Macrophage migration inhibitory factor counterregulates dexamethasone-mediated suppression of hypoxia-inducible factor-1α function and differentially influences human CD4+ T cell proliferation under hypoxia

Journal of Immunology

Volumn 186, Issue 2, 2011, Pages 764-774

  Gaber, Timo ^a,b,c   Schellmann, Saskia ^a,b   Erekul, Kerem B ^a   Fangradt, Monique ^a,b   Tykwinska, Karolina ^a,b   Hahne, Martin ^a,b,c   Maschmeyer, Patrick ^a,b,c   Wagegg, Markus ^a,b,c   Stahn, Cindy ^a,b   Kolar, Paula ^a,b   Dziurla, René ^a   Löhning, Max ^a,b   Burmester, Gerd Rüdiger ^a   Buttgereit, Frank ^a,b,c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b German Rheumatism Research Center   (Germany)

^c Berlin Brandenburg Center for Regenerative Therapies   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; CD74 ANTIGEN; DEXAMETHASONE; GLUCOCORTICOID RECEPTOR ALPHA; GLUCOSE TRANSPORTER 1; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LACTATE DEHYDROGENASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOGLYCERATE KINASE; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; HYPOXIA; INFLAMMATION; LEUKEMIA CELL LINE; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ANOXIA; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; DEXAMETHASONE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOSUPPRESSIVE AGENTS; INTRAMOLECULAR OXIDOREDUCTASES; JURKAT CELLS; MACROPHAGE MIGRATION-INHIBITORY FACTORS; RECEPTORS, GLUCOCORTICOID;

EID: 79251575592     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903421     Document Type: Article

References (37)

