R., Murphy K.G., et al. Hypothalamic actions of neuromedin U. Endocrinology 143 (2002) 4227-4234