GILZ overexpression inhibits endothelial cell adhesive function through regulation of NF-κB and MAPK activity

Journal of Immunology

Volumn 191, Issue 1, 2013, Pages 424-433

  Cheng, Qiang ^a   Fan, Huapeng ^a   Ngo, Devi ^a   Beaulieu, Elaine ^a   Leung, Patrick ^a   Lo, Camden Y ^a   Burgess, Rosemary ^a   Van Der Zwan, Yvonne G ^b   White, Stefan J ^b   Khachigian, Levon M ^c   Hickey, Michael J ^a   Morand, Eric F ^a  

^a MONASH UNIVERSITY   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GLUCOCORTICOID; GLUCOCORTICOID INDUCED LEUCINE ZIPPER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; LEUCINE ZIPPER PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MKP 1 PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATASE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CCL2 GENE; CELL ADHESION; CELL NUCLEUS; CONTROLLED STUDY; CXCL8 GENE; DNA BINDING; E SELECTIN GENE; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; GILZ GENE; HUMAN; HUMAN CELL; ICAM 1 GENE; IL 6 GENE; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; LEUKOCYTE ROLLING; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VCAM 1 GENE;

CELL ADHESION; CELL COMMUNICATION; CELL LINE; CELL MIGRATION INHIBITION; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LEUKOCYTES; MAP KINASE SIGNALING SYSTEM; MICROCIRCULATION; PRIMARY CELL CULTURE; RANDOM ALLOCATION; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84879677675     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202662     Document Type: Article

References (47)

1. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689. (Pubitemid 47327397)
2. Muller, W. A. 2002. Leukocyte-endothelial cell interactions in the inflammatory response. Lab. Invest. 82: 521-533. (Pubitemid 34522364)
3. Petri, B., M. Phillipson, and P. Kubes. 2008. The physiology of leukocyte recruitment: an in vivo perspective. J. Immunol. 180: 6439-6446.
4. Gamble, J. R., Y. Khew-Goodall, and M. A. Vadas. 1993. Transforming growth factor-beta inhibits E-selectin expression on human endothelial cells. J. Immunol. 150: 4494-4503. (Pubitemid 23133726)
5. Kubes, P., M. Suzuki, and D. N. Granger. 1991. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA 88: 4651-4655. (Pubitemid 21914599)
6. Hickey, M. J., A. C. Issekutz, P. H. Reinhardt, R. N. Fedorak, and P. Kubes. 1998. Endogenous interleukin-10 regulates hemodynamic parameters, leukocyte-endothelial cell interactions, and microvascular permeability during endotoxemia. Circ. Res. 83: 1124-1131. (Pubitemid 28533521)
7. D'Adamio, F., O. Zollo, R. Moraca, E. Ayroldi, S. Bruscoli, A. Bartoli, L. Cannarile, G. Migliorati, and C. Riccardi. 1997. A new dexamethasone-induced gene of the leucine zipper family protects T lymphocytes from TCR/ CD3-activated cell death. Immunity 7: 803-812. (Pubitemid 28064893)
8. Ayroldi, E., G. Migliorati, S. Bruscoli, C. Marchetti, O. Zollo, L. Cannarile, F. D'Adamio, and C. Riccardi. 2001. Modulation of T-cell activation by the glucocorticoid-induced leucine zipper factor via inhibition of nuclear factor kappaB. Blood 98: 743-753.
9. Di Marco, B., M. Massetti, S. Bruscoli, A. Macchiarulo, R. Di Virgilio, E. Velardi, V. Donato, G. Migliorati, and C. Riccardi. 2007. Glucocorticoid-induced leucine zipper (GILZ)/NF-kappaB interaction: role of GILZ homodimerization and C-terminal domain. Nucleic Acids Res. 35: 517-528. (Pubitemid 46232068)
10. Delfino, D. V., M. Agostini, S. Spinicelli, C. Vacca, and C. Riccardi. 2006. Inhibited cell death, NF-kappaB activity and increased IL-10 in TCR-triggered thymocytes of transgenic mice overexpressing the glucocorticoid-induced protein GILZ. Int. Immunopharmacol. 6: 1126-1134. (Pubitemid 43728169)
11. Srinivasan, M., and S. Janardhanam. 2011. Novel p65 binding glucocorticoid-induced leucine zipper peptide suppresses experimental autoimmune encephalomyelitis. J. Biol. Chem. 286: 44799-44810.
12. Mittelstadt, P. R., and J. D. Ashwell. 2001. Inhibition of AP-1 by the glucocorticoid-inducible protein GILZ. J. Biol. Chem. 276: 29603-29610.
13. Ayroldi, E., O. Zollo, A. Bastianelli, C. Marchetti, M. Agostini, R. Di Virgilio, and C. Riccardi. 2007. GILZ mediates the antiproliferative activity of glucocorticoids by negative regulation of Ras signaling. J. Clin. Invest. 117: 1605-1615. (Pubitemid 46871345)
14. Ayroldi, E., O. Zollo, A. Macchiarulo, B. Di Marco, C. Marchetti, and C. Riccardi. 2002. Glucocorticoid-induced leucine zipper inhibits the Raf-extracellular signal-regulated kinase pathway by binding to Raf-1. Mol. Cell. Biol. 22: 7929-7941. (Pubitemid 35217302)
15. Beaulieu, E., D. Ngo, L. Santos, Y. H. Yang, M. Smith, C. Jorgensen, V. Escriou, D. Scherman, G. Courties, F. Apparailly, and E. F. Morand. 2010. Glucocorticoid-induced leucine zipper is an endogenous antiinflammatory mediator in arthritis. Arthritis Rheum. 62: 2651-2661.
16. Cheng, Q., S. J. McKeown, L. Santos, F. S. Santiago, L. M. Khachigian, E. F. Morand, and M. J. Hickey. 2010. Macrophage migration inhibitory factor increases leukocyte-endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules. J. Immunol. 185: 1238-1247.
