Macrophage migration inhibitory factor promotes innate immune responses by suppressing glucocorticoid-induced expression of mitogen-activated protein kinase phosphatase-1
Abstract
The pro-inflammatory cytokine macrophage migration inhibitory factor (MIF) acts as a physiological counter-regulator of the immuno-suppressive effects of glucocorticoids. However, the mechanisms whereby MIF exerts its counter-balancing effect remain largely unknown. Here we report that MAPK phosphatase 1 (MKP-1), an archetypal member of dual specificity phosphatase that inactivates MAPK activity in response to pro-inflammatory stimuli, is a critical target of MIF-glucocorticoid crosstalk. Recombinant MIF counter-regulated in a dose-dependent fashion dexamethasone inhibition of TNF and IL-8 production by RAW 264.7 macrophages and U-937 promonocytes stimulated with lipopolysaccharides (LPS) or with LPS plus phorbol 12-myristate 13-acetate. Stimulation of RAW 264.7 macrophages with dexamethasone or dexamethasone plus LPS led to a robust up-regulation of MKP-1 mRNA and protein expressions that were counter-regulated by addition of recombinant MIF. Antisense MIF macrophages expressing reduced levels of endogenous MIF produced higher amount of MKP-1 and lower amount of TNF after exposure to dexamethasone and dexamethasone plus LPS, indicating that endogenous MIF acts in an autocrine fashion to override glucocorticoid-induced MKP-1 expression and inhibition of cytokine production. Taken together, these data identify MKP-1 as a molecular target of MIF-glucocorticoid crosstalk and provide a molecular basis for the control of macrophage responses by a pair of physiological regulators of innate immunity.
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Acute glucocorticoid exposure induces sustained expression of MKP-1 in a variety of cells including macrophages.
“Acute GC exposure induces sustained expression of MKP-1 in a variety of cells including macrophages (Roger et al., 2005).”
From The Stressed CNS: When Glucocorticoids Aggravate Inflammation (2009) · cites this paper as Roger et al., 2005
Cites
Janeway, C. A., & Medzhitov, R. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.083001.084359 · Cited by 8,394 · see citing works
Akira, S., & Takeda, K. (2004) · Nature reviews. Immunology · doi:10.1038/nri1391 · Cited by 8,312 · see citing works
Defective LPS Signaling in C3H/HeJ and C57BL/10ScCr Mice: Mutations in <i>Tlr4</i> Gene
Poltorak, A., He, X., Smirnova, I., Liu, M.-Y., Huffel, C. V., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., et al. (1998) · Science · doi:10.1126/science.282.5396.2085 · Cited by 7,631 · see citing works
NF-κB regulation in the immune system
Li, Q., & Verma, I. M. (2002) · Nature Reviews Immunology · doi:10.1038/nri910 · Cited by 4,007 · see citing works
Annane, D. (2002) · JAMA · doi:10.1001/jama.288.7.862 · Cited by 3,055 · see citing works
Auphan, N., DiDonato, J. A., Rosette, C., Helmberg, A., & Karin, M. (1995) · Science · doi:10.1126/science.270.5234.286 · Cited by 2,390 · see citing works
Macrophage migration inhibitory factor: a regulator of innate immunity
Calandra, T., & Roger, T. (2003) · Nature reviews. Immunology · doi:10.1038/nri1200 · Cited by 1,782 · see citing works
Detection of circulating tumor necrosis factor after endotoxin administration
Michie, H. R., Manogue, K. R., Spriggs, D. R., Revhaug, A., O'Dwyer, S., Dinarello, C. A., Cerami, A., Wolff, S. M., & Wilmore, D. W. (1988) · New England Journal of Medicine · doi:10.1056/nejm198806093182301 · Cited by 1,677 · see citing works
Role of Transcriptional Activation of IκBα in Mediation of Immunosuppression by Glucocorticoids
