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Macrophage migration inhibitory factor promotes glucocorticoid resistance of neutrophilic inflammation in a murine model of severe asthma

Macrophage migration inhibitory factor promotes glucocorticoid resistance of neutrophilic inflammation in a murine model of severe asthma
Macrophage migration inhibitory factor promotes glucocorticoid resistance of neutrophilic inflammation in a murine model of severe asthma

Background: Severe neutrophilic asthma is resistant to treatment with glucocorticoids. The immunomodulatory protein macrophage migration inhibitory factor (MIF) promotes neutrophil recruitment to the lung and antagonises responses to glucocorticoids. We hypothesised that MIF promotes glucocorticoid resistance of neutrophilic inflammation in severe asthma.

Methods: We examined whether sputum MIF protein correlated with clinical and molecular characteristics of severe neutrophilic asthma in the Unbiased Biomarkers for the Prediction of Respiratory Disease Outcomes (U-BIOPRED) cohort. We also investigated whether MIF regulates neutrophilic inflammation and glucocorticoid responsiveness in a murine model of severe asthma in vivo.

Results: MIF protein levels positively correlated with the number of exacerbations in the previous year, sputum neutrophils and oral corticosteroid use across all U-BIOPRED subjects. Further analysis of MIF protein expression according to U-BIOPRED-defined transcriptomic-associated clusters (TACs) revealed increased MIF protein and a corresponding decrease in annexin-A1 protein in TAC2, which is most closely associated with airway neutrophilia and NLRP3 inflammasome activation. In a murine model of severe asthma, treatment with the MIF antagonist ISO-1 significantly inhibited neutrophilic inflammation and increased glucocorticoid responsiveness. Coimmunoprecipitation studies using lung tissue lysates demonstrated that MIF directly interacts with and cleaves annexin-A1, potentially reducing its biological activity.

Conclusion: Our data suggest that MIF promotes glucocorticoid-resistance of neutrophilic inflammation by reducing the biological activity of annexin-A1, a potent glucocorticoid-regulated protein that inhibits neutrophil accumulation at sites of inflammation. This represents a previously unrecognised role for MIF in the regulation of inflammation and points to MIF as a potential therapeutic target for the management of severe neutrophilic asthma.

asthma, asthma mechanisms, cytokine biology
0040-6376
Allam, Venkata Sita Rama Raju
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Pavlidis, Stelios
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Liu, Gang
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Kermani, Nazanin Zounemat
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Simpson, Jennifer
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To, Joyce
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Donnelly, Sheila
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Guo, Yi-Ke
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Hansbro, Philip M.
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Phipps, Simon
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Morand, Eric F.
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Djukanovic, Ratko
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Sterk, Peter
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Chung, Kian Fan
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Adcock, Ian
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Harris, James
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Sukkar, Maria B.
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Allam, Venkata Sita Rama Raju
62e19ea1-c3b7-4326-87d5-a644d5d58528
Pavlidis, Stelios
2b3c21ce-683d-4fde-aae6-e68e05bdb69e
Liu, Gang
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Kermani, Nazanin Zounemat
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Simpson, Jennifer
406d8dc3-29b4-4357-82f3-6e23b4e0155b
To, Joyce
42d08b8f-4c3c-4909-b12c-51434231127e
Donnelly, Sheila
fe223c16-e8ac-41a6-bca7-131e56e555bf
Guo, Yi-Ke
450dd28e-5f7b-4a4a-899e-feeac1338330
Hansbro, Philip M.
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Phipps, Simon
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Morand, Eric F.
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Djukanovic, Ratko
d9a45ee7-6a80-4d84-a0ed-10962660a98d
Sterk, Peter
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Chung, Kian Fan
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Adcock, Ian
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Harris, James
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Sukkar, Maria B.
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Allam, Venkata Sita Rama Raju, Pavlidis, Stelios, Liu, Gang, Kermani, Nazanin Zounemat, Simpson, Jennifer, To, Joyce, Donnelly, Sheila, Guo, Yi-Ke, Hansbro, Philip M., Phipps, Simon, Morand, Eric F., Djukanovic, Ratko, Sterk, Peter, Chung, Kian Fan, Adcock, Ian, Harris, James and Sukkar, Maria B. (2022) Macrophage migration inhibitory factor promotes glucocorticoid resistance of neutrophilic inflammation in a murine model of severe asthma. Thorax, [218555]. (doi:10.1136/thorax-2021-218555).

Record type: Article

Abstract

Background: Severe neutrophilic asthma is resistant to treatment with glucocorticoids. The immunomodulatory protein macrophage migration inhibitory factor (MIF) promotes neutrophil recruitment to the lung and antagonises responses to glucocorticoids. We hypothesised that MIF promotes glucocorticoid resistance of neutrophilic inflammation in severe asthma.

Methods: We examined whether sputum MIF protein correlated with clinical and molecular characteristics of severe neutrophilic asthma in the Unbiased Biomarkers for the Prediction of Respiratory Disease Outcomes (U-BIOPRED) cohort. We also investigated whether MIF regulates neutrophilic inflammation and glucocorticoid responsiveness in a murine model of severe asthma in vivo.

Results: MIF protein levels positively correlated with the number of exacerbations in the previous year, sputum neutrophils and oral corticosteroid use across all U-BIOPRED subjects. Further analysis of MIF protein expression according to U-BIOPRED-defined transcriptomic-associated clusters (TACs) revealed increased MIF protein and a corresponding decrease in annexin-A1 protein in TAC2, which is most closely associated with airway neutrophilia and NLRP3 inflammasome activation. In a murine model of severe asthma, treatment with the MIF antagonist ISO-1 significantly inhibited neutrophilic inflammation and increased glucocorticoid responsiveness. Coimmunoprecipitation studies using lung tissue lysates demonstrated that MIF directly interacts with and cleaves annexin-A1, potentially reducing its biological activity.

Conclusion: Our data suggest that MIF promotes glucocorticoid-resistance of neutrophilic inflammation by reducing the biological activity of annexin-A1, a potent glucocorticoid-regulated protein that inhibits neutrophil accumulation at sites of inflammation. This represents a previously unrecognised role for MIF in the regulation of inflammation and points to MIF as a potential therapeutic target for the management of severe neutrophilic asthma.

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Accepted/In Press date: 15 July 2022
e-pub ahead of print date: 7 November 2022
Keywords: asthma, asthma mechanisms, cytokine biology

Identifiers

Local EPrints ID: 474049
URI: http://eprints.soton.ac.uk/id/eprint/474049
ISSN: 0040-6376
PURE UUID: 739a3c39-6645-4967-a668-3a09f932e1cd
ORCID for Ratko Djukanovic: ORCID iD orcid.org/0000-0001-6039-5612

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Date deposited: 09 Feb 2023 17:59
Last modified: 17 Mar 2024 02:34

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Contributors

Author: Venkata Sita Rama Raju Allam
Author: Stelios Pavlidis
Author: Gang Liu
Author: Nazanin Zounemat Kermani
Author: Jennifer Simpson
Author: Joyce To
Author: Sheila Donnelly
Author: Yi-Ke Guo
Author: Philip M. Hansbro
Author: Simon Phipps
Author: Eric F. Morand
Author: Peter Sterk
Author: Kian Fan Chung
Author: Ian Adcock
Author: James Harris
Author: Maria B. Sukkar

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