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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 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
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“This response was associated with phosphorylation and subsequent activation of ERK 1/2 (34, 35).”
BackgroundFlaster, H. V., Bernhagen, J., Calandra, T., & Bucala, R. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0065 · Cited by 262
Merk, M., Zierow, S., Leng, L., Das, R., Du, X., Schulte, W., Fan, J., Lue, H., Chen, Y., Xiong, H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102941108 · Cited by 243
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Bucala, R., & Donnelly, S. C. (2007) · Immunity · doi:10.1016/j.immuni.2007.03.005 · Cited by 210
“Finally, MIF antagonizes glucocorticoid induction of MAP kinase phosphatase, which is important in downregulating the MAP-kinaseactivation response (Roger et al., 2005).”
BackgroundMacrophage migration inhibitory factor is required for NLRP3 inflammasome activation
Lang, T., Lee, J. P. W., Elgass, K., Pinar, A. A., Tate, M. D., Aitken, E. H., Fan, H., Creed, S. J., Deen, N. S., Traoré, D. A. K., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04581-2 · Cited by 199
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Dual-specificity phosphatase 1: a critical regulator of innate immune responses
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Bilsborrow, J. B., Doherty, E. H., Tilstam, P. V., & Bucala, R. (2019) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2019.1656718 · Cited by 170
“MAP kinase phosphatase-1, which normally dephosphorylates and inactivates the inflammatory ERK1/2, JNK, and p38 MAP kinase signaling pathways [75,76].”
BackgroundRegulation of innate immune response by MAP kinase phosphatase-1
Wang, X., & Liu, Y. (2007) · Cellular Signalling · doi:10.1016/j.cellsig.2007.03.013 · Cited by 152
Role of MIF in Inflammation and Tumorigenesis
Bach, J., Rinn, B., Meyer, B., Dodel, R. C., & Bacher, M. (2008) · Oncology · doi:10.1159/000155223 · Cited by 138
“After applying LPS, a potent activator of the innate immune system, MIF secretion and production measured by mRNA and protein synthesis increased compared to controls. However, when adding recombinant MIF, these effects were counterregulated. Use of antisense MIF led to decreased MIF concentrations in treated macropha…”
BackgroundMitogen-activated protein kinase phosphatase (MKP)-1 in immunology, physiology, and disease
Wancket, L. M., Frazier, W. J., & Liu, Y. (2011) · Life Sciences · doi:10.1016/j.lfs.2011.11.017 · Cited by 137
“Treatment with recombinant MIF also restores TNF-α and IL-8 production in dexamethasone-treated macrophages (Roger et al., 2005).”
BackgroundInfluentialGiannoni, 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
“Similarly, steroids did not reduce TLR2 and TLR4 expression in immune and nonimmune cells (6, 9, 15, 26, 30, 35).”
BackgroundPAAN/MIF nuclease inhibition prevents neurodegeneration in Parkinson’s disease
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 123
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
“MIF has been shown to up-regulate inflammatory cytokine production by mechanisms that include sustaining MAPK phosphorylation and inhibiting the synthesis of an inhibitor of NF-κB (18, 69, 72, 73).”
BackgroundZhou, Y., Ling, E., & Dheen, S. T. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04535.x · Cited by 115
“Several lines of evidence suggest that GCs induced sustained expression of MKP-1 in various cell lines such as Hela cells (Lasa et al. 2002), osteoblasts (Engelbrecht et al. 2003), macrophages (Roger et al. 2005; Waetzig et al. 2005) and epithelial cells (Imasato et al. 2002; Sakai et al. 2004).”
BackgroundFan, 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 113
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
“known as DUSP1), a critical negative regulator of MAPK phosphorylation (16, 43).”
BackgroundMIF as a Disease Target: ISO-1 as a Proof-of-Concept Therapeutic
Al‐Abed, Y., & VanPatten, S. (2010) · Future Medicinal Chemistry · doi:10.4155/fmc.10.281 · Cited by 108
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
“Cytoplasmic phospholipase A2 and mitogen-activated protein kinase phosphatase 1 have been identified as key molecular targets of MIF-glucocorticoid crosstalk [12, 13].”