1. Gaber, T., R. Dziurla, R. Tripmacher, G. R. Burmester, and F. Buttgereit. 2005. Hypoxia inducible factor (HIF) in rheumatology: low O2! See what HIF can do! Ann. Rheum. Dis. 64: 971-980.
2. Chowdhury, R., A. Hardy, and C. J. Schofield. 2008. The human oxygen sensing machinery and its manipulation. Chem. Soc. Rev. 37: 1308-1319.
3. Bach, J. P., B. Rinn, B. Meyer, R. Dodel, and M. Bacher. 2008. Role of MIF in inflammation and tumorigenesis. Oncology 75: 127-133.
4. Baugh, J. A., M. Gantier, L. Li, A. Byrne, A. Buckley, and S. C. Donnelly. 2006. Dual regulation of macrophage migration inhibitory factor (MIF) expression in hypoxia by CREB and HIF-1. Biochem. Biophys. Res. Commun. 347: 895-903.
5. Larsen, M., S. Tazzyman, E. L. Lund, N. Junker, C. E. Lewis, P. E. Kristjansen, and C. Murdoch. 2008. Hypoxia-induced secretion of macrophage migration-inhibitory factor from MCF-7 breast cancer cells is regulated in a hypoxia-inducible factor-independent manner. Cancer Lett. 265: 239-249.
6. Oda, S., T. Oda, K. Nishi, S. Takabuchi, T. Wakamatsu, T. Tanaka, T. Adachi, K. Fukuda, G. L. Semenza, and K. Hirota. 2008. Macrophage migration inhibitory factor activates hypoxia-inducible factor in a p53-dependent manner. PLoS ONE 3: e2215.
7. Winner, M., A. C. Koong, B. E. Rendon, W. Zundel, and R. A. Mitchell. 2007. Amplification of tumor hypoxic responses by macrophage migration inhibitory factor-dependent hypoxia-inducible factor stabilization. Cancer Res. 67: 186-193.
8. Löwenberg, M., C. Stahn, D. W. Hommes, and F. Buttgereit. 2008. Novel insights into mechanisms of glucocorticoid action and the development of new glucocorticoid receptor ligands. Steroids 73: 1025-1029.
9. Stahn, C., and F. Buttgereit. 2008. Genomic and nongenomic effects of glucocorticoids. Nat. Clin. Pract. Rheumatol. 4: 525-533.
10. Kim, H. H., S. E. Lee, W. J. Chung, Y. Choi, K. Kwack, S. W. Kim, M. S. Kim, H. Park, and Z. H. Lee. 2002. Stabilization of hypoxia-inducible factor-1alpha is involved in the hypoxic stimuli-induced expression of vascular endothelial growth factor in osteoblastic cells. Cytokine 17: 14-27.
11. Kodama, T., N. Shimizu, N. Yoshikawa, Y. Makino, R. Ouchida, K. Okamoto, T. Hisada, H. Nakamura, C. Morimoto, and H. Tanaka. 2003. Role of the glucocorticoid receptor for regulation of hypoxia-dependent gene expression. J. Biol. Chem. 278: 33384-33391.
12. Wagner, A. E., G. Huck, D. P. Stiehl, W. Jelkmann, and T. Hellwig-Bürgel. 2008. Dexamethasone impairs hypoxia-inducible factor-1 function. Biochem. Biophys. Res. Commun. 372: 336-340.
13. Mace, K. A., D. H. Yu, K. Z. Paydar, N. Boudreau, and D. M. Young. 2007. Sustained expression of Hif-1alpha in the diabetic environment promotes angiogenesis and cutaneous wound repair. Wound Repair Regen. 15: 636-645.
14. Tripmacher, R., T. Gaber, R. Dziurla, T. Häupl, K. Erekul, A. Grützkau, M. Tschirschmann, A. Scheffold, A. Radbruch, G. R. Burmester, and F. Buttgereit. 2008. Human CD4(+) T cells maintain specific functions even under conditions of extremely restricted ATP production. Eur. J. Immunol. 38: 1631-1642.
15. Sander, B., J. Andersson, and U. Andersson. 1991. Assessment of cytokines by immunofluorescence and the paraformaldehyde-saponin procedure. Immunol. Rev. 119: 65-93.
16. Rubinson, D. A., C. P. Dillon, A. V. Kwiatkowski, C. Sievers, L. Yang, J. Kopinja, D. L. Rooney, M. Zhang, M. M. Ihrig, M. T. McManus, et al. 2003. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. [Published erratum appears in 2007 Nat Genet. 39: 803; 2003 Nat Genet. 34: 231] Nat. Genet. 33: 401-406.
17. Elsby, L. M., R. Donn, Z. Alourfi, L. M. Green, E. Beaulieu, and D. W. Ray. 2009. Hypoxia and glucocorticoid signaling converge to regulate macrophage migration inhibitory factor gene expression. Arthritis Rheum. 60: 2220-2231.
18. Leng, L., C. N. Metz, Y. Fang, J. Xu, S. Donnelly, J. Baugh, T. Delohery, Y. Chen, R. A. Mitchell, and R. Bucala. 2003. MIF signal transduction initiated by binding to CD74. J. Exp. Med. 197: 1467-1476.
