The role of the glucocorticoid receptor in inflammation and immunity

Journal of Steroid Biochemistry and Molecular Biology

Volumn 120, Issue 2-3, 2010, Pages 69-75

  Baschant, Ulrike ^a   Tuckermann, Jan ^a  

^a FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

Conditional knock out mice; Glucocorticoid receptor; Inflammation

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; IMMUNOSUPPRESSIVE AGENT;

ALLERGIC DISEASE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; ASTHMA; B LYMPHOCYTE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FATE; CELL TYPE; CYTOKINE RELEASE; DENDRITIC CELL; DERMATITIS; HORMONE ACTION; HUMAN; IMMUNITY; IMMUNOCOMPETENT CELL; INFLAMMATION; INFLAMMATORY DISEASE; KNOCKOUT MOUSE; MIGRATION INHIBITION; NEOPLASM; NONHUMAN; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; UNSPECIFIED SIDE EFFECT;

ANIMALS; GLUCOCORTICOIDS; HUMANS; INFLAMMATION; LYMPHOCYTES; PHAGOCYTES; RECEPTORS, GLUCOCORTICOID;

MUS;

EID: 77952951936     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2010.03.058     Document Type: Article

References (82)

1. Pratt W.B., Toft D.O. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. (Maywood) 2003, 228(2):111-133.
2. Löwenberg M., Stahn C., Hommes D., Buttgereit F. Novel insights into mechanisms of glucocorticoid action and the development of new glucocorticoid receptor ligands. Steroids 2008, 73(9-10):1025-1029.
3. Meijsing S.H., Pufall M.A., So A.Y., Bates D.L., Chen L., Yamamoto K.R. DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 2009, 324(5925):407-410.
4. John S., Sabo P.J., Johnson T.A., Sung M.H., Biddie S.C., Lightman S.L., Voss T.C., Davis S.R., Meltzer P.S., Stamatoyannopoulos J.A., Hager G.L. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol. Cell 2008, 29(5):611-624.
5. De Bosscher K., Haegeman G. Minireview: latest perspectives on antiinflammatory actions of glucocorticoids. Mol. Endocrinol. 2008, 23(3):281-291.
6. Kassel O., Schneider S., Heilbock C., Litfin M., Gottlicher M., Herrlich P. A nuclear isoform of the focal adhesion LIM-domain protein Trip6 integrates activating and repressing signals at AP-1- and NF-kappaB-regulated promoters. Genes Dev. 2004, 18(20):2518-2528.
7. He Y., Simons S.S. STAMP, a novel predicted factor assisting TIF2 actions in glucocorticoid receptor-mediated induction and repression. Mol. Cell. Biol. 2007, 27(4):1467-1485.
8. Karin M New twists in gene regulation by glucocorticoid receptor: is DNA binding dispensable?. Cell 1998, 93(4):487-490.
9. Ogawa S., Lozach J., Benner C., Pascual G., Tangirala R.K., Westin S., Hoffmann A., Subramaniam S., David M., Rosenfeld M.G., Glass C.K. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell 2005, 122(5):707-721.
10. Bougarne N., Paumelle R., Caron S., Hennuyer N., Mansouri R., Gervois P., Staels B., Haegeman G., De Bosscher K. PPARalpha blocks glucocorticoid receptor alpha-mediated transactivation but cooperates with the activated glucocorticoid receptor alpha for transrepression on NF-kappaB. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(18):7397-7402.
11. Matthews L., Berry A., Tersigni M., D'acquisto F., Ianaro A., Ray D. Thiazolidinediones are partial agonists for the glucocorticoid receptor. Endocrinology 2008, 150(1):75-86.
12. Schacke H., Berger M., Rehwinkel H., Asadullah K. Selective glucocorticoid receptor agonists (SEGRAs): novel ligands with an improved therapeutic index. Mol. Cell. Endocrinol 2007, 275(1-2):109-117.
13. Heck S., Kullmann M., Gast A., Ponta H., Rahmsdorf H.J., Herrlich P., Cato A.C. A distinct modulating domain in glucocorticoid receptor monomers in the repression of activity of the transcription factor AP-1. EMBO J. 1994, 13(17):4087-4095.