Scheinman, R. I., Cogswell, P. C., Lofquist, A. K., & Baldwin, A. S. (1995) · Science · doi:10.1126/science.270.5234.283 · Cited by 1,676 · see citing works
Akira, S. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.r300028200 · Cited by 1,486 · see citing works
Inferences, questions and possibilities in Toll-like receptor signalling
Beutler, B. (2004) · Nature · doi:10.1038/nature02761 · Cited by 1,458 · see citing works
Sun, H., Charles, C. H., Lau, L. F., & Tonks, N. K. (1993) · Cell · doi:10.1016/0092-8674(93)90383-2 · Cited by 1,156 · see citing works
MIF as a glucocorticoid-induced modulator of cytokine production
Calandra, T., Bernhagen, J., Metz, C. N., Spiegel, L. A., Bacher, M., Donnelly, T. M., Cerami, A., & Bucala, R. (1995) · Nature · doi:10.1038/377068a0 · Cited by 1,148 · see citing works
Waage, A., Halstensen, A. I., & Espevik, T. (1987) · The Lancet · doi:10.1016/s0140-6736(87)91728-4 · Cited by 1,085 · see citing works
MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia
Bernhagen, J., Calandra, T., Mitchell, R. A., Martin, S. B., Tracey, K. J., Voelter, W., Manogue, K. R., Cerami, A., & Bucala, R. (1993) · Nature · doi:10.1038/365756a0 · Cited by 1,001 · see citing works
Calandra, T., Bernhagen, J., Mitchell, R. A., & Bucala, R. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.179.6.1895 · Cited by 984 · see citing works
Neuroendocrine Regulation of Immunity
Webster, J. I., Tonelli, L., & Sternberg, E. M. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.082401.104914 · Cited by 957 · see citing works
Dual specificity phosphatases: a gene family for control of MAP kinase function
Camps, M., NICHOLS, A., & Arkinstall, S. (2000) · The FASEB Journal · doi:10.1096/fasebj.14.1.6 · Cited by 812 · see citing works
Tumor Necrosis Factor and Interleuktn-1 in the Serum of Children with Severe Infectious Purpura
Girardin, E. P., Grau, G. E., Dayer, J., Roux-Lombard, P., the J5 Study Group*, & Lambert, P.-H. (1988) · New England Journal of Medicine · doi:10.1056/nejm198808183190703 · Cited by 737 · see citing works
Protection from septic shock by neutralization of macrophage migration inhibitory factor
Calandra, T., Echtenacher, B., Roy, D. L., Pugin, J., Metz, C. N., Hültner, L., Heumann, D., Männel, D. N., Bucala, R., & Glauser, M. P. (2000) · Nature Medicine · doi:10.1038/72262 · Cited by 724 · see citing works
MIF regulates innate immune responses through modulation of Toll-like receptor 4
Roger, T., David, J. R., Glauser, M. P., & Calandra, T. (2001) · Nature · doi:10.1038/414920a · Cited by 584 · see citing works
Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1
Kleemann, R., Haußer, A., Geiger, G., Mischke, R., Burger‐Kentischer, A., Flieger, O., Johannes, F., Roger, T., Calandra, T., Kapurniotu, A., et al. (2000) · Nature · doi:10.1038/35041591 · Cited by 567 · see citing works
Mitchell, R. A., Liao, H., Chesney, J., Fingerle-Rowson, G., Baugh, J., David, J., & Bucala, R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012511599 · Cited by 514 · see citing works
Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP‐1
Kassel, O., Sancono, A., Krätzschmar, J., Kreft, B., Stassen, M., & Cato, A. C. B. (2001) · The EMBO Journal · doi:10.1093/emboj/20.24.7108 · Cited by 478 · see citing works
Mitchell, R. A., Metz, C. N., Peng, T., & Bucala, R. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.25.18100 · Cited by 448 · see citing works
Molecular mechanisms of glucocorticoid action and resistance
Schaaf, M. J. M., & Cidlowski, J. A. (2002) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(02)00263-7 · Cited by 417 · see citing works
