Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015, Article ID 347965, 16 pages
http://dx.doi.org/10.1155/2015/347965
Research Article

Sustained Interleukin-1β Exposure Modulates Multiple Steps in Glucocorticoid Receptor Signaling, Promoting Split-Resistance to the Transactivation of Prominent Anti-Inflammatory Genes by Glucocorticoids

1Department of Medicine, School of Medicine, Alcala University (UAH), Alcalá de Henares, 28805 Madrid, Spain
2Biologie des Bactéries Intracellulaires, Departement Genomes et Génétique, Institut Pasteur, 75015 Paris, France
3Immunology and Individualized Medicine, IMMPA CSIC/UAH Joint Unit, Alcalá de Henares, 28805 Madrid, Spain
4MRC & Asthma UK Centre in Allergic Mechanisms of Asthma, King’s College London, Division of Asthma, Allergy & Lung Biology, 5th Floor Tower Wing, Guy’s Hospital, London SE1 9RT, UK
5Department of Immunology and Oncology, National Biotechnology Center, Spanish National Research Council (CNB-CSIC), 28049 Madrid, Spain

Received 10 December 2014; Revised 22 February 2015; Accepted 26 February 2015

Academic Editor: Tânia Silvia Fröde

Copyright © 2015 Pedro Escoll et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. J. Barnes and I. M. Adcock, “Glucocorticoid resistance in inflammatory diseases,” The Lancet, vol. 373, no. 9678, pp. 1905–1917, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Dejager, S. Vandevyver, I. Petta, and C. Libert, “Dominance of the strongest: inflammatory cytokines versus glucocorticoids,” Cytokine & Growth Factor Reviews, vol. 25, no. 1, pp. 21–33, 2014. View at Publisher · View at Google Scholar
  3. J. M. Busillo and J. A. Cidlowski, “The five Rs of glucocorticoid action during inflammation: ready, reinforce, repress, resolve, and restore,” Trends in Endocrinology & Metabolism, vol. 24, no. 3, pp. 109–119, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Voronov, D. S. Shouval, Y. Krelin et al., “IL-1 is required for tumor invasiveness and angiogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 5, pp. 2645–2650, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Schlossmacher, A. Stevens, and A. White, “Glucocorticoid receptor-mediated apoptosis: mechanisms of resistance in cancer cells,” Journal of Endocrinology, vol. 211, no. 1, pp. 17–25, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Tchkonia, Y. Zhu, J. van Deursen, J. Campisi, and J. L. Kirkland, “Cellular senescence and the senescent secretory phenotype: therapeutic opportunities,” The Journal of Clinical Investigation, vol. 123, no. 3, pp. 966–972, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Tasdemir and S. W. Lowe, “Senescent cells spread the word: non-cell autonomous propagation of cellular senescence,” The EMBO Journal, vol. 32, no. 14, pp. 1975–1976, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. J. C. Acosta, A. Banito, T. Wuestefeld et al., “A complex secretory program orchestrated by the inflammasome controls paracrine senescence,” Nature Cell Biology, vol. 15, no. 8, pp. 978–990, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Kleiman, S. Hübner, J. M. R. Parkitna et al., “Glucocorticoid receptor dimerization is required for survival in septic shock via suppression of interleukin-1 in macrophages,” The FASEB Journal, vol. 26, no. 2, pp. 722–729, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. C. A. Dinarello, “Interleukin-1 in the pathogenesis and treatment of inflammatory diseases,” Blood, vol. 117, no. 14, pp. 3720–3732, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Del Rey, H. Besedovsky, E. Sorkin, and C. A. Dinarello, “Interleukin-1 and glucocorticoid hormones integrate an immunoregulatory feedback circuit,” Annals of the New York Academy of Sciences, vol. 496, pp. 85–90, 1987. View at Publisher · View at Google Scholar · View at Scopus
  12. R. B. Goodman, R. M. Strieter, D. P. Martin et al., “Inflammatory cytokines in patients with persistence of the acute respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 154, no. 3, pp. 602–611, 1996. View at Publisher · View at Google Scholar · View at Scopus
  13. D. S. Snyder and E. R. Unanue, “Corticosteroids inhibit murine macrophage Ia expression and interleukin 1 production,” The Journal of Immunology, vol. 129, no. 5, pp. 1803–1805, 1982. View at Google Scholar · View at Scopus
  14. K. F. Chung, “Cytokines in chronic obstructive pulmonary disease,” The European Respiratory Journal. Supplement, vol. 34, pp. 50s–59s, 2001. View at Google Scholar
  15. M. J. Staruch and D. D. Wood, “Reduction of serum interleukin-1-like activity after treatment with dexamethasone,” Journal of Leukocyte Biology, vol. 37, no. 2, pp. 193–207, 1985. View at Google Scholar · View at Scopus
