Brain-derived neurotrophic factor signaling rewrites the glucocorticoid transcriptome via glucocorticoid receptor phosphorylation

Molecular and Cellular Biology

Volumn 33, Issue 18, 2013, Pages 3700-3714

  Lambert, W Marcus ^a   Xu, Chong Feng ^a,c   Neubert, Thomas A ^a   Chao, Moses V ^a   Garabedian, Michael J ^a   Jeanneteauc, Freddy D ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^c BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; SERINE; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; MALE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; BIOLOGICAL EVOLUTION; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CONSERVED SEQUENCE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DEXAMETHASONE; GLUCOCORTICOIDS; HEK293 CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; NEURONS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; RATS; RECEPTOR, TRKB; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84883540984     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00150-13     Document Type: Article

References (69)

1. de Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. 1998. Brain corticosteroid receptor balance in health and disease. Endocrine Rev. 19:269-301.
2. Yamamoto KR. 1995. Multilayered control of intracellular receptor function. Harvey Lect. 91:1-19.
3. Hittelman AB, Burakov D, Iniguez-Lluhi JA, Freedman LP, Garabedian MJ. 1999. Differential regulation of glucocorticoid receptor transcriptional activation via AF-1-associated proteins. EMBO J. 18:5380-5388.
4. Ismaili N, Garabedian MJ. 2004. Modulation of glucocorticoid receptor function via phosphorylation. Ann. N. Y. Acad. Sci. 1024:86-101.
5. Rogatsky I, Wang JC, Derynck MK, Nonaka DF, Khodabakhsh DB, Haqq CM, Darimont BD, Garabedian MJ, Yamamoto KR. 2003. Targetspecific utilization of transcriptional regulatory surfaces by the glucocorticoid receptor. Proc. Natl. Acad. Sci. U. S. A. 100:13845-13850.
6. Webster JC, Jewell CM, Bodwell JE, Munck A, Sar M, Cidlowski JA. 1997. Mouse glucocorticoid receptor phosphorylation status influences multiple functions of the receptor protein. J. Biol. Chem. 272:9287-9293.
7. Galliher-Beckley AJ, Cidlowski JA. 2009. Emerging roles of glucocorticoid receptor phosphorylation in modulating glucocorticoid hormone action in health and disease. IUBMB Life 61:979-986.
8. Chen W, Rogatsky I, Garabedian MJ. 2006. MED14 and MED1 differentially regulate target-specific gene activation by the glucocorticoid receptor. Mol. Endocrinol. 20:560-572.
9. Galliher-Beckley AJ, Williams JG, Collins JB, Cidlowski JA. 2008. Glycogen synthase kinase 3β-mediated serine phosphorylation of the human glucocorticoid receptor redirects gene expression profiles. Mol. Cell. Biol. 28:7309-7322.
10. Chen W, Dang T, Blind RD, Wang Z, Cavasotto CN, Hittelman AB, Rogatsky I, Logan SK, Garabedian MJ. 2008. Glucocorticoid receptor phosphorylation differentially affects target gene expression. Mol. Endocrinol. 22:1754-1766.
11. Wang Z, Frederick J, Garabedian MJ. 2002. Deciphering the phosphorylation "code" of the glucocorticoid receptor in vivo. J. Biol. Chem. 277: 26573-26580.
12. Holsboer F. 2000. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23:477-501.
13. Pariante CM. 2003. Depression, stress and the adrenal axis. J. Neuroendocrinol. 15:811-812.
14. Webster MJ, Knable MB, O'Grady J, Orthmann J, Weickert CS. 2002. Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders. Mol. Psychiatry 7:985- 994.
15. van Rossum EF, Lamberts SW. 2004. Polymorphisms in the glucocorticoid receptor gene and their associations with metabolic parameters and body composition. Recent Prog. Horm Res. 59:333-357.
16. de Quervain DJ, Poirier R, Wollmer MA, Grimaldi LM, Tsolaki M, Streffer JR, Hock C, Nitsch RM, Mohajeri MH, Papassotiropoulos A. 2004. Glucocorticoid-related genetic susceptibility for Alzheimer's disease. Hum. Mol. Genet. 13:47-52.
17. Green KN, Billings LM, Roozendaal B, McGaugh JL, LaFerla FM. 2006. Glucocorticoids increase amyloid-beta and tau pathology in a mouse model of Alzheimer's disease. J. Neurosci. 26:9047-9056.
18. Holsboer F, Ising M. 2010. Stress hormone regulation: biological role and translation into therapy. Annu. Rev. Psychol 61:81-109.
19. Yehuda R, Halligan SL, Grossman R, Golier JA, Wong C. 2002. The cortisol and glucocorticoid receptor response to low dose dexamethasone administration in aging combat veterans and holocaust survivors with and without posttraumatic stress disorder. Biol. Psychiatry 52:393-403.