14. Reichardt H.M., Kaestner K.H., Tuckermann J., Kretz O., Wessely O., Bock R., Gass P., Schmid W., Herrlich P., Angel P., Schutz G. DNA binding of the glucocorticoid receptor is not essential for survival. Cell 1998, 93(4):531-541.
15. Reichardt H.M., Tuckermann J.P., Göttlicher M., Vujic M., Weih F., Angel P., Herrlich P., Schütz G. Repression of inflammatory responses in the absence of DNA binding by the glucocorticoid receptor. EMBO J. 2001, 20(24):7168-7173.
16. Tuckermann J.P., Kleiman A., Moriggl R., Spanbroek R., Neumann A., Illing A., Clausen B.E., Stride B., Forster I., Habenicht A.J., Reichardt H.M., Tronche F., Schmid W., Schutz G. Macrophages and neutrophils are the targets for immune suppression by glucocorticoids in contact allergy. J. Clin. Invest. 2007, 117(5):1381-1390.
17. Schacke H., Schottelius A., Docke W.D., Strehlke P., Jaroch S., Schmees N., Rehwinkel H., Hennekes H., Asadullah K. Dissociation of transactivation from transrepression by a selective glucocorticoid receptor agonist leads to separation of therapeutic effects from side effects. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(1):227-232.
18. Dewint P., Gossye V., De Bosscher K., Vanden Berghe W., Van Beneden K., Deforce D., Van Calenbergh S., Muller-Ladner U., Vander Cruyssen B., Verbruggen G., Haegeman G., Elewaut D. A plant-derived ligand favoring monomeric glucocorticoid receptor conformation with impaired transactivation potential attenuates collagen-induced arthritis. J. Immunol. 2008, 180(4):2608-2615.
19. McMaster A., Ray D.W. Modelling the glucocorticoid receptor and producing therapeutic agents with anti-inflammatory effects but reduced side-effects. Exp. Physiol. 2007, 92(2):299-309.
20. Abraham S.M., Clark A.R. Dual-specificity phosphatase. 1: a critical regulator of innate immune responses,. Biochem. Soc. Trans. 2006, 34(Pt 6):1018-1023.
21. Abraham S.M., Lawrence T., Kleiman A., Warden P., Medghalchi M., Tuckermann J., Saklatvala J., Clark A.R. Antiinflammatory effects of dexamethasone are partly dependent on induction of dual specificity phosphatase 1. J. Exp. Med. 2006, 203(8):1883-1889.
22. Bhattacharyya S., Brown D.E., Brewer J.A., Vogt S.K., Muglia L.J. Macrophage glucocorticoid receptors regulate Toll-like receptor 4-mediated inflammatory responses by selective inhibition of p38 MAP kinase. Blood 2007, 109(10.):4313-4319.
23. Maier J.V., Brema S., Tuckermann J., Herzer U., Klein M., Stassen M., Moorthy A., Cato A.C. DUSP1 knockout mice show enhanced susceptibility to anaphylaxis but are sensitive to glucocorticoids. Mol. Endocrinol. 2007.
24. Moser M., De Smedt T., Sornasse T., Tielemans F., Chentoufi A.A., Muraille E., Van Mechelen M., Urbain J., Leo O. Glucocorticoids down-regulate dendritic cell function in vitro and in vivo. Eur. J. Immunol. 1995, 25(10):2818-2824.
25. Kim K.D., Choe Y.K., Choe I.S., Lim J.S. Inhibition of glucocorticoid-mediated, caspase-independent dendritic cell death by CD40 activation. J. Leukcyte Biol. 2001, 69(3):426-434.
26. Piemonti L, Monti P., Allavena P., Leone B.E., Caputo A., Di Carlo V. Glucocorticoids increase the endocytic activity of human dendritic cells. Int. Immunol. 1999, 11(9):1519-1526.
27. Piemonti L., Monti P., Allavena P., Sironi M., Soldini L., Leone B.E., Socci C., Di Carlo V. Glucocorticoids affect human dendritic cell differentiation and maturation. J. Immunol. 1999, 162(11):6473-6481.
28. Kitajima T., Ariizumi K., Bergstresser P.R., Takashima A. A novel mechanism of glucocorticoid-induced immune suppression: the inhibiton of T cell-mediated terminal maturation of a murine dendritic cell line. J. Clin. Invest. 1996, 98(1):142-147.
29. Matyszak M.K., Citterio S., Rescigno M., Ricciardi-Castagnoli P. Differential effects of corticosteroids during different stages of dendritic cell maturation. Eur. J. Immunol. 2000, 30(4):1233-1242.