17. Zhang, G., C. R. Dass, E. Sumithran, N. Di Girolamo, L. Q. Sun, and L. M. Khachigian. 2004. Effect of deoxyribozymes targeting c-Jun on solid tumor growth and angiogenesis in rodents. J. Natl. Cancer Inst. 96: 683-696. (Pubitemid 38660231)
18. Santos, L. L., H. Fan, P. Hall, D. Ngo, C. R. Mackay, G. Fingerle-Rowson, R. Bucala, M. J. Hickey, and E. F. Morand. 2011. Macrophage migration inhibitory factor regulates neutrophil chemotactic responses in inflammatory arthritis in mice. Arthritis Rheum. 63: 960-970.
19. Cuvelier, S. L., and K. D. Patel. 2005. Studying leukocyte rolling and adhesion in vitro under flow conditions. Methods Mol. Biol. 290: 331-342.
20. Li, J. H., N. C. Kirkiles-Smith, J. M. McNiff, and J. S. Pober. 2003. TRAIL induces apoptosis and inflammatory gene expression in human endothelial cells. J. Immunol. 171: 1526-1533. (Pubitemid 36900088)
21. Adriaansen, J., S. W. Tas, P. L. Klarenbeek, A. C. Bakker, F. Apparailly, G. S. Firestein, C. Jorgensen, M. J. Vervoordeldonk, and P. P. Tak. 2005. Enhanced gene transfer to arthritic joints using adeno-associated virus type 5: implications for intra-articular gene therapy. Ann. Rheum. Dis. 64: 1677-1684. (Pubitemid 41667139)
22. Hamdi, H., A. Bigorgne, S. Naveau, A. Balian, L. Bouchet-Delbos, A.M. Cassard-Doulcier, M. C. Maillot, I. Durand-Gasselin, S. Prévot, J. Delaveaucoupet, et al. 2007. Glucocorticoid-induced leucine zipper: A key protein in the sensitization of monocytes to lipopolysaccharide in alcoholic hepatitis. Hepatology 46: 1986-1992.
23. Ghosh, S., and M. S. Hayden. 2008. New regulators of NF-kappaB in inflammation. Nat. Rev. Immunol. 8: 837-848.
24. Kuldo, J. M., J. Westra, S. A. Asgeirsdóttir, R. J. Kok, K. Oosterhuis, M. G. Rots, J. P. Schouten, P. C. Limburg, and G. Molema. 2005. Differential effects of NF-kappaB and p38 MAPK inhibitors and combinations thereof on TNF-alpha- and IL-1beta-induced proinflammatory status of endothelial cells in vitro. Am. J. Physiol. Cell Physiol. 289: C1229-C1239. (Pubitemid 41456839)
25. Jeffrey, K. L., M. Camps, C. Rommel, and C. R. Mackay. 2007. Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat. Rev. Drug Discov. 6: 391-403. (Pubitemid 46705202)
26. Fürst, R., T. Schroeder, H. M. Eilken, M. F. Bubik, A. K. Kiemer, S. Zahler, and A. M. Vollmar. 2007. MAPK phosphatase-1 represents a novel anti-inflammatory target of glucocorticoids in the human endothelium. FASEB J. 21: 74-80.
27. Zakkar, M., H. Chaudhury, G. Sandvik, K. Enesa, A. Luong, S. Cuhlmann, J. C. Mason, R. Krams, A. R. Clark, D. O. Haskard, and P. C. Evans. 2008. Increased endothelial mitogen-activated protein kinase phosphatase-1 expression suppresses proinflammatory activation at sites that are resistant to atherosclerosis. Circ. Res. 103: 726-732.
28. Ayroldi, E., and C. Riccardi. 2009. Glucocorticoid-induced leucine zipper (GILZ): a new important mediator of glucocorticoid action. FASEB J. 23: 3649-3658.
29. Berrebi, D., S. Bruscoli, N. Cohen, A. Foussat, G. Migliorati, L. Bouchet- Delbos, M. C. Maillot, A. Portier, J. Couderc, P. Galanaud, et al. 2003. Synthesis of glucocorticoid-induced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10. Blood 101: 729-738. (Pubitemid 36077600)
30. Cohen, N., E. Mouly, H. Hamdi, M. C. Maillot, M. Pallardy, V. Godot, F. Capel, A. Balian, S. Naveau, P. Galanaud, et al. 2006. GILZ expression in human dendritic cells redirects their maturation and prevents antigen-specific T lymphocyte response. Blood 107: 2037-2044. (Pubitemid 43289388)
31. Yang, N., W. Zhang, and X. M. Shi. 2008. Glucocorticoid-induced leucine zipper (GILZ) mediates glucocorticoid action and inhibits inflammatory cytokine-induced COX-2 expression. J. Cell. Biochem. 103: 1760-1771. (Pubitemid 351501908)
