Glucocorticoids modulate NF-κB-dependent gene expression by up-regulating FKBP51 expression in Newcastle disease virus-infected chickens

Molecular and Cellular Endocrinology

Volumn 278, Issue 1-2, 2007, Pages 7-17

  Park, Jiyoung ^a   Kim, Mijin ^a   Na, Giyoun ^a   Jeon, Iksoo ^b   Kwon, Yong kuk ^c   Kim, Jae hong ^c   Youn, Hyesook ^d   Koo, Yongbum ^a  

^a Inje University   (South Korea)

^b National Institute of Animal Science   (South Korea)

^c Avian Disease Division   (South Korea)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

FK506 binding protein 51; Glucocorticoids; Newcastle disease virus; Nuclear factor kappaB

Indexed keywords

CORTICOSTEROID; DEXAMETHASONE; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 51; FK 506 BINDING PROTEIN 52; GLUCOCORTICOID; HEAT SHOCK PROTEIN 90; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN BFL A1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOREGULATION; BIRD DISEASE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; MESSENGER RNA SYNTHESIS; NEWCASTLE DISEASE PARAMYXOVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; APOPTOSIS; BCL-X PROTEIN; CELL LINE; CHICKENS; CORTICOSTERONE; DEXAMETHASONE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HSP90 HEAT-SHOCK PROTEINS; NEWCASTLE DISEASE VIRUS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-BCL-2; TACROLIMUS BINDING PROTEINS; TISSUE DISTRIBUTION;

EID: 36549042411     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2007.08.002     Document Type: Article

References (55)