20. Jeanneteau FD, Lambert WM, Ismaili N, Bath KG, Lee FS, Garabedian MJ, Chao MV. 2012. BDNF and glucocorticoids regulate corticotrophinreleasing hormone (CRH) homeostasis in the hypothalamus. Proc. Natl. Acad. Sci. U. S. A. 109:1305-1310.
21. Chao MV. 2003. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4:299-309.
22. Angelucci F, Brene S, Mathe AA. 2005. BDNF in schizophrenia, depression and corresponding animal models. Mol. Psychiatry 10:345-352.
23. Schmidt HD, Duman RS. 2010. Peripheral BDNF produces antidepressant- like effects in cellular and behavioral models. Neuropsychopharmacology 35:2378-2391.
24. Shirayama Y, Chen AC, Nakagawa S, Russell DS, Duman RS. 2002. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 22:3251-3261.
25. Chen ZY, Jing D, Bath KG, Ieraci A, Khan T, Siao CJ, Herrera DG, Toth M, Yang C, McEwen BS, Hempstead BL, Lee FS. 2006. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314:140-143.
26. Soliman F, Glatt CE, Bath KG, Levita L, Jones RM, Pattwell SS, Jing D, Tottenham N, Amso D, Somerville LH, Voss HU, Glover G, Ballon DJ, Liston C, Teslovich T, Van Kempen T, Lee FS, Casey BJ. 2010. A genetic variantBDNFpolymorphism alters extinction learning in both mouse and human. Science 327:863-866.
27. Gray JD, Milner TA, McEwen BS. 2013. Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience 239:214-227.
28. Jeanneteau F, Chao MV. 2013. Are BDNF and glucocorticoid activities calibrated?. Neuroscience 239:173-195.
29. Numakawa T, Adachi N, Richards M, Chiba S, Kunugi H. 2013. Brain-derived neurotrophic factor and glucocorticoids: reciprocal influence on the central nervous system. Neuroscience 239:157-172.
30. Suri D, Vaidya VA. 2013. Glucocorticoid regulation of brain-derived neurotrophic factor: relevance to hippocampal structural and functional plasticity. Neuroscience 239:196-213.
31. McEwen BS. 2005. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54:20-23.
32. Tata DA, Marciano VA, Anderson BJ. 2006. Synapse loss from chronically elevated glucocorticoids: relationship to neuropil volume and cell number in hippocampal area CA3. J. Comp. Neurol. 498:363-374.
33. Watanabe Y, Gould E, McEwen BS. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588:341- 345.
34. Jeanneteau F, Garabedian MJ, Chao MV. 2008. Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect. Proc. Natl. Acad. Sci. U. S. A. 105:4862-4867.
35. Chang Q, Khare G, Dani V, Nelson S, Jaenisch R. 2006. The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49:341-348.
36. Ernfors P, Lee KF, Jaenisch R. 1994. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147-150.
37. Rohrer B, Korenbrot JI, LaVail MM, Reichardt LF, Xu B. 1999. Role of neurotrophin receptor TrkB in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J. Neurosci. 19:8919-8930.
38. Narisawa-Saito M, Iwakura Y, Kawamura M, Araki K, Kozaki S, Takei N, Nawa H. 2002. Brain-derived neurotrophic factor regulates surface expression of alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid receptors by enhancing the N-ethylmaleimide-sensitive factor/GluR2 interaction in developing neocortical neurons. J. Biol. Chem. 277:40901- 40910.
39. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193.
40. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57.
41. Huang DW, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1-13.
42. Bailey TL. 2011. DREME: motif discovery in transcription factor ChIPseq data. Bioinformatics 27:1653-1659.
43. Ma Y, Lu Y, Zeng H, Ron D, Mo W, Neubert TA. 2001. Characterization of phosphopeptides from protein digests using matrix-assisted laser desorption/ ionization time-of-flight mass spectrometry and nanoelectrospray quadrupole time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 15:1693-1700.
44. Xu CF, Lu Y, Ma J, Mohammadi M, Neubert TA. 2005. Identification of phosphopeptides by MALDI Q.-TOF MS in positive and negative ion modes after methyl esterification. Mol. Cell. Proteomics 4:809-818.
45. Reddy TE, Pauli F, Sprouse RO, Neff NF, Newberry KM, Garabedian MJ, Myers RM. 2009. Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res. 19:2163-2171.
46. Vivanco MD, Johnson R, Galante PE, Hanahan D, Yamamoto KR. 1995. A transition in transcriptional activation by the glucocorticoid and retinoic acid receptors at the tumor stage of dermal fibrosarcoma development. EMBO J. 14:2217-2228.