30. Cumberbatch M., Dearman R.J., Kimber I. Inhibition by dexamethasone of Langerhans cell migration: influence of epidermal cytokine signals. Immunopharmacology 1999, 41(3):235-243.
31. Vizzardelli C., Pavelka N., Luchini A., Zanoni I., Bendickson L., Pelizzola M., Beretta O., Foti M., Granucci F., Nilsen-Hamilton M., Ricciardi-Castagnoli P. Effects of dexamethazone on LPS-induced activationand migration of mouse dendritic cells revealed by a genome-wide transcriptional analysis. Eur. J. Immunol. 2006, 36(6):1504-1515.
32. Wiley R.E., Cwiartka M., Alvarez D., Mackenzie D.C., Johnson J.R., Goncharova S., Lundblad L., Jordana M. Transient corticosteroid treatment permanently amplifies the Th2 response in a murine model of asthma. J. Immunol. 2004, 172(8):4995-5005.
33. Rutella S., Danese S., Leone G. Tolerogenic dendritic cells: cytokine modulation comes of age. Blood 2006, 108(5):1435-1440.
34. Chamorro S., Garcia-Vallejo J.J., Unger W.W.J., Fernandes R.J., Bruijns S.C.M., Laban S., Roep B.O., Hart B.A.T., Van Kooyk Y. TLR Triggering on tolerogenic dendritic cells results in TLR2 up-regulation and a reduced proinflammatory immune program. J. Immunol. 2009, 183(5):2984-2994.
35. Reily M.M., Pantoja C., Hu X., Chinenov Y., Rogatsky I. The GRIP1:IRF3 interaction as a target for glucocorticoid receptor-mediated immunosuppression. EMBO J. 2006, 25(1):108-117.
36. Ehrchen J., Steinmuller L., Barczyk K., Tenbrock K., Nacken W., Eisenacher M., Nordhues U., Sorg C., Sunderkotter C., Roth J. Glucocorticoids induce differentiation of a specifically activated, anti-inflammatory subtype of human monocytes. Blood 2007, 109(3):1265-1274.
37. Varga G, Ehrchen J., Tsianakas A., Tenbrock K., Rattenholl A., Seeliger S., Mack M., Roth J., Sunderkoetter C. Glucocorticoids induce an activated, anti-inflammatory monocyte subset in mice that resembles myeloid-derived suppressor cells. J. Leukocyte Biol. 2008, 84(3):644-650.
38. Heasman S.J., Giles K.M., Ward C., Rossi A.G., Haslett C., Dransfield I. Glucocorticoid-mediated regulation of granulocyte apoptosis and macrophage phagocytosis of apoptotic cells: implications for the resolution of inflammation. J. Endocrinol. 2003, 178(1.):29-36.
39. Yona S., Gordon S. Inflammation: glucocorticoids turn the monocyte switch. Immunol. Cell Biol. 2007.
40. Pitzalis C., Pipitone N., Perretti M. Regulation of leukocyte-endothelial interactions by glucocorticoids. Ann. N. Y. Acad. Sci. 2002, 966:108-118.
41. Cronstein B.N., Kimmel S.C., Levin R.I., Martiniuk F., Weissmann G. A mechanism for the antiinflammatory effects of corticosteroids: the glucocorticoid receptor regulates leukocyte adhesion to endothelial cells and expression of endothelial-leukocyte adhesion molecule 1 and intercellular adhesion molecule 1. Proc. Natl. Acad. Sci. U.S.A. 1992, 89(21):9991-9995.
42. Pitzalis C., Pipitone N., Bajocchi G., Hall M., Goulding N., Lee A., Kingsley G., Lanchbury J., Panayi G. Corticosteroids inhibit lymphocyte binding to endothelium and intercellular adhesion: an additional mechanism for their anti-inflammatory and immunosuppressive effect. J. Immunol. 1997, 158(10):5007-5016.
43. Stroncek D.F., Yau Y.Y., Oblitas J., Leitman S.F. Administration of G-CSF plus dexamethasone produces greater granulocyte concentrate yields while causing no more donor toxicity than G-CSF alone. Transfusion 2001, 41(8):1037-1044.
44. Cupps T.R., Edgar L.C., Thomas C.A., Fauci A.S. Multiple mechanisms of B cell immunoregulation in man after administration of in vivo corticosteroids. J. Immunol. 1984, 132(1):170-175.
45. Cupps T.R., Gerrard T.L., Falkoff R.J., Whalen G., Fauci A.S. Effects of in vitro corticosteroids on B cell activation, proliferation, and differentiation. J. Clin. Invest. 1985, 75(2):754-761.
