A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS)

Mutations in TNFRSF1A encoding TNF receptor 1 (TNFR1) cause the autosomal dominant TNF receptor-associated periodic syndrome (TRAPS): a systemic autoinflammatory disorder. Misfolding, intracellular aggregation, and ligand-independent signaling by mutant TNFR1 are central to disease pathophysiology....

Full description

Bibliographic Details
Main Authors: Negm, Ola H., Mannsperger, Heiko A., McDermott, Elizabeth M., Drewe, Elizabeth, Powell, Richard J., Todd, Ian, Fairclough, Lucy C., Tighe, Patrick J.
Format: Article
Published: Wiley 2014
Subjects:
Online Access:https://eprints.nottingham.ac.uk/46896/
_version_ 1848797421629341696
author Negm, Ola H.
Mannsperger, Heiko A.
McDermott, Elizabeth M.
Drewe, Elizabeth
Powell, Richard J.
Todd, Ian
Fairclough, Lucy C.
Tighe, Patrick J.
author_facet Negm, Ola H.
Mannsperger, Heiko A.
McDermott, Elizabeth M.
Drewe, Elizabeth
Powell, Richard J.
Todd, Ian
Fairclough, Lucy C.
Tighe, Patrick J.
author_sort Negm, Ola H.
building Nottingham Research Data Repository
collection Online Access
description Mutations in TNFRSF1A encoding TNF receptor 1 (TNFR1) cause the autosomal dominant TNF receptor-associated periodic syndrome (TRAPS): a systemic autoinflammatory disorder. Misfolding, intracellular aggregation, and ligand-independent signaling by mutant TNFR1 are central to disease pathophysiology. Our aim was to understand the extent of signaling pathway perturbation in TRAPS. A prototypic mutant TNFR1 (C33Y), and wild-type TNFR1 (WT), were expressed at near physiological levels in an SK-Hep-1 cell model. TNFR1-associated signaling pathway intermediates were examined in this model, and in PBMCs from C33Y TRAPS patients and healthy controls. In C33Y-TNFR1-expressing SK-Hep-1 cells and TRAPS patients' PBMCs, a subtle, constitutive upregulation of a wide spectrum of signaling intermediates and their phosphorylated forms was observed; these were associated with a proinflammatory/antiapoptotic phenotype. In TRAPS patients' PBMCs, this upregulation of proinflammatory signaling pathways was observed irrespective of concurrent treatment with glucocorticoids, anakinra or etanercept, and the absence of overt clinical symptoms at the time that the blood samples were taken. This study reveals the pleiotropic effect of a TRAPS-associated mutant form of TNFR1 on inflammatory signaling pathways (a proinflammatory signalome), which is consistent with the variable and limited efficacy of cytokine-blocking therapies in TRAPS. It highlights new potential target pathways for therapeutic intervention.
first_indexed 2025-11-14T20:03:37Z
format Article
id nottingham-46896
institution University of Nottingham Malaysia Campus
institution_category Local University
last_indexed 2025-11-14T20:03:37Z
publishDate 2014
publisher Wiley
recordtype eprints
repository_type Digital Repository
spelling nottingham-468962020-05-04T20:14:05Z https://eprints.nottingham.ac.uk/46896/ A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS) Negm, Ola H. Mannsperger, Heiko A. McDermott, Elizabeth M. Drewe, Elizabeth Powell, Richard J. Todd, Ian Fairclough, Lucy C. Tighe, Patrick J. Mutations in TNFRSF1A encoding TNF receptor 1 (TNFR1) cause the autosomal dominant TNF receptor-associated periodic syndrome (TRAPS): a systemic autoinflammatory disorder. Misfolding, intracellular aggregation, and ligand-independent signaling by mutant TNFR1 are central to disease pathophysiology. Our aim was to understand the extent of signaling pathway perturbation in TRAPS. A prototypic mutant TNFR1 (C33Y), and wild-type TNFR1 (WT), were expressed at near physiological levels in an SK-Hep-1 cell model. TNFR1-associated signaling pathway intermediates were examined in this model, and in PBMCs from C33Y TRAPS patients and healthy controls. In C33Y-TNFR1-expressing SK-Hep-1 cells and TRAPS patients' PBMCs, a subtle, constitutive upregulation of a wide spectrum of signaling intermediates and their phosphorylated forms was observed; these were associated with a proinflammatory/antiapoptotic phenotype. In TRAPS patients' PBMCs, this upregulation of proinflammatory signaling pathways was observed irrespective of concurrent treatment with glucocorticoids, anakinra or etanercept, and the absence of overt clinical symptoms at the time that the blood samples were taken. This study reveals the pleiotropic effect of a TRAPS-associated mutant form of TNFR1 on inflammatory signaling pathways (a proinflammatory signalome), which is consistent with the variable and limited efficacy of cytokine-blocking therapies in TRAPS. It highlights new potential target pathways for therapeutic intervention. Wiley 2014-07 Article PeerReviewed Negm, Ola H., Mannsperger, Heiko A., McDermott, Elizabeth M., Drewe, Elizabeth, Powell, Richard J., Todd, Ian, Fairclough, Lucy C. and Tighe, Patrick J. (2014) A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS). European Journal of Immunology, 44 (7). pp. 2096-2110. ISSN 1521-4141 Autoinflammation; Protein microarray; Signalome; TNF receptor 1; TRAPS http://onlinelibrary.wiley.com/doi/10.1002/eji.201344328/abstract doi:10.1002/eji.201344328 doi:10.1002/eji.201344328
spellingShingle Autoinflammation; Protein microarray; Signalome; TNF receptor 1; TRAPS
Negm, Ola H.
Mannsperger, Heiko A.
McDermott, Elizabeth M.
Drewe, Elizabeth
Powell, Richard J.
Todd, Ian
Fairclough, Lucy C.
Tighe, Patrick J.
A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS)
title A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS)
title_full A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS)
title_fullStr A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS)
title_full_unstemmed A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS)
title_short A pro-inflammatory signalome is constitutively activated by C33Y mutant TNF receptor 1 in TNF receptor-associated periodic syndrome (TRAPS)
title_sort pro-inflammatory signalome is constitutively activated by c33y mutant tnf receptor 1 in tnf receptor-associated periodic syndrome (traps)
topic Autoinflammation; Protein microarray; Signalome; TNF receptor 1; TRAPS
url https://eprints.nottingham.ac.uk/46896/
https://eprints.nottingham.ac.uk/46896/
https://eprints.nottingham.ac.uk/46896/