Cortisol response to corticotropin and survival in septic shock
Rothwell, P. M. (1991) · The Lancet · doi:10.1016/0140-6736(91)91641-7 · Cited by 416 · see citing works
Lasa, M., Mahtani, K. R., Finch, A. J., Brewer, G., Saklatvala, J., & Clark, A. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.12.4265-4274.2000 · Cited by 413 · see citing works
Bernhagen, J., Mitchell, R. A., Calandra, T., Voelter, W., Cerami, A., & Bucala, R. (1994) · Biochemistry · doi:10.1021/bi00251a025 · Cited by 409 · see citing works
Lasa, M., Abraham, S., Boucheron, C., Saklatvala, J., & Clark, A. R. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.22.7802-7811.2002 · Cited by 381 · see citing works
Theodosiou, A. M., & Ashworth, A. (2002) · Genome biology · doi:10.1186/gb-2002-3-7-reviews3009 · Cited by 321 · see citing works
Post‐transcriptional regulation of gene expression by degradation of messenger RNAs
Bevilacqua, A., Ceriani, M. C., Capaccioli, S., & Nicolin, A. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10272 · Cited by 316 · see citing works
Chen, P., Li, J., Barnes, J., Kokkonen, G. C., Lee, J. C., & Liu, Y. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.11.6408 · Cited by 285 · see citing works
Migration inhibitory factor expression in experimentally induced endotoxemia.
Bacher, M., Meinhardt, A., Lan, H. Y., Mu, W., Metz, C. N., Chesney, J. A., Calandra, T., Gemsa, D., Donnelly, T., Atkins, R. C., et al. (1997) · Europe PMC (PubMed Central) · Cited by 281 · see citing works
Calandra, T., Spiegel, L. A., Metz, C. N., & Bucala, R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.19.11383 · Cited by 235 · see citing works
Charles, C. H., Abler, A. S., & Lau, L. F. (1992) · PubMed · Cited by 233 · see citing works
Zhang, T., Kruys, V., Huez, G. A., & Gueydan, C. (2002) · Biochemical Society Transactions · doi:10.1042/bst0300952 · Cited by 216 · see citing works
Zhao, Q., Shepherd, E. G., Manson, M. E., Nelin, L. D., Sorokin, A., & Liu, Y. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m411760200 · Cited by 207 · see citing works
The growth factor-inducible immediate-early gene 3CH134 encodes a protein-tyrosine-phosphatase.
Charles, C. H., Sun, H., Lau, L. F., & Tonks, N. K. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.11.5292 · Cited by 192 · see citing works
Nishino, T., Bernhagen, J., Shiiki, H., Calandra, T., Dohi, K., & Bucala, R. (1995) · Molecular Medicine · doi:10.1007/bf03401892 · Cited by 182 · see citing works
Hermoso, M. A., Matsuguchi, T., Smoak, K. A., & Cidlowski, J. A. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.11.4743-4756.2004 · Cited by 177 · see citing works
Engelbrecht, Y., de Wet, H., Horsch, K., Langeveldt, C., Hough, F. S., & Hulley, P. A. (2003) · Endocrinology · doi:10.1210/en.2002-220769 · Cited by 151 · see citing works
Beishuizen, A., THIJS, L. G., Haanen, C., & Vermes, I. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7570 · Cited by 145 · see citing works
Shepherd, E. G., Zhao, Q., Welty, S. E., Hansen, T. N., Smith, C. V., & Liu, Y. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408444200 · Cited by 111 · see citing works
Daun, J. M., & Cannon, J. G. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.3.r1043 · Cited by 111 · see citing works
Roger, T., Miconnet, I., SCHIESSER, A.-L., Kai, H., Miyake, K., & Calandra, T. (2005) · Biochemical Journal · doi:10.1042/bj20041243 · Cited by 79 · see citing works
Mitogen activated protein kinases as targets for development of novel anti-inflammatory drugs
Karin, M. (2004) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2004.028274 · Cited by 65 · see citing works