1. Ashburner B.P., Westerheide S.D., and Baldwin Jr. A.S. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell Biol. 21 (2001) 7065-7077
2. Bailly-Maitre B., de Sousa G., Boulukos K., Gugenheim J., and Rahmani R. Dexamethasone inhibits spontaneous apoptosis in primary cultures of human and rat hepatocytes via Bcl-2 and Bcl-xL induction. Cell Death Differ. 8 (2001) 279-288
3. Baughman G., Wiederrecht G.J., Campbell N.F., Martin M.M., and Bourgeois S. FKBP51, a novel T-cell-specific immunophilin capable of calcineurin inhibition. Mol. Cell Biol. 15 (1995) 4395-4402
4. Baughman G., Wiederrecht G.J., Chang F., Martin M.M., and Bourgeois S. Tissue distribution and abundance of human FKBP51, and FK506-binding protein that can mediate calcineurin inhibition. Biochem. Biophys. Res. Commun. 232 (1997) 437-443
5. Binder E.B., Salyakina D., Lichtner P., Wochnik G.M., Ising M., Putz B., Papiol S., Seaman S., Lucae S., Kohli M.A., Nickel T., Kunzel H.E., Fuchs B., Majer M., Pfennig A., Kern N., Brunner J., Modell S., Baghai T., Deiml T., Zill P., Bondy B., Rupprecht R., Messer T., Kohnlein O., Dabitz H., Bruckl T., Muller N., Pfister H., Lieb R., Mueller J.C., Lohmussaar E., Strom T.M., Bettecken T., Meitinger T., Uhr M., Rein T., Holsboer F., and Muller-Myhsok B. Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat. Genet. 36 (2004) 1319-1325
6. Bouwmeester T., Bauch A., Ruffner H., Angrand P.O., Bergamini G., Croughton K., Cruciat C., Eberhard D., Gagneur J., Ghidelli S., Hopf C., Huhse B., Mangano R., Michon A.M., Schirle M., Schlegl J., Schwab M., Stein M.A., Bauer A., Casari G., Drewes G., Gavin A.C., Jackson D.B., Joberty G., Neubauer G., Rick J., Kuster B., and Superti-Furga G. A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat. Cell Biol. 6 (2004) 97-105
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
8. Chen C.C. Signal transduction pathways of inflammatory gene expressions and therapeutic implications. Curr. Pharm. Des. 12 (2006) 3497-3508
9. Chen Z., Hagler J., Palombella V.J., Melandri F., Scherer D., Ballard D., and Maniatis T. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9 (1995) 1586-1597
10. Chen C., Edelstein L.C., and Gelinas C. The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol. Cell Biol. 20 (2000) 2687-2695
11. Chrousos G.P., Renquist D., Brandon D., Eil C., Pugeat M., Vigersky R., Cutler Jr. G.B., Loriaux D.L., and Lipsett M.B. Glucocorticoid hormone resistance during primate evolution: receptor-mediated mechanisms. Proc. Natl. Acad. Sci. U.S.A. 79 (1982) 2036-2040
12. Clegg N., Eroglu B., Ferguson C., Arnold H., Moorman A., and Nelson P.S. Digital expression profiles of the prostate androgen-response program. J. Steroid Biochem. Mol. Biol. 80 (2002) 13-23
13. Davies T.H., Ning Y.M., and Sanchez E.R. A new first step in activation of steroid receptors: hormone-induced switching of FKBP51 and FKBP52 immunophilins. J. Biol. Chem. 277 (2002) 4597-4600
14. Denny W.B., Valentine D.L., Reynolds P.D., Smith D.F., and Scammell J.G. Squirrel monkey immunophilin FKBP51 is a potent inhibitor of glucocorticoid receptor binding. Endocrinology 141 (2000) 4107-4113
15. Denny W.B., Prapapanich V., Smith D.F., and Scammell J.G. Structure-function analysis of squirrel monkey FK506-binding protein 51, a potent inhibitor of glucocorticoid receptor activity. Endocrinology 146 (2005) 3194-3201
16. DiDonato J., Mercurio F., Rosette C., Wu-Li J., Suyang H., Ghosh S., and Karin M. Mapping of the inducible IkappaB phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell Biol. 16 (1996) 1295-1304
17. Dong Y., Poellinger L., Gustafsson J.A., and Okret S. Regulation of glucocorticoid receptor expression: evidence for transcriptional and posttranslational mechanisms. Mol. Endocrinol. 2 (1988) 1256-1264
18. Dunn A.J., and Vickers S.L. Neurochemical and neuroendocrine responses to Newcastle disease virus administration in mice. Brain Res. 645 (1994) 103-112
19. Edelstein L.C., Lagos L., Simmons M., Tirumalai H., and Gelinas C. NF-kappa B-dependent assembly of an enhanceosome-like complex on the promoter region of apoptosis inhibitor Bfl-1/A1. Mol. Cell Biol. 23 (2003) 2749-2761
20. Evans-Storms R.B., and Cidlowski J.A. Delineation of an antiapoptotic action of glucocorticoids in hepatoma cells: the role of nuclear factor-kappaB. Endocrinology 141 (2000) 1854-1862
21. Febbo P.G., Lowenberg M., Thorner A.R., Brown M., Loda M., and Golub T.R. Androgen mediated regulation and functional implications of fkbp51 expression in prostate cancer. J. Urol. 173 (2005) 1772-1777
22. Feng B., Cheng S., Hsia C.Y., King L.B., Monroe J.G., and Liou H.C. NF-kappaB inducible genes BCL-X and cyclin E promote immature B-cell proliferation and survival. Cell Immunol. 232 (2004) 9-20
23. Freeman A.I., Munn H.L., Lyons V., Dammermann A., Seckl J.R., and Chapman K.E. Glucocorticoid down-regulation of rat glucocorticoid receptor does not involve differential promoter regulation. J. Endocrinol. 183 (2004) 365-374
24. Gascoyne D.M., Kypta R.M., and Vivanco M.M. Glucocorticoids inhibit apoptosis during fibrosarcoma development by transcriptionally activating Bcl-xL. J. Biol. Chem. 278 (2003) 18022-18029
25. Glasgow J.N., Wood T., and Perez-Polo J.R. Identification and characterization of nuclear factor kappaB binding sites in the murine bcl-x promoter. J. Neurochem. 75 (2000) 1377-1389
26. Hatada E.N., Krappmann D., and Scheidereit C. NF-kappaB and the innate immune response. Curr. Opin. Immunol. 12 (2000) 52-58
27. Hubler T.R., and Scammell J.G. Intronic hormone response elements mediate regulation of FKBP5 by progestins and glucocorticoids. Cell Stress Chaperones 9 (2004) 243-252
28. Hubler T.R., Denny W.B., Valentine D.L., Cheung-Flynn J., Smith D.F., and Scammell J.G. The FK506-binding immunophilin FKBP51 is transcriptionally regulated by progestin and attenuates progestin responsiveness. Endocrinology 144 (2003) 2380-2387