  16. J. A. Frank, J. F. Pittet, C. Wray, and M. A. Matthay, “Protection from experimental ventilator-induced acute lung injury by IL-1 receptor blockade,” Thorax, vol. 63, no. 2, pp. 147–153, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. S. W. Lee, A.-P. Tsou, H. Chan et al., “Glucocorticoids selectively inhibit the transcription of the interleukin 1β gene and decrease the stability of interleukin 1β mRNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 4, pp. 1204–1208, 1988. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Hakonarson, E. Halapi, R. Whelan, J. Gulcher, K. Stefansson, and M. M. Grunstein, “Association between IL-1beta/TNF-alpha-induced glucocorticoid-sensitive changes in multiple gene expression and altered responsiveness in airway smooth muscle,” The American Journal of Respiratory Cell and Molecular Biology, vol. 25, no. 6, pp. 761–771, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. G. B. Pier, “The challenges and promises of new therapies for cystic fibrosis,” The Journal of Experimental Medicine, vol. 209, no. 7, pp. 1235–1239, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Petrasek, S. Bala, T. Csak et al., “IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice,” Journal of Clinical Investigation, vol. 122, no. 10, pp. 3476–3489, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Coccia, O. J. Harrison, C. Schiering et al., “IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4+ Th17 cells,” The Journal of Experimental Medicine, vol. 209, no. 9, pp. 1595–1609, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Chi, S. P. Barry, R. J. Roth et al., “Dynamic regulation of pro- and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 7, pp. 2274–2279, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Gaba, S. I. Grivennikov, M. V. Do, D. J. Stumpo, P. J. Blackshear, and M. Karin, “Cutting edge: IL-10-mediated tristetraprolin induction is part of a feedback loop that controls macrophage STAT3 activation and cytokine production,” The Journal of Immunology, vol. 189, no. 5, pp. 2089–2093, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Sauer, B. Schaljo, C. Vogl et al., “Interferons limit inflammatory responses by induction of tristetraprolin,” Blood, vol. 107, no. 12, pp. 4790–4797, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. X. Qian, H. Ning, J. Zhang et al., “Posttranscriptional regulation of IL-23 expression by IFN-γ through tristetraprolin,” The Journal of Immunology, vol. 186, no. 11, pp. 6454–6464, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Molle, T. Zhang, L. Y. de Lendonck et al., “Tristetraprolin regulation of interleukin 23 mRNA stability prevents a spontaneous inflammatory disease,” Journal of Experimental Medicine, vol. 210, no. 9, pp. 1675–1684, 2013. View at Google Scholar · View at Scopus
  27. D. Berrebi, S. Bruscoli, N. Cohen et al., “Synthesis of glucocorticoid-induced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10,” Blood, vol. 101, no. 2, pp. 729–738, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Yang, M. Thangaraju, D. D. Browning et al., “IFN regulatory factor 8 mediates apoptosis in nonhemopoietic tumor cells via regulation of Fas expression,” The Journal of Immunology, vol. 179, no. 7, pp. 4775–4782, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. F. T. Ishmael, X. Fang, M. R. Galdiero et al., “Role of the RNA-binding protein tristetraprolin in glucocorticoid-mediated gene regulation,” Journal of Immunology, vol. 180, no. 12, pp. 8342–8353, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Lasa, S. M. Abraham, C. Boucheron, J. Saklatvala, and A. R. Clark, “Dexamethasone causes sustained expression of mitogen-activated protein kinase (MAPK) phosphatase 1 and phosphatase-mediated inhibition of MAPK p38,” Molecular and Cellular Biology, vol. 22, no. 22, pp. 7802–7811, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Ayroldi and C. Riccardi, “Glucocorticoid-induced leucine zipper (GILZ): a new important mediator of glucocorticoid action,” The FASEB Journal, vol. 23, no. 11, pp. 3649–3658, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Chen, I. Rogatsky, and M. J. Garabedian, “MED14 and MED1 differentially regulate target-specific gene activation by the glucocorticoid receptor,” Molecular Endocrinology, vol. 20, no. 3, pp. 560–572, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. T. van Bogaert, S. Vandevyver, L. Dejager et al., “Tumor necrosis factor inhibits glucocorticoid receptor function in mice: a strong signal toward lethal shock,” The Journal of Biological Chemistry, vol. 286, no. 30, pp. 26555–26567, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Raddatz, S. Toth, H. Schwörer, and G. Ramadori, “Glucocorticoid receptor signaling in the intestinal epithelial cell lines IEC-6 and Caco-2: evidence of inhibition by interleukin-1beta,” International Journal of Colorectal Disease, vol. 16, no. 6, pp. 377–383, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. C. M. Pariante, B. D. Pearce, T. L. Pisell et al., “The proinflammatory cytokine, interleukin-1α, reduces glucocorticoid receptor translocation and function,” Endocrinology, vol. 140, no. 9, pp. 4359–4366, 1999. View at Google Scholar · View at Scopus