THE INFLUENCE OF THE ADRENAL GLANDS ON RESISTANCE
SCOTT, W. J. M. (1924) · The Journal of Experimental Medicine · doi:10.1084/jem.39.3.457 · Cited by 21 · see citing works
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Schulte, W., Bernhagen, J., & Bucala, R. (2013) · Mediators of Inflammation · doi:10.1155/2013/165974 · Cited by 745 · see citing works
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Liu, Y., Shepherd, E. G., & Nelin, L. D. (2007) · Nature reviews. Immunology · doi:10.1038/nri2035 · Cited by 679 · see citing works
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Roger, T., Lugrin, J., Le Roy, D., Goy, G., Mombelli, M., Koessler, T., Ding, X. C., Chanson, A.-L., Reymond, M. K., Miconnet, I., et al. (2011) · Blood · doi:10.1182/blood-2010-05-284711 · Cited by 341 · see citing works
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Barnes, P. J. (2010) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2010.02.018 · Cited by 317 · see citing works
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Quax, R. A., Manenschijn, L., Koper, J. W., Hazes, J. M., Lamberts, S. W. J., van Rossum, E. F. C., & Feelders, R. A. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.183 · Cited by 310 · see citing works
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Wang, C., Zhou, J., Wang, J., Li, S., Fukunaga, A., Yodoi, J., & Tian, H. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00345-x · Cited by 311 · see citing works
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Roger, T., Froidevaux, C., Roy, D. L., Reymond, M. K., Chanson, A.-L., Mauri, D., Burns, K., Riederer, B. M., Akira, S., & Calandra, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808146106 · Cited by 267 · see citing works
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Wancket, L. M., Frazier, W. J., & Liu, Y. (2011) · Life Sciences · doi:10.1016/j.lfs.2011.11.017 · Cited by 134 · see citing works
Giannoni, É., Guignard, L., Reymond, M. K., Perreau, M., Roth‐Kleiner, M., Calandra, T., & Roger, T. (2011) · Infection and Immunity · doi:10.1128/iai.00076-11 · Cited by 135 · see citing works
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Park, H., Kam, T., Peng, H., Chou, S.-C., Mehrabani-Tabari, A. A., Song, J., Yin, X., Karuppagounder, S. S., Umanah, G. K. E., Rao, A., et al. (2022) · Cell · doi:10.1016/j.cell.2022.04.020 · Cited by 125 · see citing works
Das, R., Koo, M.-S., Kim, B.-H., Jacob, S. T., Subbian, S., Yao, J., Leng, L., Levy, R., Murchison, C., Burman, W. J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301128110 · Cited by 121 · see citing works
Zhou, Y., Ling, E., & Dheen, S. T. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04535.x · Cited by 115 · see citing works
Fan, H., Hall, P., Santos, L. L., Gregory, J. L., Fingerle‐Rowson, G., Bucala, R., Morand, E. F., & Hickey, M. J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003713 · Cited by 111 · see citing works
Cheng, Q., McKeown, S. J., Santos, L. L., Santiago, F. S., Khachigian, L. M., Morand, E. F., & Hickey, M. J. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0904104 · Cited by 110 · see citing works
MIF as a Disease Target: ISO-1 as a Proof-of-Concept Therapeutic
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Emonts, M., Sweep, F. C. G. J., Grebenchtchikov, N. I., Geurts-Moespot, A. J., Knaup, M., Chanson, A.-L., Erard, V., Renner, P., Hermans, P. W. M., Hazelzet, J. A., et al. (2007) · Clinical Infectious Diseases · doi:10.1086/514344 · Cited by 108 · see citing works