46. Herold M.J, McPherson K.G., Reichardt H.M. Glucocorticoids in T cell apoptosis and function. Cell. Mol. Life Sci. 2006, 63(1):60-72.
47. Erlacher M., Labi V., Manzl C., Bock G., Tzankov A., Hacker G., Michalak E., Strasser A., Villunger A. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J. Exp. Med. 2006, 203(13):2939-2951.
48. Erlacher M, Michalak E.M., Kelly P.N., Labi V., Niederegger H., Coultas L., Adams J.M., Strasser A., Villunger A. BH3-only proteins Puma and Bim are rate-limiting for gamma-radiation- and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood 2005, 106(13):4131-4138.
49. Vacchio M.S., Papadopoulos V., Ashwell J.D. Steroid production in the thymus: implications for thymocyte selection. J. Exp. Med. 1994, 179(6):1835-1846.
50. Pazirandeh A., Xue Y., Rafter I., Sjövall J., Jondal M., Okret S. Paracrine glucocorticoid activity produced by mouse thymic epithelial cells. FASEB J. 1999, 13(8):893-901.
51. Erlacher M., Knoflach M., Stec I.E., Bock G., Wick G., Wiegers G.J. TCR signaling inhibits glucocorticoid-induced apoptosis in murine thymocytes depending on the stage of development. Eur. J. Immunol. 2005, 35(11):3287-3296.
52. Stephens G.L., Ashwell J.D., Ignatowicz L. Mutually antagonistic signals regulate selection of the T cell repertoire. Int. Immunol. 2003, 15(5):623-632.
53. Vacchio M.S., Lee J.Y., Ashwell J.D. Thymus-derived glucocorticoids set the thresholds for thymocyte selection by inhibiting TCR-mediated thymocyte activation. J. Immunol. 1999, 163(3):1327-1333.
54. Purton J.F., Boyd R.L., Cole T.J., Godfrey D.I., Intrathymic T cell development and selection proceeds normally in the absence of glucocorticoid receptor signaling. Immunity 2000, 13(2):179-186.
55. Brewer J.A., Kanagawa O., Sleckman B.P., Muglia L.J. Thymocyte apoptosis induced by T cell activation is mediated by glucocorticoids in vivo. J. Immunol. 2002, 169(4):1837-1843.
56. Baumann S., Dostert A., Novac N., Bauer A., Schmid W., Fas S.C., Krueger A., Heinzel T., Kirchhoff S., Schutz G., Krammer P.H. Glucocorticoids inhibit activation-induced cell death (AICD) via direct DNA-dependent repression of the CD95 ligand gene by a glucocorticoid receptor dimer. Blood 2005, 106(2):617-625.
57. Lowenberg M., Tuynman J., Bilderbeek J., Gaber T., Buttgereit F., van Deventer S., Peppelenbosch M., Hommes D. Rapid immunosuppressive effects of glucocorticoids mediated through Lck and Fyn. Blood 2005, 106(5):1703-1710.
58. Lowenberg M., Verhaar A.P., Bilderbeek J., Marle J., Buttgereit F., Peppelenbosch M.P., van Deventer S.J., Hommes D.W. Glucocorticoids cause rapid dissociation of a T-cell-receptor-associated protein complex containing LCK and FYN. EMBO Rep. 2006, 7(10):1023-1029.
59. Löwenberg M., Verhaar A.P., Bilderbeek J., Marle J.V., Buttgereit F., Peppelenbosch M.P., Van Deventer S.J., Hommes D.W. Glucocorticoids cause rapid dissociation of a T-cell-receptor-associated protein complex containing LCK and FYN. EMBO Rep. 2006, 7(10.):1023-1029.
60. Brewer J.A., Khor B., Vogt S.K., Muglia L.M., Fujiwara H., Haegele K.E., Sleckman B.P., Muglia L.J. T-cell glucocorticoid receptor is required to suppress COX-2-mediated lethal immune activation. Nat. Med. 2003.
61. Wang D., Müller N., McPherson K.G., Reichardt H.M. Glucocorticoids engage different signal transduction pathways to induce apoptosis in thymocytes and mature T cells. J. Immunol. 2006, 176(3):1695-1702.
62. Mosmann T.R., Coffman R.L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 1989, 7:145-173.
63. Farrar J.D., Ouyang W., Lohning M., Assenmacher M., Radbruch A., Kanagawa O., Murphy K.M. An instructive component in T helper cell type 2 (Th2) development mediated by GATA-3. J. Exp. Med. 2001, 193(5):643-650.
