The five Rs of glucocorticoid action during inflammation: Ready, reinforce, repress, resolve, and restore

Trends in Endocrinology and Metabolism

Volumn 24, Issue 3, 2013, Pages 109-119

  Busillo, John M ^a   Cidlowski, John A ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1;

ADAPTIVE IMMUNITY; ANTIINFLAMMATORY ACTIVITY; AUTOIMMUNE DISEASE; HOMEOSTASIS; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; LYMPHATIC SYSTEM TUMOR; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION;

ADAPTIVE IMMUNITY; ANTI-INFLAMMATORY AGENTS; GLUCOCORTICOIDS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNITY, INNATE; INFLAMMATION; INFLAMMATION MEDIATORS; PITUITARY-ADRENAL SYSTEM; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84875237427     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2012.11.005     Document Type: Review

References (94)

1. Newton K., Dixit V.M. Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 2012, 4:a006049.
2. Nathan C., Ding A. Nonresolving inflammation. Cell 2010, 140:871-882.
3. Clark A.R., Belvisi M.G. Maps and legends: the quest for dissociated ligands of the glucocorticoid receptor. Pharmacol. Ther. 2012, 134:54-67.
4. Oakley R.H., Cidlowski J.A. Cellular processing of the glucocorticoid receptor gene and protein: new mechanisms for generating tissue-specific actions of glucocorticoids. J. Biol. Chem. 2011, 286:3177-3184.
5. Cole T.J., et al. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 1995, 9:1608-1621.
6. Beck I.M., et al. Crosstalk in inflammation: the interplay of glucocorticoid receptor-based mechanisms and kinases and phosphatases. Endocr. Rev. 2009, 30:830-882.
7. Barnes P.J. Mechanisms and resistance in glucocorticoid control of inflammation. J. Steroid Biochem. Mol. Biol. 2010, 120:76-85.
8. Baschant U., Tuckermann J. The role of the glucocorticoid receptor in inflammation and immunity. J. Steroid Biochem. Mol. Biol. 2010, 120:69-75.
9. Sorrells S.F., et al. The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 2009, 64:33-39.
10. Sorrells S.F., Sapolsky R.M. An inflammatory review of glucocorticoid actions in the CNS. Brain Behav. Immun. 2007, 21:259-272.
11. Akira S., et al. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
12. Pancer Z., Cooper M.D. The evolution of adaptive immunity. Annu. Rev. Immunol. 2006, 24:497-518.
13. Iwasaki A., Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 2010, 327:291-295.
14. Evans R.M. The steroid and thyroid hormone receptor superfamily. Science 1988, 240:889-895.
15. Coutinho A.E., Chapman K.E. The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol. Cell. Endocrinol. 2010, 335:2-13.
16. Brewer J.A., et al. T-cell glucocorticoid receptor is required to suppress COX-2-mediated lethal immune activation. Nat. Med. 2003, 9:1318-1322.
17. Wust S., et al. Peripheral T cells are the therapeutic targets of glucocorticoids in experimental autoimmune encephalomyelitis. J. Immunol. 2008, 180:8434-8443.
18. Bhattacharyya S., et al. Macrophage glucocorticoid receptors regulate Toll-like receptor 4-mediated inflammatory responses by selective inhibition of p38 MAP kinase. Blood 2007, 109:4313-4319.
19. Tuckermann J.P., et al. Macrophages and neutrophils are the targets for immune suppression by glucocorticoids in contact allergy. J. Clin. Invest. 2007, 117:1381-1390.
20. Stavreva D.A., et al. Ultradian hormone stimulation induces glucocorticoid receptor-mediated pulses of gene transcription. Nat. Cell Biol. 2009, 11:1093-1102.
21. Galon J., et al. Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells. FASEB J. 2002, 16:61-71.
22. Chinenov Y., Rogatsky I. Glucocorticoids and the innate immune system: crosstalk with the toll-like receptor signaling network. Mol. Cell. Endocrinol. 2007, 275:30-42.