Aeberli, D., Yang, Y. H., Mansell, A. S., Santos, L., Leech, M. T., & Morand, E. F. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.01.027 · Cited by 102 · see citing works
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The p38 MAPK Pathway in Rheumatoid Arthritis: A Sideways Look
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Han, J. M., Lee, E. K., Gong, S. Y., Sohng, J. K., Kang, Y. J., & Jung, H. J. (2018) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2018.11.003 · Cited by 94 · see citing works
Ouertatani-Sakouhi, H., El-Turk, F., Fauvet, B., Cho, M., Karpinar, D. P., Roy, D. L., Dewor, M., Roger, T., Bernhagen, J., Calandra, T., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.113951 · Cited by 93 · see citing works
Current concepts in glucocorticoid resistance
Yang, N., Ray, D. W., & Matthews, L. C. (2012) · Steroids · doi:10.1016/j.steroids.2012.05.007 · Cited by 92 · see citing works
Houdeau, É., Moriez, R., Leveque, M., Salvador–Cartier, C., Waget, A., Leng, L., Bueno, L. P., Bucala, R., & Fioramonti, J. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.12.028 · Cited by 89 · see citing works
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Mombelli, M., Lugrin, J., Rubino, I., Chanson, A.-L., Giddey, M., Calandra, T., & Roger, T. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir553 · Cited by 89 · see citing works
Self-citationSantos, L. L., Fan, H., Hall, P., Ngo, D., Mackay, C. R., Fingerle-Rowson, G., Bucala, R., Hickey, M. J., & Morand, E. F. (2010) · Arthritis & Rheumatism · doi:10.1002/art.30203 · Cited by 86 · see citing works
Milara, J., Lluch, J., Almudéver, P., Freire, J., Qian, X., & Cortijo, J. (2014) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2014.02.001 · Cited by 85 · see citing works
Stošić‐Grujičić, S., Stojanović, I., Maksimović‐Ivanić, D., Momčilović, M. B., Popadic, D. M., Harhaji-Trajkovic, L. M., Miljković, D. M., Metz, C. N., Mangano, K., Papaccio, G., et al. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21346 · Cited by 85 · see citing works
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Tilstam, P. V., Schulte, W., Holowka, T., Kim, B.-S., Nouws, J., Sauler, M., Piecychna, M., Pantouris, G., Lolis, E., Leng, L., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci127171 · Cited by 77 · see citing works
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Sánchez-Niño, M. D., Sanz, A. B., Ruiz‐Andrés, O., Poveda, J., Izquierdo, M. C., Selgas, R., Egido, J., & Ortíz, A. (2012) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2012.08.001 · Cited by 76 · see citing works
Piette, C., Deprez, M., Roger, T., Noël, A., Foidart, J., & Munaut, C. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.014589 · Cited by 76 · see citing works
Leng, L., & Bucala, R. (2006) · Cell Research · doi:10.1038/sj.cr.7310022 · Cited by 74 · see citing works
Roger, T., Delaloye, J., Chanson, A.-L., Giddey, M., Roy, D. L., & Calandra, T. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis673 · Cited by 73 · see citing works
Roger, T., Schneider, A., Weier, M., Sweep, F. C. G. J., Roy, D. L., Bernhagen, J., Calandra, T., & Giannoni, É. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514018113 · Cited by 73 · see citing works
Maltby, S., Tay, H. L., Yang, M., & Foster, P. S. (2017) · Respirology · doi:10.1111/resp.13052 · Cited by 72 · see citing works
MIF, MIF Alleles, and Prospects for Therapeutic Intervention in Autoimmunity
Bucala, R. (2012) · Journal of Clinical Immunology · doi:10.1007/s10875-012-9781-1 · Cited by 72 · see citing works
MIF: Implications in the Pathoetiology of Systemic Lupus Erythematosus