BackgroundAeberli, 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
“shown in a partially MIF deficient system achieved through the use of anti-sense [29], suggest that MIF regulation of MKP-1 expression represents a central process through which”
BackgroundResultInfluentialA Leishmania Ortholog of Macrophage Migration Inhibitory Factor Modulates Host Macrophage Responses
Kamir, D., Zierow, S., Leng, L., Cho, Y., Díaz, Y. R., Griffith, J. W., McDonald, C., Merk, M., Mitchell, R. A., Trent, J. O., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.12.8250 · Cited by 99
Macrophage migration inhibitory factor: A key cytokine in RA, SLE and atherosclerosis
Santos, L. L., & Morand, E. F. (2008) · Clinica Chimica Acta · doi:10.1016/j.cca.2008.09.014 · Cited by 96
“and IL-8 production supports this [62].”
The p38 MAPK Pathway in Rheumatoid Arthritis: A Sideways Look
Clark, A. R., & Dean, J. L. (2012) · The Open Rheumatology Journal · doi:10.2174/1874312901206010209 · Cited by 97
“Pro-inflammatory effects of MIF are thought to be mediated by inhibition of expression of DUSP1 and consequent enhancement of p38 MAPK signaling [82-85].”
BackgroundHan, 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 95
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
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
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
Histone Deacetylase Inhibitors Impair Antibacterial Defenses of Macrophages
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“E. coli and S. aureus were grown overnight at 37 C in tryptic soy broth (BD Biosciences), washed in PBS, and adjusted to 107 colony-forming units (CFU)/mL in RPMI medium containing 10% FCS. BMDMs (4 3 105 cells in 24-well cell-culture plates, Costar) were treated with TSA or VPA for 18 hours.”
MethodInfluentialSelf-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
“MIF has been reported to inhibit the expression of MKP-1 in macrophages, as demonstrated by increased expression of MKP-1 in MIF-deficient cells, leading to impaired p38 MAPK activation (58,59).”
BackgroundMilara, 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
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
“…is known that MIF acts in concert with glucocorticoids to control the ‘‘set point’’ and magnitude of the immunoinflammatory responses (Calandra et al., 1995; Roger et al., 2005) and that high levels of these hormones induce a bias toward type 2/3 immune response (for review, see Franchimont, 2004).”
BackgroundMechanisms of Disease: macrophage migration inhibitory factor in SLE, RA and atherosclerosis
Ayoub, S., Hickey, M. J., & Morand, E. F. (2008) · Nature Clinical Practice Rheumatology · doi:10.1038/ncprheum0701 · Cited by 84
“Two groups have independently reported the novel finding that MIF is a negative regulator of MKP1 expression”
BackgroundThe role of macrophage inhibitory factor in tumorigenesis and central nervous system tumors
Bach, J., Deuster, O., Balzer‐Geldsetzer, M., Meyer, B., Dodel, R. C., & Bacher, M. (2009) · Cancer · doi:10.1002/cncr.24245 · Cited by 80
Autoimmune diseases: MIF as a therapeutic target
Greven, D., Leng, L., & Bucala, R. (2010) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728220903551304 · Cited by 79
“These mechanisms include mutual regulatory actions on the expression of IK-kb, PLA2, and MAPK phosphatase (MKP-1) [15-23].”
BackgroundMIF family cytokines in cardiovascular diseases and prospects for precision-based therapeutics
Tilstam, P. V., Qi, D., Leng, L., Young, L. H., & Bucala, R. (2017) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2017.1336227 · Cited by 76
“MIF additionally downregulates the glucocorticoid-induced expression of the NF-κB inhibitor IκB [23] and the mitogen-activated protein kinase phosphatase-1, which reduces downstream MAPK activation [24].”