23. Strowig T., et al. Inflammasomes in health and disease. Nature 2012, 481:278-286.
24. Busillo J.M., et al. Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome. J. Biol. Chem. 2011, 286:38703-38713.
25. Ding Y., et al. Dexamethasone enhances ATP-induced inflammatory responses in endothelial cells. J. Pharmacol. Exp. Ther. 2010, 335:693-702.
26. Biddie S.C., et al. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol. Cell 2011, 43:145-155.
27. Rao N.A., et al. Coactivation of GR and NFKB alters the repertoire of their binding sites and target genes. Genome Res. 2011, 21:1404-1416.
28. Lannan E.A., et al. Proinflammatory actions of glucocorticoids: glucocorticoids and TNFalpha coregulate gene expression in vitro and in vivo. Endocrinology 2012, 153:3701-3712.
29. Baker C., et al. SERPINA3 (aka alpha-1-antichymotrypsin). Front. Biosci. 2007, 12:2821-2835.
30. Ishii T., et al. Augmentation of 11beta-hydroxysteroid dehydrogenase type 1 in LPS-activated J774.1 macrophages - role of 11beta-HSD1 in pro-inflammatory properties in macrophages. FEBS Lett. 2007, 581:349-354.
31. Ishii-Yonemoto T., et al. Glucocorticoid reamplification within cells intensifies NF-kappaB and MAPK signaling and reinforces inflammation in activated preadipocytes. Am. J. Physiol. Endocrinol. Metab. 2009, 298:E930-E940.
32. Langlais D., et al. Regulatory network analyses reveal genome-wide potentiation of LIF signaling by glucocorticoids and define an innate cell defense response. PLoS Genet. 2008, 4:e1000224.
33. Dittrich A., et al. Glucocorticoids increase interleukin-6-dependent gene induction by interfering with the expression of the suppressor of cytokine signaling 3 feedback inhibitor. Hepatology 2012, 55:256-266.
34. Kumar A., et al. Nuclear factor-kappaB: its role in health and disease. J. Mol. Med. (Berl.) 2004, 82:434-448.
35. Zenz R., et al. Activator protein 1 (Fos/Jun) functions in inflammatory bone and skin disease. Arthritis Res. Ther. 2008, 10:201.
36. Ogawa S., et al. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell 2005, 122:707-721.
37. Reily M.M., et al. The GRIP1:IRF3 interaction as a target for glucocorticoid receptor-mediated immunosuppression. EMBO J. 2006, 25:108-117.
38. Liberman A.C., et al. The activated glucocorticoid receptor inhibits the transcription factor T-bet by direct protein-protein interaction. FASEB J. 2007, 21:1177-1188.
39. Liberman A.C., et al. Glucocorticoids inhibit GATA-3 phosphorylation and activity in T cells. FASEB J. 2009, 23:1558-1571.
40. Kassel O., Herrlich P. Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol. Cell. Endocrinol. 2007, 275:13-29.
41. Eychene A., et al. A new MAFia in cancer. Nat. Rev. Cancer 2008, 8:683-693.
42. Johnson G.L., Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912.
43. Schule R., et al. Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor. Cell 1990, 62:1217-1226.
44. De Bosscher K., et al. Glucocorticoid repression of AP-1 is not mediated by competition for nuclear coactivators. Mol. Endocrinol. 2001, 15:219-227.
45. Heck S., et al. A distinct modulating domain in glucocorticoid receptor monomers in the repression of activity of the transcription factor AP-1. EMBO J. 1994, 13:4087-4095.
46. Liden J., et al. A new function for the C-terminal zinc finger of the glucocorticoid receptor. Repression of RelA transactivation. J. Biol. Chem. 1997, 272:21467-21472.
47. Chinenov Y., et al. Role of transcriptional coregulator GRIP1 in the anti-inflammatory actions of glucocorticoids. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:11776-11781.