Lang, T., Foote, A., Lee, J. P. W., Morand, E. F., & Harris, J. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00577 · Cited by 71 · see citing works
Bloom, J., Metz, C. N., Nalawade, S. A., Casabar, J., Cheng, K. F., He, M., Sherry, B. A., Coleman, T. R., Forsthuber, T. G., & Al‐Abed, Y. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.743328 · Cited by 68 · see citing works
Lugrin, J., Ciarlo, E., Santos, A., Grandmaison, G., Dos Santos, I., Le Roy, D., & Roger, T. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.03.004 · Cited by 67 · see citing works
Filip, A.-M., Klug, J., Çaylı, S., Fröhlich, S., Henke, T., Lacher, P., Eickhoff, R., Bulau, P., Linder, M. I., Carlsson‐Skwirut, C., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808620200 · Cited by 66 · see citing works
Mechanisms of glucocorticoid action and insensitivity in airways disease
Boardman, C., Chachi, L., Gavrila, A., Keenan, C. R., Perry, M. M., Xia, Y., Meurs, H., & Sharma, P. K. (2014) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2014.08.008 · Cited by 66 · see citing works
Ma, C., Wang, Y., Shen, A., & Cai, W. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2802 · Cited by 64 · see citing works
Human Macrophage Migration Inhibitory Factor
Kudrin, A., Scott, M., Martin, S. M., Chung, C., Donn, R. P., McMaster, A., Ellison, S. M., Ray, D. W., Ray, K. P., & Binks, M. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601103200 · Cited by 63 · see citing works
A Role for Macrophage Migration Inhibitory Factor in the Neonatal Respiratory Distress Syndrome
Kevill, K., Bhandari, V., Kettunen, M., Leng, L., Fan, J., Mizue, Y., Dzuira, J. D., Reyes‐Múgica, M., McDonald, C., Baugh, J. A., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.1.601 · Cited by 63 · see citing works
Involvement of macrophage migration inhibitory factor in cancer and novel therapeutic targets
Kindt, N., Journé, F., Laurent, G., & Saussez, S. (2016) · Oncology Letters · doi:10.3892/ol.2016.4929 · Cited by 63 · see citing works
MIF but not MIF-2 recruits inflammatory macrophages in an experimental polymicrobial sepsis model
Tilstam, P. V., Schulte, W., Holowka, T., Kim, B., Nouws, J., Sauler, M., Piecychna, M., Pantouris, G., Lolis, E., Leng, L., et al. (2021) · Kölner Universitäts PublikationsServer (Universität zu Köln) · Cited by 61 · see citing works
Roger, T., Ding, X. C., Chanson, A.-L., Renner, P., & Calandra, T. (2007) · European Journal of Immunology · doi:10.1002/eji.200737357 · Cited by 60 · see citing works
Seo, H., Cho, Y.-C., Ju, A., Lee, S., Park, B. C., Park, S. G., Kim, J., Kim, K., & Cho, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-17591-9 · Cited by 58 · see citing works
Macrophage migration inhibitory factor and glucocorticoid sensitivity
Aeberli, D., Leech, M. T., & Morand, E. F. (2006) · Rheumatology · doi:10.1093/rheumatology/kel142 · Cited by 58 · see citing works
Fan, H., Kao, W., Yang, Y. H., Gu, R., Harris, J., Fingerle‐Rowson, G., Bucala, R., Ngo, D., Beaulieu, É., & Morand, E. F. (2014) · Arthritis & Rheumatology · doi:10.1002/art.38689 · Cited by 57 · see citing works
Martin, J. R., Duncan, F. J., Keiser, T. L., Shin, S. B., Kusewitt, D. F., Oberyszyn, T. M., Satoskar, A. R., & VanBuskirk, A. M. (2008) · The FASEB Journal · doi:10.1096/fj.08-119628 · Cited by 56 · see citing works
Exploring the anti‐inflammatory activity of sulforaphane
Treasure, K., Harris, J., & Williamson, G. (2023) · Immunology and Cell Biology · doi:10.1111/imcb.12686 · Cited by 55 · see citing works