29. Johnson M.R., Wang K., Smith J.B., Heslin M.J., and Diasio R.B. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Anal. Biochem. 278 (2000) 175-184
30. Karin M., and Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18 (2000) 621-663
31. Kim J.K., Kim K.D., Lee E., Lim J.S., Cho H.J., Yoon H.K., Cho M.Y., Baek K.E., Park Y.P., Paik S.G., Choe Y.K., and Lee H.G. Up-regulation of Bfl-1/A1 via NF-kappaB activation in cisplatin-resistant human bladder cancer cell line. Cancer Lett. 212 (2004) 61-70
32. Kurihara I., Shibata H., Suzuki T., Ando T., Kobayashi S., Hayashi M., Saito I., and Saruta T. Expression and regulation of nuclear receptor coactivators in glucocorticoid action. Mol. Cell Endocrinol. 189 (2002) 181-189
33. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
34. Lee Y.J., Sung H.W., Choi J.G., Kim J.H., and Song C.S. Molecular epidemiology of Newcastle disease viruses isolated in South Korea using sequencing of the fusion protein cleavage site region and phylogenetic relationships. Avian Pathol. 33 (2004) 482-491
35. Magee J.A., Chang L.W., Stormo G.D., and Milbrandt J. Direct, androgen receptor-mediated regulation of the FKBP5 gene via a distal enhancer element. Endocrinology 147 (2006) 590-598
36. Nagarajan R.P., Chen F., Li W., Vig E., Harrington M.A., Nakshatri H., and Chen Y. Repression of transforming-growth-factor-beta-mediated transcription by nuclear factor kappaB. Biochem. J. 348 Pt 3 (2000) 591-596
37. Nuber U.A., Kriaucionis S., Roloff T.C., Guy J., Selfridge J., Steinhoff C., Schulz R., Lipkowitz B., Ropers H.H., Holmes M.C., and Bird A. Up-regulation of glucocorticoid-regulated genes in a mouse model of Rett syndrome. Hum. Mol. Genet. 14 (2005) 2247-2256
38. Oishi K., Amagai N., Shirai H., Kadota K., Ohkura N., and Ishida N. Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver. DNA Res. 12 (2005) 191-202
39. Okret S., Poellinger L., Dong Y., and Gustafsson J.A. Down-regulation of glucocorticoid receptor mRNA by glucocorticoid hormones and recognition by the receptor of a specific binding sequence within a receptor cDNA clone. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 5899-5903
40. Patchev V.K., Brady L.S., Karl M., and Chrousos G.P. Regulation of HSP90 and corticosteroid receptor mRNA by corticosterone levels in vivo. Mol. Cell Endocrinol. 103 (1994) 57-64
41. Reynolds P.D., Ruan Y., Smith D.F., and Scammell J.G. Glucocorticoid resistance in the squirrel monkey is associated with overexpression of the immunophilin FKBP51. J. Clin. Endocrinol. Metab. 84 (1999) 663-669
42. Riggs D.L., Roberts P.J., Chirillo S.C., Cheung-Flynn J., Prapapanich V., Ratajczak T., Gaber R., Picard D., and Smith D.F. The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. EMBO J. 22 (2003) 1158-1167
43. Rocha-Viegas L., Vicent G.P., Baranao J.L., Beato M., and Pecci A. Glucocorticoids repress bcl-X expression in lymphoid cells by recruiting STAT5B to the P4 promoter. J. Biol. Chem. 281 (2006) 33959-33970
44. Scammell J.G., Denny W.B., Valentine D.L., and Smith D.F. Overexpression of the FK506-binding immunophilin FKBP51 is the common cause of glucocorticoid resistance in three New World primates. Gen. Comp. Endocrinol. 124 (2001) 152-165
45. Shaw J., Zhang T., Rzeszutek M., Yurkova N., Baetz D., Davie J.R., and Kirshenbaum L.A. Transcriptional silencing of the death gene BNIP3 by cooperative action of NF-{kappa}B and histone deacetylase 1 in ventricular myocytes. Circ. Res. 99 (2006) 1347-1354
46. Sinars C.R., Cheung-Flynn J., Rimerman R.A., Scammell J.G., Smith D.F., and Clardy J. Structure of the large FK506-binding protein FKBP51, an Hsp90-binding protein and a component of steroid receptor complexes. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 868-873
47. Tamatani M., Che Y.H., Matsuzaki H., Ogawa S., Okado H., Miyake S., Mizuno T., and Tohyama M. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J. Biol. Chem. 274 (1999) 8531-8538
48. Tarte K., Jourdan M., Veyrune J.L., Berberich I., Fiol G., Redal N., Shaughnessy Jr. J., and Klein B. The Bcl-2 family member Bfl-1/A1 is strongly repressed in normal and malignant plasma cells but is a potent anti-apoptotic factor for myeloma cells. Br. J. Haematol. 125 (2004) 373-382
49. Vermeer H., Hendriks-Stegeman B.I., van der Burg B., van Buul-Offers S.C., and Jansen M. Glucocorticoid-induced increase in lymphocytic FKBP51 messenger ribonucleic acid expression: a potential marker for glucocorticoid sensitivity, potency, and bioavailability. J. Clin. Endocrinol. Metab. 88 (2003) 277-284
50. Vermeer H., Hendriks-Stegeman B.I., van Suylekom D., Rijkers G.T., van Buul-Offers S.C., and Jansen M. An in vitro bioassay to determine individual sensitivity to glucocorticoids: induction of FKBP51 mRNA in peripheral blood mononuclear cells. Mol. Cell Endocrinol. 218 (2004) 49-55
51. Wallace A.D., and Cidlowski J.A. Proteasome-mediated glucocorticoid receptor degradation restricts transcriptional signaling by glucocorticoids. J. Biol. Chem. 276 (2001) 42714-42721
52. Wochnik G.M., Ruegg J., Abel G.A., Schmidt U., Holsboer F., and Rein T. FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J. Biol. Chem. 280 (2005) 4609-4616
53. Wu B., Li P., Liu Y., Lou Z., Ding Y., Shu C., Ye S., Bartlam M., Shen B., and Rao Z. 3D structure of human FK506-binding protein 52: implications for the assembly of the glucocorticoid receptor/Hsp90/immunophilin heterocomplex. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 8348-8353
54. Yang Y., Liou H.C., and Sun X.H. Id1 Potentiates NF-{kappa}B Activation upon T Cell Receptor Signaling. J. Biol. Chem. 281 (2006) 34989-34996
55. Zong W.X., Edelstein L.C., Chen C., Bash J., and Gelinas C. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev. 13 (1999) 382-387