BackgroundMIF but not MIF-2 recruits inflammatory macrophages in an experimental polymicrobial sepsis model
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
“MIF upregulates the expression of microbial pattern recognition receptors (8, 9), counterregulates the immuno suppressive action of glucocorticoids (10), and sustains macrophage survival in the face of activation-induced apoptosis (11).”
BackgroundMIF, CD74 and other partners in kidney disease: Tales of a promiscuous couple
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
“Additional intracellular pathways involve cytoplasmic phospholipase A2, IkB1, and MKP-1 and this effect is reproduced by a MIF-(50-65) peptide that binds JAB1 [37,38].”
BackgroundPiette, 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
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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 75
“sessed by Northern blotting, using specific complementary DNA probes [15].”
BackgroundMethodRoger, 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
“This indicates that the response to E. coli is ERK1/2 dependent in newborn monocytes and is in line with the notion that MIF promotes ERK1/2 activation by reducing the expression of MKP-1, a phosphatase that inactivates ERK downstream of MEK (21, 38).”
BackgroundResultInfluentialMaltby, S., Tay, H. L., Yang, M., & Foster, P. S. (2017) · Respirology · doi:10.1111/resp.13052 · Cited by 76
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
“MKP-1 targets include MAP kinase-activated protein kinase 2, which mediates the degradation of pro-inflammatory mRNAs [33, 34].”
BackgroundMIF: 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
“GCs prevent expression of NF-ĸB-dependent genes primarily by increasing expression of IĸB.”
BackgroundInfluentialBloom, 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
“T-614 Is Additive with Glucocorticoids in Vitro—Glucocorticoid synergy has been demonstrated in the context of MIF in previous studies using RNA silencing and anti-MIF antibodies (20, 30).”
MethodLugrin, 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
“Mouse RAW 264.7 macrophages (ATCC) were cultured in RPMI 1640 medium containing 2 mM glutamine [27].”
InfluentialFilip, 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 69
“LPS, a gram negative bacterial cell wall component, is an inflammatory mediator that induces the release of TNFα from macrophage cell lines or primary monocytes (Bendrat et al. 1997; Roger et al. 2005).”
BackgroundMechanisms 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 69
“Furthermore, oxidative stress activates PI3-kinase [169,170].”
Ma, C., Wang, Y., Shen, A., & Cai, W. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2802 · Cited by 64
“These signaling cascades regulate the expression of target genes involved in inflammatory cytokine production (7,8).”
BackgroundHuman 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
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
“Glucocorticoids in low concentrations also have been shown to induce MIF secretion (41), which then exerts an autocrine/paracrine effect on glucocorticoid action (41, 43, 44).”
BackgroundInvolvement 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
“This effect may be explained by the fact that MIF inhibits mitogen-activated protein kinase (MAPK) phosphatase-1, which is induced by glucocorticoids (7).”
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
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
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 59
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
“[76] demonstrated the negative regulation of GC-induced MKP-1 by rMIF in the RAW 264.”
BackgroundFan, 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 63
“MIF inhibition of glucocorticoid sensitivity has been previously identified to be mediated via regulation of MKP-1 (16,22,36).”
BackgroundMartin, 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
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 58
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
“An empty vector served as a negative control (18).”
BackgroundAdvances 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
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 49
“Interestingly, MIF can override the effects of glucocorticoids via diverse signaling pathways that include 1) inhibition of glucocorticoid induction of I B (36), 2) inhibition of glucocorticoid-mediated transcription of MAP kinase phosphatase-1 (4, 117), and 3) autocrine and/or paracrine activation of a proinflammator…”
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 49
“Macrophage migration inhibitory factor (MIF) is a proinflammatory cytokine, causes GC resistance by blocking GC induction of the dual specificity phosphatase 1 (DUSP1) [61].”