  36. X. Wang, H. Wu, and A. H. Miller, “Lnterleukin 1alpha (IL-1alpha) induced activation of p38 mitogen-activated protein kinase inhibits glucocorticoid receptor function,” Molecular Psychiatry, vol. 9, no. 1, pp. 65–75, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Vermeer, B. I. Hendriks-Stegeman, B. van der Burg, S. C. van Buul-Offers, and M. Jansen, “Glucocorticoid-induced increase in lymphocytic FKBP51 messenger ribonucleic acid expression: a potential marker for glucocorticoid sensitivity, potency, and bioavailability,” The Journal of Clinical Endocrinology & Metabolism, vol. 88, no. 1, pp. 277–284, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. Z. Wang, J. Frederick, and M. J. Garabedian, “Deciphering the phosphorylation ‘code’ of the glucocorticoid receptor in vivo,” Journal of Biological Chemistry, vol. 277, no. 29, pp. 26573–26580, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. I. Rogatsky, J. C. Wang, M. K. Derynck et al., “Target-specific utilization of transcriptional regulatory surfaces by the glucocorticoid receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 13845–13850, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. W. Chen, T. Dang, R. D. Blind et al., “Glucocorticoid receptor phosphorylation differentially affects target gene expression,” Molecular Endocrinology, vol. 22, no. 8, pp. 1754–1766, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Y.-L. So, C. Chaivorapol, E. C. Bolton, H. Li, and K. R. Yamamoto, “Determinants of cell- and gene-specific transcriptional regulation by the glucocorticoid receptor,” PLoS Genetics, vol. 3, no. 6, p. e94, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. A. J. Galliher-Beckley, J. G. Williams, and J. A. Cidlowski, “Ligand-independent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling,” Molecular and Cellular Biology, vol. 31, no. 23, pp. 4663–4675, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. T. E. Reddy, F. Pauli, R. O. Sprouse et al., “Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation,” Genome Research, vol. 19, no. 12, pp. 2163–2171, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. S. M. Morillo, P. Escoll, A. de la Hera, and J. M. Frade, “Somatic tetraploidy in specific chick retinal ganglion cells induced by nerve growth factor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 1, pp. 109–114, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Galan, P. Dergham, P. Escoll, A. de-la-Hera et al., “Neuronal injury external to the retina rapidly activates retinal glia, followed by elevation of markers for cell cycle re-entry and death in retinal ganglion cells,” PLoS ONE, vol. 9, no. 7, Article ID e101349, 2014. View at Publisher · View at Google Scholar
  46. M. Kawata, D. Koinuma, T. Ogami et al., “TGF-β-induced epithelial-mesenchymal transition of A549 lung adenocarcinoma cells is enhanced by pro-inflammatory cytokines derived from RAW 264.7 macrophage cells,” Journal of Biochemistry, vol. 151, no. 2, pp. 205–216, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. C. M. Cahill and J. T. Rogers, “Interleukin (IL) 1β induction of IL-6 is mediated by a novel phosphatidylinositol 3-kinase-dependent AKT/IκB kinase α pathway targeting activator protein-1,” The Journal of Biological Chemistry, vol. 283, no. 38, pp. 25900–25912, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Vandevyver, L. Dejager, J. Tuckermann, and C. Libert, “New insights into the anti-inflammatory mechanisms of glucocorticoids: an emerging role for glucocorticoid-receptor-mediated transactivation,” Endocrinology, vol. 154, no. 3, pp. 993–1007, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. P. J. Murray and S. T. Smale, “Restraint of inflammatory signaling by interdependent strata of negative regulatory pathways,” Nature Immunology, vol. 13, no. 10, pp. 916–924, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. V. Picco and G. Pagès, “Linking JNK activity to the DNA damage response,” Genes and Cancer, vol. 4, no. 9-10, pp. 360–368, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. R.