32. Vallabhapurapu, S., and M. Karin. 2009. Regulation and function of NF-kappaB transcription factors in the immune system. Annu. Rev. Immunol. 27: 693-733.
33. Denk, A., M. Goebeler, S. Schmid, I. Berberich, O. Ritz, D. Lindemann, S. Ludwig, and T. Wirth. 2001. Activation of NF-kappa B via the Ikappa B kinase complex is both essential and sufficient for proinflammatory gene expression in primary endothelial cells. J. Biol. Chem. 276: 28451-28458.
34. Montgomery, K. F., L. Osborn, C. Hession, R. Tizard, D. Goff, C. Vassallo, P. I. Tarr, K. Bomsztyk, R. Lobb, J. M. Harlan, et al. 1991. Activation of endothelial-leukocyte adhesion molecule 1 (ELAM-1) gene transcription. Proc. Natl. Acad. Sci. USA 88: 6523-6527. (Pubitemid 21914979)
35. Iademarco, M. F., J. J. McQuillan, and D. C. Dean. 1993. Vascular cell adhesion molecule 1: contrasting transcriptional control mechanisms in muscle and endothelium. Proc. Natl. Acad. Sci. USA 90: 3943-3947. (Pubitemid 23134142)
36. Viatour, P., M. P. Merville, V. Bours, and A. Chariot. 2005. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30: 43-52. (Pubitemid 40093740)
37. Chen, L. F., and W. C. Greene. 2004. Shaping the nuclear action of NF-kappaB. Nat. Rev. Mol. Cell Biol. 5: 392-401.
38. Gupta, S. C., C. Sundaram, S. Reuter, and B. B. Aggarwal. 2010. Inhibiting NF-κB activation by small molecules as a therapeutic strategy. Biochim. Biophys. Acta 1799: 775-787.
39. Seldon, M. P., G. Silva, N. Pejanovic, R. Larsen, I. P. Gregoire, J. Filipe, J. Anrather, and M. P. Soares. 2007. Heme oxygenase-1 inhibits the expression of adhesion molecules associated with endothelial cell activation via inhibition of NF-kappaB RelA phosphorylation at serine 276. J. Immunol. 179: 7840-7851.
40. Buss, H., A. Dörrie, M. L. Schmitz, R. Frank, M. Livingstone, K. Resch, and M. Kracht. 2004. Phosphorylation of serine 468 by GSK-3beta negatively regulates basal p65 NF-kappaB activity. J. Biol. Chem. 279: 49571-49574.
41. Lou, X., S. Sun, W. Chen, Y. Zhou, Y. Huang, X. Liu, Y. Shan, and C. Wang. 2011. Negative feedback regulation of NF-kB action by CITED2 in the nucleus. J. Immunol. 186: 539-548.
42. Lee, J. Y., J. H. Je, K. J. Jung, B. P. Yu, and H. Y. Chung. 2004. Induction of endothelial iNOS by 4-hydroxyhexenal through NF-kappaB activation. Free Radic. Biol. Med. 37: 539-548. (Pubitemid 38901086)
43. Bueno, O. F., L. J. De Windt, H. W. Lim, K. M. Tymitz, S. A. Witt, T. R. Kimball, and J. D. Molkentin. 2001. The dual-specificity phosphatase MKP-1 limits the cardiac hypertrophic response in vitro and in vivo. Circ. Res. 88: 88-96. (Pubitemid 32064088)
44. Whitehurst, C. E., and T. D. Geppert. 1996. MEK1 and the extracellular signal-regulated kinases are required for the stimulation of IL-2 gene transcription in T cells. J. Immunol. 156: 1020-1029. (Pubitemid 26048095)
45. Hsu, Y. F., J. R. Sheu, C. H. Lin, W. C. Chen, G. Hsiao, G. Ou, P. T. Chiu, and M. J. Hsu. 2011. MAPK phosphatase-1 contributes to trichostatin A inhibition of cyclooxygenase-2 expression in human umbilical vascular endothelial cells exposed to lipopolysaccharide. Biochim. Biophys. Acta 1810: 1160-1169.
46. King, E. M., N. S. Holden, W. Gong, C. F. Rider, and R. Newton. 2009. Inhibition of NF-kappaB-dependent transcription by MKP-1: transcriptional repression by glucocorticoids occurring via p38 MAPK. J. Biol. Chem. 284: 26803-26815.
47. Ngo, D., E. Beaulieu, R. Gu, A. Leaney, L. Santos, H. Fan, Y. Yang, W. Kao, J. Xu, V. Escriou, et al. 2013. Divergent effects of endogenous and exogenous glucocorticoid-induced leucine zipper in animal models of inflammation and arthritis. Arthritis Rheum. 65: 1203-1212.