Savva, A., Brouwer, M. C., Roger, T., Serón, M. V., Roy, D. L., Ferwerda, B., ENDE, A. V. D., Bochud, P., van de Beek, D., & Calandra, T. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520727113 · Cited by 51 · see citing works
Advances and Insights for Small Molecule Inhibition of Macrophage Migration Inhibitory Factor
Trivedi‐Parmar, V., & Jorgensen, W. L. (2018) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.8b00589 · Cited by 51 · see citing works
Role of macrophage migration inhibitory factor in age-related lung disease
Sauler, M., Bucala, R., & Lee, P. J. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00339.2014 · Cited by 46 · see citing works
An emphasis on molecular mechanisms of anti-inflammatory effects and glucocorticoid resistance
Ingawale, D. K., Mandlik, S. K., & Patel, S. S. (2014) · Journal of Complementary and Integrative Medicine · doi:10.1515/jcim-2014-0051 · Cited by 48 · see citing works
Veillat, V., Lavoie, C. H., Metz, C. N., Roger, T., Labelle, Y., & Akoum, A. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.05.017 · Cited by 46 · see citing works
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Ralph, J. A., & Morand, E. F. (2008) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.12.7.795 · Cited by 48 · see citing works
Renner, P., Roger, T., Bochud, P., Sprong, T., Sweep, F. C. G. J., Bochud, M., Faust, S. N., Haralambous, E., Betts, H., Chanson, A.-L., et al. (2011) · The FASEB Journal · doi:10.1096/fj.11-195065 · Cited by 47 · see citing works
Wang, F.-F., Zhu, L., Zou, Y.-Q., Zheng, H. W., Wilson, A., Yang, C., Shen, N., Wallace, D. J., Weisman, M. H., Chen, S., et al. (2012) · Arthritis Research & Therapy · doi:10.1186/ar3828 · Cited by 46 · see citing works
MAP kinase phosphatase-1, a gatekeeper of the acute innate immune response
Kirk, S. G., Samavati, L., & Liu, Y. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.117157 · Cited by 46 · see citing works
Cvetković, I., & Stošić‐Grujičić, S. (2006) · International Immunopharmacology · doi:10.1016/j.intimp.2006.06.009 · Cited by 46 · see citing works
Treating gliomas with glucocorticoids: from bedside to bench
Piette, C., Munaut, C., Foidart, J., & Deprez, M. (2006) · Acta Neuropathologica · doi:10.1007/s00401-006-0100-x · Cited by 46 · see citing works
Vollmer, T. R., Stockhausen, A., & Zhang, J. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.400671 · Cited by 45 · see citing works
Ives, A., Roy, D. L., Théroude, C., Bernhagen, J., Roger, T., & Calandra, T. (2021) · The FASEB Journal · doi:10.1096/fj.202001605r · Cited by 44 · see citing works
The hypothalamic–pituitary–adrenal axis in critical illness
Venkataraman, S., Munoz, R., Cândido, C., & Witchel, S. (2007) · Reviews in Endocrine & Metabolic Disorders · doi:10.1007/s11154-007-9058-9 · Cited by 23 · see citing works
Zhou, C., Gao, J., Ji, H., Li, W., Xing, X., Liu, D., Guo, Q., Zhou, L., & Jing, F. (2021) · Inflammation · doi:10.1007/s10753-021-01478-z · Cited by 43 · see citing works
Association of MIF-173 gene polymorphism with inflammatory bowel disease in Chinese Han population
Fei, B., Huo-xiang, L., Yang, J.-M., & Ye, Z. (2007) · Cytokine · doi:10.1016/j.cyto.2007.10.010 · Cited by 41 · see citing works
Moonah, S. N., Abhyankar, M. M., Haque, R., & Petri, W. A. (2014) · Infection and Immunity · doi:10.1128/iai.01812-14 · Cited by 41 · see citing works
Acceleratedin vitrodifferentiation of blood monocytes into dendritic cells in human sepsis
Faivre, V., Lukaszewicz, A., Alvès, A., Charron, D. J., Payen, D. M., & Haziot, A. (2007) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2006.03287.x · Cited by 41 · see citing works
The inflammatory cytokines: molecular biomarkers for major depressive disorder?
