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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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Gao, H., Wang, Q., Yu, X., Liu, J., Bai, S., Feng, J. C., & Wu, B. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.08.038 · Cited by 25
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“Although there are inadequate data to elucidate the proinflammatory functions of MIF entirely, the mentioned mechanisms could describe its impact on glucocorticoidrelated immunosuppression [48, 53].”
BackgroundThioredoxin-1: A Promising Target for the Treatment of Allergic Diseases
Wang, J., Zhou, J., Wang, C., Fukunaga, A., Li, S., Yodoi, J., & Tian, H. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.883116 · Cited by 25
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“The negative regulator of MAPK activation, MAPK phosphatase 1 (MKP1), has been identified as a key MIF-regulated gene operative in these responses.(15,16) MKP1 (CL100, PTPN10, DUSP1, and 3CH134) is 1 of 10 MAPK phosphatases (MKPs) characterized to date which tightly control the phosphorylation of MAPKs.”
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“cDNA (100 ng total RNA equivalent) was added to a 20 ll reaction with bovine or human cytokine primers reported previously (Leutenegger et al., 2000; Roger et al., 2005; Thacker et al., 2007).”
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“Moreover, it directly inhibits the immunosuppressive actions of glucocorticoids [27] through the suppression of mitogen-activated protein kinase (MAPK) phosphatase-1 (MKP-1) [28-30].”
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Chrousos, G., & Franchimont, D. (2004) · CRC Press eBooks · doi:10.1201/9780203021941-39 · Cited by 21
Differential and cell‐type specific regulation of responses to Toll‐like receptor agonists by ISO‐1
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Gámez-Nava, J. I., Díaz-Rizo, V., Pérez-Guerrero, E. E., Muñóz-Valle, J. F., Saldaña-Cruz, A. M., Robledo, N. S. F., Jacobo-Cuevas, H., Nava-Valdivia, C. A., Alcaraz-López, M. F., Trujillo, X., et al. (2020) · Biomarker Research · doi:10.1186/s40364-020-00236-x · Cited by 15
“An interesting observation published in the literature is that MIF is a cytokine that has been observed to decrease the effect of glucocorticoids [13].”
BackgroundThe roles of macrophage migration inhibitory factor in retinal diseases
Zhang, H., Zhang, X., Li, H., Wang, B., Chen, P., & Meng, J. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.379020 · Cited by 15
MIF attenuates the suppressive effect of dexamethasone on IL-6 production by nasal polyp.
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“7 macrophages have documented MIF release and an autocrine effect, which includes an increase in ERK phosphorylation [28,29].”
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“This may be an effect of the immunosuppressive dose of prednisolone; suppression of inflammatory cells, particularly macrophages, in response to glucocorticoids has been shown to induce macrophage migration inhibitory factor (MIF) [33, 34].”
BackgroundYao, J., Leng, L., Fu, W., Li, J., Bronner, C., & Bucala, R. (2021) · Arthritis & Rheumatology · doi:10.1002/art.41753 · Cited by 12
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“However, numerous studies have contributed to the current consensus that the involvement of MIF is central in the initiation of the inflammatory response [9, 10].”
BackgroundChen, X., Chen, Y., Qi, D., & Cui, D. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110422 · Cited by 11
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“MIF is an inflammatory cytokine that actively participates in multiple stages of the inflammatory response, which can impair steroid sensitivity by counter-regulating steroid induced expression of MAPK phosphatase-1 (MKP-1) that suppresses the secretion of pro-inflammatory cytokine [10].”
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“In addition, these results agreed with a previous study (Roger et al. 2005) in which glucocorticoid induced macrophage migration inhibitory factor, resulting in a reduction of inflammatory cells, especially macrophages.”
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“In contrast to all other proinflammatory cytokines, MIF is released upon glucocorticoid stimulation and consequently acts as a physiological counter-regulator of glucocorticoid action (Calandra et al. 1995; Roger et al. 2005).”