47. Lefstin JA, Thomas JR, Yamamoto KR. 1994. Influence of a steroid receptor DNA-binding domain on transcriptional regulatory functions. Genes Dev. 8:2842-2856.
48. Wright AP, McEwan IJ, Dahlman-Wright K, Gustafsson JA. 1991. High level expression of the major transactivation domain of the human glucocorticoid receptor in yeast cells inhibits endogenous gene expression and cell growth. Mol. Endocrinol. 5:1366-1372.
49. Xiao L, Qi A, Chen Y. 2005. Cultured embryonic hippocampal neurons deficient in glucocorticoid (GC) receptor: a novel model for studying nongenomic effects of GC in the neural system. Endocrinology 146:4036- 4041.
50. Dennis G, Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4:P3. doi:10.1186/gb-2003-4-5-p3.
51. Jeanneteau F, Deinhardt K, Miyoshi G, Bennett AM, Chao MV. 2010. The MAP kinase phosphatase MKP-1 regulates BDNF-induced axon branching. Nat. Neurosci. 13:1373-1379.
52. Matsumoto K, Nishihara S, Kamimura M, Shiraishi T, Otoguro T, Uehara M, Maeda Y, Ogura K, Lumsden A, Ogura T. 2004. The prepattern transcription factor Irx2, a target of the FGF8/MAP kinase cascade, is involved in cerebellum formation. Nat. Neurosci. 7:605-612.
53. Toyoda R, Assimacopoulos S, Wilcoxon J, Taylor A, Feldman P, Suzuki-Hirano A, Shimogori T, Grove EA. 2010. FGF8 acts as a classic diffusible morphogen to pattern the neocortex. Development 137:3439- 3448.
54. Fukumoto K, Morita T, Mayanagi T, Tanokashira D, Yoshida T, Sakai A, Sobue K. 2009. Detrimental effects of glucocorticoids on neuronal migration during brain development. Mol. Psychiatry 14:1119-1131.
55. Kwok JC, Dick G, Wang D, Fawcett JW. 2011. Extracellular matrix and perineuronal nets in CNS repair. Dev. Neurobiol. 71:1073-1089.
56. Pejler G, Abrink M, Wernersson S. 2009. Serglycin proteoglycan: regulating the storage and activities of hematopoietic proteases. Biofactors 35:61-68.
57. Anacker C, Cattaneo A, Musaelyan K, Zunszain PA, Horowitz M, Molteni R, Luoni A, Calabrese F, Tansey K, Gennarelli M, Thuret S, Price J, Uher R, Riva MA, Pariante CM. 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.
58. Ayroldi E, Riccardi C. 2009. Glucocorticoid-induced leucine zipper (GILZ): a new important mediator of glucocorticoid action. FASEB J. 23:3649-3658.
59. Mikosz CA, Brickley DR, Sharkey MS, Moran TW, Conzen SD. 2001. Glucocorticoid receptor-mediated protection from apoptosis is associated with induction of the serine/threonine survival kinase gene, sgk-1. J. Biol. Chem. 276:16649-16654.
60. Reddy TE, Gertz J, Crawford GE, Garabedian MJ, Myers RM. 2012. The hypersensitive glucocorticoid response specifically regulates period 1 and expression of circadian genes. Mol. Cell. Biol. 32:3756-3767.
61. Stauber C, Altschmied J, Akerblom IE, Marron JL, Mellon PL. 1992. Mutual cross-interference between glucocorticoid receptor and CREB inhibits transactivation in placental cells. New Biol. 4:527-540.
62. Strahle U, Schmid W, Schutz G. 1988. Synergistic action of the glucocorticoid receptor with transcription factors. EMBO J. 7:3389-3395.
63. John S, Sabo PJ, Johnson TA, Sung MH, Biddie SC, Lightman SL, Voss TC, Davis SR, Meltzer PS, Stamatoyannopoulos JA, Hager GL. 2008. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol. Cell 29:611-624.
64. Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH. 1993. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855-859.
65. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB. 2005. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123: 493-505.
66. Rao NAS, McCalman MT, Moulos P, Francoijs K-J, Chatziioannou A, Kolisis FN, Alexis MN, Mitsiou DJ, Stunnenberg HG. 2011. Coactivation of GR and NFKB alters the repertoire of their binding sites and target genes. Genome Res. 21:1404-1416.
67. Galliher-Beckley AJ, Williams JG, Cidlowski JA. 2011. Ligandindependent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling. Mol. Cell. Biol. 31:4663-4675.
68. Schmidt P, Holsboer F, Spengler D. 2001. Beta(2)-adrenergic receptors potentiate glucocorticoid receptor transactivation viaGprotein beta gamma-subunits and the phosphoinositide 3-kinase pathway. Mol. Endocrinol. 15:553-564.
69. Kaur M, Chivers JE, Giembycz MA, Newton R. 2008. Long-acting beta2-adrenoceptor agonists synergistically enhance glucocorticoiddependent transcription in human airway epithelial and smooth muscle cells. Mol. Pharmacol. 73:203-214.