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A Disintegrin and Metalloproteinase 17 (ADAM17) and Epidermal Growth Factor Receptor (EGFR) Signaling Drive the Epithelial Response to Staphylococcus aureus Toxic Shock Syndrome Toxin-1 (TSST-1)
Journal article   Open access   Peer reviewed

A Disintegrin and Metalloproteinase 17 (ADAM17) and Epidermal Growth Factor Receptor (EGFR) Signaling Drive the Epithelial Response to Staphylococcus aureus Toxic Shock Syndrome Toxin-1 (TSST-1)

Laura M Breshears, Patrick M Schlievert and Marnie L Peterson
The Journal of biological chemistry, Vol.287(39), pp.32578-32587
09/21/2012
DOI: 10.1074/jbc.M112.352534
PMCID: PMC3463354
PMID: 22833676
url
https://doi.org/10.1074/jbc.M112.352534View
Published (Version of record) Open Access

Abstract

Background: The staphylococcal superantigen (SAg) toxic shock syndrome toxin-1 (TSST-1) is proinflammatory to mucosal epithelial cells by an unknown mechanism. Results: Metalloproteinases and the epidermal growth factor receptor mediate the epithelial response to TSST-1. Conclusion: Inflammatory signals from the epithelium contribute to SAg-mediated disease progression. Significance: Understanding how SAgs initiate the inflammatory cascade may provide molecular targets for the development of new therapies. Staphylococcal superantigens (SAgs), such as toxic shock syndrome toxin-1 (TSST-1), are the main cause of toxic shock syndrome (TSS). SAgs deregulate the host immune system after penetrating epithelial barriers such as the vaginal mucosa. In response to TSST-1, human vaginal epithelial cells (HVECs) produce cytokines and undergo morphological changes. The epithelial signaling mechanisms employed by SAgs remain largely unknown and are the focus of the work presented here. Analysis of published microarray data identified a network of genes up-regulated by HVECs in response to TSST-1 that includes the sheddase, a disintegrin and metalloproteinase 17 (ADAM17). Investigation revealed that the ADAM17 proteolytic targets, amphiregulin (AREG), transforming growth factor α (TGFα), syndecan-1 (SDC1), and tumor necrosis factor receptor 1 (TNFR1), are shed from HVECs in response to TSST-1. TAPI-1 (an ADAM inhibitor) completely abrogates all observed shedding and the production of the cytokine interleukin-8 (IL-8). Knock-down studies show that ADAM17, but not the closely related ADAM10, is required for AREG, TGFα, and TNFR1 shedding. Both ADAM10 and ADAM17 contribute to SDC1 shedding and IL-8 production by HVECs in response to TSST-1. EGFR signaling is critical for up-regulation of IL-8 at the transcriptional level in response to TSST-1 and is also necessary for AREG, TGFα, and TNFR1 shedding. A model is proposed describing the interactions of TSST-1, ADAMs, and the EGFR that lead to establishment of a proinflammatory positive feedback loop in epithelial cells and demonstrate a role for SAgs in the initial stages of disease.
Molecular Bases of Disease Shedding Toxic Shock Syndrome ADAM ADAMTS Signal Transduction Epidermal Growth Factor Receptor (EGFR) Epithelial Cell Mucosal Immunology Superantigen Staphylococcus aureus

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