19. Nakamura, H., Y. Makino, K. Okamoto, L. Poellinger, K. Ohnuma, C. Morimoto, and H. Tanaka. 2005. TCR engagement increases hypoxia-inducible factor-1 alpha protein synthesis via rapamycin-sensitive pathway under hypoxic conditions in human peripheral T cells. J. Immunol. 174: 7592-7599. (Pubitemid 40806263)
20. Amin, M. A., O. V. Volpert, J. M. Woods, P. Kumar, L. A. Harlow, and A. E. Koch. 2003. Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ. Res. 93: 321-329.
21. Bacher, M., C. N. Metz, T. Calandra, K. Mayer, J. Chesney, M. Lohoff, D. Gemsa, T. Donnelly, and R. Bucala. 1996. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc. Natl. Acad. Sci. USA 93: 7849-7854.
22. Makino, Y., H. Nakamura, E. Ikeda, K. Ohnuma, K. Yamauchi, Y. Yabe, L. Poellinger, Y. Okada, C. Morimoto, and H. Tanaka. 2003. Hypoxia-inducible factor regulates survival of antigen receptor-driven T cells. J. Immunol. 171: 6534-6540.
23. Gaber, T., T. Häupl, G. Sandig, K. Tykwinska, M. Fangradt, M. Tschirschmann, M. Hahne, R. Dziurla, K. Erekul, M. Lautenbach, et al. 2009. Adaptation of human CD4+ T cells to pathophysiological hypoxia: a transcriptome analysis. J. Rheumatol. 36: 2655-2669.
24. Atkuri, K. R., L. A. Herzenberg, A. K. Niemi, T. Cowan, and L. A. Herzenberg. 2007. Importance of culturing primary lymphocytes at physiological oxygen levels. Proc. Natl. Acad. Sci. USA 104: 4547-4552.
25. Kondo, N., Y. Ishii, A. Son, J. Sakakura-Nishiyama, Y. W. Kwon, M. Tanito, Y. Nishinaka, Y. Matsuo, T. Nakayama, M. Taniguchi, and J. Yodoi. 2004. Cysteine-dependent immune regulation by TRX and MIF/GIF family proteins. Immunol. Lett. 92: 143-147.
26. Kim-Saijo, M., E. M. Janssen, and K. Sugie. 2008. CD4 cell-secreted, posttranslationally modified cytokine GIF suppresses Th2 responses by inhibiting the initiation of IL-4 production. Proc. Natl. Acad. Sci. USA 105: 19402-19407.
27. Watarai, H., R. Nozawa, A. Tokunaga, N. Yuyama, M. Tomas, A. Hinohara, K. Ishizaka, and Y. Ishii. 2000. Posttranslational modification of the glycosylation inhibiting factor (GIF) gene product generates bioactive GIF. Proc. Natl. Acad. Sci. USA 97: 13251-13256.
28. Galat, A., S. Rivière, F. Bouet, and A. Ménez. 1994. A diversified family of 12-kDa proteins with a high amino acid sequence similarity to macrophage migration-inhibitory factor (MIF). Eur. J. Biochem. 224: 417-421.
29. Ghezzi, P. 2005. Oxidoreduction of protein thiols in redox regulation. Biochem. Soc. Trans. 33: 1378-1381.
30. Yan, X., R. J. Orentas, and B. D. Johnson. 2006. Tumor-derived macrophage migration inhibitory factor (MIF) inhibits T lymphocyte activation. Cytokine 33: 188-198.
31. Thiel, M., C. C. Caldwell, S. Kreth, S. Kuboki, P. Chen, P. Smith, A. Ohta, A. B. Lentsch, D. Lukashev, and M. V. Sitkovsky. 2007. Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS ONE 2: e853.
32. Zhou, Q., X. Yan, J. Gershan, R. J. Orentas, and B. D. Johnson. 2008. Expression of macrophage migration inhibitory factor by neuroblastoma leads to the inhibition of antitumor T cell reactivity in vivo. J. Immunol. 181: 1877-1886.
33. Ohta, A., E. Gorelik, S. J. Prasad, F. Ronchese, D. Lukashev, M. K. Wong, X. Huang, S. Caldwell, K. Liu, P. Smith, et al. 2006. A2A adenosine receptor protects tumors from antitumor T cells. Proc. Natl. Acad. Sci. USA 103: 13132-13137.
34. Löwenberg, M., J. Tuynman, J. Bilderbeek, T. Gaber, F. Buttgereit, S. van Deventer, M. Peppelenbosch, and D. Hommes. 2005. Rapid immunosuppressive effects of glucocorticoids mediated through Lck and Fyn. Blood 106: 1703-1710. (Pubitemid 41208584)
35. del Peso, L., M. C. Castellanos, E. Temes, S. Martin-Puig, Y. Cuevas, G. Olmos, and M. O. Landazuri. 2003. The von Hippel Lindau/hypoxia-inducible factor (HIF) pathway regulates the transcription of the HIF-proline hydroxylase genes in response to low oxygen. J. Biol. Chem. 278: 48690-48695.
36. Leng, L., W. Wang, T. Roger, M. Merk, M. Wuttke, T. Calandra, and R. Bucala. 2009. Glucocorticoid-induced MIF expression by human CEM T cells. Cytokine 48: 177-185.
37. Calandra, T., J. Bernhagen, C. N. Metz, L. A. Spiegel, M. Bacher, T. Donnelly, A. Cerami, and R. Bucala. 1995. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377: 68-71.