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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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“MIF’s critical role within the immune system is further underscored by the finding that MIF is induced by low concentrations of glucocorticoids and has the unique ability to override the anti-inflammatory and immunosuppressive effects of glucocorticoids [77, 81, 84].”
BackgroundCorticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease
Barnes, P. J. (2013) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2012.12.1564 · Cited by 708
“It is induced by corticosteroids and appears to inhibit their anti-inflammatory effects, mainly through inhibiting the induction ofMKP-1.(81)Macrophage migration inhibitory factor has also been implicated in the pathogenesis of allergic inflammation inmousemodels of asthma(82) and in the steroid resistance of asthmati…”
BackgroundMAPK phosphatases — regulating the immune response
Liu, Y., Shepherd, E. G., & Nelin, L. D. (2007) · Nature reviews. Immunology · doi:10.1038/nri2035 · Cited by 679
“found that MIF alleviated the inhibitory effect of dexamethasone on TNF and CXC-chemokine ligand 8 (CXCL8; also known as IL-8) production in a dose-dependent manne”
BackgroundGlucocorticosteroids: current and future directions
Barnes, P. J. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.01199.x · Cited by 550
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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