-M. Laberge, L. Zhou, M. R. Sarantos et al., “Glucocorticoids suppress selected components of the senescence-associated secretory phenotype,” Aging Cell, vol. 11, no. 4, pp. 569–578, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Pei, L. Li, B. L. Fridley et al., “FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt,” Cancer Cell, vol. 16, no. 3, pp. 259–266, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Romano, M. Mallardo, and M. F. Romano, “FKBP51 and the NF-κB regulatory pathway in cancer,” Current Opinion in Pharmacology, vol. 11, no. 4, pp. 288–293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. C. R. Ross, S. E. Brennan-Laun, and G. M. Wilson, “Tristetraprolin: roles in cancer and senescence,” Ageing Research Reviews, vol. 11, no. 4, pp. 473–484, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. X. Hu, K. Bardhan, A. V. Paschall et al., “Deregulation of apoptotic factors Bcl-xL and Bax confers apoptotic resistance to myeloid-derived suppressor cells and contributes to their persistence in cancer,” The Journal of Biological Chemistry, vol. 288, no. 26, pp. 19103–19115, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Banik, A. N. H. Khan, E. Walseng, B. H. Segal, and S. I. Abrams, “Interferon regulatory factor-8 is important for histone deacetylase inhibitor-mediated antitumor activity,” PLoS ONE, vol. 7, no. 9, Article ID e45422, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Piovan, J. Yu, V. Tosello et al., “Direct reversal of glucocorticoid resistance by AKT inhibition in acute Lymphoblastic leukemia,” Cancer Cell, vol. 24, no. 6, pp. 766–776, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. M. E. Guicciardi and G. J. Gores, “Cell stress gives a red light to the mitochondrial cell death pathway,” Science Signaling, vol. 1, no. 7, article pe9, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. C. A. Gebeshuber, K. Zatloukal, and J. Martinez, “miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis,” EMBO Reports, vol. 10, no. 4, pp. 400–405, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. S. H. Korn, E. F. M. Wouters, G. Wesseling, J.-W. Arends, and F. B. J. M. Thunnissen, “Interaction between glucocorticoids and β2-agonists: α and β glucocorticoid-receptor mrna expression in human bronchial epithelial cells,” Biochemical Pharmacology, vol. 56, no. 12, pp. 1561–1569, 1998. View at Publisher · View at Google Scholar · View at Scopus
  61. P. G. Woodruff, H. A. Boushey, G. M. Dolganov et al., “Genome-wide profiling identifies epithelial cell genes associated with asthma and with treatment response to corticosteroids,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 40, pp. 15858–15863, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Hu, M. B. Josephson, B. L. Diener et al., “Pro-asthmatic cytokines regulate unliganded and ligand-dependent glucocorticoid receptor signaling in airway smooth muscle,” PLoS ONE, vol. 8, no. 4, Article ID e60452, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. H. M. Reichardt, T. Umland, A. Bauer, O. Kretz, and G. Schütz, “Mice with an increased glucocorticoid receptor gene dosage show enhanced resistance to stress and endotoxic shock,” Molecular and Cellular Biology, vol. 20, no. 23, pp. 9009–9017, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. C. A. Nold-Petry, M. F. Nold, J. W. Nielsen et al., “Increased cytokine productionin interleukin-18 receptor α-deficient cells is associated with dysregulation of suppressors of cytokine signaling,” The Journal of Biological Chemistry, vol. 284, no. 38, pp. 25900–25911, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Paakinaho, H. Makkonen, T. Jääskeläinen, and J. J. Palvimo, “Glucocorticoid receptor activates poised FKBP51 locus through long-distance interactions,” Molecular Endocrinology, vol. 24, no. 3, pp. 511–525, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. L. E. Shipp, J. V. Lee, C.-Y. Yu et al., “Transcriptional regulation of human dual specificity protein phosphatase 1 (DUSP1) gene by glucocorticoids,” PLoS ONE, vol. 5, no. 10, Article ID e13754, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. V. Lamarca and L. Scorrano, “When separation means death: killing through the mitochondria, but starting from the endoplasmic reticulum,” The EMBO Journal, vol. 28, no. 12, pp. 1681–1683, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. P. C. Logan, M. D. Mitchell, and P. E. Lobie, “DNA methyltransferases and TETs in the regulation of differentiation and invasiveness of extra-villous trophoblasts,” Frontiers in Genetics, vol. 4, article 265, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Vandevyver, L. Dejager, T. van Bogaert et al., “Glucocorticoid receptor dimerization induces MKP1 to protect against TNF-induced inflammation,” The Journal of Clinical Investigation, vol. 122, no. 6, pp. 2130–2140, 2012. View at Publisher · View at Google Scholar · View at Scopus