64. Laurence A., Tato C.M., Davidson T.S., Kanno Y., Chen Z., Yao Z., Blank R.B., Meylan F., Siegel R., Hennighausen L., Shevach E.M., O'Shea J.J. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 2007, 26(3):371-381.
65. Ma C.S., Chew G.Y.J., Simpson N., Priyadarshi A., Wong M., Grimbacher B., Fulcher D.A., Tangye S.G., Cook M.C. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 2008, 205(7):1551-1557.
66. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126(6):1121-1133.
67. Campbell D.J., Ziegler S.F. FOXP3 modifies the phenotypic and functional properties of regulatory T cells. Nat. Rev. Immunol. 2007, 7(4):305-310.
68. Ramirez F., Fowell D.J., Puklavec M., Simmonds S., Mason D. Glucocorticoids promote a TH2 cytokine response by CD4+ T cells in vitro. J. Immunol. 1996, 156(7):2406-2412.
69. Franchimont D., Galon J., Gadina M., Visconti R., Zhou Y., Aringer M., Frucht D.M., Chrousos G.P., O'Shea J.J. Inhibition of Th1 immune response by glucocorticoids: dexamethasone selectively inhibits IL-12-induced Stat4 phosphorylation in T lymphocytes. J. Immunol. 2000, 164(4):1768-1774.
70. Barnes P.J. Th2 cytokines and asthma: an introduction. Respir. Res. 2001, 2(2):64-65.
71. Liberman A.C., Druker J., Refojo D., Holsboer F., Arzt E. Glucocorticoids inhibit GATA-3 phosphorylation and activity in T cells. FASEB J. 2009, 23(5):1558-1571.
72. Maneechotesuwan K., Yao X., Ito K., Jazrawi E., Usmani O.S., Adcock I.M., Barnes P.J. Suppression of GATA-3 nuclear import and phosphorylation: a novel mechanism of corticosteroid action in allergic disease. PLoS Med. 2009, 6(5):e1000076.
73. Biola A., Andréau K., David M., Sturm M., Haake M., Bertoglio J., Pallardy M. The glucocorticoid receptor and STAT6 physically and functionally interact in T-lymphocytes. FEBS Lett. 2000, 487(2):229-233.
74. Ziolkowska M., Koc A., Luszczykiewicz G., Ksiezopolska-Pietrzak K., Klimczak E., Chwalinska-Sadowska H., Maslinski W. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J. Immunol. 2000, 164(5):2832-2838.
75. Momčilović M., Miljković Ž., Popadić D., Marković M., Savić E., Ramić Z., Miljković D., Mostarica-Stojković M. Methylprednisolone inhibits interleukin-17 and interferon-gamma expression by both naive and primed T cells. BMC Immunol. 2008, 9(1):47.
76. McKinley L., Alcorn J.F., Peterson A., Dupont R.B., Kapadia S., Logar A., Henry A., Irvin C.G., Piganelli J.D., Ray A., Kolls J.K. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 2008, 181(6):4089-4097.
77. Chen X., Murakami T., Oppenheim J.J., Howard O.M. Differential response of murine CD4+CD25+ and CD4+CD25- T cells to dexamethasone-induced cell death. Eur. J. Immunol. 2004, 34(3):859-869.
78. Kang Y., Xu L., Wang B., Chen A., Zheng G. Cutting edge: immunosuppressant as adjuvant for tolerogenic immunization. J. Immunol. 2008, 180(8):5172-5176.
79. Chen X., Oppenheim J.J., Winkler-Pickett R.T., Ortaldo J.R., Howard O.M. Glucocorticoid amplifies IL-2-dependent expansion of functional FoxP3(+)CD4(+)CD25(+) T regulatory cells in vivo and enhances their capacity to suppress EAE. Eur. J. Immunol. 2006, 36(8):2139-2149.
80. Wust S., van den Brandt J., Tischner D., Kleiman A., Tuckermann J.P., Gold R., Luhder F., Reichardt H.M. Peripheral T cells are the therapeutic targets of glucocorticoids in experimental autoimmune encephalomyelitis. J. Immunol. 2008, 180(12):8434-8443.
81. Yeager M.P., Guyre P.M., Munck A.U. Glucocorticoid regulation of the inflammatory response to injury. Acta Anaesthesiol. Scand. 2004, 48(7):799-813.
82. Belvisi M.G., Hele D.J. Soft steroids: a new approach to the treatment of inflammatory airways diseases. Pulm. Pharmacol. Ther. 2003, 16(6):321-325.