48. McCoy C.E., et al. Glucocorticoids inhibit IRF3 phosphorylation in response to Toll-like receptor-3 and -4 by targeting TBK1 activation. J. Biol. Chem. 2008, 283:14277-14285.
49. Nissen R.M., Yamamoto K.R. The glucocorticoid receptor inhibits NFkappaB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 2000, 14:2314-2329.
50. Luecke H.F., Yamamoto K.R. The glucocorticoid receptor blocks P-TEFb recruitment by NFkappaB to effect promoter-specific transcriptional repression. Genes Dev. 2005, 19:1116-1127.
51. Islam K.N., Mendelson C.R. Glucocorticoid/glucocorticoid receptor inhibition of surfactant protein-A (SP-A) gene expression in lung type II cells is mediated by repressive changes in histone modification at the SP-A promoter. Mol. Endocrinol. 2008, 22:585-596.
52. Ito K., et al. Glucocorticoid receptor recruitment of histone deacetylase 2 inhibits interleukin-1beta-induced histone H4 acetylation on lysines 8 and 12. Mol. Cell. Biol. 2000, 20:6891-6903.
53. McKay L.I., Cidlowski J.A. CBP (CREB binding protein) integrates NF-kappaB (nuclear factor-kappaB) and glucocorticoid receptor physical interactions and antagonism. Mol. Endocrinol. 2000, 14:1222-1234.
54. Murphy S.H., et al. Tumor suppressor protein (p)53, is a regulator of NF-kappaB repression by the glucocorticoid receptor. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:17117-17122.
55. Baschant U., et al. Glucocorticoid therapy of antigen-induced arthritis depends on the dimerized glucocorticoid receptor in T cells. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:19317-19322.
56. Caelles C., et al. Nuclear hormone receptor antagonism with AP-1 by inhibition of the JNK pathway. Genes Dev. 1997, 11:3351-3364.
57. Kleiman A., et al. Glucocorticoid receptor dimerization is required for survival in septic shock via suppression of interleukin-1 in macrophages. FASEB J. 2011, 26:722-729.
58. Vandevyver S., et al. Glucocorticoid receptor dimerization induces MKP1 to protect against TNF-induced inflammation. J. Clin. Invest. 2012, 122:2130-2140.
59. Clark A.R. Anti-inflammatory functions of glucocorticoid-induced genes. Mol. Cell. Endocrinol. 2007, 275:79-97.
60. Smoak K., Cidlowski J.A. Glucocorticoids regulate tristetraprolin synthesis and posttranscriptionally regulate tumor necrosis factor alpha inflammatory signaling. Mol. Cell. Biol. 2006, 26:9126-9135.
61. Serhan C.N., et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 2007, 21:325-332.
62. Perretti M., D'Acquisto F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 2009, 9:62-70.
63. Gruver A.L., Sempowski G.D. Cytokines, leptin, and stress-induced thymic atrophy. J. Leukoc. Biol. 2008, 84:915-923.
64. Hick R.W., et al. Leptin selectively augments thymopoiesis in leptin deficiency and lipopolysaccharide-induced thymic atrophy. J. Immunol. 2006, 177:169-176.
65. Scheller J., et al. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 2011, 1813:878-888.
66. Duma D., et al. Sexually dimorphic actions of glucocorticoids provide a link to inflammatory diseases with gender differences in prevalence. Sci. Signal. 2010, 3:ra74.
67. Galliher-Beckley A.J., et al. Ligand-independent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling. Mol. Cell. Biol. 2011, 31:4663-4675.
68. John S., et al. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 2011, 43:264-268.
69. John S., et al. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol. Cell 2008, 29:611-624.
70. Johnson T.A., et al. Chromatin remodeling complexes interact dynamically with a glucocorticoid receptor-regulated promoter. Mol. Biol. Cell 2008, 19:3308-3322.
71. Kumar R., Thompson E.B. Gene regulation by the glucocorticoid receptor: structure:function relationship. J. Steroid Biochem. Mol. Biol. 2005, 94:383-394.