BackgroundVeillat, 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
MAPK phosphatases as novel targets for rheumatoid arthritis
Ralph, J. A., & Morand, E. F. (2008) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.12.7.795 · Cited by 48
“In the light of these studies and the literature identifying MKP1 as an effector of GC sensitivity [89,90] , we suggest that MKP1 may be a central target for immunomodulation by drugs used to treat inflammatory and malignant diseases, and that MKP1 may serve both as a molecular readout of drug sensitivity and as a tar…”
BackgroundInfluentialRenner, 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
“A fragment ranging from 1073 to 129 bp of the MIF gene of either the 794 CATT5/ 173 G, the 794 CATT6/ 173 G, the 794 CATT6/ 173 C, or the 794 CATT7/ 173 C genotype was amplified from genomic DNA using the Expand High Fidelity PCR System (Roche Applied Science), cloned in the pGEM-T Easy vector (Promega), sequenced, an…”
MethodWang, 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
“Daun and Cannon reported evidence for MIF reversal of dexamethasone induction of I Ba [31], and Roger and colleagues reported reversal of dexamethasone inhibition of NF- B by recombinant MIF [6].”
BackgroundMAP 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 47
“MIF is considered to be a counter-regulator of the immunosuppressive effects of glucocorticoids [127].”
BackgroundCvetković, I., & Stošić‐Grujičić, S. (2006) · International Immunopharmacology · doi:10.1016/j.intimp.2006.06.009 · Cited by 46
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 49
“This mechanism consists of alterations of the mRNA turnover or translation and has been demonstrated for IL-1α, IL-6, IL-8, IFN-β and granulocyte-macrophage colony-stimulating factor (GM-CSF) [86] and TNF [74].”
BackgroundMethodInfluentialVollmer, T. R., Stockhausen, A., & Zhang, J. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.400671 · Cited by 46
“For example, the pro-inflammatory cytokines IFN- andmacrophagemigration inhibitory factor (MIF) inhibit MKP-1 induction (30, 68, 69), while the anti-inflammatory cytokine IL-10 and glucocorticoids booster MKP-1 expression (29, 47, 70).”
BackgroundIves, A., Roy, D. L., Théroude, C., Bernhagen, J., Roger, T., & Calandra, T. (2021) · The FASEB Journal · doi:10.1096/fj.202001605r · Cited by 47
The hypothalamic–pituitary–adrenal axis in critical illness
Venkataraman, S. T., Munoz, R. A., Cândido, C., & Witchel, S. F. (2007) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-007-9058-9 · Cited by 45
“Are there roles for inhibition of p38 MAPK activity or enhanced MKP-1 expression in the treatment of severe sepsis/septic shock?”
BackgroundInfluentialZhou, 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 42
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
Moonah, S. N., Abhyankar, M. M., Haque, R., & Petri, W. A. (2014) · Infection and Immunity · doi:10.1128/iai.01812-14 · Cited by 41
“expression and inhibition of TNF-α production by LPS-stimulated immune cells (15, 54, 56).”
BackgroundAcceleratedin 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 40
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 42
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 39
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
“In addition to inhibition of macrophage migration, MIF blocks NK cell activity (5), decreases acute inflammation and mediates chronic inflammation, which partly promotes tumourigenesis (6-8).”
BackgroundRecruitment 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 39
Effects of glucocorticoids on inflammation and arthritis
Morand, E. F. (2007) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e32805e87d0 · Cited by 37
Comalada, M., Lloberas, J., & Celada, A. (2012) · European Journal of Immunology · doi:10.1002/eji.201242441 · Cited by 36
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
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
“Originally described as a product of activated T lymphocytes that inhibits the random migration of cultured macrophages,(5) MIF is now known as a multifunctional cytokine with potent proinflammatory, immuno-modulatory, and growth-promoting effects.(4,6) MIF has been shown to be implicated in tumorigenesis as well as i…”
BackgroundBrain 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
“Moreover, MIF’s impact on the innate immune system can be fatal in lethal endotoxic shock by counteracting the protective effects of glucocorticoids at various levels [86, 87].”
Background
Metadata
- 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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