Martin, C., Tansey, K. E., Schalkwyk, L. C., & Powell, T. R. (2014) · Biomarkers in Medicine · doi:10.2217/bmm.14.29 · Cited by 40 · see citing works
Glucocorticoid-induced MIF expression by human CEM T cells
Leng, L., Wang, W., Roger, T., Merk, M., Wuttke, M., Calandra, T., & Bucala, R. (2009) · Cytokine · doi:10.1016/j.cyto.2009.07.002 · Cited by 38 · see citing works
Xu, S., Guo, X., Gao, X. C., Xue, H., Zhang, J., Guo, X., Qiu, W., Zhang, P., & Li, G. (2016) · International Journal of Oncology · doi:10.3892/ijo.2016.3704 · Cited by 37 · see citing works
Recruitment of MAIT Cells to the Intervillous Space of the Placenta by Placenta-Derived Chemokines
Solders, M., Gorchs, L., Tiblad, E., Gidlöf, S. B., Leeansyah, E., Dias, J., Sandberg, J. K., Magalhaes, I., Lundell, A., & Kaipe, H. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01300 · Cited by 37 · see citing works
Effects of glucocorticoids on inflammation and arthritis
Morand, E. F. (2007) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e32805e87d0 · Cited by 37 · see citing works
Comalada, M., Lloberas, J., & Celada, A. (2012) · European Journal of Immunology · doi:10.1002/eji.201242441 · Cited by 36 · see citing works
Allam, V. S. R. R., Pavlidis, S. P., Liu, G., Kermani, N. Z., Simpson, J., To, J., Donnelly, S., Guo, Y., Hansbro, P. M., Phipps, S., et al. (2022) · Thorax · doi:10.1136/thorax-2021-218555 · Cited by 35 · see citing works
Veillat, V., Sengers, V., Metz, C. N., Roger, T., Leboeuf, M., Mailloux, J. R., & Akoum, A. (2012) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.05.018 · Cited by 35 · see citing works
Brain Miffed by Macrophage Migration Inhibitory Factor
Savaskan, N. E., Fingerle‐Rowson, G., Buchfelder, M., & Eyüpoglu, I. Y. (2012) · International Journal of Cell Biology · doi:10.1155/2012/139573 · Cited by 32 · see citing works
- Authors
- Roger, T., Chanson, A., Knaup‐Reymond, M., & Calandra, T.
- Affiliations
- Centre Hospitalier Universitaire Vaudois (CH)
- Corresponding author
- Calandra, Thierry
- Venue
- European Journal of Immunology
- Publisher
- Wiley
- Published
- 2005-12
- Volume
- 35
- Issue
- 12
- Pages
- 3405-3413
- ISSN
- 0014-2980 (ISSN-L)
- 1521-4141
- OpenAlex
- W2046525356
- Cited by
- 184
- References
- 48
- Citations by year
- 2025: 3 · 2024: 4 · 2023: 6 · 2022: 6 · 2021: 7 · 2020: 4 · 2019: 13 · 2018: 8 · 2017: 7 · 2016: 8 · 2015: 4 · 2014: 9 · 2013: 10 · 2012: 16
- FWCI
- 4.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Macrophage Migration Inhibitory Factor
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Tyrosine Phosphatases
- Keywords
- macrophage migration inhibitory factor, MAPK phosphatase-1, glucocorticoids, dexamethasone, innate immunity, macrophages, lipopolysaccharide, TNF-α, interleukin-8, autocrine regulation, dual-specificity phosphatase, MAPK signaling, immunosuppression
- MeSH terms
- Animals, Cell Line, Glucocorticoids, Humans, Immunity, Innate, Macrophage Migration-Inhibitory Factors, Phosphoprotein Phosphatases, Cytokines, Protein Tyrosine Phosphatases, Immediate-Early Proteins, Cell Cycle Proteins, U937 Cells, Mice, Dual Specificity Phosphatase 1, Protein Phosphatase 1
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