BackgroundThe role of MIF in periodontitis: A potential pathogenic driver, biomarker, and therapeutic target
Fang, T., Liu, L., Song, D., & Huang, D. (2023) · Oral Diseases · doi:10.1111/odi.14558 · Cited by 9
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“Another in vivo study showed that MIF could be up-regulated by endogenous glucocorticoids in rats with adjuvantinduced arthritis.(18) In humans, the serum MIF concentration is influenced by exogenous glucocorticoids even after adjusting for disease activity variables.”
BackgroundApproaching the immunophysiology of steroid resistance
Bucala, R. (2012) · Arthritis Research & Therapy · doi:10.1186/ar3820 · Cited by 7
Macrophage migration inhibitory factor as a therapeutic target in neuro-oncology: A review
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“MIF as an important pro-inflammatory cytokine, is implicated in tumors and inflammation and serves as an inflammatory mediator, inducing several immunological effects in vertebrates [27,28].”
Zhu, W.-Y., Jin, X., Ma, Y.-C., & Liu, Z.-B. (2019) · Journal of International Medical Research · doi:10.1177/0300060519893870 · Cited by 7
“Furthermore, administration of recombinant MIF has been shown to inhibit the suppressive action of glucocorticoids on proinflammatory cytokine production.(14) The inhibitive effect of MIF on glucocorticoids leads to individual variability in response to glucocorticoids because of a single nucleotide polymorphism (SNP)…”
BackgroundMitogen-activated protein kinase phosphatase-1 and septic shock
Liu, Y., & Shanley, T. P. (2008) · Journal of Organ Dysfunction · doi:10.1080/17471060701200444 · Cited by 5
“reported that MKP-1 is a critical mediator in the MIFglucocorticoid crosstalk (67).”
BackgroundContraception in Chronic Kidney Disease and Renal Transplantation
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“Furthermore, MIF is capable of overcoming the immune suppressive effects of GC at a transcriptional and post-transcriptional level by overriding the GC-induced MAPK-phosphatase-1 expression and inhibiting cytokine production [20,40].”
BackgroundSystemic Glucocorticoid Therapy for SLE
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“Кроме того, MIF оказывает супрессирующее действие на MKP-1, которая, в свою очередь, ингибирует путем дефосфорилирования провоспалительные ферменты, участвующие во внутриклеточной передаче сигнала – ERK1/2, JNK и p38 митоген-активируемую протеинкиназу [28].”
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“Recent data have shown that MAPK phosphatase 1 (MKP-1) is a critical target of MIF-glucocorticoid crosstalk [ 45 ].”
BackgroundHigh Expression of Macrophage Migration Inhibitory Factor in the Murine Lacrimal Gland
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“Furthermore, MIF’s action as an endogenous, counterregulatory mediator for glucocorticoid action has also been suggested.(13) Functional blocking of MIF by neutralizing anti-MIF antibody suppressed septic shock or delayed-type hypersensitivity in experimental animals and reduced renal injury in immunologically induced…”
BackgroundCurrent immunogenetic predisposition to tuberculosis in the Moroccan population
Qrafli, M., Najimi, M., Aouad, R. E., & Sadki, K. (2017) · International Journal of Immunogenetics · doi:10.1111/iji.12340 · Cited by 2
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“Furthermore, literature suggests that MiF can be induced by Gcs and may compromise Gc sensitivity [20]. specifically, it impairs Gcs sensitivity via MaPkinase phosphatase-1 (MKP-1) inhibition [40].”
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The Macrophage Migration Inhibitory Factor Homolog of Entamoeba histolytica Binds to
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“In another study, it has also been reported that the elevated expression of MIF could accelerate the progression of SLE in the patients through MAPK-dependent suppression of GRα (20).”
BackgroundSystemic glucocorticoid therapy for SLE
Nataraja, C., Morand, E. F., & Mak, A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-93232-5.00063-0
Huang, K., Yang, B., Xu, Z., Chen, H., & Wang, J. (2024) · Figshare · doi:10.6084/m9.figshare.26618755
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Etude des effets des médiateurs du stress sur l'immunité intestinale des porcelets
Gavaud, S. (2022) · theses.fr (ABES) · doi:10.70675/18305d3cz137az416bz9a7az499d89869fcd
Mechanisms of Altered Glucocorticoid Sensitivity
Yang, N. (2013) · Research Explorer (The University of Manchester)
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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