72. Bledsoe R.K., et al. Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell 2002, 110:93-105.
73. Grad I., Picard D. The glucocorticoid responses are shaped by molecular chaperones. Mol. Cell. Endocrinol. 2007, 275:2-12.
74. Vandevyver S., et al. On the trail of the glucocorticoid receptor: into the nucleus and back. Traffic 2012, 13:364-374.
75. Freedman N.D., Yamamoto K.R. Importin 7 and importin alpha/importin beta are nuclear import receptors for the glucocorticoid receptor. Mol. Biol. Cell 2004, 15:2276-2286.
76. Surjit M., et al. Widespread negative response elements mediate direct repression by agonist-liganded glucocorticoid receptor. Cell 2011, 145:224-241.
77. Meijsing S.H., et al. DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 2009, 324:407-410.
78. Ronacher K., et al. Ligand-selective transactivation and transrepression via the glucocorticoid receptor: role of cofactor interaction. Mol. Cell. Endocrinol. 2009, 299:219-231.
79. So A.Y., et al. Conservation analysis predicts in vivo occupancy of glucocorticoid receptor-binding sequences at glucocorticoid-induced genes. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5745-5749.
80. Lowenberg M., et al. Novel insights into mechanisms of glucocorticoid action and the development of new glucocorticoid receptor ligands. Steroids 2008, 73:1025-1029.
81. Song I.H., Buttgereit F. Non-genomic glucocorticoid effects to provide the basis for new drug developments. Mol. Cell. Endocrinol. 2006, 246:142-146.
82. Bruna A., et al. Glucocorticoid receptor-JNK interaction mediates inhibition of the JNK pathway by glucocorticoids. EMBO J. 2003, 22:6035-6044.
83. Croxtall J.D., et al. Glucocorticoids act within minutes to inhibit recruitment of signalling factors to activated EGF receptors through a receptor-dependent, transcription-independent mechanism. Br. J. Pharmacol. 2000, 130:289-298.
84. Gutierrez-Mecinas M., et al. Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:13806-13811.
85. Xiao L., et al. Glucocorticoid rapidly enhances NMDA-evoked neurotoxicity by attenuating the NR2A-containing NMDA receptor-mediated ERK1/2 activation. Mol. Endocrinol. 2010, 24:497-510.
86. Leis H., et al. Glucocorticoid receptor counteracts tumorigenic activity of Akt in skin through interference with the phosphatidylinositol 3-kinase signaling pathway. Mol. Endocrinol. 2004, 18:303-311.
87. Smith E., Frenkel B. Glucocorticoids inhibit the transcriptional activity of LEF/TCF in differentiating osteoblasts in a glycogen synthase kinase-3beta-dependent and -independent manner. J. Biol. Chem. 2005, 280:2388-2394.
88. Rhen T., Cidlowski J.A. Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. N. Engl. J. Med. 2005, 353:1711-1723.
89. Torpy D.J., Ho J.T. Corticosteroid-binding globulin gene polymorphisms: clinical implications and links to idiopathic chronic fatigue disorders. Clin. Endocrinol. (Oxf.) 2007, 67:161-167.
90. Lu N.Z., et al. International Union of Pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. Pharmacol. Rev. 2006, 58:782-797.
91. Rivest S. Interactions between the immune and neuroendocrine systems. Prog. Brain Res. 2010, 181:43-53.
92. Gross K.L., Cidlowski J.A. Tissue-specific glucocorticoid action: a family affair. Trends Endocrinol. Metab. 2008, 19:331-339.
93. Naray-Fejes-Toth A., Fejes-Toth G. Novel mouse strain with Cre recombinase in 11beta-hydroxysteroid dehydrogenase-2-expressing cells. Am. J. Physiol. Renal Physiol. 2007, 292:F486-F494.
94. Walker B.R., Andrew R. Tissue production of cortisol by 11beta-hydroxysteroid dehydrogenase type 1 and metabolic disease. Ann. N. Y. Acad. Sci. 2006, 1083:165-184.